Ecology of the macrofauna in sandy intertidal habitats...

Ecology of the macrofauna in sandy

intertidal habitats

Ecología de la macrofauna en intermareales

arenosos

Iván Franco Rodil

Thesis submitted in fulfilment of the requirements for the

degree of Doctor in Biological Sciences

Memoria presentada para optar al grado de

Doctor en Biología

Universidad de Vigo

2008

Mariano Lastra Valdor, Profesor Titular del Departamento de

Ecología y Biología Animal de la Universidad de Vigo

CERTIFICA:

Que la presente memoria titulada “Ecología de la macrofauna de

intermareales arenosos”, presentada por D. Iván Franco Rodil para optar al

Grado de Doctor en Biología, ha sido realizada bajo mi dirección en el

Departamento de Ecología y Biología Animal de la Universidad de Vigo.

Y considerando que tiene la suficiente entidad para constituir un

trabajo de Tesis Doctoral, autorizo su presentación ante el Consejo de

Departamento y la Comisión de Doctorado.

Y para que así conste y surtan los efectos oportunos, expido y firmo la

presente certificación en Vigo a 15 de Noviembre de 2007

Fdo: Mariano Lastra Valdor.

i

Acknowledgments

During the last years I have met and benefited from the attention and

generosity of many people and institutions, some of them mentioned

individually at the end of each of the following chapters, who contributed to

my development as a scientist and as a person, sometimes in unexpected ways.

First of all, I want to thank Mariano because he introduced me to the

sandy beaches world and always kept a permanent place in store for me in the

lab. Thanks to all the Benthos Team, those who were part of and those who still

remain, somehow, in this abstract body, for everything. Mónica and Germán

deserve special mention because they woke me up at the very moment and

Celia because she showed me more than “two things”. Thanks all of you for

everything.

I am very grateful to Jenny, Mark, Dave and Pete because they made

me feel at home so far away on the other side of both oceans. Because you let

me learn.

To my family, the one which chose me and the one I chose, for your

patience, warm and, above all, your unselfishness friendship. Mum, thanks for

existing. Thanks grandma for loving your friend from Vigo so much. Thanks to

the Pacific.

The present thesis was financially supported by a Ph.D. grant of the

Xunta de Galicia (Maria Barbeito P.P. 0000 300s 140.08.). Additonal travel

grants were acquired from the Universidad de Vigo and Fundación Caixa

Galicia.

Nihil obstat quominus imprimatur

Quod scripsi, scripsi (John, 19,22)

ii

Agradecimientos

Durante los últimos años he contado con el apoyo y la generosidad de

mucha gente e instituciones, algunos de ellos se mencionan de forma individual

al final de cada Capítulo, que han contribuido a mi desarrollo como científico y

como persona, a veces de maneras inesperadas.

En primer lugar gracias a Mariano por haberme introducido en el

mundo de las playas y reservarme un hueco permanente en el laboratorio.

Gracias a todo el Equipo de Bentos, a los que estuvieron en algún momento y a

los que todavía forman parte, de alguna forma, de este ente abstracto, por todo.

Una mención especial merecen Mónica y Germán por espabilarme en el

momento adecuado y Celia, por enseñarme algo más que un “par de cosas”.

Gracias a todos por todo.

Gracias a Jenny, Mark, Dave y Pete por haberme hecho sentir como en

casa al otro lado de los océanos. Por dejarme aprender.

A mi familia, la que me escogió y se dejó escoger, por vuestra

paciencia, cariño y sobre todo por esa amistad desinteresada y sin límites.

Mamá gracias por existir. A mi abuela, por querer tanto a su amigo de Vigo.

Gracias al Pacífico.

El presente trabajo ha sido financiado por una beca predoctoral de la

Xunta de Galicia (Maria Barbeito). Becas de viaje adicionales para la

realización de estancias en centros extranjeros fueron obtenidas de la

Universidad de Vigo y de la Fundación Caixa Galicia.

Nihil obstat quominus imprimatur

Quod scripsi, scripsi (Juan, 19, 22)

iii

Preface

Sandy beaches geographically dominate many regions of the

worldwide coast and underpin a substantial part of coastal economies and

developments. Sandy beaches are teeming with life, microscopic and

macroscopic. The spectrum of life in the sediment includes clams, whelks,

worms, sand hoppers, crabs and a host of smaller animals as well as

protozoans, microscopic plants, and bacteria. In addition to these residents of

the intertidal, a variety of species move up over the beach from the surf zone on

the rising tide, and others descend onto the beach from the dunes on the falling

tide. All of these components interact in a trophic network to create the open

ecosystem of the sandy beach, which exchanges materials with sea and land

becoming an important environment linking two main ecosystems.

Beaches are in a constant state of flux, accreting and eroding in

response to waves, currents, winds, storms, and sea-level change. Intertidal

areas are under increasing pressure from urbanisation, with 50% of the world’s

population now living by the coast. The beach and nearshore coastal habitats

are substantially disturbed by and can be functionally degraded through

anthropogenic activities such as process of nourishment, recreational activities

or pollution. Coastal fisheries are an important socioeconomic productive

sector with ecological relevance in these shores. Furthermore, sandy beaches

attract most of the coastal tourism and are prime sites for human recreation,

sometimes with negative environmental consequences. The sand beach

represents a productive and unique habitat supporting dense concentrations of

benthic invertebrates that feed surf fishes, resident and migrating shorebirds,

and crabs. Algal wrack deposits represent the main food resource for upper

shore consumers. Grooming with heavy equipment, to remove drift

macrophytes, debris, and trash, is common on sandy beaches in populated

regions. Removal of wrack can seriously affect beach ecosystem trophic

dynamics because this deprives the ecosystem of valuable nutrient input,

impacting wrack-dependet species and affecting shorebirds that feed on the

iv

associated invertebrates. The ecological, economic, and social implications of

rising sea level associated with global warming are far-reaching and not yet

fully anticipated by scientists or adequately contemplated in social policy.

The main aim of this study was to improve our knowledge about the

sandy beach macrofauna in the North coast of Spain. This region had not seen

any major research on sandy beach ecology, despite the great importance of

beaches in both the local marine ecosystem and the local economy. This Ph.D.

thesis consists of a general summary of the work in sandy beaches (Chapter 1)

and five accompanying chapters (Chapters 2-6). The aim of the summary is to

present an integrated account of sandy-shore ecology. The chapters are listed in

the order followed to address this overall objective and all the studies were

conducted to elucidate different aspects of the ecology of the sandy shores.

This study also includes a final section where a general discussion is presented

and which attempts to draw general conclusions of the work conducted in this

particular system.

Keywords: sandy beaches, macrofauna, intertidal zonation, morphodynamic,

exposure rate, swash, biochemical composition of sedimentary organic matter,

biopolymeric fraction, invasive species, wrack macroalgae, north of Spain.

“Everything we hear is an opinion, not a fact. Everything we see is a

perspective, not the truth.”

“Such as are your habitual thoughts, such also will be the character of your

mind; for the soul is dyed by the thoughts”.

Marcus Aurelius

v

Prefacio

Las playas dominan geográficamente muchas regiones del mundo y

apuntalan una parte sustancial del desarrollo y de la economía costera. Las

playas rebosan de vida, microscópica y macroscópica. El espectro de vida

presente incluye almejas, bígaros, gusanos, pulgas de mar, cangrejos y

pequeños huéspedes como protozoos, plantas microscópicas y bacterias.

Además de los residentes del intermareal, una gran variedad de especies suben

por la playa desde la rompiente con la marea y otros desciende desde las dunas

con la bajamar. Todos estos componentes interactúan dentro de una red trófica

creando un ecosistema playero abierto donde se intercambia material con los

ecosistemas terrestre y marino convirtiéndose un ambiente importante nexo de

dos ecosistemas principales.

Las playas están en un estado de flujo constante, de acreación y erosión

en respuesta a las olas, corrientes, vientos, tormentas y al cambio del nivel del

mar. Las zonas intermareales se encuentran bajo una presión incesante debida a

la urbanización, con un 50% de la población mundial viviendo próxima a la

costa. Tanto la playa como los hábitats costeros están sustancialmente

modificados y degradados a través de las actividades antropogénicas como los

rellenos, actividades recreativas o la contaminación directa. La actividad de

marisqueo es un sector socioeconómico muy productivo con relevancia

ecológica para los intermareales. Además, al igual que en otras regiones, las

playas españolas atraen la mayor parte del turismo costero y son lugares

principales de ocio, algunas veces con consecuencias ambientales negativas.

Las playas representan un hábitat único y productivo que aporta grandes

concentraciones de invertebrados bentónicos a la dieta de peces, aves

migratorias y residentes y cangrejos. Los depósitos de algas varadas

representan la fuente de alimento principal para los consumidores de duna. Las

actividades de limpieza con equipo pesado, para remover las algas varadas,

restos y basura, es común en las playas de regiones pobladas. La eliminación de

estos acúmulos de algas puede afectar seriamente a la dinámica trófica porque

priva al ecosistema de playa de una aportación nutritiva valiosa, produciéndose

vi

un impacto en aquellas especies dependientes de los acúmulos de algas y

afectando a aquellas aves que se alimentan de los organismos asociados. Las

implicaciones ecológicas, económicas y sociales de un aumento del nivel del

mar asociado al calentamiento global están lejos de ser totalmente previstas por

los científicos o de estar adecuadamente contempladas en la política social.

El principal objetivo de este estudio fue mejorar nuestro conocimiento

sobre la macrofauna de playas en la costa Norte de España. Esta región no ha

sido objeto de investigaciones importantes en ecología de playas, a pesar de la

gran importancia que tienen tanto en el ecosistema marino como en la

economía local. Esta tesis, presenta un resumen general de la ecología de

playas (Capítulo 1) y cinco capítulos acompañantes (Capítulos 2-6). El objetivo

del resumen es presentar un informe integrado de la ecología de playas; para

ello los capítulos se ordenan siguiendo este objetivo global y todos los estudios

fueron llevados a cabo para elucidar diferentes aspectos de la ecología de

playas. Se incluye además una sección final con una discusión general que

pretende resumir las conclusiones más relevantes del trabajo.

Palabras clave: playas, macrofauna, zonación intermareal, morfodinámica,

gradiente de exposición, swash, composición bioquímica de la materia orgánica

sedimentaria, fracción biopolimérica, especies invasoras, algas de arribazón,

norte de España.

“Todo lo que oimos es una opinión, no un hecho. Todo lo que vemos es una

perspectiva, no la verdad”

“Cuales sean tus pensamientos habituales, tal será también el carácter de tu

alma, porque los pensamientos matizan el alma”

Marco Aurelio

Table of contents

Acknowledgments .......................................................................................... i

Agradecimientos ........................................................................................... ii

Preface .......................................................................................................... iii

Prefacio........................................................................................................... v

PART I. INTRODUCTION AND AIMS. ............................................. 13

Chapter 1. General introduction. ............................................................... 14

1.1.1. Soft intertidals: sandy beaches ...................................................... 15

1.1.1.1. What is a sandy beach? .............................................................. 15

1.1.1.2. The physical environment: tidal range and system stratification

.............................................................................................................................. 18

1.1.1.3. Beach morphodynamics ............................................................. 20

1.1.2. Benthic macrofauna communities ................................................ 24

1.1.2.1. What is macrofauna? ................................................................. 24

1.1.2.2. Sandy beach macrofauna ........................................................... 26

1.1.2.3. Macrofauna distribution patterns ............................................... 27

1.1.2.4. Macrofauna zonation in the sandy beach ................................... 30

1.1.2.5. Feeding habits and survival strategies of the macrofauna ......... 33

1.1.3. Food sources in sandy beaches ..................................................... 37

1.1.3.1. Food availability ........................................................................ 37

1.1.3.2. The role of the biochemical composition and hydrodynamic

conditions.............................................................................................................. 38

1.1.4. Aims and thesis linework. ............................................................. 39

1.1.5. List of references .......................................................................... 42

PARTE I. INTRODUCCIÓN Y OBJETIVOS. .................................... 47

Capítulo 1. Introducción general. .............................................................. 48

1.1.1. Intermareal arenoso: Playas. ......................................................... 49

1.1.1.1. ¿Qué es una playa? .................................................................... 49

1.1.1.2. El ambiente físico: rango mareal y estratificación del sistema .. 51

1.1.1.3. Morfodinamismo ....................................................................... 52

1.1.2. Comunidades de la macrofauna bentónica ................................... 55

1.1.2.1. ¿Qué es la macrofauna? ............................................................. 55

1.1.2.2. Macrofauna en las playas ........................................................... 56

Table of contents

1.1.2.3. Patrones de distribución de la macrofauna ................................ 57

1.1.2.4. Zonación de la macrofauna en la playa ...................................... 59

1.1.2.5. Hábitos alimenticios y estrategias de supervivencia de la

macrofauna de playas ........................................................................................... 62

1.1.3. Fuentes de alimento en las playas ................................................. 64

1.1.3.1. Disponibilidad del alimento ....................................................... 64

1.1.3.2. El papel de la composición bioquímica y de las condiciones

hidrodinámicas. ..................................................................................................... 65

1.1.4. Objetivos y líneas de investigación de la tesis. ............................. 67

PART II. THE ECOLOGY OF SANDY BEACHES ........................... 71

Chapter 2. Environmental factors affecting benthic macrofauna along a

gradient of intermediate sandy beaches in northern Spain ..................... 72

Abstract................................................................................................... 73

2.2.1.Introduction ................................................................................... 73

2.2.2. Material and methods ................................................................... 75

2.2.2.1. Study area .................................................................................. 75

2.2.2.2. Sampling design ........................................................................ 76

2.2.2.3. Statistical analysis ...................................................................... 77

2.2.3. Results .......................................................................................... 78

2.2.3.1. Physical environment ................................................................. 78

2.2.3.2. Composition and abundance of the macrofauna ........................ 79

2.2.3.3. Relationships between macrofauna and environmental variables

.............................................................................................................................. 81

2.2.4. Discussion ..................................................................................... 83

Acknowledgments .................................................................................. 86

2.2.5. References .................................................................................... 86

Chapter 3. Community structure and intertidal zonation of the

macroinfauna in intermediate sandy beaches in temperate latitudes:

North coast of Spain. ................................................................................... 89

Abstract................................................................................................... 90

2.3.1. Introduction .................................................................................. 91

2.3.2. Material and methods. .................................................................. 93

2.3.2.1. Study area .................................................................................. 93

2.3.2.2 Sampling design ......................................................................... 94

Table of contents

2.3.2.3. Statistical analysis ...................................................................... 95

2.3.3. Results .......................................................................................... 97

2.3.3.1. Physical environment ................................................................. 97

2.3.3.2. Composition and abundance of the Macrofauna ........................ 99

2.3.3.3. Intertidal zonation of the macroinfauna ................................... 100

2.3.3.4. Relationships between macroinfauna and environmental

variables. ............................................................................................................. 105

2.3.4. Discussion ................................................................................... 106

2.3.4.1. Macrofaunal characteristics ..................................................... 106

2.3.4.2. Zonation patterns of the macroinfauna .................................... 106


variables. ............................................................................................................. 112

Acknowledgments ................................................................................ 114

2.3.5. References .................................................................................. 115

PART III. THE IMPORTANCE OF EXPOSURE ON SANDY

BEACH MACROFAUNA: HYDRODINAMIC CONDITIONS AND

FOOD AVAILABILITY. ..................................................................... 120

Chapter 4. Macroinfauna community structure and biochemical

composition of sedimentary organic matter along a gradient of wave

exposure in sandy beaches (NW Spain). .................................................. 121

Abstract................................................................................................. 122

3.4.1. Introduction ................................................................................ 123

3.4.2. Material and methods ................................................................. 125

3.4.2.1. Study area ................................................................................ 125

3.4.2.2. Sampling design ...................................................................... 126

3.4.2.3. Biochemical analysis. .............................................................. 127

3.4.2.4. Data analysis. ........................................................................... 128

3.4.3. Results ........................................................................................ 129

3.4.3.1. Physical environment ............................................................... 129

3.4.3.2. Composition and abundance of the macroinfauna ................... 131

3.4.3.3. Intertidal distribution of the macroinfauna .............................. 132

3.4.3.4. Organic matter composition..................................................... 133

3.4.4. Discussion ................................................................................... 138

3.4.4.1. Macroinfauna characteristics in a gradient of exposure ........... 138

Table of contents

3.4.4.2. Biochemical composition of sedimentary organic matter ........ 142

Acknowledgements .............................................................................. 146

3.4.5. References .................................................................................. 147

PART IV. THE ROLE OF FOOD AVAILABILITY IN SANDY

BEACHES: SPATIAL AND TEMPORAL PATTERNS. .................. 151

Chapter 5. Seasonal variability in the vertical distribution of benthic

macrofauna and sedimentary organic matter in an estuarine beach (NW

Spain). ............................................................................................. 152

Abstract................................................................................................. 153

4.5.1. Introduction ................................................................................ 154

4.5.2. Material and methods. ................................................................ 156

4.5.2.1. Study area ................................................................................ 156

4.5.2.2. Sampling design ...................................................................... 157

4.5.2.3. Biochemical composition of the sedimentary organic matter .. 158

4.5.2.4. Data analysis ............................................................................ 158

4.5.3. Results. ....................................................................................... 160

4.5.3.1. Environmental characteristics. ................................................. 160

4.5.3.2. Macrobenthic community. ....................................................... 161

4.5.3.3. Organic matter composition and chlorophyll a content. .......... 167

4.5.3.4. Relationships between sedimentary organics and benthic fauna.

............................................................................................................................ 169

4.5.4. Discussion ................................................................................... 171

4.5.4.1. Benthic macrofauna community. ............................................. 171

4.5.4.2 Spatial and temporal changes in organic matter composition and

Chl a content. ...................................................................................................... 173

4.5.4.3. Relationships between environmental variables and benthic

macrofauna. ........................................................................................................ 177

Acknowledgements .............................................................................. 179

4.5.5. References. ................................................................................. 179

Chapter 6. Diferential effects of native and invasive algal wrack on

macrofaunal assemblages inhabiting exposed sandy beaches. .............. 182

Abstract................................................................................................. 183

4.6.1. Introduction ................................................................................ 183

4.6.2. Methods ...................................................................................... 186

Table of contents

4.6.2.1. Study area ................................................................................ 186

4.6.2.2. Experimental design ................................................................ 187

4.6.2.3. Laboratory analysis .................................................................. 188

4.6.2.4. Statistical analysis .................................................................... 189

4.6.3. Results ........................................................................................ 192

4.6.3.1. Microclimatic conditions of wrack patches: humidity and

temperature ......................................................................................................... 192

4.6.3.2. Analysis of the total organic matter and nutritional value ....... 192

4.6.3.3. Macrofauna abundance, number of species and diversity ....... 197

4.6.3.4. Analysis of variance of selected species: Patterns of colonisation

and succession .................................................................................................... 199

4.6.3.5. Analysis of assemblages in wrack patches .............................. 202

4.6.3.6. Influence of environmental variables on macrofauna

assemblages. ....................................................................................................... 203

4.6.4. Discussion ................................................................................... 205

4.6.4.1. Patterns of colonisation and succession ................................... 205

4.6.4.2. Abiotic factors affecting macrofaunal assemblages ................. 209

Acknowledgments ................................................................................ 213

4.6.5. References .................................................................................. 213

PART V. GENERAL DISCUSSION. ................................................. 217

5.7.1. The ecology of sandy beaches in the northern coast of the Iberian

Peninsula. ............................................................................................................ 218

5.7.1.1. Environmental factors affecting benthic macrofauna. ............. 219

5.7.1.2. Community structure and macrofauna zonation ...................... 220

5.7.1.3. Relationship between macroinfauna and environmental variables

............................................................................................................................ 221

5.7.2. The importance of exposure on sandy beach macrofauna:

hydrodynamic conditions and food availability. ................................................. 222

5.7.2.1. Macrofauna characteristics in a gradient of exposure .............. 223

5.7.2.2. Effect of the biochemical composition of sedimentary organic

matter on macrofauna ......................................................................................... 224

5.7.3. The role of food availability in the macrofauna community

structure of sandy beaches: spatial and temporal patterns. ................................. 225

5.7.3.1. Seasonal variability in the benthic macrofauna distribution and

food availability in a sheltered estuarine beach. ................................................. 226

Table of contents

5.7.3.2. Effect of invasive algal wrack in macrofauna assemblages in an

exposed sandy beach........................................................................................... 229

5.7.4. Open questions. .......................................................................... 232

5.7.5. List of references. ....................................................................... 235

PARTE V. DISCUSIÓN GENERAL. ................................................. 238

5.7.1. La ecología de playas de la costa norte de la Península Ibérica. . 239

5.7.1.1. Factores ambientales que afectan a la macrofauna bentónica. 240

5.7.1.2. Estructura de la comunidad y zonación de la macrofauna ....... 242

5.7.1.3. Relación entre la macrofauna y las variables ambientales ....... 243

5.7.2. La importancia de la exposición en la macrofauna de playas:

condiciones hidrodinámicas y disponibilidad de alimento. ................................ 245

5.7.2.1. Características de la macrofauna de playas en un gradiente de

exposición ........................................................................................................... 245

5.7.2.2. Efecto de la composición bioquímica de la materia orgánica en la

macrofauna ......................................................................................................... 247

5.7.3. El papel de la disponibilidad de alimento en la estructura de la

comunidad de playas: patrones espaciales y temporales. .................................... 248

5.7.3.1. Variabilidad estacional en la distribución de la macrofauna

bentónica y de la disponibilidad de alimento en una playa estuárica protegida. . 248

5.7.3.2. Efecto de las algas invasoras sobre la asociación macrofaunística

de una playa expuesta ......................................................................................... 252

5.7.4. Cuestiones abiertas. .................................................................... 256

PART VI. GENERAL CONCLUSIONS ............................................. 260

PART VII. APPENDIX ....................................................................... 264

PART I. INTRODUCTION AND AIMS.

“If the doors of perception were cleansed everything would appear to man as it

is, infinite. For man has chosen himself up, till he sees all things through

narrow chinks of his cavern”.

William Blake

Chapter 1. General introduction.

Chapter 1 Introduction

15

1.1.1. Soft intertidals: sandy beaches

1.1.1.1. What is a sandy beach?

Commonly known as sandy beaches, soft intertidals are very dynamic

environments, hostiles and cosmopolitans (McLachlan, 1996) which have been

defined to cover a wide range of environments in several forms, sometimes

with some lack of rigour.

“a wave-deposited accumulation of sand lying between modal wave

base (i.e. the maximum depth at which a wave can transport sediment towards

the shoreward) and upper swash limit” (Short, 1999).

As stated in this definition, three basic requirements arise to have a

sandy beach: sand, waves and tides. It is the sand that is transported by waves

and tides to the shoreline that forms the sandy beach. These three factors

together determine the morphodynamic, faunistic communities; as well as the

quantity and the quality of the organic matter (i.e. food availability) that we

find in the beaches. In this study, sandy beaches will be considered exposed

sandy shorelines possessing three dynamic zones: a zone of wave shoaling

seaward of the breaker point, a surf zone of breaking waves and a swash zone

of final wave dissipation on the subaerial beach. The nature and extent of each

of these zones will ultimately determine the beach morphodynamics (Figure

1.1).

Sand, and by extension sediment, can be classified according to its

origin and its grain size. The most common sediment component is silica,

generally in quartz form (terrestrial origin) although it is also frequent the

presence of carbonate (marine origin) sand. Sometimes sediment can be made

of shell hash, volcanic or coralline material and rocks pebble shaped, from

different origin. Sediment grain size is generally defined according to the scale

of Wenthworth (Buchanan, 1984) in phi units (φ = -log2 Ø) but in this study

and in most of the current papers about sandy beach ecology the metric scale


16

units are normally used. Everything between 63 µm and 2 mm (0<φ<4) is

defined as sand. Sediment grain size has been considered decisive in the

macroinfauna community structure in most of the outstanding sandy beach

ecology papers (e.g. Jaramillo and González, 1991; McLachlan and Dorvlo,

2005; Defeo and McLachlan, 2005) and it will be also considered in this study.

Figure 1.1. Features of a high energy sandy beach at mid tide (Modified from Short,

1999).

A wave is, in general, a wind-driven transport of energy through water. Waves

remain stable as long as the wave height (H) is less than 1/7 of the wave length

(L) (Figure 1.2.). Wave action penetrates the water column to a depth of

approximately half of the wave length. Close to the shore, water depth will

decrease to a point where the base of the wave will touch the sea floor. From

here on, the wave will not only transport energy but also sediment material.

This is the modal wave base from Short’s definition and therefore the lower

edge of the beach. The waves will start compacting, the wave length will

decrease and the H/L ratio increases. This is known as shoaling (Fig. 1.1.). The


17

velocity in the lower part of the wave will slow down because of the dragging

created by the sediment and the wave becomes depth-dependent; meanwhile

the upper part of the wave is moving with a different speed (Fig. 1.2.). The

wave will collapse when the H/L ratio surpasses the stability point of 1/7, this

is called breaking zone. The last phase of the wave action, after the point of

breaking, is where the water runs up and down the beach profile, called swash

zone where the wave energy is dissipated. The zone with surfing waves is the

surf zone (Fig. 1.1.).

Figure 1.2. Changes of a wave entering a beach (modified from Thurman and Burton,

2001) and schematic representation of a wave collapsing.

The point of breaking is a very turbulent area characterised by coarser

sediment, water loaded with sand and strong current (Figure 1.3.). The swash

zone reaches the intertidal as a water film, covering and spraying part of the

beach face depending on wave strength, tide range and also beach slope and

Waves reaching critical 1:7 ratio

ratio


18

Swash

Effluent line

Unsaturated sand

Surf zone

Breaker

includes the highest point reached by the highest wave and a water zone almost

stagnant. Traditionally the swash zone was divided in two parts: a saturated

part, always with water, and an unsaturated one reached periodically by the

highest waves with a successive drainage between wave and wave. The surfing

and saturated swash zones are also known as the sublittoral beach environment;

meanwhile the unsaturated zone belongs to the mesolittoral zone (Dahl, 1952).

Depending on the dynamic conditions of the tide and waves there will be a

wider or smaller submerge part in the beach, even during the spring tides.

Eventually, there is a spray zone that is never covered by water and belongs to

the upper part of the beach normally composed by some type of dune system.

This environment is also known as the supralittoral or subterrestrial zone,

constantly dried and where desiccation and temperature are the main stress

factors for the fauna.

Figure 1.3. Pine Knoll Shore (North Carolina). The different zones of the beach

including the effluent line

1.1.1.2. The physical environment: tidal range and system stratification

Tides are not required for beach formation; however increasing tide

range will, in combination with wave conditions, contribute substantially to

beach morphology. Tides cause main impact changing constantly the shoreline

face both horizontally and vertically depending on the tide range and beach


19

profile. In areas of high tide range, the tidal variation in nearshore water depth

can also modify breaker wave height by increasing wave shoaling at low tide.

The shoreline mobility also shifts the swash, surf and wave shoaling zones

(Short, 1999). The tidal regime were classified by Davies (1964) in three main

types (Figure 1.4.): microtidal (TR < 2 m), mesotidal (2 < TR < 4 m) and

macrotidal (TR > 4 m). The highest point reached by the waves during the

spring high tide is traditionally considered as the upper limit in sandy

intertidals, according to the sandy beach definition we are using (Figure 1.5.).

Due to the tidal variation, during low tide sandy beaches show a wide zone

where water drainage occurs. Particularly on exposed beaches, the great

vertical extent of the system and the drainage it experiences at low tide permit

the subdivision of the intertidal beach into layers or strata.

Figure 1.4. Traditional descriptive classifications based on qualitative observations and

tidal range.

Various schemes have been proposed to describe this (Salvat, 1964;

McLachlan, 1980) and one such scheme is shown in Figure 1.6. The layers

range from dry surface sand at the top of the shore to permanently saturated

sand lower down water table and linked to the swash. The permanently

saturated layers have little circulation and tend to become stagnated, while the


20

resurgence zone has gravitational water drainage through it during ebb tide; the

retention zone loses gravitational water but retains capillary moisture at low

tide. The retention lower limit is defined by the upper limit of capillary rise

above the water table during low tide. The zone of retention represents

optimum conditions for interstitial fauna, since there is a good balance between

water, oxygen and food input, physical stability and lack of stagnation

(McLachlan and Brown, 2006).

Figure 1.5. Tidal zonation scheme (modified from Short, 1999)

But sandy beaches are much more than the coastal shoreline. The

intertidal is a linkage environment between marine and terrestrial ecosystem.

We can make a general division in two ecological systems: the wind-driven

dune, with subterrestrial species exposed mainly to air and a wave and tide-

driven intertidal with water breather species. Further subdivision in the

intertidal will be deeply discussed in Chapter 3.

1.1.1.3. Beach morphodynamics

Sandy beach morphology is mainly due to the interactions between

sediment characteristics, wave exposure and marine currents, also called beach

morphodynamics. Since exposed sandy beaches are mostly considered as

physically controlled environments, the first beach classifications were focused

on the hydrodynamic processes underlying the depositional form (Short and


21

Wright, 1984) which span a continuum from reflective beaches, narrow and

steep, to dissipative systems, which are wide and flat. A series of intermediate

states are recognised between the above extremes.

Figure 1.6. Stratification of the interstitial system of an exposed sandy beach (after

Salvat, 1964 in McLachlan and Brown, 2006)

Within this general scheme, many variations are possible, creating a

wide range of beach types. Variations can be due to sediment type, sediment

grain size, wave action, exposure, tidal range and shore morphology. Many of

these factors are interdependent. Sediment grain size, for instance, depends on

the wave action, which in its turn depends on exposure and shore morphology.

Most beach type classifications are based on three parameters: sediment grain

size, wave action and tidal range. The most widely accepted classification using

these parameters (Figure 1.7.) was introduced by Masselink and Short (1993).

On the horizontal axis, Dean’s parameter (Ω = Hb / Ws * T), a function of

sedimentation velocity (Ws), breaker height (Hb) and breaker period (T),

divides the beaches into three types: reflectives (Ω < 1), intermediates (1 < Ω <


22

6) and dissipatives (Ω > 6). The relative tide range (RTR = MSR/Hb) on the

vertical axis is calculated from the mean spring tidal range and the breaker

height and increases with increasing tidal influence on the beach (see 1.1.1.2.).

Figure 1.7. Conceptual model covering beaches of all tide ranges, based on the

dimensionless fall velocity (Ω) and the relative tide range (RTR) (after Short, 1996).

When RTR < 3 and Ω < 2, the microtidal beach types dominate. When RTR is between

3 and 12, tide range increasingly modifies the wide intertidal beach. When RTR > 12,

the transition to tide dominated beaches is entered (modified from McLachlan and

Brown, 2006).

Reflective beaches are characterised by steep slopes and coarse

sediment. The waves break on the beach face itself, eliminating a surf zone.

The swash zone is narrow with high velocity. Dissipative beaches, in contrast,

have waves breaking far out at sea, and a wide surf zone, where much of the

wave is dissipated. This results in very flat beaches with fine to very fine sands.

An intermediate beach is anything in between, it is characterised by high

temporal variability and the most common beach type in the world (Fig. 1.7).

All the beach classification systems include some kind of wave

information (Davies, 1964; Masselink and Short 1993). Although wave regime


23

is probably the most important agent in sandy beach formation, it is difficult to

measure in the field. It can also be questioned to what extent the wave regime

at a given day is representative for the waves that formed the beach as it is on

that day. Both Dean’s parameter and RTR are predictive rather than descriptive

tools (Short, 1999). Therefore, several beach classification parameters, which

do not require wave measurements and which are descriptive, have been

developed. The Beach State Index (BSI), used to compare beaches subject to

differing tide ranges (McLachlan et al., 1993), involved multiplying Dean’s

parameter by a tidal factor, and this gave good correlations when a wide range

of beach types with different tide range is considered (see Chapters 2 and 3).

More recently, (see McLachlan and Dorvlo, 2005) the Beach Index and the

Beach Deposit Index (BI and BDI) were developed. These indexes are based on

a measure of beach face slope multiplied by a measure of sand particle size and

both are easy to measure in the field. The former includes tidal range, which is

useful on a large spatial scale when areas from different regions are compared

(see Chapter 4). The BDI is only suitable for studies on a smaller spatial scale,

with no or minor differences in tidal range between the studied sites.

Beaches are not only classified according to their morphodynamic, but

also according to exposure. A very comprehensive classification scheme was

proposed by McLachlan (1980) and although it is based on indirect variables,

with parameters difficult to measure in the field or with high temporal and

spatial variability, this classification is particularly important for ecological

studies since unifies relevant ecological concepts. Four categories, from very

sheltered to very exposed, are defined with a rating system based on wave,

biological and morphodynamic characteristics (Table 1.1.).

Sandy beaches are a very dynamic system where spatial and temporal

changes in physical and morphological characteristics are common. Sandy

beaches are physically controlled environments where communities are

structured by the independent responses of individual species to physical

factors, such as sediment texture and swash conditions (e.g. McArdle and

McLachlan, 1992; McLachlan, 1996; Defeo and McLachlan, 2005).


24

Sediment texture determines porosity (i.e., the volume for space

between the sand grains), permeability (i.e., the rate of drainage of water

through the sand) and penetrability (i.e. the force needed to penetrate the sand)

of the sand, and as such the filtration rate of the swash water and the water

content of the beach. This results in a higher permeability but lower porosity of

the sand. The water saturation level on beaches with coarse sand is much lower.

Therefore, the interstitial water table (i.e., level below which sediment

is completely water saturated) will surface lower on the beach. This surfacing

of the interstitial water table, or the transition between unsaturated and

saturated surface sand is called the effluent line (EL) and is easily seen as a

“glassy layer” (Fig. 1.3.).

Swash, the run-up and run-off of water on the beach face, is the

transferring agent of wave energy and water to the beach. The swash

characteristics are crucial in the formation of beaches. The swash period,

velocity and interval, in theory, are less favourable or “harsher” on reflective

beaches, with shorter swash periods and intervals and higher swash velocities,

especially at low tide. (McArdle and McLachlan, 1992; Short, 1999). Swash is

directly dependent on wave conditions and beach morphology and slope.

1.1.2. Benthic macrofauna communities

1.1.2.1. What is macrofauna?

Definitions of macrofauna or macrobenthos vary according to

different authors. Mees and Jones (1997) defined macrobenthos as all marine

fauna that is dependent of the sediment and retained on a sieve with 1 mm

mesh-size. Further subdivision includes three groups: endobenthos (i.e.,

animals living in the sediment), epibenthos (i.e., animals living on the

sediment) and hyperbenthos (i.e., animals living in the water column). These

categories do not display sharp boundaries and some species, for instance, live

partially hyperbenthic, partially endobenthic. In general, this kind of division is

based on the sampling device.


25

Parameter Rating Score

Wave action Practically absent 0

Variable, slight to moderate,

wave height seldom exceeds 0,5m. 1

Continuous, moderate,

wave height seldom exceeds 1 m. 2

Continuous, heavy,

wave height mostly exceeds 1m. 3

Continuous, extreme,

Wave height never less than 1.5 m. 4

Surf zone width Very wide, waves first break on bars 0

(only if wave action Moderate, waves usually break

score >1m) 50-100 m from shore 1

Narrow, large waves break on beach 2

% very fine sand >5% 0

(65-125m) 1-5% 1

<1% 2

Slope of the intertidal

Median particle diameter (m) >1/10 1/10-1/15 1/15-1/25 1/25-1/50 >1/50

>710 (>0.5) 5 6 7 7 7

500-710 (1-0.5). 4 5 6 7 7

350-450 (1.5-1). 3 4 5 6 7

250-350 (2-1.5). 2 3 4 5 6

180-250 (2.5-2). 1 2 3 4 5

180 (>2.5). 0 0 1 2 3

Depth of reduced layer (cm) 0-10 0

10-25 1

25-50 2

50-80 3

>80 4

Stable burrows Present 0

Absent 1

Maximum score 20

Minimum score 0

Score Beach type Description

1-5 Very sheltered Virtually no wave action, shallow reduced

layers, abundant macrofaunal burrows

6-10 Sheltered Little wave action, reduced layers present,

usually some macrofaunal burrows

11-15 Exposed Moderate to heavy wave action, reduced

layers deep if present, usually no burrows

16-20 Very exposed Heavy wave action, no reduced layers,

macrofauna only of tough motile fauna

Table 1.1. Rating scheme for assessing the degree of exposure of sandy beaches,

modified from McLachlan (1980)


26

Some other authors extend this size definition to all animals that are

retained on a 0.5 mm mesh-sized sieve (e.g. Brazeiro and Defeo, 1996; Defeo

and Martínez, 2003). In this study we use the macrofauna definition as

endobenthos, those animals that live buried in the sediment and are sampled by

means of a metal cylinder core (Ø= 25 and 15.5 cm) and a 1 mm mesh-sized

sieve (Figure 1.8.).

Figure 1.8. 1 mm sieving bag and metallic cylinder (25 cm Ø) for sampling procedure

During long time, ocean sandy beaches have been regarded as marine

deserts and the biological study has been traditionally lagged behind that of

rocky shores and other ecosystems with obvious exuberant life. The typical

sandy beach nature of constant change is the main macrofauna community

organizer (McLachlan, 1983). Although sandy beaches, at first sight, look

uniform and devoid of living organisms they are teeming with life, microscopic

and macroscopic.

1.1.2.2. Sandy beach macrofauna

Sandy beach macrofauna, as defined above, consists mainly of animals

belonging to three taxa: Crustacea, Annelida (mainly Polychaeta) and

Mollusca. Species composition and distribution of sandy beach macrofauna

change at different spatial scales. There are differences in macroscale (between


27

different coastal areas and latitudes) mesoscale (within one beach along shore

and cross-shore) and microscale (biological interactions locally). Whereas the

processes at the macro and mesoscale are physically driven on exposed sandy

beaches, biological interactions such as predation or competition start to play a

role on the microscale (Defeo and McLachlan, 2005; McLachlan and Brown,

2006). Due to these processes at different scales, there is a huge variety in

macrofaunal species richness, abundance and biomass in sandy beach

ecosystem1. Although there are several studies focused on meio and

microfauna, macrofauna forms are by far the better known. They are the main

component in the fauna community dwelling sandy beaches and they are also

easier to collect and identify. The main macrofauna characteristics are the high

mobility and burrowing adaptations to the sediment. It has been suggested that

crustaceans dominate the most exposed beaches and polychaetes the most

sheltered beaches with molluscs reaching maximum abundance in intermediate

situations (Dexter, 1983), although there are many exceptions in this theoretical

distribution (see Chapters 3 and 4).

1.1.2.3. Macrofauna distribution patterns

Within one geographical region the general pattern in sandy beach

macrofauna is a decrease in species richness, abundance and biomass when

moving along the morphodynamic gradient (Figure 1.9.); i.e., from the

dissipative to the reflective beach state. This pattern, which is found at any

place in the world, is now considered one paradigm in sandy beach ecology

(e.g. Defeo and McLachlan 2005; McLachlan and Brown, 2006). Beaches can

be described by a set of physical parameters; most of them could be potential

structuring factors for sandy beach macrofauna. In fact, sandy beaches are

considered physically controlled environments where the role of biological

1 Ecosystem in this text refers to a system made of individuals of many species, within

a delimited area, and involved in an interaction process, expressed by means of energy

exchange or a sequence of birth and death, and one of the results can be the evolution at

species level and the succession at system level. (Margalef, 1995).


28

factors in structuring beach communities2 is dubious (McLachlan and

Jaramillo, 1995). There is a general trend, for instance, of increasing species

richness with decreasing grain size and beach face slope, increasing tidal range

and intertidal width and/or decreasing harsh swash climate (e.g. Jaramillo and

McLachlan, 1993; Brazeiro, 1999; McLachlan and Dorvlo, 2005).

The main hypothesis proposed to explain the relationship between

macrofauna and beach morphodynamic is known as “Swash Exclusion

Hypothesis”. This hypothesis states that the decrease in species richness,

abundance and biomass is caused by increasing harshness of the swash climate

together with a steeper slope and coarser sand. In some situations, species can

be excluded from extreme systems (McLachlan et al., 1995). This theory

suggests that the burrowing ability could be a determinant factor in species

2 Community concept: Ecologists study the distributions, abundances and interactions

among organisms at a variety of spatial scales of organization. The problem arises

when the whole set of species found in the same place is considered. Communities are

supposedly the actual units of study for many ecologists and there seem to be two, very

different ways of viewing a community. One is that species exist in integrated

communities that have persistent features through time and are repeated in different

places. Thus, the ecological community of species is organized, structured and

integrated. The species are interdependently interactive and, often, it is presumed that

the interactions are, at least in part, responsible for maintaining the entity. The

alternative view describes community as the collection of organisms that are found in

the same place at the same time. They may or may not interact. They coexist because

they have similar physiological responses to physical components of the environment

and/or they have similar needs for resources of food and shelter. Alternatively, some of

them may be present because they need others as prey. The reality is probably

somewhere in between. To avoid some of the confusion associated with the term

community, the two ecological approaches will here be referred to using the term

“community” for tightly-knit, consistent sets of species and “assemblage” will be used

for the more loosely associate set of co-occurring species, where the whole set of

species is not a repeatable, identifiable set (Underwood, 2006).


29

distribution and community structure from different beach types (Dugan et al.,

2004). Those species with better burrowing capacity would be able to inhabit

successfully reflective beaches with steeper slopes and very active swash

climate.

In contrast, in flat slope beaches, organisms with a much wider range

of behavioural and morphological adaptations are expected. Furthermore, it is

important to have in mind the existence of semi-terrestrial species, less

influenced by the swash climate, which generally have autonomous active

movement on upper beach levels (Defeo and McLachlan, 2005).

Figure 1.9. General conceptual model relating biological descriptors and beach state

(after Defeo and McLachlan, 2005). At a finer scale and under more dissipative

conditions, biological factors become more important. (R: reflective; I: intermediate; D:

dissipative; UD: ultradissipative; TF: tidal flat)

At population level this was translated into the “Habitat Harshness Hypothesis”

(Defeo et al., 2001) which postulates that on reflective beaches the harsh

environment forces macrofauna to divert more energy towards maintenance,

leaving less for reproduction and causing higher mortality. Brazeiro (2001)

found that not only swash and sediment characteristics but also the accretion-


30

erosion dynamics on beaches could influence sandy beach macrofauna. All

these existing ideas were synthesised in the “Hypothesis of Macroscale

Physical Control” (McLachlan and Dorvlo, 2005) where two levels of factors

controlling the macroscale patterns are identified. The first level is controlled

by two main factors, tidal range and latitude which determine the maximum

number of species that can occur under ideal conditions in a particular region.

Furthermore, a second level is controlled by swash climate, sediment grain size

and beach stability which limit the actual species count through exclusion of

less well-adapted species under harsher, more reflective conditions.

1.1.2.4. Macrofauna zonation in the sandy beach

Faunal zonation is a well described feature of intertidal zones and has

been much studied in marine ecology. Zonation on sandy beaches is not nearly

as visible as on rocky shores. This is probably a consequence of the dynamic

environment of the beach and the shifting populations that occupy it. Like the

macroscale, macroinfauna communities and assemblages are primarily

physically structured (McLachlan, 1983). The macrofauna is spread alongshore

and cross-shore. In fact beach length is thought to play an important role with a

decrease in species richness with decreasing beach length (Brazeiro, 1999). In

general macrofaunal populations are most developed in the middle of a beach,

with a unimodal bell-shaped distribution towards both sides. Other factors that

can influence the along shore distribution of macrofaunal species include the

presence of rocky shores, human impact, estuarine input or the shape of the

beach (McLachlan and Brown, 2006). Cross-shore variability can be divided

into general macrofaunal patterns and zonation; i.e., the sum of the response of

each species to cross-shore gradients. The general cross-shore pattern is an

increase in species number towards the subtidal area (e.g. McLachlan and

Jaramillo, 1995; McLachlan and Brown, 2006).

Many studies have been published on the zonation of sandy beach

macrofauna (McLachlan and Jaramillo, 1995). Two general zonation schemes

have been traditionally used to determine distributions of organisms on sandy

beaches: Dahl (1952) defined three biological zones in terms of typical


31

crustacean fauna inhabiting each zone, and Salvat (1964) defined four physical

zone based on sand moisture content across shore (Figure 1.10. and Fig. 1.6.).

The correspondence between both schemes is fairly good and zonation schemes

proposed by other authors can generally be considered variations on these two

schemes. Perhaps the most elementary, but also widely applicable, zonation

scheme for sandy shores is that proposed by Brown (in McLachlan, 1983, cited

in Mclachlan and Brown, 2006). This suggests that only two zones can be

recognised on sandy shores (see Chapter 3): a zone of air-breathers (mainly

crustaceans and insects) at and above the drift line and a zone of water-

breathers below this. The general conclusion from the latter studies was that it

was difficult to fit the data neatly into any one of the schemes proposed

(McLachlan and Jaramillo, 1995; McLachlan and Brown, 2006).

Several studies in different regions have suggested that different beach types

and physical factors might cause differences in zonation (e.g. Trevallion et al.,

1970; Bally, 1983; Jaramillo et al., 1993; McLachlan y Jaramillo, 1995).

Quantitative analysis give partial support for three zones, but the number of

recognizable zones depends on beach type, reflective beaches having fewer

zones than dissipative beaches (McLachlan and Jaramillo, 1995; Defeo and

McLachlan, 2005). In dissipative and intermediate beaches, lower zones

present high macrofauna abundance and species richness and may frequently

be subdivided in three or even four different zones towards the most dissipative

cases. In the other hand, impoverished fauna was found downshore on

reflective beaches due to the harsh hydrodynamic conditions (Figure 1.11.). At

the extremes of beach morphodynamics, only the supralittoral zone may be

found on extreme reflective beaches and up to four zones are recognised on

wide dissipative beaches. In general, zones are clearest at the top of the shore

and become increasingly blurred moving downshore (McLachlan and

Jaramillo, 1995) where there is no clear agreement with Dahl’s scheme on

extreme reflective beaches (Fig. 1.9.).


32

Figure 1.10. Overview of the three most common zonation schemes for sandy beach

macrofauna (after McLachlan and Brown, 2006). ELWS: Extreme Low Water Spring

Tide; EHWS: Extreme High Water Spring Tide.

It should be noted that zonation on sandy beaches is an extremely

variable phenomenon, on both, the short and the long term (Brazeiro and

Defeo, 1996). Moreover, zones are not defined by sharp boundaries, making

the identification of zonation patterns difficult and often not statistically

supportable (Brazeiro, 1999). The causes and mechanisms for maintenance of

intertidal zones are complex and individual species exhibit great variability and

considerable overlaps with other species. Locomotory and migratory

adaptations of the fauna shuffle and recreate zones daily and with each tidal

cycle. These points indicate a dynamic and variable scenario but it is clear that

zonation occurs, although is not precise, and attempting to delineate it too

finely would be hazardous. At the population level, zonation patterns and

patchiness respond to an environment that is spatially and temporally structured

by sharp gradients. As faunal zones are dynamic, temporal studies are needed


33

for a full picture of zonation patterns, requiring intensive sampling to provide

unbiased estimates.

Biological factors are known to be of key importance in the

establishment and maintenance of zonation on rocky shores, with recruitment,

predation and competition all playing central roles (Underwood and Denley,

1984). On soft shores, however, factors controlling communities are different

(Peterson, 1991). Competition for space is unlikely to be important, because the

mobility of the macrofauna and vertical distribution through the sediment (see

Chapter 5). Because of this mobility, larval recruitment is less critical in

establishing or maintaining zones than in sessile species on rocky shores;

rather, it may play a role in the initial establishment of populations on a beach

(Brown, 1983). The only biological factors likely to be important in affecting

zonation on sandy beaches are predation and competition for food.

1.1.2.5. Feeding habits and survival strategies of the macrofauna

Ocean sandy beaches are a hostile, physically controlled environment

and conditions can vary considerably over very short time periods. Hence,

macrofauna inhabiting sandy beaches should be highly adapted to this dynamic

habitat. Food input to soft intertidals can be defined as erratic and unpredictable

in occurrence and it is strongly related to the external input from the water

column; either as particulate organic matter or as detritic dissolved organic

matter ready to be absorbed or filtrated. Food inputs to beaches may be divided

into the categories listed in Table 1.2. The resident primary producers on

beaches are epipsammic diatoms. On sheltered beaches and flats of fine sand

these may contribute to a measurable, but never high, primary productivity

(McLachlan and Brown, 2006). Several morphological and behavioural

solutions have evolved to cope with the dynamic and variable conditions on

sandy beaches.


34

Food type Source Remarks

Benthic microflora Beach sand On sheltered beaches

Surf diatoms, flagellates Surf water In well-developed surf zones

Stranded macrophytes The sea Near kelp beds, seagrass meadow,

estuaries, etc

Carrion The sea Especially near seabird and seal

colonies

Particulates The sea -

Dissolved organics The sea -

Insects The land Particularly during strong,

offshore winds

Organic detritus The land From dune vegetation

Table 1.2. Food sources for sandy beaches (modified from McLachlan and Brown,

2006).

Trophic groups among the intertidal macrofauna include predators,

scavengers, filter/suspension feeders and deposit feeders (the later only

important on relatively sheltered shores). Most of the food that is consumed in

sandy beaches is exogenous through swash (Romar and McLachlan, 1986) or

wrack input (Colombini and Chelazzi, 2003; Dugan et al., 2003), making

predation amongst macrofaunal species less important. The absence of attached

macrophytes on intertidal sands dictates a predominance of filter feeders and

scavengers among the resident invertebrate macrofauna. There are few highly

specialised feeders on sandy beaches, opportunism being the order of the day.

The number of carnivorous species in sandy beaches is very limited

and some of them feed on the interstitial meiofauna (McLachlan, 1990).

Scavengers, however, are very common on sandy beaches and they accept a

wide variety of food and will typically turn predator when the opportunity

arises because carrion represents a highly erratic food supply. These animals

have developed a number of feeding methods and have acquired several

morphological and behavioural adaptations to locate and consume carrion

efficiently. They can be found anywhere on a beach, from the sublittoral fringe

to the foredunes. In the turbulent environment of the sandy beach, suspended

food is always available, although it may be variable in nature and quantity.

Filter/suspension feeders usually dominate the community making direct

filtering of the swash or interstitial (McLachlan and Brown, 2006) and consist

largely of bivalves. Where conditions are optimal on exposed beaches (for


35

example, in dissipative situations where rich surf diatoms develop), suspension

feeders can maintain huge populations and biomass.

Figure 1.11. Diagrammatic representation of the zonation patterns of the intertidal

macroinfauna in sandy beaches of southern Chile (after Jaramillo et al. 1993).

1.Orchestia tuberculata (Amphipoda), 2.Excirolana hirsuticauda, 3.E. braziliensis,

4.E. monodi (Isopoda), 5.Phalerisidia maculata (Coleoptera), 6.Emerita analoga

(Anomura), 7.Bathypoireiapus magellanicus, 8.Huarp sp., 9.Phoxocephalopsis

mehuinensis (Amph.), 10.Nepthys impresa (Polychaeta), 11.Macrochiridothea setifer,

12.Chaetilia paucidens (Isop.), 13.Lepidopa chilensis (Anom), 14.Bellia picta

(Brachyura), 15.Mesodesma donacium (Bivalvia).

In most situations, and certainly on reflective and intermediate beaches,

motile feeders and scavenger/predators dominate the sandy beach macrofauna.

Where the fauna is impoverished, such as on steep beaches with coarse sand

(Fig. 1.11.), supralittoral macrofauna such as talitrids amphipods may be most

important as a consequence of the absence of truly intertidal forms. Deposit


36

feeders are usually a minor component, except on sheltered shores and in the

sublittoral. Sheltered intertidals are stable enough to allow the construction of

semipermanent burrows deposit feeders. Riccardi and Bourget’s (1999)

analysis of broad community patterns in marine sedimentary communities

showed that deposit feeders increase with more sheltered conditions, finer

sediments and flatter slopes with carnivores also preferring more sheltered

shores.

Macrofauna inhabiting exposed sandy beaches is basically dependent

on phytoplankton and marine macrophytes inputs because of the scant primary

production occurrence on this habitat itself (Inglis, 1989; McLachlan and

Brown, 2006). The sea is by far the more important source of food, supplying

particulates for the filter feeders and carrion and plant debris for the

scavengers. The size of beach populations is therefore probably closely related

to the richness of the inshore waters, particularly in terms of particulate

material (see Chapters 4, 5, and 6). The most important predatory pressure on

sandy beaches is exogenous as well: birds or insects from land and fish or large

crustaceans from the sea.

Other survival strategies refer to the locomotory and migration

adaptations, burrowing mechanisms and orientation. The extremely dynamic

nature of nutrition on sandy beaches in terms of availability and location

highlights the advantage of high mobility of macrofauna which is crucial for

optimising feeding time, reproduction and escape response. Generally, this

predator escape response consists of deep burrowing during low tide, although

some forms have swimming or crawling escape responses (McLachlan and

Brown, 2006). The locomotory and migratory adaptations itself originate from

the combination of three environmental challenges: the instability of the

substratum, the swash action and tide. There exist a number of burrowing

mechanisms depending on the species, whether it is a soft-bodied animal such

as polychaetes and molluscs or a crustacean with rigid exoskeleton. These

mechanisms, as well as reproduction are not the aim of this thesis and will not

be discussed further.


37

1.1.3. Food sources in sandy beaches

1.1.3.1. Food availability

It has been shown that food availability is a major structuring factor of

marine benthos affecting structure and metabolism of the marine benthic

community (e.g. Pearson and Rosenberg, 1987; Graf, 1989; Dugan et al.,

2003), and that species diversity in intertidal soft-sediments is strongly

correlated with food availability (Withlaton, 1981). Moreover, food resources

may be one of the most probable explanations for marine population patchiness

(Decho and Fleeger, 1988) and for benthic community distribution, temporal

variability and metabolism (Montagna, et al., 1983; Rudnick et al., 1985). Food

availability is tightly linked to the biochemical composition of organic matter

(Danovaro et al., 1993) and determining organic matter composition is crucial

in assessing food quality and quantity in benthic ecological studies (see

Chapters 4 and 5).

The biochemical composition of organic matter is the result of the

dynamic equilibrium between external inputs, autochthonous production and

heterotrophic utilisation (Fabiano and Danovaro, 1994). Organic matter in

marine sediments is composed of labile and refractory compounds (Fabiano

and Danovaro, 1994). Simple sugars, fatty acids and proteins that are rapidly

mineralised have been used to assess the labile portion of organic matter

(Fichez, 1991; Danovaro et al., 1993). These labile compounds have been used

to estimate the nutritional value of the sediment (Buchanan and Longbottom,

1970). The biochemical composition of sedimentary organic matter has been

broadly researched in many marine ecosystems, such as deep sea (Danovaro et

al., 1993), semi-enclosed marine systems (Pusccedu et al., 1999), subtidal

sandy sediments (Fabiano et al., 1995), seagrass bed (Danovaro et al., 1994)

and estuarine environments (Fabiano and Danovaro, 1994). However, in spite

of the importance of the biochemical composition of the sedimentary organic

matter (i.e. carbohydrates, lipids and proteins), there is a conspicuous lack of

information about concentrations and variability of these compounds in

intertidal sediments (Incera et al., 2003a).


38

1.1.3.2. The role of the biochemical composition and hydrodynamic

conditions

It is generally admitted that biological richness, abundance and

biomass differ significantly between sheltered and exposed intertidal

environments. Sheltered intertidals have a high abundance and diversity being

important nursery areas for a large number of vertebrate and invertebrate

species (Adam 1990). In the other hand, explained in previous section,

biological richness diminishes with increasing exposure of the intertidal (Fig.

1.9.). This is supposed to be a consequence of the different physical and

hydrodynamic features found between these two opposite intertidal habitats

(McLaclhlan, 1983) and it is suggested that the major hydrodynamic stress of

exposed localities limits their biological richness (McLachlan et al., 1996).

Other hypothesis rather than the Swash Exclusion Hypothesis can be proposed

to explain the relationship between macrofauna and beach characteristics

without being mutually exclusive. The larger availability of organic matter and

the higher retention of organic particles in flat as opposed to steep slope

beaches can explain the observed macrofaunal pattern, i.e., higher abundance

and diversity in sheltered shores compared to exposed beaches (Incera et al.,

2003a, b).

Beach profile and morphodynamics have relevant consequences on the

macrofaunal distribution patterns in the sediments, not only because of the

hydrodynamic activity but also because of the several nutritive contributions

throughout the intertidal profile. While, downshore in the exposed intertidal the

species richness diminishes, macrofauna finds a more stable environment upper

on the shore (Defeo and Gómez, 2005). This tidal level is less influenced by the

swash climate and insects and crustaceans inhabiting this zone are well adapted

to desiccation (McLachlan, 1990; Little, 2000). Invertebrate macrofauna

communities dwelling the supratidal depend largely upon allochthonous inputs

such as drift macrophytes and other stranded material (see Chapter 6)

associated with oceanographic processes (Colombini and Chelazzi, 2003,

Dugan et al., 2003). Sheltered beaches have more favourable environmental


39

conditions and higher sediment stability (see Chapters 4 and 5), which favour a

much wider range of behavioural and morphological adaptations.

Many exposed sandy beaches worldwide receive large amounts of drift

seaweed, known as wrack, from offshore algal beds and closer rocky intertidal

shores (Inglis, 1989; Rossi and Underwood, 2002; Dugan et al., 2003). The

importance of beach accumulations of wrack on the ecology of sandy beaches

has been well supplied in the literature (see Colombini and Chelazzi, 2003 and

references therein). Algal wrack deposits represent the main food resource for

upper shore detritus feeders like talitrid amphipods, oniscoid isopods and

tenebrionid and staphylinid beetles (Colombini and Chelazzi, 2003; Dugan et

al., 2003; Olabarria et al., 2007). Disturbance by wrack has been implicated as

a potentially important factor structuring local assemblages of invertebrates.

Furthermore, wrack also acts as a refuge supply for the supralittoral fauna,

mainly terrestrial and semiterrestrial arthropods, providing an opportunity to

study seaweed debris both as a food resource and shelter habitat (Inglis, 1989;

Colombini and Chelazzi, 2003). The origin and composition of sedimentary

organic matter have been proposed as one of the key factors, together with the

physical environment, for the control of the beach fauna (Incera et al., 2003b).

1.1.4. Aims and thesis linework.

Intertidal shoreline is a threaten ecosystem under increasing pressure

from urbanisation, with 50% of the world’s population now living by the coast

(GESAMP 1990). Because of the overwhelming rate of development on coastal

shorelines during the last decades and the vulnerability of this fragile

ecosystem in this region, there is growing public demand for sustainable

management intervention focused on the use, control and preservation of these

areas (Peterson et al., 2000, Peterson and Bishop, 2005). Furthermore, sandy

beach ecosystem is a highly productive interface between land and sea put at

severe risk of dramatic future modification from impacts of global warming

and consequent sea level rise (Brown and McLachlan, 2002; Peterson and

Bishop, 2005).


40

Together with the recreational interest, we have to take heed of the

outstanding anthropogenic activities in the northern coast of Spain. Galician

coast is well known due to the important production of marine species with

economical interest. For instance, clam and cockle collection by hand is a

common activity in this highly productive area. Coastal shellfish fisheries are

an important socioeconomic productive sector with ecological relevance in

Galician sandy shores. This, together with other economical activities, causes a

relevant effect in the structure and organization of benthic communities from

the intertidals.

Part II. The ecology of sandy beaches.

During this thesis, no quantitative studies had been published on the

macrofauna of sandy beaches from the North coast of Spain. Even more, few

general studies on mesotidal sandy beaches from temperate regions in Europe

have been accomplished. Hence, a baseline study about the ecology of sandy

beaches from this shoreline was required to start this study, and this was the

main task of the second part of this thesis.

Chapter 2 deals with the effect of several environmental factors on

benthic macrofauna inhabiting the most typical kind of exposed soft intertidal

worldwide, i.e., intermediate sandy beaches. The impact of morphodynamics

and abiotic factors on ten intermediate sandy beaches along the north coast of

the Iberian Peninsula was analysed following a gradient of exposure. Several

characteristics of sandy beach fauna were utilised; highlighting biotic factors

such as species richness, macrofauna abundance and biomass. This pioneer

study on sandy beach ecology was complemented with a broader analysis about

intertidal community structure and macrofauna zonation in Chapter 3. This

chapter of the thesis offers a more detailed study of the intertidal zonation,

focused on macrofauna community dynamics in intermediate sandy beaches.

The results obtained in this chapter were compared with several traditional

zonation schemes and it was suggested a possible macrofauna community

distribution and zonation based on the peculiar beach profile found in this

region. Different morphodynamic parameters and biotic factors were further


41

analysed and discussed. These two chapters have been published in Estuarine,

Coastal and Shelf Science.

Part III. The importance of exposure rate in the community structure:

hydrodynamic conditions and food available.

Chapter 4 goes deep in the characteristics of macrofauna community

structure, focusing on wave exposure and food availability in sandy beaches.

The effects of several physical parameters and food availability were analysed

and compared between sheltered and exposed sandy beaches. Both effects have

been considered main factors affecting community structure and benthic

metabolism. The results obtained in this study reaffirm the macrofauna

zonation patterns found previously in intermediate sandy beaches from the

North coast of Spain (Chapter 3). Furthermore, this study underline exposed

sandy beaches as physically controlled environments; while in sheltered

sedimentary environments biological interactions become more important. The

aims of this study were to investigate the influence of the physical

characteristics on the intertidal macroinfauna community along a gradient of

wave exposure and the importance of the food available in beaches with

different hydrodynamic conditions. The results and conclusions obtained in this

chapter were published in Hydrobiologia.

Part IV. The role of food availability in sandy beaches: spatial and

temporal patterns.

Due to the importance of external food inputs in the macrofauna

community structure of sandy beaches, this part of the thesis analysed

separately two types of beaches based on the exposure rate, i.e., sheltered and

exposed. Food availability is a potentially important determinant of consumer

abundance in natural communities, and the densities and growth rates of

consumers may be positively associated with food supply (in situ or

allochthonous) in soft intertidals. Macrofauna communities inhabiting sandy

beaches are supported almost entirely by allochthonous inputs of organic

material, mainly phytoplankton and marine macrophytes (macroalgae,

seagrasses). The role of food available in the exposed intertidal studied was

focused particularly on the wrack input, while in the sheltered intertidal the


42

effect of the biochemical composition of sedimentary organic matter in benthic

macrofauna community was stressed.

Chapter 5 describes the seasonal variability in the vertical distribution

of the benthic macrofauna and sedimentary parameters in a sheltered estuarine

beach. This chapter investigates the relationship between biochemical

composition of the sedimentary organic matter and macroinfauna from a

sheltered beach. This chapter was accepted for publication in Estuaries and

coasts.

In Chapter 6 we used experimental manipulation of algal wrack, i.e.,

artificial patches of macrophytes to test hypotheses about influences on

macrofaunal assemblages inhabiting the upper shore level and drift line of

different sites along an exposed sandy beach. We investigated the abundance of

colonising individuals and species and also succession processes (i.e., sequence

of colonisation and species replacement) and time variability. The novelty of

this study includes the effect of invasive wrack species on macrofaunal

assemblages on sandy beaches. This chapter was accepted for publication in

Journal of Experimental Marine Biology and Ecology.

Part V. General discussion.

In the general discussion, Chapter 7, all results of the previous chapters

were integrated and discussed. Some general concepts in sandy beach ecology

are confirmed, while others are put into question, and new ideas are proposed

based on collected results and observations.

1.1.5. List of references

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473pp.

Bally, R. 1983. Intertidal zonation on sandy beaches of the west coast of South

Africa. Cahiers de Biologie Marine 24: 85-103.

Brazeiro, A. 1999. Community patterns in sandy beaches of Chile: richness,

composition, distribution and abundance of species. Revista Chilena de

Historia Natural 72: 99-111.

Brazeiro, A. 2001. Relationship between species richness and morphodynamics

in sandy beaches: what are the underlying factors?. Marine Ecology

Progress Series 224: 35-44.


43

Brazeiro, A. and Defeo, O. 1996. Macroinfauna zonation in microtidal sandy

beaches: is it possible to identify patterns in such variable

environments. Estuarine Coastal and Shelf Science 42: 523-536.

Brown, A.C. 1983. The ecophysiology of sandy beach animals, a partial

review. In Sandy beaches as ecosystems, A. McLachlan and T.

Erasmus (eds.), The Hague:Junk 575-605.

Brown, A.C. and McLachlan, A. 2002. Sandy shore ecosystems and the threats

facing them: some predictions for the year 2025. Environmental

Conservation 29: 62-77.

Buchanan, J. 1984. Sediment analysis. In: Holme and McIntyre (eds.). Methods

for the study of marine benthos. Oxford and Edinburg Blackwell

Scientific Publications: 41-65.

Buchanan, J.B. and Longbottom, M.R. 1970. The determination of organic

matter in marine muds: the effects of the presence of coal and the

routine determination of proteins. Journal of Experimental Marine

Biology and Ecology 5: 158-169.

Colombini, I. and Chelazzi, L. 2003. Influence of marine allochthonous input

on sandy beach communities. Oceanography and Marine Biology:

Annual review 41: 115-159.

Dahl, E. 1952. Some aspects of the ecology and zonation of the fauna on sandy

beaches. Oikos 4: 1-27.

Danovaro, R., Fabiano, M. and Della Croce, N. 1993. Labile organic matter

and microbial biomasses in deep-sea sediments (Eastern Mediterranean

Sea). Deep sea Research 40: 953-965.

Danovaro, R., Fabiano, M. and Boyer, M., 1994. Seasonal changes of benthic

bacteria in a seagrass bed (Posidonia oceanica) of the Ligurian Sea in

relation to origin, composition and fate of the sediment organic matter.

Marine Biology 119: 489-500.

Davies, J. 1964. A morphogenic approach to Word shorelines. A. Geomorphol.

8: 127-142.

Decho, A.W. and Fleeger, J.W. 1988. Microscale dispersion of meiobenthic

copepods in response to food-resource patchiness. Journal of

Experimental Marine Biology and Ecology 118: 229-243.

Defeo, O. and Martínez, G. 2003. The habitat harshness hypothesis revisited:

life history of the isopod Excirolana braziliensis in sandy beaches with

contrasting morphodynamics. Journal of Marine Biological

Association of United Kingdom 83: 331-340.

Defeo, O and McLachlan, A. 2005. Patterns, processes and regulatory

mechanisms in sandy beach macrofauna. A multiscale analysis. Marine

Ecology Progress Series 295: 1-20.

Defeo, O. and Gómez, J. 2005. Morphodynamics and habitat safety in sandy

beaches: life-history adaptations in a supralittoral amphipod. Marine

Ecology Progress Series 293. 143-153.

Defeo, O., Gómez, J. and Lercari, D. 2001. Testing the swash exclusion

hypothesis in sandy beach populations: the mole crab Emerita

brasiliensis in Uruguay. Marine Ecology Progress Series 212. 159-170.


44

Dexter, D.M. 1983. Community structure of intertidal sandy beaches in New

South Wales, Australia. In McLachlan, A. and T. Erasmus (Eds.),

Sandy Beaches as Ecosystems. The Hague: Junk.

Dugan, J., Hubbard, D.M., McCrary, M.D. and Pierson, M.O. 2003. The

response of macrofauna communities and shorebirds to macrophyte

wrack subsidies on exposed sandy beaches of southern California.

Estuarine Coastal and Shelf Science 58S: 25-40.

Dugan, J., Jaramillo, E., Hubbard, D.M., Contreras, H. and Duarte, C. 2004.

Competitive interactions in macroinfaunal animals of exposed sandy

beaches. Oecologia 139: 630-640.

Fabiano, M. and Danovaro, R. 1994. Composition of organic matter in

sediments facing a river estuary (Tyrrhenian Sea): relationships with

bacteria and microphytobenthic biomass. Hydrobiologia 277: 71-84.

Fabiano, M., Danovaro, R. and Fraschetti, S. 1995. A 3-year time series of

elemental and biochemical composition of organic matter in subtidal

sandy sediments of the Ligurian Sea (north-western Mediterranean).

Continental Shelf Research 15: 1453-1469.

Fichez, R. 1991. Composition fate of organic matter in submarine cave

sediments; implications for the biogeochemical cycle of organic

carbon. Oceanologica Acta 14: 369-377.

GESAMP (Joint Group of Experts on the Scientific Aspects of Marine

Pollution) 1990. The state of the environment. Blackwell Scientific

Publications, Oxford.

Graf, G. 1989. Pelagic-benthic coupling in a deep-sea benthic community.

Nature 341: 437-439.

Incera, M., Cividanes, S.P., López, J. and Costas, R. 2003a. Role of

hydrodynamic conditions on quantity and biochemical composition of

sediment organic matter in sandy intertidal sediments (NW Atlantic

coast, Iberian Peninsula). Hydrobiologia 497: 39-51.

Incera, M, S.P. Cividanes, M. Lastra & J. López 2003b. Temporal and spatial

variability of sedimentary organic matter in sandy beaches on the

northwest coast of the Iberian Peninsula. Estuarine, Coastal and Shelf

Science 58: 55-61.

Inglis, G., 1989., The colonisation and degradation of stranded Macrocystis

pyrifera (L.) C. Ag. by the macrofauna of a New Zealand sandy beach.

Journal of Experimental Marine Biology and Ecology 125: 203- 217.

Jaramillo, E. and Gonzales, M. 1991. Community structure of the macrofauna

along a dissipative-reflective range of beach category in southern

Chile. Studies on Neotropical Fauna and Environment 26: 193-212.

Jaramillo, E. and McLachlan, A. 1993. Community and population responses

of the macroinfauna to physical factors over a range of exposed sandy

beaches in south-central Chile. Estuarine Coastal and Shelf Science 37:

615-624.

Jaramillo, E., McLachlan, A. and Coetzee, P., 1993. Intertidal zonation patterns

of macroinfauna over a range of exposed sandy beaches in south

central Chile. Marine Ecology Progress Series 101: 105-118.

Little, C., 2000. The Biology of Soft Shores Estuaries. Oxford University Press,

N. York. 252pp


45

Margalef, R. 1996. Ecología. Ed. Omega. 951 pp.

Masselinck, G. and Short, A. 1993. The effect of tide range on beach

morphodynamics and morphology: a conceptual beach model. Journal

of Coastal Research 9 (3): 785-800.

Mees, J. and Jones, M. 1997. The hyperbenthos. Oceanography and Marine

Biology: Annual review 35: 221-255.

McArdle, S and McLachlan, A., 1992. Sand beach ecology: Swash features

relevant to the macrofauna. Journal of Coastal Research. 8: 398-407.

McLachlan, A. 1980. The definition of Sandy Beaches in Relation to Exposure:

Simple Rating System. South African Journal of Science. 76, 137-138.

McLachlan, A. 1983. Sandy beach ecology: a review. In: A. McLachlan and T.

Erasmus, (eds.). Sandy Beaches as Ecosystems. Junk. The Hague, The

Netherlands. 321-380 pp.

McLachlan, A. 1990. Dissipative beaches and macrofauna communities on

exposed intertidal sands. Journal of Coastal Research 1, 57-71.

McLachlan, A. 1996. Physical factors in benthic ecology: effects of changing

sand particle size on beach fauna. Marine Ecology Progress Series 131:

205-217.

McLachlan, A. and Jaramillo, E., 1995. Zonation on Sandy Beaches.

Oceanography and Marine Biology: an Annual Review 33: 305-335.

McLachlan, A. and A. Dorvlo 2005. Global patterns in sandy beach

macrobenthic communities. Journal of Coastal Research 21(4): 674-

687.

McLachlan, A., Brown, A.C., 2006. The ecology of sandy shores. Acad. Press,

Amsterdam.

McLachlan, A., Jaramillo, E., Donn, E. and Wessels, F., 1993. Sandy Beach

Macrofauna Communities and their Control by the Physical

Environment: A Geographical Comparison. Journal of Coastal

Research 15: 27-38.

McLachlan, A., Jaramillo, E., Defeo, O., Dugan, J., de Ruyck, A. and Cohetes,

P. 1995. Adaptations of bivalves to different beach types. Journal of


McLachlan, A., de Ruyck A. and Hacking, N. 1996. Community structure on

sandy beaches: patterns of richness and zonation in relation to tide

range and latitude. Revista Chilena de Historia Natural 69: 451-467.

Montagna, P.A., Coull, C.B., Herring, T.L. and Dudley, B.W. 1983. The

relationship between abundances of meiofauna and their suspected

microbial food (diatoms and bacteria). Estuarine, Coastal and Shelf

Science 17: 381-394.

Olabarria, C., Lastra, M. and Garrido, J. 2007. Succession of macrofauna on

macroalgal wrack of an exposed sandy beach: Effects of patch size and

site. Marine Environmental Research 63: 19-40.

Pearson, T.H. and R. Rosenberg 1987. Feast and famine: Structuring factors in

marine benthic communities. In Gee, J.H.R. & P. S. Giller (eds.).

Organization of Communities, Past and Present. Blackwell Scientific

Publication, Oxford: 373-395.

Peterson, C.H. 1991. Intertidal zonation of marine invertebrates in sand and

mud. American Scientist 79: 236-249.


46

Peterson, C.H., Hickerson, D.H.M., and Johnson, G.G. 2000. Short-term

consequences of nourishment and bulldozing on the dominant large

invertebrates of a sandy beach. Journal of Coastal Research 16: 368-

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Peterson, C.H. and Bishop, M.J. 2005. Assessing the environmental impacts of

beach nourishment. Bioscience 55: 887-896.

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Seasonal and spatial changes in the sediment organic matter of a semi-

enclosed marine system (W-Mediterranean Sea). Hydrobiologia 397:

59-70.

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biomass in marine intertidal communities. Marine Ecology Progress

Series 185: 21-35.

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accumulations. Journal of Fish Biology 28: 93-104.

Rossi, F., and Underwood, A.J. 2002. Small-scale disturbance and increased

nutrients as influences on intertidal macrobenthic assemblages:

experimental burial of wrack in different intertidal environments.

Marine Ecology Progress Series 241, 29-39.

Rudnick, D.T., Elmgren, R. and Frithsen, J.B. 1985. Meiofaunal prominence

and benthic seasonality in a coastal marine ecosystem. Oecologia 67:

157-168.

Salvat, B. 1964 Les conditions hydrodynamiques interstitielle des sédiment

meubles intertidaux et la répartition verticale de la jeune endogée C.R

Academie Sciences Paris, 259:1567-1579

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embaymentisation in beach classifications: a review. Revista Chilena

de Historia Natural 69: 589-604.

Short, A. 1999. Handbook of beach and shoreface morphodynamics. J. Wiley

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McLachlan, A., Erasmus, T. (Eds.) Sandy Beaches as Ecosystems.

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preliminary account of two sandy beaches in south west India. Marine

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diversity. Journal of Experimental Marine Biology and Ecology 53: 31-

45.

PARTE I. INTRODUCCIÓN Y OBJETIVOS.

(Según el acuerdo de 18/06/04 firmado por la Comisión de Doctorado de la

Universidad de Vigo acerca del idioma en que puede escribirse la Tesis doctoral).

Capítulo 1. Introducción general.

Capítulo 1 Introducción

49

1.1.1. Intermareal arenoso: Playas.

1.1.1.1. ¿Qué es una playa?

Comúnmente conocidas como playas, los intermareales arenosos son

ambientes muy dinámicos, hostiles y cosmopolitas (McLachlan, 1996) que han

sido definidos de múltiples maneras para un amplio rango de ambientes, a

veces incluso de forma poco rigurosa.

“una acumulación de arena depositada por el oleaje comprendida entre

la base modal de la ola (i.e. la máxima profundidad a la cual la ola puede

transportar sedimento hacia la orilla) y el límite superior de su zona de batida”

(Short, 1999).

De esta definición surgen los tres requisitos básicos que conforman una

playa: arena, oleaje y la marea. La arena que se ve transportada por el oleaje y

las mareas hacia la orilla conforma una playa. Estos tres factores, en su

conjunto van a determinar la morfodinámica, las comunidades faunísticas; así

como la cantidad y la calidad de la materia orgánica (i.e. disponibilidad de

alimento) que nos encontramos en las playas. En este estudio las playas serán

consideradas, por tanto, como áreas litorales arenosas expuestas al mar

incluyendo la zona de asomeramiento (“shoaling”), la zona de rompiente

(“surf”) y la zona de batida (“swash”) donde se disipa el oleaje (Figura 1.1).

La arena, y por extensión el sedimento, pueden ser clasificados de

acuerdo con su origen y el tamaño de grano. El componente más común de la

arena es el sílice, generalmente en forma de cuarzo (lo que indicaría un origen

terrestre) aunque también es frecuente la presencia de carbonatos (origen

marino). En algunas ocasiones la arena puede estar formada por cascajo de

conchas, materiales volcánicos, coralinos o rocas de diferente origen en forma

de guijarros. Aunque en sedimentología el tamaño de grano se define de

acuerdo con la escala de Wenthworht (Buchanan, 1984) en unidades phi (φ = -

log2 Ø), en este estudio y en la mayoría de los trabajos actuales sobre ecología

de playas se utiliza la escala métrica decimal. Así, cualquier tipo de sedimento


50

entre 63 μm y 2 mm (0<φ<4) se definirá como arena. El tamaño de grano ha

sido considerado determinante en la estructura de la comunidad faunística en

todos los trabajos relevantes sobre ecología de playas (e.g. Jaramillo y

González, 1991; McLachlan y Dorvlo, 2005; Defeo y McLachlan, 2005) y será

también tratado en este estudio.

Una ola es, en general, el transporte de energía dirigida por el viento a

través del agua. La ola permanece estable mientras que la altura de la misma

(H) sea inferior a 1/7 de su longitud (L) (Figura 1.2.). La acción del oleaje

penetra en la columna de agua hasta una profundidad de aproximadamente la

mitad de la longitud de la ola. Cerca de la orilla, la profundidad del agua

disminuye hasta un punto donde la base de la ola toca el fondo marino. A partir

de aquí, la ola ya no transporta sólo energía sino también material

sedimentario. Esta es, según la definición de Short, la base modal de la ola y

por tanto el límite inferior de nuestra playa. Las olas a partir de este momento

empiezan a compactarse, la longitud de la ola disminuye y la proporción entre

la altura y la longitud de la ola aumenta. Esto corresponde con lo que se

denomina asomeramiento (Fig. 1.1.). La velocidad de la parte baja de la ola se

ralentiza progresivamente debido al arrastre creado por el sedimento y la ola se

hace dependiente de la profundidad; mientras que la parte superior de la ola se

mueve con una velocidad diferente (Fig. 1.2.). La rotura de la ola se produce

cuando la proporción H / L sobrepasa el punto de estabilidad de 1/7 en la zona

de rompiente del oleaje. En la última fase, tras la rotura de la ola, la lámina de

agua llega a la línea de costa y asciende por la pendiente de la playa y

posteriormente desciendo por efecto de la gravedad, mientras la energía de la

ola se disipa. Esta parte se conoce como la zona de batida o zona de swash

(Fig. 1.1.).

La zona de rompiente es un área de rotura turbulenta caracterizada por

una arena conchífera gruesa, agua cargada de arena en suspensión y fuerte

corriente (Figura 1.3.). La zona de batida alcanza la playa, salpicando y

cubriendo la pendiente en forma de una pequeña película de agua dependiendo

entre otras cosas de la fuerza de la ola y del rango mareal; así como de la

pendiente de la playa. Comprende el nivel máximo de subida de las olas y una


51

zona de agua casi estancada. Tradicionalmente la zona de swash se ha dividido

en una parte saturada, siempre ocupada por el agua, y una insaturada, mojada

periódicamente por las grandes olas y caracterizada por un drenaje sucesivo

entre ola y ola. La zona de rompiente y la de batida saturada se conocen

también como ambiente sublitoral de la playa, mientras que la zona insaturada

correspondería con el mesolitoral (Dahl, 1952). Dependiendo de las

condiciones dinámicas de marea y oleaje habrá una zona de mayor o menor

tamaño permanentemente sumergida en la playa, incluso durante las mareas

más vivas. Finalmente nos encontramos con una zona de riego que nunca va a

estar cubierta por el oleaje pero que sufre la aspersión del mismo. Corresponde

a la parte más alta de la playa y normalmente está compuesta por algún tipo de

complejo dunar. Este ambiente se conoce también con el nombre de zona

supralitoral o subterrestre permanentemente seca y donde la desecación y la

temperatura son los factores de estrés principales para la fauna.

1.1.1.2. El ambiente físico: rango mareal y estratificación del sistema

Las mareas no son un elemento esencial para la formación de una

playa; sin embargo, un aumento de su rango mareal contribuirá

sustancialmente, junto con el oleaje, a la morfología de la playa. Las mareas

provocan impactos esenciales ya que cambian continuamente el perfil de la

orilla, tanto horizontalmente como verticalmente dependiendo del rango mareal

y del perfil del intermareal. En zonas de gran rango mareal, la variación de la

marea puede modificar la rotura de la ola aumentando la zona de

asomeramiento en bajamar. La movilidad de la orilla por sí misma también

cambia las zonas de batida, rompiente y asomeramiento (Short, 1999). Los

ambientes de marea fueron clasificados por Davies (1964) en tres tipos (Figura

1.4.): micromareales (TR < 2 m), mesomareales (2 < TR < 4 m) y

macromareales (TR > 4 m). El punto más alto alcanzado por el oleaje en

mareas vivas se toma tradicionalmente como el límite superior del intermareal

arenoso (“spring high tide”), de acuerdo con la definición de playa que estamos

utilizando (Figure 1.5.). Debido a la variación mareal, durante la bajamar las

playas muestran una zona amplia donde se produce drenaje de agua.


52

Particularmente en el sistema de playas expuestas, la gran extensión vertical

que experimenta el sistema y el drenaje permite una subdivisión del intermareal

en capas o estratos.

Varios esquemas se han propuesto para explicar esto (Salvat, 1964;

McLachlan, 1980) y uno de los más utilizados se puede ver en la Figura 1.6.

Las capas se extienden desde una superficie de arena seca en la parte alta de la

playa hasta una zona permanentemente saturada bajo la capa freática y ligada al

swash. Las últimas capas tienen una menor circulación y tienden a estancarse,

mientras que en la zona de resurgencia el agua drena gravitacionalmente a

través del sedimento durante el flujo de la marea. En el límite superior de esta

zona aparece la capa freática. La zona de retención es el lugar óptimo para la

fauna intersticial ya que se ve alcanzada por el agua de todas las mareas

creándose un buen balance entre la disponibilidad de oxígeno, agua y alimento

así como cierta estabilidad física (McLachlan y Brown, 2006). También pierde

el agua gravitacional pero queda retenida el agua por capilaridad durante la

bajamar quedando el sedimento húmedo pero no saturado.

Pero una playa es mucho más que la zona litoral. El intermareal

arenoso es un ambiente que sirve de enlace entre el ecosistema marino y el

terrestre. De una forma general podemos incluir al menos dos sistemas

ecológicos: uno dunar, con fauna predominantemente terrestre y controlada

principalmente por el viento y una zona de oleaje con fauna marina controlada

por las olas y las mareas. Las posibles divisiones que nos podemos encontrar en

esta última zona se discutirán en profundidad en el Capítulo 3.

1.1.1.3. Morfodinamismo

La morfología de las playas se debe fundamentalmente a interacciones

entre los procesos de sedimentación, el oleaje y las corrientes marinas, en lo

que se dio por llamar morfodinámica de playas. Las primeras clasificaciones de

las playas fueron hechas atendiendo a los procesos hidrodinámicos que están

detrás de su forma deposicional (Short y Wright, 1984) obteniéndose dos tipos

de playas: disipativas y reflectivas. Esta primera impresión se vio ampliada con


53

estudios posteriores, clasificando múltiples estados intermedios entre estos dos

extremos.

Dentro de este esquema general, nos encontramos con múltiples

variaciones generando un rango amplio de tipos de playas. Estas variaciones

serán debidas al tipo de sedimento, tamaño del grano, oleaje, morfología de la

orilla, rango mareal y exposición del intermareal. Muchos de estos factores son

a su vez interdependientes. El tamaño de grano, por ejemplo, depende de la

acción del oleaje, la cual a su vez depende del grado de exposición y del perfil

de la orilla. La mayor parte de las clasificaciones de las playas están basadas en

tres parámetros: el tamaño de grano del sedimento, el oleaje y el rango mareal.

La clasificación de playas más ampliamente aceptada (Figura 1.7.), usando

estos parámetros, fue introducida por Masselinck y Short (1993). En el eje

horizontal, el parámetro Dean (Ω = Hb / Ws * T) se encuentra en función de la

velocidad de sedimentación de las partículas (Ws), la altura media de la ola en

la rompiente (Hb) y el periodo de la ola (T) y divide las playas en tres tipos:

reflectivas (Ω < 1), intermedias (1 < Ω < 6) y disipativas (Ω > 6). El rango

mareal relativo (RTR = MSR/Hb) en el eje vertical se calcula a partir de la

media del rango mareal de mareas vivas y la altura media de la ola en la

rompiente y su importancia aumenta a medida que se incrementa la influencia

mareal en la playa (ver 1.1.1.2.).

Una playa reflectiva se caracteriza por pendientes pronunciadas y

sedimento grueso. Se asocia a un oleaje de baja energía donde la ola rompe

directamente encima del perfil de la playa, sin apenas zona de rompiente. La

zona de batida es estrecha y de gran velocidad. Por el contrario, la playa

disipativa tiene tendencia a un aplanamiento de la pendiente con arenas más

finas. Se amplia la zona de rompiente, lo que promueve la aparición de barras

de arena paralelas a la orilla, lo que provoca que las olas se rompan y formen

de nuevo varias veces. Las olas rompen lejos de la playa y la energía se disipa a

lo largo de la rompiente. Una playa intermedia será cualquier tipo de playa

que se encuentre entre estos dos tipos y su principal característica es la

variabilidad, además de ser el tipo de playa más frecuente (Fig. 1.7).


54

Todos los intentos de clasificar las playas incluyen de alguna forma

información sobre el oleaje (Davies, 1964; Masselink y Short 1993). Aunque el

régimen del oleaje probablemente es el agente más importante en la formación

de playas, es difícil de medir en el campo y se puede cuestionar hasta qué punto

este régimen, en un momento dado, es representativo de las olas que han

conformado la playa. Además, tanto el parámetro Dean como el RTR han sido

criticados como medidas exclusivamente predictivas y no descriptivas (Short,

1999). Por lo tanto se han ido desarrollando parámetros de clasificación de las

playas que no requieran medidas del oleaje y/o que sean herramientas más

descriptivas. Un primer intento a partir de una serie de estudios comparativos

(McLachlan et al., 1993) creó el índice del estado de la playa (BSI, en sus

siglas en inglés), limitándose a combinar los efectos del parámetro Dean y del

RTR (ver Capítulos 2 y 3). Otros parámetros más recientes (ver McLachlan y

Dorvlo, 2005) son el índice de playa y el índice de depósito de playa (BI y

BDI). Ambos usan la pendiente del intermareal y la información del sedimento,

dos parámetros que pueden ser medidos fácilmente en la playa. El primer

índice también incluye el rango mareal, lo que facilita la comparación entre

playas a una escala espacial mayor (ver Capítulo 4). Mientras que el BDI se

presta más a estudios de una escala espacial menor, con ninguna o menor

diferencia en el rango mareal entre las playas estudiadas.

Además de por la morfodinámica, las playas se pueden clasificar

también en función de su grado de exposición. Aunque se basa en variables

indirectas, con parámetros difíciles de medir o con gran variabilidad espacio

temporal, unifica una serie de conceptos ecológicamente relevantes. Una

clasificación de fácil comprensión fue propuesta por McLachlan, (1980)

estableciendo cuatro categorías, desde muy expuesta a muy protegida, definidas

en base al oleaje y características biológicas y morfodinámicas (Tabla 1.1.).

Una playa es un sistema altamente dinámico en donde los cambios

espaciales y temporales de las características físicas y morfológicas son

habituales. Factores físicos como la textura del sedimento y las condiciones del

swash han sido reconocidos desde hace mucho tiempo como definitorios de la


55

respuesta de la macrofauna bentónica de los intermareales arenosos (e.g.

McArdle y McLachlan, 1992; McLachlan, 1996; Defeo y McLachlan, 2005).

La textura del sedimento determinará, entre otras cosas, la porosidad

del sustrato (i.e. el volumen del espacio entre los granos de arena), la

permeabilidad (i.e. la tasa de percolación del agua a través de la arena) y la

penetrabilidad (i.e. la fuerza necesaria para penetrar en la arena); así como la

velocidad de filtración del agua en el sedimento y el contenido en agua de la

propia playa. En general, las arenas más gruesas filtran mucha más agua pero

retienen mucha menos. Esto da como resultado una mayor permeabilidad pero

menor porosidad de la arena y por tanto, el nivel de saturación en agua en

playas de grano más grueso es mucho menor. Por tanto, la superficie del nivel

freático (i.e. nivel por debajo del cual el sedimento está saturado en agua) se

encuentra más baja en este tipo de playa. Esta superficie del nivel freático, o la

transición entre superficie de arena saturada e insaturada, se denomina línea

efluente (EL) y se reconoce visualmente en las playas como un lámina de

espejo (Fig. 1.3.).

El swash es el agente que transfiere energía del oleaje y agua a la playa.

Como tal, las características del swash son cruciales en la formación de playas.

El periodo, la velocidad y el intervalo del swash son, en teoría, menos

favorables para la macrofauna en las duras condiciones de las playas

reflectivas, con cortos periodos e intervalos y mayor velocidad de swash

especialmente a nivel de la bajamar (McArdle y McLachlan, 1992; Short,

1999). El swash además es directamente dependiente de las condiciones del

oleaje así como de la morfología y pendiente de la playa.

1.1.2. Comunidades de la macrofauna bentónica

1.1.2.1. ¿Qué es la macrofauna?

Las definiciones de macrofauna o macrobentos varían de acuerdo con

los diferentes autores. Así por ejemplo, Mees y Jones (1997) definen el

macrobentos como toda fauna marina dependiente del sedimento y que se ve


56

retenida por un tamiz de luz de malla de 1 mm. Una mayor subdivisión de este

término englobaría a otros tres grupos: el endobentos (i.e. animales que viven

en el sedimento), epibentos (i.e. animales que viven sobre el sedimento) e

hiperbentos (i.e. animales que viven en la columna de agua por encima del

fondo marino). Estas categorías no tienen límites bien definidos ya que algunas

especies, por ejemplo, son parcialmente endobentónicas e hiperbentónicas. En

general, las divisiones se basan en el material de muestreo empleado. Además

otros autores extienden el término de macrofauna a todos aquellos animales

retenidos en un tamiz de luz de malla de 0.5 mm (e.g. Brazeiro y Defeo, 1996;

Defeo y Martínez, 2003). En este estudio usaremos el término macrofauna para

aquellos animales que viven enterrados en el sedimento y han sido muestreados

por medio de un corer cilíndrico de extracción y una bolsa de malla de 1 mm

(Figura 1.8.).

Durante mucho tiempo las playas han sido consideradas desiertos

marinos y olvidadas como importante fuente de estudio a favor del visualmente

más exuberante litoral rocoso. La naturaleza de cambio constante típica de las

playas ha sido considerada como la fuerza estructurante principal de las

comunidades macrofaunísticas (McLachlan, 1983). Pero a pesar de su

apariencia uniforme y su, a primera vista, pobreza faunística, las playas pueden

estar habitadas por una gran diversidad faunística y de riqueza de especies.

1.1.2.2. Macrofauna en las playas

La macrofauna dominante de las playas, tal y como la hemos definido

anteriormente, consiste principalmente en animales pertenecientes a tres

taxones: Crustacea, Annelida (principalmente poliquetos) y Mollusca. La

composición y distribución de esta macrofauna está supeditada y adaptada a un

ambiente tan dinámico como es el del intermareal arenoso. Así; las diferencias

faunísticas que nos encontramos a macroescala (entre las distintas geografías y

latitudes costeras), mesoescala (zonación dentro de una misma playa debida al

hidrodinamismo de la misma) o incluso a nivel de microescala (interacciones


57

tales como la depredación y competencia) han dado lugar a un ecosistema1 con

una gran riqueza específica, abundancia y biomasa (McLachlan y Brown,

2006). Aunque también se han realizado estudios que comprenden la

meiofauna y la microfauna, la macrofauna es uno de los componentes más

notables de la fauna presente en las playas y el más fácil de recolectar e

identificar. Las características más destacables son su gran movilidad y

habilidad para enterrarse rápidamente en el sedimento. Se ha sugerido que los

crustáceos dominan en general las playas más expuestas y los poliquetos las

más protegidas mientras que los moluscos serían los más abundantes en

situaciones intermedias (Dexter, 1983) aunque esta distribución teórica varía en

muchas ocasiones (ver capítulos 3 y 4).

1.1.2.3. Patrones de distribución de la macrofauna

Dentro de una misma región geográfica, el patrón general de la

macrofauna de playas muestra un descenso en la riqueza específica, la

abundancia y la biomasa a lo largo de un gradiente morfodinámico (Figura

1.9.), desde un estado disipativo más suave a uno reflectivo más duro. Este

patrón, que aparece en cualquier latitud del planeta, se ha convertido ya en un

paradigma en la ecología de playas (e.g. Defeo y McLachlan 2005; McLachlan

y Brown, 2006). Las playas pueden ser descritas mediante un conjunto de

parámetros físicos, la mayor parte de los cuales son factores estructurantes de la

composición faunística. De hecho se consideran ambientes controlados

físicamente, donde el papel de los factores biológicos a la hora de estructurar

las comunidades2 a veces es dudoso (McLachlan y Jaramillo, 1995).

1 Por ecosistema en este texto, se hace referencia a un sistema formado por individuos

de muchas especies, en el seno de un ambiente definido, e implicados en un proceso de

interacción, expresable bien como intercambio de materia y energía, bien como una

secuencia de nacimientos y muertes, y uno de cuyos resultados es la evolución a nivel

de las especies y la sucesión a nivel de sistema entero (Margalef, 1995).

2 En ecología se estudian las distribuciones, abundancias y las interacciones entre los

organismos en una variedad de escalas espaciales de organización. El problema surge a

la hora de considerar a todo el conjunto de especies que encontramos en el mismo

lugar. La comunidad es supuestamente la unidad real de estudio de muchos ecólogos y

tiene al menos dos puntos de vista diferentes a la hora de determinar este concepto. Un

punto de vista considera a las especies como integrantes de comunidades que tienen


58

La riqueza específica, por ejemplo, aumenta a medida que disminuye el tamaño

de grano y la pendiente de la playa, a medida que aumenta el rango mareal y la

anchura del intermareal y/o a medida que disminuye la dureza del swash (e.g.

Jaramillo y McLachlan, 1993; Brazeiro, 1999; McLachlan y Dorvlo, 2005).

La principal hipótesis propuesta para explicar la relación entre la

macrofauna y la morfodinámica de las playas se conoce como la “Hipótesis de

Exclusión del Swash” (SEH en sus siglas en inglés). En esta hipótesis se

sugiere que las condiciones de dureza del swash, junto con un perfil de

pendiente pronunciada determinan un descenso progresivo en la diversidad y

abundancia de la macrofauna. Esto puede llevar, en situaciones extremas, a la

completa exclusión de especies intermareales en dicha zona (McLachlan et al.,

1995). Esta teoría sugiere que la capacidad de las especies para enterrarse

podría ser un factor determinante en la distribución de las especies y en la

estructura de la comunidad en playas con distinta pendiente (Dugan et al.,

2004). Las especies con mayor capacidad de enterramiento serían por tanto

capaces de habitar con éxito playas de pronunciada pendiente y swash muy

activo. Como contraste, en playas con una pendiente más suave podremos

encontrarnos con organismos con un rango más amplio de comportamientos y

adaptaciones morfológicas. Además hay que tener en cuenta la existencia de

especies semiterrestres que viven en la parte superior de los intermareales

una serie de características que han persistido en el tiempo (e.g. la composición de

especies) y que se repite en distintos lugares. Por tanto desde este punto de vista la

comunidad de especies está organizada, estructurada e integrada. Las especies son

interdependientes e interactivas y a veces se presume que las interacciones son, al

menos en parte, responsables en el mantenimiento de la entidad. El punto de vista

alternativo presupone que el término comunidad se usa para describir el conjunto de

organismos que se encuentran en el mismo lugar en el mismo momento. Pueden o no

ser interdependientes, pueden o no interactuar. Existe coexistencia debido a que tienen

las mismas respuestas fisiológicas al ambiente y/o las mismas necesidades alimenticias

o de protección o alternativamente porque algunas especies son necesarias como

presas. La realidad posiblemente, como en la mayor parte de las ocasiones, se

encuentre en algún punto en el medio de estas dos consideraciones. Para evitar

confusiones, las dos aproximaciones ecológicas van a ser referidas aquí usando el

término “comunidad” para el fuertemente relacionado y consistente conjunto de

especies y el término “asociación” para la relación más holgada de especies

concurrentes, donde el conjunto total de especies no es un grupo repetible o

identificable de forma coherente (Underwood, 2006).


59

arenosos con independencia de los efectos del swash y que no van a mostrar

ninguna de estas tendencias (Defeo y McLachlan, 2005). En términos de

población faunística esto se ha traducido en la llamada “Hipótesis de la Dureza

del Hábitat” (HHH; Defeo et al., 2001) que predice que en playas reflectivas la

dureza del ambiente obliga a la macrofauna a emplear una gran parte de su

energía en sobrevivir, dejando menos cantidad disponible para la reproducción

y provocando además una mayor mortalidad. Brazeiro (2001) incluye además

del swash, las dinámicas de acreación-erosión de las playas como posible

influencia en la estructura de la macrofauna. Todas estas ideas han sido

sintetizadas en la “Hipótesis del Control Físico a Macroescala” (McLachlan y

Dorvlo, 2005) donde dos niveles de factores controlarán los patrones

principales de distribución faunística a nivel de macroescala. El primer nivel

posee dos factores principales; el rango mareal y la latitud, que determinarán el

número de especies que pueden ocurrir en condiciones ideales en una región

determinada. El segundo nivel mediado por el swash, el tamaño del sedimento

y la estabilidad de la playa que actuarán como factores excluyentes de aquellas

especies menos adaptadas a las condiciones duras del estado reflectivo.

1.1.2.4. Zonación de la macrofauna en la playa

La zonación faunística en intermareales es una característica bien

descrita y estudiada en ecología de playas. La zonación en playas no es, ni de

cerca, tan visible como en el litoral rocoso, probablemente como consecuencia

del ambiente tan dinámico de la playa y las poblaciones tan cambiantes que la

ocupan. Al igual que a nivel de macroescala, la variabilidad en los factores

físicos se considera la primera fuerza que controla las comunidades

macroinfaunales y sus asociaciones en las playas (McLachlan, 1983). La

macrofauna se distribuye a lo largo y ancho del intermareal. De hecho se han

encontrado fuertes relaciones entre la riqueza de especies y la longitud de la

playa (Brazeiro, 1999). En general las poblaciones macrofaunísticas están más

desarrolladas en la zona media de la playa presentando una distribución

unimodal en forma de campana hacia los lados. Otros factores, como la

presencia de zonas rocosas, el impacto antropogénico, aportes de estuarios o la


60

forma de la propia playa van a afectar la distribución longitudinal de la

macrofauna en playas (McLachlan y Brown, 2006). En el caso de la

distribución horizontal a través del perfil de la playa, la macrofauna muestra

unos patrones generales o zonación; es decir, nos encontramos con la suma de

las respuestas de cada especie al gradiente intermareal. El patrón tradicional de

distribución horizontal muestra un aumento en el número de especies a medida

que nos dirigimos a la línea de agua (McLachlan y Jaramillo, 1995; McLachlan

y Brown, 2006).

Se han hecho varios intentos para establecer esquemas de zonación de

la macrofauna de playas (ver McLachlan y Jaramillo, 1995). Dos de ellos han

sido los más utilizados tradicionalmente: el esquema de Dahl (Dahl, 1952) que

divide la playa en tres zonas distintas basándose en la distribución de

crustáceos y las cuatro zonas físicamente delimitadas del esquema de Salvat

(Salvat, 1964) basado en el contenido en agua del sedimento a través del

intermareal (Figura 1.10. y Fig. 1.6.). La correspondencia entre ambos

esquemas es bastante buena y el resto de las zonaciones propuestas por

diversos autores generalmente pueden considerarse variaciones de estos dos

esquemas. Un esquema que quizás sea el más elemental, pero también el que se

puede aplicar más ampliamente, fue propuesto por Brown (en McLachlan,

1983 y citado en McLachlan y Brown, 2006) sugiriendo que sólo se podían

reconocer claramente dos zonas en los intermareales arenosos (ver capítulo 3).

Una zona habitada por animales de vida aérea (básicamente crustáceos) por

encima del punto más alto de sedimento depositado por las olas (drift line) y

otra habitada por verdaderas especies marinas en contacto directo con el agua.

La conclusión general, y una de las ideas más comúnmente citada, es que no

existe una zonación clara en las playas (McLachlan y Brown, 2006).

Varios estudios en diversas regiones del planeta sugieren que los

distintos tipos de playas y los diferentes factores físicos podrían causar

variaciones en la zonación de la macrofauna (e.g. Trevallion et al., 1970; Bally,

1983; Jaramillo et al., 1993; McLachlan y Jaramillo, 1995). Por un lado, las

playas disipativas e intermedias poseen una mayor riqueza en las zonas

inferiores del intermareal mostrando una división en tres e incluso cuatro zonas


61

diferentes de distribución de especies. En el otro lado las playas reflectivas

muestran un empobrecimiento de la fauna intermareal sobre todo a causa del

mayor hidrodinamismo en la zona inferior de la playa. En este último caso se

dibuja una única zona de especies en el supralitoral o como mucho dos franjas

diferentes de especies cuando las condiciones no son tan duras (Figura 1.11.).

En general se puede considerar que las zonas son más fáciles de delimitar en

las partes altas de la orilla mientras que el esquema se desdibuja a medida que

nos dirigimos hacia la zona de batida (McLachlan y Jarmillo, 1995) donde la

aplicabilidad del esquema de Dahl desaparece en las zonas inferiores de las

playas reflectivas extremas (Fig. 1.9.). Una dificultad añadida para establecer

un esquema zonal se debe a la capacidad locomotora y a las adaptaciones

migratorias de la mayor parte de las criaturas que habitan el intermareal.

Podemos decir que la zonación en playas es un fenómeno

extremadamente variable tanto a corto como a largo plazo (Brazeiro y Defeo,

1996). Además, las zonas no están definidas por límites precisos, mostrando un

solapamiento zonal considerable entre las distintas especies lo que hace este

trabajo mucho más dificultoso y a menudo con poca validez estadística

(Brazeiro, 1999). Todo esto muestra un patrón espacial discreto de la

macrofauna de playas en forma de parches o manchas que se relacionan entre sí

y que muestran una cierta dinámica o cambio tanto en el espacio como en el

tiempo.

Los factores biológicos son una clave importante en el establecimiento

y mantenimiento de la zonación en el litoral rocoso, con reclutamiento,

depredación y competición jugando un papel central (Underwood y Denley,

1984). En intermareales arenosos, sin embargo, los factores que controlan la

comunidad son diferentes (Peterson, 1991). La competencia por el espacio, por

ejemplo es de improbable importancia debido a la movilidad de la fauna y a

cierta distribución vertical de la fauna en el sedimento (ver Capítulo 5). A

causa de esta movilidad, el reclutamiento de las larvas es menos crítico a la

hora de establecer las zonas que en un litoral rocoso aunque sí puede jugar un

papel inicial importante en el establecimiento de las poblaciones en la playa

(Brown, 1983). Los factores biológicos más importantes en la zonación de la


62

macrofauna en playas se centran más en la depredación y la competencia por el

alimento.

1.1.2.5. Hábitos alimenticios y estrategias de supervivencia de la

macrofauna de playas

Las playas son ambientes hostiles muy controlados físicamente, donde

las condiciones pueden variar considerablemente en periodos cortos de tiempo.

Por tanto, la fauna que habita los intermareales arenosos debe estar muy

adaptada a este ambiente tan dinámico. El aporte alimenticio en los

intermareales se puede definir como errático e impredecible y está fuertemente

unido al variado aporte externo proveniente de la columna de agua; ya sea en

forma de restos orgánicos particulados o de materia orgánica disuelta lista para

ser absorbida o filtrada. Los principales aportes alimenticios disponibles,

aunque limitados, para la macrofauna bentónica se presentan en la Tabla 1.2.

Los intermareales más protegidos y la llanura intermareales pueden alcanzar

valores de producción primaria medibles aunque no muy elevados (McLachlan

y Brown, 2006). Diferentes características morfológicas y adaptativas han

surgido para hacer frente a las condiciones dinámicas y variables de las playas.

Los grupos tróficos presentes en los intermareales incluye carnívoros,

carroñeros, filtradores/suspensívoros y depositívoros (estos últimos son más

importantes en playas protegidas). La mayor parte del alimento que se consume

en una playa es de origen exógeno a través del swash (Romer y McLachlan,

1986) o de las algas varadas (Dugan et al., 2003) haciendo que la depredación

directa entre las especies sea menos importante. La ausencia de macrófitas

asociadas al sedimento intermareal promueve la predominancia de organismos

filtradores y carroñeros entre la macrofauna de invertebrados residente en el

intermareal.

El número de especies carnívoras en las playas está bastante limitado y

una parte importante de este grupo se alimenta de la meiofauna (McLachlan,

1990). Los carroñeros, sin embargo son muy comunes en las playas y pueden

actuar como carnívoros en tiempos de escasez, ya que esta fuente de alimento

tiende a ocurrir de forma variable. Se encuentran desde la franja dunar hasta la


63

zona sublitoral. Estas especies son oportunistas y han adquirido varias

adaptaciones morfológicas y comportamentales para localizar y consumir

restos de forma eficiente. Otro tipo de hábito trófico muy abundante en las

playas es el de los organismos suspensívoros que filtran de forma general el

agua del swash o intersticial (McLachlan y Brown, 2006). En un ambiente tan

turbulento como una playa expuesta, la comida en suspensión está siempre

disponible aunque puede variar en cantidad y tipo. Los filtradores normalmente

dominan la comunidad del intermareal arenoso y consisten fundamentalmente

en moluscos bivalvos y algún crustáceo. En condiciones óptimas en playas

expuestas, por ejemplo en situación disipativa con gran cantidad de diatomeas

acumulándose en la zona de rompiente, los suspensívoros pueden mantener

grandes poblaciones y aportar gran biomasa al ecosistema.

En muchas situaciones, y sobre todo en playas reflectivas e

intermedias, los carroñeros/depredadores móviles dominan la macrofauna.

Donde la fauna es pobre, como en las playas de mucha pendiente y sedimento

grueso (Fig. 1.11.), la fauna del supralitoral tal como los talítridos anfípodos

son muy importantes como consecuencia de la ausencia de verdaderas formas

intermareales. Los depositívoros son más importantes en playas protegidas y en

la zona sublitoral. En estas zonas protegidas el sedimento es lo suficientemente

estable para permitir la construcción de galerías semipermanentes. Un análisis

amplio hecho por Riccardi y Bourget (1999) demuestra el aumento de

depositívoros con las condiciones protegidas, sedimento más fino y pendientes

más suaves con un consecuente aumento de los carnívoros.

La macrofauna que habita en las playas expuestas depende

exclusivamente de los aportes fitoplanctónicos exógenos y de algas macrófitas

de arribazón a causa de la escasez de producción primaria en ese hábitat (Inglis,

1989; McLachlan y Brown, 2006). La zona marina es la más importante fuente

de alimento, aportando partículas para los filtradores y restos orgánicos de

distintos orígenes (detritus de origen animal y plantas o algas) para los

carroñeros. Las características de las poblaciones que nos encontramos en un

intermareal están fuertemente relacionadas con la riqueza en el agua costera,

particularmente en términos del material particulado (ver Capítulos 4, 5 y 6).


64

La mayor presión depredadora también es de origen externo; aves y/o insectos

desde la zona terrestre y peces o grandes crustáceos desde el mar.

Otras estrategias de supervivencia son la movilidad, la migración, el

enterramiento y la orientación. La naturaleza extremadamente dinámica del

ambiente de playa en términos de disponibilidad y localización de alimento

reflejan las ventajas que supone la existencia de una fauna de gran movilidad,

sobre todo para optimizar el tiempo de alimentación y reproducción, así como

para poder escapar de un depredador. Normalmente las técnicas de escape se

centran sobre todo en la capacidad de enterramiento durante la bajamar, aunque

algunas formas son capaces de nadar o reptar (McLachlan y Brown, 2006). La

actividad locomotora y migratoria se originan de la combinación de los tres

factores ambientales principales: la inestabilidad del sustrato, la acción del

oleaje y la marea. Existe un número variable de mecanismos de enterramiento

en el caso de la macrofauna dependiendo del grupo que estemos tratando, ya

sea un organismo de cuerpo blando como un poliqueto o un molusco o un

organismo con un rígido exoesqueleto como los crustáceos. Estos mecanismos,

al igual que la reproducción no son el objetivo de estudio de esta tesis así que

no se procederá a una discusión sobre el tema.

1.1.3. Fuentes de alimento en las playas

1.1.3.1. Disponibilidad del alimento

Se ha demostrado que la disponibilidad de alimento es uno de los

principales factores que afectan a la estructura y metabolismo de la comunidad

bentónica marina (e.g. Pearson y Rosenberg, 1987; Graf, 1989; Dugan et al.,

2003) y que las diversidad de especies en los intermareales de fondos blandos

está fuertemente relacionada con dicha disponibilidad (Withlaton, 1981).

Además, la fuente de alimento puede ser uno de las explicaciones para la

distribución y asociación de las distintas poblaciones (Decho y Fleeger, 1988) y

para la distribución de la comunidad bentónica, su variabilidad temporal y el

metabolismo (Montagna, et al., 1983; Rudnick et al., 1985). La disponibilidad

del alimento está fuertemente relacionada con la composición de la materia


65

orgánica (Danovaro et al., 1993) por lo que determinar la composición de dicha

materia es crucial a la hora de valorar la calidad y cantidad de alimento en los

estudios de ecología bentónica (ver Capítulos 4 y 5).

La composición bioquímica de la materia orgánica no es más que el

resultado de un equilibrio dinámico entre los aportes exógenos, la producción

autóctona y el uso heterotrófico (Fabiano y Danovaro, 1994). La materia

orgánica en los sedimentos marinos está compuesta de una fracción lábil y otra

más refractaria (Fabiano y Danovaro, 1994). Los azúcares simples, ácidos

grasos y proteínas son rápidamente mineralizados y por tanto han sido usados

para valorar la porción lábil de la materia orgánica (Fichez, 1991; Danovaro et

al., 1993). Estos componentes más lábiles han sido usados tradicionalmente

para estimar el valor nutricional del sedimento (Buchanan y Longbottom,

1970). La composición bioquímica de la materia orgánica sedimentaria ha sido

ampliamente investigada en diversos ecosistemas marinos, como los fondos

marinos (Danovaro et al., 1993), sistemas semicerrados (Pusccedu et al., 1999),

fondos submareales (Fabiano et al., 1995), praderas de fanerógamas (Danovaro

et al., 1994) y sistemas estuáricos (Fabiano y Danovaro, 1994). Sin embargo, y

a pesar de la importancia de la composición bioquímica de la materia orgánica

sedimentaria (i.e. carbohidratos, lípidos y proteínas) hay muy poca información

sobre las concentraciones y variabilidad de estos compuestos en intermareales

arenosos (Incera et al., 2003a).

1.1.3.2. El papel de la composición bioquímica y de las condiciones

hidrodinámicas.

Se considera, de una forma general, que tanto los valores de la

abundancia como los de la biomasa de la macrofauna bentónica difieren

significativamente entre un intermareal expuesto y otro protegido. Así, los

intermareales más protegidas tienen una fauna muy abundante y diversa siendo

importantes como zona de cría de diversas especies de peces e invertebrados

(Adam 1990). Por el contrario, y como ya se explicó anteriormente, a medida

que aumenta el grado de exposición en un intermareal, la riqueza biológica

disminuye (Fig. 1.9.). Esto ha sido sugerido como una consecuencia de las


66

distintas características físicas e hidrodinámicas de estos dos ambientes tan

opuestos (McLaclhlan, 1983) e implica que el mayor estrés hidrodinámico de

las localidades expuestas es el factor limitante de la riqueza biológica

(McLachlan et al., 1996). Junto a la ya comentada “Hipótesis de Exclusión del

Swash”, surgen otras hipótesis que pueden explicar la relación entre la

macrofauna y las características de las playas sin ser necesariamente

excluyentes entre sí. La gran cantidad de materia orgánica en los intermareales

protegidos puede llegar a inducir una repuesta significativa en la macrofauna

bentónica que podría explicar, de forma parcial, la abundancia y diversidad

faunística de estos ambientes comparados con los intermareales expuestos

(Incera et al., 2003a, b).

La morfodinámica y el perfil de la playa condicionarán de alguna

manera la distribución y los patrones faunísticos de la misma; no sólo por la

actividad hidrodinámica, sino también por los distintos aportes nutritivos

presentes a lo largo del perfil del intermareal. Mientras que la parte inferior de

las playas más expuestas sufre una disminución de la riqueza específica, la

macrofauna encuentra un ambiente mucho más estable en la zona supralitoral

de las mismas (Defeo y Gómez, 2005). Esta zona alejada del swash está

habitada generalmente por insectos o crustáceos bien adaptados a la desecación

(McLachlan, 1990; Little, 2000) y considerados organismos dependientes de

aportes orgánicos alóctonos tan específicos como las algas de arribazón (ver

Capítulo 6) asociadas a distintos procesos oceanográficos (Colombini y

Chelazzi, 2003, Dugan et al., 2003). Las playas más protegidas tienen unas

condiciones ambientales más favorables y una mayor estabilidad sedimentaria

(ver Capítulos 4 y 5) lo cual favorece un rango mucho más amplio de

comportamientos y de adaptaciones morfológicas y tróficas.

Muchas playas expuestas de todas las latitudes reciben grandes

cantidades de algas provenientes del submareal e intermareales rocosos

próximos (Inglis, 1989; Rossi y Underwood, 2002; Dugan et al., 2003). La

importancia de estas acumulaciones, sobre todo en playas expuestas, ha sido

documentado en la literatura previamente (ver Colombini y Chelazzi, 2003).

Estos depósitos representan la fuente principal de alimentación para


67

organismos detritívoros como anfípodos talítridos, isópodos y coleópteros

(Colombini y Chelazzi, 2003; Dugan et al., 2003; Olabarria et al., 2007). Estas

acumulaciones de algas también actúan como refugio para la fauna del

supralitoral, principalmente artrópodos terrestres y semiterrestres, aportando

una oportunidad para estudiar este material tanto como una fuente de alimento

como de protección. (Inglis, 1989; Colombini y Chelazzi, 2003). El origen y la

composición bioquímica de la materia orgánica han sido propuestos como

factores claves, junto con el medio ambiente físico, para el control de la

comunidad bentónica de playas (Incera et al., 2003b).

1.1.4. Objetivos y líneas de investigación de la tesis.

Los intermareales son ecosistemas que están bajo una incesante presión

antropogénica debida fundamentalmente a la urbanización del litoral, con

aproximadamente un 50% de la población mundial viviendo junto a la costa

(GESAMP, 1990). A causa de la arrolladora tasa de desarrollo que se ha

producido en los últimos años en la línea costera y de la vulnerabilidad de este

frágil ecosistema, la demanda para una intervención sostenible en el litoral

centrada en su uso, control y preservación es acuciante. Además, el ecosistema

de playas es un punto de unión altamente productivo situado entre la tierra y el

mar en severo riesgo de una futura modificación dramática como consecuencia

del aumento del nivel del mar, en ciertas regiones, debido al calentamiento

global (Brown y McLachlan, 2002; Peterson y Bishop, 2005).

Al interés recreativo y lúdico típico de las zonas costeras hay que

añadir la relevante importancia industrial y pesquera del litoral en el norte de

España. La costa gallega es bien conocida como lugar de producción de

especies marinas de gran interés económico. La recolección manual de almejas

y berberechos del intermareal es una actividad muy común en esta área tan

productiva. Esta y otras actividades económicas tienen un efecto relevante en la

estructura y organización de las comunidades bentónicas de los intermareales.

Parte II. La ecología de las playas arenosas.

Al comienzo de este estudio, ningún trabajo cuantitativo sobre la

macrofauna de playas en España había sido publicado; además, se puede decir


68

que muy pocos estudios se habían llevado a cabo sobre la ecología de playas en

regiones de latitudes templadas, sobre todo en Europa. Por tanto, un estudio

inicial sobre la ecología de la macrofauna de intermareales de la costa norte de

la Península Ibérica es requisito esencial para iniciar este trabajo y en esta tarea

se ha centrado esta primera parte de la tesis.

El Capítulo 2 se centra en el efecto que tienen varios factores

ambientales sobre la macrofauna bentónica que reside en el tipo de playa

expuesta más característica del litoral a escala mundial. Se sometió a estudio el

efecto de diversas variables abióticas en un gradiente de diez playas

intermedias a lo largo de la costa norte de la Península Ibérica. Varias

características bióticas fueron utilizadas, destacando la riqueza de especies, la

abundancia y la biomasa de la macrofauna. Este estudio pionero de la ecología

de la macrofauna de playas del norte de España se completa con un análisis

más amplio y profundo sobre la estructura de la comunidad y la zonación

intermareal de la macroinfauna de la misma región. El Capítulo de 3 de esta

tesis es un complemento del capítulo anterior, centrado en la dinámica de las

comunidades macrofaunísticas de playas de tipo intermedio. Los resultados se

comparan con los distintos esquemas tradicionales de zonación que han sido

propuestos para la macroinfauna de playas y se sugiere una distribución

característica de la macrofauna basada en el peculiar perfil de las playas de esta

región. Distintos parámetros morfodinámicos y variables biológicas fueron

analizadas y discutidas. Los resultados de estos dos capítulos fueron publicados

en la revista Estuarine, Coastal and Shelf Science.

Parte III. La importancia del grado de exposición en la estructura de la

comunidad: condiciones hidrodinámicas y disponibilidad de alimento.

El capítulo 4 de esta sección ahonda en las características de la

estructura de la comunidad de macrofauna de las playas pero poniendo énfasis

en el efecto del gradiente de exposición al oleaje y en la disponibilidad de

alimento. Los efectos de los parámetros físicos y la disponibilidad de alimento

son analizados comparativamente entre playas protegidas y expuestas. Se

consideran ambos efectos como factores principales que pueden afectar a la

estructura y metabolismo de la comunidad bentónica marina. Además de


69

comprobar y reafirmar los patrones de zonación y cómo afecta la exposición a

la distribución faunística, se pone de relieve el paradigma del control físico en

las playas expuestas. También se analiza el posible patrón que regula

principalmente el aumento de los parámetros bióticos en los intermareales

protegidos, donde las interacciones biológicas se convierten en un factor

importante en la estructura macrofaunística. Los resultados y conclusiones

obtenidas en este capítulo han sido publicados en la revista Hydrobiologia.

Parte IV. El papel de la disponibilidad de alimento en las playas:

patrones espaciales y temporales.

Dada la importancia de los aportes alimenticios externos en la

estructura de la comunidad macrofaunística, en esta parte del estudio se

analizan dos tipos de playas definidos por su grado de exposición, protegida y

expuesta, y como afecta la disponibilidad del alimento en cada una de las dos

situaciones. En ambos casos, los aportes alimenticios son externos, pero

mientras que en el intermareal expuesto se estudia el aporte exógeno más

característico, las algas macrófitas de arribazón, en el intermareal protegido se

pone más énfasis en la composición bioquímica del sedimento y su influencia

en la estructura de la comunidad. En el capítulo 5 se realiza un estudio sobre la

variabilidad estacional y la distribución vertical de la materia orgánica

sedimentaria de una playa estuárica protegida y su relación con la macrofauna.

Este capítulo ha sido aceptado para su publicación en la revista científica

Estuaries and coasts.

En el capítulo 6 el estudio se centra en la influencia de los aportes de

macroalgas sobre las comunidades macrofaunísticas y en sus distintos tipos de

asociación. No sólo se presenta la abundancia de las especies colonizadoras,

sino también los procesos de sucesión (i.e. secuencia de colonización y

reemplazamiento de especies) y su variación en el tiempo. Un factor novedoso

de este estudio consiste en valorar el efecto de un alga invasiva sobre la

macrofauna de una playa como aporte exógeno y compararlo con el efecto de

un alga nativa. Este capítulo ha sido aceptado para su publicación en la revista

Journal of Experimental Marine Biology and Ecology.


70

Parte V. Discusión general.

En la discusión general del capítulo 7, todos los resultados de los

capítulos anteriores se han integrado y discutido. Algunos conceptos generales

sobre la ecología de las playas son confirmados mientras que otros se ponen en

cuestión y nuevas ideas y posibles nuevos objetivos de investigación se han

propuesto basados en los resultados y observaciones obtenidos.

PART II. THE ECOLOGY OF SANDY BEACHES

“And the more we learn of the nature of things, the more evident is it that what

we call rest is only unperceived activity; that seeming peace is silent but

strenuous battle. In every part, at every moment, the state of the cosmos is the

expression of a transitory adjustment of contending forces; a scene of strife, in

which all the combatants fall in turn. What is true of each part is true of the

whole.”

-Thomas Henry Huxley,

Evolution and Ethics

Content:

Rodil, I.F. and Lastra, M. 2004 Environmental factors affecting benthic

macrofauna along a gradient of intermediate sandy beaches in northern

Spain. Estuarine Coastal and Shelf Science 61: 37-44.

Rodil, I.F., Lastra, M. and Sánchez-Mata, A.G. 2006 Community

structure and intertidal zonation of the macroinfauna in intermediate

sandy beaches in temperate latitudes: North coast of Spain. Estuarine

Coastal and Shelf Science 67: 267-279.

Chapter 2. Environmental factors affecting benthic

macrofauna along a gradient of intermediate sandy

beaches in northern Spain

Rodil, I.F., and Lastra, M.

Published in Estuarine, Coastal and Shelf Science (2004). 61:37-44.

Chapter 2 Environmental factors

73

Abstract

Ten sandy beaches along the north coast of Spain were studied during

September 1999 to analyse the number of species, abundance and biomass of

macroinfauna along a gradient of intermediate beach types and exposure range.

Faunal samples were collected with metallic cylinders (25 cm diameter,15 cm

depth) at 10 equally spaced shore levels along six replicated transects separated

randomly and extending from above the drift line to the low tide swash zone.

Exposure rate, Dean’s parameter (Ω), beach state index (BSI) and relative tidal

range (RTR) were estimated at each beach. Length and width of the beach,

intertidal slope, sorting and median grain size and also swash amplitude and

wave characteristics were measured. Number of species was between 10 and

29. Macrofaunal abundances ranged between 4962 and 71228 ind. m-1 and

between 31 and 329 ind. m-2, while biomass (ash free dry weight) per square

meter of beach ranged between 0.027 and 0.278 g m-2 and between 3 and 61 g.

m -1. Results show some significant trends: number of species is the biotic

variable more affected by physic and morphodynamic factors, increasing

linearly with relative tidal range and decreasing with increasing average grain

size; the same trend was observed from exposed to very exposed beaches; the

biomass decreased exponentially with increasing average grain size. These

trends agree with previous studies in different coasts in the world where coarse

sands limit the benthic macrofauna. The morphodynamic parameters such as

Dean’s parameter and Beach State Index did not show a predictive value. The

results suggest that different characteristics of benthic macrofauna communities

in intermediate beaches can be affected in different ways by the physical

processes involved in beach morphodynamics.

Keywords: sandy beaches; benthic macrofauna; morphodynamic state;

exposure rate; swash; northern Spain.

2.2.1. Introduction

Beaches are present in all coasts, latitudes and climates worldwide,

having a wide spectrum of sizes, morphologies, exposure range and

oceanographic conditions, together with a high diversity in biotic


74

characteristics. The most dynamic of soft bottom habitats (McLachlan, et al.,

1996), exposed sandy beaches occur on the open coasts of tropical and

temperate regions (Davies, 1972). Exposed sandy beaches can be described in

terms of the interaction between wave exposure, tide ranges and sediment

characteristics, also called beach morphodynamics. This ecosystem harbours a

diverse and abundant macroinfauna, with Crustacea, Polychaeta and Bivalvia

being the most typical taxa (Brown and McLachlan, 1990). Since exposed

sandy beaches are mostly considered as physically controlled environments,

interactions between the main parameters have been frequently analysed.

Several studies on micro and mesotidal coasts have shown trends in intertidal

macroinfauna, with community structure related to beach morphodynamic and

wave environment (McLachlan et al., 1981; Defeo et al., 1992; McLachlan, et

al. 1993; McLachlan et al., 1996).

McLachlan et al. (1993) found that beach type, defined by the

dimensionless Dean’s parameter (Ω = Hb/ (Ws x T), where Hb is breaker

height in cm, Ws the sand fall velocity in cm.s-1 (Gibbs et al., 1971) and T the

wave period in seconds, is a good predictor of species richness, abundance and

biomass for microtidal beaches across different geographic regions, thus

classifying beach types into reflective, intermediate and dissipative. The scale

for the morphodynamic state would be as follow: Ω > 6 dissipative beach, Ω <

1 reflective beach and 1< Ω < 6 in the intermediate case. When tidal range

varies among different coastal areas, tidal effects must be taken into account

since elevated tidal energy (i.e. tidal range greater than 2-3 m) increases the

dissipative nature of beaches (Masselink and Short, 1993). To account for this,

McLachlan et al. (1993) created the beach state index (BSI = log [(Hb x M/Ws

x T x E) + 1]), where M is the maximum tide range and E is the theoretical

equilibrium tide for which the earth covered in water (E=0.8 m). Based upon a

comparative study of about 70 beaches, McLachlan et al., 1993; suggested the

following scale for BSI: <0.5 reflective beaches, 0.5-1 low to medium energy

intermediate beaches, 1.0.-1.5 high energy intermediate-dissipative beaches,

1.5-2.0 fully dissipative beaches, and > 2.0 ultradissipative macrotidal beaches.


75

Studies on beach fauna in relation to morphodynamic state indicate that

Dean’s and BSI are generally well correlated with community variables such as

number of species, abundance per linear meter and biomass (Jaramillo and

McLachlan, 1993; McLachlan et al. 1993; Hacking, 1998; McLachlan et al.

1998; Nell, pers. comm..). The biotic characteristics of exposed sandy beaches

have been related to many abiotic factors and physical variability has been

emphasised as the primary force controlling macroinfaunal communities

(McLachlan, 1983 a review). Beach morphology seems to have relevant

consequences on the intertidal macrofauna zonation, and McLachlan (1990)

and McLachlan et al. (1981) found significant correlations between

macroinfaunal community parameters and grain size, beach face slope and

beach type. Thus, species richness, as well as total abundance and biomass of

the macroinfauna tend to increase from narrow beaches having coarse sands

and steep slopes (i.e. reflective beaches, sensu Short and Wright, 1983), to

wider beaches having finer sands and flatter slopes (i.e. dissipative beaches,

sensu Short and Wright, 1983). Hence, macroinfaunal changes are related to

changes in physical characteristics occurring along a gradient of beach

morphodynamic types (Brazeiro 2001).

Following previous works, the aim of this study was to analyse the

macroinfauna community of exposed sandy beaches along the northern coast of

Spain. Variation in number of species, biomass and abundance of the intertidal

macrofauna was analysed along a coastal area where mostly intermediate sandy

beaches occur, with different morphologies and exposure conditions. The

significance of physical and morphodynamic parameters facing biotic factors

has been tested when only intermediate type of beach was present.

2.2.2. Material and methods

2.2.2.1. Study area

Ten sandy beaches on the northern coast of Spain, Oyambre, Liencres,

Langre, Berria, Laredo, Salvaje, Bakio, Laga, Zarautz and Hendaya (Fig.1),

were sampled during low spring tides of September 1999. Beaches were


76

located along circa 300 km of coast along the southern coast of the Bay of

Biscay, including the regions of Cantabria and Vasque Country. Tides in this

shore are semidiurnal and mesotidal, with maximum ranges close to 4 m.

Figure 1. Location of the ten sandy beaches studied at northern part of Spain.

2.2.2.2. Sampling design

Macrofauna sampling was carried out at six replicated transects

randomly-separated at the central area of each beach during low tide. At each

transect, 10 equally spaced shore levels extending from above the drift line

(level 10) to the low swash zone (level 1) were sampled. Previous studies of

macroinfauna in exposed beaches (Bally, 1983) showed that the highest

abundances are usually found in the first 15-20 cm depth, so, samples were

collected with metallic cylinders of 25 cm of diameter penetrating 15 cm depth

into the substrate. An area of 0.3 m2 was sampled at each level, the sediment

sieved through 1 mm mesh and the residue was preserved in 4% formalin. The

result was 3 m2 of total sampling surface in each beach; that means enough

surface in order to get a high percentage (90%) of the total number of species

and total abundance in temperate beaches, following Jaramillo et al., (1995).

FRANCEGULF OFBISCAY

Santander

Bilbao San Sebastián

Oya

mbre

Lie

ncre

s

Langre

Berr

iaLare

do

Hen

daya

Zara

utz

Laga

Bakio

43ºN

44ºN

4ºW 3ºW 2ºW

25 km


77

The individuals were later sorted from the sediments, identified and counted in

the laboratory.

Shell-free biomass was determined by drying at 100ºC for 24 hours

and 500ºC for 6 hours, obtaining ash free dry weigh values (A.F.W.D.).

Abundance and biomass values per running meter (i.e. estimates of total

macroinfauna in an intertidal across shore transect 1 m wide) were obtained by

linear interpolation between sampling levels, after obtaining mean values of

biomass and abundances per m2.

Three samples of sediment for grain size analyses were collected at

each level by inserting a 3 cm diameter metal corer to a depth of 15 cm. Grain

size of sand was analysed using a Coulter LS 200 laser diffraction particle size

analyser and the coarser fraction (> 2 mm) by dry sieving (Folk, 1980). Wave

height was estimated by measuring the height of breaking waves with

graduated poles against the horizon. Beach slope at each site was determined

by Emery’s profiling technique (Emery, 1961). From the average wave height

(Hb), wave period (T) and sand fall velocity of particles (values estimated

using the mean grain-size from the swash zone and conversion tables given by

Gibbs et al., 1971) dimensionless Dean’s parameter (Gourlay, pers.comm.;

Short and Wright, 1983) was calculated. The wave period was the time interval

between breakers and swash environment was estimated measuring maximum

swash amplitude, calculated as the distance between highest and lowest turning

point of the upswash and backswash respectively during five minutes period.

Beach State Index, from McLachlan et al. (1993), was also calculated in order

to analyse differences due to different tidal range in the ten studied beaches.

The 20-point rating system proposed by McLachlan (1980) was used to

estimate the wave exposure rate at each beach.

2.2.2.3. Statistical analysis

Regression analyses to test for relationships between biotic and abiotic

variables were carried out with SPSS program. The value of α (0.05) was

modified with the sequential Bonferroni correction when the same dependent


78

0

2

4

6

8

0

2

4

6

8

0 100 200 300

02468

m a

bo

ve lo

w t

ide level

02468

02468

02468

02468

02468

02468

0 100 200 300

02468

Oyambre Salvaje

Liencres

Langre Laga

Bakio

Berria

Laredo Hendaya

Zarautz

variable was analysed against various independent variables, according to

Holm (1979).

2.2.3. Results

2.2.3.1. Physical environment

The beach face morphology is shown in Fig. 2. The slopes varied

between 1/22 (Bakio) and 1/48 (Oyambre and Laredo). The physical

characteristics of substrate are shown in Table 1. Sands from these beaches

ranged from coarse (564 µm in Bakio) to medium sands (260 µm Berria) and

sediments were very poorly sorted, varying between 1.5 φ and 1.8 φ, indicating

a moderate grain selection in all the beaches sampled. Mean wave periods

during sampling dates varied from 12 s (Oyambre) to 17 s (Hendaya), with

wave heights from 0.31 m (Laredo) to 2.09 m (Zarautz). Maximum swash

amplitude ranged from 11 to 49 m (Table 1).

Figure 2. Beach face slopes at the ten sites sampled.


79

The values of dimensionless Dean’s parameter (table 1) tend to include

most of these beaches in the intermediate morphodynamic state, except the

beaches of Laredo and Hendaya which were close to a reflective state (sensu

Short and Wright, 1983). BSI values (Table 1) classified some of the beaches in

low to medium energy intermediate types (Langre, Laredo, Salvaje, Bakio,

Laga and Hendaya) and others in high energy intermediate/dissipative beaches

(Oyambre, Liencres, Berria and Zarautz). The 20-point rating system proposed

by McLachlan (1980) defined the beach of Hendaya as sheltered (maximum

score = 10), the beaches of Langre (15) and Laredo (12) as exposed, whereas

the rest of the beaches were defined as very exposed (> 15).

2.2.3.2. Composition and abundance of the macrofauna

Characteristics of the macrofauna community are shown in Table 2.

The number of species was highest at the beach of Laredo (29) and the lowest

at Salvaje and Bakio (10). Density values as high as 329 ind.m-2 were found at

Salvaje while 31 ind.m-2 were found at Liencres. Biomass values ranged

between 0.03 and 0.278 g.m-2. Abundances per running meter ranged between

4962 (Liencres) and 71228 ind.m-1 (Salvaje) and biomass per running meter

ranged between 3 (Bakio) and 61 g. m-1 (Laredo).


80

Ta

ble

1.

Ph

ysi

cal

char

acte

rist

ics

of

10

bea

ches

of

no

rther

n S

pai

n.

a Len

gth

of

bea

ch.

b W

idth

of

bea

ch

c Mea

n ±

SD

of

the

mea

sure

d v

alues

at e

ach s

am

ple

d t

ran

sect.

d M

ean ±

SD

of

the

mea

sure

d v

alues

duri

ng l

ow

tid

e (n

> 3

0)

e Sen

su M

cLac

hla

n’s

(1

98

0)

rati

ng s

yst

em (

i.e.

[w

ave

acti

on,

surf

zo

ne

wid

th,

% v

ery f

ine

sand

, m

edia

n p

arti

cle

dia

met

er a

nd

slo

pe,

dep

th o

f re

duce

d l

ayer

s, s

tab

le b

urr

ow

s.]

Ω:

D

ea

n’

s

pa

ra

me

te

r.

M.

G.

S.

M

ea

n

gr

ai

n

si

ze

.

Wave

s

Beach

L (

m)a

W (

m)b

Inte

rtid

al slo

pe

M.G

.S.

(µm

)cS

ort

ing

cP

eriod (

s)d

Hb (

m)

ΩR

TR

Sw

as

h

(m

)B

SI

Exp

osure

rating

e

Oya

mbre

1800

200

1/4

7.9

344±79

1.7

±0.1

12

1.2

51.9

23.1

625

1.0

216[3

,1,2

,6,3

,1]

Lie

ncre

s2800

180

1/3

4.3

527±41

1.6

±0.1

15

2.0

92.4

01.8

918

1.1

119[4

,1,2

,7,4

,1]

Lang

re800

194

1/4

4.6

400±57

1.6

±0.1

12

0.9

11.3

64.3

421

0.8

915[2

,0,2

,6,4

,1]

Berr

ia2000

260

1/5

5.9

260±21

1.6

±0.1

14

1.1

72.2

43.4

622

1.0

916[2

,1,2

,6,4

,1]

Lare

do

4250

243

1/4

8.2

270±17

1.7

±0.1

15.7

0.3

10.4

913.2

13

0.5

412[1

,1,2

,5,2

,1]

Salv

aje

752

200

1/3

2.

438±46

1.6

±0.0

14.5

2.8

01.1

81.4

139

0.8

317[4

,1,2

,7,3

,1]

Bakio

540

115

1/2

2.1

9564±40

1.5

±0.1

16.4

1.4

01.1

62.8

16

0.8

317[3

,1,2

,6,4

,1]

Lag

a574

178

1/4

2.4

1542±61

1.7

±0.1

12.1

0.8

31.0

94.8

16

0.8

16[2

,0,2

,7,4

,1]

Zara

utz

2500

180

1/3

8.2

457±28

1.6

±0.1

13.3

3.2

11.9

21.2

49

1.0

219[4

,1,2

,7,4

,1]

Hendaya

3000

145

1/4

7.4

315±39

1.8

±0.0

17

0.3

80.5

110.4

19

0.5

410[1

,0,1

,5,2

,1]


81

2.2.3.3. Relationships between macrofauna and environmental variables

The biplots of biotic variables (i.e. number of species, abundance and

biomass) versus abiotic factors (BSI, RTR, slope, average grain size and

exposure) are shown in fig. 3. No significant correlation at α = 0.05 was found

among macrofaunal characteristics with slope or BSI. Beach State Index has

been used as a modification of the Dean’s parameter to compare beaches from

different geographic areas with different tide ranges (McLachlan et al., 1993).

A very significant linear correlation between Dean morphodynamic parameter

and Beach State Index was obtained, since no different tidal range was found in

the studied beaches (BSI =0.43+0.3 Dean; r2 = 0.97, p <0.0001, powerα = 0.05

=1.0). Since Dean’s parameter should really only be used for microtidal

beaches and BSI combines this with a measure of tide range, we think BSI may

be more appropriate here. Consequently, Dean’s parameter has not been

included in the analysis.

Table 2. Characteristics of the macrofauna at the northern studied beaches. a Means of the values at each sampled transect.

The correlations between number of species and average grain size and

exposure rating were not significant when they were modified with the

sequential Bonferroni correction. Thus, the findings should be interpreted

cautiously. The number of species was linearly correlated with RTR (number

of species = 9.32 + 1.19 x RTR; r2 = 0.75, p<0.01, powerα = 0.05 = 0.94).

Macrofaunal number of species was also linearly correlated with average grain

size (number of species = 28.01 – 0.032 x grain size; r2 = 0.424, p<0.05,

Biomass

Beach Number of species Abundance (ind.m-1

) Density (ind.m-2

)a

(gm-1

) g(m-2

)

Oyambre 14 22954 106±37 23 0.121

Liencres 13 4962 31±17.2 25 0.128

Langre 16 11563 60±9.7 9 0.044

Berria 16 17110 70±55.5 49 0.199

Laredo 29 35245 143±13.2 61 0.278

Salvaje 10 71228 329±98.7 15 0.072

Bakio 10 9157 76±14.2 3 0.03

Laga 14 7549 45±9.6 5 0.027

Zarautz 11 28904 155±32.3 11 0.058

Hendaya 16 17902 105±25 26 0.178


82

powerα = 0.05 = 0.54) and with exposure rating (number of species =34.8 – 1.27 x

exposure rating; r2 = 0.426, p<0.05, powerα = 0.05 = 0.54). Biomass, either in m-2

or as m-1, was exponentially and linearly correlated with average grain size,

respectively (biomass [g.m-2] = 0.041 + 3.25 exp (-0.011 grain size); r2 = 0.77,

p<0.01, powerα = 0.05 = 0.95), (log biomass [g.m-1] = 78.5 – 0.13 x grain size; r2

= 0.64, p<0.01, powerα = 0.05 = 0.83).

RTR

2 4 6 8 10 12

r2 =0.75

M.G.S

300 400 500

r2 = 0.64

BSI

0,5 1,0 1,5 2,0

Nu

mb

er

of

sp

ec

ies

5

10

15

20

25

Exposure rate

10 12 14 16 18

De

ns

ity

(in

d.

m-2

)

100

200

300

Ab

un

da

nc

e

(in

d.

m-1

)

20000

40000

60000

Bio

ma

ss

(g.

m-2

)

0,05

0,10

0,15

0,20

0,25

Oyambre

Liencres

Langre

Berria

Laredo

Salvaje

Bakio

Laga

Zarautz

Hendaya

Slopes

0,01 0,02 0,03 0,04

r2 =0.77

r2 =0.42r2 =0.42

Lo

g b

iom

as

s

(g.

m-1

)

0,01

0,1

1

10

Beaches

Figure 3. Biplots of average values of biomass, abundance, density and number of

species vs. BSI (sensu Short and Wright, 1983), RTR, intertidal slope, median swash

grain size and exposure rating (sensu McLachlan, 1980a). Lines indicate significant

regressions at α= 0.05.


83

2.2.4. Discussion

Community analysis shows that macroinfauna values of density (31 to

329 ind.m-2) and biomass (0.03 to 0.27 g.m-2) of the 10 intermediate sandy

beaches in northern Spain were included within the range of density and

biomass values obtained in exposed sandy beaches worldwide (e.g. McLachlan

et al., 1981a; Defeo et al., 1992; Jaramillo et al., 1993; McLachlan et al., 1996,

Hacking, 1997). Results of number of species, ranging from 10 to 29, were

similar to values obtained in beaches from other temperate latitudes such as

Belgium (Degraer et al. 1999) and California (Dugan, et al. 2003), but differ

from results for beaches in Chile and Uruguay, where values obtained were

lower (Defeo et al., 1992; McLachlan et al. 1993; Jaramillo et al., 1993).

Moreover, a wider range of differences in species richness can be observed by

comparison with intermediate beaches from lower latitudes. Thus, the present

values are higher than those found in South African beaches (McLachlan et al.,

1981a), lower than values obtained in Oman (McLachlan et al., 1998) and

similar to species richness found in beaches sampled in Australia (McLachlan,

1996; Hacking, 1998). It is thought that this high variability comes from poorly

known factors such as biogeographic, latitudinal and oceanographic conditions

and particular local events, rather than just beach morphodynamic differences.

The general patterns found on sandy beach macroinfauna show a

negative correlation between species richness and exposure rating and grain

size (McLachlan and Jaramillo, 1995; McLachlan, 1996) as the present results

confirm. The greater the grain size and the higher the exposure rate, the higher

flushed and oxygenated interstitial spaces will be (McLachlan, 1989), resulting

in fewer macroinfauna by effects of waves and currents in exposed sandy

beaches. Conversely, reduction in beach exposure and average grain size can be

more favourable for macroinfauna (McLachlan and Jaramillo, 1995;

McLachlan et al., 1996).

The results plotted in Figure 3, show that number of species is the

biotic parameter most affected by the abiotic factors, increasing linearly with

RTR and diminishing from exposed to very exposed beaches and also


84

diminishing with increasing average grain size, although we have worked with

only a limitated range of particles, from 260 to 564µm. On the other hand,

biomass, either in g.m-2 or as log (g.m-1) decreases exponentially with

increasing average grain size. These trends agree with the predictions of

McLachlan et al., 1981b and Brown and McLachlan 1990, stating a negative

relationship between grain size and biomass. McLachlan et al. 1993 found all

these trends in beaches of United States, Australia and South Africa, and

Jaramillo, et al., 1993 found the same trends in beaches of Chile. Furthermore,

Hacking (1997) and Nell (pers. comm.) found the same trends in beaches of

Australia and South Africa respectively.

There are not enough differences in face slope, among the ten beaches

studied, to determine macrofauna trends since significant correlations have not

been found with any community variable. This low predictive value can be

partially related to the similarity of intermediate beach profiles in our ten

sampled beaches (Coefficient of Variation, C.V. = 31%) as compared with

variability of number of species (C.V. =35%), abundance m-2 (C.V. =73%),

abundance m-1 (C.V. =82%), biomass m-2 (C.V. =70%) and biomass m-1 (C.V.

=80%). This result differs from previous studies where steep slopes limit beach

macroinfauna (McLachlan et al., 1981a and McLachlan, 1990).

No significant trend was found between morphodynamic state of the

beaches (Dean’s parameter and BSI) and macrofauna. This has been shown

previously in present beaches for meiofauna (Rodriguez et al., 2003), and it is

opposite to the general patterns of sandy beach macroinfauna found in previous

studies (McLachlan, et al., 1981a; McLachlan, 1983 a review; Brown and

McLachlan, 1990; Jaramillo et al., 1993; McLachlan et al. 1993; McLachlan et

al., 1996; McLachlan et al. 1998 and Hacking, 1998). Since the parameters

(Dean and BSI), that include variables such as period and wave height did not

show significant correlations with our community characteristics, the

importance of these morphodynamic parameters seems to decrease. Dean’s

parameter values from Laredo and Hendaya show them as reflective beaches

instead of real intermediate-dissipative beaches, as it is stated by their beach

face slopes (1/48 and 1/47, respectively) and grain size (270±17 and 315±39


85

µm, respectively). The low values of Dean’s and BSI parameters are mostly

because of the low height break of the waves observed during the sampling

period. Moreover, the values obtained from wave height and period on these

beaches have a wide range of variation at different periods of time throughout

the year (Lastra, pers. com.). Therefore, it can be suggested that beach

morphodynamics described by Dean’s and BSI parameters have low capacity

in predicting community characteristics in the ten intermediate beaches studied

here. The validity of morphodynamic parameters have been generally

demonstrated when a full range of beach types are included in the analysis, i.e.

from reflective to dissipative (Jaramillo et al., 1993; McLachlan et al. 1993;

Jaramillo and McLachlan, 1993).

On the other hand, when only intermediate beaches are studied, the

different community characteristics seem to be affected by different abiotic

factors. The number of species is better explained by the exposure rating

(although this was not significant when we used Bonferroni´s correction) than

by variables such as Dean’s parameter or even beach slope, while biomass is

only affected by mean grain size. This confirms that a greater ensemble of

variables should be taken into account in the ecology of sandy beach

macroinfauna, as previously suggested by McLachlan et al., 1996 and Brazeiro

2001. Hence, this shows that communities of sandy beach invertebrates are

limited by more different ecological factors than a single key factor.

In the case of RTR (Fig.3.), there was a significant correlation with

number of species; so when the tide range becomes more significant than wave

energy, number of species increases. Further than this, Dean’s parameter is

smaller in those beaches (Laredo and Hendaya) where RTR reached high

values. Most of the studied beaches showed a broken profile roughly separated

by mean sea level into an upper steep beach, followed by a lower flat

downshore as previously found in beaches from Scotland (Eleftheriou and

Nicholson, 1975) and in the North West coast of Spain (de la Huz, pers.

comm.). The beaches studied have strongly interacting conditions of tide and

wave energy, resulting in broad flat beaches, tide-dominated on the lower

shores but tending towards swash control in the upper intertidal. When beaches


86

become increasingly tide dominated, they tend toward tidal flats and become

highly dissipative, where intertidal fauna is rich, while the high tidal zones are

reflective and poorer in fauna (Brown and McLachlan, 1990). No significant

correlation was found between swash amplitude and any of the biotic variables

in the 10 studied beaches.

In conclusion, the intertidal benthic macrofauna inhabiting intermediate

sandy beaches of northern Spain could not be fully related to beach

characteristics studied because of the limited range of beaches studied. There is

no unique key factor affecting benthic macrofauna, but several ecological

factors influence to the different community variables. More studies covering a

complete spectrum of beach types, environmental variables and exposure rates

are needed to check trends and general patterns in the intermediate type of

beaches, which is the dominant morphodynamic type along the northern coast

of Spain. We also need to check McLachlan & Turner’s (1993) predictions in

relation to morphodynamics where intermediate situations are likely to be the

optimum conditions for the development of an abundant interstitial fauna.

Acknowledgments

We thank K. Aerts for helping in laboratory works and C. de la Huz,

M. Incera, J. López, M. Pita and J.G. Rodríguez for field assistance. This

research was supported by The University of Vigo (64102C859) and the

Autonomous Government of Galicia (XUGA30105A98).

2.2.5. References

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in sandy beaches: what are the underlying factors?. Marine Ecology

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Brown, A. C., McLachlan, A. 1990 Ecology of sandy shores. Elsevier.

Amsterdam (328 pp.).

Davies, J. L. 1972 Geographic variation in coastal development. Longmans.

London (204 pp.)

Defeo, O., Jaramillo, E., Lyonnet, A. 1992 Community structure and intertidal

zonation of the macroinfauna on the Atlantic coast of Uruguay. Journal

of Coastal Research. 8, 830-839.


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Degraer, S., Mouton, I., De Neve, L., Vincx, M. 1999 Community structure and

intertidal zonation of the macrobenthos on a macrotidal, ultra-

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Dugan, J., Hubbard, D.M., McCrary, M.D., Pierson, M.O., 2003. The response

of macrofauna communities and shorebirds to macrophyte wrack

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Eleftheriou, A., Nicholson, M. D. 1975 The effects of exposure on beach fauna.

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Emery, K. O. 1961 A Simple Method of Measuring Beach Profiles. Limnology

and Oceanography. 6, 90-93.

Folk, R. L. 1980 Petrology of sedimentary rocks. Hemphill Publishing

Company. Austin, TX. (182 pp.).

Gibbs, R. J., Matthews, M. D., Link, D. A. 1971 The relationship between

sphere size and settling velocity. Journal of Sedimentary Petrology. 41,

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Hacking, N. 1998 Macrofaunal community structure of beaches in northern

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Holm, S. 1979 A simple sequentially rejective multiple test procedure Scandinavian Journal of Statistics. 6, 65-70.

Jaramillo, E., McLachlan, A. 1993 Community and population response of the

macroinfauna to physical factors over a range of exposed sandy

beaches in South-central Chile. Estuarine, Coastal and Shelf Science.

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Jaramillo, E. McLachlan, A., Coetzee, P. 1993 Intertidal zonation patterns of

macroinfauna over a range of exposed sandy beaches in south central

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Jaramillo, E., McLachlan, A., Dugan, J. 1995 Total simple area and estimates

of species richness in exposed sandy beaches. Marine Ecology


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Erasmus (Eds.), Sandy beaches as ecosystems (pp. 321-380). Junk. The

Hague.

McLachlan, A. 1989 Water filtration by dissipative beaches. Limnology and

Oceanography. 34, 774-780.

McLachlan, A. 1990 Dissipative beaches and macrofauna communities on

exposed intertidal sands. Journal of Coastal Research. 6, 57-71.

McLachlan, A. 1996.Physical factors in benthic ecology: effects of changing

sand particle size on beach fauna. Marine Ecology Progress Series.

131, 205-217.

McLachlan, A., Wooldridge, T.,Dye, A. H. 1981 The ecology of sandy beaches

in southern Africa. South African Journal of Zoology. 16, 219-231.

McLachlan, A., Erasmus, T., Dye, A. H., Wooldridge, T., van der Horst, G.,

Rossouw, G., Lasiak, T. A., McGwynne, L. 1981 Sand beach


88

energetics: an ecosystem approach towards a high energy interface,

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McLachlan, A., Turner, I. 1993 The interstitial environment of Sandy Beaches.

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McLachlan, A., Jaramillo, E., Donn, E., Wessels, F. 1993 Sandy Beach



Research. 15, 27-38.

McLachlan, A., Jaramillo, E. 1995 Zonation on sandy beaches. Oceanography

and Marine Biology: An annual review. 33, 305-333.

McLachlan, A., de Ruyck, A., Hacking, N. 1996 Community structure on


range and latitude. Revista Chilena de Historia Natural. 69, 451-467.

McLachlan, A., Fisher, M., Al-Habsi, H. N., Al-Shukairi, S. S., Al-Habsi, A.

M. 1998 Ecology of sandy beaches in Oman. Journal of Coastal

Conservation. 4, 1-10. Masselink, G., Short, A.D. 1993 The effect of tide range on beach

morphodynamics and morphology: a conceptual beach model. Journal

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Rodríguez, J. G., Lastra, M., López, J. 2003 Meiofauna distribution along a

gradient of sandy beaches in northern Spain. Estuarine Coastal and

Shelf Science. 56, 1-7.

Short, A. D., Wright, L. D. 1983 Physical variability of sandy beaches. A.

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144. Junk. The Hague.

Chapter 3. Community structure and intertidal zonation

of the macroinfauna in intermediate sandy beaches

in temperate latitudes: North coast of Spain.

Rodil, I.F., Lastra, M., and Sánchez-Mata, A.G.

Published in Estuarine, Coastal and Shelf Science (2006). 67: 267-279

Chapter 3 Community structure

90

Abstract

Nineteen intermediate exposed sandy beaches, located along the

northern coast of Spain, were sampled during the summer of 1999. Data from

ten of the beaches, located at the eastern part of this coast, was previously

reported to evaluate environmental factors affecting benthic macrofauna. Data

from nine of the beaches, located at the western part of this coast, was included

to compare community structure and intertidal zonation of the macroinfauna on

intermediate sandy beaches in temperate latitudes. Morphodynamic parameters

such as Dean’s parameter (Ω), Beach State Index (BSI) and relative tide range

(RTR) were estimated at each beach. Beach length, width, intertidal slope,

medium grain size, sorting, swash amplitude and wave characteristics were also

analysed. The highest macroinfaunal densities and biomass occurred at the mid

and lower shore levels of each beach. Crustaceans, mainly cirolanid isopods,

were the dominant group found on these beaches, whereas molluscs were the

least representative. In general, the relationship between community structure

and beach morphodynamics was similar to that found for the macroinfauna

worldwide; suggesting that macroinfauna in intermediate sandy beaches is

affected, in the same way, by the physical processes associated with different

beach types. Histograms and kite diagrams representing the intertidal

distribution of the macroinfauna and multivariate analysis were used to show

the zonation pattern on these exposed beaches. Intertidal slope values and

beach profile pattern was found similar in all the beaches sampled. We

hypothesized that this particular beach profile could influence the pattern of

macroinfauna zonation. All the nineteen beaches have two zones in common:

the supralittoral zone of air breathers present on all shores at and above the drift

line and the littoral zone extending from the drift line down the midshore to just

above the water table outcrop. Ordination analyses identified two possible

zones within the lower beach levels on seven of the beaches, but this can not be

clearly established. The Monte Carlo permutation test was used to select beach

slope, length and wave height as the best predictor variables of macroinfaunal


91

characteristics and it seems that the species most affected by the main variables

showed the clearest zonation on the beaches.

Keywords: intermediate sandy beaches; benthic macrofauna; intertidal

zonation; beach morphodynamics; swash climate; northern Spain.

2.3.1. Introduction

Sandy beaches are the most dynamic of soft bottom habitats

(McLachlan et al., 1996) and dominate the world’s temperate and tropical

shorelines (Davies, 1972). Despite their uniform appearance and comparative

poverty, intertidal zones of exposed beaches harbour a marine fauna of great

ecological diversity. Crustacea, Polychaeta and Bivalvia rank among the most

common macroinfaunal taxa (Brown and McLachlan, 1990), while Nematoda,

Harpacticoidea, Plathelmintha and Oligochaeta dominate meiofaunal groups on

sandy beaches (McLachlan, 1980).

Macrofaunal zonation on sandy beaches is a distinctive and well-

described phenomenon of intertidal zones (McLachlan and Jaramillo, 1995);

several attempts have been made to construct zonation schemes for sandy

beach macroinfauna. Two general zonation schemes have been commonly used

to determine distributions of organisms on sandy beaches: Dahl (1952) defined

three biological zones in terms of a typical crustacean fauna inhabiting each

zone, and Salvat (1964) defined four physical zones. These zones can be

recognised by the species found, and Dahl’s zonation pattern can easily been

superimposed on Salvat’s scheme. This scenario only represents the position

during low tide and, because of the highly mobile fauna, such zones would not

be expected to have sharp boundaries and, in fact, they often overlap

(McLachlan, 1983; Degraer et al., 1999).

It has been shown that beach type can be used as a reliable predictor of

species richness, abundance and biomass of the macroinfauna (e.g. McLachlan,

1990; McLachlan et al. 1993, Jaramillo and McLachlan, 1993). Swash

characteristics, which are distinctive for each type of beach (e.g. McArdle and

McLachlan, 1992), may also influence the community structure of the

macroinfauna (e.g. Jaramillo et al., 1993). Slope is closely related to swash


92

climate, which becomes less harsh as the beach face slope flattens (McArdle

and McLachlan, 1992). Environmental changes, associated with the

morphodynamic gradient, seem to have a relevant consequence on the intertidal

macroinfauna and on the zonation patterns. The relationship between species

richness and beach morphodynamics is supported by one common

generalization in sandy beach ecology: the macroinvertebrates decreasing along

a morphodynamic gradient from the dissipative to the reflective conditions

(sensu Short and Wright, 1983) (e.g. Defeo et al., 1992; Jaramillo and

McLachlan, 1993; McLachlan, et al., 1996; Brazeiro, 1999). Intermediate

beaches belong to the morphodynamic sandy beach type produced by moderate

to high waves, fine to medium sand, and long wave periods with intermediate

surf zones characterized by bars, troughs and rip currents (Wright and Short,

1983). The importance of understanding the ecology of intermediate sandy

beaches derives from the fact of there being the most common morphodynamic

beach type (Short, 1996; Alongi, 1998) and one of the most extended intertidal

systems worldwide.

The pioneering studies carried out on intermediate beaches in northern

Spain found no relationships between morphodynamic state and species

richness, biomass or abundance of macroinfauna (Rodil and Lastra, 2004) and

meiofauna (Rodríguez et al., 2003). In larger geographical studies, including

sandy beaches from areas with different oceanographic conditions and other

variables such as Chlorophyll-a concentration in the water column could be a

key factor explaining macrofaunal patterns. A key physical characteristic

typical of these beaches was a profile with a steep foreshore followed by a flat

lower shore, also found on Scottish beaches (Eleftheriou and Nicholson, 1975)

and on the North West coast of Spain (de la Huz, pers. comm.). This profile

creates a reflective character for the upper part of these beaches, while the

lowest part of the shores exhibits dissipative properties. We hypothesized that

this particular profile could give rise to a zonation other than that expected for

intermediate sandy beaches with a more regular or monotonic profile; at the

same time, the idea that such beaches may support more species due to the

variation in swash climate across the beach profile could be investigated. In


93

fact, this factor should be predicted to be more important for species that

interact directly with the swash than for those that inhabit the supralittoral dry

zones. Clear population responses to beach type have not been observed in

supralittoral macroinfauna (Contreras et al., 2003, Defeo and Martínez 2003),

which seems to be less influenced by the swash climate. To examine this

hypothesis, results were analysed from nineteen intermediate sandy beaches,

located in the northern coast of Spain, to evaluate the zonation of intertidal

macrofauna and compared with results from other intermediate beaches

worldwide. This paper provides a description of faunal zonation, composition

and density of the macroinfauna on intermediate morphodynamic beaches

along the northern shoreline of the Iberian Peninsula. Changes in community

structure along the beach profile and factors influencing these patterns are also

considered.

2.3.2. Material and methods.

2.3.2.1. Study area

Nine sandy beaches along the Northwest coast of Spain; Peñarronda,

Otur, San Pedro, Xagó, Xivares, La Espasa, Vega, Toranda and Andrín were

sampled in order to establish a reliable zonation scenario in intermediate sandy

beaches including the data previously obtained from ten eastern beaches on this

coast (Rodil and Lastra, 2004); Oyambre, Liencres, Langre, Berria, Laredo,

Salvaje, Bakio, Laga, Zarautz and Hendaya (Fig. 1). All beaches were located

from 43º 25’ N, 7º 00’ W to 43º 44’ N, 1º 50’ W and spanned a total of 800 Km

of coastline.

Sampling was carried out during spring low tides of September 1999 to

avoid variability linked to seasonal cycle (as community dynamics, species life

cycle, water temperature, storm events, accretion-erosion dynamics, etc) (Lima,

et al., 2000; Jaramillo et al., 2001; Brazeiro, 2001; Defeo and Rueda, 2002).

Tides on this coast are semidiurnal and mesotidal, with a medium tidal range of

three meters.


94

Figure 1. Location of the 19 intermediate sandy beaches studied on the northern coast

of Spain.

2.3.2.2 Sampling design

For all 19 beaches, macrofauna sampling was carried out at six

replicated transects haphazardly separated at the central area of each beach

during low tide. At each transect, 10 equally spaced shore levels extending

from above the drift line (level 10) to the low swash zone (level 1) were

sampled. Previous studies of macroinfauna on exposed beaches (Bally, 1983)

showed that the highest abundances are usually found in the first 15-20 cm

depth. Thus, samples were collected with 25 cm diameter metal cylinders

penetrating 15 cm deep into the substrate. An area of 0.3 m2 was sampled at

each level, the sediment was sieved through 1 mm mesh and the residue was

Zar autz

Lar edo

B err ia

Lan g re

Lien cre s

An dr in

Veg a

Xiv ares

Xag óPeñ arro nd a

San Ped ro

La E sp asa

Tor and a Oy amb re

Salv aje Lag a

B akio

Hen day a

Otu r


95

preserved in 4% formalin. The result was 3 m2 of total sampling surface on

each beach; this being sufficient surface to collect a high percentage (90%) of

the total number of species and abundance in temperate beaches (Jaramillo, et

al., 1995). The individuals were later sorted from the sediments, identified and

counted in the laboratory.

Shell-free biomass of all the species was determined by drying at

100ºC for 24 hours and then at 500ºC for 6 hours, obtaining ash free dry weight

values. Abundance and biomass per running meter (i.e. estimates of total values

in an intertidal across shore transect 1 m wide) were obtained by linear

interpolation between sampling levels, after obtaining mean values per m2.

Three samples of sediment for grain size analyses were collected at

each level by inserting a 3 cm diameter metal corer to a depth of 15 cm. Grain

size of sand was analysed using a Coulter LS 200 laser diffraction particle size

analyser, and the coarser fraction (> 2 mm) by dry sieving (Folk, 1980). Wave

height was estimated by measuring the height of breaking waves with

graduated poles against the horizon. Beach slope at each site was determined

by Emery’s profiling technique (Emery, 1961). From the average wave height

(Hb), wave period (T) and sand fall velocity of particles (values estimated

using the mean grain-size from the swash zone and conversion tables given by

Gibbs, et al., 1971) dimensionless Dean’s parameter (Ω) was calculated (Short

and Wright, 1983). The wave period was the time interval between breakers

and swash environment was estimated measuring maximum swash amplitude,

calculated as the distance between the highest and the lowest turning point of

the upswash and backswash respectively, within a five-minute period. Beach

State Index (BSI), from McLachlan et al. (1993), was also calculated in order

to analyse differences due to differing tide range on the nineteen beaches

studied. The rating system proposed by McLachlan (1980) was used to

categorize the beaches in relation to the wave exposure rate.


To aid interpretation of species zonation, density values (abundances

per square meter) were calculated and used to plot histograms ands kite


96

diagrams to describe distribution patterns across the beach face. Non-metric

multidimensional scaling ordinations (MDS), with the Bray-Curtis similarity

index, and Cluster analysis (Bray-Curtis index, group-average linkage) were

performed in order to elucidate faunistic belts on the beaches studied.

Measurement of goodness-of-fit of the MDS ordination was given by the stress

value (S); where low stress factor (S<0.2) corresponds to a good ordination

with no real prospect of a misleading interpretation (Clarke and Warwick,

1994). The presence of highly abundant species was standardized with a double

square root transformation. Pairwise analysis of similarities (ANOSIM, Clarke

1993) was carried out to test the null-hypothesis that there were no differences

(at α = 0.05) in the composition of the macroinfaunal assemblages at different

beaches. This was also applied for each beach location separately to assess the

significance of possible macroinfaunal zonation among levels. R is

approximately zero if the null hypothesis is true and close to one when the

lowest similarity appears to occur. MDS, Cluster analysis and ANOSIM were

performed using the PRIMER 5 software package (Clarke and Warmick 1994).

Also, in order to explore any potential relationship between measured

environmental parameters and densities of the macroinfaunal major species, the

technique of Canonical Correspondence Analysis (Hill’s scaling,

downweighting of rare major species) was performed. A previous Monte Carlo

permutation test was first performed to select the environmental variables,

which significantly explained the variability in the abundance of the

macroinfauna (α = 0.05 after 1999 permutations). Canonical correspondence

analysis (CCA) and the Monte Carlo permutation tests were carried out with

CANOCO 4.5 for Windows (ter Braak 1995). The variance explained by the

CCA model was calculated as the sum of eigenvalues axes (Borcard, et al.,

1992). Species with a higher than 20% presence of the overall macroinfauna

identified were selected from the beaches sampled to perform the CCA model.

Macroinfauna densities and environmental values were standardized prior to

analysis to reduce extreme values and to provide better canonical coefficient

comparisons (ter Braak, 1986 and Zar, 1996).


97

2.3.3. Results


Physical characteristics of all 19 beaches analysed are shown in Table

1. The characteristics of the nine western beaches are similar to those found for

the ten eastern beaches, which were analysed in Rodil and Lastra (2004), in

terms of sediment substrate (t17 = 1.86, p = 0.08), tide range (t17 = 1.8, p = 0.09)

and beach slope (t17 = 0.51, p = 0.62). Furthermore, all the nineteen

intermediate sandy beaches showed a general decrease in mean grain size at the

upper part of the shoreline (MGS [μm] = 403 - 6.5 x distance to shoreline [m];

R2 = 0.691, p < 0.001).

Eastern beaches were found longer than beaches at the western part of

the coastline (t17 = 2.77, p = 0.013). Six beaches from the western part

(Peñarronda, Otur, San Pedro, La Espasa, Vega and Andrín) share the same

peculiar broken profile as Oyambre, Liencres, Langre, Bakio, Laga, and

Zarautz in the eastern part (Rodil and Lastra, 2004): the upper levels, with a

steep foreshore, differing further from more dissipative levels on the lowest flat

part of the beach profile.

The values of dimensionless Dean’s parameter and BSI values (Table

1) generally categorized all of these beaches as intermediate in morphodynamic

state (sensu Short and Wright, 1983), following the comparative studies from

McLachlan et al. (1993). Dean (t17 = -2.19, p = 0.042) and BSI (t17 = -3.05, p <

0.01) values were significantly higher in beaches located at the western part of

the coastline. The rating system proposed by McLachlan (1980) classified all

the beaches from exposed (11 to 15) to very exposed (16 to 20). Beaches at the

eastern part of the coastline were found to be significantly more exposed (t17

=4.4, p < 0.01) than those located at the western part.


98

Wav

es

Bea

ch

L

(m)a

W

(m)b

Inte

rtid

al

slo

pe

Med

ian g

rain

size

(µ

m)c

So

rtin

gc

Per

iod (

s)d

Hb

(m

)

Dea

n´s

par

amet

er

RT

R

Sw

ash

amp

litu

de(

m)

BS

I

Exp

osu

re

rati

ng

e

Peñ

arro

nd

a 6

00

2

18

1/4

5

36

7±

78

2

.0±

0.2

1

1.5

0

.92

1

.1

4.5

2

5

0.9

1

1[2

,2,2

,4,0

,1]

Otu

r 6

00

2

00

1/3

2

35

5±

1

.0±

0.2

1

3

1.0

2

1.6

4

2

2

1

11

[2,2

,2,4

,0,1

]

San

Ped

ro

34

0

18

7

1

/35

2

66

±8

1

.0±

0.0

1

0.7

0

.86

2

4

.8

14

1

.1

12

[2,2

,2,5

,0,1

]

Xag

ó

83

0

22

6

1

/46

2

70

±6

0

1.0

±0.2

8

.2

1.1

5

2.8

0

.5

24

1

.2

11

[3,1

,2,4

,0,1

]

Xiv

ares

8

00

2

36

1/5

2

27

2±

34

1

.3±

0.0

1

2.6

0

.96

1

.5

4.3

1

9

1

12

[2,2

,2,5

,0,1

]

La

Esp

asa

11

50

18

2

1

/34

4

27

±8

6

1.5

±0.3

1

5.3

2

.07

2

.7

0.3

3

3

1.2

1

2[4

,1,2

,4,0

,1]

Veg

a

14

40

23

0

1

/45

3

09

±2

0

1.3

±0.0

1

3.1

1

.71

2

.6

2.4

2

5

1.1

1

1[4

,1,2

,3,0

,1]

Tora

nd

a 3

00

1

35

1/2

8

24

3±

13

1

.3±

0.0

1

2.6

1

.49

3

2

.7

29

1

.2

11

[3,1

,2,4

,0,1

]

And

rín

24

0

15

6

1

/37

3

18

±2

9

1.3

±0.0

1

1.8

1

,9

3.2

2

.2

11

1

.3

12

[4,1

,2,4

,0,1

]

Oyam

bre

1

80

0

20

0

1

/48

3

44

±7

9

1.7

±0.1

1

2

1.2

5

1.9

2

3.2

2

5

1.0

2

16

[3,1

,2,6

,3,1

]

Lie

ncr

es

28

00

18

0

1

/34

5

27

±4

1

1.6

±0.1

1

5

2.0

9

2.4

1

.9

18

1

.11

1

9[4

,1,2

,7,4

,1]

Lan

gre

8

00

1

94

1/4

5

40

0±

57

1

.6±

0.1

1

2

0.9

1

1.3

6

4.3

2

1

0.8

9

15

[2,0

,2,6

,4,,1

]

Ber

ria

20

00

26

0

1

/56

2

60

±2

1

1.6

±0.1

1

4

1.1

7

2.2

4

3.5

2

2

1.0

9

16

[2,1

,2,6

,4,,1

]

Lar

edo

4

25

0

24

3

1

/48

2

70

±1

7

1.7

±0.1

1

6

0.3

1

0.4

9

13

.2

13

0

.54

1

2[1

,1,2

,5,2

,1]

Sal

vaj

e 7

52

2

00

1/3

2

43

8±

46

1

.6±

0.0

1

4.5

2

.8

1.1

8

3.8

3

9

0.8

3

17

[4,1

,2,7

,3,1

]

Bak

io

54

0

11

5

1

/22

5

64

±4

0

1.5

±0.1

1

6

1.4

1

.16

2

.8

16

0

.83

1

7[3

,1,2

,6,4

,1]

Lag

a 5

74

1

78

1/4

2

54

2±

61

1

.7±

0.1

1

2

0.8

3

1.0

9

4.8

1

6

0.8

3

16

[2,0

,2,7

,4,1

]

Zar

autz

2

50

0

18

0

1

/38

4

57

±2

8

1.6

±0.1

1

3.3

3

.21

1

.92

2

.64

4

9

1.0

2

19

[4,1

,2,7

,4,1

]

Hen

day

a 3

00

0

14

5

1

/47

3

15

±3

9

1.8

±0.0

17

0

.38

0

.51

1

0.4

1

9

0.5

4

10

[1,0

,1,5

,2,1

]

Ta

ble

1.

Ph

ysic

al

chara

cte

risti

cs o

f 1

9 n

ort

hern

beaches o

f S

pain

. a L

en

gth

of

beach.

b W

idth

of

beach

c M

ean ±

SD

of

the m

easure

d v

alu

es a

t each s

am

ple

d t

ran

sect.

d M

ean ±

SD

of

the m

easure

d v

alu

es d

uri

ng l

ow

tid

e (

n>

30

)

e s

ensu M

cL

achla

n´s

(1

98

0)

rati

ng s

yste

m (

i.e.

[w

ave a

cti

on,

surf

zo

ne w

idth

, %

very

fine s

and

, m

ed

ian p

art

icle

dia

mete

r a

nd

slo

pe,

dep

th o

f

red

uced

layers,

sta

ble

burr

ow

s .

]


99

2.3.3.2. Composition and abundance of the Macrofauna

Macroinfauna was dominated by crustacean species (84%), Isopoda

(62.6%) and Amphipoda (17.7%) being the main components of this group.

Polychaetes (11.2%) and molluscs (2.6%) were also present but in lower

abundances. In the supralittoral zone, a mixture of terrestrial and marine

adapted animals was present. Hence, a variety of coleopterans, dipterans and

pupae of uncertain origin, found above the drift line, were excluded from the

final analysis due to low occurrence in all the nineteen beaches sampled.

Oniscoidean isopods and talitrid amphipods were included instead, due to the

high abundances found in the supralittoral part of the beaches. Number of

species, abundance and biomass of macroinfauna of the nineteen beaches are

shown in Table 2. Macroinfauna biomass (from 0.056 to 0.452 g.m-2) and

number of species (from 9 to 15) found in the nine western beaches were

similar to the values from the ten eastern beaches reported in Rodil and Lastra,

2004.

Beach

Number of

species Abundance Biomass

(ind.m-1) (ind.m-2)a (gm-1) (gm-2)

Peñarronda 13 29990 125±71 25 0,106

Otur 11 17172 71±33 52 0,214

San Pedro 10 81829 338±148 54 0,222

Xagó 13 99484 409±387 46 0,452

Xivares 14 95695 395±369 42 0,172

La Espasa 14 43212 180±132 13 0,056

Vega 15 44260 182±121 40 0,162

Toranda 12 38778 160±71 68 0,125

Andrín 9 87714 363±164 27 0,112

Oyambre 14 22954 106±37 23 0.121

Liencres 13 4962 31±17.2 25 0.128

Langre 16 11563 60±9.7 9 0.044

Berria 16 17110 70±55.5 49 0.199

Laredo 29 35245 143±13.2 61 0.278

Salvaje 10 71228 329±98.7 15 0.072

Bakio 10 9157 76±14.2 3 0.03

Laga 14 7549 45±9.6 5 0.027

Zarautz 11 28904 155±32.3 11 0.058

Hendaya 16 17902 105±25 26 0.178

Table 2. Characteristics of the macrofauna at the northern beaches studied. a Mean’s ± SD of the values at each sampled transect.


100

Macroinfauna abundance from the western beaches (from 71 to 409 ind.m-2)

was found significantly higher (t17 = -2.88, p = 0.01) than the abundance found

in the eastern part of the coastline (from 31 to 329 ind.m-2).

MDS analysis (S < 0.2), performed by pooling the sampling levels on

each beach, suggested that the macrofauna communities from the beaches

sampled could be grouped into two broad categories: beaches from the western

part (except Otur; O) and eastern beaches (Fig. 2). The low stress value (S =

0.15) found in the MDS analysis (Fig. 2a) gives a potentially useful two-

dimensional picture, although additional information about the overall structure

would be desirable. The combination of clustering and ordination analyses can

be an effective way of checking the representations (Clarke and Warwick,

1994). Thus, in Figure 2b, the two geographical groups of beaches detected by

the cluster analysis were found to be superimposed on the MDS ordination,

with a Bray Curtis Similarity higher than 40%, which ensures that both plots

(Fig. 2a and b) are an accurate representation of the relationship among the

beaches. ANOSIM results also established a difference (as noted in the MDS

from Fig. 2) between western and eastern beaches, (R = 0.585; p<0.01). This

result must be interpreted with caution since the low R value does not mean

really low similarity between beaches. Laredo showed lower similarity

compared with eastern beaches (R = 0.754; p<0.05) and the lowest with

western beaches (R = 0.948; p<0.05).

2.3.3.3. Intertidal zonation of the macroinfauna

The distribution of the macroinfauna in the lower part of the beaches

was more variable along the East to West gradient than the community

patterns above. Intertidal variability as total abundance (density values

per m2) of the macroinfauna (averaged for all the19 beaches) and the

across-shore distribution of the major species was calculated to plot

histograms (with error bars) and kite diagrams to describe zonation

patterns (Figs. 3 and 4). Total abundance and biomass showed no high


101

across-shore variability even though a peak of abundance was noted at

the upper part of the saturation zone and at the retention zone.

Figure 2. a) Biplot resulting from the multidimensional beach analyses of the

macroinfauna total abundance (density values per square metre).b) Dendogram

resulting from hierarchical cluster analyses of the macroinfauna density values.

(Pe:Peñarronda,O:Otur,SP:SanPedro,Xg:Xagó,Xi:Xivares,Es:Espasa,V:Vega,To:Toran

da,A:Andrín,Oy:Oyambre,Li:Liencres,Lgr:Langre,Be:Berria,Lar:Laredo,Sv:Salvaje,Bk

:Bakio,Lg:Laga,,Z:Zarautz, H:Hendaya).

The upper zone of the beaches was characterised by talitrid amphipods

such as Talitrus saltator (33±16 ind.m-2), Talorchestia brito (2±1ind.m-2) and

Talorchestia deshayesii (1±0 ind.m-2). Air-breathing isopod Tylos europaeus

(2±1 ind.m-2) was also found at the drying beach level (D). Retention zone (Rt)

was mainly characterised by the cirolanid isopods Eurydice pulchra (91±9

ind.m-2) and E. affinis (26±7 ind.m-2), which were also found at the drying zone

in high abundances (65±60 ind.m-2 and 47±40 ind.m-2 respectively), and by the

amphipod Haustorius arenarius (26±7 ind.m-2). Bathyporeia pelagica was also

found at this part of the intertidal zone (2±1ind.m-2). Ophelia bicornis was the

most common member of the polychaeta group at the Rt (19±6 ind.m-2) and D

zones (18±9 ind.m-2).

O y

L i

L g r

B e

L a r

S vB k

L gZ

H

P

O

S P

X g

X v

E sV

T

A

S tre s s : 0 ,1 5

L a rH

L g r

L g

L iO y

B eOZ

S v

B kTP

S PX v

X gA

E sV

2 0 4 0 6 0 8 0 1 0 0

B r a y C u r t i s S i m i l a r i t y

w e s t e r n

b e a c h e s

e a s t e r n

b e a c h e s

a) b)

western beaches

eastern beaches


102

Figure 3. Histograms showing intertidal variability as total abundance (density values

per m2) of the macroinfauna (averaged from all the nineteen beaches).a) Macroinfauna

species found in the saturation zone of the beaches b) Macroinfauna species from the

resurgence and retention part of the beaches (Donax trunculus was found in both

levels). c) Macroinfauna species from the dry upper zones of the beaches. d) Cirolanid

isopods of the genus Eurydice (mean abundances) were found to span throughout the

intertidal. Values of total averaged density and number of species found in all the

nineteen beaches were also plotted.

Cum

opsis

fagei

Dis

pio

sp

Drilo

nere

is f

ilum

Eocum

a d

ollfu

si

Gastr

osaccus s

pin

ifer

Gastr

osaccus s

anctu

s

Hid

robia

ulv

ae

Nephty

s c

irro

sa

Spio

phanes b

om

byx

Scole

lepis

squam

ata

Ponto

cra

tes a

renarius

Avera

ged d

ensity (

ind.m

-2)

0

25

50

75

100

125

150

175

200

Port

um

nus la

tip

es

Sphaero

ma r

ugic

auda

Angulu

s t

enuis

Donax t

runculu

s

Bath

ypore

ia p

ela

gic

a

Hausto

rius a

renarius

Ophelia

bic

orn

is

Avera

ged d

ensity (

ind.m

-2)

0

20

40

60

80

100

120

140

a) b)

c) d)

Eury

dic

e p

ulc

hra

Eury

dic

e a

ffin

is

Tota

l density

n s

pecie

s

Avera

ged d

ensity (

ind.m

-2)

0

250

500

750

1000

1250

1500

1750

2000

2250

2500

Tylo

s e

uro

paeus

Talo

rchestia

deshayesii

Talo

rchestia

brito

Talitr

us s

altato

r

Avera

ged d

ensity (

ind.m

-2)

0

10

20

30

40

50

60


103

Figure 4. Distribution of the macroinfaunal densities and biomass of the main species

in morphodynamic type intermediate beaches on the north coast of Spain. Density

values are expressed in ind.m-2 and biomass values in g.m-2 (averaged from all the

nineteen beaches). Lines separate the physical zones of the intertidal (sensu Salvat

1964); D = dry zone; Rt= retention zone; Rs = resurgence zone; S = swash zone).

The Resurgence (Rs) and saturation (S) zones were also completely

dominated by crustaceans. Cirolanid isopods of the genus Eurydice were once

again the dominant organisms (E. pulchra: 75±33 at Rs and 88±21 ind.m-2 at

S). The amphipod Pontocrates arenarius (17±4 at Rs and 29±8 ind.m-2 at S

zone) and the isopod, Sphaeroma rugicauda (9±2 at Rs and 12±5 ind.m-2 at S)

Sphaeroma rugicauda

Scolelepis squamata

Donax trunculus

Gastrosaccus sanctusOphelia bicornis

Pontocrates arenarius

Haustorius arenarius

Talitrus saltator

Eurydyce pulchra

130

130

35

35

35

35

35

35

35

300Total indiv.

Drilonereis filum

Talorchestia deshayesii

Tylos europaeus

5

5

5

Bathyporeia pelagica

Nepthys cirrosa 5

5

Spiophanes bombyx5

35

S Rs Rt D

Talorchestia brito

Eurydyce affinis

DRtRsS

m above low tide m above low tide

0.25 Total biomass

5

35Number of species

1 42 3 1 42 3


104

were found at this part of the beach. The polychaetes Drilonereis filum (2±0 at

Rs and 1±0 ind.m-2 at S) and carnivorous Nepthys cirrosa (2±1 at Rs and 4±0

ind.m-2 S) were also found at these levels; meanwhile, the spionids Scolelepis

squamata (27±1 ind.m-2) and Spiohpanes bombyx (4±2 ind.m-2) were mostly

abundant toward the swash zone of the beach. Benthoplanktonic mysids of the

genus Gastrosaccus are good indicators of the lower shore, corresponding to

the saturated lower and subtidal parts of the beach. Gastrosaccus sanctus was

restricted to the lowest tidal level (14±1 ind.m-2). Donax trunculus was the

main species representing the Mollusc group from the retention to saturation

levels; the highest abundance was found at the retention zone (11±1 ind.m-2)

and decreasing downshore (5±2 ind.m-2 at Rs).

Biplots resulting from the MDS analysis for total macroinfauna

abundances (Fig. 5) show that macroinfauna assemblages were quite similar in

all the sampled beaches. A measure of goodness-of-fit of the MDS ordination

was given by the low stress value (S < 0.1). All of the beaches appeared to split

into two distinct zones; at least the upper part of the beach (levels 9 and 10,

sometimes with level 8) seems to differ from the lower shoreline levels.

Statistical values of R in ANOSIM analysis indicate the degree of

discrimination between the levels. The R statistic itself is a useful comparative

measure of the degree of separation of sites (Clarke and Warwick, 1994;

Legendre and Legendre, 1998). ANOSIM results, for differences among levels

at each sampled beaches, revealed a significant difference in community

composition between the upper (a) and the lower part (b) of the shoreline

(Table 3). All the beaches sampled showed this simple and clear separation,

and only some of them (San Pedro, Xivares, Vega, Toranda, Oyambre,

Liencres and Laredo) showed a possible third division (b1 for the levels closer

to the dry zone and b2 for the lowest levels downshore) separating the lower

part of the shoreline where Rt, Rs and S levels occur, but without any clear

zonation pattern.


105


variables.

An ordination biplot for the major species of macroinfauna (Fig. 6) was

obtained using Canonic Correspondence Analysis (CCA) to evaluate the

relationship between environmental variables and macroinfauna densities. The

Monte Carlo permutation test showed that the macroinfauna community

changed significantly with beach length (p < 0.001), slope (p < 0.05) and wave

height (p < 0.05) after 1999 permutations. Arrows represent environmental

variables and the length of them shows the importance of each variable (ter

Braak, 1986). The direction of arrowheads represents increasing values for

environmental variables, and the projection of the species onto the arrows

shows the environmental preference of the biota (ter Braak, 1986). This gives

an approximation of the weighted averages of the species with respect to

environmental variables (ter Braak, 1995; Legendre and Legendre, 1998).

These environmental variables explained about 45.8% of the macroinfauna

density variation. The first and second axis, explained by the environmental

variables, accounted for 57% of the species-environment correlations. The sum

of all canonical eigenvalues was 80% (F = 3.076, p< 0.001). The position of the

macroinfauna groups in the biplots reflects the contribution of each group to

the variance explained by the first two axes (ter Braak, 1986). Thus, the

numbers of Scolelepis squamata, Pontocrates arenarius, Gastrosaccus sanctus,

Eurydice pulchra, E. affinis, Sphaeroma rugicauda, Nephtys cirrosa,

Haustorius arenarius, Portumnus latipes and Talitrus saltator were the least

explained by the environmental variables since their positions in the CCA

model were close to the origin (plotted with triangles in Figure 6).

Thus, Donax trunculus reaches the highest densities at beaches with

longer shoreline and with medium-high wave height (Hb) values. Cumopsis

fagei and Bathyporeia pelagica show the highest density values at beaches with

medium-high values of either Hb or beach length. High density values of

Nepthys cirrosa and Portumnus latipes were noted with medium-high Hb

values. Talorchestia brito and Ophelia bicornis show the highest density values

on beaches with low slope values.


106

2.3.4. Discussion

2.3.4.1. Macrofaunal characteristics

The macroinfauna values recorded in the nine eastern beaches (Table

2) seem to be in accordance with the range of values obtained in the ten

western beaches (Rodil and Lastra, 2004) and with those values obtained in

morphodynamic intermediate beaches worldwide (e.g. Defeo et al., 1992;

Jaramillo et al., 1993; McLachlan, et al., 1996, Hacking, 1998). We have found

that macroinfauna abundances (ind.m-2) are significantly higher in the western

than in the eastern beaches, but no difference in biomass or number of species

was found within this geographical gradient.

Molluscs, crustaceans and polychaetes have been reported to be the

three most abundant macrofaunal taxa on sandy beaches worldwide (Pichon,

1967; McLachlan, 1983). Crustaceans (amphipods and isopods) were the most

diverse and abundant group, in abundance and species number, on the beaches

studied here, while molluscs were the least abundant group. The cirolanid

isopod Eurydice pulchra was the most common species occurring on every

beach, spanning the entire intertidal zone. The intertidal distribution of the

majority of macroinfauna species was more restricted than that of Eurydice

pulchra. Most species encountered were concentrated in the lower and middle

levels of the beaches, corresponding to the Saturation and Resurgence beach

zones, with some intrusions into the Retention zone (sensu Salvat 1964).

2.3.4.2. Zonation patterns of the macroinfauna

Several zonation schemes have been proposed for macroinfauna of

sandy beaches (e.g. Dahl, 1952; Salvat, 1964; Pichon, 1967; Trevallion et al.,

1970); but classification and ordination techniques have been recently used to

examine intertidal distributions in many areas of the world (e.g. Donn and

Crockcroft, 1989; McLachlan, 1990; Raffaeli, et al., 1991; Defeo, et al., 1992;

McLachlan, et al., 1996; McLachlan et al., 1998).


107

A1A

2

A3

A4A

5

A6

A7

A8

A9

A10

2D

Str

ess: 0.0

5

BK

1

BK

2B

K3

BK

4

BK

5

BK

6

BK

7B

K8

BK

9B

K10

2D

Str

ess: 0.0

9

BE

1BE

2

BE

3

BE

4B

E5

BE

6

BE

7 BE

8B

E9

BE

10

2D

S

tress: 0.03

H1H

2

H3

H4

H5

H6H7

H8

H9

H10

2D

Str

ess: 0.0

4

LG

1LG

2LG

3

LG

4LG

5LG

6

LG

7

LG

8

LG

9

LG

10

2D

Str

ess: 0.0

3

ES

1E

S2

ES

3E

S4

ES

5E

S6

ES

7E

S8

ES

9E

S10

2D

Str

ess: 0.0

1

LG

R1

LG

R2

LG

R3

LG

R4

LG

R5

LG

R6

LG

R7

LG

R8

LG

R9

LG

R10

2D

S

tress: 0.01

LR

1

LR

2

LR

3

LR

4

LR

5 LR

6LR

7LR

8

LR

9LR

10

2D

S

tress: 0.06

LI1

LI2

LI3

LI4LI5

LI6

LI7

LI8

LI9

LI1

0

2D

S

tress: 0.04

O1

O2

O3

O4

O5

O6

O7

O8

O9

O10

2D

S

tress: 0.06

OY

1

OY

2O

Y3

OY

4O

Y5

OY

6O

Y7

OY

8

OY

9O

Y10

2D

S

tress: 0.01

P1

P2

P3

P4P5

P6

P7

P8

P9

P10

2D

S

tress: 0.04

SV

1S

V2

SV

3S

V4

SV

5

SV

6S

V7

SV

8

SV

9S

V10

2D

S

tress: 0.03

SP

1S

P2

SP

3S

P4

SP

5S

P6

SP

7S

P8S

P9

SP

10

2D

S

tress: 0.01

TO

1

TO

2T

O3

TO

4T

O5

TO

6

TO

7T

O8

TO

9

TO

10

2D

S

tress: 0.08

VG

1V

G2

VG

3V

G4

VG

5

VG

6

VG

7

VG

8V

G9

VG

10

2D

S

tress: 0.05

XV

1

XV

2X

V3

XV

4X

V5

XV

6XV

7

XV

8

XV

9

XV

10

2D

Str

ess: 0.0

5

Z1

Z2

Z3

Z4

Z5

Z6

Z7

Z8

Z9

Z1

0

2D

Str

ess: 0

XG

1

XG

2 XG

3X

G4

XG

5

XG

6

XG

7

XG

8

XG

9

XG

10

2D

S

tress: 0.08

ba a

b

a

b

b

a

ab

a

b2

b1

a

b

b

a

a

b2

b1

a

b

bb

2

b1

a

b

a

b2

b1

b

b

a

a

b

b

b2

b1

b

a

a

b

a

b

bab

a

Fig

ure

5.

Bip

lots

result

ing

fr

om

th

e

mu

ltid

imen

sio

nal

scali

ng

analy

sis

o

f th

e

macro

infa

una (d

ensit

y valu

es exp

ressed

as in

d.m

-2) b

each

zo

nati

on o

n each b

each.

Lett

ers i

nd

icate

beach

nam

es (

as i

n F

igure 2

) w

hil

e n

um

bers r

ep

resent

sam

pli

ng l

evels

(1

-10

).L

ett

er “a” gro

up

up

per b

each le

vels

and

“b

” th

e rest

of

the d

ow

nsho

re le

vels

.

Furth

er d

ivis

ion (b

1 and

b

2) rep

resents

p

ro

bab

le zo

nati

on d

ow

nsho

re (see T

ab

le 3

fo

r

sig

nif

icant

co

rrela

tio

ns).


108

The beaches that we studied along the northern coast of Spain (Rodil

and Lastra, 2004) showed a broken profile roughly separated by mean sea level

into an upper steep beach, followed by a lower flat downshore, as was

previously found in Scottish beaches (Eleftheriou and Nicholson, 1975) and on

the North West coast of Spain (de la Huz, pers. comm.). The main consequence

of this profile is that the Rs level covers a broad zone of the beaches, which is

characterised by high macroinfauna abundance. Moreover, this situation does

not help to make a clear separation between Rs and Rt zones on some of the

sampled beaches, and these levels seem to be the same on some beaches, such

as Zarautz, Langre and Espasa.

Sharp boundaries in macroinfauna zonation were not found in these

beaches; zonation on sandy beaches has been considered as an artificial

division of a continuum, with overlap between adjoining zones (Degraer et al.,

1999). The intertidal distribution of the macroinfauna on the sandy beaches

studied here showed a great complexity since most common species are able to

occupy different tidal levels with a variety of conditions. However, we found

some evidence for the occurrence of major biological zones on the

beaches sampled. Histograms (Fig. 3) and kite diagrams (Fig. 4) representing

the intertidal distribution of the macroinfauna and the multivariate analysis

(Fig. 5) showed that intertidal zonation was not clear in the beaches studied and

it was not possible to fit our results with the previously described general

patterns of zonation on sandy beaches (Dahl or Salvat’s zonation). The

ordination analysis found two zones with clear separation between supratidal

levels (9 and 10, occasionally including level 8) and the lower beach levels.

The high shore zone was clearly evident as a group, and MDS analysis

indicated a boundary between high and low shore assemblages for these

beaches; apart from this, other major biological zones were difficult to discern

(Fig 4). Our results suggest that intermediate beaches with this particular

profile generally display a typical macroinfaunal zonation divided into two

main zones: a narrow high-shore assemblage of air-breathing species below

which there is a wide zone of water-breather species (e.g. Brown and

McLachlan 1980). The special profile of the intermediate sandy beaches


109

studied here seems to fit well with this zonation scenario. Rafaelli et al., 1991

found the same zonation trend on Scottish beaches. We believe that is not

possible to establish a clear delimitation pattern in the lower part of the

intertidal for beaches with this particular profile, even though the ordination

and clustering analyses identify two possible different zones within the lower

beach part (b1 closer to the supralittoral levels of the beach and b2 in the lower

part) on a few of the beaches studied (San Pedro, Xivares, Vega, Toranda,

Oyambre, Liencres and Laredo). In general, this separation is much less

marked than that found between the upper (a) and lower zones (b1 and b2).

Thus, although we can elucidate a trend in some of the beaches for lower shore

zonation, the general pattern showed that zonation appeared unclear and

blurred in the lower shore levels (McLachlan and Jaramillo, 1995).

The zonation patterns described for intermediate beaches of Northern

Spain could be roughly related to Dahl’s scheme (1952), with a supralittoral

zone dominated by talitrid amphipods, considered indicative of the

subterrestrial fringe on exposed sandy beaches (McLachlan, 1983; McLachlan,

1988; Defeo et al., 1992; McLachlan et al., 1998). The intertidal zone, which

includes Rt and Rs zones, has a diverse macroinfauna, mainly cirolanid isopods

and haustoriid amphipods, and includes a lower saturation zone, directly

affected by the swash climate, where the spionid Scolelepis squamata and the

mysid Gastrosaccus sanctus occur. These species or congeners are frequently

found in the swash environment of most of the beaches studied worldwide

(Hayward and Ryland, pers. comm.; McLachlan, et al., 1981; McLachlan et al.,

1998). The lower zone of the studied beaches also harboured the highest

species richness and the highest abundances. This is a characteristic found on

the lower shore of sandy beaches in the United States (McLachlan, 1990),

South Africa (Bally, 1983; Wendt and McLachlan, 1985) and Chile (Jaramillo,

et al., 1993). Different works suggest a positive relationship between

abundance (density per m2) and species richness of macroinfauna and water

content of the sediment (Bally, 1983; Wendt and McLachlan, 1985; Defeo, et

al., 1992).


110

Ea

ster

n b

each

esO

YL

iL

gr

Be

Lr

Sv

Bk

Lg

ZH

R%

R%

R%

R%

R%

R%

R%

R%

R%

R%

Glo

bal

tes

t R

0.9

72

0.1

**0

.75

63

.6*

0.9

98

2.2

*0

.71

40

.5*

0,8

0.2

**-

--

--

--

--

-

Bea

ch l

evel

s

a-b

0.8

97

2.2

*0

.60

32

.2*

--

--

0.8

36

2.2

*0

.58

70

.5**

0.5

87

0.5

**0

.89

30

.8**

0.6

38

2.2

*0

.91

42

.2*

a-b

10

.99

84

.8*

0.8

13

3.6

*-

--

-0

.97

93

.6*

--

--

--

--

--

b1-b

20

.93

81

.8*

0.7

53

.6*

--

--

0.6

46

3.6

*-

--

--

--

--

-

Wes

tern

bea

ches

PO

SP

Xg

Xv

Es

Vg

To

A

R%

R%

R%

R%

R%

R%

R%

R%

R%

Glo

bal

tes

t R

--

--

0.9

48

0.1

**

--

0.8

40

.1**

--

0.7

63

0.6

**

0.7

82

0.2

**

--

Bea

ch l

evel

s

a-b

0.9

78

2.2

*0

.71

62

.2*

0.6

72

2.2

*0

.79

72

.2*

0.8

52

.2*

0.7

56

2.2

*0

.60

31

.7*

0.8

36

2.2

*0

.95

72

.2*

a-b

1-

--

-0

.78

66

.7-

-1

25

--

0.3

71

15

.60

.53

3.3

--

b1-b

2-

--

-0

.92

50

.8**

--

0.7

61

.2*

--

0.6

43

2.8

*0

.65

63

.6*

--

Ta

ble

3.

One

way

AN

OS

IM t

esti

ng f

or

dif

fere

nce

s b

etw

een

bea

ch l

evel

s: u

pp

er p

art

of

the

bea

ch (

a) a

nd

lo

wer

par

t (b

). P

oss

ible

div

isio

n d

ow

nsh

ore

was

des

crib

ed a

s b

1 a

nd

b2

. S

ee F

igure

4

fo

r le

vel

as

sem

bla

ges

. (*

sign

ific

ant

dif

fere

nce

; **ver

y si

gnif

ican

t

dif

fere

nce

; - n

o s

ignif

icant

dif

fere

nce

).

[(W

este

rn b

each

es;

P:

Peñ

arro

nd

a, O

: O

tur,

SP

: S

an P

edro

, X

g:

Xag

ó,

Xv:

Xiv

ares

, E

s:

Esp

asa,

Vg:

Veg

a, T

o:

Tora

nd

a, A

: A

nd

rín);

(E

aste

rn

bea

ches

; O

y:

Oyam

bre

, L

i: L

iencr

es,

Lgr:

Lan

gre

, B

e: B

erri

a, L

r: L

ared

o,

Sv:

Sal

vaj

e,

Bk:

Bak

io,

Lg:

Laga,

Z:

Zar

autz

, H

: H

end

aya)

.


111

-1.0 1.0

-1.0

1.0

Scolp

Pont

Donax

Gast

Bath

SphaerE pulE aff

Neph

Ophelia

Haut

Port

Talorc

CumopTalit salt

slope

long

Hb

Figure 6. Biplot resulting from the Canonical Correspondence Analysis. Full line

arrows for the environmental variables. Circles for the species most affected by

environmental parameters. The least affected species were plotted with triangles. Data

obtained from the averaged abundance values for all the beaches. (Talorc: Talorchestia britto, Ophelia: Ophelia bicornis, Gast: Gastrosaccus sanctus, Neph:

Nephtys cirrosa, Port: Portumnus latipes, Donax: Donax trunculus, Bath: Bathyporeia pelagica,

Cumop: Cumopsis fagei, Haut: Haustorius arenarius, Scolp: Scolelepis squamata, Sphaer:

Sphaeroma rugicauda, Talit salt: Talitrus saltator, E pul: Eurydice pulchra, E aff: Eurydice

affinis).

Some of the species of sandy beach macroinfauna exhibit some degree

of differential zonation of size classes worldwide (e.g. Dexter, 1977; Haley,

1982). Donax trunculus was found to show zonation by size on the Atlantic

coast (Ansell and Lagardère, 1980; de la Huz et al, 2002), with the smallest

individuals highest on the shore, and the largest confined to the lower saturated

zone in several temperate shorelines. The result of having the high numbers of

Donax trunculus at the Rt zone of the sampled beaches (11±1 ind.m-2) could be

related to the preference and zonation pattern of this species in the intertidal

zone. This also has been shown in other latitudes with Donax serra (Lastra and

McLachlan, 1996; Soares et al., 1996). Medium grain size showed a decrease


112

in all the nineteen intermediate sandy beaches at the upper part of the shoreline

(see Results section) which could explain this intraspecific zonation due to the

sediment preference (de la Huz et al., 2002).


variables.

Macroinfauna abundance and distribution in sandy beaches depend on

several physical and biological factors. Studies on United States, Australia and

South African sandy shores (McLachlan et al., 1993) and beaches from Chile

(Jaramillo and McLachlan, 1993) suggest that beach face slope and mean grain

size were the dominant patterns in community composition. Thus, there is a

general trend of decreasing species richness with increasing particle size and

beach face slope (steeper beaches), and increasing from reflective to dissipative

conditions. Short (1996), suggested that variables such as wave height and

period, sand size, beach slope and embayment dimensions can provide the key

elements in a global sandy beach classification. Furthermore, McArdle and

McLachlan (1992) suggested beach slope and wave height as the most

important factors controlling swash climate. Thus, swash climate on the beach

profile is the most important aspect of the environment by animals inhabiting

exposed sandy beaches, as McLachlan et al. (1993) subsequently refined in

their “swash exclusion hypothesis”. The pioneering studies carried out on

intermediate beaches on the northern coast of Spain found no significant trends

between the swash climate or the morphodynamic state with the macroinfauna

(Rodil and Lastra, 2004), confirming that communities in this type of beach are

controlled by several ecological factors rather than by a single key factor

(McLachlan et al., 1996; Brazeiro, 2001).

Mean grain size and beach face slope showed no significant variation

along the West to East beach gradient. In spite of the geographical continuum

formed by all the sampled beaches, water mass characteristics along the North

coast of Spain are determined by variations in coastal productivity at different

spatial scales. We believe that macroinfauna differences (ind.m-2) found

between the two groups of beaches arise from the chlorophyll-a concentration


113

gradient rather than from physical differences between beaches. The existence

of the upwelling event that is common along the eastern boundary of the North

Atlantic between 10º and 44ºN (Wooster et al., 1976) and focused in the North

west coast of Spain (Molina, 1972) can be involved in this gradient. Upwelling

favourable winds tend to increase the residual flows into the estuaries and rías

(Blanton et al., 1984; Prego and Fraga, 1992) and, consequently, the net influx

of nutrient-rich deeper water. Chlorophyll-a is a good index of the

phytoplankton concentration and food availability in the water column (Menge

et al., 1997). This fertilization leads to the high primary production, which

results in benthic enrichment (López-Jamar et al., 1992) and seems to dilute

when we move eastern through the North coast of Spain (Fernández and Bode,

1991; Teira et al., 2001; Lastra et al., 2006). Thus, it could be argued that

proximity to such upwelling areas leads to higher macroinfaunal abundance

values because of greater food availability due to the increase in productivity.

Canonical analysis (Fig. 6) indicates that environmental parameters

such as slope, beach length (long) and wave height (Hb) are the most important

factors explaining variability in the species density. In general terms, there is a

negative correlation between macroinfauna density and increasing beach face

slope, while no positive correlation with grain size was found. Species whose

density was not well explained by the environmental variables (found close to

the axis origin in Fig. 6) were generally found spanning the whole beach profile

(Figs. 3 and 4). Species broadly ordinated along the first CCA axis (Donax

trunculus, Bathyporeia pelagia and Cumopsis fagei) were found mainly at the

Rt and Rs zones (Fig. 4) and positively correlated with beach length and wave

height (Fig. 6). Other species such as Talorchestia brito and Ophelia bicornis,

found mainly at the upper levels, reached higher density values in beaches with

lower values of the three environmental variables (Fig. 6). The species with the

clearest zonation had the most significant relations with the environmental

variables. An increase in beach length together with more dissipative

conditions (low slope and high wave height) seems to affect these species

positively. Talitrus saltator was another invertebrate harbouring the upper part

of the beach but, in this case, no relations were found with any of the


114

environmental variables in the CCA. It seems that this kind of amphipod is not

affected by morphodynamic conditions. The abundances of Donax trunculus,

which also showed an intraspecific zonation, Bathyporeia pelagica and

Cumopsis fagei, which were found mainly at the lowest part of the shore, were

well explained by wave height and beach length but were not well explained by

beach slope. In general terms, variations in the environmental variables and

particular conditions of the beaches will affect macroinfauna densities and

distribution; but it seems that the species most affected by the environmental

variables were also those that showed more distinct zonation. Thus,

supralittoral macroinfauna was the least affected by the beach type while

species harbouring the lower levels, dependent on the swash regime, were more

affected by the main environmental variables.

In conclusion, macrofauna on intermediate exposed sandy beaches

from this geographical area showed no clear intertidal zonation, even though

they had two zones in common: a supralittoral zone (dry zone) and a littoral

zone. Subdivision of the lower part including Rt, Rs and S zones cannot be

clearly established. Community characteristics are affected by physical factors.

Beach length, slope and wave height were found to be the main variables

affecting macroinfauna on intermediate beaches, as previous works have

suggested. But it seems that the species with the clearest zonation were found

to be the best explained by the environmental variables than species with no

sharp boundaries in their distribution along the beach profile. Furthermore, it

seems that community characteristics in the beaches studied are not just, but

also by other factors dependent on oceanographic conditions and coastal

processes, determining critical characteristics such as water temperature and

food availability.

Acknowledgments

We would like to thank K. Aerts for helping with laboratory work and

C. de la Huz, M. Incera, J. López, M. Pita, G. Rodríguez, S. Cividanes and R.

Costas for field assistance. We also thank Dr. J.G. Rodríguez for critically

reading the manuscript and valuable comments and to the anonymous referees


115

who redirected the content of the original manuscript. Thanks also to Ian

Emmett for language revision. This research initiative was supported by the

University of Vigo (64102C859) and the Government of Galicia (XUGA

30105A98).

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PART III. THE IMPORTANCE OF EXPOSURE ON

SANDY BEACH MACROFAUNA: HYDRODINAMIC

CONDITIONS AND FOOD AVAILABILITY.

“What a trifling difference must often determine which shall survive,

and which perish!”

-Charles Darwin

letter to Asa Gray

Content:

Rodil, I.F., Lastra, M. and López, J. 2007. Macroinfauna community

structure and biochemical composition of sedimentary organic matter

along a gradient of wave exposure in sandy beaches (NW Spain).

Hydrobiologia 579: 301-316.

Chapter 4. Macroinfauna community structure and

biochemical composition of sedimentary organic matter

along a gradient of wave exposure in sandy beaches (NW

Spain).

Rodil, I.F., Lastra, M., and López, J.

Published in Hydrobiologia (2007). 579:301-316

Chapter 4 Community structure and biochemical composition

122

Abstract

Six sandy beaches on the North West coast of Spain, exposed to

different wave action, were sampled in order to study the macroinfauna

community and the biopolymeric fraction (proteins, lipids and carbohydrates)

of sedimentary organic matter. According to McLachlan’s rating system

(1980), three of them were classified as sheltered and the other three as

exposed beaches. Sampling was carried out during August 2004 at three tidal

levels: high, medium and low. Macroinfauna community and organic matter

concentrations were found to be significantly different when sheltered and

exposed beaches were compared. Macroinfauna diversity (H’), abundances and

biomass became increasingly enriched along a gradient from exposed to

sheltered beaches. Macroinfauna mean abundance was found higher in

sheltered (ranked from 1535±358 to 15062±5771 ind m-2) than in exposed

beaches (from 150±41 to 5518±1986 ind m-2). Macroinfauna biomass ranged

from 3.2 to 14.7 g m-2 and species richness from 25 to 27 in sheltered localities;

while in exposed beaches, biomass ranged from 0.2 to 2.3 g m-2 and the number

of species from 5 to 14. The biopolymeric carbon concentration (BPC) was

significantly higher in sheltered (from 84.7±44.7 to 163.3±34.8) than in

exposed (from 30.3±7.5 to 78.7±12.3) beaches. The low hydrodynamic

conditions of sheltered beaches favoured the settlement of organic rich fine

sediments, being supported by the higher protein to carbohydrate ratio found in

the exposed (from 23.5±0.9 to 32.7±4.4), rather than in the sheltered localities

(from 6.2±0.7 to 13.6). Mean macroinfauna abundances were higher at medium

and low tidal levels in both sheltered and exposed beaches. Crustacea was

found to be the main group inhabiting the upper part of both types of beaches,

dominating all tidal levels of exposed sandy beaches. Mollusca and Polychaeta

groups were dominant in sheltered beaches at the medium and lower levels.

There was a significant negative relationship between the BPC and the beach

face slope; thus, BPC decreased as the intertidal slope increased. It seems that

exposed sandy beaches are mainly physically-controlled; whereas hospitable


123

sheltered beaches let other factors, such as biochemical compounds enrich the

benthic fauna scenery.

Keywords: sandy beaches; exposure gradient; macroinfauna;

biochemical composition of sedimentary organic matter; biopolymeric fraction;

intertidal sediments.

3.4.1. Introduction

Sandy beaches are the most dynamic systems of soft bottom habitats

and the most widely distributed intertidal ecosystem, dominating both

temperate and tropical shores. Ecological studies in sandy beaches mostly dealt

with the faunal community structure and their relationship with environmental

conditions (such as wave energy and sand particle size).

It is generally admitted that biological richness, abundance and

biomass differ along a gradient of exposure rating (McLachlan, 1983;

McLachlan et al., 1996). The macrofauna of sandy beaches includes most

major invertebrate taxa, although it has been recognized that Bivalvia,

Crustacea and Polychaeta are the dominant groups (Brown and McLachlan,

1990). There is a trend for crustaceans to be more abundant in exposed beaches

and molluscs to be more abundant in the sheltered intertidal (McLachlan,

1983), although there are many exceptions (Dexter, 1983). In exposed

environments, intertidal fauna is mainly controlled by physical conditions

(McLachlan et al., 1993); it is suggested that the major hydrodynamic stress of

exposed localities limits their biological richness (McLachlan et al., 1996) and

several ecological factors influence the different community variables rather

than a single key factor (Brazeiro, 2001; Rodil and Lastra, 2004). In contrast,

higher macroinfauna abundance, biomass and diversity are found in sheltered

sedimentary environments (Adam, 1990) where biological interactions become

more important due to the higher species number and the higher proportion of

specialists found in those zones (Brown and McLachlan 1990).

It has been shown that food availability is one of the main factors

affecting community structure and benthic metabolism (Pearson and

Rosenberg, 1987; Grant and Hargrave, 1987; Thompson and Nichols, 1988;


124

Graf, 1989; Dugan et al., 2003). However, little is known about the amount of

food available on the intertidal sediment and its relationship with the

macroinfauna community. Several studies have shown the strong relation

between food availability and the biochemical composition of organic matter

(e.g. Tenore and Hanson, 1980; Danovaro et al., 1993). This biochemical

composition is the result of the equilibrium between external inputs,

autochthonous production and heterotrophic utilisation (Fabiano and Danovaro,

1994). The organic matter plays a major role within the detritus food chain. In

fact, the quality and quantity of organic matter in surface sediments are

recognised as primary nutritional sources affecting benthic fauna dynamics and

metabolism (Brown and McLachlan, 1990; Grant and Hargrave, 1987, Graf,

1989; Fabiano et al., 1995; Colombini et al., 2000). Food resources are one of

the most probable explanations for marine population patchiness (Decho and

Fleeger, 1988); thus, changes of sedimentary organic matter in marine

environments will affect spatial distribution, metabolism and dynamics of all

benthic organisms, from bacteria to macrofauna (Grant and Hargrave, 1987;

Graf, 1989; Duineveld et al, 1997). Organic matter in marine environments is

composed of labile and refractory compounds; however, only the former have

been used to estimate the nutritional value of the sediment (Buchanan and

Longbottom, 1970) because they consist of simple sugars, proteins and fatty

acids that are easily mineralised by bacteria and thus potentially available for

higher trophic levels (Fichez, 1991; Danovaro et al., 1993). Several studies

have estimated the fraction of sedimentary organic matter available for

consumers through the determination of biochemical classes of organic

compounds (i.e. carbohydrates, proteins and lipids), which are assumed to be

easier to digest and assimilate (Fichez, 1991; Danovaro et al., 1993; Fabiano et

al., 1995; Dell’Anno et al., 2000). The large amount of organic matter reaching

the sediments in sheltered intertidal areas are expected to induce a significant

benthic response (Josenfson and Conley, 1997), which could partially explain

the high abundance and diversity of the macroinfauna in these environments

compared to exposed intertidal sediments. Recent studies have pointed out that

the labile fraction of sedimentary organic matter can be used to describe the


125

trophic state and organic enrichment of marine coastal ecosystems (Dell’Anno

et al., 2002). There is a lack of information concerning the biochemical

composition of intertidal sediments and its direct relation with benthic

macrofauna. Most of the studies of macroinfauna community in sandy beaches

do not include detailed information of the biochemical composition from the

sediment and the influence of this variable on the distribution and abundance of

species. Recently, the origin and biochemical composition of organic matter

have been proposed as one of the key factors, together with the physical

environment (McLachlan, 1990), for the control of the beach fauna (Incera et

al., 2003).

In this paper, we analysed the macroinfauna structure and composition

of sedimentary organic matter over a range of intertidal sediments exposed to a

different degree of wave action (from sheltered to exposed). The aims of this

study are to investigate: (1) the influence of the physical characteristics on the

intertidal macroinfauna community along a gradient of wave exposure; (2) the

biochemical variability of the sedimentary organic matter in beaches with

different hydrodynamic conditions, and also (3) the relationship between

biochemical composition of the sedimentary organic matter and macroinfauna.

3.4.2. Material and methods

3.4.2.1. Study area

Six sandy beaches located on the northwest coast of Spain (Fig. 1) were

sampled during the low spring tides of August 2004. These localities are

influenced by a mesotidal regime with a mean tidal range of ca. 3 m.

According to their geographical situation in the ría system (sensu Méndez and

Vilas, 2005), these sandy beaches were subject to a different degree of wave

exposure. Three of them, namely Broña, Bornelle and Cabanas, located in the

inner part of the ría (from 42º 46’ to 42º 49’ N and from 8º 55’ to 9º 1’ W) were

characterised by low exposure conditions. According to the 20-point rating

system proposed by McLachlan (1980), this group was considered as sheltered

beaches. The others, namely Xeiruga, Baldaio and Niñóns, located in the outer


126

part of the ría (from 43º 17’ to 43º 18’ N and from 8º 40’ to 8º 54’ W) were

characterised as exposed beaches (McLachlan, 1980).

Figure 1. Location of the study area and localities sampled on the northwest coast of

Spain.


Sampling was carried out at six replicated transects (in triplicate),

randomly separated, at the central area of each beach, after ebbing, at three

tidal levels (high, medium and low). Following the traditional sandy beach

zonation; high level correspond to Salvat’s dry zone (1964) and Dhal’s

supralittoral fringe (1952); medium level correspond to Salvat’s retention zone

and Dhal’s midlittoral zone and low level correspond to Salvat’s saturation

N iñó ns X eiruga

Ca ba na s

Broñ a

Born el le

Ba lda io


127

zone and Dahl’s sublittoral zone. Macroinfauna samples were collected with 25

cm diameter metal corer penetrating 15 cm depth into the substrate. The

sediment was sieved through 1 mm mesh and the residue was preserved in 4%

formalin. The individuals were later sorted from the sediments, identified and

counted in the laboratory. Shell-free biomass of all the species was determined

by drying at 100ºC for 24 hours and then 500ºC for 6 hours, obtaining ash free

dry weight values.

Three sediment samples were collected by hand coring from sediment

surface down to 15 cm depth at the three tidal levels. Each sediment sample

was mixed and subsamples were taken for the analysis of lipids, proteins and

carbohydrates. All subsamples were frozen at -30ºC until further processing.

Moreover, three samples of sediment for grain size analyses and water content

were also collected at each tidal level by inserting a 3 cm diameter corer to a

depth of 15 cm. Shear strength (kPa) of saturated sediments was also

determined with a shear vane tester and measurements were carried out in the

upper 5 cm of the sediment. Grain size analysis was carried out by means of a

Coulter Counter LS200. Beach slope (Slope=1/R; R=intertidal width/ height of

the high intertidal level) estimated for the entire beach was determined by

Emery’s profiling technique (Emery, 1961). Wave height and wave period

were estimated in order to calculate dimensionless Dean’s parameter (Ω)

according to Short and Wright (1983) and Beach State Index (BSI) according

to McLachlan et al., 1993 was also calculated. Finally, the new beach index

(BI) formulated by McLachlan and Dorvlo (2005) was calculated as follows:

[BI = log10 (Mz x TR)/ S]; where TR is the tidal range, S is the beach slope and

Mz is the mean sand particle size expressed in (phi units + 1), to avoid negative

values (McLachlan and Dorvlo, 2005).

3.4.2.3. Biochemical analysis.

All data were normalized to sediment dry weight after desiccation

(60ºC, 24 h) and finely powdered with a pestle (Pulverisette 2, Fritsch). Total

proteins (PRT) were determined using the method of Lowry & Rosebrough

(1951) modified by Markwell et al. (1978). Concentrations are referred as


128

bovine serum albumin (BSA) equivalents. Total carbohydrates (CHO) were

analysed according to Dubois et al. (1956) and expressed as glucose

equivalents. Total lipids (LIP) were extracted from dried samples using

chloroform and methanol solution according to the method of Bligh and Dyer

(1959) and Marsh and Weinstein (1966) and measured as tripalmitine

equivalents. All analyses were carried out on three replicates (about 0.5-2.5 g

of sediment was used for each analysis). For each biochemical analysis, blanks

were made using the same sediments previously treated in a muffle furnace

(500ºC 6 h).

Protein, carbohydrate and lipid concentrations were converted into

carbon equivalents, using 0.49, 0.40 and 0.75 conversion factors, respectively

(Fabiano et al., 1995). Biopolymeric carbon concentration (BPC) was

calculated according to Fabiano and Danovaro (1994) as the sum of proteins,

carbohydrates and lipid converted to carbon equivalents according to Fichez,

1991. The BPC is considered a reliable estimate of the fraction of total organic

matter readily available to benthic consumers (Fabiano et al., 1995). Protein to

carbohydrate ratio (PRT:CHO) was also calculated and assumed as an

estimation of organic material ageing (Fabiano et al., 1997).

3.4.2.4. Data analysis.

Pearson’s correlation and regression analysis were carried out to test

for relationships between biotic and abiotic variables in all the beaches.

Macroinfauna community and organic matter content were assessed by a two-

way ANOVA analysis, with exposure (sheltered vs. exposed) and tidal levels

(high, medium and low) as factors (Sokal and Rohlf, 1995). When a significant

difference was observed (p<0.05), a Tukey’s pairwise comparison test was also

performed to elucidate possible differences between levels of a factor

(exposition rate and tidal levels). The relationship between BPC and exposure

rate across tidal level was determined by ANCOVA. All these statistical

analysis were performed using SPSS version 12.0.

Primary description of faunal assemblages at high taxonomic level was

performed by normalizing the proportion of the relative abundances of the main


129

invertebrate taxa; i.e., Crustacea, Mollusca and Polychaeta, were plotted on

ternary graphs arranged as an equilateral triangle with scatter and lines.

Non-metric multidimensional scaling ordination (MDS), with the Bray-

Curtis similarity index, was performed to describe possible changes on the

macroinfauna community between exposed and sheltered beaches and among

different beach tidal levels. Measurement of goodness-of-fit of the MDS

ordination was given by the stress value (S); where low stress factor (S<0.2)

corresponds to a good ordination with no real prospect of a misleading

interpretation (Clarke and Warwick, 1994). The presence of highly abundant

species was standardized with a double square root transformation. Pairwise

analysis of similarities (ANOSIM, Clarke 1993) was carried out to test the null-

hypothesis that there were no differences (at α = 0.05) in the composition of the

macroinfaunal assemblages at different beaches (sheltered vs. exposed) and at

different tidal levels. The nature of the community groupings identified in the

MDS ordinations was further explored by applying the similarity percentages

program (SIMPER), to determine the contribution of individual species to the

average dissimilarity between type of beaches (exposed vs. sheltered) and tidal

levels (Clarke, 1993; Clarke and Warmick, 1994). These analyses were

performed using the PRIMER 5 software package.

3.4.3. Results


The profile and the beach face slope for each locality are shown in

Figure 2. Beach profile showed reflective conditions in the exposed group of

beaches (Xeiruga, Baldaio and Niñóns), being narrower and steeper than in

sheltered localities (Broña, Bornelle and Cabanas) (t6=2.83, p<0.05). A full

characterization of physical variables and indices of the sandy beaches

analysed are provided in Table 1. The values of the dimensionless Dean’s

parameter, categorized Broña, Bornelle and Cabanas as reflective (Ω<1) and

Xeiruga, Baldaio and Niñóns as intermediate-reflective (1<Ω<2) in

morphodynamic state. BSI classification included all the beaches in the


130

intermediate morphodynamic state (0.5<BSI<1) and new BI index classified all

the localities studied as mesotidal intermediate beaches (B.I.>2).

Figure 2. Intertidal beach slope of the studied localities. S: beach slope (intertidal

width/height of the high intertidal level).

The mean grain size (M.G.S.) values obtained in sheltered localities

presented finer grain sand (from 241 to 294 μm) than the exposed intertidal

localities (from 389 to 571 μm) (t6=2.97, p<0.05). Swash amplitude was higher

(from 4 to 8 m) and shear strength was significantly lower (from 3.6 to 5.4

KPa) in the exposed localities (t6=2.8, p<0.05). There is a significant linear

correlation between exposure rate and medium grain size (M.G.S.= 44.65 x

Exposure -123.7; R2=0.740, p<0.05) and Shear strength (Shear strength= 16.4 –

0.88 x Exposure; R2=0.666, p<0.05). Sediment water content decreased

significantly with increasing tidal level (two-way crossed ANOVA F=20.7,

p<0.01; R2=0.704) and Tukey’s post hoc test showed that differences occurred

Distance from low tide level (m)

0 40 80 120 1600

2

4

6

8

Broña

S = 1/27

0

2

4

6

8Xeiruga

S = 1/22

Cabanas

S = 1/30

Bornelle

S = 1/70

Heig

ht

ab

ove lo

w t

ide level (m

)

0

2

4

6

8Baldaio

S = 1/14

Niñóns

S = 1/12

0 40 80 120 160


131

between high and low levels (p=0.01) and between high and medium levels

(p<0.01); while no significant water content differences occurred between

medium and low levels and between localities (exposed vs. sheltered).

Table 1. Physical characteristics of the six sandy beaches. a Length of beach. b Width of beach c Mean ± SD of the measured values at each sampled transect. d Mean of the measured values during low tide (n> 30) e Wave height (n>30) f sensu McLachlan´s (1980) rating system (i.e. [wave action, surf zone width,% very

fine sand, median particle diameter and slope, depth of reduced layers, stable

burrows.])

3.4.3.2. Composition and abundance of the macroinfauna

The number of species, mean abundance and biomass (Table 2 and Fig.

3) were found higher in sheltered localities. Number of species was found

significantly higher in sheltered rather than in exposed beaches (Table 3) and

also the interaction between tidal level and exposure rate was found

significantly different (p=0.03) for this variable. Hence, species richness

showed a different pattern of variability between tidal levels in the beaches.

The number of species dropped sharply with decreasing tidal level in the

exposed beaches and rose in sheltered localities (Figure 3). Polychaeta and

Mollusca abundances increased significantly from exposed to sheltered beaches

(Table and Fig. 3). Figure 4 shows mean total abundance (ind m-2) of the main

groups of macroinfauna at each tidal level in the two types of beaches.

Mollusca (p<0.01) and Polychaeta (p<0.05) mean abundances were found to be

significantly higher (Tukey’s post hoc test) at the low part of the beaches rather

than at the upper levels (Fig. 4). Interaction between exposure and tidal level

Beach L (m)a

W (m)b

Slope (1/S) Shear strengthc

M.G.S (μm)c

Swash (m) Ω BSI B.I. Exposure ratingf

T (s)d

Hb (m)e

Broña 490 88 1/27 9.3±1.3 241±18 6.5 0.1 2.5 0.5 0.5 2.41 8 [1,0,2,4,1,0]

Bornelle 550 170 1/70 9.7±0.7 294±24 7.9 0.24 3 0.52 0.52 2.84 10 [0,0,2,7,1,0]

Cabanas 255 100 1/26 6.02±2.0 277±80 5 0.11 3.1 0.59 0.55 2.34 10 [0,0,2,7,1,0]

Xeiruga 490 86 1/22 5.4±2.5 389±76 8.4 0.7 7.6 1.56 0.9 2.27 12 [1,0,2,7,1,1]

Baldaio 3650 55 1/14 3.6±1.9 398±53 8.7 0.7 8 1.33 0.84 2.10 13[1,0,2,7,2,1]

Niñóns 170 50 1/12 5.1±2.0 571±31 6.6 1.1 4 1.89 0.98 2.01 14 [1,1,2,7,2,1]

Waves


132

was significant for Polychaeta group, meaning that the increase in Polychaeta

abundances was stronger in sheltered conditions (Table 3). The abundance of

macroinfauna is remarkably low at the medium tidal level differing from other

results (i.e. Brown and McLachlan, 1990; Degraer et al., 1999; Janssen and

Mulder, 2005). Biomass values (g m-2) were significantly higher in sheltered

condition, but no differences among tidal levels were found. On the other hand,

mean abundance values did not display significant differences between exposed

and sheltered conditions (Table 3). Sheltered sandy beaches were dominated by

Crustacea at the high tidal levels (99% of the mean total abundance) and by

Polychaeta at medium (84.4%) and low (76.3%) levels. Exposed sandy beaches

were completely dominated by Crustacean at high (100%) and medium

(76.6%) tidal levels, whereas Polychaeta dominated low levels (94.5%).

Mollusca were the less abundant macroinfauna group in all the beaches

sampled and dominated in none of the tidal levels (Fig. 5). Macroinfauna

diversity (H’) was also significantly and inversely correlated with the exposure

rating (H’= 3.46 – 0.142 x Exposure, R2=0.45; p<0.01).

Beach

Species

richness Abundance (ind.m-2)a Biomass (g.m-2) H’b Jc

Broña 25 1535±358 3.2±2 2,9 0.62

Bornelle 26 15062±5771 14.7±11 2,1 0.46

Cabanas 27 5261±1597 7.2±7 2,4 0.5

Xeiruga 8 1475±488 1±0.9 2,2 0.73

Baldaio 5 150±41 0.2±0.1 1,5 0.63

Niñóns 14 5518±1986 2.3±1.9 1,9 0.51 Table 2. Macroinfauna characteristics at the studied beaches.

a Mean’s ± SD of the values at each sampled transect. b Shannon-Wiener diversity index (calculated using neperian logarithms). c Evenness was calculated using Pielou’s J (J = H’/H’max.).

3.4.3.3. Intertidal distribution of the macroinfauna

The one-way ANOSIM (Table 4) found significant differences in

community macroinfauna structure between exposed and sheltered beaches

(global test, p<0.01); significant differences were also found when medium and

low tidal levels were compared between localities (exposed vs. sheltered).

ANOSIM test showed differences in each locality between high and the rest of


133

the tidal levels (Table 5). MDS ordination analysis of the macroinfauna

community assessed the relationships between localities and tidal levels. High

tidal levels, from both morphodynamic types (exposed and sheltered), were

found closer related than other tidal levels, forming an aggregated group

separated from the rest of the tidal levels sampled (Table 4 and Fig. 6).

Finally, similarity-percentages analysis (SIMPER) of square-root

transformed macroinfauna data, showed that macroinfauna differences between

medium tidal levels from sampled beaches (exposed vs. sheltered) were due to

the high abundance contribution of both Polychaeta, Scolelepis squamata and

Ophelia bicornis (15.5 and 15.2% respectively) in sheltered beaches. The

analysis between lower levels from the localities (exposed vs. sheltered)

showed that the high abundance of the Polychaeta Malacoceros fuliginosa

(18.1%) in sheltered beaches, contributed to the main dissimilarity at this level

(see Appendix A-D, Part III).

3.4.3.4. Organic matter composition

Significant differences were noted in the biochemical compounds

concentrations (i.e. protein, carbohydrate and lipid) between exposed and

sheltered sandy beaches (Table 6). Thus, in the sheltered intertidal sediments,

protein, carbohydrate and lipid concentrations were higher than in the exposed

ones (mean concentrations at the three tidal levels). Proteins were the dominant

compound in both groups of beaches (63.4% and 80.2% for sheltered and

exposed localities respectively), followed by lipids (30 and 17%) and

carbohydrates (7 and 3%). Protein concentrations ranged from 104±38 to

239.5±61 and from 64.7±33.5 to 117.1±49 μg g-1 dry weight (d.w.) in sheltered

and exposed sediments respectively. Carbohydrates ranged from 11.8±4.2 to

22.5±12.5 and from 2.4±1.3 to 4.4±2.1 μg g-1 d. w. and lipid concentrations

ranged from 41.5±40.5 to 114.2±38 and from 16.2±10.8 to 20.3±12.6 μg g-1 d.

w., respectively (Figure 7). PROT:CHO ratio was significantly higher in the

exposed (values from 23.5±0.9 to 32.7±4.4) than in the sheltered

conditions(from 6.21±0.7 to 13.6±5.73).


134

Figure 3. Mean total macroinfauna abundance (ind m-2) and biomass (g m-2) expressed

as ash free weight dry and species richness in sheltered (closed bars) and exposed (open

bars) localities at the three tidal levels (high, medium and low). Mean ± standard error

(SE) is presented.

Abu

ndan

ce (i

nd m

- 2)

0

5

10

15

A.F

.D.W

. (g

m- 2

)

0

2000

4000

6000

8000

10000

Tidal level

Num

ber

of s

peci

es

0

5

10

15

20

High Medium Low


135

Table 3. Summary of two-way crossed ANOVA results of exposure (exposed vs.

sheltered) and tidal level (high, medium, low) effect on macroinfauna abundance

(ind.m-2) and biomass (g.m-2).

*Data were converted using a log (X +1) transformation prior to the analysis as

described by Clarke (1993). Bold values indicate significant differences (P < 0.05).

The BPC fraction was found to be significantly higher in the sheltered

intertidal (Table 6) and those values were also found to be higher at the low

than at the high tidal level of the intertidal (p<0.05, Tukey’s post hoc test). No

significant difference was found between medium and low or medium and high

tidal levels. There was a significant negative relationship between BPC mean

concentrations (μg g-1 d.w.) at the three tidal levels and beach slope (S),

meaning that BPC concentrations become increasingly impoverished as the

intertidal slope increased (along the gradient from sheltered to exposed

beaches). Interaction between tidal level and intertidal slope was not significant

[ANCOVA; tidal level effect: F2,11=14.08, p=0.001; intertidal slope

(covariable): F1,11=5.35, p=0.041; tidal level*intertidal slope: F2,11=1.185,

p=0.342 (n.s.)]; thus, the relationship described above was similar in all the

tidal levels analysed in all the beaches. There was also a significant and inverse

correlation between BPC and the exposure rate (BPC=3.35 – 0.13 x Exposure,

R2= 0.723; p<0.05) and a direct correlation between PRTO:CHO and the

exposure rate (PROT:CHO=3.91 x Exposure – 24.63, R2=0.89; p<0.05).

Correlation between PROT:CHO and intertidal slope was found not to be

significant.

Biomass* Crustacean Polychaeta Mollusca Species

abundance* abundance* abundance* richness

F ratio p F ratio p F ratio p F ratio p F ratio p

Exposure 9,34 0.01 0.016 0.9 15.87 0.002 5.91 0.032 72 0.02

Tidal level 0.625 0.55 0.55 0.59 5.12 0.025 9.34 0.004 1.88 0.195

Exp x tid lev 1.02 0.39 0.48 0.62 5.12 0.02 0.81 0.47 4.81 0.03


136

Figure 4. Mean total abundance (ind m-2) ± SE of the main macroinfauna groups in

sheltered and exposed sandy beaches at the three tidal levels.

Results showed a significant and direct relationship between organic

matter compounds and macroinfauna community (mean values obtained at the

three tidal levels in all the beaches). Thus, there were an increase in

macroinfauna diversity (H’), species richness and in the abundance of some of

Sheltered beaches

Abu

ndan

ces

(ind

m-2

)

0

1000

4000

6000

8000

Exposed beaches

Tidal level

High Medium Low

Abu

ndan

ces

(ind

m-2

)

0

1000

4000

5000

6000 Crustacea

Mollusca

Polychaeta

Others


137

the taxonomic groups (log transformed data) with proteins [(Species

richness=9.7 + 0.061 x prot; R2=0.23, p<0.05); (Polychaeta abundance=0.01 x

prot. – 0.643; R2=0.61, p<0.01)], carbohydrates [(H’=0.03 x cho + 1.87;

R2=0.437, P<0.01), (Species richness=1.94 – 0.015 x cho; R2=0.61, p<0.01),

(Polychaeta abundance=0.05 x cho – 0.1; R2=0.44, p<0.01)], lipids [(Mollusca

abundance=0.71 + 0.02 x lip; R2=0.31, P<0.05), (Polychaeta abundance = 0.1 –

0.043 x lip; R2 = 0.4, p<0.01)] and BPC [( Species richness=1.9 – 0.002 x BPC;

R2=0.45, p<0.01), (Polychaeta abundance=0.01 x BPC – 0.52; R2=0.62,

p<0.01) ] concentration values.

Figure 5. Ternary plot in three axis of the relative abundances (%) from the main

macroinfauna groups in sheltered (filled circles) and exposed (open circles) localities at

the three tidal levels (H: high, M: medium, L: low). 100% corresponds with the whole

sum of the Crustacea, Mollusca and Polychaeta percentage.

Crustacea

0 10 20 30 40 50 60 70 80 90 100

Mollusca

0

10

20

30

40

50

60

70

80

90

100

Polychaeta

0

10

20

30

40

50

60

70

80

90

100

M L

L M

H


138

Table 4. Results of the ANOSIM and pair-wise tests for difference on macroinfauna

community structure between tidal levels (exposed vs. sheltered).

Table 5. Results of the ANOSIM and pair-wise tests for difference on macroinfauna

community structure between tidal levels of exposed and sheltered beaches.

3.4.4. Discussion

3.4.4.1. Macroinfauna characteristics in a gradient of exposure

Results obtained in this study suggest that macroinfauna community, in

terms of abundance, biomass and species richness, was more complex and

diverse in sheltered than in exposed sandy beaches. This has been the general

trend found in other studies where an exposure increase led to a decrease in

biotic variables (Dexter, 1992; McLachlan et al., 1993; Jaramillo and

McLachlan, 1993; McLachlan et al., 1996; Rodil and Lastra, 2004). Correlation

and regression analysis showed a direct effect of exposure rating on

morphodynamic beach conditions. Thus, M.G.S and shear strength were

R p

Global test 0.884 0.001

Levels compared (exp. vs. shelt.)

High-high 0.963 0.1

Medium-medium 0.833 0.002

Low-low 0.98 0.003

Exposed beaches Sheltered beaches

R p R p

Global test 0.352 0.04 0.528 0.036

Levels compared

High-Medium 0.75 0.03 0.98 0.03

High-Low 0.996 <0.01 0.996 <0.01

Medium-Low 0.607 0.13 0.786 0.06


139

significantly related to exposure. There was a positive relationship between

water content and macroinfauna (two-way ANOVA F=20.7, p<0.01), meaning

that the lower tidal level, with higher water content, harboured a richer

macroinfauna community due to the lower desiccation time, lower temperature

change and the higher feeding time available for the organisms (Wendt and

McLachlan, 1985). Supratidal levels, where environmental conditions are harsh

for truly marine macrofauna, showed lower number of species and were

dominated exclusively by crustaceans such as talitrid amphipods and cirolanid

isopods. The ability of this macroinfauna to utilize the upper levels of sandy

beaches must relate to their adaptations to avoid desiccation (McLachlan, 1990;

Little, 2000). Exposed sandy beaches with short swashes and steep slopes

harbour a rich macrofauna community which find a more stable environment in

the supralittoral zone (Defeo and Gómez, 2005); meanwhile, the number of

species inhabiting the lower part diminished sharply. No significant differences

in the biotic variables were found when supralittoral community from exposed

and sheltered localities were compared. Most of the species at this level (talitrid

amphipods, isopods and insects) have been considered wrack-associated

macrofauna and they largely depend on allochthonous inputs associated with

oceanographic processes (Colombini and Chelazzi, 2003; Dugan et al, 2003).

Sheltered beaches, with more favourable environmental conditions and

sediment stability, showed higher significant values of macrofauna abundance,

biomass and species richness than in exposed intertidal when medium and low

tidal levels, from both environments, were compared. Low macroinfauna

values obtained at the medium tidal level in both, exposed and sheltered

beaches could be due to the special beach profile. These beaches showed a

broken profile roughly separated by mean sea level into an upper steep beach

followed by a lower flat downshore, as was previously found on beaches from

the north coast of Spain (Rodil and Lastra, 2004). Medium tidal level was

located close to this broken profile where hydrodynamic forces occurred

directly during tidal flow affecting macroinfauna zonation and probably

macroinfauna abundance and biomass (Rodil et al., 2006).


140

Figure 6. Biplots resulting from the multidimensional scaling analysis of the

macroinfauna (density values expressed as ind m-2) and species richness on each beach.

[(Sheltered localities: filled circles; Br: Broña, Bo: Bornelle, Ca: Cabanas; Exposed

localities: open circles; Ni:Niñóns, Ba: Baldaio, Xe: Xeiruga). (Capital letters indicate

tidal level: A: high, B: medium; C: low)].

Hydrodynamic and beach morphodynamic effect on biotic variables is

now considered a paradigm in ecology of sandy beaches at the community

level (Defeo and McLachlan, 2005). Swash climate and sand particle size will

define the response of the macroinfauna due to the increasing harshness in

these factors. The macroinfauna biomass and species richness in the studied

localities diminished significantly when the exposure rating increases (coarse

sediment and short and turbulent swashes). Mollusca and Polychaeta mean

abundances diminished significantly with the exposure rating and there were

also significant differences between tidal levels (Table 3). Both faunistic

groups increased their mean abundances significantly at the medium and low

tidal levels where a significant increase in water content also occurs. This part

of the beach is considered to be under optimal conditions of sand moisture,

BrA

BrB

BrC

BoA

BoB

BoC

CaA

CaB

CaC

XeA

XeB

XeC

NiA

NiB

NiC

BaA

BaB

BaC

Stress: 0,06


141

penetrability and temperature, following the Habitat Favourability Hypothesis,

(Defeo et al., 2001). Thus, high densities of truly marine species will be able to

occupy this part of the sandy beaches, where more gentle physical conditions

are found, competing for space and food. Mollusca was the least abundant of

all the macroinfauna groups found in sheltered localities, and the bivalves

Cerastoderma edule and Donax trunculus were the main components. Species

belonging to this group were not found in any of the exposed localities. This

kind of intertidal locality, with harsher physical conditions and coarser

sediment, can have a negative effect on burrowing and respiration rate and

growth of filter feeder D. trunculus (de la Huz et al., 2002). Sheltered sandy

beaches, with lower hydrodynamic conditions will favour accumulation of

organic matter potentially available to benthic deposit-feeders. Abundance

variation of Polychaeta moving downshore was different in both groups of

beaches. There was an increase in the mean abundance values of this group in

the medium and low tidal levels of the beaches, but it was only significant in

sheltered conditions. Most of the species belonging to this group were deposit-

feeders being favoured by the settlement of organic rich sediments. Dexter’s

(1983) work suggests that crustaceans and polychaetes dominate the most

exposed and sheltered beaches respectively, with molluscs reaching maximum

abundance in intermediate situations. It is generally admitted in sandy beach

ecology that the number of species, macrofauna density and biomass increase

along a morphodynamic gradient from reflective to dissipative conditions

(Defeo et al., 1992, Jaramillo and McLachlan, 1993, McLachlan et al., 1996)

and also, sandy shores show an increase in the biotic variables as exposure

decreases (McLachaln, 1990). On the other hand, Crustacea mean abundances

did not change significantly in any of the situations mentioned above and this

group was found almost exclusively at the high tidal levels of all the sampled

localities (Fig. 4). Supralittoral forms are less influenced by the swash climate

and generally have autonomous active movement on this part of the beaches.


142

Table 6. Summary of two-way crossed ANOVA results of exposure (exposed vs.

sheltered) and tidal level (high, medium, low) effect on organic sedimentary compounds.

Bold values indicate significant differences at p< 0.005

BPC: biopolymeric carbon concentrations

3.4.4.2. Biochemical composition of sedimentary organic matter

The amount of biopolymeric fraction that can be found in coastal

sediments is a minor fraction of the organic carbon pool found in the water

column (Danovaro and Fabiano, 1997). The quality and quantity of organic

matter in surface sediments have been considered to of particular importance in

determining the amounts of material potentially available to consumer

organisms, thus affecting community structure and benthic metabolism

(Thompson and Nichols, 1988; Graf, 1989). In this study, biochemical

compounds concentrations of sedimentary organic matter showed significant

differences between sheltered and exposed beaches. Thus, biochemical

concentrations were higher in sheltered localities, probably related to the

morphodynamic and physicochemical characteristics of this kind of sandy

beaches. This suggests that BPC concentrations could be one of the factors

responsible for the increase of benthic macrofauna in sheltered localities. The

lack of relationship between some of the macrofaunal descriptors and sediment

biochemical composition could be due to the snapshot sampling design. We are

aware that these results could change when considering longer temporal scales

but the observed patterns of macrofauna and biochemical compounds seem to

be better related in sheltered beaches than in exposed ones. The low

hydrodynamic conditions of sheltered localities favour accumulation of organic

matter in addition to the settlement of fine sediments which limit the renewal of

interstitial water. The relative contribution of the biochemical compounds to

Proteins Carbohydrates Lipids BPC PROT:CHO

F ratio p F ratio p F ratio p F ratio p F ratio p

Exposure 9.497 0.01 1.438 0.003 1.188 0.005 2.123 0.001 28.1 0.01

Tidal level 3.849 0.051 0.891 0.436 1.7 0.224 4.861 0.02 2.43 0.6

Exposure x tidal level 2.295 0.143 0.545 0.593 1.317 0.304 2.961 0.2 0.59 0.25


143

the total organic pool was clearly dominated by proteins, followed by lipids and

carbohydrates. BPC concentrations were also significantly higher at medium

and low tidal levels, in all the beaches sampled, compared with the supralittoral

level (Table 6 and Fig. 7).

Figure 7. Overall mean protein, carbohydrate and lipid concentrations at the three tidal

levels and different exposure (sheltered: closed bars; exposed: open bars). Standard

deviation is represented.

The intertidal slope of the beach is one of the parameters used to

estimate the degree of hydrodynamic forces on intertidal sandy beaches

(McLachlan, 1980) and this factor usually increases with increasing exposure.

Lipids

Tidal level

0

30

60

90

120

150

Carbohydrates

Bio

po

lym

eri

c c

arb

on

co

nc

en

tra

tio

ns

(µ

g g

-1 d

ry w

eig

ht)

0

10

20

30

40

Proteins

0

50

100

150

200

250

300

350

High Medium Low


144

The exposed sampled localities showed a significant increase in the reflective

slope conditions (t6=2.83, p<0.05) due to the harsher morphodynamic

conditions. BPC concentrations were found significantly and inversely

correlated with the intertidal slope from all the beaches; although no significant

differences in the BPC concentration was found among the three tidal levels of

the sandy beaches. Thus, it seems that biopolymeric concentrations follow a

similar pattern that is shown by organisms increasing from exposed intertidal

with steeper slopes to sheltered sandy beaches with flatter slopes.

Organic matter availability is the result of the interactions between

physical and biological processes. A significant and inverse correlation

between BPC concentrations and the exposure rate was also found, which

confirms the drop of material potentially available to consumer organisms

when we move through a gradient of sandy beach exposure. It seems that the

control of beach fauna is complex and determined not only by the physical

environment but also by several ecological factors including the biochemical

composition of the organic matter in the sediments.

The protein to carbohydrate ratio (PROT:CHO) has been used to assess

the ‘age’ of sediment organic matter (Cauwet, 1978). Since proteins are more

readily used by bacteria than carbohydrates (Newell and Field, 1983), high

PROT:CHO ratios (>1) are generally associated with recently produced organic

matter. By contrast, low ratios suggest the presence of aged organic matter and

the role of proteins as a potentially limiting factor for benthic consumers

(Danovaro et al., 1993; Fabiano et al., 1995). In this study, average

PROT:CHO ratios and biochemical compounds obtained were similar to other

intertidal works (Cividanes et al., 2002; Incera et al., 2003) but they ranked

high when compared with the subtidal ratios reported in the literature

(Danovaro et al., 1993; Fabiano et al., 1995). Carbohydrate concentrations in

other works were found to be higher in the deep-sea (Danovaro et al., 1993),

being a characteristic of highly oligotrophic or detritic environments. Our

results suggest that most of the sedimentary organic matter in these beaches

was recently produced and that protein is not a limiting factor for consumer’s

growth.


145

Figure 8. Relationship between intertidal slope (S) and biopolymeric carbon

concentrations (μg g-1 d.w. of sediment) of sedimentation at the three tidal levels.

Sheltered localities are presented as filled circles and exposed localities as open circles.

[ANCOVA; tidal level effect: F2,11 = 14.08, p = 0.001; intertidal slope (covariable):

F1,11 = 5.35, p = 0.041; tidal level*intertidal slope: F2,11 = 1.1815, p = 0.342 (n.s.)].

High tidal level

0 20 40 60 80 100

0

20

40

60

80

100

120

140

Low tidal level

Slope

0 20 40 60 80 100

60

80

100

120

140

160

180

200

220

Medium tidal level

0 20 40 60 80 100

Ca

rbo

n o

f th

e b

iop

oly

me

ric

fra

cti

on

20

40

60

80

100

120

140

160

180

Xeiruga

Xeiruga

Niñons

Baldaio

Cabanas

Broña

Bornelle

Xeiruga

Baldaio

Baldaio

Niñons

Niñons

Broña

Broña

Bornelle

Bornelle

Cabanas

Cabanas


146

The higher ratios found in exposed rather than in sheltered sandy beaches

indicate that there is little dead organic matter accumulation in exposed

localities, probably due to the strong hydrodynamic conditions. It seems that

with decreasing exposure, beaches tend to behave as storage sites of organic

matter (Little, 2000), with a higher accumulation rate. The high PROT:CHO

ratio, together with the high concentrations of BPC classified these beaches as

eutrophic systems (sensu Dell’Anno et al., 2002). Moreover, since proteins

constituted the main dominant fraction of BPC (on average, 63.4% and 80.2%

for sheltered and exposed localities respectively) and carbohydrates showed the

lowest values measured in all the beaches, the organic matter seems to be

mostly of ‘newly-generated’ detritus and autochthonous origin. Although the

high organic matter concentrations found in the sheltered intertidal could be

better explained by the influence of temporal allochthonous inputs of carbon

and organic material since little primary production occurs on the beach itself

(Brown and McLachlan, 1990).

Thus, the results obtained showed that the dominant species in

sheltered beaches belong to the deposit-feeder group (above all from

Polychaeta group), which base their feeding on organic sedimentary

assimilation (Brown and McLachlan, 1990; Knox, 2000). Subterrestrial species

dominate the upper tidal levels of all the beaches; they will be the main

macroinfauna group in the exposed localities since they do not depend on the

swash climate but upon allochthonous inputs such as wrack macroalgae. It has

been suggested in the literature that fauna decreasing along a gradient from

sheltered to exposed beaches is caused by the increase in harsh swash climate

and coarser grain size (McLachlan et al., 1996). In this study we have

confirmed this fact but moreover, the biochemical compounds and the BPC

concentrations decreasing along the same gradient of exposure, suggests

largely that food quality could be a main factor affecting macroinfauna

community in the intertidal.

Acknowledgements

We are extremely grateful to S.Gil and M.Lago for helping us with

laboratory work and for their invaluable assistance during sampling. This


147

research was supported by the Government of Spain (Ministerio de Medio

Ambiente; CICIT, REN2002-03119) and the Regional Government of Galicia

(Augas de Galicia and XUGA PGIDIT02RMA30101PR). Funds to I.F. Rodil

were provided by a Ph.D. grant from the Xunta de Galicia (Predoctorales Xunta

P.P. 0000 300S 140.08). We wish to thank two anonymous referees for kindly

advising us on some details of this paper.

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PART IV. THE ROLE OF FOOD AVAILABILITY IN

SANDY BEACHES: SPATIAL AND TEMPORAL

PATTERNS.

“We may infer from these facts, what havoc the introduction of any new

beast of prey must cause in a country, before the instincts of the

aborigines become adapted to the stranger’s craft or power.”

-Charles Darwin

Journal of Researches

Contents:

Rodil, I.F., Cividanes, S., Lastra, M. and López, J. Seasonal variability

in the vertical distribution of benthic macrofauna and sedimentary

organic matter in an estuarine beach (NW Spain). Estuaries and coasts

(accepted, in press).

Rodil, I.F., Olabarria, C., Lastra, M. and López, J. Differential effects

of native and invasive algal wrack on macrofaunal assemblages

inhabiting exposed sandy beaches. Journal of Experimental Marine

Biology and Ecology (accepted, in press).

Chapter 5. Seasonal variability in the vertical distribution

of benthic macrofauna and sedimentary organic matter in

an estuarine beach (NW Spain).

Chapter 5 Seasonal variability in an estuarine beach

153

Abstract.

This study was designed to investigate seasonal changes on food

available for benthic consumers in relation to tidal levels and sediment depth in

an estuarine beach. The relationships between the biochemical characteristics

of sedimentary organic matter and benthic macrofauna were analysed quarterly

over two years (from January 1997 to January 1999), in an estuarine soft

intertidal zone from the NW coast of Spain (42º 64’ 04’’N; 8º 88’ 36’’W).

Sediment samples were collected in order to provide a two-dimensional view of

macroinfauna distribution in the intertidal zone and its relationship with the

quantity and quality of the organic matter. The nutritional value of organic

matter (i.e., lipid, protein and carbohydrate) and the content of chlorophyll a of

the sediment were measured. Macrofaunal assemblages and food availability in

the sediment were studied at three tidal levels on the shore: two intertidal and

one supratidal.

Macroinfauna and biochemical compounds showed a clear vertical

stratification with the highest macrofaunal abundance at the superficial layer of

the sediment, where redox potential discontinuity was also observed.

Crustaceans were found mainly inhabiting the supratidal level of the estuarine

beach, while, polychaetes and molluscs occupied the intertidal level. Food

availability, measured as biopolymeric carbon, and also chlorophyll a from the

sediment were better related to macroinfauna abundance, biomass and

abundance of main taxonomic groups. Macrofauna assemblages showed

particular distribution in both vertical and horizontal ranges suggesting specific

preferences to several abiotic factors. No clear seasonal pattern was found in

macrofauna and sedimentary organic characteristics suggesting that

macrofaunal assemblages are controlled by complex and unpredictable factors,

including small scale changes in substrate and hydrological characteristics.

Keywords: Estuarine beaches; macroinfauna; spatial and temporal patterns;

biopolymeric carbon; food availability; sedimentary organic matter; NW Spain.


154

4.5.1. Introduction

Intertidal macroinfauna is regarded as an important component of

marine communities, occupying a key role in the breakdown and incorporation

of organic matter into sediments in coastal ecosystems (Levin et al., 2001).

Intertidal invertebrate communities show temporal and spatial patterns which

are the result of the ability of species to cope with changes in physical and

biological factors associated with major environmental gradients, such as tidal

influence, exposure rate and water and substrate characteristics. Soft sediments

present important biotic and abiotic variations, not only at spatial and temporal

scales, but also in terms of vertical distribution. Several sediment

characteristics such as compactness, water content or grain size are able to

influence the vertical distribution of the macroinfauna.

The organic matter in the sediment, as well as dead material, plays a

major role within the detritus food chain because it includes living organisms

such as bacteria and microalgae, which have been considered one of the most

nutritive food sources (Grémare, 1994; McIntyre et al., 1996). Quantity and

quality of organic matter in surface sediments are recognised primary factors

affecting benthic fauna dynamics and metabolism as well as community

structure (Fabiano et al., 1995; Dugan et al., 2003). The distribution of benthic

communities in sandy intertidals is well known (e.g. Peterson, 1991, Dittmann,

2000). Little is known, however, about the characteristics of food available and

its relationship with the macroinfauna community in the intertidal zone.

Food availability is related to the biochemical composition of organic

matter and several studies have estimated the fraction of sedimentary organic

matter available for consumers by determining the biochemical classes of

organic compounds (i.e. carbohydrates, proteins and lipids), which are assumed

to be easier to digest and assimilate (Fabiano et al., 1995). The concentration of

biochemical compounds and the percentage of total organic matter (TOM) have

been used to estimate the nutritive value of the sediment. Chlorophyll a

concentration in the sediment has been measured as a surrogate of microalgae

biomass and has been widely used in the literature (e.g. Fabiano et al., 1995;

Grémare et al., 1997).


155

The large amount of organic matter reaching the intertidal zone in

sheltered areas is expected to induce a significant benthic response which could

partially explain the high abundance and diversity of the macroinfauna in these

environments compared to other coastal ecosystems such as exposed sandy

beaches (e.g. Incera et al., 2006; Rodil et al., 2007). The nutritive value of

sedimentary organic matter may show marked seasonal changes and low values

have often been found in late spring and summer (Grémare et al., 1997; Rossi,

2002). Furthermore, the availability of food resources could be important in

regulating the dynamics of benthic macrofauna (Rossi et al., 2001).

Much of the previous macroinfauna research on soft intertidals is

restricted to general considerations of the factors influencing individual species

and macroinfauna assemblages, while analyses of vertical and horizontal

zonation are scarce. The main purpose of this study was to characterise a two-

dimensional view of macroinfauna distribution along a tidal gradient in an

estuarine beach in order to understand its relationships with environmental

parameters and food availability. Data on the sedimentary organic matter and

environmental parameters from 1997 was previously published in Cividanes et

al., 2002. This study provides longer term seasonal data for the vertical and

horizontal distribution of substratum characteristics and macrofaunal species.

In this paper, we test hypotheses regarding influences on macrofaunal

assemblages inhabiting an estuarine beach. In particular, we test the hypothesis

that (1) the environmental conditions vary between the supratidal and the

intertidal zones and through sediment depth, (2) the quality and quantity of

sedimentary organic matter, i.e., food available, differ over the tidal level,

through sediment depth and over time and, as a result, (3) macrofauna

assemblages vary over time and space in the estuarine beach. Furthermore, we

predicted that macrofauna variability and distribution are strongly related to

specific factors such as food availability.


156

Figure 1. Location of the estuarine beach (Barraña) on the NW coast of Spain. a)

Relative position of Galicia and the intertidal b) Intertidal slope and temporal changes

observed throughout the study period (1997-1999). Approximate situation of the three

levels on the shore (HTL: high tidal level; MTL: medium tidal level; LTL: low tidal

level).

4.5.2. Material and methods.

4.5.2.1. Study area

The study site is located in the Ria of Arousa, on the NW coast of the

Iberian Peninsula (Figure 1a). Barraña is a sheltered beach, 2150 m long,

influenced by a mesotidal regime with a mean tidal range of 3 m. This sandy

intertidal zone is located in the inner part of the ria (sensu Méndez and Vilas,

2005) delimited by a local river mouth and characterised by low wave

exposure, shallow reduced sediment layers and the presence of macrofaunal

burrows. This ria is tide-dominated and the beach studied was flushed

Barraña

a

Distance (m)

0 100 200 300

He

igh

t (m

)

0

1

2

3

4

5

b

HTL

MTL

LTL


157

regularly. The intertidal profile was measured (Fig. 1b) and no significant

differences were found over time (F8,15 = 0.067, p > 0.05). Barraña is affected

by large amounts of allochthonous organic matter. In this study, algal mats

were present throughout the entire intertidal range (350 m long), but lower on

the shore, as they moved about with tides and waves.


From January 1997 to January 1999, sediment samples were collected

quarterly during spring low tide. Sampling was carried out at three replicated

transects, randomly separated, at the central area of the beach at three tidal

levels; one supratidal (high) and two intertidal (medium and low). Due to beach

morphology, medium tide level appeared covered with some water resembling

a pond during ebbing, which created a unique environment (Figure 1b).

Macroinfauna samples were collected with a 15.5 cm diameter metal corer

penetrating 25 cm deep into the substrate (n = 3) at each transect (188.7 cm2

surface area). The samples were divided into 5 layers (0-5, 5-10, 10-15, 15-20,

20-25 cm depth). The sediment was sieved through 1 mm mesh and the

individuals were sorted from the sediments, identified and counted in the

laboratory. Shell-free biomass of all the species was determined by drying at

100ºC for 24 hours and then 500ºC for 6 hours, obtaining ash free dry weight

values.

Sediment samples for biochemical and chlorophyll a analyses were

collected in three replicates by hand coring (15.5 cm inner diameter core) at the

three tidal levels. Samples were also vertically sliced into five layers; each

layer was homogenized by hand mixing and subsamples (frozen at -30 ºC) were

taken for the analysis of sedimentary organic matter, grain size and water

content. Mean grain size was performed by means of a Coulter Counter LS 200

and sediment shear strength by means of a shear vane meter. Sediment water

content was estimated as the difference between wet and dry weight (60 ºC, 72

h) and expressed as a percentage. Temperature (ºC) and redox potential (Eh)

were measured at 5 cm intervals down to 25 cm sediment depth.


158

4.5.2.3. Biochemical composition of the sedimentary organic matter

Biochemical compounds of organic matter were evaluated by

spectrophotometric analyses of lipid, carbohydrate and protein concentration in

the sediment. For all analyses, 0.5-2.5 g of sediment was used (data normalised

to sediment dry weight; sed dw). All biochemical analyses were conducted on

sediment samples previously oven dried at 60 ºC until weight was constant and

finely powdered with a pestle. Total lipids (Bligh and Dyer, 1959),

carbohydrates (Dubois et al., 1956) and proteins (Markwell et al., 1978) were

analysed. The sum of the main biochemical classes; i.e. the nutritional value,

was reported as the biopolymeric carbon (BPC sensu Fabiano et al., 1995),

assumed as a reliable estimate of the labile fraction available to benthic

consumers. The protein to carbohydrate ratio (PROT:CHO) was also calculated

to assess the age of the organic material. A detailed description of the analyses

is reported in Cividanes et al. (2002).

Total sediment carbon (TOC) and nitrogen (TN) were determined on

sediment subsamples (15-20 mg) in order to obtain BPC:TOC (%) and C:N

ratio, which were used as a food and quality index respectively . The residual

fraction of the organic carbon (complex organic matter, COM; Fichez, 1991)

was determined as the difference between TOC and BPC. Analyses of dry

weight sediment chlorophyll a (Chla, μg g-1) were extracted following

Lorenzen (1967). The chlorophyll a content was assessed by homogenizing

samples from all five depth layers.

4.5.2.4. Data analysis

Data from macrozoobenthic communities were analysed in terms of

number of species, abundance (ind m-2) and biomass (g m-2). Relative

contribution of the major macrobenthic groups (i.e. Crustacea, Mollusca and

Polychaeta) and also contribution of five major trophic groups (i.e. subsurface

and surface deposit feeders, suspension feeders, carnivores and others) as

percentage of the total individual numbers were tested to elucidate dominance

and trophic characteristics of the macroinfauna (Pearson and Rosenberg, 1987).


159

Temporal and spatial fluctuations in biochemical and macrofauna

variables were assessed by a four-factor orthogonal analysis of variance with

year (1997 and 1998), month (January, April, July and October), tidal level

(high, medium and low) and depth (0-25 cm) as fixed factors (Sokal and Rohlf,

1995). When necessary, transformations were used to achieve the assumptions

of homogeneity and normality. A posteriori Tukey’s pairwise comparison test

was also performed to elucidate possible differences between levels of a factor

(p < 0.05). Multivariate analyses were used to determine temporary differences

in the species composition of the benthic assemblage and to assess which

species mainly contributed towards the seasonal differences. Data was carried

out on transformed data (4th square root) using the Bray-Curtis index and

group average linkage for non-metric multidimensional scaling (MDS). The

discrimination of fauna assemblages along tidal levels and over time was tested

with one-way ANOSIM. Species typifying assemblages were identified using

the SIMPER program (Clarke, 1993). The link between the biotic pattern and

abiotic variables was explored using the biological environmental gradients

(BIO-ENV) procedure, which aimed to select the environmental variables

subset that maximises the rank correlation (ρ) between biotic and abiotic

similarity matrix (PRIMER). Whenever possible, general patterns among

particulate organic matter, biochemical characteristics, environmental variables

and benthic macrofauna were assessed using principal component analysis

(PCA; CANOCO 4.5). A generalised linear model (GLM) with a log-linear

model (Poisson error term and forward multiple logistic-regression analysis)

was used to compare the relationships between biotic and abiotic variables.

This model is more flexible and better suited for analysing ecological

relationships which can be poorly represented by classical Gaussian

distributions (Guisan et al., 2002). The significance of the independent

variables was tested using the χ2-test (Wald statistic; Statistica 6.0).


160

Table 1. Summary of analyses of variance of the effect of time (Year: 1997 and 1998;

Month: January, April, July, October), tidal level (i.e. high, medium and low) and

sediment depth (0-25 cm) on several environmental variables. (N = 360). Data from

1999 (one month) was not included. M.G.S.: mean grain size, S.S.: shear strength; Eh:

redox potential T: Temperature; W.C.: water content. Significance levels: *: p < 0.05;

**: p < 0.01; ***: p < 0.001; ns: p > 0.05. +log transformed data

4.5.3. Results.

4.5.3.1. Environmental characteristics.

Mean grain size (M.G.S.) and shear strength (S.S.) showed significant

differences over the tidal level and through sediment depth (Table 1) but this

pattern was not consistent over time (i.e., significant Y x M x L x D

interaction). M.G.S. and S.S. increased with sediment depth (Tukey’s post hoc

test). Grain size was coarser at the high tidal level (HTL) than at the mid

(MTL) and low tidal levels (LTL) and S.S. was lower at the supratidal level.

Compactness was lower in January, while sediment was coarser in July and

October (post hoc test). Positive values of redox potential (Eh) were found at

the HTL, although they became negative at the intertidal levels through

sediment depth (post hoc test). Redox potential discontinuity (RPD) was

observed at 5-10 cm depth at the intertidal and this pattern was consistent over

space and time (i.e., no significant Y x M x L x D interaction). Water content

and temperature showed a seasonal pattern, between months, ranging from

16% (July 1997, HTL, 15-20 cm) to 25% (January 1997, LTL, 5-10 cm depth)

Source of variation M.G.S.+ S.S.

+ Eh T W.C.

d.f. p p p p p

Year (Y) 1 n.s n.s *** *** n.s.

Month (M) 3 *** *** *** *** ***

Tidal level (L) 2 *** *** *** *** ***

Depth of the sediment (D) 4 *** *** *** n.s. ***

Y*M 3 ** *** *** *** ***

Y*L 2 * *** *** *** *

M*L 6 *** *** *** *** ***

Y*M*L 6 ** *** *** *** ***

Y*D 4 n.s. *** ** n.s. *

M*D 12 ** ** * * n.s.

Y*M*D 12 *** * n.s. *** n.s.

L*D 8 *** ** *** *** **

Y*L*D 8 *** n.s. n.s. n.s. n.s.

M*L*D 24 * ** n.s. *** n.s.

Y*M*L*D 24 * *** n.s. n.s. n.s.


161

and from 10.9 ºC (January 1998, HTL, 0-5 cm) to 22 ºC (July 97, HTL, 20-25

cm) respectively. These patterns were consistent over space and time (no

significant Y x M x L x D interaction).

4.5.3.2. Macrobenthic community.

All the biotic variables varied significantly over the tidal level and

through sediment depth (Table 2) but this pattern was not consistent over time

(i.e. significant Y x M x L x D interaction). Macrofauna abundance was higher

in July and October than in April and January and biomass and the number of

species were higher in July (post hoc tests). As regards vertical distribution

(Figure 2), abundance, biomass and number of species were found to be higher

in the superficial sediment level (0-15 cm, post hoc test). The MTL presented

the highest macroinfauna abundances (17124±4931 ind m-2, October 1997),

biomass (2.061±0.202 g m-2, April 1997) and species values (26, July 1997)

and the HTL the lowest values (18±16 ind m-2, April 1998; 0.001±0.001 g m-2,

January 1998 and 1 species, April 1998). Biotic variables obtained from MTL

were found to be significantly higher than those from LTL (post hoc test).

The contribution of the main macroinvertebrate groups changed at the

three tidal levels and with sediment depth and there was some temporal

variation (Table 2 and Figure 3). Polychaeta and Mollusca were the most

representative groups in the overall intertidal macroinfauna accounting for 53%

and 36%, respectively. Polychaeta showed no significant differences between

months (post hoc test) but was found to be significantly higher at the intertidal

(MTL>LTL>HTL) and in the sediment surface (5>10>15=20=25 cm depth).

This pattern was not consistent over space and time (i.e., significant Y x M x L

x D interaction). The relative contribution of this group accounted for 28%

(January 1999) to 98% (April 1998) at the MTL and from 56% (July 1998) to

91% (July 1997) at the LTL. The density of molluscs was also higher at the

intertidal level (MTL>LTL>HTL) and in the sediment surface (0-15 cm) in

July and January (post hoc test) and this pattern was consistent over time

(Table 2).


162

Ta

ble

2.

Su

mm

ary o

f anal

yse

s o

f var

iance

of

the

effe

ct o

f ti

me

(Yea

r: 1

99

7 a

nd

19

98

; M

onth

: Ja

nuar

y,

Ap

ril,

July

, O

cto

ber

), t

idal

lev

el

(i.e

. hig

h,

med

ium

and

lo

w)

and

sed

iment

dep

th (

0-2

5 c

m)

on m

acro

infa

una

abu

nd

ance

(in

d m

-2),

bio

mas

s (g

m-2

), n

um

ber

of

spec

ies

and

abund

ance

of

the

thre

e m

ain t

axo

no

mic

gro

up

s. D

ata

fro

m 1

99

9 w

as n

ot

inclu

ded

. (N

= 3

60

). S

ignif

ican

ce l

evel

s: *

: p

< 0

.05

;

**:

p <

0.0

01

; ***:

p <

0.0

01

; ns:

p >

0.0

5. +

log t

ransf

orm

ed d

ata

A

bu

nd

an

ce

Sou

rce

of

vari

ati

on

Ab

un

dan

ce+

Bio

mass

S

pec

ies

Poly

chaet

es

Moll

usc

s C

rust

ace

an

s+

d.f

. p

p

p

p

p

p

Yea

r (Y

) 1

***

***

***

*

n.s

. **

*

Month

(M

) 3

***

**

***

n.s

. n.s

. **

*

Tid

al l

evel

(L

) 2

***

***

***

***

***

**

*

Dep

th o

f th

e se

dim

ent

(D)

4

***

***

***

***

***

n

.s.

Y*M

3

n.s

. *

n.s

. **

n.s

. **

Y*L

2

***

***

***

**

n.s

. **

*

M*L

6

***

n.s

. **

***

n.s

. **

Y*M

*L

6

***

n.s

. ***

***

n.s

. **

*

Y*D

4

n.s

. n.s

. n.s

. ***

n.s

. n

.s.

M*D

12

**

n.s

. n.s

. **

*

n.s

.

Y*M

*D

12

*

**

*

***

n.s

. *

L*D

8

***

***

***

***

***

**

Y*L

*D

8

n.s

. n.s

. n.s

. **

n.s

. n

.s.

M*L

*D

24

**

*

n.s

. ***

**

n.s

.

Y*M

*L

*D

24

**

*

*

***

n.s

. n

.s.


163

20-2

5

15-2

0

10-1

5

5-1

0

0-5

20-2

5

15-2

0

10-1

5

5-1

0

0-5

20-2

5

15-2

0

10-1

5

5-1

0

0-5

Ab

un

da

nc

e (

ind

/m2

)

05

00

01

00

00

15

00

02

00

00

20-2

5

15-2

0

10-1

5

5-1

0

0-5

J 9

7

A 9

7

O 9

7

O 9

7

Sediment depth

20-2

5

15-2

0

10-1

5

5-1

0

0-5

Ju

97

20-2

5

15-2

0

10-1

5

5-1

0

0-5

A 9

7

20-2

5

15-2

0

10-1

5

5-1

0

0-5

Bio

ma

ss

(g

/m2

)

24

68

J 9

7

Ab

un

da

nc

e (

ind

/m2)

01000

2000

3000

20-2

5

15-2

0

10-1

5

5-1

0

0-5

Bio

ma

ss

(g

/m2

)

10

20

30

MT

LH

TL

Ju

97

20-2

5

15-2

0

10-1

5

5-1

0

0-5

20-2

5

15-2

0

10-1

5

5-1

0

0-5

20-2

5

15-2

0

10-1

5

5-1

0

0-5

Ab

un

da

nc

e (

ind

/m2

)

02

00

04

00

06

00

08

00

0

20-2

5

15-2

0

10-1

5

5-1

0

0-5

J 9

7

A 9

7

Bio

ma

ss

(g

/m2

)

36

91

21

5

LT

L

Ju

97

O 9

7

Fig

ure 2

. V

ert

ical

dis

trib

uti

on

of

the a

bu

nd

ance (

m-2

±sd

) an

d b

iom

ass

(g.m

-2±

sd)

of

the m

acro

infa

una a

t th

e t

hre

e t

idal

levels

(HT

L.

MT

L a

nd

LT

L)

over

tim

e (

J: J

anuary

. A

: A

pri

l. J

u.

July

. O

: O

cto

ber

fro

m 1

99

7 t

o 1

99

9).


164

Bio

mass (

µg

/m2

)

51

01

52

02

5

20-2

5

15-2

0

10-1

5

5-1

0

0-5

20-2

5

15-2

0

10-1

5

5-1

0

0-5

20-2

5

15-2

0

10-1

5

5-1

0

0-5

20-2

5

15-2

0

10-1

5

5-1

0

0-5

20-2

5

15-2

0

10-1

5

5-1

0

0-5

20-2

5

15-2

0

10-1

5

5-1

0

0-5

20-2

5

15-2

0

10-1

5

5-1

0

0-5

Sediment depth

20-2

5

15-2

0

10-1

5

5-1

0

0-5

Ab

un

dan

ce (

ind

/m2)

05

00

01

00

00

15

00

02

00

00

20-2

5

15-2

0

10-1

5

5-1

0

0-5

Ab

un

dan

ce (

ind

/m2)

02

00

04

00

06

00

08

00

0

20-2

5

15-2

0

10-1

5

5-1

0

0-5

Bio

mass (

µg

/m2)

10

20

30

J 9

9

20-2

5

15-2

0

10-1

5

5-1

0

0-5

O 9

8

20-2

5

15-2

0

10-1

5

5-1

0

0-5

Ju 9

8

20-2

5

15-2

0

10-1

5

5-1

0

0-5

A 9

8

20-2

5

15-2

0

10-1

5

5-1

0

0-5

Bio

mass (

µg

/m2

)

24

68

J 9

8

Ab

un

dan

ce (

ind

/m2

)

05

00

10

00

15

00

20

00

20-2

5

15-2

0

10-1

5

5-1

0

0-5

HT

LM

TL

LT

L

A 9

8

J 9

8

O 9

8

Ju 9

8

O 9

8

Ju 9

8

A 9

8

J 9

8

J 9

9

J 9

9

Fig

ure 2

. V

ert

ical

dis

trib

uti

on

of

the a

bu

nd

ance (

m-2

±sd

) an

d b

iom

ass

(g.m

-2±

sd)

of

the m

acro

infa

una a

t th

e t

hre

e t

idal

levels

(HT

L.

MT

L a

nd

LT

L)

over

tim

e (

J: J

anuary

. A

: A

pri

l. J

u.

July

. O

: O

cto

ber

fro

m 1

99

7 t

o 1

99

9).


165

This group accounted for about 3% (April 1997) to 71% (January 1999) at the

MTL and from 2% (October 1997) to 41% (January 1998) at the LTL. Most of

the crustaceans (mainly Talitrid amphipods) were found at the supratidal (post

hoc test) with significant seasonal variability (July=October>January=April),

accounting for 5% (January 1998) to 100% (October 1998) of the overall

macroinfauna at this level.

Figure 3. Temporal changes in the abundance of the three taxonomic groups

(Polychaetes. molluscs and crustaceans) and number of species with tidal levels and

sediment depths. Mean average (ind.m-2) and standard deviation are shown.

0-5 cm 5-10 cm 10-15 cm 15-20 cm 20-25 cm depth

HTL

Ja97A97Ju97O97Ja98A98 J98 O98Ja99

Ab

un

dan

ce P

oly

ch

aeta

(in

d/m

2)

0

1000

2000

3000

Ja97A97Ju97O97Ja98A98 J98 O98Ja99

Ab

un

dan

ce C

rusta

cea (

ind

/m2

)

0

1000

2000

3000

Ja97A97Ju97O97Ja98A98 J98 O98Ja99

Ab

un

dan

ce M

oll

usca (

ind

/m2

)

0

1000

2000

3000

Ja97A97Ju97O97Ja98A98 J98 O98Ja99

nu

mb

er

of

sp

ecie

s

0

5

10

15

MTL

Ja97A97Ju97O97Ja98A98 J98 O98Ja99

0

2000

4000

6000

8000

10000

12000

14000

Ja97A97Ju97O97Ja98A98 J98 O98Ja99

0

2000

4000

6000

8000

10000

12000

14000

Ja97A97Ju97O97Ja98A98 J98 O98Ja99

0

2000

4000

6000

8000

10000

12000

14000

Ja97A97Ju97O97Ja98A98 J98 O98Ja99

0

5

10

15

LTL

Ja97A97Ju97O97Ja98A98 J98O98Ja99

0

2000

4000

6000

8000

10000


0

2000

4000

6000

8000

10000


0

2000

4000

6000

8000

10000


0

5

10

15


166

A classification of the macrobenthic organisms into five different

trophic groups (see Appendix IV) gave a numerical dominance of subsurface

and surface deposit-feeders at the MTL (87%, April 1998 and 72%, January

1999) and LTL (62%, April 1997 and 93%, July 1997). The trophic group

classified as “others” as the main dominant at the HTL and carnivores

accounted for 29% at the LTL (April 1998).

Figure 4. Non-metric multidimensional scaling (MDS) analysis of the macroinfauna

(ind m-2). Letters indicate months (J: January; A: April; Ju: June; O: October) and

numbers indicate years (1997. 1998, 1999). : high tidal level; : medium tidal

level; low tidal level.

The macroinfauna assemblage showed significant differences over time

(ANOSIM global test; R = 0.594, p < 0.05). The MDS analysis for total

macroinfauna abundances and species (Figure 4) presented the intertidal levels

clearly separated (R = 0.802, p < 0.001). Macrofauna assemblage from HTL

showed significant differences with MTL (R = 0.892, p < 0.001) and LTL (R =

0.942, p < 0.001) and also significant dissimilarity was found between MTL

and LTL (R=0.737, p < 0.001). The organisms mainly responsible for the tidal

level differences (SIMPER) were the talitrid Talorchestia deshayesii (33% of

J97

J97

J97

A97A97

A97

JU97

JU97

JU97

O97

O97

O97

J98

J98

J98

A98

A98

A98

JU98 JU98

JU98

O98

O98

O98

J99

J99

J99

2D Stress: 0,12


167

the total contribution) and several insect larvae (28.8%) at the HTL; the

polychaeta Capitella sp. (22.4%) and the gastropod Hydroid vulvae (16%) at

the MTL and the polychaeta Spoil falconries (19.3%) and the bivalve Lories

luminaries (14.7%) at the LTL. The abundance of Capitella sp. (7.2 %) and

Hydroid vulvae (6.7%) were the most responsible for the dissimilarities over

time (complete list of species in Appendix IV).

4.5.3.3. Organic matter composition and chlorophyll a content.

The annual average concentration during the study period for

carbohydrate, lipid and protein was 289±224, 596±496 and 1226±1060 μg g-1

sed dw, respectively (Figure 5). The statistical analyses revealed that the

nutritive value of the sediment displayed significant variability (Table 3)

although it was not consistent over space and time (i.e., significant Y x M x L x

D interaction). Maxima concentrations were found at the MTL and diminished

with sediment depth (post hoc test). Protein concentrations were higher during

winter and spring than in summer (April>January=October>July), while

carbohydrate and lipid concentrations were higher in summer and autumn (post

hoc test). The BPC showed a similar trend to protein pattern (this figure is

therefore not shown) with maximum values in April at the MTL (significant M

x L x D interaction). PROT:CHO ratio showed significant variability (Table 3)

but this pattern was not consistent over space and time (i.e., significant Y x M x

L x D interaction). This ratio was higher at the beginning of the year

(January>April>July=October) and significant differences were found among

tidal levels (MTL>LTL=HTL).

Seasonal variations of the elemental composition of sedimentary

organic matter across space were plotted in Figure 6. Total organic carbon

(TOC), complex organic matter (COM) and total nitrogen (TN) presented

significant variability (Table 3) but this pattern was not consistent over space

and time (i.e., significant Y x M x L x D interaction).


168

The composition of sedimentary organic matter reached the highest values at

the MTL (post hoc test). TOC and COM concentrations were found lower in

winter (January<April=July=October) and in the sediment surface

(5=10=15=20<25 cm). TN showed seasonal variability with higher values at

the end of the summer (October>July=April>January) and in the sediment

surface (5=10>15=20>25 cm).

Figure 5. Temporal variations in the concentrations of carbohydrates, proteins and

lipids with tidal levels and sediment depths. Values are given as micrograms per gram

sediment dry weight (µg g-1 sed d.w. ± sd).

The BPC: TOC ratio indicated that BPC accounted for a relevant fraction of the

total organic carbon (44%). Higher C:N ratio values were recorded at the MTL,

ranging between 4.4 (January 1997, 0-5 cm) and 22.5 (January 1998, 20-25

cm). Chlorophyll a (Chl a; 4.55±4.18 μg g -1 sed dw on annual average)


Carbohydrates (µg g-1 sed d.w.)

0

200

400

600

800

1000

HTL

0

1000

2000

3000

4000

5000

Ja97A97 J97 O97Ja98A98 J98 O98Ja99

0

500

1000

1500

2000

Proteins (µg g-1 sed d.w.)

0

200

400

600

800

1000

0

1000

2000

3000

4000

5000

Ja97A97 J97 O97Ja98A98 J98 O98Ja99

0

500

1000

1500

2000

MTL

LTL

Lipids (µg g-1 sed d.w.)

0

200

400

600

800

1000

0

1000

2000

3000

4000

5000

Ja97A97 J97 O97Ja98A98 J98 O98Ja99

0

500

1000

1500

2000


169

showed seasonal variability (Fig. 6 and Table 3) but this pattern was not

consistent over space and time (i.e., significant Y x M x L x D interaction).

Higher concentrations were found in summer and late summer

(October>July>April=January) at the intertidal (MTL>LTL=HTL) in the

sediment surface.

4.5.3.4. Relationships between sedimentary organics and benthic fauna.

According to BIO-ENV (Table 4), the best correlations (ρs) were found

with sediment grain size and water content and also with some biochemical

compounds such as BPC, prot:cho, C:N, TOC, COM and Chl a. Although this

procedure does not give the direction of such correlations, it can indicate that

these variables possibly influence the differences in community structure. The

projection of variables based on environmental, biochemical and faunal

parameters recorded during the time of study was plotted in Figure 7. The first

and second axes accounted for 63.0% and 15.1% of the variance respectively.

The positive axis linked several faunal characteristics such as number of

species, biomass and abundance of polychaetes to the biochemical compounds

(BPC) and Chl a. Macroinfauna abundance appeared to be associated with the

same biochemical variables. Furthermore, biomass of the macroinfauna showed

high positive values associated with TOC, TN and BPC:TOC. Faunal

parameters were also associated with environmental parameters such as water

content. The abundance of crustaceans was positively associated to some of the

environmental parameters such as Eh, M.G.S. and S.S. These results were

further supported by multiple regression analysis (Table 5).


170

Sou

rce

of

vari

ati

on

Pro

tein

+

Carb

oh

yd

rate

+

Lip

id+

BP

C†

TO

C

CO

M†

TN

p

rot:

cho

C

hlo

rop

hyll

a+

d.f

. p

p

p

p

p

p

p

p

p

Yea

r (Y

) 1

***

***

***

***

***

**

***

***

***

Month

(M

) 3

***

***

***

***

***

***

***

***

***

Tid

al l

evel

(L

) 2

***

***

***

***

***

***

***

***

***

Dep

th o

f th

e se

dim

ent

(D)

4

***

***

***

***

***

***

***

***

***

Y*M

3

***

***

***

***

**

***

***

***

***

Y*L

2

***

n.s

. n.s

. *

n.s

. n.s

. ***

***

n.s

.

M*L

6

***

***

***

***

***

***

***

***

***

Y*M

*L

6

***

***

***

***

***

***

***

***

***

Y*D

4

***

**

*

n.s

. n.s

. n.s

. n.s

. n.s

. ***

M*D

12

***

*

n.s

. n.s

. n.s

. n.s

. n.s

. n.s

. ***

Y*M

*D

12

n.s

. n.s

. n.s

. n.s

. *

**

n.s

. **

***

L*D

8

***

**

n.s

. *

***

***

***

*

***

Y*L

*D

8

***

n.s

. n.s

. n.s

. ***

***

n.s

. n.s

. n.s

.

M*L

*D

24

***

***

n.s

. *

***

**

n.s

. **

***

Y*M

*L

*D

24

***

**

*

n.s

. ***

***

*

*

***

Ta

ble

3.

Su

mm

ary o

f anal

yse

s o

f var

iance

of

the

effe

ct o

f ti

me

(Yea

r: 1

99

7 a

nd

199

8;

Mo

nth

: Ja

nuar

y,

Ap

ril,

July

, O

cto

ber

), t

idal

lev

el (

i.e.

hig

h,

med

ium

and

lo

w)

and

sed

iment

dep

th (

0-2

5 c

m)

on t

he

org

anic

mat

ter

com

po

siti

on (B

PC

: b

iop

oly

mer

ic ca

rbo

n;

TO

C:

tota

l o

rgan

ic

carb

on;

CO

M:

co

mp

lex o

rganic

mat

ter;

TN

: to

tal

nit

rogen)

and

chlo

rop

hyll

a c

once

ntr

atio

ns.

Dat

a fr

om

19

99

was

no

t in

clud

ed (

N =

36

0).

Sig

nif

icance

lev

els:

*:

p <

0.0

5;

**:

p <

0.0

01

; ***:

p <

0.0

01

; ns:

p >

0.0

5.

†B

PC

(i.

e.,

the

sum

of

pro

tein

s, c

arb

oh

yd

rate

s an

d l

ipid

s);

CO

M (

i.e.

, th

e d

iffe

ren

ce b

etw

een T

OC

and

BP

C).

+lo

g t

ransf

orm

ed

dat

a


171

Figure 6. Temporal variations in total organic carbon (TOC), total nitrogen (TN),

complex organic matter (COM) and Chl a concentrations (µg g-1 sed d.w. ± standard

deviation) with tidal levels and sediment depths. (+Chl a data was log-transformed).

4.5.4. Discussion

4.5.4.1. Benthic macrofauna community.

Analysis of distribution of benthic macrofauna from the studied beach

demonstrated that the tidal levels sampled were characterised by distinct faunal

densities and species composition. Polychaetes and molluscs occurred mainly

at the intertidal level and crustaceans tended to occur higher on the shore as

they are less susceptible to desiccation. Abundance, biomass and number of

species were negatively related to sediment depth. Differences in depth


HTL

MTL

LTLLTL

Ja97 A97J97O97Ja98 A98J98 O98Ja99

Chl a+ (µg g-1 d-1 sed d.w.)

0,01

0,1

1

10

0,01

0,1

1

10

0,01

0,1

1

10

Ja97 A97J97O97Ja98 A98J98 O98Ja99

COM (µg g-1 sed d.w.)

0

2000

4000

6000

8000

10000

12000

14000

0

2000

4000

6000

8000

10000

12000

14000

0

2000

4000

6000

8000

10000

12000

14000

TOC (µg g-1 sed d.w.)

0

2000

4000

6000

8000

10000

12000

14000

0

2000

4000

6000

8000

10000

12000

14000

0

2000

4000

6000

8000

10000

12000

14000

Ja97 A97J97O97Ja98 A98J98 O98Ja99

TN (µg g-1 sed d.w.)

0

200

400

600

800

1000

1200

1400

0

200

400

600

800

1000

1200

1400

0

200

400

600

800

1000

1200

1400

Ja97 A97J97O97Ja98 A98J98O98Ja99


172

distribution of organisms could be related to differences in sediment

characteristics that conditioned organism’s ability to burrow. Variations in

mean grain size and compactness with sediment depth (higher M.G.S and S.S.)

and tidal level (lower M.G.S and higher S.S. at the MTL) could influence

macroinfauna distribution in the intertidal. Sediment characteristics, however,

were not able to explain macroinfauna variation alone. Several works have

noted that vertical zonation could be further controlled by the position of the

Redox Potential Discontinuity (RPD) layer since animals are dependent on

dissolved oxygen for their respiration (Rosenberg et al., 2003; Steyaert et al.,

2003). The RPD was found in the intertidal level at the 5-10 cm depth and

macroinfauna was mainly concentrated on the sand surface or subsurface

(~75%).

The intertidal levels on sheltered beaches are considered to be under

optimal environmental conditions in terms of humidity, temperature and food

supply for marine macroinfauna. These beaches are not as physically controlled

environments as exposed beaches and benthic macrofauna will be favoured by

accumulations of organic matter (Defeo et al., 2001; Incera et al., 2006; Rodil

et al., 2007). Maximum concentration of BPC; i.e., food available, was found at

the MTL. The presence of larger amounts of organic matter (macroalgae

coverage), higher biochemical concentrations and water content could promote

higher macroinfauna abundances and species richness at the MTL rather than at

the LTL.

Most of the species inhabiting the intertidal level belonged to the

deposit-feeder’s group, favoured by organic rich supply on the sediment

surface during winter and spring. Deposit-feeders are able to rapidly exploit

food resources and conspicuous abundance of this trophic group has been

related to a marked increase in proteins (Rossi et al., 2001). The occurrence of

suspension feeders was restricted to the lower intertidal level, probably because

they can only feed at high tide and they cannot exist where submergence is

brief (Dittman, 2000). Bivalves were scarce in April, probably due to the local

clam gathering activities during the previous months. The increase in mollusc

density and biomass in July could be explained by the obligatory close season


173

starting in April (see http://www.pescadegalicia.com). Clam and cockle

collection by hand is a common activity in this area which involves regular

sediment disturbance and also macroalgae removal. Some of the changes

presented over time in the macroinfauna community from Barraña could be an

echo of disturbance effects rather than of trophic responses.

Despite the constant dominance of few abundant species on this beach,

high variability of the community was observed throughout the study period.

Several works have suggested that further control of the structure and dynamics

of the macroinfauna community from the intertidal could be related to

fluctuations in the availability of food resources (e.g. Rossi et al., 2001).

4.5.4.2 Spatial and temporal changes in organic matter composition and

Chl a content.

The high concentrations of biochemical compounds recorded in the

sediment could be related to the specific characteristics of this beach; i.e.

sheltered conditions favour accumulation of organic matter in the intertidal

(Nordström, 1992, Cividanes et al., 2002).

From analysis of the biochemical composition of organic matter, the

BPC accounted for about 44% of TOC and proteins were the dominant fraction

of BPC (58%). A significant fraction of the BPC (42%) was presented as

material of a more refractory composition but the overall organic matter can be

considered of recent production. The PROT:CHO ratio, displayed high values

(5.2), indicating that protein availability should not be considered as a limiting

factor for benthic consumers (Fabiano et al., 1995). The rise in proteins meant

an increment in the quality of food available and the particularly high protein

values recorded in winter could be related to allochthonous inputs, reflecting

the characteristics of a eutrophic system (Danovaro, 1996).


174

Table 4. Summary of results from BIO-ENV. Combination of n environmental

variables, k variables at a time (1,2,3,…n), giving largest rank correlations (ρs) between

biotic and abiotic similarity matrices for each k. Bold indicates best combination

overall. MGS: Mean grain size; WC: water content; BPC: biopolymeric carbon; TOC:

total organic carbon; COM: complex organic matter; Chl a: chlorophyll a.

Barraña is located at the inner part of the ria where the deposit of

terrigenous and anthropogenic material was present along the intertidal level

(Cividanes et al., 2002). This could to some extent, be related to the seasonal

variability found in the organic matter availability. There was a decrease in the

PROT:CHO ratio in summer and at the beginning of autumn, probably because

of the lack of sea input, low river flux, high temperatures and solar radiation

which usually characterise this season. During this period of the study, less

amount of algal detritus (field observation) and high values of refractory

organic matter were found, suggesting scarce availability and low quality of

food resources. The progressive decomposition of this debris during summer

could cause a rapid depletion of the labile fraction and an accumulation of the

most refractory components such as carbohydrates and lipids (Danovaro et al.,

2002). This suggests the presence of aged organic matter with a largely detritic

origin caused by the algal-wrack decomposition. Carbohydrate concentrations

were higher in July and October, which could be related to the macroalgae

accumulation and consistent decomposition process; while, proteins displayed

higher values in winter and spring.

k Best variable combinations (ρs)

1 TOC

(0.475)

2 WC; TOC BPC; TOC

(0.487) (0.483)

3 WC; BPC; TOC WC; TOC; COM

(0.486) (0.477)

4 WC; BPC; TOC; COM WC; BPC; TOC; C:N

(0.487) (0.506)

5 MGS; prot:cho; TOC;COM;C:N WC; BPC; TOC; COM; C:N MGS; BPC; TOC; COM; Chl a

(0.514) (0.510) (0.473)


175

Inte

rcep

t M

GS

E

h

WC

B

PC

T

OC

C

OM

C

:N

Ch

loro

ph

yll

a

Abundan

ce

Est

imat

e 1.5

7

-0.0

01

-0

.001

0.0

5

0.4

5

0.4

7

-0.1

4

0.0

7

-0.0

01

S

tandar

d e

rror

0.5

4

0.0

01

0.0

00

0.0

2

0.1

2

0.0

6

0.0

6

0.0

1

0.0

4

W

ald s

tati

stic

8.6

1.2

24.9

7.1

2

15.1

66.8

6.1

5

159.4

1

0.0

01

AIB

+

Est

imat

e 4.0

4

-0.0

1

0.0

01

-0.0

5

-0.6

7

0.1

7

0.1

8

-0.0

2

0.4

8

S

tandar

d e

rror

0.8

9

0.0

01

0.0

00

0.0

3

0.2

0

0.0

9

0.0

8

0.0

1

0.0

5

W

ald s

tati

stic

20.5

6

37.4

2

2.5

5

2.6

0

11.0

1

3.4

6

4.7

2.4

3

81.5

Ab

ud

an

ce o

f m

ain

gro

up

s

Poly

chae

ta

Est

imat

e 0.8

1

-0.0

03

-0

.001

0.0

8

1.2

6

0.0

5

0.2

2

0.0

7

0.1

1

S

tandar

d e

rror

0.7

9

0.0

01

0.0

00

0.0

3

0.1

7

0.0

8

0.0

9

0.0

1

0.0

5

W

ald s

tati

stic

1.0

5

11.0

7

22.0

4

8.7

7

52.6

1

0.3

4

5.9

0

78.4

1

4.7

2

Moll

usc

a E

stim

ate

-7.8

1

0.0

05

-0

.001

0.3

1

-0.1

3

0.5

1

0.1

1

0.0

9

-0.3

2

S

tandar

d e

rror

1.0

8

0.0

01

0.0

00

0.0

4

0.1

7

0.0

8

0.0

8

0.0

11

0.0

7

W

ald s

tati

stic

52.0

4

20.9

7

1.3

1

65.1

0.6

2

39.1

2

1.5

7

64.5

19.4

Cru

stac

ea

Est

imat

e 19.4

-0

.01

-0

.02

-0.4

1

2.9

4

2.0

4

-3.6

7

0.1

1

0.0

9

S

tandar

d e

rror

2.0

3

0.0

02

0.0

02

0.0

7

1.2

3

0.3

8

0.4

7

0.0

2

0.1

2

W

ald s

tati

stic

91.2

29.6

3

108.3

36.3

5.6

27.9

61.3

27.1

0.5

7

T

ab

le 5

. S

um

mar

y o

f th

e gener

alis

ed l

inea

r m

od

els

(Po

isso

n d

istr

ibuti

on)

ind

icat

ing

var

iab

les

that

wer

e si

gnif

ican

t (i

n b

old

). M

.G.S

.: m

ean

gra

in s

ize;

Eh:

red

ox p

ote

nti

al;

W.C

.: w

ater

co

nte

nt;

BP

C:

bio

po

lym

eric

car

bo

n;

TO

C:

tota

l o

rgan

ic c

arb

on;

CO

M:

com

ple

x o

rganic

matt

er.

+T

he a

ver

age i

nd

ivid

ual

bio

mass

(A

IB)

in e

ach

sam

ple

was

calc

ula

ted

as

bio

mas

s d

ivid

ed b

y a

bund

ance

per

sp

ecie

s (m

g m

-2 d

ry w

eig

ht)

and

it

was

use

d a

s an e

stim

atio

n o

f th

e av

erag

e o

rgan

ism

siz

e


176

High TOC concentrations and low BPC:TOC ratio supported these

findings related to the carbohydrate increase during summer. Allochthonous

inputs are usual incidents during winter, due to weather conditions, which

promote accumulation of dead seaweed on the beach face and therefore

introduce new organic matter in the intertidal. Some benthic animals may

indeed benefit from drifting algal mats as a key resource; i.e food and/or

refuge, and its availability can affect diversity and abundance of intertidal

animals including shorebirds (e.g. Norkko and Bonsdorff, 1996; Colombini and

Chelazzi, 2003; Dugan et al., 2003; Kelaher and Levinton, 2003). Intermediate

amounts of drift algae increase the nutrient levels and it is under such

conditions that macrofauna are most likely to utilise the extra organic material

(Norkko and Bonsdorff, 1996; Nordström, et al., 2006). Although low BPC

concentrations were found at the HTL, the high BPC:TOC percentage at the

supratidal suggests an improvement of the organic matter quality which will

benefit macroinfauna dwelling at this level. These findings were also supported

by the low C:N ratio found which points to a high nutritive organic matter.

Chlorophyll a concentrations in the sediment are used as a proxy of the

amount of organic matter produced by benthic microalgae. Large fluctuations

in the concentration of Chl a were found in January, in line with the literature

which reported frequently peaks during winter and spring (e.g. Trueblood et al.,

1994; Rossi, 2002). The particularly high values of Chl a observed in January

1997 at the MTL are difficult to explain. High deposition of algal detritus and a

low decomposition rate over the winter period can create an ideal environment

for microbial productivity with a subsequent increase in photosynthetic activity

(Kelaher and Levinton, 2003). The following months were characterised by

high macroinfauna abundance and biomass when temperatures increase. The

increased availability of microbial biomass could further increase the

abundance and biomass of the macroinfauna such as deposit-feeding

invertebrates inhabiting the intertidal during that time. Overall mean values of

Chl a were low because of the low concentrations found at the supratidal level,

but data from the mid-low tidal levels (4.65±2.1 and 7.6±5.2 µg g-1 sed dw)


177

PCA Axis I

PC

A A

xis

II

-0.6 1.0

-0.4

0.6

Tidal level

Sed dept

MGS

Shear strength

Eh

T

Water contentprot

cho

lip

prot:cho

BPC

TOC

BPC:TOC

TN

C:N

Chl-a

implied a very important contribution of autochthonous primary production and

classified this beach as organic marine rich system (Fabiano et al., 2004).

Figure 7. Projection of the considered variables (i.e., environmental variables,

sedimentary organic matter and biochemical compounds and macroinfauna

characteristics) in the first plane of the PCA based on the measurements carried out

during the study period.( : average individual biomass;

: biomass; : number of species;

: mean abundance; : abundance of crustaceans;

: abundance of polychaetes; : abundance of

molluscs). The average individual biomass was calculated as biomass divided by

abundance per species and it was used as an estimation of the average organism size

4.5.4.3. Relationships between environmental variables and benthic

macrofauna.

This study showed the importance of food availability in a benthic

macrofauna community that relied on seasonal deposition of sedimentary

organic matter at the intertidal. Food quality and quantity have the potential to

cause substantial spatio-temporal variation in the structure of macrofauna


178

assemblages in estuarine beaches. This conclusion is supported by PCA and

multiple regression analysis which indicated that biochemical compounds and

Chl a were the main factors explaining benthic macrofauna distribution in the

intertidal level. Macroinfauna characteristics and abiotic factors such as organic

matter and Chl a, were always found to be higher at the intertidal level, where

swash action occurs, than at the supratidal. The swash zone has been

considered a key area controlling macroinfauna from the intertidal and the

importance of the swash climate on the macrofaunal assemblages and on the

food available present in sediments of sandy beaches has been recently stated

(Incera et al., 2006). Although it was shown that inputs of microalgae biomass

can occur in winter and contribute to increase the nutritional value of the

sediment, a general pattern of increasing resources of food in winter and/or in

spring and decreasing in summer and autumn is not possible to refer to here.

We can elucidate that there was an increase in quality of the food available in

winter due to the higher protein concentrations meaning that the organic matter

was recently produced at that time. However, in summer and late summer there

was an accumulation of aged organic matter.

Multiple regression analysis were in line with the PCA and BIO-ENV

results and a positive correlation between sedimentary organics and

macroinfauna characteristics, such as biomass, macrofauna abundance and

abundance of polychaetes and crustaceans, was found. These analyses showed

the existence of tight relationships between macroinfauna and food quality but

the distributions of factors such as pigment and nutrients are often depth

dependent. Therefore, caution is called for when correlating depth profiles of

different variables. There is a positive relationship between BPC and

macroinfauna, but GLM showed some lack of fit between biochemical

compounds and quantitative characteristics of macroinfauna. This could be

related to the concentrations of carbohydrates (14%) and to the lipids (28%)

which are compounds with a more refractory composition than proteins.

The conclusions from this study should be treated as predictions that

point to the most important experimental manipulation to be conducted next.

This study showed that macrofauna from estuarine sheltered beaches is not just


179

driven by physical forces (e.g. level of dryness, wave action) but also by the

distribution of its primary food sources. Macrofauna organisms showed

preferences both in vertical and horizontal ranges suggesting a specific

distribution which is related to specific sensitivity by several abiotic factors,

including food availability. In relation to this, the assessment of vertical and

horizontal variability and the relative structure of the macroinfauna community

displayed a strong heterogeneity over time, suggesting that macrofauna in

estuarine beaches can be related to complex and unpredictable factors.

Acknowledgements

The authors thank the “Benthos Team” from the University of Vigo for

their assistance during sampling. We are grateful to three anonymous

reviewers, whose critical and constructive comments strengthened this paper.

This research was supported by the Regional Government of Galicia

(PGIDIT02RMA30101PR) and the University of Vigo (C505 122F 64102). I.F.

Rodil was supported by a Ph.D. grant from the Xunta de Galicia (programa

María Barbeito).

4.5.5. References.

Bligh, E.G. and Dyer, W. 1959. A rapid method for total lipid extraction and

purification. Canadian Journal of Biochemistry and Physiology 37,

911-917.

Cividanes, S., Incera, M. and López, J. 2002. Temporal variability in the

biochemical composition of sedimentary organic matter in an intertidal

flat of the Galician coast (NW Spain). Oceanologica Acta. 25: 1-12.

Clarke, K.R., 1993. Non-parametric multivariate analyses of changes in

community structure. Australian Journal of Ecology. 18: 117-143.

Colombini, I. and Chelazzi, L. 2003. Influence of marine allochthonous input

on sandy beach communities. Oceanography and Marine Biology:

Annual Review. 41: 115-159.

Danovaro, R. 1996. Detritus-Bacteria-Meiofauna interactions in a seagrass bed

(Posidonia oceanica) of the NW Mediterranean. Marine Biology 127:

1-13.

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Limnology and Oceanography 39: 1440-1454.

Chapter 6. Differential effects of native and invasive algal

wrack on macrofaunal assemblages inhabiting exposed

sandy beaches.

Chapter 6 Effect of native and invasive algal wrack

183

Abstract

Many sandy beaches worldwide receive large amounts of drift seaweed,

known as wrack, from offshore algal beds and closer rocky intertidal shores.

Despite the important influence of algal wrack on macrofaunal assemblages from

different coastal systems, relatively little attention has been paid to the

macrofaunal responses in sandy beaches to macrophyte wrack supplies. Algal

wrack is a key resource, i.e. for food and/or refuge, for beach invertebrates while

its availability can affect diversity and abundance of intertidal animals including

shorebirds, but the role of certain types of wrack and its location on the shore has

not been examined experimentally to date. In this paper, we use experimental

manipulation of two species of brown seaweeds, i.e. artificial wrack patches made

up of the native macroalgae Saccorhiza polyschides (Lightfoot) Batters and the

invasive species Sargassum muticum (Yendo) Fensholt, to test hypotheses about

influences on macrofaunal assemblages inhabiting the drift line and supratidal

levels of exposed beaches. Results pointed out that different types of wrack

deposits were not used uniformly by invertebrates. Nutritional value differed

between the two species of wrack. In most cases, the carbohydrates, lipids and

organic carbon content were greater in patches of S. muticum than in patches of S.

polyschides. Data also provided evidences that nutritional content and

microclimatic conditions of wrack deposits, i.e. temperature and humidity,

affected macrofaunal assemblages.

Keywords: invasive species; experimental manipulation; macrofaunal

assemblages; macroalgal wrack; sandy beaches.

4.6.1. Introduction

Many sandy beaches worldwide receive large amounts of drift seaweed

from offshore algal beds and closer rocky intertidal shores (Inglis, 1989; Rossi

and Underwood, 2002; Dugan et al., 2003). Macrofauna inhabiting exposed

sandy beaches is basically dependant on phytoplankton and marine

macrophytes inputs because of the scant primary production occurrence on this


184

habitat itself (Inglis, 1989; Dugan et al., 2003; McLachlan and Brown, 2006).

The importance of beach accumulations of wrack on the ecology of sandy

beaches has been previously documented in the literature (see Colombini and

Chelazzi, 2003 and references therein). Algal wrack deposits represent the

main food resource for upper shore detritus feeders such as talitrid amphipods,

tylid and oniscoid isopods besides tenebrionid and staphylinid beetles

(Colombini et al., 2000; Dugan et al., 2003). Wrack also acts as a refuge for the

supralittoral fauna, mainly terrestrial and semiterrestrial arthropods, providing

an opportunity to study seaweed debris both as a food resource and shelter

habitat (Inglis, 1989; Colombini et al., 2000; Jędrzejczak, 2002a, b; Olabarria

et al., 2007).

Despite the important influence of algal wrack on macrofaunal

assemblages from different coastal systems, relatively little attention has been

paid to the macrofaunal responses in sandy beaches to macrophyte wrack

supplies (see Olabarria et al., 2007). Algal wrack is a key resource for beach

invertebrates and its availability can affect diversity and abundance of intertidal

fauna including shorebirds (Dugan et al., 2003; McLachlan and Brown, 2006),

but the role of type of wrack and its location on the shore has not been

examined experimentally so far. On sandy beaches, wrack is deposited

throughout the entire intertidal range creating a patchy scenario of bare and

wrack occupied areas (Valiela and Reitsma, 1995; Colombini et al., 2000;

Rossi and Underwood, 2002). Sandy beaches are by no means homogeneous

habitats. Not only they reflect macroinvertebrate patchiness, but also reflect

important changes in structure and biodiversity of assemblages along their

slope (see McLachlan and Jaramillo, 1995). The spatial distribution of wrack

debris along the beach profile should be a very important factor since the

higher the seaweed is located on the beach the longer it is presumably present

on the intertidal zone. Close to the swash zone, in the lower part of the

intertidal, mats of wrack are mainly driven by the physical forces of waves,

tides and sediment movement during the entire period of stranding. Wrack

deposits at the supratidal undergo dehydration, ageing and finally become

covered by wind-blown sand. After a period of decomposition and decay,


185

wrack will release nutrients, particularly N and P, which can enhance benthic

microalgae and stimulate growth of aerobic and anaerobic bacteria. Processes

are complex and depend on the amount and taxonomic composition of wrack

(Rossi and Underwood, 2002; Jędrzejczak, 2002a). For example, different

seaweeds may vary in physical structure (levels of branching, toughness),

nutritional values and decomposition rates which could potentially influence

wrack-associated macrofauna. Different physical structures of seaweeds may

also modify microclimatic conditions, i.e. temperature and humidity of wrack

deposits. Therefore, different types of wrack might influence the structure and

function of animal assemblages and determine taxonomic composition, number

and turnover of species. In fact, several studies indicate that population

densities, behaviour and feeding rates of invertebrates on sandy beaches are

likely affected by the type of macroalgal wrack arriving to the intertidal (e.g.

Valiela and Rietsma, 1995; Colombini et al., 2000; Pennings et al., 2000;

Goecker and Kåll, 2003).

Accumulations of dead seaweed on the beach face are a ubiquitous

feature of Galician sandy beaches (NW Spain), where heaps of macroalgae

frequently stranded, mainly consisting of brown macrophytes such as

Saccorhiza polyschides, Sargassum muticum, Fucus spp., and Laminaria

saccharina (Olabarria et al., 2007). The amount and type of stranded material

also vary at different spatio-temporal scales. In summer, for example,

considerable amounts of S. polyschides and S. muticum are stranded on beaches

creating a mosaic of bare and wrack affected areas (pers. obs.). In this context,

it would be interesting to take heed of the effect of both species on the

macrofaunal assemblages inhabiting exposed sandy beaches. Another

important point to consider is the origin of both species, since S. polyschides is

a native seaweed species, whereas S. muticum is an invasive species. This

species is native to SE Asia, but its actual distribution as invasive algae is

spanned all through the world, including Europe, the Mediterranean Sea and

the west coast of North America (Britton-Simmons, 2004). This seaweed has

been first reported in Spain in 1985 (Casares et al., 1987) invading rapidly the

highly productive rocky shores or macroalgae beds. It was first observed on the


186

Galician coast in 1986 (see Pérez-Cirera et al. 1989) and has successfully

colonised most of the Galician estuaries increasing its abundance rapidly. The

rapid spread of S. muticum might have important effects on the composition,

structure and organization of local assemblages on rocky shores and sandy

beaches (via stranded seaweed). In fact, exotic species have been reported to

have strong impacts on local ecosystems, changing species diversity, trophic

structure and dynamics of populations, negatively affecting ecosystem

processes (Carlton, 1996). So far, no studies have compared the effects of types

of stranded seaweed (native versus exotic species) on macrofaunal assemblages

dwelling on exposed sandy beaches.

In this paper, we used experimental manipulation of two types of

brown seaweeds, i.e. artificial wrack patches comprising the native macroalgae

S. polyschides and the invasive species S. muticum, to test hypotheses about

influences on macrofaunal assemblages inhabiting the drift line and supratidal

zone (i.e. dune) at two different sites along an exposed sandy beach. In

particular, we test the hypothesis that (1) the microclimatic conditions, i.e.

temperature and humidity, vary between both types of wrack, (2) the nutritional

content of the two types of wrack is different, (3) abundance of colonizing

individual and species differ in the two types of wrack, (4) succession varies

between wrack types, and (5) as a result, macrofaunal assemblages are different

in each type of wrack. Furthermore, we predicted that responses in wrack

patches located at the drift line would differ from the patches located at the

supratidal because wrack patches placed at this level remain longer on the

beach. Finally, we predicted that responses could differ among sites because of

their slightly different environmental conditions.

4.6.2. Methods

4.6.2.1. Study area

The study site of Ladeira (42º 34’ 33’’N; 9º 3’ 16’’ W) is an

intermediate exposed sandy beach about 1400 m long and 130 m wide (low

spring tide), sheltered by a large and active dune system, located in the


187

Corrubedo beach-lagoon complex. This beach is influenced by a mesotidal

regime with a medium tidal range of 3 m.

Two sites about 500 m apart were chosen for this experiment (Site A

and Site B, hereafter). Site A was located at the northern part of the beach,

while site B was located at the southern part. The environmental characteristics

of the two sites differed slightly in terms of the slope, granulometry,

temperature and wind exposure. The slopes varied between 1/27 (Site A) and

1/24 (Site B). Sand was mainly made of fine fraction ranging from 251.2±24.8

(Site B, Drift) to 182.4±1.34 µm (Site A, Drift) and sediments were well sorted

varying between 1.34±0.07 and 1.56± 0.02 φ at Sites A and B respectively.

Temperature in the sediment underneath wrack patches ranged from 30.6±0.47

(Site A, Dune) to 31.6±0.94 ºC (Site B, Dune), whereas temperature in bare

sediment ranged from 29.7±0.94 (Site A, Dune) to 30.1±0.73 ºC (Site B,

Dune). The predominant wind was from northerly (F3,3= 12.26; P< 0.05) being

more intense at Site A (F1,64= 8.71; P< 0.01; SNK tests, P< 0.05).

4.6.2.2. Experimental design

The experiment started on 13 June 2006 and lasted for 21 days.

Manipulative experiment was performed at Sites A and B. The day before

starting the experiment, 250 kg of fresh seaweeds, S. polyschides and S.

muticum, were collected by hand from surrounding rocky intertidal areas, taken

to the laboratory, weighed and separated in plastic bags of 2.5 kg ±0.50 g. At

the field, medium squared-patches (0.25 m2; 2.5 kg ±0.50 g wet weight) of the

two types of seaweed (twelve patches of each type) were haphazardly placed

on the highest mark of the drift line and on the base of the dune parallel to the

shoreline, i.e. 24 patches per tidal level (N= 48 per site). Each patch was placed

1 to 2 metres apart and its location on the beach determined by calculating a

random distribution on the computer.

On days 3, 7, 12 and 21 of the experiment, three randomly chosen

replicate patches of each type of wrack were collected at each site from the

dune and also from the drift line. The associated fauna was retained by

enclosing each patch within a 50 x 50 sieve of 1 mm mesh size. Then


188

insecticide was sprayed to prevent mobile fauna, such as adult dipterans and

coleopterans, from escaping, and after 5 minutes, the seaweed and any visible

fauna transferred to a plastic bag. Macrofauna underneath each wrack patch

was also collected with a 10 cm diameter stainless-steel corer penetrating 20

cm depth into the substratum (n = 3). Samples were taken from the centre of

the patches to avoid possible edge effects. Three control replicates (3 cores per

replicate), 50 cm apart from the wrack patches and separated by 1 m, were also

taken at each site in order to measure the normal abundance of invertebrates in

nearby bare sediment.

Subsamples of wrack (± 5 g) for biochemical composition analysis

were collected (n=3) at each time and frozen at -30ºC until further processing.

In addition, temperature (˚C) was measured inside the wrack patches (n=3).

Four aeolian sediment traps were buried vertically with their rims flush with

the beach surface in the dune of both sites surrounding the wrack patches. An

inlet and an outlet tube, connected to the chamber trap, were exposed and

orientated to the main wind directions. These devices were designed as

sediment collectors in order to assess the intensity of aeolian processes and to

measure horizontal sediment transport by wind (Goossens and Offer, 2000).

The amount of sand collected on sampling days was measured as relative total

grain mass (g day-1) and the predominant wind direction was established.

During the whole experiment none of the sediment traps were found totally

filled up by wind action.

4.6.2.3. Laboratory analysis

Sediment samples (n=3) from underneath wrack patches were weighed

and then oven-dried at 60ºC until a constant weight was obtained. Sediment

water content; i.e. humidity, was estimated as the difference between wet and

dry weight.

Wrack patches were collected, washed and sieved through a 1 mm

mesh. The retained macrofauna was sorted and identified to the lowest possible

taxonomic level. The total organic matter of wrack was measured as the

difference of dried seaweed (60ºC to a constant weight) before and after


189

ignition in a muffle furnace at 500 ˚C for 4 hours. Estimating total organic

matter content in wrack does not provide a good indication of the portion

available for consumers. Therefore, the nutritional value of the wrack during

the decay process was done through the determination of the main biochemical

classes of organic compounds (i.e. carbohydrates, proteins and lipids) which

are assumed to estimate the food potentially available for consumers, either

bacteria (Fichez, 1991; Fabiano et al., 1995; Dell’Anno et al., 2000) or higher

trophic levels (Dugan et al., 2003). For all analyses, about 0.15-0.2 g of

seaweed frond subsamples were used for each analysis (data normalized to

seaweed dry weight). All biochemical analyses were conducted on samples

previously oven dried at 60 ºC until constant weight was achieved and finely

powdered with a pestle. Total lipids (Bligh and Dyer, 1959; Marsh and

Weinstein, 1966), carbohydrates (Dubois et al., 1956) and proteins (Markwell

et al., 1978) were analysed and measured as μgg-1. The sum of the main

biochemical classes was reported as the biopolymeric carbon (BPC sensu

Fichez, 1991) assumed as a reliable estimate of the labile fraction available to

benthic consumers. Analyses of dry weight samples (n=3) of Chlorophyll a

(Chl a, μg g-1) from seaweed fronds were extracted following Lorenzen (1967).

Chl a can be used as a surrogate of benthic microalgae biomass (Rossi and

Underwood, 2002).


Changes in number of individuals, number of species, abundance of

main representative species and diversity (Shannon-Weaver index) were

analysed using a 4-factor orthogonal analysis of variance. Moreover, changes

in the content of organic matter, carbohydrates, lipids, proteins and chlorophyll

a in the wrack were also analysed following the same model. Type of wrack (2

levels), Height on the shore (2 levels), Time (4 levels) were fixed factors and

Site (2 levels) was random. Any interaction that was sufficiently small with a

probability ≥0.25 was pooled. Before analysis, the homogeneity of variances

was evaluated with Cochran’s test (Winer et al., 1991) and data were


190

transformed when necessary. A posteriori multiple comparisons were done

using Student-Newman-Keul’s (SNK) tests (α= 0.05).

Four factor orthogonal non-parametric multivariate analyses of

variance (PERMANOVA) were used to test the hypothesis about differences

among wrack-associated macrofaunal assemblages (Anderson, 2001). Only

significant effects (p<0.05) were further investigated through a series of pair-

wise comparisons using the appropriate terms in the model. This statistical

method was used because experiment designs were relatively complex

(involving four factors) and because, similar to most other studies on

assemblages, the data did not meet the assumptions of traditional multivariate

statistical analyses (e.g., MANOVA). This method improves on previous ones

because it allows the direct additive partitioning of variation, which enables

tests of multivariate interactions in complex experimental designs. The statistic

test (pseudo-F) is calculated from a symmetric dissimilarity matrix. P-values

are then obtained by permutation tests. Here, the P-values for each term in the

model were generated using 5,000 permutations. To graphically visualize

multivariate patterns in assemblages, non-metric multidimensional scaling

(nMDS) was used to produce two-dimensional ordination plots. Species that

mostly contributed to the dissimilarity/similarity among the two types of wrack

were identified using SIMPER analysis (Clarke, 1993). The BIO-ENV analysis

(PRIMER) was used as an exploratory tool to define suites of abiotic variables

that best determine the macrofaunal assemblages. For that purpose, biotic and

abiotic matrices were constructed using Bray-Curtis dissimilarity (square-root

transformed) and Euclidean distances, respectively.

To compare the relationships between presence/absence of main taxa,

total number of individuals, total number of species, diversity and abiotic

variables, two types of regression models were used. Firstly, we used the

logistic regression model, which falls within the general framework of GLMs

(McCullagh and Nelder, 1989), to analyse the relationship between a binary

response variable (presence/absence) and several explanatory variables (abiotic

predictors). All variables were simultaneously used in a forward multiple

logistic-regression analysis to derive a multivariate model that would predict


191

the presence or absence of main taxa. The odds of an event occurring (i.e. the

probability an event occurs relative to its converse) were calculated in order to

know if there was a relationship between the presence of the species and each

of the predictor variables. Secondly, we used a GLM with a Poisson error term

and a log link function, known as a log-linear model, which can be used

effectively when the predictors are continuous and the response variable is a

count (Quinn and Keough, 2002). This model is more flexible and better suited

for analyzing ecological relationships that can be poorly represented by

classical Gaussian distributions (Guisan et al., 2002 and references therein).

The significance of the independent variables was tested using the χ2-test

(P<0.05) on the Wald statistic (Statistica 6.0).

Source Humidity Temperaturea,b

df MS F MS F

Wrack (W) 1 1027.75 84.81 0.0092 49.33

Site (S) 1 0.938 1.08 0.0701 54.86***

Height (H) 1 1.281 0.29 0.0013 0.77

Time (T) 3 3.61 0.95 0.0429 0.86

W X S 1 12.119 14.01*** 0.0002 0.15

W X H 1 1.629 0.40 0.0006 19.70

W X T 3 2.491 4.85 0.0297 14.40*

S X H 1 4.459 5.16* 0.0017 1.31

S X T 3 3.795 4.39*** 0.0500 39.14***

H X T 3 0.284 0.22 0.0000 0.00

W X S X H 1 4.046 4.68* 0.0000 0.02

W X S X T 3 0.513 0.59 0.0021 1.61

W X H X T 3 0.393 1.49 0.0154 2.77

S X H X T 3 1.322 1.53 0.0016 1.26

W X S X H X T 3 0.264 0.31 0.0055 4.33**

Residual 64 0.864 0.0013

*p<0.05

**p<0.01

***p<0.001 a ln (x+1) tranformed data bsignificant differences with control data (bare sediment)

Table 1. Summary of analyses of variance for Temperature (ºC) and Humidity (%) in

wrack patches at the different sites and heights on the shore.


192

4.6.3. Results

4.6.3.1. Microclimatic conditions of wrack patches: humidity and

temperature

Humidity varied between wrack patches, but the variation was not

consistent across heights on the shore and sites (i.e. a significant Wrack x Site x

Height interaction, P< 0.05; Table 1). Humidity was higher in patches of S.

polyschides than S. muticum, but only in the dune at Site A (SNK tests, P<

0.05). Temperature measured inside the patches differed between wrack types,

but, once again, differences were not consistent over space and time (i.e.

significant Wrack x Site x Height x Time interactions; Table 1). For example,

at site A, temperature in patches of S. polyschides was higher than in patches of

S. muticum, but only in the dune on day 12 and in the drift line on day 3 (SNK

tests, P< 0.05). At site B, temperature in patches of S. polyschides was higher

than in patches of S. muticum in the drift line on days 3 and 12 and in the dune

on day 12 at Site B.

4.6.3.2. Analysis of the total organic matter and nutritional value

Total organic matter varied significantly among wrack types (Table 2),

but this variation was not consistent between sites and heights on the shore (i.e.

a significant Wrack x Site x Height interaction, P<0.05). The total organic

matter was greater in patches of S. muticum than in S. polyschides at all sites

and heights on the shore (Figs. 1a, b, c, d). However, there was more organic

content in patches of S. muticum in the dune at Site A than at Site B (Fig. 1a, b;

SNK tests, P< 0.05). In contrast, patches of S. polyschides in the dune had more

organic content at site B than at Site A. (Fig. 1a, b; SNK tests, P< 0.05).


193

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2

0.0

1

0.2

5

2509

.11

0.1

0

706.3

3

0.4

W X

H

1

3521

.3

1.3

5411

6.7

6.0

1

0.0

8

2.2

7

0.1

8

4.4

5

1174

52.3

0.7

4

2285

.4

21.9

4

W X

T

3

469.5

0.7

2

1495

1.1

0.9

9

0.3

1

29.1

1*

0.1

1

13.7

2*

9545

17.5

25.9

3*

2837

3.6

81.1

**

S X

H

1

1361

.3

4.1

6597

6.9

12.2

***

0.0

01

0.0

9

0.0

4

1.8

4

1749

17.1

5

7.2

**

3690

.24

1.9

6

S X

T

3

168.0

4

0.5

1832

2.7

3.4

*

0.0

1

0.5

4

0.0

6

2.6

5+

7441

4.5

3.0

4*

797.5

8

0.4

2

H X

T

3

70.1

1.9

4999

.72

0.1

1

0.0

5

9.0

1+

0.2

9

8.1

+

2911

6.9

0.2

4

1386

.94

0.1

7

W X

S X

H

1

2702

.7

8.1

**

9003

.56

1.7

0.0

4

3.4

0.0

4

1.7

1587

40.7

6.5

*

104.2

0.0

6

W X

S X

T

3

652.6

1.9

5

1507

0.1

2.8

+

0.0

1

0.9

4

0.0

1

0.3

2

3681

4.2

1.5

1

349.8

0.2

W X

H X

T

3

373.6

1.7

1377

.7

0.7

0.0

1

0.5

0

0.0

14

0.6

5584

.2

0.1

5

1633

.9

0.5

S X

H X

T

3

35.2

0.1

1

4398

1.9

8.1

***

0.0

1

0.5

1

0.0

4

1.5

2

1204

42.3

4.9

3**

8364

.8

4.4

5**

W X

S X

H X

T

3

220.9

0.7

1955

.6

0.4

0.0

1

0.9

3

0.0

25

1.1

3670

6.2

1.5

3322

.82

1.7

Resid

ual

64

334.2

5

5427

.9

0.0

1

0.0

24

2444

4.8

1879

.11

+m

arg

ina

lly s

ign

ific

ant

(0.0

4<

p<

0.0

5);

*p

<0

.05

;**p

<0.0

1;*

**p

<0

.00

1; a

ln (

x+1

) tr

an

sfo

rmed

da

ta; b

sig

nific

ant

diffe

ren

ces w

ith

con

tro

l

Ta

ble

2.

Sum

mar

y o

f anal

yse

s o

f var

iance

fo

r th

e o

rganic

mat

ter,

pro

tein

s, c

arb

ohyd

rate

s,li

pid

s, b

iop

oly

mer

ic c

arb

on (

BP

C)

and

Chlo

rop

hyll

a

(C

hl

a) i

n w

rack p

atch

es.

Typ

e o

f w

rack (

W),

Hei

ght

on t

he

sho

re (

H),

Tim

e (T

) ar

e fi

xed

fac

tors

and

Sit

e (S

) is

a r

and

om


194

.

Figure 1. Mean (±SE; n=3) amount of organic matter (g), in wrack patches

across heights on the shore (Dune and drift levels), sites (A and B) and over

time. Points show an exponential decay model for the two types of wrack: [S.

polyschides: a) y = 197.1e -0.021x R2 = 0.51; b) y = 219.3e -0.026 R2 = 0.77; c) y =

198.5e -0.019x R2 = 0.48; d) y = 216.5e -0.022x R2 = 0.73) and S. muticum: a) y =

378e -0.008x R2 = 0.47; b) y = 354.5e -0.015x R2 = 0.5; c) y = 361.8e -0.014x R2 =

0.53; d) y = 348.9 e -0.013x R2 = 0.4)]. : S. polyschides dune level; : S.

muticum dune level; S. polyschides drift level; S. muticum drift level.

Site A

0 3 6 9 12 15 18 21 24

Org

an

ic m

att

er (

g)

0

100

200

300

400

500

Site B

0 3 6 9 12 15 18 21 24

0

100

200

300

400

500

Time (days)

0 3 6 9 12 15 18 21 24

Org

an

ic m

att

er (

g)

0

100

200

300

400

500

0 3 6 9 12 15 18 21 24

0

100

200

300

400

500

Time (days)

(a)

(c)

(b)

(d)


195

Nutritional value, i.e. proteins, carbohydrates and lipids, varied

significantly between wrack types, but patterns differed (illustrated by

biopolymeric carbon concentration in Fig.2; Table 2). Protein concentrations

(μg. g-1) were found significantly greater in patches of S. muticum than in S.

polyschides, but this pattern was not consistent across sites and over time (i.e. a

significant Wrack x Site x Time interaction, P<0.05). For example, protein

concentrations were greater in patches of S. polyschides than in S. muticum at

Site B on day 3. Although lipids and carbohydrates tended to be more abundant

in patches of S. muticum than in patches of S. polyschides, this trend was not

consistent over time (i.e. Wrack x Time interaction, P<0.05). Lipids showed

this pattern on days 3, 7 and 21, whereas carbohydrates followed this pattern on

days 12 and 21. The nutritional composition of wrack measured as

biopolymeric carbon concentration (BPC), varied among wrack patches

although this pattern was not consistent over space (i.e. Wrack x Site x Height

interaction, P< 0.05) nor over time (i.e. Wrack x Time interaction, P< 0.05)

(Fig. 2a). There was more BPC in patches of S. muticum than in patches of S.

polyschides, but this trend varied between heights on the shore and sites. For

example, there was more BPC in patches of S. muticum in the dune than in the

drift line at Site A (SNK tests, P< 0.05). Moreover, BPC in patches of S.

muticum was more abundant than in patches of S. polyschides, but only on days

3 and 7 (SNK tests, P< 0.05).

Chorophyll a concentration varied significantly among wrack patches,

but this variation was not consistent over time (i.e. a significant interaction

Wrack x Time interaction, P< 0.01; Table 2). Chlorophyll a was in greater

concentration in patches of S .polyschides than in patches of S. muticum on

days 3, 7 and 12 (SNK tests, P< 0.05 illustrated in Fig 2b by wrack patches

located in the dune).


196

Fig

ure

2.

Mea

n (

±S

E;

n =

3)

am

ou

nt

of

a) B

iop

oly

mer

ic c

arb

on a

cro

ss s

ites

(A

and

B)

and

hei

ghts

on t

he

sho

re (

Dun

e an

d d

rift

lev

els

) and

b)

Chlo

rop

hyll

a c

once

ntr

atio

ns

in

the

du

ne

level

at

th

e tw

o

site

s o

ver

ti

me.

D

iffe

ren

t le

tter

s re

pre

sent

sig

nif

ican

t

dif

fere

nce

s and

sa

me

lett

ers

rep

rese

nt

no

si

gnif

icant

dif

fere

nce

s.

S

. po

lysc

hid

es

dune;

S

. p

oly

sch

ides

dri

ft;

S. m

uti

cum

dune;

S

. m

uti

cum

dri

ft.


197

4.6.3.3. Macrofauna abundance, number of species and diversity

Analyses of macrofauna data were based in pooled data, i.e. individuals

in wrack patches and underneath the wrack patches. This decision was made

because (1) there was a very small number of individuals and species in bare

sediment, i.e. controls, (2% of the total number of individuals) and (2)

individuals found in bare sediment and underneath the wrack patches belonged

to the same species that colonised wrack.

A total number of 7,820 individuals belonging to 29 species were

collected in wrack patches (Table 3). Larval stages of different species

accounted for 66% of total number of individuals. Two coleopteran species, the

tenebrionid Phaleria cadaverina and the histerid Hipocacculus rubripes, and

two dipteran species from the family Anthomyiidae in larvae stage accounted

for 90% of the total abundance. The arachnid Arctosa variana and three species

of coleopteran Cercyon littoralis, Hipocaccus dimidiatus maritimus and Cafius

xantholoma accounted for ~ 4% of the total abundance.

Colonisation of all wrack patches was very rapid. Most species

colonised patches within 3 days (25 species) and only a few new species

colonised by day 7 (2 species), 12 (1 species) and 21 (1 species). Abundances

varied significantly between both types of wrack, but this variation was not

consistent between heights on the shore over time (i.e. a significant Wrack x

Height x Time interaction, P<0.05; Table 4). Abundances in patches of S.

polyschides were larger than in patches of S. muticum in the dune on days 3, 7

and 12 and in the drift line on days 3 and 7 (showed in Fig. 3a; SNK tests, P<

0.05). Abundance of larvae was significantly larger in patches of S. polyschides

on day 3 (Fig. 3b; Table 4), whereas the number of larvae in patches of S.

muticum did not vary over time (SNK tests, P> 0.05). Number of species and

diversity varied between wrack types, but this pattern was not consistent over

time (i.e. significant Wrack x Time interactions; Table 3). The number of

species was larger in patches of S. muticum on day 3, whereas it was larger in

S.polyschides than S.muticum on days 7 and 12 (Fig. 3c). Diversity followed


198

the same trend as the number of species except for day 21 when diversity

varied significantly between wrack types (Fig. 3d).

species S. polyschides S. muticum

Bare

sediment

Phylum Annelida

Cl. Oligochaeta

Enchytraeidae

sp1 1(0.02) 1 (0.06)

Phylum Arthropoda

Supercl. Chelicerata

Ord. Aranei

Lycosidae

Arctosa varinana (C.L. Koch, 1848) 59 (0.95) 5 (0.32) 2 (1.56)

Thomisidae

Xysticus sp. (C.L. Koch, 1835) 1(0.02)

Supercl. Crustacea

Ord. Amphipoda

Talitridae

Talorchestia deshayesii (Audouin,

1826) 36 (0.58) 33 (2.1)

Ord. Isopoda

Tylidae 2 (0.13)

Tylos europaeus (Arcangeli, 1938) 2 (0.03) 1 (0.78)

Cirolanidae Dana, 1852

Eurydice affinis (Hansen, 1905) 5 (0.08) 5 (0.32)

Supercl. Insecta

Ord. Coleoptera

Hydrophilidae

Cercyon littoralis (Gyllenhal, 1808) 107 (1.72) 82 (5.2) 13 (10.2)

Histeridae

Hypocacculus rubripes (Erichson,

1834) 466 (7.47) 251 (15.9) 5 (3.91)

Hypocaccus dimidiatus maritimus

(Stephens, 1830) 162 (2.6) 13 (0.82) 3 (2.34)

Staphylinidae

Aleochara (Emplenota) grisea

(Kraatz, 1856) 2 (0.03)

Cafius (Cafius) xantholoma

(Gravenhorst, 1806) 116 (1.86) 101 (6.4) 2 (1.56)

Phytosus (Phytosus) spinifer (Curtis,

1838) 3 (0.05) 2 (0.13)

sp1 4 (0.06) 4 (0.25)

Tenebrionidae

Phaleria cadaverina (Fabricius, 1792) 2062 (33.05) 990 (62.7) 86 (67.2)

Phylan gibbus (Fabricius, 1775) 5 (0.08) 5 (0.32)

Ord. Diptera

Subord. Nematocera


199

Infraord. Muscomorpha

sp1 8 (0.13) 4 (0.25)

sp2 3(0.05)

Empididae

sp1 18 (0.29) 9 (0.57) 2 (1.56)

sp2 6 (0.38)

Drosophilidae

sp1 2 (0.03)

Infraord. Calyptratae

Anthomyiidae

sp1 3009 (48.23) 11 (0.7) 1 (0.78)

sp2 99 (1.55) 2 (0.13) 9 (7.03)

Muscidae

sp1 23 (0.37) 20 (1.27)

sp2 2 (0.03) 2 (0.139

Infraord. Tabanomorpha

Fam Tabanidae

sp1 29 (0.46) 20 (1.27) 4 (3.13)

Infraord. Bibionomorpha

Bibionidae

sp1 1 (0.02)

Infraord. Tipulomorpha

Limoniidae

sp1 15 (0.24) 8 (0.51)

Ord. Neuroptera

Myrmeleonidae

Myrmelon (Myrmeleon) formicarius

(Linnaeus, 1767) 4 (0.06) 2 (0.13)

Ord. Orthoptera

Fam. Acrididae

sp1 1(0.02)

Ord. Trichoptera

sp1 1 (0.02) 1 (0.06)

Table 3. Total number and percent composition (in brackets) of macroinvertebrates in

wrack patches.

4.6.3.4. Analysis of variance of selected species: Patterns of colonisation

and succession

Colonisation patterns in the most abundant species varied between

heights on the shore levels, sites and over time. Those species that mostly

contribute to the dissimilarity between wrack patches over time were identified

and analysed separately (Fig. 4). Anthomyiidae sp1 was the most abundant

species (3009 individuals, 48% of the total abundance). This species was more

abundant in patches of S. polyschides contributing with the highest dissimilarity


200

among wrack types (17.33%), but this pattern was not consistent over time (i.e.

a significant Wrack x Time interaction, P<0.05; Table 5). This species was

more abundant in patches of S. polyschides than in patches of S. muticum only

on days 3 and 7 (SNK tests, P< 0.05; Fig. 4a). The pattern of this variation was

consistent across heights on the shore and sites (i.e. no significant interaction).

The contribution of the rest of the species was very similar between wrack

patches. Adults of P. cadaverina did not show significant differences among

wrack patches consistently over space and time (i.e. no significant interactions;

Table 5). However, abundance of this species varied over time (7

days>21days>12days>3days; SNK tests, P<0.05; Fig. 4b). Larvae of P.

cadaverina followed a different pattern from adults varying between wrack

patches, but inconsistently across heights on the shore (i.e. Wrack x Height

interaction, P<0.05). Larvae were more abundant in patches of S. polyschides

than in S. muticum in the dune, whereas this pattern was the opposite in the

drift line (Fig. 4c). Abundance of C. littoralis varied between wrack patches,

although this variation was not consistent across sites (i.e. significant Wrack x

Site interaction; P< 0.05; Table 5). This species was more abundant in patches

of S. muticum than in S. polyschides, but only at Site B (SNK tests, P< 0.05;

Fig. 4d). H. rubripes varied significantly between wrack patches, but there was

no consistency between heights (i.e. Wrack x Height interaction, P< 0.05;

Table 5), nor over time (i.e. Wrack x Time interaction, P< 0.05; Table 5). This

species was more abundant in patches of S.polyschides than in S. muticum in

the drift line, whereas the pattern was the opposite in the dune (SNK tests, P<

0.05; Fig. 4e). In addition, H. rubripes was more abundant in patches of S.

polyschides on days 3, 7 and 12, whereas the pattern was the opposite on day

21 (SNK tests, P<0.05; Fig. 4e). Abundance of the arachnid A. variana differed

between wrack patches, but this variation was not consistent over space and

time (i.e. significant Wrack x Site x Height x Time interaction, P< 0.05; Table

5). For example, this species was more abundant in patches of S. polyschides

than in patches of S. muticum on day 12 in the drift and dune line at both sites,

and only in the drift line at Site B on day 21 (Fig. 4f).


201

So

urc

e

T

ota

l A

bu

nd

an

ce

a,b

Larv

ae a

bu

nd

an

ce

a,b

Sp

ecie

s r

ich

ne

ss

b

D

ivers

ity

a,b

En

tire

ass

em

bla

ge

a

df

MS

F

MS

F

MS

F

MS

F

MS

P

seud

o-F

Wra

ck (

W)

1

12.0

3

233.4

*

68.0

2

275.3

5*

18.3

7

12.2

5

0.0

1

0.9

2

1549

5

1.9

Site

(S

) 1

0.9

4

4.1

8*

0.0

3

0.0

8

2.6

6

0.8

7

0.0

5

2.1

7

1243

3

20.9

6**

*

Heig

ht (H

) 1

1.9

8

0.7

3

22.3

2

7.8

4

1.0

4

0.6

9

0.0

3

301.1

*

6485

.1

1.9

1

Tim

e (

T)

3

7.7

1

88.2

4**

12.8

8

44.4

8**

75.2

9

44.4

3**

0.0

16

3.0

5

601

7.8

6**

*

W X

S

1

0.0

5

0.2

3

0.2

4

0.5

4

1.5

0.4

9

0.0

12

0.5

2

8153

13.7

4**

*

W X

H

1

0.6

2

229.3

*

9.8

2

43.8

4

1.0

4

6.2

5

0.0

03

0.8

1591

.5

1.2

6

W X

T

3

3.8

7

25.7

2*

5.3

2

23.8

4*

22.4

6

13.2

5*

0.7

90

42.4

4**

3219

3.5

6*

S X

H

1

2.7

0

11.9

7**

2.8

4

6.2

8*

1.5

0

0.4

9

0.0

00

0.0

0

3402

.4

5.7

3**

*

S X

T

3

0.0

8

0.3

9

0.2

9

0.6

4

1.6

9

0.5

5

0.0

05

0.2

3

457.8

4

0.7

7

H X

T

3

0.0

1

0.0

6

1.2

1

8.6

9+

2.7

9

0.4

4

0.0

27

0.5

3

717.4

5

0.4

1

W X

S X

H

1

0.0

03

0.0

1

0.2

2

0.4

9

0.1

6

0.0

5

0.0

03

0.1

5

1263

.2

2.1

3

W X

S X

T

3

0.1

5

0.6

7

0.2

2

0.4

9

1.6

9

0.5

5

0.0

18

0.8

1

904.8

1.5

2

W X

H X

T

3

0.4

7

27.9

5*

0.9

9

4.4

7

1.6

2

1.2

4

0.0

00

0.0

0

1425

1.5

S X

H X

T

3

0.1

6

0.7

2

0.1

4

0.3

1

6.3

6

2.0

7

0.0

51

2.2

3

1758

2.9

6**

*

W X

S X

H X

T

3

0.0

1

0.0

7

0.2

2

0.4

9

1.3

0

0.4

2

0.0

34

1.4

8

955.2

1.6

1

Resi

du

al

64

0.2

2

0.4

5

3.0

7

0.0

23

593.3

+m

arg

ina

lly s

ign

ifica

nt

(0.0

4<

p<

0.0

5);

*p<

0.0

5;*

*p<

0.0

1;*

**p

<0

.00

1; a

ln (

x+1

) tr

an

sfo

rmed

da

ta; b

sig

nifi

can

t diff

ere

nce

s w

ith c

on

tro

l

T

ab

le 4

. S

um

mar

y o

f anal

yse

s o

f var

iance

(to

tal

nu

mb

er o

f in

div

idual

s, l

arvae

ab

und

ance

, sp

ecie

s ri

chness

and

Sh

anno

n-W

iener

’s d

iver

sity

ind

ex)

and

PE

RM

AN

OV

A (

enti

re a

ssem

bla

ge)

(n =

3).

Typ

e o

f w

rack

(W

), H

eig

ht

on

the

sho

re (

H),

Tim

e (

T)

are

fixed

fac

tors

and

Sit

e (

S)

is a

rand

om

.


202

Figure 3. Mean (±SE, n = 3) of a) abundance of individuals in the dune and drift levels

at Site A; b) abundance of larvae in the dune at site A; c) number of species in the drift

at site B; d) diversity in the drift level at site B over time. Different letters represent

significant differences and same letters represent no significant differences. S.

polyschides dune; S. polyschides drift; S. muticum dune; S. muticum drift.

4.6.3.5. Analysis of assemblages in wrack patches

Macrofaunal assemblages varied between types of wrack, but the

direction and magnitude of these differences were inconsistent between sites

(i.e. significant Wrack x Site interaction, pseudo-F(1,64)= 18.84; P< 0.001; Table

4) and over time (i.e. significant Wrack x Time interaction, pseudo-F(3,3)= 3.58,

P< 0.01; Table 4). The interactions were caused by variation in direction and

magnitude of differences among wrack patches, which is clearly illustrated in

Ab

un

da

nce o

f in

div

idu

als

0

50

100

150

200

250

300

350

Time (Days)

Sp

ecie

s ric

hn

ess

0

2

4

6

8

10

12

14

Time (Days)

H'

0.0

0.4

0.8

1.2

1.6

2.0(c)

a ba

a ab

b

a

(d)

a

aa

a

b

b

b

b

(a)

cc

b

a

b

a

cb

bb

c a aa

aa Larv

ae a

bu

nd

an

ce

0

50

100

150

200

250(b)

b

a

a

b

ab b

a

3 7 12 21 3 7 12 21


203

Fig. 5. Another way of illustrating this is by examining Bray-Curtis

dissimilarities (Table 6). First, the dissimilarity between macrofaunal

assemblages in patches of S. polyschides and those in S. muticum was greater at

Site A than B. In other words, macrofaunal assemblages in patches of S.

polyschides were more similar to those in patches of S. muticum at Site B.

Second, the dissimilarity between macrofaunal assemblages in patches of S.

polyschides and those in S. muticum was greater on days 3 and 12 than on days

7 and 21. Finally, the magnitude of change between assemblages in patches of

S. polyschides and S. muticum was similar on days 3 and 12 and on days 7 and

21 (Table 6).

4.6.3.6. Influence of environmental variables on macrofauna

assemblages.

The total organic content of wrack, concentrations of carbohydrates

and Chl a best explained the pattern of macrofaunal assemblages (Table 7).

Carbohydrates content accounted for as much variance alone as when

combined with total organic content and Chl a. Nevertheless, the best

combination overall did not explain a high percentage of variance (ρs= 0.335;

P< 0.01).

For each main species, a multiple stepwise logistic regression was run

with all abiotic variables together (Table 8). Several of the environmental

variables included in this analysis explained variation for five species. For

example, the effect of temperature and chlorophyll a in patches of S.

polyschides on the probability of P. cadaverina larvae being present, were

significant. This means that for a 1% increase in temperature and chlorophyll a

content, a patch of S. polyschides has a 0.436 and 1.014 more chance of having

a larva than not, respectively (Table 8).


204

Fig

ure

4.

Mea

n n

um

ber

(±

SE

; n

=3

) o

f in

div

idual

s o

ver

tim

e. a

) A

nth

om

yii

dae

sp

1 i

n t

he

dune

level

at

site

A.

b)

P.

cadave

rin

a

aver

aged

in t

he

du

ne

at s

ite

B.

c) P

cad

ave

rin

a (

larv

ae s

tage)

aver

aged

in t

he

dune

and

dri

ft l

evel

s at

sit

e A

. d

) C

. li

tto

rali

s in

the

du

ne

acro

ss s

ites

(A

and

B).

e)

H. ru

bri

pes

in t

he

dune

and

dri

ft l

evel

s at

sit

e B

. f)

A.

vari

an

a a

cro

ss h

eights

on t

he

sho

re a

nd

sit

es.

Dif

fere

nt

lett

ers

rep

rese

nt

sig

nif

icant

dif

fere

nce

s an

d s

am

e le

tter

s m

ean n

o s

ignif

ican

t d

iffe

rence

s.

S.

po

lysc

hid

es d

une;

S.

po

lysc

hid

es d

rift

; S

. m

uti

cum

dune;

S

. m

uti

cum

dri

ft

0

25

50

75

100

125

P. ca

da

veri

na

(la

rvae

)

05

10

15

20

25

30

Tim

e (

Da

ys)

05

10

15

20

A. va

ria

na

Mean (±SE) no. of individual

02468

10

C. li

tto

rali

s

05

10

15

20

25

Sit

e A

Sit

e B

aa

aa

a

a

aa

ab

bb

Sit

e A

Sit

e B

aa

aa

a

a

a

b

ca

b

b

(d)

(f)

0

50

100

150

200

250

An

tho

myi

ida

e sp

1P

. c

ad

ave

rin

a

a

b

a

ba

a

aa

a

a

a

b

aa

a

aa

aa

a

b

a

a

aa

ba

a

b

a

(a)

(b)

(c)

(e)

a

a

a

a

a

a

ab

b

b

b

bb

H. ru

bri

pes

aa

37

12

21

37

12

21

3

7

12

21

37

12

21

37

12

21

3

7

12

21

3

7

12

21

3

7

12

21


205

Effects of temperature, humidity, chlorophyll a and carbohydrates in patches of

S. muticum on the probability of C. littoralis being present were also

significant. However, only the effect of carbohydrates content in wrack was

relatively stronger on the presence of this species. In general, although the

effects were significant for some environmental predictors, the effect size was

small. In contrast, total abundance of individuals and total abundance of larvae

showed significant effects with most of the environmental predictors in both

types of wrack (see log-linear models; Table 8). However, the environmental

predictors explaining variability of total abundance and abundance of larvae

varied between types of wrack, i.e. lipids content for total abundance and

chlorophyll a for larvae abundance. Results of the log-linear model for total

number of species and diversity were omitted since there were no significant

effects for any of the predictor variables tested.

4.6.4. Discussion

4.6.4.1. Patterns of colonisation and succession

Results indicate that abundances of individuals were significantly

larger in wrack patches than those found in bare sand, i.e. controls located

nearby wrack patches. It is clear that algal wrack indeed promotes an increase

in population abundances of sandy beach macrofauna, either because it

provides their main source of food or refuge from environmental conditions

and/or due to predation (e.g. Inglis, 1989; Colombini et al., 2000).The number

of species found in this study (29) is similar to those reported in previous

studies elsewhere (Jędrzejczak, 2002b, Dugan et al., 2003), but lesser in

number than in a previous wok conducted in an adjacent beach (Olabarria et al.,

2007). In our study, the major components of the algal wrack were dipteran

flies and tenebrionid and staphylinid beetles. Several authors have noticed that

talitrid amphipods are considered primary macroinfaunal colonisers of fresh

algal wrack stranded on sandy beaches (e.g. Griffiths and Stenton-Dozey, 1981;

Inglis, 1989; Colombini et al., 2000).


206

So

urc

e

A

nth

om

yii

da

e s

p1

P

. c

ad

av

eri

na

P. c

ad

av

eri

na

(la

rva

)

C.

litt

ora

lis

H.

rub

rip

es

A.

va

ria

na

df

MS

F

MS

F

MS

F

MS

F

MS

F

MS

F

Wra

ck (

W)

1

30.8

2

21

.9*

0.7

7

2.8

7

5.7

7

20.2

6

2.3

7

1.6

7

0.1

1

0.4

4

2.5

51.5

Site

(S

) 1

0.5

4

3.9

8

4.7

1

7.3

3*

2.9

3

6,8

9*

0.3

4

1.1

3

0.2

3

0.6

3

0.4

1

6.8

*

He

igh

t (H

) 1

0.3

8

2.1

5

5.3

2

2.0

3

3.2

6

36.6

0.0

8

206

.6**

11.6

25.7

0.5

5

4.3

6

Tim

e (

T)

3

9.2

2

64.4

**

3.6

6

22.8

*

0.2

0.1

1

1.0

9

1.4

9

3.3

5

4.0

0.5

3

1.6

2

W X

S

1

0.1

4

1.0

3

0.2

7

0.4

1

0.2

8

0.6

7

1.4

2

4.7

1*

0.2

4

0.6

5

0.0

5

0.8

W X

H

1

0.0

7

0.5

6

6.2

4

44.1

1.4

3

913

.9*

0.0

8

0.1

7

1.9

4

266

.2*

0.4

3

5.9

W X

T

3

7.8

6

85.8

**

2.9

2.2

8

2.1

8

2.3

1

0.6

1

1.4

7

2.4

7

10.4

*

0.6

2

2.3

0

S X

H

1

0.1

8

1.3

2

2.6

2

4.1

*

0.8

9

2.0

9

0.0

0

0.0

0

0.4

5

1.2

3

0.1

2

2.0

7

S X

T

3

0.1

4

1.0

6

0.1

6

0.2

5

1.7

3

4.0

6*

0.7

4

2.4

5

0.8

4

2.2

7

0.3

3

5.3

9**

H X

T

3

0.0

1

0.4

4

0.7

4

1.9

1.8

9

12.4

1*

0.1

6

0.3

6

0.3

9

6.1

0

0.1

0

0.4

5

W X

S X

H

1

0.1

2

0.8

9

0.1

4

0.2

2

0.0

1

0.0

1

0.4

4

1.4

6

0.0

1

0.0

2

0.0

7

1.2

W X

S X

T

3

0.0

9

0.6

8

1.2

7

1.9

8

0.9

4

2.2

2

0.4

2

1.3

8

0.2

4

0.6

4

0.2

7

4.4

7**

W X

H X

T

3

0.2

2

2.1

8

2.0

1

1.9

5

0.4

4

0.6

8

0.2

5

0.7

5

1.3

9

6.1

3

0.2

4

1.0

8

S X

H X

T

3

0.0

15

0.1

2

0.3

9

0.6

1

0.1

5

0.3

6

0.4

4

1.4

7

0.0

6

0.1

8

0.2

3

3.8

5*

W X

S X

H X

T

3

0.1

01

0.7

5

1.0

3

1.6

0.6

4

1.5

1

0.3

3

1.1

0

0.2

3

0.6

1

0.2

2

3.7

*

Re

sid

ua

l 64

0.1

35

0.6

4

0.4

2

0.3

0.3

7

0.0

6

*p<

0.0

5; **

p<

0.0

1;

***p

<0

.00

1

Ta

ble

5.

Su

mm

ary o

f anal

yse

s o

f var

iance

fo

r ab

und

ance

of

each s

pec

ies.

Typ

e o

f w

rack (

W),

Hei

ght

on t

he

sho

re (

H),

T

ime

(T)

are

fixed

fac

tors

and

Sit

e (S

) is

a r

and

om

. D

ata

wer

e ln

(x+

1)

tran

sfo

rmed

.


207

The scarcity of these amphipods in the area of study might be related to the

specific environmental conditions in the beach during the sampling period,

when high temperatures and very strong winds following the first sampling day

dried off most of the wrack patches. In fact, previous studies have shown that

locomotory behaviour of talitrids is strongly influenced by weather conditions

such as relative humidity of air, sand temperature and moisture (e.g. Colombini

et al., 1998; Fallaci et al., 1999).

The pattern of colonisation varied between wrack types. The total

number of individuals was larger in patches of S. polyschides than in patches of

S. muticum. This difference in abundance became more evident within 3 days

and diminished over time, although the sharpest differences occurred in the

abundance of several larvae species. It is interesting to highlight that the

number of species and diversity reached higher values in patches of S. muticum

than in S. polyschides on day 3, but this pattern was reverted from day 7

onwards. On day 3, the largest abundances in native wrack patches were related

mainly to larvae belonging to the same species, i.e. Anthomyiidae sp 1. Thus,

dominance of larvae, can explain the small number of species and low diversity

found in native patches at that time. After day 3, larvae abundance dropped,

and both number of species and diversity increased to reach higher values in

patches of S. polyschides than those in S. muticum. Reproduction, larval

settlement or recruitment can be stimulated by an increase in food (Ford et al.,

1999, Bolam et al., 2000). In the case of flies, adults are insignificant

consumers of algae-exuded substances, but lay eggs in wrack which may

contribute greatly to the breakdown of kelp tissue as a result for their own

feeding activity and through the spread of microorganisms (Griffiths and

Stenton-Dozey, 1981; Inglis, 1989). Within the first days of experiment, the

increase in number of fly larvae could be related to the movements of adults

towards patches of S. polyschides, which can offer a more suitable habitat and

constitute a source of food for these species (see Norkko and Bonsdorff, 1996).

For example, the physical structure and/or specific microclimatic conditions in

native wrack patches might favour chiefly dipteran oviposition and breeding.


208

Figure 5. Non-metric multidimensional scaling (nMDS) for differences in assemblages

among wrack patches across heights on the shore (dune and drift), sites (A and B) and

over time (n = 3). :S. muticum dune; :S. muticum drift; :S. polyschides; :S.

polyschides drift.

Most species (87%) colonised the wrack patches within 3 days.

Different species showed different patterns of colonisation suggesting that life-

history attributes, such as their colonising and competitive abilities, and

mobility of different taxa, may be important factors contributing to explain

such patterns (see Wilson, 1994). Changes in habitat quality also affect

dynamics of local populations (Bonte et al., 2003). Variations in trophic

habitats of different species may play an important role in pattern of succession

together with different qualitative stages of decomposition and ageing of wrack

(Olabarria et al., 2007). Herbivorous species such as C. littoralis rapidly

colonised all the patches and remained present over time. The scavenger P.

cadaverina that feeds on different sources of organic debris (Jaramillo et al.,

2003) peaked on day 7. Carnivorous species such as the histerid H. rubripes

and the spider A. variana were early colonisers in both types of wrack, but their

abundances were larger on days 7 and 21. This increase in abundance of

predators may be related to the increase in abundance of larvae and immature

3 days

Site A

Site B

7 days 12 days

Stress: 0,06Stress: 0,06

21 days









209

individuals which are likely to serve as food source. Apart from Anthomyiidae

sp1 that was clearly more abundant in patches of S. polyschides on day 3,

abundances of rest of species showed differences between wrack types, but this

trend was not consistent over space and/or over time. This suggests that other

factors, apart from the type of wrack, are influencing the patterns of

colonisation and succession. For example, variation may be related to

progressive microclimatic changes of wrack accumulations due to their

different position across the beach, i.e. dune and drift at the two sites slightly

varied in environmental conditions (e.g. Colombini et al., 2002; Jędrzejczak

2002a,b). In fact, several studies have pointed out that responses of

macrofaunal assemblages to wrack deposits vary depending on sites located a

few metres or kilometres apart (Rossi and Underwood, 2002; Colombini and

Chelazzi, 2003; Dugan et al., 2003) and on seasonality (Ford et al., 1999).

Time (days) Dissimilarity (%) between wrack

3 61

7 55

12 61

21 50

Site

A 63

B 52 Pairwise comparisons from PERMANOVA; 4999 permutations of raw data.

Data were square root transformed.

Table 6. Mean Bray-Curtis dissimilarities (%) between wrack patches.

(S. muticum vs. S. polyschides).

4.6.4.2. Abiotic factors affecting macrofaunal assemblages

There were some evidences to support the hypothesis that macrofaunal

assemblages changed in response to the wrack type, but patterns varied over

space and over time. Results indicated that carbohydrates, organic matter and

chlorophyll a variables best described the observed patterns in macrofaunal

assemblages. Moreover, temperature and humidity had some influence on the

presence of some species in wrack patches (see Table 8).


210

Different types of wrack can offer different quality and/or quantity of

food availability for macrofauna, which leads to complex patterns of

macrofaunal response (Ford et al., 1999; Rossi and Underwood, 2002). Results

indicated that nutritional value of wrack (mostly carbohydrates, lipids and

organic matter content) differed between the two types of wrack. In most cases,

the carbohydrates, lipids and organic content were greater in patches of S.

muticum than in patches of S. polyschides. In contrast, the chlorophyll a

concentration (used as a proxy of benthic microalgae biomass) was greater in

patches of S. polyschides than in patches of S. muticum in most cases. Benthic

microalgae may account for a large proportion of the carbon budget of a detrital

food-web and may play an important role in moderate fluxes of carbon in

coastal sediments (e.g. Herman et al., 2000). In fact, a greater concentration of

benthic microalgae in S. polyschides might be related to a lesser content of

polyphenols in laminarian seaweeds since the colonisation process in these

organisms is related to the polyphenol content (Van Alstyne et al., 1999).

k Best variable combinations (ρs)

1 CHO

(0.326)

2 O.M., CHO Chl a, CHO

(0.335) (0.316)

3 O.M., CHO, Chla H, O.M., CHO

(0.323) (0.307)

4 H, O.M., CHO, Chla

(0.309)

Table 7. Combinations of environmental variables, taken k at a time, giving

largest rank correlation ρs between biotic and abiotic similarity matrices; bold

indicates best combination overall. CHO: carbohydrate; O.M.: organic matter; Chl a: chlorophyll a; H: humidity.

In this context, the role of microphytobenthos in the flux of nutrients in

sediment is very important. Nutrients can be released from wrack patches and

are likely to be used by microphytobenthos, which may play a major role in the

flux of nutrients in the sediments, representing a direct or indirect source of

food for some invertebrates (Rossi and Underwood, 2002). Strong variation in

patch quality, i.e. nutritional value, may give rise to source-sink dynamics


211

affecting the local macrofaunal assemblages inhabiting patches of wrack (see

Bonte et al., 2003).

Although temperature and humidity influenced the presence of some

species (e.g. C. littoralis and H. rubripes in patches of S. muticum, total

abundance in the two types of patches; Table 8) the effect was not very strong.

Temperature and humidity varied between the two types of wrack although

inconsistently over space and time. Slight differences in these parameters could

affect colonisation by different invertebrate species. In fact, variation in

microclimatic conditions of wrack deposits has been considered an important

factor affecting behaviour, locomotory activity and distribution of several

arthropod species inhabiting beach-dune systems (e.g. Colombini et al., 1998;

Fallaci et al., 1999).

Apart from differences in nutritional value and microclimatic

conditions between the two types of wrack, differences in structure, i.e.

complexity, of wrack patches might play an important role in variability of

macrofaunal assemblages. Different structures due to morphological

differences of seaweeds cause variability in habitat quality, i.e. shelter from

predation (e.g. Vandendriessche et al. 2006). In some cases, preference of

invertebrates for certain seaweed species seems to be related to factors such as

availability, habitat provision or refuge from predation rather than nutritional

value (e.g. Wakefield and Murray, 1998).


212

Sa

cch

ori

za p

oly

sch

ides

S

arg

ass

um

mu

ticu

m

Lo

gis

tic r

egress

ion

In

terc

ep

t T

H

O

.M.

pro

t ch

o

Lip

C

hl

a

In

terc

ep

t T

H

O

.M.

pro

t ch

o

Lip

C

hl

a

An

tho

myii

dae s

p1

E

stim

ate

4

8.9

8

0.7

3

-0.7

2

0.0

84

-0

.03

0

.00

2

-0.0

04

0

.00

4

6

0.9

-0

.4

-0.4

7

-0.0

01

-0

.01

0

.00

1

-0.0

01

-0

.01

W

ald

st.

0

.66

2

.41

0

.96

2

.29

4

.58

0

.33

4

0.2

01

0

.14

1

0

.19

5

1.4

5

0.1

1

0.0

01

2

.86

0

.91

0

.05

6

0.7

7

o

dd

s ra

tio

-

2.0

8

0.4

8

1.0

9

0.9

71

1

.00

1

0.9

96

1

.00

4

-

0.6

7

0.6

25

0

.99

9

0.9

9

1.0

01

0

.99

9

0.9

93

P.

ca

da

veri

na

E

stim

ate

2

1.3

-0

.83

0

.76

-0

.03

-0

.01

-0

.00

0

-0.0

01

0

.01

4

-8

.44

0

.57

-0

.18

0

.01

4

0.0

1

0.0

01

-0

.00

1

-0.0

5

(lar

vae s

tage)

Wald

st.

3

.97

4

.23

0

.41

0

.25

2

0.9

83

0

.00

1

0.0

21

3

.87

0.0

14

1

.47

0

.07

0

.27

0

.98

0

.14

0

.04

3

3.5

5

o

dd

s ra

tio

-

0.4

4

2.1

4

0.9

7

0.9

93

0

.99

9

0.9

99

1

.01

4

-

1.7

7

0.8

35

1

.01

4

1.0

1

1.0

00

0

.99

9

0.9

55

C.

litt

ora

lis

Est

imate

6

.87

-0

.11

-0

.07

0

.02

1

0.0

01

0

.00

1

-0.0

02

-0

.01

17

6.9

-0

.73

-1

.62

-0

.05

-0

.01

0

.00

2

-0.0

01

-0

.02

W

ald

st.

0

.03

0

.53

0

.02

5

0.6

81

0

.03

2

0.5

35

0

.23

9

1.9

41

4.3

9

5.4

0

3.8

7

2.1

1

2.2

1

4.7

8

0.1

61

4

.93

o

dd

s ra

tio

-

0.9

0

.93

2

1.0

21

1

.00

0

1.0

01

0

.99

8

0.9

94

- 0

.48

4

0.1

97

0

.95

2

0.9

92

1

.00

2

0.9

98

0

.98

3

H.

rub

rip

es

Est

imate

9

1.4

5

-0.3

-0

.79

-0

.05

-0

.01

0

.00

1

0.0

08

-0

.03

48

4.7

0

.19

9

-4.8

1

-0.2

04

-0

.03

0

.00

2

0.0

1

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213

In summary, this study indicates that the different wrack deposits, i.e. native

versus invasive algal wrack, were not used uniformly by invertebrates. Data

also provides evidences that nutritional content and microclimatic conditions of

wrack deposits, i.e. temperature and humidity, affected macrofaunal

assemblages. It is important to emphasize that since correlation does not prove

causation, the conclusions from this study should be treated as predictions that

point to the most important experimental manipulation to be conducted next,

not as conclusions to be set in stone. Experimental manipulation to test

hypotheses regarding the physical structure of wrack and stable isotope

analyses to provide clues about the origin of invertebrate’s food sources and

trophic flows in beaches are the next step. In addition, results indicate that

replacement of native wrack deposits by exotic wrack may have important

effects on macrofaunal assemblages on sandy beaches. A change in the type (or

amount) of seaweed wrack entering a beach may alter the macrofaunal

assemblages and ecosystem function. Thus, the effect of the invasive seaweed

S. muticum may have an effect that is spread away from the points of invasion,

i.e. intertidal and subtidal rocky shores. An assessment of impact on different

marine ecosystems may be important criteria in assessing the impact of this

invasive species and the prioritization of exotic management.

Acknowledgments

We thank the authorities of the Corrubedo Nature Park for funding,

permission and technical assistance as well as to all the colleagues who assisted

us in field work. This research has also been supported by the Spanish Ministry

of Education and Science (CGL2005-02269). Funds to I.F.Rodil were provided

by a Predoctoral grant (XUGA, P.P. 0000 300S 140.08).

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PART V. GENERAL DISCUSSION.

“Tell me and I will forget. Show me and I may remember. Involve me and I

will understand”.

-Confucius

Part V General Discussion

218

5.7.1. The ecology of sandy beaches in the northern coast of the

Iberian Peninsula.

During the time of this thesis, we have investigated a wide range of

beaches along a major part of Spain’s Atlantic coastline. These beaches were

sampled quantitatively which enables us to make a general description of the

macrofauna community structure from this European region. Most of the

beaches from this coast are highly exposed (sensu McLachlan, 1980) to the

ocean processes; subjected to a mesotidal regime (2 and 4 m.), which is quite

different from most of the traditional studies in microtidal sandy beaches (e.g.

Jaramillo et al., 1993; McLachlan et al., 1993). In terms of beach typology,

sandy beaches from this region can predominantly be classified as intermediate,

with average slopes of 1/22-1/52. Sediment size is medium and not very well

sorted becoming progressively finer on the supratidal.

When starting to work in a region where little to no research has been

done, it is important to construct a baseline study that can be used as a

reference for future work. The first and second part of this thesis (see Chapters

1, 2 and 3) analyse the basic characteristics of the Spanish sandy beach

macrofauna, such as species composition and richness, the spatial distribution

and zonation of the macrofauna or the main environmental factors affecting

benthic macrofauna. Although no temporal study was followed in this part of

the thesis, the comparative snapshot sampling of 19 sandy beaches of the same

type and from the same region, allows a fundamental and representative

analyses of the macrofauna structure. The emphasis of this part of the thesis

was put on spatial, short-term effects. However, there is growing evidence that,

at least on microtidal beaches, the temporal scale is very important in sandy

beach ecology (e.g. Brazeiro and Defeo, 1996; Degraer et al., 1999; Dugan et

al., 2004). The lack of replication in time of several of the ecological studies

(Chapters 2, 3 and 4) is one of the, if not the most important limitation of this

thesis. Although the results from these chapters suggest that macrofauna is

primarily structured spatially, the information is far too limited to state that the

temporal scale is less important on mesotidal, temperate beaches. The results


219

from various chapters of this thesis make us confident, however, that tackling

the appropriate spatial scale is at least as important as using an adequate

temporal scale.

5.7.1.1. Environmental factors affecting benthic macrofauna.

The results obtained in Chapter 2 showed that the number of species

was the biotic parameter most affected by the abiotic factors, increasing

linearly with tide range and diminishing with exposure rate. Other important

biotic factors such as biomass decreased exponentially with increasing average

grain size. This supports one common generalisation in sandy beach ecology:

the macroinvertebrates decreasing along a morphodynamic gradient from the

dissipative to the reflective conditions and from sheltered to exposed beaches.

Mean grain size was negatively related to biotic factors such as species richness

or biomass. There are a number of reasons to assume that this relationship is a

causal event. For instance, many species find it difficult or nearly impossible to

burrow in coarse sediment (Lastra and McLachlan, 1996; de la Huz et al.,

2002), thereby seriously hampering their survival chances. A long burial time

increases the predation risk and the probability to be swept away by the next

incoming swash. Furthermore, coarse sand provides a less stable anchoring

substrate, increasing the chance to be washed out of the sediment. Sediment

grain size indirectly impacts the fauna through its influence on swash and sand

bed permeability. Grain size variation, within the same beach, may promote

intraspecific zonation such as in the case of the bivalve Donax trunculus. The

smallest individuals were found highest on the shore, and the largest confined

to the lower saturated zone coping with swash climate and coarser sand.

Morphodynamic variability in a sandy beach is determined by sediment

range and wave regime but it is also important to include the effect associated

to the tides. Tide range has not been included in beach classification parameters

because traditional studies were carried out in microtidal beaches. However,

tide range is an important agent in mesotidal beach formation, and when tide

range becomes more significant that wave energy, the number of species

increases. Dean’s parameter does not take tides into account, and therefore is


220

inadequate to cover meso or macrotidal situations. Another index was used to

compare beaches subjected to differing tide ranges. BSI gave good correlations

when a wide range of beach types were considered (Hacking, 1997). Our study

was concentrated on a limited geographic region, in which only part of the

spectrum of conditions are present. In this region, Dean’s parameter or BSI

have a low capacity to identify the roles of the various individual physical

factors controlling beach communities. New indexes such as BSI or BI (see

McLachlan and Dorvlo, 2005) will be more effective in macroscale

comparisons. The recent availability of comparable results of quantitative

beach surveys from many regions, however, allows for a database to be

compiled that covers most beach types and latitudes to enabling a broader

comparison of global trends (e.g. McLachlan and Dorvlo, 2005; Defeo and

McLachlan, 2005).

When only intermediate beaches are studied, the different community

characteristics seem to be affected by different abiotic factors. The number of

species in sandy beaches from this region is better explained by the exposure

rate than by traditional morphodynamic parameters or even beach slope. This

confirms that a greater ensemble of variables should be taken into account in

the ecology of sandy beach macrofauna and that communities of sandy beach

invertebrates are limited by a wider range of ecological factors rather than a

single key factor.

5.7.1.2. Community structure and macrofauna zonation

Crustaceans were the most abundant macrofaunal group, in abundance

and species number, while molluscs and polychaetes were the least abundant

groups (Chapters 2 and 3). The general cross-shore pattern observed in beaches

from this region confirms the current knowledge in sandy beach ecology:

species richness increases downshore (e.g. McLachlan and Brown, 2006).

Intertidal zonation is a well-studied phenomenon and although general patterns

have been established in some particular cases (see 1.1.2.4. for details), there is

no clear zonation pattern and in most of the cases it is considered an artificial

division of a continuum with an overlap between adjoining zones (McLachlan


221

and Jaramillo, 1995; Degraer et al., 1999). However, results obtained in this

study suggest an elementary, but also widely applicable, zonation scheme for

sandy shores. This divides the studied beaches in two zones: a zone of air-

breathers at and above the driftline and a zone of water breathers below this.

The special profile of the intermediate sandy beaches studied here seems to fit

well with this zonation scenario. These beaches showed a broken profile

roughly separated by mean sea level into an upper steep beach, followed by a

lower flat downshore which has to cope with swash and wave climate. Zones

are clearest and narrowest at the top of the shore and become increasingly

blurred and wide moving downshore. The supralittoral zone of air breathers,

present on all shores, is typically inhabited by crustaceans. True intertidal

species dwell in the littoral zone, present on all except the harshest reflective

beaches, extending from the drift line down the midshore to just above the

water table outcrop (Defeo and McLachlan, 2005). Although we can elucidate a

trend in some of the beaches for lower shore zonation, the general pattern

shows that zonation appears unclear and blurred in the lower shore levels.

5.7.1.3. Relationship between macroinfauna and environmental variables

Macroinfauna abundance and distribution in sandy beaches depend on

several physical and biological factors. Beaches can be described by a set of

physical parameters such as tide range, sediment grain size, exposure rate,

swash climate and/or accretion-erosion dynamics, which could be potential

structuring factors for sandy beach macrofauna (Brazeiro, 2001, McLachlan

and Dorvlo, 2005). Results obtained in this study indicate that environmental

parameters such as slope, beach length and wave height were the most

important factors explaining variability in the species density. These patterns

are tightly related to beach morphodynamics. Sandy beaches with higher slope

and wave height present coarser sediment size and reflective characteristics.

Within one geographical region, the general pattern in sandy beach macrofauna

shows a decrease in species richness, abundance and biomass when moving

from dissipative to the reflective beach state. This pattern, which is found at

any latitude, is now considered one of the paradigms in sandy beach ecology


222

(Defeo and McLachlan, 2005). Furthermore, McArdle and McLachlan (1992)

suggested beach slope and wave height as the most important factors

controlling swash climate, which is the most important aspect of the

environment by fauna inhabiting exposed sandy beaches. Those species with

the clearest zonation were found to be the best explained by the environmental

variables than species with no sharp boundaries in their distribution along the

beach profile.

It seems that community characteristics in the beaches studied are not

just determined by beach morphodynamics, but also by other factors dependent

on oceanographic conditions and coastal processes, determining critical

characteristics such as food availability. In spite of the geographical continuum

formed by all the 19 studied beaches, water mass characteristics along the north

coast of Spain are determined by variations in coastal productivity at different

spatial scales. We believe that macroinfauna differences found between

beaches arise from the chlorophyll concentration gradient rather than from

physical differences between beaches. The existence of an upwelling event,

common along the eastern boundary of the North Atlantic between 10º and 44º

N and focused on the North West coast of Spain (Wooster et al., 1976) can be

related to the macrofauna differences found along this beach gradient (west-

east). There is a net influx of nutrient rich deeper water and this fertilisation

leads to the high primary production, which results in benthic enrichment and

seems to dilute to the east through the north coast of Spain (Lastra et al., 2006).

It could be argued that proximity to such upwelling areas leads to higher

macroinfaunal abundance values because of greater food availability due to the

increase in productivity.

5.7.2. The importance of exposure on sandy beach macrofauna:

hydrodynamic conditions and food availability.

Macrofauna communities inhabiting sandy beaches are supported

almost entirely by allochthonous inputs of organic materials because little

primary production occurs on the beach itself. In many temperate regions, the

major sources of allochthonous organic material to sandy beach macrofauna are


223

phytoplankton and marine macrophytes. Depending on food quality and

quantity in the intertidal, macrofauna community structure and trophic relations

can vary. Beaches lack attached macrophytes except in rare cases of sheltered

beaches with seagrass meadows extending onto the lower shore. Food chains

mainly begin and end in the sea but the land can also play a relative main role

in food availability. Results obtained in Part II of this thesis (Chapter 4) suggest

that macroinfauna community, in terms of abundance, biomass and species

richness, is more complex and diverse in sheltered environments than in

exposed sandy beaches. This reflects the general trend found in traditional

studies where an exposure increase led to a decrease in biotic variables (e.g.

Jaramillo and McLachlan, 1993; McLachlan et al., 1993).

5.7.2.1. Macrofauna characteristics in a gradient of exposure

Supratidal levels, where environmental conditions are harsh for truly

marine macrofauna, showed lower number of species and were dominated

exclusively by crustaceans, mainly talitrid amphipods. The ability of this kind

of organisms to utilise the upper levels of sandy beaches must relate to their

adaptations to avoid desiccation (McLachlan, 1990). Exposed sandy beaches

with short swashes and steep slopes harbour a rich macrofauna community

which find a more stable environment in the supralittoral zone (Defeo and

Gómez, 2005); while the number of species inhabiting the lower part

diminished sharply. In fact, no significant differences in the biotic variables

were found when comparing supralittoral community from exposed and

sheltered localities. Most of the species at this level have been considered

wrack-associated macrofauna and they largely depend on allochthonous inputs

associated with oceanographic processes (see Chapter 6). Sheltered beaches,

with more favourable environmental conditions and sediment stability, showed

higher significant values of biotic factors than exposed beaches when mid and

low tide levels were compared. The results from this study support the “Swash

Exclusion Hypothesis”, which states that the decrease in species richness,

abundance and biomass is caused by increasing harshness of the swash (see

section 1.1.2.3), but no significant effect was found at the supratidal, where


224

swash climate is barely perceptible. Moreover, it is suggested that species

living at the supratidal level show relative independence of swash climate

effects with no clear response to beach type, and those species that follow

predictions of the SHE are mainly represented by intertidal forms (Defeo and

Gómez, 2005).

Swash climate and sand particle size may define the response of the

macroinfauna. Molluscs and polychaetes diminished significantly due to the

increasing harshness and exposure rate of the exposed intertidal. Both faunistic

groups increased their mean abundances significantly at the mid and low tidal

levels in sheltered beaches, where more stable physical conditions are found,

following the Habitat Favourability Hypothesis (Defeo et al., 2001). The

exposed intertidal, with harsher physical conditions and coarser sediment can

have a negative effect on burrowing, respiration rate and growth of filter feeder

bivalves, such as Donax trunculus. Sheltered sandy beaches, with lower

hydrodynamic conditions will favour accumulation of organic matter

potentially available to benthic deposit-feeders, mainly polychaetes, which are

the dominant trophic group in this type of intertidal.

5.7.2.2. Effect of the biochemical composition of sedimentary organic

matter on macrofauna

In Chapter 4, biochemical compounds concentrations of sedimentary

organic matter showed significant differences between sheltered and exposed

beaches. This can be related to the morphodynamic and physicochemical

characteristics of sandy beaches. Furthermore, a significant inverse correlation

between slope, exposure rate and BPC concentration was found. The exposed

sandy localities showed a significant increase in the reflective slope conditions

due to the harsher morphodynamic conditions. It seems that biopolymeric

concentrations follow a similar pattern that was also shown by organisms,

increasing from exposed intertidal with steeper slopes to sheltered sandy

beaches with flatter slopes.

Proteins constituted the main dominant fraction of the biochemical

composition of sedimentary organic matter in sheltered and exposed localities.


225

This was even more important downshore close to the swash climate. The fact

that proteins were the main dominant fraction of BPC and carbohydrates

showed the lowest values measured in all the localities, indicate that the

organic matter may be mostly of newly generate origin. The PROT:CHO ratio

has been used to assess the “age” of sediment organic matter. This ratio was

found high enough to suggest that most of the sedimentary organic matter in

these beaches was recently produced and that protein is not a limiting factor for

consumer’s growth (Fabiano et al., 1995). However, protein concentrations, on

average, were lower in sheltered (63.4%) than in exposed (80.2%) sandy

beaches, but there was a higher concentration of organic matter in sheltered

localities. This could be better explained by the influence of temporal

allochthonous inputs since little primary production occurs on the beach itself.

It seems that the low hydrodynamic conditions of sheltered localities favours

accumulation of organic matter (see Chapter 5), while exposed sandy beaches

depend much more on the episodic inputs such as wrack debris (see Chapter 6).

The food available in the intertidal may be the result of the interaction

and equilibrium between physical and biological processes. There is enough

evidence to suggest that macrofauna sandy beaches are not just physically

controlled (although this can be a main factor) but other ecological factors,

including biochemical composition of sedimentary organic matter, may have

relevant influence in the macrofauna community structure of sandy beaches.

5.7.3. The role of food availability in the macrofauna community

structure of sandy beaches: spatial and temporal patterns.

Two sandy beaches, with different exposure rate, were studied

separately in part IV of this thesis in order to know the effect of food available

on macrofauna assemblages. In Chapter 5, the relationships between the

biochemical characteristics of sedimentary organic matter and benthic

macrofauna were analysed over two years in one estuarine sandy beach from

the NW coast of Spain. Due to the importance of exogenous organic input in

sandy beaches, Chapter 6 dealt with the relevant influence of algal wrack on

macrofaunal assemblages in one exposed sandy beach from NW coast of Spain.


226

With these two studies we tried to identify the role of the organic matter

contribution in the observed intertidal macrofauna variability.

5.7.3.1. Seasonal variability in the benthic macrofauna distribution and

food availability in a sheltered estuarine beach.

Analysis of distribution of benthic macrofauna from Barraña (Chapter

5) demonstrated that the tidal levels sampled were characterised by distinct

faunal densities and species composition. Polychaetes and molluscs occurred

mainly at the intertidal level, while crustaceans tended to occur higher on the

shore (see 5.7.2.1.). Abundance, biomass and number of species were

negatively related to sediment depth. In addition to the horizontal level,

significant differences in depth distribution of macrofauna were found. This

could be related to differences in sediment characteristics, such as grain size or

compactness, which may condition organism’s ability to burrow. Sediment

characteristics, however, were not able to explain macroinfauna variation

alone. Vertical zonation could be further controlled by the presence and

position of the Redox Potential Discontinuity (RPD) layer since fauna is

dependent on dissolved oxygen for their respiration The RPD was found in the

intertidal at the 5-10 cm depth and macroinfauna was concentrated on the sand

surface or subsurface (~75%).

The intertidal levels on sheltered beaches are considered to be under

optimal environmental conditions in terms of humidity, temperature and food

supply for marine macroinfauna. Benthic macrofauna will be favoured by

accumulations of organic matter (Defeo et al., 2001) because of the lower

hydrodynamic conditions in sheltered beaches. Maximum concentrations of

food available, macrofauna abundance and species richness were found at the

medium tidal level. The peculiar profile of this beach, together with more

gentle environmental conditions, increased the amount of organic matter and

water content in the medium tidal level. These particular conditions may

promote macrofauna abundance and species richness in this part of the

intertidal, compared to the supratidal or downshore. Most of the species

inhabiting the intertidal level belonged to the deposit-feeder’s group, favoured


227

by organic rich supply on the sediment surface during winter and spring.

Deposit-feeders are able to rapidly exploit food resources and conspicuous

abundance of this trophic group has been related to a marked increase in

proteins (Rossi et al., 2001). The occurrence of suspension feeders was

restricted to the lower intertidal level, probably because they can only feed at

high tide and they cannot exist where submergence is brief.

Despite the constant dominance of few abundant species on this beach,

high variability of the community was observed throughout the study period,

which could be related to fluctuations in the availability of food resources.

From analysis of the biochemical composition of organic matter, the labile

fraction accounted for an important part of the organic matter accumulated in

the intertidal and proteins were the dominant fraction. The rise in proteins

meant an increment in the quality of food available. The particularly high

protein values recorded in winter could be related to allochthonous inputs,

which are more common at this time of the year. There was a decrease in the

PROT:CHO ratio in summer and at the beginning of autumn, probably because

of the lack of sea input, high temperatures and solar radiation which usually

characterise this season. During this period of the study, less algal detritus and

high values of refractory organic matter were found, suggesting scarce

availability and low quality of food resources. The progressive decomposition

of this debris during summer could cause a rapid depletion of the labile fraction

of the organic matter. This suggests the presence of aged organic matter with of

a largely detritic origin caused by the algal-wrack decomposition.

Allochthonous inputs are usual incidents during winter, which promote

accumulation of dead seaweed on the beach face and therefore introduce new

organic matter in the intertidal. Some benthic animals may indeed benefit from

drifting algal mats as a key resource.

Chlorophyll a concentrations in the sediment reported frequent peaks

during winter and spring, with the particularly high values of Chl a that may be

related to the high deposition of algal detritus and a low decomposition rate

over the winter period. This can create an ideal environment for microbial


228

productivity with a subsequent increase in photosynthetic activity (Kelaher and

Levinton, 2003).

This study showed the importance of food availability in a benthic

macrofauna community that relied on seasonal deposition of sedimentary

organic matter at the intertidal. Food quality and quantity have the potential to

cause substantial spatio-temporal variation in the structure of macrofauna

assemblages in estuarine beaches. The statistical analyses indicated that

biochemical compounds and Chl a were the main factors explaining benthic

macrofauna distribution in the intertidal level. Macroinfauna characteristics and

abiotic factors, such as organic matter and Chl a, were always found to be

higher at the intertidal level, where swash action occurs, than at the supratidal.

The swash zone has been considered a key area controlling macroinfauna from

the intertidal and the importance of the swash climate on the macrofaunal

assemblages and on the food available present in sediments of sandy beaches

has been recently stated (Incera et al., 2006).

Multiple regression analyses were in line with the results obtained, a

positive correlation between sedimentary organics and macroinfauna

characteristics, such as biomass, macrofauna abundance and abundance of

polychaetes and crustaceans, was found. These analyses showed the existence

of tight relationships between macroinfauna and food quality but the

distributions of factors such as pigment and nutrients are often depth

dependent. Therefore, caution is called for when correlating depth profiles of

different variables. The conclusions from this study should be treated as

predictions that point to the most important experimental manipulation to be

conducted next. This study showed that macrofauna from estuarine sheltered

beaches is not just driven by physical forces but also by the distribution of its

primary food sources. Macrofauna organisms showed preferences both in

vertical and horizontal ranges suggesting a specific distribution which is related

to specific sensitivity by several abiotic factors, including food availability. The

assessment of vertical and horizontal variability and the relative structure of the

macroinfauna community displayed a strong heterogeneity over time,


229

suggesting that macrofauna in estuarine beaches can be related to complex and

unpredictable factors.

5.7.3.2. Effect of invasive algal wrack in macrofauna assemblages in an

exposed sandy beach

Several studies have examined macrophytes brought to beaches by the

sea and stay temporally as wrack debris in the intertidal. These may be salt-

marsh grasses from estuaries, seagrasses from sheltered subtidal sands, or

macroalgae from rocky shores and subtidal reefs. Most beaches receive a small

amount of such inputs, but in some situations the input may be substantial,

especially after winter storms. Wrack is fed upon directly by some organisms

associated with the dune and drift line, such as talitrids amphipods, isopods,

and insects. This material dominates the sandy beach food chains (for review,

see Colombini and Chelazzi, 2003). However, much decomposition is

accomplished by bacteria, and breakdown can be completed in days to weeks,

depending on the debris (Griffiths et al., 1983; Jędrzejczak, 2002). Wrack also

acts as a refuge supply for the supralittoral fauna, ovoposition and larval

development, either for terrestrial or marine invertebrates.

It is clear that algal wrack indeed promotes an increase in population

abundances of sandy beach macrofauna, either because it provides their main

food source or refuge from environmental conditions and/or predation. In

Chapter 6, the major components of the algal wrack were dipteran flies (mainly

larvae) and tenebrionid and staphylinid beetles. Talitrid amphipods are

considered primary macroinfaunal colonisers of fresh algal wrack stranded on

sandy beaches. The scarcity of these amphipods in the area of study might be

related to the specific environmental conditions during the sampling period,

when high temperatures and very strong winds following the first sampling day

dried off most of wrack patches. Previous studies have shown that locomotory

behaviour of talitrids is strongly influenced by weather conditions such as

relative humidity of air, sand temperature and moisture (e.g. Colombini et al.,

1998; Fallaci et al., 1999).


230

The presence of wrack made of invasive macroalgae (Sargassum

muticum) and wrack made of native macroalgae (Saccorhiza polyschides)

promote two different colonisation patterns. The total number of individuals

was larger in patches of S. polyschides than in patches of S. muticum. This

difference in abundance became more evident within 3 days and diminished

over time, although the sharpest differences occurred in the abundance of

several larvae species. It is interesting to highlight that the number of species

and diversity reached higher values in patches of S. muticum than in S.

polyschides on day 3, but this pattern was reverted from day 7 onwards. At the

beginning of this study, the largest abundances in native wrack patches were

related mainly to larvae belonging to the same species, i.e. Anthomyiidae sp 1.

This dominance can explain the small number of species and low diversity

found in native patches at that time. After day 3, larvae abundance dropped,

and both number of species and diversity increased to reach higher values in

patches of S. polyschides than those in S. muticum. Reproduction, larval

settlement or recruitment can be stimulated by the presence of the wrack debris

(Bolam et al., 2000). In the case of flies, adults are insignificant consumers of

algae-exuded substances, but lay eggs in wrack which may contribute greatly to

the breakdown of kelp tissue as a result for their own feeding activity and

through the spread of microorganisms. It seems that wrack made of native

macroalgae is a more suitable habitat and represent a very important feeding

source. Maybe the physical structure and/or specific microclimatic conditions

in native wrack patches might favour chiefly dipteran oviposition and breeding.

Most species colonised the wrack patches quickly but different species

showed different patterns of colonization suggesting that life-history attributes,

such as their colonising and competitive abilities, and mobility of different

taxa, may be important factors contributing to explain such patterns.

Herbivorous species such as Cercyon littoralis colonised all the patches rapidly

and remained present over time. The scavenger P. cadaverina that feeds on

different sources of organic debris peaked on day 7. Carnivorous species (H.

rubripes and A. variana) were early colonisers in both types of wrack, but their

abundances were larger on days 7 and 21. This increase in abundance of


231

predators may be related to the increase in abundance of larvae and immature

individuals which are likely to serve as food source. Although the species

found in the two types of wrack patches are different there was not a consistent

trend across space and/or time. This suggests that other factors apart from type

of wrack are influencing the patterns of colonization and succession. For

example, variation may be related to progressive microclimatic changes of

wrack accumulations due to their different position across the beach.

There were some evidences to support the hypothesis that macrofaunal

assemblages changed in response to wrack type, but patterns varied across

space and time. Results indicated that carbohydrates, organic matter and

chlorophyll a variables best described the observed patterns in macrofaunal

assemblages. Moreover, temperature and humidity had some influence in the

presence of some species in wrack patches. Slight differences in these

parameters could affect colonization by different invertebrate species, because

variation in microclimatic conditions of wrack deposits have been considered

an important factor affecting behaviour, locomotory activity and distribution of

several arthropod species inhabiting beach-dune systems (Colombini et al.,

1998). Nutritional value of wrack (mostly carbohydrates, lipids and organic

matter content) differed between the two types of wrack. In most cases, the

carbohydrates, lipids and organic content were greater in patches of S. muticum

than in patches of S. polyschides. In contrast, the chlorophyll a concentration

(used as a proxy of benthic microalgae biomass) was greater in patches of S.

polyschides than in patches of S. muticum in most cases. In fact, a greater

concentration of benthic microalgae in S. polyschides might be related to a

lesser content of polyphenols in laminarian seaweeds since process of

colonization in these organisms is related to the polyphenols content. Brown

algal polyphenolic compounds protect plants from pathogens or damage by UV

radiation, while deterring feeding by herbivores (Van Alstyne et al., 1999).

Nutrients can be released from wrack patches and are likely to be used by

microphytobenthos, which may play a major role in the flux of nutrients in the

sediments, representing a direct or indirect source of food for some

invertebrates (Rossi and Underwood, 2002).


232

Apart from differences in nutritional value and microclimatic

conditions between the two types of wrack, differences in structure, i.e.

complexity, of wrack patches might play an important role in variability of

macrofaunal assemblages. Different structure due to morphological differences

of seaweeds causes variability in quality of habitat, i.e. shelter from predation.

In some cases, preference of invertebrates for certain seaweed species seems to

be related to factors such as availability, habitat provision, or refuge from

predation rather than nutritional value (Wakefield and Murray, 1998).

The results obtained in this study indicate that replacement of native

wrack deposits by exotic wrack may have important effects on macrofaunal

assemblages on sandy beaches. A change in the type or amount of seaweed

wrack entering a beach may alter the macrofaunal assemblages and ecosystem

function.

5.7.4. Open questions.

The most prominent question that arises from this study on sandy beach

macrofauna reported in this thesis is what happens at different temporal scales.

As faunal zonation is dynamic, temporal studies are needed for a full picture of

zonation patterns (Chapters 2, 3, and 4), requiring intensive sampling; f.i.

bimonthly during a year, to provide unbiased estimates. Although the sampling

load would be very high, temporal replication, following seasonal trends, is a

main factor to have in mind when variability is found in the results. In fact,

there might be as much variability from one week to another as from one

season to another. The simplest solution is to sample more often, either to

detect the temporal trend or to create replication while sampling in an attempt

to avoid confusion in the interpretation of the data.

Concerning macrofauna distribution through the intertidal, the cross-

shore variability of benthic community of sandy beaches was well

accomplished in Chapter 3. The along shore distribution of macrofauna on a

beach is one of the least studied topics in sandy beach research, and only

limited information is available. In general, macrofaunal populations are most

developed in the middle of a beach, with a unimodal bell-shaped distribution


233

towards both sides. Although the sites chosen within each beach studied can be

considered representatives of the whole intertidal, a selection of different sites

within the same beach could underline some of the causes of macrofauna

zonation variability. Once again, sampling load would be excessive.

In Chapter 4, along-shore distribution was widely covered due to the

short length of the intertidal studied. Concerning horizontal distribution, three

representative tide levels were chosen. Two intertidal affected by the swash

climate, and one supratidal not affected by the swash climate. By sampling

these three levels we were able to study specific aspects of the three most

representative environments of the beach: the low swash environment, having

an assemblage of typically intertidal species; the truly intertidal part of the

beach; and the supratidal zone, where only resistant and semiterrestrial species

are present. It is important to point out that both exposed and sheltered beaches

are geographically associated, exposed at North and sheltered at South (Chapter

4). With this design, spatial and exposure effects may be confounded. Although

there is an obvious geographical separation between sheltered and exposed

beaches, previous studies indicated that the values for number of species,

biomass and chlorophyll a were higher in beaches from the NW coast of Spain

due to the influence of the seasonal upwelling event located in this same area of

the Iberian Peninsula (Lastra et al., 2006). However, a thorough study of sandy

beaches with different exposure rate should include intertidal habitats with the

same exposure rate in the same area of study. For instance, it would be

interesting to include three exposed and three sheltered sandy beaches from the

same location and compare them with the same number and type of beaches

from another location. Furthermore, the lack of fit between some biochemical

compounds and quantitative characteristics of macroinfauna may be clarified

when including seasonal sampling.

The lack of seasonal sampling in previous Chapters was partially

solved in Chapter 5, where seasonal variability in benthic macrofauna

distribution and food availability was studied. However, no clear seasonal

pattern was found in macrofauna and sedimentary organic characteristics

suggesting that macrofaunal assemblages are controlled by complex and


234

unpredictable factors. The influence of anthropogenic impacts, very difficult to

assess or predict, can be main factors influencing seasonal variability. It would

be more desirable to study locations without direct human impacts, in “wild

conditions”, or select a cluster of beaches, with the same morphodynamic

conditions from different geographical locations to clarify natural seasonal

variability from more complex external effects.

Studying the impact of a long-term change on macrofauna is

logistically very difficult. A field monitoring campaign over many years, with a

reasonable resolution (monthly or bimonthly), should be combined with

mesocosmos experiments on indicator species. Additionally, keeping

macrofauna in laboratory conditions might prove very valuable for additional

studies. Studying environmental factors in situ, such as swash climate, cannot

reveal all of the information about the mechanisms behind the behaviour and

distribution of sandy beach macrofauna. To understand the underlying

mechanisms, it is crucial to have independent control over the different

physical parameters, which explains the need for laboratory experiments. So

far, experimental work on macrofauna using aquariums or tanks allow work on

crucial factors such as type of sediment, beach slope, swash climate (period,

velocity) or indicator species. For instance, estimates of the feeding rates and

food preferences of different macrofauna species would be beneficial from

laboratory experiments. The pioneer studies carried out in Lastra et al., 2007 (in

press) showed a first attempt to estimate the feeding rates and preferences of

Talitrid amphipods and their impact on food sources. This was accomplished

by a series of field and laboratory experiment evaluating different factors such

as wrack species, consumers size and temperature effect. This study elucidated

species behaviour from different geographical areas to compare the specific use

of food sources such as wrack macroalgae by these organisms. Experimental

manipulation to test hypotheses about physical structure of wrack and stable

isotope analyses to provide clues about the origin of invertebrate’s food sources

and trophic flows in beaches may be the next step.

It is important to have in mind the effect of invasive species in future

studies because the replacement of native species by exotic organisms may


235

have important effects on macrofaunal assemblages on sandy beaches. The

effect of the invasive seaweed S. muticum may have an effect that is spread

away from the points of invasion, i.e. intertidal and subtidal rocky shores. An

assessment of impact on different marine ecosystems may be important criteria

in assessing the impact of this invasive species and the prioritization of exotic

management (see Chapter 6).

The assemblages supported by beach-cast macrophytes are important

prey sources commonly exploited by a number of shorebirds and, therefore, are

a basic element of food webs acting as an important link between marine and

terrestrial ecosystems (Hubbard and Dugan, 2003; Orr et al., 2005). Wrack-

cleaning activities done on beaches used as recreational areas might have

important cascading effects on the species diversity and abundance, and

consequently affect both marine and terrestrial habitats.

It is important to emphasise that since correlation does not prove

causation, the conclusions from this thesis should be treated as predictions that

point to the most important experimental manipulation to be conducted next,

not as conclusions to be set in stone.

5.7.5. List of references.

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macroalgal mats on intertidal sandflats: an experimental study. Journal

of Experimental Marine Biology and Ecology 249, 123-137.

Brazeiro, A., Defeo, O., 1996. Macroinfauna zonation in microtidal sandy

beaches: it is possible to identify patterns in such variable

environments. Estuarine, Coastal and Shelf Science 42: 523-536.


in sandy beaches: what are the underlying factors? Marine Ecology

Progress Series. 224: 35-44.

Colombini, I., Aloia,A., Fallaci,M., Pezzoli,G., Chelazzi,L., 1998. Spatial use

of an equatorial coastal system (East Africa) by an arthropod

community in relation to periodically varying environmental

conditions. Estuarine, Coastal and Shelf Science 47: 633-647.

Colombini, I., Chelazzi, L., 2003. Influence of marine allochthonous input on

sandy beach communities. Oceanography and Marine Biology: An

Annual Review 41, 115-159.

De la Huz, R., M. Lastra, M., López, J. 2002. The influence of sediment grain

size on burrowing, growth and metabolism f Donax trunculus L.

(Bivalvia: Donacidae): Journal of Sea Research 47: 85-95.


236

Defeo, O., Gómez, J., Lercari, D. 2001 Testing the swash exclusion hypothesis

in sandy beach populations: the mole crab Emerita brasiliensis in

Uruguay. Marine Ecology Progress Series 212: 159-170.

Defeo, O., Gómez, J. 2005. Morphodynamics and habitat safety in sandy


Ecology Progress Series. 293: 143-153.

Defeo, O., McLachlan, A. 2005 Patterns, processes and regulatory mechanisms

in sandy beach macrofauna: a multi-scale analysis. Feature article:

Review. Marine Ecology Progress Series. 295: 1-20.

Degraer, S.,Mouton, I., de Neve, L., Vincx, M. 1999. Community structure and

intertidal zonation of the macrobenthos on a macrotidal, ultra-

dissipative sandy beach : summer-winter comparison. Estuaries 22:

742-752.

Dugan, J., Jaramillo, E., Hubbard, D.M., Contreras, H., Duarte, C., 2004.

Competitive interactions in macroinfaunal animals of exposed sandy

beaches. Oecologia 139: 630-640.

Fabiano, M., Danovaro, R., and Fraschetti, S. 1995. A 3-year time series of




Fallaci, M., Aloia, A., Audoglio, M., Colombini, I., Scapini, F., Chelazzi, L.,

1999. Differences in behavioural strategies between two sympatric

talitrids (Amphipoda) inhabiting an exposed sandy beach of the French

Atlantic Coast. Estuarine Coastal and Shelf Science 48: 469-482.

Griffiths, C.L., and Stenton-Dozey, J.M. 1981. The fauna and rate of

degradation of stranded kelp. Estuarine Coastal and Shelf Science 12:

645-653.

Hacking, N. 1998. Macrofaunal community structure of beaches in northern

New South Wales, Australia. Marine Freshwater Research 49: 47-53.

Hubbard, D.M., Dugan, J.E., 2003. Shorebirds use o fan exposed sandy beach

in southern California.Estuarine, Coastal and Shelf Science 58S: 41-54.

Incera, M., Lastra, M., and López, J. 2006. Effect of swash climate and food

availability on sandy beach macrofauna along the NW coast of the

Iberian Peninsula. Marine Ecology Progress Series 261: 85-97.

Jaramillo, E., McLachlan, A. 1993. Community and population response of the



37: 615-624.

Jaramillo, E., McLachlan, A., Coetzee, P., 1993. Intertidal zonation patterns of

macroinfauna over a range of exposed sandy beaches in south central

Chile. Marine Ecology Progress Series 101, 105-118.

Jędrzejczak, M.F., 2002. Stranded Zostera marina L. vs wrack fauna


term pilot study. Part I. Driftline effects of fragmented detritivory,

leaching and decay rates. Oceanologia 44(2): 273-286.

Kelaher, B.P. and Levinton, J.S. 2003. Variation IN detrital enrichment causes

spatio-temporal variation in soft-sediment assemblages. Marine



237

Lastra, M., McLachlan, A., 1996. Spatial and temporal variations in

recruitment of Donax serra Röding (Bivalvia: Donacidae) on an

exposed sandy beach of South Africa. Revista Chilena de Historia

Natural 69: 631-639.

Lastra, M., de La Huz R., Sánchez-Mata, A.G., Rodil I.F., Aerts K., Beloso S.,

López J., 2006. Ecology of exposed sandy beaches in northern Spain:

environmental factors controlling macrofauna communities. Journal of

Sea Research 55: 128-140.

Lastra, M., Dugan, J., Page, M., Hubbard, D., Rodil, I.F., (in press). Processing

of allochthonous macrophyte subsidies by sandy beach consumers:

estimates of feeding rates and impacts on food resources. Marine

Biology.

McArdle, S., McLachlan, A., 1992. Sand beach ecology: Swash features


McLachlan, A., 1980. The definition of sandy beaches in relation to exposure:

simple rating system. South African Journal of Science 76: 137-138.


exposed intertidal sands. Journal of Coastal Research 1: 57-71.

McLachlan, A., Jaramillo, E., Donn, E., F. Wessels 1993. Sandy beach

macrofauna communities and their control by the physical

environment: a geographical comparison. Journal of Coastal Research

15: 27-38.

McLachlan, A., Jaramillo, E., 1995. Zonation on sandy beaches. Oceanography

and Marine Biology 33, 305-335.

McLachlan, A., Dorvlo, A. 2005. Global patterns in sandy beach macrobenthic

communities. Journal of Coastal Research 21(4): 674-687.


Amsterdam.

Orr, M., Zimmer, M., Jelinski, D.E., Mews, M., 2005. Wrack deposits on

different beach types: spatial and temporal variation in the pattern of

subsidy. Ecology 86: 1496-1507.

Rossi, F., Como, S., Corti, S. and Lardicci, C. 2001. Seasonal variation of a

deposit-feeder assemblage and sedimentary organic matter in a

brackish basin mudflat (Western Mediterranean, Italy). Estuarine

Coastal Shelf Science 58: 353-366.

Rossi, F., Underwood, A.J. 2002. Small-scale disturbance and increased


experimental burial of wrack in different intertidal environments.

Marine Ecology Progress Series 241: 29-39.

Van Alstyne, K.L., McCarthy, J.J., Hustead, C.L., Duggins, D.O., 1998.

Geographic variation in polyphenolic levels of Northeastern Pacific

kelps and rockweeds. Marine Biology 133: 371-379.

Wakefield, R.L., Murray, S.N., 1998. Factors influencing food choice by the

seaweed-eating marine snail Norrisia norrisi (Trochidae). Mar. Biol.

130, 631-642.

Wooster, W.S., Bakun, A., McLain, D.R., 1976. The seasonal upwelling cycle

along the eastern boundary of the North Atlantic. Journal of Marine

Research 34(2): 131-141.

PARTE V. DISCUSIÓN GENERAL.

(Según el acuerdo de 18/06/04 firmado por la Comisión de Doctorado de la

Universidad de Vigo acerca del idioma en que puede escribirse la Tesis doctoral).

Parte V Discusión general

239

5.7.1. La ecología de playas de la costa norte de la Península Ibérica.

Durante el periodo de este estudio, se ha investigado un amplio número

de playas a lo largo de la línea costera del norte de España. Estas playas han

sido muestreadas de forma cuantitativa lo que nos ha proporcionado la

información básica para obtener una descripción general de la estructura de la

comunidad macrofaunística de las playas de esta región. La gran mayoría de

playas que nos encontramos en esta costa son intermareales expuestos (sensu

McLachlan, 1980) a la acción oceánica; sometidas a un régimen mesomareal

(entre 2 y 4 m.), lo cual lo aleja de la gran mayoría de estudios tradicionales de

playas micromareales (e.g. Jaramillo et al., 1993; McLachlan et al., 1993). En

términos de tipología, las playas expuestas de esta región son

predominantemente intermedias con un promedio de pendiente muy variable

(1/22 a 1/52) y un tamaño de grano de tipo medio no muy bien clasificado que

se va haciendo progresivamente más fino a medida que nos dirigimos a la zona

supralitoral de las playas.

La costa Norte de la Península Ibérica es una región donde se han

llevado a cabo muy pocos estudios de ecología de playas. Uno de los objetivos

de la presente tesis es establecer una base de investigación que sirva como

referencia para futuros trabajos y experimentos. La primera y segunda parte de

esta tesis (ver Capítulos 1, 2 y 3) analizan las características principales de la

ecología y de la estructura de la macrofauna; tales como la riqueza y

composición de especies, la distribución espacial y zonación de la macrofauna

o los efectos de las principales variables ambientales que afectan a la

macrofauna bentónica. Aunque no se ha realizado un seguimiento temporal de

la comunidad macrofaunística de estas playas, lo cual le puede restar algo de

fiabilidad al estudio, el muestreo instantáneo comparativo de diecinueve playas

del mismo tipo y de una misma región nos ofrece un análisis representativo

fundamental de la estructura faunística. El énfasis en el análisis de las variables

ambientales en este estudio se ha centrado en el efecto espacial o en los efectos

que se producen en un periodo corto de tiempo. Sin embargo, hay una

evidencia clara, al menos en las playas micromareales, de que la escala

Part V Discusión general

240

temporal es muy importante en el estudio de la ecología de playas (e.g.

Brazeiro y Defeo, 1996; Degraer et al., 1999; Dugan et al., 2004).

Probablemente la pérdida de replicación en el tiempo de alguno de los capítulos

de este estudio (Capítulos 2, 3 y 4) sea una de las más importantes limitaciones

de esta tesis. Aunque los resultados de estos capítulos sugieren que la

macrofauna está principalmente estructurada en el espacio, la información

obtenida está demasiado limitada como para establecer que la escala temporal

es menos importante en un rango mesomareal de playas de regiones templadas.

Sin embargo, los resultados de los primeros capítulos de esta tesis nos

proporcionan la suficiente confianza como para asumir que abordar estos

estudios con la escala espacial adecuada es al menos tan importante como usar

la escala temporal adecuada.

5.7.1.1. Factores ambientales que afectan a la macrofauna bentónica.

Los patrones de variación de, por ejemplo, la riqueza específica se

explican mejor por el grado de exposición de las distintas playas. Los

resultados obtenidos muestran que el número de especies es el parámetro

biológico más afectado por los parámetros ambientales, aumentando de forma

lineal con el rango mareal y disminuyendo con el aumento en el grado de

exposición. Otro factor biótico importante como es la biomasa de la

macrofauna disminuye exponencialmente con un aumento del tamaño medio

del sedimento. Esto demuestra una de las características de los intermareales

arenosos más y mejor documentadas: la disminución de los factores bióticos

(i.e., riqueza específica, abundancia y biomasa de la macrofauna) cuando

pasamos de un estado de playa disipativo a otro reflectivo (i.e., condiciones de

mayor pendiente y tamaño de grano), así como a una mayor exposición. El

tamaño de grano se vio negativamente relacionado con factores bióticos tales

como la riqueza específica o la biomasa. Hay varias razones para asumir que

esta relación es de tipo causal. Por ejemplo, muchas especies pueden encontrar

difícil o incluso ser incapaces de enterrarse en arenas gruesas (Lastra y

McLachlan, 1996; de la Huz et al., 2002) y por tanto verse en dificultades para

sobrevivir debido al aumento de las posibilidades de ser depredado o barrido


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por el swash. Además, el sedimento más grueso proporciona un sustrato mucho

menos estable y, de forma indirecta, afecta a la fauna debido a su influencia en

el swash y a la permeabilidad del sedimento. La variación del tamaño de grano

dentro de una misma playa puede provocar una zonación intraespecífica como

en el caso del bivalvo Donax trunculus. Los individuos más jóvenes y

pequeños de esta especie se distribuyen más hacia la zona supralitoral con

sedimentos más finos mientras que los adultos, más grandes, lo hacen hacia la

zona baja del intermareal afectada por el swash y con sedimentos más gruesos.

La variabilidad morfodinámica de una playa está determinada por el

rango de sedimento y el cambio en el oleaje pero también hay que incluir el

efecto asociado a las mareas. El rango mareal no se ha incluido en los estudios

tradicionales porque éstos se han venido realizando en playas micromareales.

Sin embargo, en las playas mesomareales de este estudio, este parámetro

influye decisivamente en la estructura de la comunidad. A medida que aumenta

el rango mareal y se hace significativamente más importante que la energía del

oleaje, el número de especies también aumenta. Comprobamos que la

morfodinámica descrita por los parámetros Dean y BSI tiene una escasa

capacidad para predecir las características de la comunidad de las playas de

esta región. La validez de estos parámetros morfodinámicos ha sido demostrada

de forma general en estudios donde se incluyen en el análisis un amplio rango

de tipos de playas, i.e. de reflectivas a disipativas, mientras que en el presente

estudio las playas poseen características morfodinámicas y de exposición muy

similares. Además el parámetro Dean ha sido típicamente utilizado en

situaciones micromareales donde la influencia mareal es escasa o inapreciable,

pero parece ser poco eficaz para cubrir situaciones meso o macromareales. Otro

índice muy utilizado en la ecología de playas, el BSI, ha sido probado con éxito

cuando se comparan áreas con diferente rango mareal (Hacking, 1997) y por

tanto no se puede aplicar a cualquier tipo de estudio, ya que la mayor parte de

ellos se concentran en regiones geográficas limitadas en donde sólo una parte

del espectro de condiciones está presente. Quizás el mejor uso de este índice, al

igual que otros nuevos como el BDI o el BI (ver McLachlan y Dorvlo, 2005),

provenga de la disponibilidad actual de resultados de los estudios de playas de


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distintas regiones, lo que proporciona una base de datos comparable de la

mayoría de tipos de playas y latitudes, a partir de los cuales es posible realizar

estudios de tendencias a un nivel global (e.g. McLachlan y Dorvlo, 2005;

Defeo y McLachlan, 2005).

De forma más general, cuando nos centramos en el estudio de playas de

tipo intermedio, las diferentes características de la comunidad parecen

afectadas por varios factores ambientales. Así, en las playas de este estudio la

variación de la comunidad se explica mejor por el grado de exposición que por

los tradicionales parámetros morfodinámicos o incluso que por la pendiente de

la playa. La exposición representa a varios factores ambientales, confirmando

que la ecología de la macrofauna de playas se ve afectada por un conjunto de

variables y que no existe un único factor ambiental determinante y definitivo.

5.7.1.2. Estructura de la comunidad y zonación de la macrofauna

Los taxones dominantes de estas playas son los comunes a nivel

mundial, siendo los crustáceos el grupo más diverso y abundante, y en menor

número se encuentran los poliquetos y sobre todo los moluscos. El patrón

general de distribución horizontal de la macrofauna confirma el conocimiento

general en ecología de playas: la riqueza de especies aumenta hacia los niveles

inferiores de las playas (e.g. McLachlan y Jaramillo, 1995; McLachlan y

Brown, 2006). La zonación de los intermareales es un fenómeno bastante

estudiado y aunque se han establecido patrones generales para algunos casos

concretos (ver 1.1.2.4. para más detalles) no existe una zonación clara para las

playas y en muchos casos se ha considerado cualquier tipo de división como

artificial en un ambiente que refleja un continuo con superposición de zonas

adyacentes (McLachlan y Jaramillo, 1995; Degraer et al., 1999). Sin embargo

en las playas intermedias de este estudio hemos encontrado alguna evidencia de

una posible división biológica en zonas principales. Quizás el esquema de

zonación más elemental, pero también el más aplicable, se refiera a una típica

zonación dividida en dos zonas principales: una zona estrecha en la parte más

alta de la playa donde se encuentra una típica asociación de especies semi-

terrestres, y por debajo de la cual nos encontramos una zona ocupada por una


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asociación de diversas especies verdaderamente marinas (e.g. McLachlan y

Jaramillo, 1995, McLachlan y Brown, 2006). Las características del perfil de

estas playas muestran una influencia directa sobre la estructura y distribución

de las comunidades macrofaunísticas. Las playas estudiadas muestran un perfil

roto de forma abrupta en el nivel mareal medio, que divide el intermareal en

una parte supralitoral de mayor pendiente seguida por una planicie litoral en la

parte baja de la playa supeditada a la acción del oleaje y del swash. La zona

supralitoral es la más evidente y los diversos análisis efectuados indican un

claro límite entre esta parte de la playa y el resto del intermareal siguiendo la

forma del perfil de la playa. Esta zona, que posee una comunidad característica

del supralitoral, es habitual en todas las playas expuestas (McLachlan y

Jaramillo, 1995). El perfil de playa que nos hemos encontrado en este estudio

parece que concuerda bien con esta descripción. Aunque se puede encontrar

alguna subdivisión de la parte baja del intermareal (dos o incluso tres zonas),

creemos que establecer una delimitación clara de zonas no es plausible con este

perfil de playa tan particular.

5.7.1.3. Relación entre la macrofauna y las variables ambientales

La abundancia y distribución de la macrofauna de playas dependen de

varios factores físicos y biológicos. Aquellos factores físicos considerados

tradicionalmente como los más influyentes en la distribución de la macrofauna

serían el rango mareal, el tamaño de grano del sedimento, la exposición, la

acción del swash y la dinámica de acreación y erosión (e.g. Brazeiro, 2001,

McLachlan y Dorvlo, 2005). Todos estos factores están ligados de alguna

manera a la morfodinámica de las playas. Los resultados obtenidos en esta tesis

indican que parámetros ambientales como la pendiente, la altura de la ola y la

longitud de la playa son los factores ambientales que mejor explican la

variabilidad en la densidad de especies. Los dos primeros factores estarían

relacionados con la morfodinámica que determina las características típicas de

una playa expuesta. Las playas con mayor pendiente y altura de ola presentan

un tamaño de grano más grueso y con características de las playas reflectivas.

El efecto en las variables biológicas producido por la hidrodinámica y la


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morfodinámica de las playas se considera un paradigma en ecología de playas

(Defeo y McLachlan, 2005). Hay una tendencia a la disminución del número de

especies a medida que aumentan las características reflectivas de una playa (i.e.

pendiente más pronunciada y mayor tamaño de grano) y su exposición al oleaje

(Jaramillo y McLachlan, 1993). Además, McArdle y McLachlan (1992) han

sugerido que tanto la altura de la ola como la pendiente de la playa son los

factores más relacionados con las características del swash, el cual a su vez es

el factor ambiental que más afecta a la macrofauna de las playas expuestas.

Parece que las especies con una más clara zonación están también mejor

explicadas por las variables ambientales que aquellas especies con límites de

zonación no tan definidos en su distribución a lo largo del perfil de las playas.

El hecho de no encontrar un patrón claro de influencia de los factores

ambientales sobre la estructura de la comunidad y no encontrar tendencias

significativas entre el swash y el estado morfodinámico con la macrofauna nos

confirma que las comunidades en las playas de esta región están controladas no

sólo por un conjunto de factores ecológicos sino también por otros factores que

pueden ser más dependientes de las condiciones oceanográficas y de los

procesos costeros. A pesar del continuo geográfico que representan las 19

playas de este estudio, las características de la masa de agua a lo largo de la

costa norte española están determinadas por variaciones de la productividad a

diferentes escalas espaciales. Creemos que las diferencias faunísticas

encontradas entre las playas son, en gran parte, debidas al gradiente de

concentración de clorofila de esta región y no sólo a posibles diferencias físicas

de los intermareales. La existencia de un evento de resurgencia común a lo

largo del límite Este del Atlántico Norte en las coordenadas 10º y 44º N y

centrado en el Noroeste de la costa de España (Wooster et al., 1976) puede

estar relacionada con las diferencias faunísticas encontradas a lo largo de

nuestro gradiente de playas (Oeste-Este). La resurgencia tiende a producir un

flujo neto de agua de profundidad rica en nutrientes que llega a la costa norte

española generando un proceso de fertilización que aumenta la producción

primaria y parece que este efecto se ve diluido a medida que nos movemos

hacia el Este a lo largo de la costa norte de España (Lastra et al., 2006). Por


245

tanto, parece razonable pensar que el aumento de la abundancia

macrofaunística en las áreas próximas a este evento se deba a un aumento de la

disponibilidad de alimento debida al aumento en la productividad.

5.7.2. La importancia de la exposición en la macrofauna de playas:

condiciones hidrodinámicas y disponibilidad de alimento.

Las comunidades macrofaunísticas que viven en los intermareales

arenosos se mantienen casi enteramente gracias a los aportes externos de

materia orgánica ya que muy poca producción primaria se genera en la playa.

En la mayor parte de las regiones templadas, las fuentes principales de materia

orgánica exógena son el fitoplancton y las algas macrófitas. Dependiendo de la

cantidad y calidad del alimento disponible en el intermareal, la estructura de la

comunidad macrofaunística y sus relaciones tróficas puede variar. Las playas

carecen de algas macrófitas asociadas al sedimento que sirvan de alimento y/o

protección a la macrofauna, excepto en casos especiales de playas estuáricas

muy protegidas con praderas de fanerógamas. Las cadenas tróficas en los

intermareales empiezan y acaban principalmente en el mar pero incluso el

ecosistema terrestre puede desarrollar un papel importante en la disponibilidad

de alimento. Los resultados obtenidos en la parte III de esta tesis sugieren que

la comunidad macrofaunística, en términos de abundancia, biomasa y riqueza

específica es más compleja y diversa en playas protegidas que en las más

expuestas siguiendo la premisa tradicional de estudios anteriores que reflejan

una disminución de las variables bióticas con el aumento de la exposición

(Jaramillo y McLachlan, 1993; McLachlan et al., 1993).

5.7.2.1. Características de la macrofauna de playas en un gradiente de

exposición

El supralitoral de las localidades estudiadas muestran una riqueza de

especies baja ya que las condiciones son más duras para la macrofauna

típicamente marina, y el dominio es casi exclusivo de los crustáceos;

básicamente anfípodos talítrido. Este tipo de organismos están adaptados para

evitar la desecación (McLachlan, 1990; Little, 2000) por lo que son mayoría en


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este nivel del intermareal. Además, en el caso de las playas expuestas, estos

crustáceos encuentran en el supralitoral un lugar estable para establecerse

(Defeo y Gómez, 2005) mientras que disminuyen en número hacia el swash.

De hecho, en este estudio, no se han encontrado diferencias significativas entre

los supralitorales de las playas expuestas y los de las protegidas. La mayor

parte de las especies supralitorales han sido consideradas dependientes de las

algas varadas que llegan a las playas asociadas a distintintos procesos

oceanográficos (ver Capítulo 6). Los intermareales protegidos que hemos

estudiado presentan unas condiciones ambientales más favorables y con una

mayor estabilidad que las playas expuestas, lo que se refleja en los valores

significativamente más altos de abundancias, biomasas e incluso de la riqueza

específica cuando se comparan con los niveles medios e inferiores de los

intermareales expuestos. Los resultados obtenidos aquí apoyan la hipótesis de

exclusión del swash, la cual predice que los organismos de los niveles

inferiores de las playas expuestas se verán excluidos por el clima del swash

(ver sección 1.1.2.3), pero no a nivel supramareal donde la acción del swash es

inapreciable. Se ha propuesto además que los organismos de este nivel son

relativamente independientes del régimen del swash, dando lugar a una serie de

respuestas variables a los cambios en el tipo de playa (Defeo y Gómez, 2005).

Tanto las características del swash como del tamaño del sedimento

definirán la repuesta de la macrofauna. El grupo de los moluscos y el de los

poliquetos son los más afectados a medida que aumenta la dureza y la

exposición del sistema intermareal. Ambos grupos aumentan sus abundancias

en los niveles inferiores del intermareal donde se presupone la existencia de

unas condiciones físicas más estables siguiendo la hipótesis del hábitat

favorable (Defeo et al., 2001). En el caso de las playas expuestas estudiadas no

se encontraron especies pertenecientes al grupo de los moluscos y muy pocos

poliquetos. Este tipo de intermareal con condiciones físicas más duras y tamaño

de grano más grueso tienen un efecto negativo en la capacidad de

enterramiento, tasa de respiración y alimento de bivalvos filtradores, como es el

caso de Donax trunculus. En las playas más protegidas, con menor

hidrodinamismo, se ve favorecida la acumulación de materia orgánica,


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fundamentalmente de origen exógeno, disponible para los depositívoros

bentónicos, sobre todo los poliquetos, que se convierten en el grupo dominante

en estos intermareales.

5.7.2.2. Efecto de la composición bioquímica de la materia orgánica en

la macrofauna

En este estudio se han encontrado diferencias significativas en las

concentraciones de materia orgánica entre las playas protegidas y las expuestas,

probablemente relacionado con las características morfodinámicas más suaves

de estos intermareales. Además, se ha encontrado una relación inversamente

proporcional entre la pendiente y el grado de exposición de la playa y la

concentración de BPC en el sedimento. Las playas expuestas de este estudio

muestran un ligero aumento en el tamaño de grano y en la pendiente del

intermareal por lo que parece que las concentraciones de BPC siguen un patrón

similar al de los organismos, que aumentan en número desde las playas

expuestas de pendiente más pronunciada a aquellas más protegidas y con

pendientes más suaves.

La aportación más importante de la composición bioquímica al

sedimento intermareal de este estudio, ya sea expuesto o protegido, se debe a

las proteínas y ocurre de forma más significativa en los niveles inferiores

próximos al swash. El hecho de que las proteínas sean la fracción dominante

del BPC y que los carbohidratos muestren los valores más bajos indica que la

materia orgánica de estas localidades tiene un posible origen de producción

reciente o incluso autóctono. De hecho la relación PROT:CHO, que refleja la

edad de la materia orgánica del sedimento, es lo suficientemente alta como para

suponer que la mayor parte de dicha materia es de producción reciente y que

las proteínas no son limitantes para el crecimiento de los consumidores del

intermareal (Fabiano et al., 1995). Sin embargo, el porcentaje promedio de

proteínas encontrado en las localidades protegidas (63,4 %) es menor que en las

expuestas (80,2 %) mientras que hay una mayor cantidad de materia orgánica

en las playas protegidas, lo que puede indicar una mayor influencia de la

materia orgánica exógena en estos intermareales. Parece que a medida que


248

disminuye el grado de exposición del intermareal éste se convierte en lugar de

acumulo de materia orgánica (ver Capítulo 5) mientras que las playas expuestas

dependen más de los aportes externos esporádicos como por ejemplo las algas

varadas en el intermareal (ver Capítulo 6).

La disponibilidad final de materia orgánica será el resultado de la

interacción entre los procesos físicos y biológicos que tengan lugar en el

intermareal. Los resultados de este estudio sugieren que el control de la

macrofauna de playas no está determinado exclusivamente por el ambiente

físico y, aunque éste pueda ser un factor fundamental, otros factores

ecológicos, incluyendo la composición bioquímica de la materia orgánica en el

sedimento van a influir también en la estructura de la comunidad

macrofaunística.

5.7.3. El papel de la disponibilidad de alimento en la estructura de la

comunidad de playas: patrones espaciales y temporales.

En la parte IV de esta tesis se estudiaron en dos playas con diferente

grado de exposición el efecto que tiene la disponibilidad de alimento en la

estructura de la comunidad bentónica. En el Capítulo 5 se discuten los

resultados de un estudio realizado en una playa estuárica protegida a lo largo de

dos años, teniendo en cuenta el valor nutricional de la materia orgánica

sedimentaria y su relación con la macrofauna bentónica. Dada la importancia

de la materia orgánica exógena en las playas, el Capítulo 6 presenta un estudio

de estos aportes en forma de algas varadas y como afectan a la comunidad

faunística de un intermareal expuesto. Con estos dos estudios pretendemos

identificar el papel que tienen los aportes de materia orgánica en la variabilidad

observada en la macrofauna de intermareales.

5.7.3.1. Variabilidad estacional en la distribución de la macrofauna

bentónica y de la disponibilidad de alimento en una playa estuárica

protegida.

El análisis temporal de la distribución de la macrofauna bentónica en

una playa estuárica protegida (Barraña) nos demuestra que los niveles mareales


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estudiados presentan una diferente diversidad faunística. Poliquetos y moluscos

aparecen principalmente en el nivel intermareal y los crustáceos tienden a

situarse en los niveles más altos de la playa ya que son menos susceptibles a la

desecación. Además de a nivel horizontal, se han encontrado claras diferencias

en la distribución vertical de la macrofauna. Esto puede ser debido a las

diferencias en las características del sedimento, como el tamaño de grano o la

compactación, que pueden condicionar la capacidad de enterramiento de los

organismos. Sin embargo, las características del sedimento no son capaces de

explicar por sí solas las diferencias encontradas en la distribución de la fauna

bentónica. La distribución en profundidad de estos organismos podría

explicarse mejor por la presencia y posición de la discontinuidad del potencial

redox (RPD) ya que los organismos bentónicos son dependientes del oxígeno

disuelto para respirar. El RPD en esta playa se encontró en el límite de los 5-10

cm que representaba a su vez la franja de mayor concentración de la

macrofauna (75%).

Los intermareales protegidos presentan óptimas condiciones

ambientales para la macrofauna en términos de humedad, temperatura y aporte

alimenticio. El bajo hidrodinamismo hace que el intermareal protegido sea más

independiente de las condiciones físicas que cualquier playa expuesta y la

macrofauna bentónica se ve favorecida por las acumulaciones de la materia

orgánica (Defeo et al., 2001). El nivel medio de este intermareal es el más rico

en términos de abundancia y riqueza específica y también destaca por la

presencia de concentraciones máximas de BPC; i.e., alimento disponible. El

perfil característico de esta playa, junto a las condiciones ambientales más

favorables aumenta la presencia de la materia orgánica y del contenido en agua

en el nivel medio. Estas condiciones pueden fomentar la abundancia y la

riqueza faunística en este parte de la playa, en comparación con el nivel más

bajo del intermareal o el supralitoral. La mayor parte de las especies que se

encontraron en el intermareal pertenecen al grupo de los depositívoros,

favorecidos por la mayor acumulación de materia orgánica en el sedimento

durante el invierno y la primavera. Los depositívoros son organismos capaces

de explotar los recursos de forma rápida y eficiente y un aumento de su


250

abundancia se ha relacionado con un aumento en la concentración de proteínas

(Rossi et al., 2001). Por otro lado, los organismos suspensívoros se encuentran

restringidos a la parte más baja del intermareal ya que no resisten largos

periodos de exposición.

Durante este estudio se ha encontrado una gran variabilidad en la

estructura y dinámica de la comunidad macrofaunística que podría estar

relacionada con las fluctuaciones en la disponibilidad y en la calidad de los

recursos alimenticios. Una parte importante de la materia acumulada en esta

playa pertenece a la porción más lábil y las proteínas, a su vez, fueron la

fracción mayoritaria de dicha porción, lo que implica que la materia orgánica es

en su mayoría de producción reciente. El aumento en proteínas, sobre todo en

invierno, provoca un incremento en la calidad del alimento disponible y se

puede relacionar de forma directa con aportes de origen exógeno que son más

habituales en esta época del año. El descenso en la concentración de proteínas y

de la relación PROT:CHO en la época estival y comienzos del otoño puede

deberse a la disminución en el aporte marino, aumento de las temperaturas y de

la radiación solar típicas de esta estación. Durante este periodo disminuye el

aporte de detritus orgánico en forma de algas y aumenta la fracción refractaria

de la materia orgánica. El aumento de procesos de descomposición en verano

puede ser el responsable principal de la disminución de la fracción más lábil de

la materia orgánica, lo que sugiere una menor disponibilidad de recurso

alimenticio y un aumento de materia orgánica vieja causada por la

descomposición de las algas varadas. Durante el invierno se pueden producir

aportes exógenos episódicos que provocan la acumulación de algas varadas en

los intermareales introduciendo materia orgánica nueva. Algunos animales

bentónicos se benefician de estos a portes clave.

La concentración de clorofila en el sedimento presenta picos de

abundancia en invierno y los valores particularmente elevados podrían

relacionarse con la deposición de algas y las bajas tasas de descomposición

durante este periodo que pueden generar un ambiente ideal para la

productividad microbiana con un consecuente aumento en la actividad

fotosintética (Kelaher y Levinton, 2003). Las grandes variaciones en algunos


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casos (Enero 1997) son difíciles de explicar y puede que tengan una relación

importante con la presencia puntual de un mayor volumen de algas varadas en

el intermareal y con bajas tasas de descomposición en esta época.

Este estudio muestra la importancia de la disponibilidad de alimento

para la comunidad macrobentónica de las playas. Además, la cantidad y la

calidad del alimento tienen la capacidad de producir un cambio sustancial en la

variación espacio-temporal en la estructura de las asociaciones

macrofaunísticas. Los análisis realizados establecen que tanto la disponibilidad

de alimento como la clorofila son los principales factores que explican la

distribución de la macrofauna en los niveles intermareales. Tanto la

macrofauna como la materia orgánica o la clorofila son más abundantes en el

nivel intermareal donde la acción del swash es más efectiva que en el

supramareal. La importancia del alimento disponible y del tipo de swash se han

establecido recientemente como los factores claves en el control de la

macrofauna de los intermareales de fondos blandos (Incera et al., 2006).

Aunque no podemos establecer un patrón estacional claro, podemos

dilucidar que se produce un aumento en la calidad del alimento disponible en

invierno, debido fundamentalmente a la contribución de la concentración de

proteína. En verano y a finales de verano lo que se produce básicamente es una

acumulación de materia orgánica más antigua que disminuye la calidad del

alimento presente en el sedimento.

Los análisis de regresión múltiple corroboran los resultados obtenidos y

muestran una correlación positiva entre la materia orgánica sedimentaria y las

características de la macroinfauna (biomasa, abundancia de la macrofauna,

abundancia de poliquetos y crustáceos). Aunque parece que hay una fuerte

relación entre la macrofauna y la calidad del alimento disponible, no se puede

establecer una causación directa; entre otras cosas porque la distribución de

algunos de los factores, como los pigmentos y los nutrientes, son dependientes

de la profundidad. Las conclusiones obtenidas en esta parte del estudio deben

ser tratadas como predicciones que apunten a la manipulación experimental

como el siguiente paso a dar en el proceso de investigación. Este estudio nos

muestra que la macrofauna de playas estuáricas protegidas no está determinada


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de forma exclusiva por las fuerzas físicas sino que hay una relación

determinada por las fuentes de alimento. La macrofauna en este estudio ha

mostrado una serie de preferencias en su distribución vertical y horizontal en el

intermareal que sugiere que la distribución específica depende de una

sensibilidad concreta hacia varios factores entre los que se incluye la

disponibilidad de alimento. Finalmente, podemos decir que la valoración de la

variabilidad vertical y horizontal y la estructura relativa de la comunidad

macrofaunística muestra una fuerte heterogeneidad temporal lo que sugiere que

la macrofauna de playas estuáricas está relacionada con factores complejos e

impredecibles.

5.7.3.2. Efecto de las algas invasoras sobre la asociación macrofaunística

de una playa expuesta

Varios estudios han examinado el papel de las algas que llegan a las

playas desde el mar y permanecen temporalmente depositadas en el

intermareal. Su origen es diverso, desde praderas de fanerógamas de zonas

estuáricas protegidas a macroalgas procedentes de los intermareales rocosos o

del submareal más próximos. La mayor parte de las playas reciben una pequeña

cantidad de estos aportes, pero en algunas situaciones puede ser sustancial,

especialmente después de las tormentas invernales.

Las algas varadas son usadas como alimento por algunos organismos

asociados a la duna y a la zona de berma de la playa, tales como anfípodos

talítridos, isópodos e insectos, dominando por completo las cadenas tróficas de

las playas expuestas (Colombini y Chelazzi, 2003). Sin embargo la mayor parte

de la descomposición de esta materia la realizan bacterias, lo que puede llevar

mucho tiempo, dependiendo del tipo de material varado en la playa (Griffiths et

al., 1983; Jędrzejczak, 2002). Estos acúmulos de algas pueden servir también

de protección, ovoposición y como lugar de desarrollo de larvas de diversas

especies de invertebrados, tanto marinos como típicamente terrestres.

La abundancia tan significativa de organismos hallados en los

acúmulos de algas en la playa estudiada (Ladeira) demuestra la importancia de

los varamientos en los intermareales expuestos. Los resultados obtenidos


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muestran una abundancia mayoritaria de moscas del orden Diptera

(principalmente larvas) y de coleópteros de las familias Staphylinidae y

Tenebrionidae. Aunque los anfípodos talítridos han sido considerados como los

principales colonizadores y consumidores de las macroalgas varadas (Inglis,

1989; Colombini et al., 2000) nuestro estudio muestra un escaso número de

especies de esta familia. La escasez puede ser debida a las duras condiciones

ambientales que encontramos en la playa durante el periodo de estudio. Las

altas temperaturas y el fuerte viento caracterizaron los días siguientes al

establecimiento del experimento lo que provocó una secado rápido de los

parches de algas. De hecho, estudios previos han demostrado que el

comportamiento de los talítridos está fuertemente influido por las condiciones

climáticas del momento, tales como la humedad del aire y del sedimento así

como la temperatura de la arena (e.g. Scapini et al., 1992; Colombini et al.,

1998; Fallaci et al., 1999).

La presencia de acúmulos de un alga invasora (Sargassum muticum)

frente a los acúmulos conformados por un alga nativa (Saccorhiza polyschides)

promovió dos tipos diferentes de patrones de colonización. En términos de

números totales de individuos los resultados fueron más abundantes en aquellos

parches de S. polyschides que en los parches de S. muticum. Está diferencia fue

muy evidente a los tres días de empezar el experimento y se fue haciendo

menor a medida que pasaba el tiempo y las diferencias más abultadas se

centraron en la abundancia de las especies de larvas. Sin embargo, la diversidad

y el número de especies promedio fueron mayores en los acúmulos de

S.muticum al tercer día, aunque este patrón se revirtió en los días siguientes. Al

comienzo del estudio las mayores abundancias encontradas en los acúmulos de

alga nativa fueron debidas casi exclusivamente a una larva de la misma especie

de mosca, (Anthomyiidae sp 1). Esta dominancia explica el bajo número de

especies y la baja diversidad encontrada en los acúmulos de alga en los

primeros días del estudio. A partir del día tres la abundancia de larvas

disminuyó de forma progresiva y tanto el número de especies como la

diversidad aumentaron hasta alcanzar mayores valores en S. polyschides. La

presencia de estos acúmulos de algas en los intermareales puede estimular la


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reproducción, la puesta de huevos, el establecimiento de larvas o el

reclutamiento de distintas especies (Bolam et al., 2000). En el caso de las

moscas, los adultos son insignificantes consumidores de algas pero encuentran

en estos restos un lugar ideal para la ovoposición. Estos huevos intervendrán

decisivamente en la descomposición de las algas, bien directamente por

consumo de las macrófitas o propagando microorganismos consumidores del

tejido. Por los resultados obtenidos en este estudio, parece que los acúmulos de

algas nativas son un hábitat más apto y constituyen una fuente de alimento para

estas especies. Quizás la estructura física y/o las condiciones microclimáticas

características de esta especie de alga pueden favorecer específicamente la

ovoposición y el desarrollo de larvas de dípteros.

La mayor parte de las especies colonizaron rápidamente los acúmulos

de los dos tipos de algas (87 % en los tres primeros días) pero los patrones de

colonización fueron distintos según la especie y sus hábitos tróficos, siguiendo

las distintas etapas de descomposición y envejecimiento de las algas. Las

especies de herbívoros como el coleóptero Cercyon littoralis colonizan pronto

los dos tipos de parches de algas y permanecieron presentes todo el tiempo de

estudio. Un poco más tarde aparecen especies de carroñeros como el

tenebrionido Phaleria cadaverina y especies de carnívoros (H. rubripes y A.

variana) que presentan su mayor abundancia a los siete días y su presencia se

extiende hasta el final del experimento. Este aumento de especies depredadoras

y carroñeras puede estar directamente relacionado con la abundancia de larvas

e individuos inmaduros que pueden servir de fuente de alimento. Aunque las

especies encontradas en los dos tipos de algas son diferentes, no se ha

encontrado una tendencia consistente a lo largo del tiempo y del espacio. Esto

lo que sugiere es que otros factores además del tipo de alga están influyendo en

los patrones de colonización y sucesión. Por ejemplo, las variaciones

encontradas pueden estar relacionadas con cambios microclimáticos

progresivos debidos a las diferentes posiciones de las algas en la playa; tanto la

zona de duna como la de berma presentan condiciones ambientales variables.

Los resultados de este estudio muestran evidencias suficientes para

apoyar la hipótesis de que la asociación macrofaunística cambia como


255

respuesta al tipo de alga presente en el intermareal. Los carbohidratos, la

materia orgánica e incluso la clorofila son las variables que mejor describen los

patrones de asociación de la macrofauna. Además, tanto la temperatura como la

humedad tienen alguna influencia en la presencia de algunas de las especies en

los parches de algas. Pequeñas variaciones de estos parámetros ambientales

pueden afectar a la colonización por diversas especies, ya que las condiciones

microclimáticas de los depósitos de algas han sido consideradas como factores

que afectan de manera importante el comportamiento de varias especies de

artrópodos (Colombini et al., 1998). El valor nutricional de las algas difiere

entre los dos tipos de algas. En la mayoría de los caso, el contenido orgánico

(fundamentalmente lípidos y carbohidratos) es mayor en S. muticum y la

Clorofila a (indicativo de la biomasa de microalga bentónica) en S. polyschides.

El contenido de microalgas bentónicas puede tener un papel importante en la

regulación de los flujos de carbono a los intermareales costeros (Herman et al.,

2000) y, de hecho, una mayor concentración podría relacionarse con un menor

contenido en polifenoles en las hojas de laminarias (S. polyschides). El

contenido en polifenoles de las algas pardas tiene como funciones proteger al

alga de patógenos o rayos UV e incluso para disuadir a los herbívoros (Van

Alstyne et al., 1999). Los nutrientes liberados de los acúmulos de algas pueden

ser utilizados directamente por el microfitobentos que a su vez pueden regular

el flujo de nutrientes al sedimento ya que representan, directa o indirectamente,

una fuente alimenticia para algunos invertebrados (Rossi y Underwood, 2002).

Aparte de las diferencias en el valor nutricional y en las condiciones

microclimáticas de los dos tipos de algas, la distinta estructura y complejidad

de los parches podría jugar un papel importante en la variabilidad encontrada

en la asociación macrofaunística. La distinta morfología y estructura de las

macroalgas provoca una variabilidad importante en la calidad del hábitat que

afectará a la capacidad de protección o la conveniencia del lugar de

ovoposición. En algunos casos, la preferencia de los invertebrados por ciertas

especies de algas pueden estar relacionadas con factores tales como la

disponibilidad y la provisión de hábitat o de refugio más que por el valor

nutricional (e.g. Wakefield y Murria, 1998).


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Los resultados obtenidos en este estudio indican que un

reemplazamiento de los depósitos de algas nativas varados en las playas por

acúmulos de algas alóctonas puede tener efectos importantes en la estructura de

la comunidad de la fauna de invertebrados. Un cambio en el tipo o cantidad de

alga de arribazón que llega a una playa puede alterar la asociación

macrofaunística y por tanto el funcionamiento del ecosistema en su conjunto.

5.7.4. Cuestiones abiertas.

Quizás la cuestión más importante que surge del estudio realizado

sobre la estructura de la comunidad macrofaunística de playas, resumido en

esta tesis, sea el efecto de las diferentes escalas temporales. Debido a que la

zonación de la fauna es dinámica, estudios temporales de los Capítulos 2, 3 y 4

(correspondientes a las partes II y III) nos podría mostrar un patrón de zonación

más claro, lo que requiere un muestreo temporal intensivo, p.ej.

bimensualmente durante un año, que nos proporcione estimaciones imparciales.

La replicación temporal, siguiendo por ejemplo las posibles diferencias

estacionales, es un factor importante al tener en cuenta la variabilidad de los

resultados obtenidos. De hecho, podría encontrarse más variabilidad de una

semana a otra que entre estaciones por lo que en la mayor parte de los estudios

es recomendable muestrear a menudo, tanto para detectar una tendencia

temporal como para crear réplicas de muestreo en el tiempo (Underwood,

1997) que eviten confusiones en la interpretación de los datos.

En cuanto a la distribución de la macrofauna, el trabajo realizado sobre

la zonación en el Capítulo 3 cubre un aspecto importante de la comunidad

bentónica en playas, como es su distribución a través del perfil intermareal.

Otro punto de interés estaría relacionado con la distribución a lo largo de la

playa. Aunque los lugares escogidos dentro de las playas pueden asumirse

representativos del resto del intermareal, una selección de dos o incluso tres

sitios distintos dentro de cada una de las playas muestreadas podría realzar las

posibles diferencias en la distribución espacial de la macrofauna dentro de un

mismo intermareal. Una vez más, el trabajo de muestrear 19 intermareales


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teniendo en cuenta una mayor variación espacial implicaría un diseño

logísticamente muy complicado.

En el Capítulo 4, la distribución longitudinal de la macrofauna en la

playa estuvo bien cubierta debido a la escasa anchura del intermareal estudiado

para la ocasión. En el caso de la distribución horizontal, los tres niveles

mareales escogidos en este estudio son suficientemente representativos de las

características ambientales específicas del gradiente mareal.

Es importante señalar que las playas expuestas y protegidas

seleccionadas en este estudio están asociadas geográficamente. Con este diseño

el efecto espacial y el de exposición pueden confundirse. Aunque hay una

obvia separación geográfica entre los intermareales expuestos y los protegidos,

estudios previos indican que valores de variables ecológicas tan importantes

como el número de especies, la biomasa y la clorofila a son más altos en las

playas del Noroeste de la costa española debido a la influencia de la

resurgencia estacional localizada en esta zona de la Península Ibérica (Lastra et

al., 2006). Sin embargo, un futuro estudio más exhaustivo de estos

intermareales debería incluir playas de la misma exposición en la misma área

de estudio. Un trabajo estadísticamente más preciso debería incluir al menos

tres playas expuestas y tres protegidas de la misma ría y compararlas con otras

tres playas de cada tipo en otra ría distinta. Además, la pérdida de relación

existente entre alguno de los descriptores bióticos y la composición bioquímica

del sedimento podrían haberse clarificado, una vez más, incluyendo la

variación temporal.

El estudio presentado en el Capítulo 5 solventa alguna de las

incertidumbres creadas por la falta de un estudio temporal más completo. Sin

embargo, la estructura de la comunidad o la composición bioquímica de la

materia orgánica del sedimento de la playa de Barraña no presentan un patrón

temporal característico. La influencia de factores antropogénicos de difícil

análisis y predicción pueden haber sido fundamentales a la hora de conformar

un patrón estacional tan poco claro. Un estudio en localidades sin efectos

antrópicos directos o la comparación de localidades de distintas áreas

geográficas podría contribuir a clarificar algo más los resultados obtenidos. En


258

este estudio se refleja también la importancia de tener datos y antecedentes de

aquellos lugares influidos por las actividades antrópicas y también en

condiciones ideales para ver si se los cambios producidos obedecen a patrones

temporales naturales o a otros efectos externos más complejos.

Un seguimiento del trabajo de campo durante varios años, con una

resolución razonable (mensual o bimensual) puede clarificar la falta de patrón

de distribución o de comportamiento faunísticos o la falta de relación entre

factores bióticos y abióticos, pero deberían ser combinados con experimentos

de distinta índole. Así, el uso de especies indicadoras o la manipulación de las

fuentes externas de alimento usando mesocosmos o trabajando en el laboratorio

sería un complemento esencial de los estudios tradicionales de playas.

Estudiar factores ambientales in situ, como por ejemplo el swash, no

revela toda la información sobre los mecanismos que están detrás del

comportamiento y la distribución de la macrofauna de playas. Para entender los

mecanismos que subyacen en la dinámica de playas, es crucial tener un control

independiente sobre los diferentes parámetros físicos, lo que exige la necesidad

de distintos experimentos. Así, el uso de acuarios o tanques pueden

proporcionar resultados valiosos que permitan trabajar con factores tan

cruciales como el tipo de sedimento, la pendiente, regular el efecto del swash

(periodo, velocidad) o trabajar con especies clave. El estudio de preferencias

alimenticias de las distintas especies también se verán beneficiadas de

experimentos en laboratorio o mesocosmos en intermareales. Trabajos como el

de Lastra et al., 2007 (enviado) son pioneros en la manipulación controlada de

especies de talítridos y en el análisis de sus preferencias alimentarias, tanto en

laboratorio como en el intermareal, que permiten elucidar el comportamiento

de especies de la macrofauna bentónica de distintas áreas geográficas y

comparar el uso específico que hacen estos organismos de las distintas fuentes

externas de alimento que llegan a las playas.

La existencia de correlación no prueba causación de ningún tipo, por lo

que las conclusiones que obtenemos de este estudio deben ser tomadas como

predicciones que ayuden a las manipulaciones experimentales como el paso

natural que debe seguir a un estudio descriptivo. En el caso de las algas varadas


259

y especies invasivas, distintos experimentos en laboratorio podrían comprobar

diversas hipótesis a cerca de la influencia de la estructura física de los distintos

tipos de alga; un análisis de isótopos estables nos proporcionaría las pistas

necesarias sobre el origen y las preferencias de las fuentes alimenticias de los

invertebrados así como de los flujos tróficos en playas. Es importante tener en

cuenta el efecto de las especies invasoras para el futuro de los estudios en

ecología de playas ya que pueden afectar irreversiblemente a la comunidad

faunística y al funcionamiento del ecosistema. El efecto provocado por un alga

alóctona como S. muticum puede extenderse rápidamente de sus puntos de

invasión originales, ya sea el intermareal o submareal rocoso, a los

intermareales arenosos más cercanos. Es importante, por tanto, mantener un

estudio de valoración de los impactos que se producen en los distintos

ecosistemas marinos como criterio básico para valorar el impacto directo de

especies alóctonas que pone en evidencia la necesidad de una gestión prioritaria

de los efectos de las distintas especies invasoras en los ecosistemas costeros.

Las asociaciones macrofaunísticas que aparecen en los depósitos de

algas varadas en las playas expuestas son también recursos importantes para

numerosas especies de aves y, por lo tanto, son una parte básica de la red

trófica actuando como un nexo de unión fundamental entre los ecosistemas

marino y terrestre (Hubbard y Dugan, 2003; Orr et al., 2005). Actividades tan

comunes, en zonas costeras con gran concentración turística, como la limpieza

de playas puede provocar efectos irreversibles que determinen la diversidad y

abundancia de especies, afectando consecuentemente a estos dos ecosistemas.

PART VI. GENERAL CONCLUSIONS

Part VI General Conclusions

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1. The intertidal benthic macrofauna inhabiting intermediate sandy beaches of

northern Spain cannot be fully related to morphodynamic beach characteristics

because of the limited range of beaches studied. The number of species is better

explained by the beach exposure rate and tide range rather than by traditional

variables such as Dean’s parameter or beach slope.

2. There is a trend in the sandy beaches studied where an exposure increase leads

to a decrease in biotic variables due to the increase in hydrodynamic

conditions, i.e. harsh swash climate and coarser grain size. There is no unique

key factor affecting benthic macrofauna but several ecological factors influence

the different community variables.

3. Community characteristics from intermediate sandy beaches are affected by

several physical factors. Beach length, slope and wave height are the main

variables affecting macroinfauna assemblages. An increase in beach length

together with more dissipative conditions, i.e. low slope and high wave height,

affect species positively. It seems that macrofauna community characteristics in

sandy beaches are not just determined by beach morphodynamics, but also by

other factors dependent on oceanographic conditions and coastal processes,

determining critical characteristics such as food availability.

4. Macrofauna from intermediate exposed sandy beaches shows no clear intertidal

zonation although two specific zones can be established: a narrow dry high-

shore assemblage of air-breathing species, i.e. the supralittoral zone, below

which there is a wide zone of water-breather species, i.e. the littoral zone.

Species with the clearest zonation pattern are the best explained by the

environmental variables than species with no sharp boundaries in their

distribution along the beach profile.

5. Analyses of distribution of benthic macrofauna along the intertidal demonstrate

that the tidal levels are characterised by distinct faunal densities and species

composition. Macroinfauna community, in terms of abundance, biomass and

species richness is more complex and diverse in sheltered than in exposed

sandy beaches. Crustaceans, mainly talitrids amphipods and cirolanid isopods,

are the dominant group in the supratidal level of both, exposed and sheltered

beaches; while polychaetes and molluscs occupy the intertidal level in sheltered


262

intertidals with more favourable environmental conditions, sediment stability

and organic matter accumulation.

6. Macroinfauna and biochemical compounds showed a clear vertical

stratification with the highest values and concentrations at the superficial layer

of the sediment, where redox potential discontinuity was also observed.

Macrofauna organisms showed preferences both in vertical and horizontal

ranges suggesting a specific distribution which is related to specific sensitivity

to several abiotic factors, including food availability. This emphasizes how

complex the ecology of organisms inhabiting this apparently simple intertidal

habitat might be.

7. The relative structure of the macroinfauna community display a strong

heterogeneity over time, suggesting that macrofaunal assemblages in estuarine

beaches are controlled by complex and unpredictable factors, including small

scale changes in substrate and hydrological characteristics. The existence of a

strong anthropogenic influence may add an important variability factor in the

sedimentary organic distribution and macrofauna community structure of the

intertidal.

8. There is evidence to suggest that food quality can be a main factor, together

with the hydrodynamic conditions, affecting macroinfauna community in the

intertidal. The distribution patterns of macroinfauna beach assemblages result

from a combination of biotic (such as food availability) and abiotic (such as

beach slope, sand particle size or swash climate) factors. It seems that exposed

sandy beaches are mainly physically controlled, whereas hospitable sheltered

beaches let other factors, such as food availability, enrich the benthic fauna

scenery. The observed patterns of macrofauna and biochemical compounds

seem to be better related in sheltered beaches than in exposed ones.

9. Macroinfauna distribution and trophic structure are directly related to the

quantity and quality of the sedimentary organic matter of the intertidal. The

main trophic group inhabiting sheltered intertidal zones belonged to the deposit

feeders, basically formed by polychaetes. This group seems to be regulated by

the availability of sedimentary food resources. Most of the subterrestrial

species at the supratidal level have been considered wrack-associated


263

macrofauna and they depend on allochthonous inputs associated with

oceanographic processes rather than on the swash climate.

10. It is important to consider macrophyte wrack supply together with physical

factors in order to better understand the processes that influence community

structure on sandy beaches. There is some evidence to support that macrofaunal

assemblages change in response to time, and different responses at different

sites may be related to different environmental conditions. Wrack deposits are

important in determining spatial and temporal patterns of macrofaunal

distribution on exposed sandy beaches.

11. Different types of wrack deposits, i.e. native versus invasive algal wrack, are

not used uniformly by invertebrates. There is evidence to support that

nutritional content and microclimatic conditions of wrack deposits affect

macrofaunal assemblages of exposed beaches. The replacement of native wrack

deposits by exotic wrack may have important effects on macrofaunal

assemblages on sandy beaches. A change in the type or amount of seaweed

wrack entering a beach may alter the macrofaunal assemblages and ecosystem

function.

12. The effect of the invasive seaweed S. muticum may have an effect that is spread

away from the points of invasions, i.e. intertidal and subtidal rocky shores. An

assessment of impact on different marine ecosystems may be important criteria

in assessing the effect of this invasive species and the prioritization of exotic

management.

PART VII. APPENDIX

Part VII Appendix

265

PART II: Chapters 2 and 3.

Appendix A. List of macrofauna collected in all the sandy beaches sampled. (+

Presence).

Sp

ecie

s

Peñ

arr

on

da

O

tur

S. P

ed

ro

Xag

ó

Xiv

are

s

Esp

asa

Veg

a

To

ran

da

A

nd

rín

Mollu

sca

Donax tru

nculu

s

+

Cru

sta

cea

Bath

yp

ore

ia p

ela

gic

a

+

Cum

opsis

fa

gei

+

Dio

genes p

ug

ilato

r

+

Eury

dic

e p

ulc

hra

+

+

+

+

+

+

+

+

+

Eury

dic

e a

ffin

is

+

+

+

+

+

+

+

+

+

Gastr

osaccus n

orm

an

i

Gastr

osaccus s

anctu

s

+

+

+

+

+

+

+

Gastr

osaccus s

pin

ifer

+

Hasto

rius a

renari

us

+

+

+

+

+

+

+

+

+

Mysid

acea

in

det.

+

Ponto

cra

tes a

renari

us

+

+

+

+

+

+

+

+

+

Port

um

nus latipes

+

+

+

+

+

Sph

aero

ma h

oo

keri

+

Sph

aero

ma r

ug

icau

da

+

+

+

+

+

+

+

+

+

Talit

rus s

alta

tor

+

+

+

+

+

Talo

rchestia b

rito

+

+

Talo

rchestia d

eshayesii

+

Tylo

s e

uro

peaus

+

+

Uro

thoe

pu

lche

lla

+

Part VII Appendix

266

Sp

ecie

s (

co

nti

nu

ati

on

) P

eñ

arr

on

da

O

tur

S. P

ed

ro

Xag

ó

Xiv

are

s

Esp

asa

Veg

a

To

ran

da

A

nd

rín

Poly

cha

eta

Dis

pio

uncin

ata

+

Ete

one lo

nga

+

Mala

coero

s fu

ligin

osu

s

+

Nephty

s ci

rrosa

+

+

+

+

+

+

+

+

Ophelia

bic

orn

is

+

+

+

Ph

yllo

doci

dae in

det.

+

Sco

lele

pis

squ

am

ata

+

+

+

+

+

+

+

+

Sig

alio

n m

ath

ildae

+

+

Oth

ers

Hym

eno

pte

ra

+

+

+

Nem

ert

ea

+

+

+

+

+

+

+

+

+

Olig

ach

aeta

Ara

ne

i +

+

+

Dip

tera

+

+

+

+

+

+

+

+

+

Cole

opte

ra

+

+

+

+

Part VII Appendix

267

Sp

ecie

s (

co

nti

nu

ati

on

) O

yam

bre

L

ien

cre

s

La

ng

re

Be

rria

L

are

do

S

alv

aje

B

ak

io

La

ga

Z

ara

utz

H

en

da

ya

Mollu

sca

An

gu

lus t

en

uis

+

Do

nax t

run

cu

lus

+

+

+

Hyd

rob

ia u

lva

e

+

+

Cru

sta

ce

a

Ba

thyp

ore

ia p

ela

gic

a

+

+

+

+

Cu

mo

psis

fa

gei

+

+

+

Dio

ge

ne

s p

ug

ila

tor

+

+

Eo

cu

ma

do

llfu

si

+

Eu

ryd

ice

pu

lch

ra

+

+

+

+

+

+

+

+

+

+

Eu

ryd

ice

aff

inis

+

+

+

+

+

+

Ga

str

osa

ccu

s n

orm

an

i

+

Ga

str

osa

ccu

s s

anctu

s

+

+

+

+

+

+

+

+

+

Ga

str

osa

ccu

s s

pin

ife

r

+

+

+

Ha

sto

riu

s a

ren

ari

us

+

+

+

+

+

+

+

Idoth

ea n

eg

lecta

+

Mic

rode

uto

pus d

am

no

nie

nsis

+

Mic

rode

uto

pus s

p.

+

Mysid

ace

a in

det.

+

+

Pa

raja

ssa

pe

lag

ica

+

Po

nto

cra

tes a

ren

ari

us

+

+

+

+

+

+

+

+

+

Po

rtu

mnu

s la

tip

es

+

+

+

+

+

+

Sp

ha

ero

ma r

ug

ica

ud

a

+

+

+

+

+

+

+

Ta

litr

us s

alta

tor

+

Ta

lorc

hestia

bri

to

+

+

Ta

lorc

hestia

de

sh

aye

sii

+

Uro

tho

e b

revic

orn

is

+

Part VII Appendix

268

Sp

ecie

s (

co

nti

nu

ati

on

) O

yam

bre

L

ien

cre

s

Lan

gre

B

err

ia

Lare

do

S

alv

aje

B

akio

L

ag

a

Zara

utz

H

en

da

ya

Uro

thoe

pose

idonis

+

Poly

cha

eta

Dis

pio

uncin

ata

+

Drilo

nere

is filu

m

+

Gly

cera

tridacty

la

+

Lum

bri

neri

s s

p.

+

Nephty

s c

irro

sa

+

+

+

+

+

Ophelia

bic

orn

is

+

+

+

+

Ophelia

neg

lecta

+

Para

done

is s

p.

+

Scole

lepis

squ

am

ata

+

+

+

+

+

+

Sig

alio

n m

ath

ildae

+

Sig

alio

n s

quam

atu

m

+

+

Spio

phan

es b

om

byx

+

Syl

lidae ind

et

+

Oth

ers

Insecta

+

+

+

+

Nem

ert

ea

+

+

+

+

+

+

+

Olig

achaeta

+

+

+

+

+

Ara

ne

i

+

+

Dip

tera

+

Cole

opte

ra

+

+

+

Pla

the

lmin

tes in

det.

+

Echin

ocard

ium

sp

.

+

Part VII Appendix

269

PART III: Chapter 4.

Appendix A. List of macrofauna collected in all the sandy beaches sampled.

Trophic group: suspension feeders: f; surface detritus feeders: s; subsurface

detritus feeders: b; carnivores: c; others: o (+ Presence).

Taxa Sheltered beaches Exposed beaches

Trophic group Broña Bornelle Cabanas Xeiruga Baldaio Niñons

Nemertea + + +

Polychaeta

Arenicola marina b + + +

Eteone longa c + + +

Glycera tridactyla c + +

Leptonereis glauca c +

Malacoceros fuliginosa s +

Nereis diversicolor c +

Nereis pelagica c +

Nereis spp. c + + +

Nephtys cirrosa c +

Ophelia bicornis b + +

Ophelia radiata b +

Ophelia sp. b +

Perinereis cultrifera o +

Phyllodoce laminosa c + +

Scololepis squamata s + + + + + +

Spiophanes bombyx s +

Spio filicornis s +

Mollusca

Calionymus maculatus o +

Cerastodema edule f + + +

Donax trunculus f + +

Tapes decussatus f +

Tellina tenuis s +

Venerupis rhomboides f +

Crustacea

Atylus guttatus s +

Bathyporeia pelagica s +

Caprella penanitis o +

Carcinus maenas c + +

Crangon crangon o +

Eurydice affinis c + + +

Eurydice pulchra c + + + + +

Gammarus locusta s +

Gammarus salinus s +

Gammarus sp. s +

Gastrosaccus spinifer o +

Haustorius arenarius s + +

Part VII Appendix

270

Taxa (continuation) Sheltered beaches Exposed beaches

Trophic group Broña Bornelle Cabanas Xeiruga Baldaio Niñons

Crustacea

Idotea baltica o +

Idotea emarginata o +

Idotea metallica o +

Idotea neglecta o + +

Idotea pelagica o + +

Isaea montagus o +

Lembos websteri s + Pontocrates

arenarius s + Sphaeroma

rugicauda o + +

Talitrus saltator o + + +

Talorchestia britto o + + + + + Talorchestia

deshayesii o + +

Tylos europaeus o + + + +

Urothoe elegans s +

Platyhelminthes o +

Insecta

Coleoptera spp. o + + +

Diptera spp. o +

Hymenoptera spp. o + +

Aranei o + +

Part VII Appendix

271

Appendix B. Summary of SIMPER analysis comparing sheltered and exposed

sandy beaches. δi: contribution of species i to the Bray-Curtis similarity matrix

between both groups of beaches. Σδi: accumulative percentange.

Average similarity: 41,03

Sheltered Average Exposed Average

Species abundance abundance δi(%) Σδi (%)

Talorchestia britto 2975.91 933.5 11.44 11.44

Idotea pelagica 5.55 1383.0 6.30 17.74

Talorchestia deshayesii 249.75 801.42 5.78 23.53

Tylos europaeus 906.87 79.92 5.34 28.87

Haustorius arenarius 175.38 0.00 4.37 33.24

Nemertea spp. 177.60 0.00 4.05 37.30

Eurydice affinis 0.00 101.01 3.85 41.15

Scololepis squamata 513.93 218.67 3.85 44.99

Ophelia bicornis 250.86 250.86 3.19 48.18

Nereis spp. 79.92 0.00 2.93 51.11

Malacoceros fuliginosa 103.53 0.00 2.86 53.97

Talitrus saltator 341.88 8.88 2.85 56.82

Glycera tridactyla 93.24 0.00 2.67 59.50

Cerastoderma edule 55.50 0.00 2.33 61.82

Arenicola marina 46.62 0.00 2.26 64.09

Crangon crangon 38.85 0.00 2.18 66.27

Gammarus locusta 36.63 0.00 1.96 68.23

Eteone longa 25.53 0.00 1.79 70.02

Eurydice pulchra 34.41 71.04 1.73 71.75

Gammarus salinus 26.64 0.00 1.59 73.34

Donax trunculus 29.97 0.00 1.57 74.91

Gammarus sp. 36.63 0.00 1.56 76.47

Idotea metallica 24.42 0.00 1.44 77.91

Angulus tenuis 22.20 0.00 1.32 80.64

Ophelia sp. 12.21 0.00 1.32 80.64

Nereis diversicolor 22.20 0.00 1.29 81.93

Idotea emarginata 25.53 0.00 1.28 83.21

Idotea neglecta 21.09 4.44 1.20 84.41

Carcinus maenas 7.77 0.00 1.07 85.48

Sphaeroma rugicauda 4.44 18.87 0.00 86.47

Perinereis cultrifera 7.77 0.00 0.98 87.45

Urothoe elegans 9.99 0.00 0.93 88.38

Spiophanes bombyx 5.55 0.00 0.83 89.21

Leptonereis glauca 6.66 0.00 0.80 90.01

Part VII Appendix

272

APPENDIX C Summary of SIMPER analysis comparing high and medium

and high and low tidal levels in sheltered sandy beaches.

Average dissimilarity: 97.04

High average abundance

Medium average abundance δi(%) Σδi (%)

Tylos europaeus 2713.95 0.00 8.23 8.23



Talitrus saltator 1015.65 0.00 7,21 31.02





Nereis spp. 0.00 116.55 4.96 61.26

Donax trunculus 0.00 69.93 4.44 65.70

Eurydice pulchra 0.00 46.62 4.02 69.72

Eteone longa 0.00 43.29 3.95 73.67


Crangon crangon 0.00 23.31 3.32 80.56

Ophelia sp. 0.00 16.65 2.99 83.55

Carcinus maenas 0.00 6.66 2.12 85.67


Ophelia radiata 0.00 3.33 1.53 89.32




Low average abundance δi(%) Σδi (%)


Malacoceros fuliginosa 0.00 3083.58 5.40 11.51



Tylos europaeus 2713.95 3.33 4.33 24.94




Nereis spp. 0.00 123.21 3.24 38.48

Gammarus sp. 0.00 109.89 3.16 41.65

Gammarus locusta 0.00 103.23 3.12 44.77

Crangon crangon 0.00 89.91 3.03 47.80

Gammarus salinus 0.00 76.59 2.92 50.73

Idotea emarginata 0.00 69.93 2.86 53.59


Idotea metallica 0.00 59.94 2.76 59.19

Idotea neglecta 0.00 49.95 2.64 61.83


Idotea baltica 0.00 36.63 2.44 66.86

Angulus tenuis 0.00 33.30 2.38 69.24

Part VII Appendix

273

Eteone longa 0.00 33.30 2.38 71.62


Urothoe elegans 0.00 26.64 2.23 76.15

Perinereis cultrifera 0.00 19.98 2.05 78.20

Donax trunculus 0.00 16.65 1.93 80.13

Leptonereis glauca 0.00 16.65 1.93 82.06

Carcinus maenas 0.00 16.65 1.93 83.99

Idotea pelagica 0.00 13.32 1.79 85.78


Venerupis decussata 0.00 9.99 1.61 89.00

Phyllodoce laminosa 0.00 6.66 1.37 90.37

APPENDIX D. Summary of SIMPER analysis comparing high and medium

and high and low tidal levels in exposed sandy beaches.



Medium average abundance δi(%) Σδi (%)

Idotea pelagica 4145.85 0.00 21.62 21.62




Atylus guttatus 13.32 0.00 6.91 69.49


Idotea neglecta 13.32 0.00 6.91 83.30





Low average abundance δi(%) Σδi (%)

Idotea pelagica 414.585 0.00 15.89 15.89




Tylos europaeus 93.24 0.00 8.67 66.42


Atylus guttatus 13.32 0.00 5.08 79.11


Idotea neglecta 13.32 0.00 5.08 89.27


Part VII Appendix

274

T

rophic

January

A

pri

l

Ju

ly

Oct

ober

Speci

es

gro

up

HT

L

MT

L

LT

L

HT

L

MT

L

LT

L

HT

L

MT

L

LT

L

HT

L

MT

L

LT

L

Poly

cha

eta

Are

nic

ola

mari

na

b

- +

+

-

+

+

- +

+

-

+

+

Arici

ida

e in

det.

o

- -

- -

- -

- -

+

- -

+

Bocc

ard

ia s

p.

o

- -

- -

- -

- +

-

- -

-

Capite

lla c

apita

ta

b

+

+

+

- +

+

-

+

+

+

+

+

Cirra

tulid

ae in

det.

b

- -

+

- -

- -

- -

- -

-

Ete

one lo

nga

c

- +

+

-

+

+

- +

+

-

+

+

Gly

cera

tid

act

yla

c

- -

+

- +

+

-

+

- -

+

+

Hete

rom

ast

us

filifo

rmis

b

- -

- -

- -

- -

- -

- +

Lan

ice c

onch

ilega

s

- -

+

- -

+

- -

- -

- +

Mala

coce

ros

fulig

inosu

s s

- +

+

-

+

- -

+

- +

+

+

Nephty

s ca

eca

c

- -

- -

- +

-

- -

- -

-

Nephty

s h

om

berg

ii c

- -

+

- -

- -

- -

- +

-

Nephty

s in

cisa

c

- -

- -

- -

- -

+

- -

-

Nepth

ys s

p.

c -

- +

-

- +

-

+

+

- -

-

Nere

is d

ivers

icolo

r c

- +

+

-

+

+

- +

-

+

+

+

Nere

is s

p.

c -

- -

- +

-

- +

-

- -

-

Orb

iniid

ae in

det.

o

- +

+

-

- -

- -

+

- -

+

Pect

inari

a k

ore

ni

b

- -

+

- -

- -

- -

- -

-

Phyl

lod

oce

lam

inosa

c

- -

+

- -

+

- -

+

- +

+

Phyl

lod

oce

sp.

c -

- +

-

+

+

- -

+

- -

-

Pra

eg

eria

rem

ota

o

- -

- -

- -

- -

- -

- -

Pse

ud

opo

lydora

sp.

s -

+

- -

- -

- -

+

- +

+

PART IV: Chapter 5.

Appendix A. List of species collected in the estuarine beach sampled

(Barraña). Trophic group: suspension feeders: f; surface detritus feeders: s;

subsurface detritus feeders: b; carnivores: c; others: o (+ Presence).

HTL: high tidal level; MTL: medium tidal level; LTL: low tidal level.

Part VII Appendix

275

T

rophic

January

A

pri

l

July

O

cto

ber

Specie

s

gro

up

HT

L

MT

L

LT

L

HT

L

MT

L

LT

L

HT

L

MT

L

LT

L

HT

L

MT

L

LT

L

Pygospio

ele

gans

s

- +

-

- +

-

- +

+

+

+

-

Scolo

plo

s a

rmig

er

b

- -

- -

- +

-

- -

- -

-

Spio

filic

orn

is

s

- +

+

-

+

+

- +

+

-

+

+

Spio

phan

es b

om

byx

s

- +

-

- +

-

- -

- -

+

+

Str

eb

losp

io c

f. d

ekhuyzen

i s

- -

- -

- -

- -

- -

- -

Cru

sta

cea

Aori

dae in

det.

c

- +

-

- -

- -

- -

- -

+

Carc

inus m

aen

as

c

- +

-

- +

-

- +

+

-

- +

Cra

ngo

n c

rang

on

o

- +

-

- +

-

- +

+

-

+

-

Cope

pod

a inde

t.

o

-

+

- -

- -

- +

-

- -

Cum

acea inde

t.

o

- -

- -

- -

- +

+

-

- -

Cum

opsis

go

odsir

i o

- -

- -

- -

- +

+

-

- -

Cum

opsis

long

ipes

o

- -

- -

- -

- +

-

- -

-

Cyath

ura

cari

nata

s

- +

-

- +

-

- +

+

-

+

-

Eury

dic

e a

ffin

is

c

+

- -

- -

- -

- -

+

- -

Eury

dic

e n

aylo

ri

c

- -

- -

- -

- -

- -

- -

Gam

maru

s s

alinus

s

- +

+

-

- -

- +

-

+

- -

Gastr

osaccus s

anctu

s

o

- +

+

-

+

- -

+

+

- -

+

Hausto

rius a

ren

arius

s

- -

- -

- -

- -

+

- -

-

Hete

rota

na

is b

ers

tedi

o

- -

- -

- -

- -

+

- -

-

Hyale

sp.

c

- -

- -

- -

- +

+

-

- -

Idote

a m

eta

llic

a

o

- -

- -

- -

- -

- +

-

-

Idote

a n

egle

cta

o

- -

- -

- +

-

+

- -

- -

Iphin

oe

trisp

inosa

s

- -

- -

- -

- +

+

-

- -

Jassa falc

ata

o

- -

- -

- -

- -

+

- -

-

Mic

rode

uto

pus g

ryllo

talp

a

s

- -

- -

- -

- -

- -

+

+

Mysid

ae in

det.

o

- +

+

-

- +

-

- +

-

- -

Para

mysis

helleri

o

- +

-

- -

- -

+

- -

- -

Talitr

us s

alta

tor

o

+

- -

+

- -

+

- -

+

+

-

Part VII Appendix

276

T

rophic

January

A

pri

l

July

O

cto

ber

Specie

s

gro

up

HT

L

MT

L

LT

L

HT

L

MT

L

LT

L

HT

L

MT

L

LT

L

HT

L

MT

L

LT

L

Talo

rchestia b

ritto

o

- -

- -

- -

+

- -

- -

-

Talo

rchestia d

eshayesii

o

+

- -

+

- +

+

-

+

+

+

+

Tylo

s e

uro

paeus

o

+

- -

- -

- -

- -

- -

-

Uro

thoe

pose

idonis

s

- -

+

- -

+

- -

- -

- +

Mollu

sca

Abra

tenu

is

s

- +

-

- -

- -

- -

- -

-

Ang

ulu

s ten

uis

s

- -

+

- -

+

- -

+

- -

-

Cera

sto

derm

a e

du

le

f -

+

+

- +

+

-

+

+

- +

+

Donax v

ari

ega

tus

f -

- -

- -

- -

- +

-

- -

Ensis

ensis

f

- -

+

- -

- -

- -

- -

-

Hydro

bia

ulv

ae

s

+

+

- -

+

- +

+

+

+

+

-

Lorip

es lucin

alis

s

- +

+

-

- +

-

- +

-

- +

Scro

bic

ula

ria p

lan

a

s

- +

+

-

+

- -

+

- -

+

-

Tapes d

ecussatu

s

f -

+

- -

- +

-

- -

- +

-

Telli

na te

nuis

s

- -

+

- -

- -

- -

- -

-

Telli

nacea

ind

et.

s

- +

+

-

- -

- -

- -

+

-

Ven

eru

pis

pu

llastr

a

f -

- -

- -

- -

+

- -

- -

Oth

ers

Insecta

inde

t o

+

- +

+

-

- +

-

- +

-

-

Cole

opte

ra larv

ae

o

+

- -

- -

- -

- -

+

- -

Dip

tera

larv

ae

o

+

- -

- -

- -

- -

- -

-

Nem

ert

ea ind

et.

c

- +

-

- +

-

- +

+

-

- +

Olig

ochaeta

inde

t.

o

+

+

+

+

+

- +

+

-

+

+

+

Part VII Appendix

277

Appendix B. Summary of SIMPER analysis comparing tidal levels from

Barraña. δi: contribution of species i to the Bray-Curtis similarity matrix

between both groups of beaches. Σδi: accumulative percentange. HTL: high

tide level; MTL: medium tide level; LTL: low tide level.


HTL Average abundance

MTL Average abundance δi(%) Σδi (%)

Capitella capitata 0.00 467.00 12.37 12.37

Hydrobia ulvae 2.00 706.00 10.99 23.36

Taorchestia deshayesii 77.00 0.00 8.76 32.12


Spio filicornis 0.00 49.00 7.87 48.71

Malacoceros fuliginosus 0.00 48.00 7.83 56.54




Insect larvae 7.00 0.00 4.18 77.48

Eteone longa 0.00 6.00 3.91 81.40

Abra tenuis 0.00 3.00 2.79 84.19

Tellinacea indet. 0.00 2.79 2.79 89.76

Pygospio elegans 0.00 2.79 2.79 89.76

Aoridae indet. 0.00 3.00 2.79 92.55


HTL Average abundance

LTL Average abundance δi(%) Σδi (%)


Taorchestia deshayesii 77.00 0.00 10.60 22.16

Spio filicornis 0.00 70.00 10.37 32.53


Urothoe poseidonis 0.00 24.00 7.83 48.38

Phyllodoce sp 0.00 20.00 7.41 55.79

Loripes lucinalis 0.00 17.00 7.03 62.82

Gastrosaccus sanctus 0.00 5.00 4.36 67.18

Bivalvia indet. 0.00 3.00 3.37 70.55

Insect (larvae) 7.00 1.00 3.37 73.92

Mysidae indet. 0.00 2.00 2.67 76.59

Hydrobia ulvae 2.00 0.00 2.67 79.27

Eteone longa 0.00 2.00 2.67 81.94

Lanice conchilega 0.00 2.00 2.67 84.61

Nephtys hombergii 0.00 2.00 2.67 87.28

Tylos europaeus 0.00 0.00 1.69 88.97

Insect 0.00 1.00 1.69 90.66

Part VII Appendix

278

Average dissimilarity: 66.23* Appendix B

(continuation) MTL Average abundance

LTL Average abundance δi(%) Σδi (%)

Hydrobia ulvae 706.00 0.00 13.01 13.01




Phyllodoce sp 0.00 20.00 6.04 40.36

Loripes lucinalis 0.00 17.00 5.73 46.09



Gastrosaccus sanctus 0.00 5.00 3.55 59.63


*Results from the main species with the highest dissimilarity.

Appendix C. Summary of SIMPER analysis comparing two years in Barraña.

δi: contribution of species i to the Bray-Curtis similarity matrix between both

groups of beaches. Σδi: accumulative percentange.

Average dissimilarity: 46.84*

1997 Average

abundance 1998 Average

abundance δi(%) Σδi (%)



Hydrobia ulvae 746.50 559.50 4.38 13.84

Oligochaeta indet. 45.50 15.50 3.90 17.74

Pygospio elegans 46.00 0.50 3.62 21.36



Phyllodoce laminosa 0.00 4.50 2.21 29.42

Glycera tidactyla 5.50 0.25 2.16 31.59



Spio filicornis 53.25 161.50 1.92 37.57

Tapes decussatus 1.75 0.00 1.78 39.36

Decapod indet 14.25 0.00 1.78 41.13

Scrobicularia plana 14.50 3.00 1.77 42.90

Nephtys hombergii 10.25 0.25 1.76 44.66

Crangon crangon 0.25 2.00 1.73 46.39


Cyathura carinata 2.50 0.25 1.69 49.78

*Results from the main species with the highest dissimilarity.

Part VII Appendix

279

Appendix D. Environmental variables from January 97 to October 97. (HTL: high tidal level; MTL:medium tidal level; LTL: low tidal level).

Mea

n g

rain

siz

e (μ

m)

Sh

ea

r

st

re

ng

th

(

kP

a)

R

ed

ox

p

ot

en

ti

al

(

mV

)

Wa

te

r

co

nt

en

t

(%

)

Tem

per

ature

(ºC

)

De

pt

h

(c

m)

H

TL

M

TL

L

TL

H

TL

M

TL

L

TL

H

TL

M

TL

L

TL

H

TL

M

TL

L

TL

H

TL

M

TL

L

TL

0

-5

3

40

.6

±1

0.

4

23

9.

7±

44

2

04

.5

±3

.9

3

.3

±0

.4

4

.5

±1

.3

5

.1

±1

.3

2

24

.7

±2

2.

2

57

.3

±4

3

40

±5

6.

6

21

.3

±0

.5

2

3±

1.

3

25

±0

.3

1

3.

3±

0.

1

12

.1

±0

.2

1

3.

2±

0.

2

5

-1

0.

3

38

.4

±1

2.

5

26

4.

7±

23

.8

1

98

.3

±4

.9

1

1.

3±

1.

7

6.

7±

1.

4

7.

5±

1.

4

22

6.

7±

17

.2

-

66

.3

±3

7.

2

-

15

8.

5±

40

2

0±

2

23

.5

±1

.7

2

5±

1

13

.2

±0

.1

1

2±

0.

1

12

.8

±0

.1

Ja

nu

ar

y

97

1

0-

15

.

34

4.

5±

34

3

11

.2

±4

8.

1

19

3.

2±

3.

8

17

.1

±1

.2

7

.8

±1

9

.9

±2

.1

2

31

.7

±1

9

-1

03

.7

±1

9

-2

09

.5

±8

1

8.

3±

1

24

±1

2

4±

0.

2

13

.1

±0

.1

1

1.

8±

0.

1

12

.7

±0

.1

1

5-

20

4

17

.4

±3

3.

3

34

6.

1±

28

.7

1

97

.3

±9

.8

2

0.

7±

0.

7

12

.9

±1

.4

1

3.

4±

1.

9

24

2.

5±

3.

5

-1

17

±1

0.

6

-

22

6±

15

.6

1

8.

3±

1

23

±1

.2

2

4±

0.

3

12

.9

±0

.2

1

1.

7±

0.

1

12

.5

±0

.1

2

0-

25

4

03

.1

±8

8

37

7.

7±

96

.5

2

19

.7

±1

5.

4

-

-

-

24

2±

4

-1

17

±1

0.

6

-

22

6±

15

.6

1

9.

2±

1

23

±1

.3

2

4.

7±

0.

5

-

-

-

0

-5

3

18

±1

3.

2

23

2.

7±

12

.3

2

11

.9

±6

.4

3

.2

±0

.6

4

.1

±0

.8

4

.6

±0

.5

1

78

±5

9

-

16

3.

5±

10

1

-

11

9±

15

1

21

±1

2

2±

1

24

±1

1

9.

3±

0.

1

16

.7

±0

.1

1

4.

4±

0.

2

5

-1

0.

3

28

±1

0

24

7.

8±

12

2

02

.4

±2

.8

5

.3

±1

.4

6

.2

±1

.2

1

1±

1.

4

21

1±

35

-

34

8±

12

4.

5

-4

15

±3

3

20

±0

2

2±

1

23

±0

.4

1

9.

9±

0.

1

16

.5

±0

.2

1

4.

3±

0.

1

Ap

ri

l

97

1

0-

15

.

34

6.

8±

5.

3

28

4.

7±

15

1

97

.7

±6

.2

1

0.

1±

2.

7

9.

9±

1.

5

16

±1

.5

2

26

±1

9

-

34

7±

21

2.

5

-

50

6±

43

.4

1

9+

0.

5

21

.6

±1

2

3±

0.

2

20

.2

±0

.3

1

6.

4±

0.

1

14

.5

±0

.1

1

5-

20

3

59

±2

3

39

.6

±3

0

20

5.

5±

8.

7

14

±2

1

3.

8±

1.

1

22

±2

.3

2

63

±1

8

-4

44

±1

13

-

53

0±

5

18

±0

.4

2

2±

1

23

±0

.5

1

9.

4±

0.

3

16

±0

.2

1

4.

7±

0.

1

2

0-

25

4

03

.6

±2

8.

7

40

7.

5±

58

.8

2

10

±7

.3

-

-

-

2

76

±2

0

-4

79

±7

7

-

53

2.

3±

14

1

8.

3±

0.

5

22

.4

±1

.2

2

3.

6±

0.

4

18

±0

.3

1

5.

7±

0.

1

14

.9

±0

.1

0

-5

3

68

.3

±1

2

21

7.

9±

10

.8

1

91

.2

±4

.2

2

.3

±1

3

.8

±0

.6

3

.4

±0

.7

1

86

.5

±5

9

-1

55

±1

01

-

12

5±

15

1

19

.2

±0

.3

2

2±

0.

7

24

±1

1

8.

6±

0.

3

15

.8

±0

.3

1

7.

9±

0.

2

5

-1

0.

3

66

.4

±1

3.

3

25

0.

2±

9.

7

18

8.

6±

3.

3

5.

9±

2

6.

5±

1.

5

8.

7±

1.

1

20

0±

35

-

36

5±

12

4.

5

-

39

4.

3±

33

1

8.

5±

0.

7

21

±1

.5

2

3±

0.

5

20

.1

±0

.6

1

5.

5±

0.

2

16

.8

±0

.2

Ju

ly

9

7

10

-1

5.

3

55

.8

±3

.1

2

59

.7

±1

6.

8

18

9.

4±

6

8.

5±

2.

8

9.

2±

1.

3

14

.3

±1

.8

2

37

.3

±1

9

-

33

0±

21

2.

5

-

53

1±

43

.4

1

8±

0.

8

22

±0

.3

2

4±

0.

2

21

.3

±0

.5

1

5.

4±

0.

2

16

.1

±0

.2

1

5-

20

3

98

±6

.6

3

17

.5

±1

8.

2

19

1.

5±

5

12

.2

±3

.1

1

2.

4±

1.

1

18

.1

±1

.7

2

50

±1

8

-4

66

±1

12

-

50

3.

5±

5

16

±0

.3

2

2±

0.

2

23

±1

2

1.

9±

0.

4

15

.7

±0

.2

1

5.

9±

0.

1

2

0-

25

4

03

.3

±3

7.

5

40

2.

4±

25

.7

2

22

±2

4.

7

-

-

-

28

9.

8±

20

-

45

5±

77

-

55

9±

13

.7

1

7.

7±

2

23

.5

±2

.2

2

3.

4±

5

22

.2

±0

.2

1

6±

0.

2

15

.9

±0

.1

0

-5

3

59

.4

±5

0.

1

23

8.

9±

14

.7

2

13

.4

±6

.3

3

.3

±0

.4

5

.2

±1

.1

3

.2

±1

.3

2

10

±1

3.

2

-1

76

±2

4

-2

82

.3

±7

2

0±

1.

5

21

.5

±1

2

1.

5±

1.

5

17

.3

±0

.2

1

7.

4±

0.

1

17

.6

±0

.1

5

-1

0.

3

34

.7

±2

2.

6

26

4.

9±

11

.6

2

21

.1

±5

.6

5

.7

±1

.6

8

.5

±1

.7

9

.3

±1

.3

2

05

±1

3.

2

-2

28

±1

1.

5

-0

5±

13

.2

1

9±

0.

5

21

±2

2

2±

2

17

.5

±0

.1

1

7.

4±

0.

1

17

.6

±0

.1

Oc

to

be

r

97

1

0-

15

.

40

2.

9±

50

.8

3

14

.4

±1

9.

5

22

0.

2±

5.

8

7.

3±

1.

5

11

±2

1

3.

5±

1.

7

22

2±

10

.4

-

23

2±

3

-

31

3.

3±

13

1

7±

0.

6

21

.4

±1

.5

2

2±

1

17

.5

±0

1

7.

5±

0.

1

17

.8

±0

.1

1

5-

20

3

66

.9

±1

7.

8

37

8.

5±

30

.3

2

38

.3

±1

4.

9

11

.7

±1

.8

1

2.

9±

2.

5

18

.1

±2

.1

2

28

±1

2.

6

-2

62

±3

3.

3

-

31

8.

3±

13

1

7.

4±

1

21

.5

±1

.2

2

2.

5±

1.

7

17

.6

±0

1

7.

5±

0.

1

17

.8

±0

.1

20

-2

5

41

3.

9±

60

.6

4

51

.8

±3

6.

7

26

2±

0.

1

-

-

-

22

5±

13

-

27

8.

3±

34

-

32

7±

3.

5

18

±1

2

2.

6±

1

22

±2

1

7.

6±

0

17

.6

±0

.1

1

7.

7±

0.

1

Part VII Appendix

280

Me

an

gra

in s

ize

(μ

m)

S

he

ar

s

tr

en

gt

h

(k

Pa

)

Re

do

x

po

te

nt

ia

l

(m

V)

W

at

er

c

on

te

nt

(

%)

T

em

pe

ratu

re (

ºC)

De

pt

h

(c

m)

H

TL

M

TL

L

TL

H

TL

M

TL

L

TL

H

TL

M

TL

L

TL

H

TL

M

TL

L

TL

H

TL

M

TL

L

TL

0

-5

4

08

.8

±1

1.

3

22

0.

6±

13

.3

2

14

.3

±1

.2

4

.9

±0

.5

2

.6

±1

1

.8

±0

.1

2

15

±7

.1

-

21

8±

9

-1

77

±5

1.

3

21

±0

.6

2

3±

1.

1

24

±0

1

0.

9±

0.

1

12

.7

±0

.3

1

3.

5±

0.

1

5

-1

0.

4

08

.7

±2

9

24

2.

4±

16

2

07

.7

±3

.5

7

.7

±0

.5

6

.1

±0

.6

5

.4

±0

.8

2

25

±7

.1

-

40

5±

30

.4

-

38

7±

15

.3

1

9±

0.

5

22

.5

±0

.2

4

24

±1

1

1.

3±

0.

1

13

±0

.2

1

3.

4±

0

Ja

nu

ar

y

98

1

0-

15

.

39

5.

1±

30

.5

2

60

.9

±1

2.

2

21

2.

7±

4.

2

8.

4±

0.

5

7±

0.

7

8±

1

22

0±

0

-4

51

±1

6.

5

-4

70

±0

1

9±

1.

1

22

±0

.5

2

3±

0.

4

11

.5

±0

.1

1

3.

1±

0.

2

13

.4

±0

1

5-

20

3

79

.4

±3

3

37

6.

8±

23

.1

2

07

±2

.8

8

.9

±0

.4

8

.3

±0

.6

1

0.

2±

1.

6

22

0±

0

-4

73

±1

5.

3

-5

12

.5

±1

1

19

±2

2

2±

1.

5

23

.5

±0

.2

1

1.

7±

0.

1

13

.1

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1

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0

2

0-

25

4

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3.

7

34

0.

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68

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2

09

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±1

-

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2

07

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±1

8

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70

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4

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30

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4

18

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1

24

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1

1.

8±

0.

1

13

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1

3.

6±

0

0

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3

63

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2

23

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6

18

8.

7±

1

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1

4.

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0.

5

2.

9±

0.

5

16

3.

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21

-

24

3.

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55

-

85

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1

21

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2

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1

24

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1

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0.

1

15

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1

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7±

0.

1

5

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0.

3

68

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0.

7

25

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11

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1

91

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0.

6

8.

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0.

6

14

3.

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31

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49

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1

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2

21

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2

4.

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4

15

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±0

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1

5.

6±

0

15

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±0

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Ap

ri

l

98

1

0-

15

.

35

2.

3±

19

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2

79

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8.

1

19

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13

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9

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1

0.

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1.

7

10

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1

66

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8

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17

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2

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85

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1

20

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1.

2

23

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1

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0.

1

15

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1

5.

7±

0.

1

1

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20

3

29

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3

43

4±

84

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1

86

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1

1.

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1.

7

11

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1

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1.

8

16

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7±

46

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-

45

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1

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0.

3

20

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2

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6

15

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1

5.

7±

0

15

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2

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25

3

98

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7

35

7.

3±

31

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2

19

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8

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77

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25

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0

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0

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4

08

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7

24

9.

4±

11

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1

98

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4

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3

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4

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2

20

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48

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0

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4

19

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2

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1

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3

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3

83

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8

11

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7

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9

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2

25

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1

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92

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4

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80

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1

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1.

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1

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ly

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8

10

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3

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8

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17

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03

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6

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6

26

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1

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1.

5

17

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1

5.

9±

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2

16

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2

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25

3

81

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7

44

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2

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2

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2

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18

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2

16

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3

35

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2

15

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1

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2.

7

3.

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0.

6

4.

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0.

7

4.

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0.

3

21

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6

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43

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1

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1

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2

16

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2

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3

72

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3.

5

23

6.

6±

13

1

73

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7

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7

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9

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2

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36

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1.

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1

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5

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3

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1

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0.

1

17

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Oc

to

be

r

98

1

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15

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35

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6

31

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1

79

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3

11

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1

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6

22

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5

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17

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2

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3

70

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2

40

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7±

79

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1

85

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9±

4.

5

13

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1

6.

5±

1.

3

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6

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55

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8

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8

17

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2

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1

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2

16

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1

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3±

0

2

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25

4

23

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0.

4±

50

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3

91

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8.

4

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8±

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47

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3.

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38

1

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1.

2

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2

4.

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0.

6

15

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1

6.

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1

17

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0

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4

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5

24

6.

2±

25

2

26

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6

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±0

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4

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3

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2

20

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37

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0.

6

-4

67

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1.

5

20

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2

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0.

5

24

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1

1.

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0.

1

11

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1

2.

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1

5

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0.

7

42

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7

24

2.

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4.

1±

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1

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1.

2

7.

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6

7.

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1.

1

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6

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73

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9

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40

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6

18

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2

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1.

4

23

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±0

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1

1.

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0

11

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±0

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1

2.

4±

0

Ja

nu

ar

y

99

1

0-

15

.

35

6.

5±

55

2

76

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1.

1

21

3.

1±

3.

4

17

.9

±1

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1

0.

5±

1.

7

14

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2

02

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-

31

7±

25

.2

-

37

3.

3±

50

2

0±

1.

5

22

±1

2

3.

3±

0.

4

11

.7

±0

.1

1

1.

7±

0

12

.4

±0

.1

1

5-

20

3

63

.5

±6

8.

2

39

5.

8±

10

5.

6

22

4.

7±

19

.3

1

9.

9±

2.

3

13

.4

±2

.3

1

7.

7±

1.

6

20

3±

6

-3

67

±3

1

-4

53

±3

1

18

.1

±0

.3

2

2.

3±

1.

3

24

.2

±0

.5

1

1.

8±

0.

1

11

.7

±0

.1

1

2.

5±

0

2

0-

25

4

54

.9

±1

08

.5

4

89

.5

±4

9.

7

20

6.

3±

8.

2

-

-

-

21

0±

0

-3

80

±2

0

-4

95

±3

1.

2

17

.6

±1

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2

3±

1.

1

23

±1

1

1.

9±

0.

1

11

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±0

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1

2.

5±

0

Part VII Appendix

281

Appendix E. Relative contribution of the major macrobenthic groups to the individual densities at the three tidal levels sampled during the period of study. Values are presented as percentages of the respective total abundance [n: abundance (ind.m2) ± sd; number of species is presented in brackets] of three replicated samples per tidal level. A full circle being 100%.

n = 1210±338 n = 107±71n = 6533±979

Polychaetes

Crustaceans

Molluscs

Others

J97

Ap 97

O97

Ju97

J 98

A98

O98

Ju98

J99

n = 1655±463 n = 8402±1638 n = 765±267

HTLMTLLTL

n = 1673±481n = 12442±6693n = 7725±1602

n = 409±320n = 6764±1887n = 4130±1851

n = 125±71n = 11445±570n = 908±231

n = 1869±445n = 17124±4931n = 2563±463

n = 534±285n =6497±3880n = 5465±2314

n = 3168±1157n = 552±160

n =2261±587n = 4948±2955n = 534±338

n = 18±16

Part VI Appendix

282

Appendix F. Contribution of four major trophic groups in percentage of the total individual numbers at the three tidal levels from Barraña. (sb: subsurface deposit-feeder; s: surface deposit-feeder; sf: suspension feeder; c: carnivore; o: others). HTL: high tidal level; MTL: medium tidal level; LTL: low tidal level.

MTL

0

20

40

60

80

100

sb

s

c

o

sf

HTL

% f

ee

din

g t

yp

e

0

20

40

60

80

100

LTL

Ja97A97Ju97O97Ja98A98 J98 O98Ja99

0

20

40

60

80

100

Ecology of the macrofauna in sandy intertidal habitats...

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