Diversity of epiphytic bryophytes of the Colombian … · Diversity of epiphytic bryophytes of the...

Diversity of epiphytic bryophytes of the Colombian Amazon

Laura Victoria Campos Salazar

Universidad Nacional de Colombia

Facultad de Ciencias, Instituto de Ciencias Naturales

Bogota, Colombia

2016

Diversity of epiphytic bryophytes of

the Colombian Amazon

Laura Victoria Campos Salazar

Tesis presentada como requisito parcial para optar al título de:

Doctor en Ciencias-Biología

Directores

PhD Hans ter Steege Naturalis Biodiversity Center, The Netherlands

Dr Jaime Uribe Melendez

Instituto de Ciencias Naturales

Univerisdad Nacional de Colombia

Grupo de Investigación:

Biología de las Criptogamas de Colombia

Universidad Nacional de Colombia

Facultad de Ciencias, Instituto de Ciencias Naturales

Bogota, Colombia

2016

A las comunidades indígenas de la Amazonia Colombiana que a pesar de la

adversidad, se esfuerzan por mantener su tradición y cultura.

To the indigenous communities in the Colombian Amazon who, despite adversity,

strive to maintain their traditions and culture.

Acknowledgments I am grateful to the Universidad Nacional de Colombia, to Instituto de Ciencias Naturales,

and to my professors during my doctoral studies in Science-Biology for contributing to my

professional training. I also thank the Naturalis Biodiversity Center in the Netherlands for

its facilities and support during the completion of my doctoral internship, the Sylvius

Laboratory at the University of Leiden (Netherlands) for having supported and supervised

the development of my studies of population genetics, the Simpson Laboratory at The

University of Texas (Austin) for training in molecular techniques, the Instituto de Estudios

Amazonicos SINCHI for its facilities in the organization and execution of field trips,

COLCIENCIAS for funding this study (Doctorados Nacionales, Beca Francisco José de

Caldas - Bicentenario) and the organization IDEA WILD, which provided supplies and

climbing equipment for sampling epiphytic bryophytes in the Colombian Amazon.

I would like to express my sincere gratitude to my supervisor Hans ter Steege, for his

continued assistance, patience and collaboration along this path, without whose

invaluable support and contributions it would not have been possible to complete this

study. From Hans I learned about the complexity of the Amazon in a warm and friendly

way. I am also grateful to Jaime Uribe for being a constant guide in this process and for

instilling in me through the years a taste and enthusiasm for biology and the taxonomy of

bryophytes.

My sincere thanks also goes to Sylvia Mota de Oliveira for her valuable comments on the

study, our discussions about the ecology of bryophytes in the Amazon, and her gentle

encouragement to keep moving forward. Many thanks to Michael Stech and William

Usaquén for their outstanding contributions to the development and analysis of my the

results of the genetic study of populations, to Rob Gradstein, for his suggestions

throughout the project and for his significant support and interest in the identification of

some species, to Juan Carlos Benavides for his critical comments that helped enrich and

improve the results of the investigation, and to Mary Lou Price for her helpful corrections

and suggestions on the manuscript.

I am also indebted to Kevin Beentjes and Amalia Diaz, who trained me in handling

molecular techniques with kindness and patience and to my colleagues during my

internship in Leiden (Annik Lang, Renato Grama, Sutthiratana Khaopakro, Mega Atria,

Nor Hidayan, Yotsawate Sirichamorn, Tanawat Chaowasku and Hermesson Cassiano),

for making my stay in the Netherlands enjoyable and entertaining and for training me in

handling statistical packages.

I also thank the people who made my stay and sampling of bryophytes through the

Colombian Amazon a success through their suggestions, recommendations and contacts:

Dairon Cárdenas, Luis Fernando Jaramillo, Maria Cristina Peñuela, Jorge Contreras,

Maklin Muñoz, Sebastian Barreto and John Gonzaga. In addition, I'm grateful to my field

assistants, who became my friends: Alfredo, Ever Kuiri, Silverio, Eugenio, Roman and

Mauricio. From them I learned about the Amazonian culture and understood the

importance of silence to hear the jungle. I also thank the Andoke, Kubeo, and Uitoto

indigenous communities for their hospitality and their willingness to help in my fieldwork,

for the long hours they spent with me in the jungle and in the malocas teaching me their

language and culture.

Kind thanks to teachers José Murillo, Argenis Bonilla, Favio González, Orlando Rangel,

Jaime Aguirre, and Orlando Rivera, for their support and encouragement in the initial

stages of this project. Throughout this process I was always surrounded by amazing

people who with their valuable friendship and interest contributed to initiating and

completing this project: Amalia Díaz, Mary Lou Price, Nancy de Heer, Valentijn Hoogwerf,

Sebástian Hoogwerf, Maklin Muñoz, Marcel Montoya, Henry Garcia, Mábel Báez, Rodrigo

Bernal, Juan Carlos Benavides, Jorge Contreras and Emanuel Cataño.

Lastly, I thank my mother and sisters for their constant support over the years, and I

especially thank Jaime for being my complement and my role model, but above all for

being an inexhaustible source of patience and love.

Agradecimientos Agradezco a la Universidad Nacional de Colombia, al Instituto de Ciencias Naturales y a

los profesores que tuve durante mis estudios de posgrado en Ciencias-Biología por haber

aportado en mi formación profesional. A Naturalis Biodiversity Center en Holanda, por las

facilidades y apoyo durante la realización de mi pasantía doctoral, al Laboratorio Sylvius

de la Universidad de Leiden (Holanda) por haberme apoyado y supervisado en el

desarrollo de mis estudios de genética de poblaciones, al Laboratorio Simpson de la

Universidad de Texas (Austin), por los cursos recibidos y la capacitación en técnicas

moleculares. Al Instituto de Estudios Amazónicos SINCHI, por las facilidades en la

organización y ejecución de mis salidas de campo. A Colciencias por la financiación de

este estudio (Doctorados Nacionales Beca Francisco José de Caldas - Bicentenario) y a

la organización IDEA WILD, quien proporcionó los suministros y equipos de escalada

para el muestreo de los briófitos epífitos en la Amazonía Colombiana.

Agradezco de manera especial a mis directores Hans ter Steege por su constante

asesoría y colaboración a lo largo de este camino, sin su invaluable apoyo y aportes no

hubiera sido posible el desarrollo de este proyecto, de Hans aprendí de forma cálida y

amable, más de la complejidad de la amazonía, y Jaime Uribe por ser un guía constante

en este proceso, por inculcarme a través de los años el gusto y entusiasmo por la

biología y taxonomía de los briófitos.

A Sylvia Mota de Oliveira por sus valiosos comentarios, por nuestras conversaciones en

torno a la ecología de los briofitos en la Amazonia, y por su amable voz para seguir

siempre adelante. A Michael Stech y William Usaquén por sus notables aportes en el

desarrollo y análisis de los resultados obtenidos en mi estudio genético de poblaciones. A

Rob Gradstein, por sus sugerencias a lo largo del proyecto y por su significativa ayuda e

interés en la identificación de algunas especies. A Juan Carlos Benavides por sus

comentarios críticos que permitieron enriquecer y mejorar los resultados de la

investigación. A Mary Lou Price por las útiles correcciones y sugerencias sobre el

manuscrito.

A Kevin Beentjes y Amalia Díaz quienes con amabilidad y paciencia me capacitaron en el

manejo de técnicas moleculares. A mis compañeros en la pasantía en Leiden (Annik

Lang, Renato Grama, Sutthiratana Khaopakro, Mega Atria, Nor Hidayan, Yotsawate

Sirichamorn, Tanawat Chaowasku and Hermesson Cassiano), por haber hecho de los

días de estadía en Holanda más amenos y entretenidos, y por la capacitación en el

manejo de paquetes estadísticos.

También agradezco a las personas que por medio de sugerencias, recomendaciones y

contactos, permitieron que mi estadía y muestreo de briofitos a través de la Amazonía

Colombiana fuera un éxito, Dairon Cárdenas, Luis Fernando Jaramillo, María Cristina

Peñuela, Jorge Contreras, Maklin Muñoz, Sevastian Barreto y John Gonzaga. A los

auxiliares de campo, auxiliares que se convirtieron en mis amigos, de ellos aprendí parte

de la cultura amazónica y entendí la importancia del silencio para escuchar la selva,

Alfredo, Silverio, Eugenio, Ever Kuiri, Román y Mauricio. Agradezco también, a las

comunidades indígenas: Andoke, Kubeo y Uitoto por su hospitalidad y disposición para

ayudar en el trabajo de campo, por las largas horas compartidas en la selva y en las

malocas tratando de aprender algo de su lengua y su cultura.

Agradezco amablemente a los profesores José Murillo, Argenis Bonilla, Favio González,

Orlando Rangel, Jaime Aguirre y Orlando Rivera, por su ayuda y estímulo en las fases

iniciales de este proyecto. Durante todo este proceso siempre estuve rodeada de

grandes personas que con su valiosa amistad e interés aportaron para iniciar y culminar

este proyecto, Amalia Díaz, Mary Lou Price, Nancy de Heer, Valentijn Hoogwerf,

Sebástian Hoogwerf, Maklin Muñoz, Marcel Montoya, Henry Garcia, Mábel Báez, Rodrigo

Bernal, Juan Carlos Benavides, Jorge Contreras y Emanuel Cataño.

A mi madre y hermanas, por el acompañamiento constante durante estos años y a Jaime

por ser mi complemento y ejemplo a seguir, pero sobre todo por ser fuente inagotable de

paciencia y amor.

Diversity of epiphytic bryophytes

of the Colombian Amazon

Abstract and Resumen

XI

Abstract This thesis deals with the bryoflora, structure, and diversity of the communities of

epiphytic bryophytes in a vertical gradient in four lowland rain forests of the Colombian

Amazon. The gradient was studied in four sites and included 64 phorophytes across 2300

km2. Each phorophyte was divided into six height zones. In order to carry out the

sampling from the base to the top of the trees, we climbed the trees, using the static rope

technique. In this thesis I present a taxonomic and floristic study. Eighteen new records of

epiphytic bryophytes to Colombia and 109 new departamental records are reported. Each

new record for Colombia is provided with comments, illustrations, and a description of

diagnostic characteristics for each taxon. Information about localities, altitude, and

distribution on the trees is also given. Many of these new records were from the forest

canopy. The high number of new records was to be expected since the canopy of the

Amazonian forests of Colombia has been little studied. The study presents the first

inventory of epiphytic bryophytes across the Colombian Amazon, with 2827 records of

bryophytes recorded from 64 trees sampled from the base to the canopy. Our inventory

contained 160 species (116 liverworts and 44 mosses), distributed in 26 families and 64

genera. The average number of species per locality was 75, and the average number per

plot was 9. We found floristic similarities among localities in the Colombian Amazon.

Species richness was similar among the sites, except for Putumayo, where the number of

species was slightly higher, very possibly influenced by species migrating from the

northern Andes. We also determined that the species were distributed in a clear vertical

zonation pattern along the host trees, suggesting that the species composition of the

epiphytic bryophyte communities at local and regional scales can be explained by niche

assembly. This conclusion is also supported by the presence of a high percentage of

indicator species across the Colombian Amazon, showing a high specificity of species for

a particular microhabitat within the forest. Finally, we provide a genetic population study

conducted with molecular techniques, using the liverwort Cheilolejeunea rigidula as our

model species, which shows that growth can be found from the base of the trunk to the

upper canopy. For this study we included individuals from Guayana and Brazil to

determine the connectivity and genetic structure of this species across the Amazon

region. The statistical analyses and molecular data allowed us to establish the presence

of a clear genetic differentiation. The spatial structure of the ITS indicated an east-to-west

and north-to-south gradient with a gradual differentiation of subpopulations. The gradient

is additionally supported by a weak relationship between genetic distance and geographic

distance. The further apart the individuals are, the less similar their genetic structure is,

indicating limitations not in the dispersion but in the sexual reproduction of Cheilolejeunea

rigidula. The genetic structure of the subpopulations of C. rigidula provided us with

insights into the evolution of tropical liverworts.

Keywords: Amazon, bryophytes, epiphytes, genetic structure, indicator species, niche

assembly, vertical distribution.

Resumen

Esta tesis tiene como objetivo el estudio de la brioflora, estructura y diversidad de las

comunidades de briófitos epífitos en un gradiente vertical en cuatro bosques húmedos de

tierras bajas de la Amazonía colombiana. El gradiente fue estudiado en cuatro sitios e

incluyó 64 forófitos través de 2.300 km2. Cada forófito fue dividido en seis zonas de

altura. Con el fin de llevar a cabo la toma de muestras en las diferentes zonas de la base

a la cima de los árboles, se utilizó la técnica de cuerda estática para subir a los árboles.

En este estudio se presenta un estudio taxonómico y florístico. Se reportan dieciocho

nuevos registros de briófitos epífitos para Colombia y 109 nuevos registros

departamentales. Cada nuevo registro para Colombia está provisto de comentarios,

ilustraciones científicas y una descripción de los caracteres diagnósticos para cada taxón.

También se da información sobre las localidades, la altitud y la distribución de los

árboles. Muchos de estos nuevos registros provenian del dosel. El elevado número de

nuevos registros encontrados era de esperarse ya que el dosel de los bosques

amazónicos de Colombia ha sido poco estudiado. En este estudio se presenta el primer

inventario de briófitos epífitos en toda la Amazonía colombiana con 2827 registros de

briofitas registrados a partir de 64 árboles muestreados desde la base hasta el dosel.

Nuestro inventario contiene 160 especies (116 hepáticas, 44 musgos), distribuidos en 26

familias y 64 géneros. El número promedio de especies por localidad fue de 75, y el

promedio por parcela fue de 9. Encontramos similitudes florísticas entre lugares de la

Amazonía colombiana. La riqueza de especies fue bastante similar entre sitios, con

excepción de Putumayo, donde el número de especies fue ligeramente superior muy

posiblemente influenciado por las especies que migran desde los Andes del Norte.

También se identificó que las especies se distribuyen en un patrón de zonación vertical

libre a lo largo de los árboles huéspedes. Esto nos dio la confianza para explicar que el

ensamble de nicho está abordando la composición de las especies de las comunidades

briófitos epífitos a escalas locales y regionales. Lo anterios también fue apoyada por la

presencia de un alto porcentaje de especies indicadoras través de la Amazonía

colombiana, que muestra una alta especificidad de especies para un microhábitat

particular. Por último, presentamos un estudio de genetica de poblaciones, para ello

empleamos técnicas moleculares, y usamos la especies de hepatica Cheilolejeunea

rigidula como nuestra especie modelo. Esta especie se puede encontrar distribuida

desde la base del tronco hasta la copa de los árboles. Para este estudio se incluyeron

individuos de Guayana y Brasil para determinar la conectividad y la estructura genética

de esta especie en toda la región amazónica. Los análisis estadísticos y los datos

moleculares nos dieron las herramientas para establecer la presencia de una clara

diferenciación genética. La estructura espacial basados en el marcador nuclear ITS

indica la dirección este a oeste y el gradiente norte-sur con una progresiva diferenciación

de las subpoblaciones. El gradiente es, además, el apoyo de una relación debil entre la

distancia genética y la distancia geográfica. Cuanto más alejadas los individuos estan,

más diferentes es su estructura genética, lo que indica las limitaciones no en la

dispersión, pero si en la reproducción sexual de Cheilolejeunea rigidula. La estructura

genética de las subpoblaciones de esta especie nos proporcionan perspectivas de la

evolución de las hepáticas tropicales.

Palabras clave: Amazon, briofitas, distribución vertical, epifitas, estructura genética,

especies indicadoras, nicho.

XV

Contents

PAG.

ACKNOWLEDGMENTS ............................................................................................................. V

ABSTRACT .............................................................................................................................. XI

CONTENTS ............................................................................................................................ XV

LIST OF FIGURES ................................................................................................................... XVI

LIST OF TABLES .................................................................................................................... XIX

1. INTRODUCTION .............................................................................................................. 22

2. NEW RECORDS OF EPIPHYTIC BRYOPHYTES FROM THE COLOMBIAN AMAZON ................. 32

3. THE EPIPHYTIC BRYOPHYTE FLORA OF THE COLOMBIAN AMAZON ................................... 60

4. VERTICAL DISTRIBUTION AND DIVERSITY OF EPIPHYTIC BRYOPHYTES IN THE COLOMBIAN

AMAZON. .............................................................................................................................. 74

5. GENETIC POPULATION STRUCTURE OF CHEILOLEJEUNEA RIGIDULA (NEES & MONT.) R.M.

SCHUST. IN THE AMAZON REGION .......................................................................................... 96

6. CONCLUSIONS AND RECOMMENDATIONS ..................................................................... 118

A. APPENDIX 1: SPECIES - CHAPTER 3 ................................................................................. 121

B. APPENDIX 2: SPECIES INDICATOR ANALYSIS - CHAPTER 4 ............................................... 127

REFERENCES ........................................................................................................................ 135

XVI

List of figures

PAG. Figure 1-1. Geographical limits of Amazonia (http://earthobservatory.nasa.gov). ........... 23 Figure 1-2. Geographical limits of the Colombian Amazon, according to (SINCHI, 2010).

....................................................................................................................................... 25 Figure 2-1. Map of the study area, showing the sampling localities in the Colombian

Amazon. ......................................................................................................................... 35 Figure 2-2. Syrropodon flexifolius Mitt. A. Habit. B. Leaf, showing hyaline border. ......... 37 Figure 2-3. Ceratolejeunea ceratantha (Nees & Mont.) Steph. A. Habit, ventral view. B.

Underleaf. C. Leaf, showing ocelli. - Ceratolejeunea confusa R.M. Schust. D. Gynoecium

and perianth. E. Habit, ventral view. ............................................................................... 39 Figure 2-4. Ceratolejeunea laetefusca (Austin) R.M. Schust. A. Habit, ventral view. B.

Underleaf. C. Leaf, showing ocelli. - Ceratolejeunea desciscens (Sande Lac.) Schiffn. D.

Portion of the stem, showing leaf and underleaf. E. Habit, ventral view. ......................... 41 Figure 2-5. Cheilolejeunea aneogyna (Spruce) A. Evans. A. Habit, ventral view. B.

Portion of shoot showing lobule with two overlapping, paired teeth. - Cheilolejeunea

clausa (Nees & Mont.) R.M. Schust. C. Lobule. D. Habit, ventral view. .......................... 43 Figure 2-6. Cheilolejeunea neblinensis Ilk.-Borg. & Gradst. A. Lobule showing paired

teeth at apex. B. Habit, ventral view. - Cololejeunea cardiocarpa (Mont.) A. Evans. C.

Habit. D. Leaf apex. E. Lobule. ....................................................................................... 44 Figure 2-7. Diplasiolejeunea buckii Grolle, A. Habit, ventral view. B. Underleaf. C. Apex of

the lobule. - Cololejeunea diaphana A. Evans. D. Leaf. E. Habit, ventral view. ............... 46 Figure 2-8. Drepanolejeunea anoplantha (Spruce) Steph. A. Habit, ventral view. B. Leaf,

dorsal view, showing ocelli. - Leptolejeunea exocellata (Spruce) A. Evans. C. Leaf, dorsal

view, showing ocellus. D. Habit, ventral view. ................................................................. 48

Figure 2-9. Microlejeunea aphanella (Spruce) Steph. A. Habit, ventral view, showing one

reduced lobule. B. Portion of shoot, showing ocelli, dorsal view. - Schiffneriolejeunea

amazonica Gradst. C. Habit, ventral view. D. Leaf, showing the lobule. ......................... 49 Figure 2-10. Verdoornianthus griffinii Gradst. A. Gynoecium and perianth, ventral view. B.

Habit, showing leaves with inrolled lobules. - Verdoornianthus marsupifolius (Spruce)

Gradst. C. Leaf, showing orbicular lobule with inflexed apex. D. Habit, ventral view. ...... 51 Figure 2-11. Cheilolejeunea urubuensis (=Vitalianthus) (Zartman & I.L.Ackerman)

R.L.Zhu & Y.M.Wei. A. Habit with perianth, ventral view. B. Apical portion of lobule. -

Telaranea pecten (Spruce) J.J. Engel & G.L. Merr. C. Habit, showing uniseriate leaves. 52 Figure 3-1. Species-accumulation curves for epiphytic bryophytes measured on sixteen

host trees (left) and ninety-six plots (right), in each site. ................................................. 64 Figure 3-2. Boxplot of differences in species richness between the four localities in four

localities of the Colombian Amazon: Amazonas AM, Caquetá CA, Putumayo PU, and

Vaupés VA ..................................................................................................................... 65 Figure 3-3. SAD - Species abundance distribution based on the complete dataset. (O

range points are representing the nine species that recorded the 36% of the records in the

data set). ........................................................................................................................ 69 Figure 3-4. Summary of the species richness per family in four localities of the Colombian

Amazon: Amazonas AM, Caquetá CA, Putumayo PU, and Vaupés VA .......................... 69 Figure 4-1. Map of the study area, showing the sampling localities in the Colombian

Amazon. ......................................................................................................................... 78 Figure 4-2. Schematic plots of 50 x 50m per locality, showing the distance. .................. 79

Figure 4-3. Schematic height zones on a full-grown tree. Z1: tree base; Z2: lower trunk;

Z3: upper trunk; Z4: inner canopy; Z5: middle canopy; Z6: outer canopy........................ 79 Figure 4-4. Boxplot of differences in species richness between the six height zones ..... 83

Figure 4-5. DCA ordination (species scores) of 160 epiphytic bryophytes species and 384

plots across the Colombian Amazon. Different symbols represent the different height

zones: 1 (circle), 2 (triangle), 3 (square), 4 (plus), 5 (reverse triangle), and 6 (asterisk). . 84 Figure 4-6. DCA ordination (species scores) per locality of species (AM: 99 species, CA:

92, PU: 122, VA: 98) and plots (96 each one). Different symbols represent the different

height zones: 1 (circle), 2 (triangle), 3 (square), 4 (plus), 5 (reverse triangle), and 6

(asterisk). ....................................................................................................................... 85

Figure 4-7. DCA ordination of 160 epiphytic bryophytes species and 384 plots across the

Colombian amazon. Different symbols represent the locality of the plots, AM: Amazonas

(circle), CA: Caquetá (triangle), PU: Putumayo (square), and VA: Vaupés (plus). .......... 86 Figure 4-8. Correlation for the Colombian Amazon between the DCA1 and the height

zones. R2= 0.772, P<0.001 ............................................................................................ 86

Figure 4-9. Correlation for each site, showing the coefficient. AM Amazonas, CA

Caquetá, PU Putumayo and VA Vaupés. ....................................................................... 87 Figure 4-10. Correlation between geographical distance among the trees and species

composition similarity using the bray-curtis similarity index among the 384 plots. ........... 88 Figure 5-1. Cheilolejeunea rigidula (Nees & Mont.) R. M. Schust., showing characteristic

underleaves with cuneate bases. ................................................................................... 98 Figure 5-2. Schematic full-grown tree showing the two sections (canopy and trunk) and

six height zones, Z1: tree base; Z2: lower trunk; Z3: upper trunk; Z4: inner canopy; Z5:

middle canopy; Z6: outer canopy. ................................................................................... 99 Figure 5-3. Study sites in the Amazon basin where the shoot samples were collected: 1. Pto. Colombia (Putumayo); 2. La Gamitana (Caquetá); 3. Macaquiño (Vaupés); 4. El

Zafire (Amazonas), all Colombia; 5. Mabura Hill (Guiana); 6. Manaus (Brazil) and 7. Tapajos (Brazil). ............................................................................................................. 99 Figure 5-4. A - Lobule of Cheilolejeunea aneogyna (Spruce) A. Evans, showing paired

lobule teeth. B - Lobule of Cheilolejeunea rgidula (Nees & Mont.) R. M. Schust., showing

lobule apex with one tooth. ............................................................................................103 Figure 5-5. NJ tree derived from a Neighbor joining analysis of Cheilolejeunea rigidula

and Cheilolejeunea aneogyna, including 11 taxa related to those species and two

outgroup species. ..........................................................................................................107 Figure 5-6. Haplotype network of Cheilolejeunea rigidula using the chloroplast marker

(psbA). Dashes correspond to non-sampled or extinct haplotypes. Haplotypes are

represented by colored areas (geographic regions) and by pie diagrams whose size is

proportional to the haplotype frequency. ........................................................................109 Figure 5-7. Haplotype network of Cheilolejeunea rigidula using the chloroplast marker

(atpB). Dashes correspond to non-sampled or extinct haplotypes. Haplotypes are


proportional to the haplotype frequency. ........................................................................109

Figure 5-9. Mantel test showing the relationship between genetic distance (Tamura Nei)

and geographical distance (Degrees) of pairs of shoots from different localities ............114

XIX

List of tables

Table 2-1. New records of liverworts (Marchantiophyta) to Amazonia: Amazon: AM,

Caquetá: CA, Putumayo: PU and Vaupés: VA................................................................ 53 Table 2-2. New records of mosses (Bryophyta) to Amazonia. Amazon: AM, Caquetá: CA,

Putumayo: PU and Vaupés: VA. ..................................................................................... 56 Table 3-1. Site location and characteristics for the four study sites: Amazonas: AM,

Caquetá: CA, Putumayo: PU, and Vaupés: VA............................................................... 61 Table 3-2. Distribution of species richness at family and genera level, and genera

richness at family level in Colombian Amazon. ............................................................... 64 Table 3-3. Species diversity by locality ........................................................................... 64 Table 3-4. Family richness in the four sites in the Colombian Amazon. .......................... 66

Table 3-5. Number of species per genus in the 4 sites of the Colombian Amazon. ........ 67 Table 3-6. The most abundant families in the four localities and the proportional

distribution of records (in percent). ................................................................................. 68 Table 4-1. Distribution of overall species diversity of mosses and liverworts across the six

height zones in the four localities of the Amazonia. ........................................................ 82 Table 4-2. Species richness and frequency for the three most diverse families across the

six height zones. R: records per zone and Sp: number of species per zone. .................. 83 Table 4-3. Two informative axes from DCA per site, showing the variation in percentage

and the correlation coefficient ......................................................................................... 84 Table 5-1. Primers used in this study. ...........................................................................101

Table 5-2. Samples of Cheilolejeunea rigidula, with locations, zone of the tree where they

were collected, and markers successfully sequenced. Amazonas (AM), Caquetá (CA),

Putumayo (PU), Vaupés (VA), Manaus (MAN), Mabura Hill (MAB), and Tapajos (TAP).

Trunk zone (1, 2, 3) and canopy zone (4, 5, 6). .............................................................101 Table 5-3. Species used to realize the distance analyses based on the Neighbor Joining

(NJ) algorithm (Sequences from GenBank) and geographinc origin of the sample. .......104

Table 5-4. Molecular variance analysis in Cheilolejeunea rigidula from the variation

observed at seven Localities: Amazonas, Caquetá, Putumayo, Vaupés, Manaus, Mabura

Hill and Tapajos. The p-value represents the result of a test consisting of 1023

permutations. ................................................................................................................111 Table 5-5. Molecular variance analysis in Cheilolejeunea rigidula from the variation

observed at six groups (height zone in the tree, zone 1 to zone 6). ...............................111 Table 5-6. Molecular variance analysis AMOVA and Fixation index Fst, in Cheilolejeunea

rigidula from the variation observed at two groups (sections in the tree, canopy and trunk).

The p-value represents the result of a test consisting of 1023 permutations. .................112 Table 5-7. Haplotypic (h) and nucleotidic (π), diversity of the geographical regions with

their corresponding standard deviation (SD). .................................................................112 Table 5-8. Haplotypic (h) and nucleotidic (π), diversity of the height zones in the tree, with

their corresponding standard deviation (SD). .................................................................113 Table 5-9. Haplotypic (h) and nucleotidic (π), diversity of the sections in the tree, with

their corresponding standard deviation (SD). .................................................................113

Reserve El Zafire, Amazon

Chapter 1 22

1. Introduction

The amazon region is notable for its great biodiversity of the ecosystems in the world.

Exact figures to quantify the diversity do no yet exist and estimates of species number are

still increasing. Nevertheless, the understanding of the origin and distribution of the

biodiversity in the Amazonian forest are becoming better (Hoorn & Wesselingh, 2011;

Stropp, 2011; ter Steege et al., 2000, 2013).

The bryophytes are an important component of the diversity in the Amazonia. They are

very small plants with alternation of generations in which the haploid gametophyte is

dominant and the sporophyte remains united to the gametophyte and is fed by it. The

three major groups of bryophytes - mosses, liverworts, and hornworts - comprise the

earliest lineages of land plants derived from green algal ancestors. These plants have an

elemental morpho-anatomy, lack lignin and vascular tissues, present severe ecological

restrictions and are highly dependent on microclimatic conditions. Nevertheless,

Bryophytes play a substantial role in nutrient cycling. For example, they release nutrients

that are made available to other organisms by leaching upon decomposition and, to a

more limited extend, by herbivory. In addition, bryophytes sometimes form symbiosis with

cyanobacteria that are capable of fixing atmospheric nitrogen. Bryophytes are also

important in process of vegetation succession and soil formation. For instance, they may

promote soil formation by accelerating physical and chemical weathering, by trapping

wind-blown organic and inorganic material, and by contributing directly to undecomposed

organic matter (Vanderpoorten & Goffinet, 2009).

Bryophytes include nearly 15,000 species in more than 1200 genera worldwide. In

Colombia, according to the most recent catalogs, there are 932 species of mosses,

corresponding to 255 genera and 62 families (Churchill, 2016): 713 species of liverworts

in 131 genera and 39 families (Gradstein & Uribe, 2016); and 13 species in seven genera

and four families of hornworts (Gradstein & Uribe, 2016). Just how abundant the three

groups of bryophytes are in Colombia is shown by the following figures reported for

tropical America: 2600 species of mosses in 402 genera and 76 families, 1350 species of

Chapter 1 23

liverworts in 191 genera and 41 families, and 30 species of hornworts in 10 genera and 3

families (Gradstein et al., 2001).

1.1 Amazonian Forest

The Amazon rain forest covers an area of nearly 6.8 km2 in the northern part of South

America and has the largest rainforest on the earth (Figure 1-1). Humid forest covers

approximately 80% of this (5.5 million km2); the remaining 20% is covered by dry forest

(1%), flooded forest (3%), grass and scrublands (5%), short or sparse vegetation (1%),

and agricultural and urban areas (10%) (Stropp, 2011). The forests located in lowland

Amazonia grow in areas characterized by a mean annual temperature above 24°C, an

elevation below 700m, and a mean annual rainfall above 1,400 mm (Eva et al., 2005).

Figure 1-1. Geographical limits of Amazonia (http://earthobservatory.nasa.gov).

http://earthobservatory.nasa.gov/

Chapter 1 24

The Amazon River is 6400 km long, from its source in the Andes to its mouth in the

Atlantic, and the drainage basin includes a variety of landscapes such as Tepuyes in the

north, the forested slopes at the foot of the Andes in the west, and the wide tracts of

rainforest in the central part of the basin (Hoorn & Wesselingh, 2011). Amazonian forests

include principally forest communities that are defined by local environment and soil type.

Dry-land forests (bosques de tierra firme) comprise areas with natural vegetation that is

not subject to flooding, situated in higher areas. Floodplain forests (bosques de planicie

inundable) are subjected to seasonal flooding during periods of high river level. Based on

the type of water, two different habitats can be identified, Varzéa (comprises forest

located along white water rivers) and Igapó (comprises forest located along black water

and mixed water rivers). Other small environments are found, but they cover smaller

areas, as secondary forest (bosques secundarios), lacustrine environments (ambientes

lacustres), swamps (zonas anegadas), and river beaches (ambiente de playas) (Rudas &

Prieto, 2005). These lowland Amazonian forests grow on a variety of tropical soil types,

as ferralsols, acrisols, plinthosols, gleysols, cambisols, leptosols, arenosols, fluvisols,

regosols, lixisols, podzols, alisols, histosols, and nitisols (Quesada et al., 2011).

The amazon system plays a significant role in the climate of the world as it produce about

20% of the oxygen. In addition, the rainforest is responsible for 10% of the net primary

productivity of the whole terrestrial biosphere (Subramaniam et al., 2008). The present

study focuses on dry-land forests (bosques de tierra firme). This forest is the dominant

forest type, covering approximately 80% of the total area of Amazonia (ter Steege et al.,

2000, 2013). The range of the canopy height in this forest type is 25 to 35m, and the

understory is usually dense (Ribeiro, 1999).

1.2 Colombian Amazon

The Colombian Amazonia has an area of 483.911 km2, which represents 42% of the

national land area and 6% of the Amazon region. The following territories of the

Amazonas are represented here, including 17 protected areas, Amazonas, Caquetá,

Guainía, Guaviare, Putumayo and Vaupes and partially Vichada, Meta, Cauca, and

Chapter 1 25

Nariño (Figure 1-2). The area includes parks, reserves, and flora and fauna sanctuaries

together representing 17.2% of the Amazon region. One can find rock sediments from the

Tertiary and outcrops of the Guiana Shield, represented by the Serranías Naquen, La

Lindosa, Chiribiquete and Taraira.

The Colombian Amazon belongs to two of the largest watersheds in the world, those of

the Orinoco and Amazon rivers. Several rivers also drain into them, many of which have

their sources in the Andean mountain range. The largest rivers in the region in Colombia

are: Guaviare, Vaupés, Caquetá, Putumayo and Amazon. The Colombian Amazon is flat

with hilly and irregular areas and soil that ranges from badly drained soils in the alluvial

plains to extremely well drained surfaces with igneous or metamorphic origins. Much of

the soil is fine and medium, but some areas have sandy soils (Cortés et al., 1979).

Figure 1-2. Geographical limits of the Colombian Amazon, according to (SINCHI, 2010).

In general, the Amazonian soils have very low fertility, due to high acidity and very low or

absent cationic interchange capacity, as well as base saturation, very low phosphorous

content and very high aluminum content. Organic material content is almost absent in

horizontal surfaces and practically absent in underlying horizontals (Rangel, 2008).

Chapter 1 26

1.3 Bryophyte Ecology

Their high capacity to retain water, store carbon and heavy metals makes bryophytes very

important in the water economy of the forests. As poikilohydric plants, they are

significantly affected by external environmental conditions, making them effective

indicators of ecological conditions. However, today we know that microclimatic conditions

are what most affect the distribution of bryophytes and that the hypothesis of Baas

Becking (1934), that “everything is everywhere, but the environment selects” is what best

explains the distribution of bryophytes in tropical forests (Estébanez et al., 2011).

The small size of the plants makes them less dependent on meso or macroclimatic

conditions. Furthermore, the quantity and size of the diaspores, sexual as well as asexual,

make long-distance dispersion easier, so that the area of distribution is very wide. While

the above is completely true when distributions on a family level are analyzed, given that

75% of them have a cosmopolitan or subcosmopolitan distribution (Tan & Pócs, 2000),

when the distribution of genera or species is analyzed, it is observed that they are more

limited and are subject to strong geographical restrictions. In spite of the fact that many

aspects of the biogeography of bryophytes are still unknown, these show patterns very

similar to those of angiosperms and apparently are affected by similar geographical

barriers. In bryophytes these impediments are diminished by their characteristic long-

distance dispersion capacity, however. As a result, some have very wide distribution

areas and Bryophytes show very low endemism percentages (Estébanez et al., 2011).

Bryophyte species grow on substrates that are patchily distributed. They are more

strongly linked to substrate patches than are vascular plants. For these reasons,

metapopulation theory is particularly applicable to bryophytes. A metapopulation is a set

of populations linked by dispersal. A patch is the place with the conditions that are

suitable for the species. Where the species is present in a patch it is referred to as a local

population. Local dynamics are caused by population processes and interactions with

other species. The local population may eventually become extinct –local extinction- in

which case it can only re-occur if it is successfully dispersed from another local population

in the metapopulation. The occupancy, is determinate by the balance between local

extinctions and colonizations (Goffinet & Shaw, 2009). The study of the abundance and

Chapter 1 27

composition of bryophyte communities in different strata of the forest has shown that the

canopy can harbor more species than the undergrowth (Gradstein, 1992; Mota de

Oliveira, 2010) and that the high sensibility to microclimatic conditions can be related to

the establishment and formation of communities, manifesting species that are exclusive to

certain strata and other species that are present in any strata; in this way ecological

groups are formed, such as specialist epiphytes (heliophiles and ombrophiles) and

generalist epiphytes (Mota de Oliveira, 2010; Richards, 1984).

Ecological communities composed of bryophytes are represented by a number of species

that coexist, with different cover, niche amplitude, and specificity in relation to the

microhabitat and growth patterns that are manifested as a response to ecophysiological

characteristics (Cornelissen & ter Steege, 1989; Mota de Oliveira et al., 2009; Mota de

Oliveira & ter Steege, 2013; Richards, 1984). Gimingham and Birse (1957) showed that

the spectrum of growth pattern in several communities was related to the physical factors

of the environment, especially to light and humidity.

The composition of bryophyte species communities in Amazonian forests has been

attributed to two processes: dispersal (dispersal limitation) and niche (environmental

conditions). These two processes affect the composition of the community. In addition, by

means of field studies, it has been possible to establish that the importance of each

process depends not only on the scale but also on the biology of the group studied (Mota

de Oliveira, 2010).

The distribution of bryophytes along a vertical gradient (high areas on a tree) is widely

known (Cornelissen & ter Steege, 1989; Sylvia Mota de Oliveira, 2010; Richards, 1984;

Gradstein, 1992). The restriction of some species of bryophytes to the canopy has also

been observed in Amazonian forests (Cornelissen & ter Steege, 1989). This, in addition to

the capacity of the species to adapt to lower areas of the tree when a wide clearing

appears in the canopy (Acebey et al., 2003), sustains the clear idea of the niche effect,

understood as the relationship between the presence of the species and the

environmental conditions. In this way communities of epiphytic bryophytes in tropical rain

forests show a gradient in composition from the base to the top of the trees. However,

these studies have been done mainly on a local scale. To be able to determine which

Chapter 1 28

biological mechanism addresses the composition and structure of the communities of

epiphyte bryophytes to a greater degree, it is necessary to perform studies on a local

scale (sites) and on a regional scale (Colombian Amazon).

1.4 Bryophyte studies in the Colombian Amazon

In older studies on bryophytes in the Amazon, very few records from the Colombian

Amazon were included, principally because these studies took place in larger water

basins such as the Orinoco, Rio Negro and Amazon. Although we are sure that Spruce, in

his trips, “touched” territory that is now Colombia, we have no evidence that he took

collections there. In the Colombian Amazon, work relating to epiphytic bryophytes was

recently carried out. Ruiz & Aguirre (2004) studied the vertical distribution of bryophytes

on different types of phorophytes in several landscapes of Tarapaca (Amazonas), finding

specificity of species in the canopy and the undergrowth; they also analyzed the

selectivity of the species in different types of habitats. Benavides (2004) studied the

floristic abundance and composition of bryophytes in two types of forests in the

Colombian Amazon: in non-flooded forests of solid ground and in flooded forests in the

floodable plains of the Caquetá River, finding differences in the distribution of bryophyte

life forms and habitat in the two types of forest. Benavides (2006) presented the

abundance of moss and liverwort species and the distribution of bryophytes in the

undergrowth in four different types of forests in Caquetá (Amazon).

In addition, some studies of bryophyte communities in the Amazon have considered

regional approximations (Benavides et al., 2006; Florschütz-de Waard & Bekker, 1987;

Gradstein et al., 1990; Mota de Oliveira, 2010) and local studies in the region correspond

principally to inventories based on samplings of the undergrowth, with some exceptions

(Lisboa, 1976; Zartman, 2003). These studies in the Amazon have allowed an

approximation of the abundance of bryophyte species, which varies from 40 to 120

species per hectare (Mota de Oliveira, 2010).

Chapter 1 29

1.5 Scope and outline of this thesis

This study was designed to respond to the following question: What is the contribution of

dispersal and niche effect on the structure of the bryophyte community in the Colombian

Amazon? To answer this question, I designed the following hypothesis: On a regional

scale, niche assembly is determining the species composition in the epiphyte bryophyte

community. To answer the question and define the validity of our hypothesis, this study

was structured in the following manner:

Chapter 2. Based on botanical material studied, new records of species in the Colombian

Amazon and in Colombia are presented. This chapter provides illustrations, discusses

diagnostic characteristics, and gives information on localities and species distribution

throughout the high areas.

Chapter 3. In this chapter the floristic characterization of epiphyte bryophytes in the

Colombian Amazon is presented, drawn from botanical collections obtained in fieldwork.

Lists of species, genera and families are included.

Chapter 4. Studying species composition of communities in six zones of trees from four

forests in the Colombian Amazon; we determine whether vertical zoning exists; in other

words, does the species show a preference for different high areas in the trees. A species

indicator analysis is included in order to classify species as specialist or generalist. In

addition, this chapter establishes whether the composition of bryophyte communities is

related to geographical distance, that is, whether a pattern exists throughout the region of

the Caquetá, Vaupes, Putumayo and Amazonas departments.

Chapter 5. One of the most abundant species of the Amazonian water basin,

Cheilolejeunea rigidula, was selected to study dispersal throughout the Amazon using

molecular markers. Data obtained in this study and some data obtained by (Mota de

Oliveira, 2010) were used. The genetic distance between different localities was

compared in order to establish relationships among the individuals.

Chapter 1 30

Chapter 6. In this final chapter, we will summarize and conclude the research

contributions of this dissertation, as well as discuss directions for future research in the

Amazon.

Macaquiño community, Vaupés

Chapter 2 32

2. New records of epiphytic bryophytes from the Colombian amazon

Published in Crytogamie, Bryologie 35(1): 77-92, 2014. Additions to the Catalogue of Hepaticae of Colombia II - (Campos, Gradstein, Uribe, & ter Steege, 2014). Published in Phytotaxa, 152(1): 50-52, 2013. Transfer of Vitalianthus urubuensis (Lejeuneaceae) to Cheilolejeunea - (Wei, He, Gradstein, Campos, & Zhu, 2013).

2.1 Introduction

The flora of bryophytes in Colombia is very rich and it is characterized by a high diversity.

In Colombia Marchantiophyta includes 797 species: 713 accepted species (in 39 families

and 131 genera) and 84 doubtful species (Gradstein & Uribe, 2016). Colombia ranks

second among the countries of tropical America, after Brazil (ca. 725 accepted species;

(Gradstein & Costa, 2003). Ecuador ranks third with ca. 700 accepted species and about

80 doubtful ones (León-Yánez et al., 2006; Benitez & Gradstein, 2011; Benitez et al.,

2012; Schäfer-Verwimp et al., 2013), followed by Costa Rica with 574 species (Dauphin,

2005) and Bolivia with 477 species and numerous doubtful ones (Churchill et al., 2009).

The Catalogue of Hepaticae and Anthocerotae of Colombia (Uribe & Gradstein, 1998)

reported 832 species of liverworts. Since this publication many additional species of

liverworts have been reported for Colombia. Ninety-one species have been newly

recorded from Colombia, including 63 species of Lejeuneaceae, 7 of Lepidoziaceae, 6 of

Frullaniaceae, 3 of Plagiochilaceae, 2 of Calypogeiaceae, Metzgeriaceae and Ricciaceae,

and 1 each of Acrobolbaceae, Cephaloziaceae, Cephaloziellaceae, Lophocoleaceae,

Pallaviciniaceae and Scapaniaceae. Four species from Colombia were described as new

to science: Acrobolbus caducifolius R.M. Schust. (Schuster, 2001), Frullania dulimensis

Uribe, (Uribe, 2006), Harpalejeunea grandis Grolle & M.E. Reiner (Grolle & Reiner–

Drehwald, 1999) and Harpalejeunea scabra Gradst. & Schäf.-V. (Gradstein & Schäfer-

Verwimp, 2011). In addition, more than 200 species have been reduced to synonymy or

are considered doubtful records (Gradstein & Uribe, 2016).

Chapter 2 33

In addition, Bryophyta has 932 accepted species (in 62 families and 255 genera) and 22

doubtful ones (Churchill, 2016). Among the neotropical countries, Colombia ranks as the

most diverse with 932 accepted species, followed by Bolivia with 918 species (Churchill et

al., 2009), Brazil with 911 (Pinheiro da Costa et. al., in prep.), Ecuador with 807, Peru with

775, and Venezuela with 734 (Churchill, 2009). The estimates for Colombia and other

Neotropical countries reflect both the continued changes provided by revisionary studies

and the criteria applied to accepted species for checklists. Revisionary studies are more

likely to reduce the number of previously described species, but some additional species

may also be found.

In this chapter illustrations and brief discussions of diagnostic morphological characters

are given for each species. Information about localities, elevation and occurrence of the

species in the different tree height zones is also given.

2.2 Methods The data in this study were obtained in fieldwork in four localities of the Colombian

Amazon over a period of 5 months (January, February, March, April and May). The

specimens were processed at the Herbario Nacional Colombiano (COL). Some

collections were deposited at the Herbario Amazonico Colombiano (COAH).

Nomenclature of bryophytes was based on (Gradstein & Uribe, 2016), and (Churchill,

2016).

2.2.1 Study area

Fieldwork was carried out in four non–seasonally flooded forests in the southern section

of the Colombian Amazon, in Amazonas, Caquetá, Putumayo and Vaupés departments.

These forests occupy fairly well-drained soils that are relatively rich in available nutrients.

Canopy height varied from 30 to 40 m. All new records were collected in forest at

elevations between 100 and 230m.

Chapter 2 34

These forests have an average annual rainfall of ca. 3 300 millimeters. December -

January has the lowest monthly values whereas the maximum monthly values are from

May to June. The average temperature in the region is 25.3°C, with a minimum level of

21°C and a maximum level of 30.2°C. June and August have the lowest minimum values

while the maximum values are in December and January. Some dominant Angiosperm

families in the forest are Fabaceae, Rubiaceae, Melastomataceae, Moraceae,

Annonaceae, Araceae, Euphorbiaceae, Clusiaceae, Lauraceae, Arecaceae (SINCHI,

2010).

Four study sites were selected; their location is as follows (Figure 2-1):

1. "Reserve El Zafire" in the eastern part of the Department Amazonas, in the

Trapezio amazónico (3°59’ S and 69°53’ W).

2. "Raudal La Gamitana" in the southeastern part of the Department Caquetá, near

the Yarí River (0°14’ S and 72°25’ W).

3. "Corregimiento Puerto Colombia" in the southeastern part of the Department

Putumayo (0°36’ N and 74°21’ W).

4. "Macaquiño community" in the northeastern section of the Department Vaupés

(1°16’ N and 70°6’ W).

2.2.2 Data collection

Epiphytic bryophytes were sampled on mature trees in 6 height zones, from the base to

the outer canopy zones (1: tree base; 2: lower trunk; 3: upper trunk; 4: inner canopy; 5:

middle canopy; 6: outer canopy) as described by Cornelissen and ter Steege (1989) and

climbed using a static rope technique (Perry, 1978; ter Steege & Cornelissen, 1988; ter

Steege & Cornelissen, 1988). Epiphylls were not included. The communities of

bryophytes were sampled on 64 trees (16 trees in each site study), using six plots of 40

cm2 per tree, as described by Mota de Oliveira (2009). Thus, there were 96 plots per

study site and a total of 384 for the Colombian Amazon. Samples of all species were

collected for identification in the laboratory and subsequently deposited in the Herbario

Nacional Colombiano (COL) with some duplicated in the Herbario Amazonico Colombiano

Chapter 2 35

(COAH). Nomenclature of bryophytes was based on (Gradstein & Uribe, 2016), and

(Churchill, 2016).

Figure 2-1. Map of the study area, showing the sampling localities in the Colombian Amazon.

New records for Colombia and the Colombian Amazon are listed in alphabetical order

according to family. The records for Colombia provide comments, illustrations and

description of diagnostic characters for each taxon. Information about localities, altitude

and distribution on the trees is also given.

2.3 Results and discussion Eighteen liverworts species new to Colombia were collected (Campos et al., 2014):

seventeen species of Lejeuneaceae and one of Lepidoziaceae. The species in

Lejeuneaeaceae include Ceratolejeunea ceratantha (Nees & Mont.) Steph.,

Chapter 2 36

Ceratolejeunea confusa R.M. Schust., Ceratolejeunea desciscens (Sande Lac.) Schiffn.,

Ceratolejeunea laetefusca (Austin) R.M. Schust., Cheilolejeunea aneogyna (Spruce) A.

Evans., Cheilolejeunea clausa (Nees & Mont.) R.M. Schust., Cheilolejeunea neblinensis

Ilk.-Borg. & Gradst., Cheilolejeunea urubuensis (=Vitalianthus) (Zartman & I.L.Ackerman)

R.L.Zhu & Y.M.Wei, Cololejeunea cardiocarpa (Mont.) A. Evans., Cololejeunea diaphana

A. Evans, Diplasiolejeunea buckii Grolle, Drepanolejeunea anoplantha (Spruce) Steph.,

Leptolejeunea exocellata (Spruce) A. Evans., Microlejeunea aphanella (Spruce) Steph.,

Schiffneriolejeunea amazonica Gradst., Verdoornianthus griffinii Gradst., Verdoornianthus

marsupifolius (Spruce) Gradst. and Telaranea pecten (Spruce) J.J. Engel & G.L. Merr., in

Lepidoziaceae. In addition, one moss species new to Colombia was collected:

Syrropodon flexifolius Mitt. from Calymperaceae family. This study also reports new

records of epiphytic bryophytes to four departments of the Colombian Amazon, 36

species to Amazonas department, 58 species to Caquetá, 71 species to Putumayo and

56 species to Vaupés (Table 2-1, Table 2-2). The current list enumerates 82 species of

liverworts (spread across 39 genera and 9 families) and 27 species of mosses (in 13

genera and 11 families).

Chapter 2 37

NEW RECORDS TO COLOMBIA

CALYMPERACEAE Syrropodon flexifolius Mitt. (Figure 2-2 A-B) Plants tufted, soft, glossy, green to yellowish-green above, darker in older parts, often

tinged with pink below. Syrropodon flexifolius is characterized by dimorphic, long and

crispate-flexuous leaves when dry, and spreading to recurved when moist. Margins

usually bordered all around with elongate hyaline cells (Reese, 1993).

In the tree height zones 3, 4 and 5, alt. 115-220m. L.V. Campos 731 (COL). El Zafire

(Amazonas), Puerto Colombia (Putumayo) and Macaquiño (Vaupés).

Figure 2-2. Syrropodon flexifolius Mitt. A. Habit. B. Leaf, showing hyaline border.

Chapter 2 38

Lejeuneaceae

Ceratolejeunea ceratantha (Nees & Mont.) Steph. (Figure 2-3 A-B-C)

Plant characterized by leaves with seriate ocelli in a broken row, a toothed leaf apex and

ovate underleaves. This species may be confused with C. cubensis but the latter species

has leaves with 1-2 basal ocelli, which are not arranged in a row. Ceratolejeunea

ceratantha can also be confused with C. rubiginosa but the latter has moniliate ocelli (in

an unbroken row) and a toothed dorsal leaf margin (Dauphin, 2003).

In tree height zones 1, 2 and 3, alt. 115-190 m. L.V. Campos 720 (El Zafire, Amazonas),

and 731 (Macaquiño, Vaupés) (COL). General distribution: tropical America (Dauphin,

2003).

Ceratolejeunea confusa R.M. Schust. (Figure 2-3 D-E)

Characterized by underleaves 3-5 × stem width and perianths with 5 rounded keels

without horns. Ceratolejeunea confusa can be confused with C. cornuta but the latter

species differs by spherical lobules and horned perianths.

In tree height zones 2, 4, 5 and 6, alt. 140-210 m. L.V. Campos 721 (La Gamitana,

Caquetá), 733 (Puerto Colombia, Putumayo), and 734 (Macaquiño, Vaupés) (COL).

General distribution: tropical South America, Costa Rica (Dauphin, 2003).

Ceratolejeunea desciscens (Sande Lac.) Schiffn. (Figure 2-4 D-E)

This species can be easily recognized by its entire underleaves, leaves with (1-) 2-6 ocelli

in an unbroken row, usually entire leaf margins and perianths with bulbous horns

(Dauphin, 2003; Fulford, 1945). Utriculi are apparently absent. Ceratolejeunea desciscens

is a member of subg. Ceratolejeunea and the only species of this subgenus occurring in

lowland areas, the other members are montane taxa.

In tree height zones 1, 2, 3, 4 and 5, alt. 120-225 m. L.V. Campos 702 (La Gamitana,

Caquetá), 735 (Puerto Colombia, Putumayo), and 736 (Macaquiño, Vaupés) (COL).

General distribution: northern South America (Dauphin, 2003).

Chapter 2 39

Figure 2-3. Ceratolejeunea ceratantha (Nees & Mont.) Steph. A. Habit, ventral view. B.

Underleaf. C. Leaf, showing ocelli. - Ceratolejeunea confusa R.M. Schust. D. Gynoecium

and perianth. E. Habit, ventral view.

Chapter 2 40

Ceratolejeunea laetefusca (Austin) R.M. Schust. (Figure 2-4 A-C)

This species is recognized by caducous leaves, small underleaves that are two times

wider than the stem and perianths without horns. By the lack of perianth horns and

caducous leaves this species can be confused with C. guianensis, from which it can be

distinguished by its plane leaves, ovate underleaves with spreading segments, and the

absence of flagelliferous branches (Dauphin, 2003).

In tree height zones 2, 3, 4 and 5, alt. 130-210 m. L.V. Campos 703 (El Zafire,

Amazonas), and 737 (Puerto Colombia, Putumayo) (COL). General distribution: tropical

America (Dauphin, 2003).

Cheilolejeunea aneogyna (Spruce) A. Evans (Figure 2-5 A-B)

This species can usually be recognized by the leaves with a flat and rounded leaf apex,

paired lobule teeth, underleaves 2.5-4x stem width and frequent presence of

microphyllous branches with caducous leaves.

Cheilolejeunea aneogyna can be confused with C. oncophylla, which shares with C.

anaeogyna the somewhat recurved, obtuse leaf apex and mamillose leaf cells with

somewhat thickened outer wall. However, C. oncophylla has a much more strongly

thickened outer cell wall, smaller underleaves (usually less than 2.5 x stem width), smaller

trigones and lacks microphyllous branches and caducous leaves. Moreover, C.

oncophylla occurs mainly in montane forests (rarely in lowland rainforests; Gehrig-Downie

et al., in press) whereas C. anaeogyna is restricted to lowland rain forests areas of

tropical South America (Schäfer-Verwimp et al., 2013).

In tree height zones 1, 2, 3, 4, 5 and 6, alt. 100-210 m. L.V. Campos 704 (La Gamitana,

Caquetá), 738 (El Zafire, Amazonas), 739 (Puerto Colombia, Putumayo), and 740

(Macaquiño, Vaupés) (COL). General distribution: Amazonia, southeastern Brazil, coastal

Ecuador (Schäfer-Verwimp et al., 2013).

Chapter 2 41

Figure 2-4. Ceratolejeunea laetefusca (Austin) R.M. Schust. A. Habit, ventral view. B.

Underleaf. C. Leaf, showing ocelli. - Ceratolejeunea desciscens (Sande Lac.) Schiffn. D.

Portion of the stem, showing leaf and underleaf. E. Habit, ventral view.

Chapter 2 42

Cheilolejeunea clausa (Nees & Mont.) R.M. Schust. (Figure 2-5 C-D)

Plants large, with some caducous leaves. The outstanding character of C. clausa are the

large underleaves which are as wide as long or longer than wide, with the base widely

rounded and insertion line deeply arched. This species may be confused with C. trifaria

but in the latter the underleaves are wider than long. Moreover, C. trifaria is autoicous (C.

clausa is dioicous), (Gradstein & Costa, 2003).

In tree height zones 3, 4 and 5, alt. 120-210 m. L.V. Campos 722 (El Zafire, Amazonas),

and 741 (Puerto Colombia, Putumayo) (COL). General distribution: tropical America

(Gradstein & Costa, 2003).

Cheilolejeunea neblinensis Ilk.-Borg. & Gradst. (Figure 2-6 A-B).

Cheilolejeunea neblinensis is readily recognized by the enlarged cells along the lobule

keel, which are usually bulging outward, resulting in a crenate keel (Ilkiu-Borges &

Gradstein, 2008). The ovate-triangular lobule is tubular in appearance due to the inrolled

free margin, and has paired teeth at the apex like in Cheilolejeunea anaeogyna.



(Macaquiño, Vaupés) (COL). General distribution: Amazonia, Guayana Highlands (Ilkiu-

Borges & Gradstein, 2008; Mota de Oliveira & ter Steege, 2013).

Cheilolejeunea urubuensis (Zartman & I.L.Ackerman) R.L.Zhu & Y.M.Wei. (Figure 2-11

A-B)

This unusual species is easily recognized by the presence of a long unbroken row of large

and bright, golden-brown ocelli in the leaves, female bracts and perianths. The leaf apices

in C. urubuensis are rounded, the lobules rectangular with a long curved tooth, the

underleaf lobes elongate, obtuse and slightly diverging, and the perianths are rather flat,

widened to the apex and 4-keeled with two wide lateral keels. Within tropical America,

Cheilolejeunea urubuensis is the only vittate species in the genus (Wei et al., 2013).

Chapter 2 43

Figure 2-5. Cheilolejeunea aneogyna (Spruce) A. Evans. A. Habit, ventral view. B.

Portion of shoot showing lobule with two overlapping, paired teeth. - Cheilolejeunea

clausa (Nees & Mont.) R.M. Schust. C. Lobule. D. Habit, ventral view.

Chapter 2 44

Figure 2-6. Cheilolejeunea neblinensis Ilk.-Borg. & Gradst. A. Lobule showing paired

teeth at apex. B. Habit, ventral view. - Cololejeunea cardiocarpa (Mont.) A. Evans. C.

Habit. D. Leaf apex. E. Lobule.

Chapter 2 45

In tree height zones 5 and 6, alt. 100-220 m. L.V. Campos 713 (La Gamitana, Caquetá),

757 (El Zafire, Amazonas), 758 (Puerto Colombia, Putumayo), and 759 (Macaquiño,

Vaupés) (COL). General distribution: Amazonia (Zartman & Ackerman, 2002; Wei et al.,

2013; Mota de Oliveira & ter Steege, 2013).

Cololejeunea cardiocarpa (Mont.) A. Evans (Figure 2-6 C-E).

A common species, easily recognized by the whitish group of elongate dead cells at the

leaf apex. Sometimes they are finger-like extending from the apex. The leaf lobes in C.

cardiocarpa are typically elongate-ovate in shape and tapering to a narrowly rounded

apex, the leaf cells are thin-walled and smooth, and the lobule has 2 teeth.

In tree height zone 6, alt. 120-190 m. L.V. Campos 705 (La Gamitana, Caquetá), 745

(Puerto Colombia, Putumayo), and 746 (Macaquiño, Vaupés) (COL). General distribution:

pantropical (Gradstein & Costa, 2003).

Cololejeunea diaphana A. Evans (Figure 2-7 D-E)

This species has ovate-lanceolate leaves with entire margins and an obtuse apex. The

first tooth of the lobule consists of slightly elongate-rounded cells and is straight, pointing

to the leaf apex.

In tree height zone 1, alt. 180-190 m. L.V. Campos 724 (Macaquiño, Vaupés) (COL).

General distribution: pantropical (Gradstein & Costa, 2003 as Aphanolejeunea

truncatifolia Horik.).

Diplasiolejeunea buckii Grolle (Figure 2-7 A-C)

This species can be recognized by the strongly elongate lobules with a T-shaped first

tooth and by the large underleaves, which are about three times wider than the stem, with

segments 8-10 cells long. The lobules are inflated but never strongly swollen–involute

(Grolle, 1992)

In tree height zone 6, alt. 140-200 m. L.V. Campos 707 (La Gamitana, Caquetá), and 747

(Macaquiño, Vaupés) (COL). General distribution: a rare species from northern Amazonia

(Grolle, 1992)

Chapter 2 46

Figure 2-7. Diplasiolejeunea buckii Grolle, A. Habit, ventral view. B. Underleaf. C. Apex of

the lobule. - Cololejeunea diaphana A. Evans. D. Leaf. E. Habit, ventral view.

Chapter 2 47

Drepanolejeunea anoplantha (Spruce) Steph. (Figure 2-8 A-B)

This species is characterized by having two elongate ocelli in an unbroken row at the leaf

base, well-developed, fully inflated lobules, and narrowly elongated, upright leaves which

are usually more than 2 times longer than wide (Gradstein & Costa, 2003).



(Macaquiño, Vaupés) (COL). General distribution: West Indies, tropical South America

(Gradstein & Costa, 2003).

Leptolejeunea exocellata (Spruce) A. Evans (Figure 2-8 C-D)

This plant is easily recognized by the entire leaf margins, the rather short leaves with

obtuse to acute apices and, especially, by the large ocellus at the leaf base and the lack

of any further ocelli in the lamina (Gradstein & Costa, 2003).

In tree height zone 4, alt. 190 m. L.V. Campos 727 (Puerto Colombia, Putumayo) (COL).

General distribution: common throughout tropical America (Gradstein & Costa, 2003).

Microlejeunea aphanella (Spruce) Steph. (Figure 2-9 A-B)

This minute species is characterized by the obtuse to acute leaf apex, the smooth keel

and the presence of reduced lobules (Gradstein & Costa, 2003). In tree height zone 2, alt.

190 m. L.V. Campos 728 (Macaquiño, Vaupés) (COL). General distribution: a rare

species from Brazil, French Guiana and Colombia (Gradstein & Costa, 2003).

Schiffneriolejeunea amazonica Gradst. (Figure 2-9 C-D)

This species is characterized by the dull brown plant color, rectangular lobules with two

teeth, undivided underleaves, gynoecia without innovations and the perianth with two

long, sharp ventral keels extending over more than ½ the perianth length (Gradstein &

Ilkiu-Borges, 2009).

In tree height zone 6, alt. 180 m. L.V. Campos 729 (Macaquiño, Vaupés) (COL). General

distribution: Amazonia, Guianas (Gradstein & Costa, 2003).

Chapter 2 48

Figure 2-8. Drepanolejeunea anoplantha (Spruce) Steph. A. Habit, ventral view. B. Leaf,

dorsal view, showing ocelli. - Leptolejeunea exocellata (Spruce) A. Evans. C. Leaf, dorsal

view, showing ocellus. D. Habit, ventral view.

Chapter 2 49

Figure 2-9. Microlejeunea aphanella (Spruce) Steph. A. Habit, ventral view, showing one

reduced lobule. B. Portion of shoot, showing ocelli, dorsal view. - Schiffneriolejeunea

amazonica Gradst. C. Habit, ventral view. D. Leaf, showing the lobule.

Chapter 2 50

Verdoornianthus griffinii Gradst. (Figure 2-10 A-B)

This plant is characterized by the olive-green to brownish plant color, entire leaves with ±

isodiametric cells, one-toothed lobules, undivided underleaves, gynoecia without

innovations and perianths with 4-5 entire to slightly toothed keels. The leaf lobule in V.

griffinii is rectangular, about twice longer than wide and inflated over its whole length, with

a plane apex (Gradstein, 1994).

In tree height zone 6, alt. 100-210 m. L.V. Campos 711 (La Gamitana, Caquetá), 751 (El

Zafire, Amazonas), 752 (Puerto Colombia, Putumayo), and 753 (Macaquiño, Vaupés)

(COL). General distribution: Amazonia, French Guiana (Gradstein, 1994; Mota de Oliveira

& ter Steege, 2013).

Verdoornianthus marsupifolius (Spruce) Gradst. (Figure 2-10 C-D)

This species is close to V. griffinii but differs from the latter by the shorter, ovate-orbicular

lobule with the free margin folded inwards at the apex, forming a small apical pouch

(Gradstein, 1994).

In tree height zones 5 and 6, alt. 100-225 m. L.V. Campos 712 (La Gamitana, Caquetá),

754 (El Zafire, Amazonas), 755 (Puerto Colombia, Putumayo), and 756 (Macaquiño,

Vaupés) (COL). General distribution: northern Amazonia (Gradstein, 1994).

LEPIDOZIACEAE

Telaranea pecten (Spruce) J.J. Engel & G.L. Merr. (Figure 2-11 C)

Plants very small, made up of filamentose leaves consisting of only one single row of 3-5

cells. The perianths are elongate and laciniate at mouth (Fulford, 1968).

In tree height zone 1, alt. 135-215 m. L.V. Campos 730 La (Gamitana, Caquetá), and 760

(Macaquiño, Vaupés) (COL). General distribution: a rare species from northern Amazonia

and Guyana; in addition, the species has been recorded without voucher from Puerto

Rico (Engel & Merrill, 2004).

Chapter 2 51

Figure 2-10. Verdoornianthus griffinii Gradst. A. Gynoecium and perianth, ventral view. B.

Habit, showing leaves with inrolled lobules. - Verdoornianthus marsupifolius (Spruce)

Gradst. C. Leaf, showing orbicular lobule with inflexed apex. D. Habit, ventral view.

Chapter 2 52

Figure 2-11. Cheilolejeunea urubuensis (=Vitalianthus) (Zartman & I.L.Ackerman)

R.L.Zhu & Y.M.Wei. A. Habit with perianth, ventral view. B. Apical portion of lobule. -

Telaranea pecten (Spruce) J.J. Engel & G.L. Merr. C. Habit, showing uniseriate leaves.

Chapter 2 53

Table 2-1. New records of liverworts (Marchantiophyta) to Amazonia: Amazon: AM,

Caquetá: CA, Putumayo: PU and Vaupés: VA.

Species AM CA PU VA

Aneuraceae

Riccardia amazonica (Spruce) S.W. Arnell

X

Calypogeiaceae

Calypogeia laxa Gottsche & Lindenb. X X X X

Calypogeia tenax (Spruce) Steph.

X X

Mnioloma parallelogramum (Spruce) R.M. Schust.

X

X

Cephaloziaceae

Odontoschisma variabile (Lindenb. & Gottsche) Trev.

X

Frullaniaceae

Frullania apiculata(Reinw. et al.) Nees

X

Frullania caulisequa(Nees) Nees

X

X

Frullania kunzei (Lehm. & Lindenb.) Lehm. & Lindenb.

X

X

Lejeuneaceae

Anoplolejeunea conferta(Meissn.) A. Evans

X X X

Archilejeunea crispistipula(Spruce) Steph.

X X X

Archilejeunea fuscescens (Hampe ex Lehm.) Fulford

X X

Archilejeunea ludoviciana (Lehm.) Geissler & Gradst.

X

Archilejeunea parviflora (Ness) Schiffn. X X X X

Ceratolejeunea coarina (Gottsche) Steph. X X

Ceratolejeunea cornuta (Lindenb.) Schiffn.

X

Ceratolejeunea cubensis (Mont.) Schiffn. X X X X

Ceratolejeunea guianensis (Ness & Mont.) Steph.

X X X

Cheilolejeunea adnata (Kunze ex Lehm.) Grolle X

Cheilolejeunea holostipa (Spruce) Grolle & R.-L. Zhu X X X

Cheilolejeunea oncophylla (Ångstr.) Grolle & M.E. Reiner X X

Cheilolejeunea trifaria (Reinw. et al.) Mizut.

X X X

Cololejeunea contractiloba A. Evans X X X X

Cololejeunea gracilis (Jovet-Ast) Pócs & Bernecker

X

Colura cylindrica Herzog

X

Chapter 2 54

Species AM CA PU VA

Colura greig - smithii Jovet-Ast X X X X

Colura sagittistipula (Spruce) Steph.

X X X

Colura tenuicornis (A. Evans) Steph.

X X X

Cyclolejeunea luteola (Spruce) Grolle X X X X

Cyclolejeunea peruviana (Lehm. & Lindenb.) A. Evans

X

Diplasiolejeunea brunnea Steph.

X

Diplasiolejeunea cavifolia Steph.

X X

Drepanolejeunea araucariae Steph. X

X X

Drepanolejeunea crucianella (Tayl.) A. Evans

X

Drepanolejeunea lichenicola (Spruce) Steph

X X X

Drepanolejeunea orthophylla (Nees & Mont.) Bischl.

X

Drepanolejeunea palmifolia (Nees) Steph.

X

Frullanoides liebmanniana (Lindenb. & Gottsche)

X

Harpalejeunea oxyphylla (Nees & Mont.) Steph. X X X X

Harpalejeunea tridens (Besch. & Spruce) Steph. X

Lejeunea adpressa Nees

X

Lejeunea boryana Mont.

X X X

Lejeunea flava (Sw.) Ness

X

Lejeunea laetevirens Nees & Mont.

X

Lejeunea phyllobola Nees & Mont. X X

X

Lejeunea reflexistipula (Lehm. & Lindenb.) Gottsche

X

Lepidolejeunea involuta (Gottsche) Grolle

X X X

Leptolejeunea elliptica (Lehm. & Lindenb.) Schiffn. X

X X

Lopholejeunea eulopha (Tayl.) Schiffn. X

X X

Lopholejeunea subfusca (Nees) Schiffn. X

X X

Metalejeunea cucullata (Reinw. et al.) Grolle

X X X

Microlejeunea bullata (Tayl.) Steph. X X X X

Microlejeunea epiphylla Bischl. X

X

Pictolejeunea picta (Gottsche ex Steph.) Grolle X

Prionolejeunea aemula (Gottsche) A. Evans

X

Prionolejeunea denticulata (Weber) Schiffn.

X X

Prionolejeunea mucronata (Sande Lac.) Steph.

X

Chapter 2 55

Species AM CA PU VA

Prionolejeunea scaberula (Spruce) Steph.

X

Pycnolejeunea macroloba (Ness & Mont.) Schiffn.

X X X

Rectolejeunea berteroana (Gottsche ex Steph.) A. Evans

X

Rectolejeunea emarginuliflora (Gottsche) A. Evans X X X X

Shiffneriolejeunea amazonica Gradst.

X

Symbiezidium barbiflorum (Lindenb. & Gottsche) A. Evans X

X

Symbiezidium dentatum Herzog X

X

Symphyogyna brasiliensis (Nees) Nees & Mont.

X X X

Thysananthus amazonicus (Spruce) Schiffn.

X X

Xylolejeunea crenata (Nees & Mont.) X.L. He & Grolle

X X X

Lepidoziaceae

Bazzania cuneistipula (Gottsche & Lindenb.) Trevis. X

X

Bazzania diversicuspis Spruce

X X X

Bazzania hookeri (Lindenb.) Trevis.

X X

Micropterygium leiophyllum Spruce

X X

Micropterygium parvistipulum Spruce

X X

Micropterygium pterygophyllum (Nees) Trevis.

X X

Micropterygium trachyphyllum Reimers

X

Monodactylopsis monodactyla (Spruce) R.M. Schust. X X X X

Telaranea diacantha (Mont.) J.J. Engel & Merril

X

Lophocoleaceae

Chiloscyphus coadunatus (Sw.) J.J. Engel & R.M. Schust.

X

Leptoscyphus porphyrius (Nees) Grolle X X X X

Plagiochilaceae

Plagiochila disticha (Lehm. & Lindenb.) Lindenb.

X

X

Plagiochila montagnei Ness X

X X

Plagiochila simplex (Sw.) Lindenb. X X X X

Radulaceae

Radula javanica Gottsche

X

Radula mammosa Spruce X

Chapter 2 56

Table 2-2. New records of mosses (Bryophyta) to Amazonia. Amazon: AM, Caquetá: CA,

Putumayo: PU and Vaupés: VA.

Species AM CA PU VA

Calymperaceae

Calymperes erosum Müll.Hal. X X

Calymperes othmeri Herzog X X X

Calymperes rubiginosum (Mitt.) W.D. Reese

X

Syrrhopodon africanus (Mitt.) Paris

X

Syrrhopodon cryptocarpus Dozy & Molk.

X

Syrrhopodon fimbriatus Mitt.

X X X

Syrrhopodon hornschuchii Mart.

X

Syrrhopodon lanceolatus (Hampe) W.D. Reese

X

Syrrhopodon leprieurii Mont.

X X

Syrrhopodon ligulatus Mont. X X X

Syrrhopodon parasiticus (Brid.) Paris

X

Syrrhopodon simmondsii Steere

X X

Syrrhopodon xanthophyllus Mitt.

X X X

Fissidentaceae

Fissidens prionodes Mont.

X

Fissidens steerei Grout X X X X

Hypnaceae

Rhacopilopsis trinitensis (Müll.Hal.) E. Britton & Dixon X

Leucobryaceae

Leucobryum martianum (Hornsch.) Müll.Hal.

X

Octoblepharaceae

Octoblepharum albidum Hedw.

X

Octoblepharum pulvinatum (Dozy & Molk.) Mitt.

X

Octoblepharum stramineum Mitt.

X

X

Calymperaceae

Leucophanes molleri Müll.Hal. X

X X

Macromitriaceae

Schlotheimia torquata (Hedw.) Brid.

X

Chapter 2 57

Species AM CA PU VA

Phyllodrepaniaceae

Mniomalia viridis (Mitt.) Müll.Hal.

X

Pottiaceae

Hyophila involuta (Hook.) A. Jaeger X X X

Sematophyllaceae

Sematophyllum subpinnatum (Brid.) E. Britton X

Trichosteleum papillosum (Hornsch.) A. Jaeger

X

Thuidiaceae

Pelekium schistocalix Touw X

La Gamitana, Caquetá

Chapter 3 60

3. The epiphytic bryophyte flora of the Colombian amazon

Published in Caldasia 37(1): 47-59, 2015. The epiphytic bryophyte flora of the Colombian Amazon – (Campos, ter Steege, & Uribe, 2015).

3.1 Introduction

Bryophytes are important in terms of species richness and cover in many habitats, as well

as for ecosystem functioning (Goffinet & Shaw, 2009). Bryophytes are the first colonizers

of various different types of substrates, and in several landscapes produce a major part of

the biomass. In addition, epiphytic bryophytes are an integral component of forest

ecosystems and represent a significant part of the plant species diversity (Lesica et al.,

1991). They have important ecosystem functions as they increase structural complexity,

influence nutrient cycles and moisture retention, and provide habitats for plants and

animals (Rhoades et al., 1995).

Tropical forests harbor a rich diversity of bryophytes, because of their complexity and

variety of microhabitats (Gradstein, 1992). In the Colombian Amazon nearly of 221

species of bryophytes have been recorded, including 114 liverworts distributed in eleven

families and 44 genera, and 107 mosses, distributed among 23 families and 49 genera

(Churchill, 2016; Gradstein & Uribe, 2016). For the Amazon region an estimated 188

genera and 700 species of mosses and liverworts have been reported (Gradstein et al.,

2001). In Colombia, inventories and floristic studies on bryophytes have principally

focused on the Andean area. There are very few studies on bryophyte diversity patterns

in the Colombian Amazon, only one of these (Ruiz & Aguirre, 2004) sampled the trees,

and studied the vertical distribution of bryophyte diversity on different types of

phorophytes in several landscapes of Tarapacá (Amazonas). Other studies in the

Colombian Amazon (Benavides et al., 2006, 2004) focused on the bryophyte diversity in

flooded and non-flooded forests along the Caquetá River, and two areas of the

Chiribiquete and Araracuara regions.

Chapter 3 61

Here we provide the most updated inventory of the epiphytic bryophyte flora along of 64

trees distributed in four localities across the Colombian Amazon. Epiphytic bryophytes

were sampled on mature rainforest trees, from the base to the outer canopy. All the

species were collected in the framework of the project “Diversity of epiphytic bryophytes in

the Colombian Amazon”.

3.2 Methods

3.2.1 Study area

Fieldwork was carried out in four non-flooded seasonally forests in the Colombian

Amazon. This forest is the dominant forest type in the region and covers ca. 80% of the

total area of the Amazon basin (ter Steege et al., 2000), occupies fairly well drained and

non-flooded clayey soils. The forests have an average annual rainfall of ca. 3.300

millimeters. December - January has the lowest monthly means whereas the maximum

monthly means are from May to June. The average temperature in the region is 25.3°C,

with a minimum level of 21°C and a maximum level of 30.2°C. June and August have the

lowest minimum values while the maximum values are in December and January. Some

dominant Angiosperm families in the forest are Fabaceae, Rubiaceae, Melastomataceae,

Moraceae, Annonaceae, Araceae, Euphorbiaceae, Clusiaceae, Lauraceae, Arecaceae

(SINCHI, 2010). Canopy height of upland forest in the study sites varied from 30 to 40 m.

Four study sites were selected; their location and characteristics are showed in Figure 2-1 of the Chapter II and Table 3-1

Table 3-1. Site location and characteristics for the four study sites: Amazonas: AM,

Caquetá: CA, Putumayo: PU, and Vaupés: VA

Site Localities Alt. Lat. Long. AT MaxT MinT AP

AM "Reserve Zafire" 123 -3,99 -69,892 25.9 31.3 20.1 2832

CA "La Gamitana" 134 -0,244 -72,413 26.3 32.0 20.8 2891

PU "Puerto Colombia" 230 -0,608 -74,345 25.2 31.8 20.6 2893

VA "Macaquiño" 190 1,275 -70,1 25.6 31.6 20.6 3384

Chapter 3 62

Alt: Altitude, AT: Annual Temperature, MaxT: Max. Temperature, MinT: Min.

Temperature, AP: Annual Precipitation. Data from Bioclim (Hijmans et al., 2005).

3.2.2 Data Collection

Epiphytic bryophytes were sampled on mature trees, from the base to the outer canopy.

Epiphylls were not included. To climb trees a static rope technique was used as described

by Perry (1978), ter Steege (1998), ter Steege & Cornelissen (1988). The communities of

bryophytes were sampled on 64 trees (16 trees in each site study), using six plots of 40

cm2 per tree, as described by Mota de Oliveira (2009). Thus, there were 96 plots per

study site and a total of 384 for the Colombian Amazon.

Samples of all species were collected for identification in the laboratory and subsequently

deposited in the Herbario Nacional Colombiano (COL) with some duplicated in the

Herbario Amazonico Colombiano (COAH). Nomenclature of bryophytes was based on

Gradstein & Uribe (2016), and Churchill (2016).

3.2.3 Data Analysis

Epiphytic Species presence - absence matrices were prepared for all localities per tree as

well as per plot. Species abundance was not measured due to the difficulty of separating

the small individuals and to the variations in plant size. To quantify community structure

(species accumulation curves per locality and abundance distribution for the complete

dataset) we used frequency, viz. number of plots per site in which each species was

present, as a surrogate for abundance. Frequency values ranged from 1 to 96, being the

maximum number of plots per locality. Species richness per tree in each locality was

compared using the Shannon Index and by calculating evenness (Chao et al., 2005;

Magurran, 2013). The floristic similarity of epiphytic bryophytes in each study site was

tested with the Jaccard Similarity Coefficient (Magurran, 2013).

Chapter 3 63

3.3 Results

Eighteen liverworts species new to Colombia were collected seventeen species of

Lejeuneaceae and one of Lepidoziaceae (Campos et al., 2014), and one moss species

new to Colombian from Calymperaceae family (Chapter II). The 384 plots on 64 sampled

trees yielded 2827 records of bryophytes. The inventory contained 160 species (116

liverworts, 44 mosses), in 26 families and 64 genera; 95% of the species could be

identified. The epiphytic bryophyte flora was dominated by liverworts, which included 72%

of all bryophyte species. Most of them were leafy liverworts of the family Lejeuneaceae,

only two thallose species were recorded, Riccardia amazonica (Spruce) Gradst and

Symphyogyna brasiliensis (Nees) Nees & Mont.

The richness distributions showed a high proportion of families with few genera and

species, as well as a high proportion of genera with few species. Eleven families (42%)

and 32 genera (50%) were represented by one species; and twelve families (46%) were

represented by one genus. Twelve families (46%) and 27 genera (42%) were represented

by two to five species; and 13 families (50%) were represented by one genus (Table 3-2).

The average number of species per locality was 102. Species richness was highest in the

Putumayo site with 122 species (23 families, 57 genera), followed by Amazonas with 99

species (20 families, 48 genera), Vaupés with 98 species (15 families, 45 genera), and

Caquetá with 92 species (16 families, 41 genera) (Table 3-3, Figure 3-1).

From 160 species identified, 51 (32%) occur in all sites, 35 (22%) in three localities, 28

(18%) in two localities and 46 (28%) were restricted to one locality (Appendix). The

highest proportion of species recorded from only one locality was found in Putumayo

(15.6%). The number of bryophytes species per tree varied from 18 to 42 and the average

number of species per plot (40 cm2) was eight. The mean number of species per tree was

highest in the Putumayo site with 30.4±4.66, followed by Vaupes with 28.3±5.8,

Amazonas 26.5±4.0 and Caquetá with 25.8±4.72 (P<0.01). The Shannon index was

slightly higher in Putumayo (H´= 4.2) than in Amazonas (H´= 4.0), Caquetá (H´= 3.9) and

Vaupes (H´= 3.9), but evenness was similar in all localities (E = 0.5).

Chapter 3 64

Table 3-2. Distribution of species richness at family and genera level, and genera

richness at family level in Colombian Amazon.

Number of species

Families Genera Number of genera

Families # % # % # %

1 11 42 32 50 1 12 46 2 – 5 12 46 27 42 2 – 5 13 50 6 – 10 0 0 4 6 6 – 10 0 0 10 – 15 1 4 1 2 10 – 15 0 0 >15 2 8 0 0 >15 1 4

Table 3-3. Species diversity by locality

Locality S R SP SR Amazonas 99 675 8 5 Caquetá 92 668 7 2.5 Putumayo 122 763 8 15.6 Vaupés 98 721 8 6.2 Total 160 2827 8 7.3

S (total number of species), R (total number of records), SP (average species per plot),

SR (percentage of species restricted to each locality).

Figure 3-1. Species-accumulation curves for epiphytic bryophytes measured on sixteen

host trees (left) and ninety-six plots (right), in each site.

Chapter 3 65

The percentage of floristic similarity between the four sites in the Colombian Amazon was

53%, with a coefficient correlation of 0,69. The highest floristic similarity was found

between Caquetá – Vaupés and between Putumayo - Amazonas (59% and 57% each

one), and Putumayo-Vaupes was the lower similarity with 49%. In terms of species

richness there were no significant differences between the four localities (ANOVA; F =

2.52; p = 0.066), (Figure 3-2)

Figure 3-2. Boxplot of differences in species richness between the four localities in four

localities of the Colombian Amazon: Amazonas AM, Caquetá CA, Putumayo PU, and

Vaupés VA

Families, genera and species recorded are listed in Table 3-4 and Table 3-5, and in the

Appendix. The families with the highest number of records were Lejeuneaceae with 1556

(55% of the total), followed by Calymperaceae (294, 10%), Lepidoziaceae (224, 8%),

Octoblepharaceae (157, 6%) and Sematophyllaceae (138, 5%).

Chapter 3 66

Table 3-4. Family richness in the four sites in the Colombian Amazon.

Families Genera Species Lejeuneaceae 27 85 Calymperaceae 3 19 Lepidoziaceae 4 12 Plagiochilaceae 1 5 Sematophyllaceae 3 5 Calypogeiaceae 2 3 Frullaniaceae 1 3 Octoblepharaceae 1 3 Cephaloziaceae 1 2 Fissidentaceae 1 2 Hypnaceae 2 2 Lophocoleaceae 2 2 Macromitriaceae 2 2 Pilotrichaceae 2 2 Subtotal 52 (81,2%) 147 (92 %) Σ families with only one genera recorded 12 (18,8%) 13 (8%) Total 64 160

These five families also attained the highest abundance in each locality with few

exceptions, viz. Leucobryaceae in Caquetá and Cephaloziaceae in Vaupes (Table 3-6).

Lejeuneaceae, Calymperaceae and Lepidoziaceae were the most species-rich families,

with 85, 19 and 12 species, respectively. The most frequent genera in terms of number of

records were Cheilolejeunea (308 records), Pycnolejeunea (235), Archilejeunea (230)

Ceratolejeunea (214), Syrrhopodon (184), Octoblepharum (157), Bazzania (143),

Leucobryum (128), Sematophyllum (126) and Drepanolejeunea (114). These ten genera

accounted for the 65% of the total genera records. Syrropodon and Lejeunea were the

most species-rich genera, with 14 and 10 respectively, followed by Ceratolejeunea and

Cheilolejeunea with 9 species. The most frequent moss species in number of records

were Leucobryum martianum (128 records), Sematophyllum subsimplex (120),

Octoblepharum albidum (90) and Leucophanes molleri (89). These species included 33%

of the total moss records. The most frequent liverworts were Archilejeunea fuscescens

(162 records), Pycnolejeunea macroloba (119), Pycnolejeunea contigua (116),

Ceratolejeunea cornuta (103), Cheilolejeunea aneogyna (101), Cheilolejeunea rigidula

Chapter 3 67

(71) that accounted for the 54% of the liverwort records. As shown in Figure 3-3 (SAD -

species abundance distribution) these nine species included the 36% of the records in the

complete data set.

Table 3-5. Number of species per genus in the 4 sites of the Colombian Amazon.

Genera Species Syrrohopodon 14 Lejeunea 10 Ceratolejeunea 9 Cheilolejeunea 9 Drepanolejeunea 8 Plagiochila 5 Archilejeunea 4 Bazzania 4 Calymperes 4 Cololejeunea 4 Colura 4 Micropterygium 4 Prionolejeunea 4 Diplasiolejeunea 3 Frullania 3 Harpalejeunea 3 Lopholejeunea 3 Microlejeunea 3 Octoblepharum 3 Telaranea 3 Acroporium 2 Calypogeia 2 Cyclolejeunea 2 Fissidens 2 Leptolejeunea 2 Odontoschisma 2 Pycnolejeunea 2 Radula 2 Rectolejeunea 2 Sematophyllum 2 Symbiezidium 2 Verdoornianthus 2 Subtotal 128 (80 %)

Chapter 3 68

Genera Species Σ families with only one species 32 (20%) Total 160

Lejeuneaceae had the highest species richness by far in all four localities. In each site this

family included more than 50% of all bryophyte species (Amazonas and Caquetá 51%,

Putumayo 54%, Vaupés 57%). The next-highest species richness was seen in

Calymperaceae, Lepidoziaceae, Plagiochilaceae and Calypogeiaceae, at all four localities

(Figure 3-4). The Amazonas site has the largest proportion of families represented by

one species (65%), followed by Putumayo (52%), Caquetá (50%) and Vaupes (40%).

Table 3-6. The most abundant families in the four localities and the proportional

distribution of records (in percent).

Family Amazonas Caquetá Putumayo Vaupes

Lejeuneaceae 53.0 56.4 56.7 53.8

Calymperaceae 14.0 10.4 9.8 6.6

Lepidoziaceae 7.4 7.9 4.4 12.0

Octoblepharaceae 6.8 4.0 5.4 6.4

Sematophyllaceae 5.5 4.6 6.5 2.8

Leucobryaceae 5.2 4.8 3.9 4.3

Plagiochilaceae 1.8 3.0 3.3 1.6

Calypogeiaceae 1.6 1.6 0.6 2.3

Frullaniaceae 0.0 1.3 0.0 1.7

Cephaloziaceae 0.7 1.5 1.0 6.1

Stereophyllaceae 1.0 0.4 1.6 0.4

Lophocoleaceae

Other

0.7

1.6

2.5

1.2

1.8

4.7

0.5

1.2

Chapter 3 69

Figure 3-3. SAD - Species abundance distribution based on the complete dataset. (O

range points are representing the nine species that recorded the 36% of the records in the

data set).

Figure 3-4. Summary of the species richness per family in four localities of the Colombian

Amazon: Amazonas AM, Caquetá CA, Putumayo PU, and Vaupés VA

0

20

40

60

80

100

120

140

160

180

0 20 40 60 80 100 120 140 160 180

Num

ber o

f rec

ords

Species rank in abundance

0 20 40 60 80

Lejeuneaceae

Calymperaceae

Lepidoziaceae

Plagiochilaceae

Calypogeiaceae

Octoblepharaceae

Sematophyllaceae

Number of species

Fam

ilies

of b

ryop

hyte

s

VA PU CA AM

Chapter 3 70

3.4 Discussion

With 160 species recorded from 64 trees sampled from the base to the canopy, this study

is the first inventory of epiphytic bryophytes across the entire Colombian Amazon. Most of

the species recorded are widespread in the Amazon basin and also occur in Brazil,

Colombia, French Guiana, Guyana, and Ecuador (Benavides et al., 2006, 2004; Churchill,

1994; Mota de Oliveira et al., 2009; Mota de Oliveira & ter Steege, 2013; Zartman & Ilkiu-

Borges, 2007; Gradstein & Uribe, 2016; Churchill, 2016). Nevertheless, there is also a

high number of new records for the Colombian Amazon, especially in the Lejeuneaceae

(Campos et al., 2014). Many of these new records are from the forest canopy. Since the

canopy of the Amazonian forests of Colombia had been little studied, the high number of

new records found was to be expected.

Our results are consistent with the recent bryophyte inventory of the Amazon region by

Mota de Oliveira and ter Steege (2013), which focused on sites in eastern Ecuador,

Brazil, French Guiana, Guyana and used the same sampling method. In that recent study

72 trees were sampled and 261 species of epiphytic bryophytes distributed in 97 genera

and 29 families were identified. The average number of species per locality was 75, and

the average per plot was 9 species. In both studies Lejeuneaceae, Calymperaceae,

Plagiochilaceae and Sematophyllaceae were the most species-rich families.

Archilejeunea fuscescens, Ceratolejeunea cornuta, Cheilolejeunea rigidula,

Sematophyllum subsimplex and Octoblepharum albidum were the most common species.

The results of this study are also in agreement with the general description of the

bryophyte flora of the Amazon region by Gradstein (2001).

The Lejeuneaceae family was clearly the most dominant in the Colombian Amazon with

more than 50% of all species. Dominance of this family has also been reported in other

studies on lowland rain forest areas, e.g. by Mota de Oliveira and ter Steege (2013) with

47%, Gradstein (1995) with 70%, and Gradstein (2006) with 75%. These results and our

data show the importance of this family in the flora of tropical lowland forests (Richards,

1984; Schuster, 1983). It can be related with the consideration that Lejeuneaceae is the

most advanced and most highly specialized family among the leafy liverworts (e.g.,

Heinrichs et al., 2007; Wilson et al., 2007).

Chapter 3 71

There were floristic similarities between localities in the Colombian Amazon. The

localities share a high percentage of species, 72% presents in more than one site (32% in

all sites, 22% in three sites and 18% in two sites) and 28% of species restricted to one

site (Appendix). Species richness (number of species per site) was rather similar among

sites, except for Putumayo where the number of species was slightly higher. This could

be related to the influence of the northern Andes. Putumayo is the site with the highest

elevation in the study (230 m). This condition may favor the presence of Andean species.

Surprisingly, most of the species found only in Putumayo (80%) have a predominant

Andean distribution (Churchill, 2016; Gradstein & Uribe, 2016). The northern Andes has a

highly diverse vegetation and flora, due to the variation in climate and elevation

(Gradstein et al., 2001). Mota de Oliveira & ter Steege (2013) in their study, of nine

localities, also reported a higher number of species in the locality with the highest

elevation, which was also adjacent to the Andes.

Puerto Colombia, Putumayo

Chapter 4 74

4. Vertical Distribution and Diversity of Epiphytic Bryophytes in the Colombian

Amazon.

4.1 Introduction

Bryophytes are a conspicuous and important component of the epiphytic flora in tropical

rainforests (Frahm & Gradstein, 1991; Acebey et al., 2003; Wolf, 1993). Bryophytes are

important in terms of ecosystem functioning and species richness (Goffinet & Shaw,

2009). In addition, bryophytes influence forest nutrient cycles by expanding surface areas,

thereby increasing atmospheric deposition of nutrients (Nadkarni, 1986) and are

important in the regulation of hydrological cycles (Veneklaas & Van Ek, 1990).

In lowland Amazonian forests bryophytes are generally found segregated across a

vertical zonation on host trees (Cornelissen & ter Steege, 1989; Gradstein et al., 1990;

Montfoort & Ek, 1990; Mota de Oliveira et al., 2009; Mota de Oliveira & ter Steege, 2013,

2015). Despite the relevance of the vertical stratification of Amazonian epiphytic

bryophytes, bryophyte research in the Colombian Amazon has been restrictedto the

understory (Benavides et al., 2006, 2004).

Microclimate and bark structure (texture, chemistry) are considered important and

determining factors in the distribution and establishment of the epiphytic bryophytes within

the forest. The inclination of the trunk and branches also contributes to the vertical

distribution of the cryptogamic epiphytes (Cornelissen & ter Steege, 1989; Richards,

1984; Szövényi et al., 2004). Because of their poikilohydric nature, bryophytes are

sensitive indicators of climatic conditions and environmental changes. Bryophyte

assemblages show rapid changes in composition and vertical shifts on the host trees

when microclimatic conditions change due to deforestation or habitat transformation

(Acebey et al., 2003; Frego, 2007; Sporn et al., 2010).

The distribution of bryophytes along phorophytes in the rainforest can be associated with

species-specific preferences to microclimatic conditions. The characteristics of the

Chapter 4 75

environment change from the bottom of the rainforest upwards into the canopy (Allee,

1926); in the canopy temperatures are higher and humidity is lower than on the forest

floor limiting the ability of drought intolerant species to survive (Kumagai et al., 2001). In

this way, some species may grow in an euphotic habitat, in full light (on the outer

branches and twigs of the canopy) or under a significant amount of light in exposed

branches in the interior but still receiving full sunlight. A different group species grow in

oligophotic habitats, in shady and moist conditions (growing on the lower part of the

canopy, trunks, small trees, decaying wood and ground surface). Some species are

generalists and can be found in both habitats (Gradstein & Pócs, 1989). According to

Richards (1984) sun (canopy) and shade (understory) epiphytes are ecological

“specialists,” while those occurring in almost all height zones are ecological “generalists”.

An important element in understanding diversity and its dynamics is to understand the

factors that determine how species coexist. The coexistence of species in communities

has been explained by two mechanisms, niche assembly or dispersal assembly (Mouillot,

2007). Both processes can drive community composition, and the relative importance is

related to the scale and the biology group under study (Mota de Oliveira et al., 2009).

Following Hubbell (2001) niche assembly states that communities are groups of

interacting species whose presence or absence is based on the ecological niches or

functional roles of the species, and dispersal assembly holds that communities are open,

species come and go, and their presence or absence is dictated by random dispersal and

stochastic local extinction.

The restriction of bryophytes species to the canopy has also been observed in

Amazonian forests (Cornelissen & ter Steege, 1989; Mota de Oliveira & ter Steege, 2013,

2015). Additionally, canopy species can survive in lower areas of the tree when clearings

occur in the canopy (Acebey et al., 2003). The vertical displacement of species in

disturbed habitats supports the idea of a niche effect. The niche effect can be understood

as the relationship between the presence of the species and the environmental

conditions. In this way communities of epiphytic bryophytes in tropical rain forests show a

gradient in composition from the base to the top of the trees, mainly related to their

physiological adaptations to the light intensity and air humidity (Holz et., 2002; Wolf,

1993).

Chapter 4 76

Dispersal ability is of great importance for plants, which commonly occupy spatially and

temporally limited substrate patches (Pohjamo et al., 2006). In general, bryophytes

species have broad geographic ranges that are frequently found in more than one

continent. Bryophytes have a tendency to exhibit wider distributions than vascular plants

(Vanderpoorten & Goffinet, 2009). In bryophytes, a few mechanisms play an important

role in dispersal. For instance, rain splash acting on the spores and vegetative gemmae is

a mechanism for short-range dispersal in the understory. Wind on the contrary is a long-

range dispersal mechanism of species growing in the outer canopy. In this case, species

able to grow in exposed areas have a better chance of effective dispersal than species in

sheltered sites. The easiness with which spores are collected by the wind and transported

allows them to travel several kilometers because of the small size and low weight of the

spores (Miller & McDaniel, 2004; Sundberg et al., 2006). However, the success of the

establishment for spore dispersed depends also on the suitability of the substrate or

habitat (Hallingbäck, 2002).

In order to study the significance of dispersal vs. habitat limitation, Lloret (1994),

compared the success of the three dominant forest floor mosses in colonizing

experimental gaps of 1m2. All three species colonized after experimental planting,

suggesting that the environmental conditions were not limiting. The experiment indicated

that two of the species were dispersal-limited, while the other was not. Short-distance

dispersal may often be by originated from vegetative fragments or specialized asexual

diaspores produced in many species. In that case, it is generally concluded that the most

effective dispersal is in the centimeter range (Laaka-Lindberg et al., 2003).

The present manuscript aims to understand the local and regional variation of epiphytic

bryophyte composition across the Colombian Amazon. We describe the epiphytic

communities of bryophytes in four localities, in Amazonas, Caquetá, Putumayo and

Vaupés departments, we also studied how are the communities structured and what are

the main environmental or spatial conditions that drive community structure and

composition. We focused on the vertical distribution of the different bryophyte

communities along the phorophytes to be able to determine the contribution of dispersal

and niche assembly in the structure of the communities. This is the first study to date that

includes sampling of whole trees including the canopy across the Colombian Amazon.

Chapter 4 77

The purpose is to analyze the vertical distribution, studying species composition of

communities in six zones of trees from the four forests; we aim to determine whether

vertical zonation exists. We explore whether the species show a preference for different

height zones in the trees. A species indicator analysis is included in order to classify

species as specialist or generalist. In addition, in this study we establish whether the

composition of bryophyte communities is related to geographical distance.

We expect the results to show a substantial set of indicator species, a clear vertical

gradient, and niche fidelity among sites, although with little geographic structure since our

hypothesis is based on the niche assembly principle implying that habitat specialization is

the dominant factor affecting the species assemblage of epiphytic bryophytes in the

Colombian Amazon.

4.2 Materials and methods Study area

Fieldwork was carried out in four upland forests in the Colombian Amazon. Upland forest

occupies fairly well drained and non-flooded clayey soils. The upland forest is the

dominant forest type, covering ca. 80% of the total area of Amazonia (ter Steege et al.,

2000, 2013). Canopy height of upland forest in the localities of the study varied from 30

to 40 m.

Four study sites were selected; their location is as follows (Figure 4-1):

1. "Reserve El Zafire" in the eastern part of the Department Amazonas, in the

Trapezio amazónico (3°59’ S and 69°53’ W).

2. "Raudal La Gamitana" in the southeastern part of the Department Caquetá, near

the Yarí River (0°14’ S and 72°25’ W).

3. "Corregimiento Puerto Colombia" in the southeastern part of the Department

Putumayo (0°36’ N and 74°21’ W).

4. "Macaquiño community" in the northeastern section of the Department Vaupés

(1°16’ N and 70°6’ W).

Chapter 4 78

The forests have an average annual rainfall of ca. 3,300 millimeters. December - January

has the lowest monthly means whereas the maximum monthly means are from May to

June. The average temperature in the region is 25.3°C, with a minimum of 21°C and a

maximum of 30.2°C. June and August have the lowest minimum values while the

maximum values are in December and January. Some dominant Angiosperm families in

the forest are Fabaceae, Rubiaceae, Melastomataceae, Moraceae, Annonaceae,

Araceae, Euphorbiaceae, Clusiaceae, Lauraceae, Arecaceae (SINCHI, 2010).

Figure 4-1. Map of the study area, showing the sampling localities in the Colombian Amazon.

Data collection

For each locality we established four plots of 50 x 50 m. According to Gradstein (1992)

and Frahm (2003), within the plot we selected four trees, the overall sample size for each

locality was of 16 trees (Figure 4-2). We sampled 64 full canopy trees on 4 sites in the

Colombian Amazon. We sampled epiphytic bryophytes on mature rainforest trees that

were stratified in 6 height zones: 1- tree base; 2- lower trunk; 3- upper trunk; 4- inner

canopy; 5- middle canopy; 6- outer canopy after Cornelissen and ter Steege (1989),

Chapter 4 79

(Figure 4-3). The 6 zones were treated as a surrogate for the microclimatic gradient

found from the base to the top of the forest. We used the static rope technique to climb

the trees in order to carry out the sampling in the different height zones (Perry, 1978; ter

Steege, 1998; ter Steege & Cornelissen, 1988).

Figure 4-2. Schematic plots of 50 x 50m per locality, showing the distance.

Figure 4-3. Schematic height zones on a full-grown tree. Z1: tree base; Z2: lower trunk;

Z3: upper trunk; Z4: inner canopy; Z5: middle canopy; Z6: outer canopy.

We sampled the bryophyte communities according to standard procedures, using one plot

of 40cm2 to sample each height zone. We had 6 aggregate plots for each tree, 96 for

Chapter 4 80

each locality, and 384 for the Colombian Amazon. We did not use abundance in our

research as size variation made it impossible to separate out individuals of each

species. Instead, frequency, measured as the number of plots in which each species was

found, was used as a surrogate of species abundance (Mota de Oliveira & ter Steege,

2013). Frequency was set to vary in the range of 1 to 96, the minimum and maximum

frequency possible at each site. In addition, we used the vertical zonation on the trees to

act as a surrogate for the differences in microclimatic conditions.

Samples of all species were collected for laboratory examination, and the identification of

all species of liverworts and mosses was done using light microscopy. The specimens

were processed at the National Colombian Herbarium (COL). Some collections were

deposited at the Herbario Amazonico Colombiano (COAH). The nomenclature of

bryophytes was based on Frey & Stech (2009), Gradstein & Uribe (2016), and Churchill,

(2016). However, changes or alterations to the names of some species were made in

accordance with more recent publications.

Data analysis We used Detrended Corresponded Analysis (DCA) for plot ordination, using the

abundance data. We calculated the explained variation (R2) as the correlation between

the matrixes of distances in similarity between the plots, calculated as Sorensen

distances. We correlated the scores of the plots in the first axis of the ordination with their

respective height zone, as this was the expected main environmental gradient. In

addition, a Permutational Multivariate Analysis of Variance using a distance matrix in

each locality was carried out to calculate similarity among communities and to test if the

similarities among communities in the priori height zone classification were significantly

different from similarities among sites.

We evaluated the relationship between species composition and distance using a Mantel

Test (Legendre & Legendre, 1998). This test is used to test the null hypothesis of no

relationship between two (distance) matrices (McCune et al., 2002). All the analyses were

conducted in R statistical software and the vegan package (Team, 2014).

Chapter 4 81

We determined the preference of the species for each of the six height zones in each of

the localities using Indicator Species Analysis (Dufrêne & Legendre, 1997). The indicator

species analysis takes into account the relative abundance of a species in a high

frequency and relative species in this area. The indicator value (IV) weighs the

preferences of the species for a particular zone using the distribution of the relative

frequencies. A randomization procedure tests for the significance of the indicator value

obtained for each species.

We calculated the weighted average height zone for all species in the four localities. The

height zone of the species was based on the abundance and number of occurrences per

zone; the number indicates the mean zone preference. We compared the zone

preference among the same species to verify whether those species considered specialist

by the indicator species analysis in the locality separately maintained their preferred zone

across the region.

4.3 Results Species Richness

The survey of epiphytic bryophytes across the Colombian Amazon (Amazonas, Caquetá,

Vaupés and Putumayo departments), using 384 (40 cm2) plots on 64 trees, resulted in

2827 occurrences of bryophytes. We found an overall of 160 (morpho-) species of

bryophytes (116 liverworts and 44 mosses) (Campos et al., 2015). The bryophyte species

identified belonged to 26 families and 64 genera. Eighteen liverwort species were new

records for Colombia, including seventeen species of Lejeuneaceae and one of

Lepidoziaceae (Campos et al., 2014).

The richest families were Lejeuneaceae, Calymperaceae and Lepidoziaceae with 85, 19

and 12 species respectively. Syrropodon and Lejeunea were the most species-rich

genera, with 14 and 10 respectively, followed by Ceratolejeunea and Cheilolejeunea with

9 species each. The most common species were Archilejeunea fuscescens (Hampe &

Lehm.) Fulford, Leucobryum martianum (Hornsch.) Hampe ex Müll. Hal., Sematophyllum

subsimplex (Hedw.) Mitt., Pycnolejeunea macroloba (Mont.) Schiffn., Pycnolejeunea

contigua (Nees) Grolle, Ceratolejeunea cornuta (Spruce) Steph., and Cheilolejeunea

Chapter 4 82

aneogyna (Spruce) A. Evans. These species represent 30% of the total epiphytic

bryophyte records. Detailed information about general richness is given in Chapter III.

The highest number of species was found in the upper trunk (Z3) with 86 species,

followed by the tree base (Z1) with 78 species, the lower trunk (Z2) and the inner canopy

(Z4) with 77 species each, the middle canopy (Z5) with 75, and the outer canopy (Z6) with

59 species (Table 4-1). The upper trunk had the highest number of records (527-18% of

all records), while the outer canopy had the lowest number of records (376-13.3% of all

records). In terms of species richness there were significant differences between the six

height zones (F5,378 = 9.1; p < 0.05), (Figure 4-4).

Table 4-1. Distribution of overall species diversity of mosses and liverworts across the six

height zones in the four localities of the Amazonia.

Zone Lw Mo S R R% IS IF RS Ss

1 53 25 78 526 18 24 9 14 0.58

2 49 28 77 447 15.8 3 1 2 0.52

3 62 24 86 527 18.6 9 1 1 0.52

4 57 20 77 511 18 8 1 4 0.51

5 53 22 75 440 15.5 4 0 4 0.47

6 52 7 59 376 13.3 14 2 9 0.58

Lw: Number of liverworts species, Mo: Number of mosses species, S: Total number of species, R:

Number of records, R%: Proportion of records, IS: Number of indicator species, IF: Number of

indicator families, RS: Number of restricted species. Ss: Average Sorensen similarity.

Chapter 4 83

Figure 4-4. Boxplot of differences in species richness between the six height zones

The families with the highest number of records and species were Lejeuneaceae,

Calymperaceae and Lepidoziaceae (Table 4-2). This was also found in all of the sites we

studied. Nevertheless, Lejeuneaceae showed a special vertical distribution because the

records and number of species increased with the height zone (zone 1 to 6), while in the

other families the number of species and records tended to decrease. Table 4-2. Species richness and frequency for the three most diverse families across the

six height zones. R: records per zone and Sp: number of species per zone.

Families Zone 1 Zone 2 Zone 3 Zone 4 Zone 5 Zone 6 R Sp. R Sp. R Sp. R Sp. R Sp. R Sp.

Lejeuneaceae 148 31 189 35 274 44 285 43 298 43 362 50

Calymperaceae 90 12 74 13 63 11 46 10 18 3 3 3

Lepidoziaceae 81 11 44 7 42 7 32 6 25 5 - -

Chapter 4 84

Vertical distribution

We found a gradual differentiation of the bryophyte communities across the tree height

zones, with communities from the base of the tree different from the communities found in

the canopy (Figure 4-5). The two first DCA axes explained 63% of the total variation in

species composition (Table 4-3). The stratification of the bryophyte communities across

the height zones was repeated in each of the four sites Amazonas, Caquetá, Putumayo

and Vaupés (Figure 4-6).

Figure 4-5. DCA ordination (species scores) of 160 epiphytic bryophytes species and 384

plots across the Colombian Amazon. Different symbols represent the different height

zones: 1 (circle), 2 (triangle), 3 (square), 4 (plus), 5 (reverse triangle), and 6 (asterisk).

Table 4-3. Two informative axes from DCA per site, showing the variation in percentage

and the correlation coefficient

Eigenvalues DCA1 Variation DCA2 Variation R2 P<0.001 Amazonas 0.711 49.6% 0.363 25.3% 0.819

Caquetá 0.716 39.7% 0.385 21.4% 0.790

Putumayo 0.710 36.4% 0.474 24.3% 0.735

Vaupés 0.681 43.2% 0.351 22.3% 0.840

Chapter 4 85

Figure 4-6. DCA ordination (species scores) per locality of species (AM: 99 species, CA:

92, PU: 122, VA: 98) and plots (96 each one). Different symbols represent the different

height zones: 1 (circle), 2 (triangle), 3 (square), 4 (plus), 5 (reverse triangle), and 6

(asterisk).

We also found that the second axis of the DCA shows a gradual differenciation from

Vaupes to Putumayo to Caqueta to Amazonas (Figure 4-7). We found a strong

correlation between height and the position of the plot on the first axis of the DCA for the

combined data set (r2=0.772, P<0.001), (Figure 4-8). The correlation was also significant

for analyses of each site separately (Figure 4-9). Vaupes had the highest correlation

while Putumayo had the lowest among the sites.

Chapter 4 86

Figure 4-7. DCA ordination of 160 epiphytic bryophytes species and 384 plots across the

Colombian amazon. Different symbols represent the locality of the plots, AM: Amazonas

(circle), CA: Caquetá (triangle), PU: Putumayo (square), and VA: Vaupés (plus).

Figure 4-8. Correlation for the Colombian Amazon between the DCA1 and the height

zones. R2= 0.772, P<0.001

Chapter 4 87

Figure 4-9. Correlation for each site, showing the coefficient. AM Amazonas, CA

Caquetá, PU Putumayo and VA Vaupés.

The composition of the species at the different height zones was tested using a

Permutational Multivariate Analysis of Variance using the height zones and localities as

factors. The Permanova analysis used the average Sorensen similarity as the response

variable. We found significant differences in the species composition among the different

sites using specific contrasts: Amazonas (Fp=6.7, R2=0.27, Pr=0.001), Caquetá (Fp=7.3,

R2=0.28, Pr=0.001), Putumayo (Fp=5.5, R2=0.23, Pr=0.001,) and Vaupés (Fp=9.1,

R2=0.33, Pr=0.001). The highest similarity of the height zones among sites was found in

the base of the tree (Z1), followed by the upper canopy (Z6), and the lowest was found in

the middle canopy (Z5), followed by the inner canopy (Z4) (Table 4-1).

We found a weak effect of distance on the composition of the plots (Figure 4-10). The

results showed a low correlation between distances in species composition and

geographical distance using all the plots simultaneously (Mantel’s r=0.23, P<0.0001)

Chapter 4 88

Figure 4-10. Correlation between geographical distance among the trees and species

composition similarity using the bray-curtis similarity index among the 384 plots.

Indicator Species Analysis (ISA)

We identified 63 indicator species in our study. The tree base (Z1) had the highest

number of indicator species, followed by the outer canopy (Z6), the upper trunk (Z3), the

inner canopy (Z4), the middle canopy (Z5) and the lower trunk (Z2). In the case of

indicator families, 14 families were detected; the Z1 had the highest number of families,

followed by Z6, Z2, Z3 and Z4 (Table 4-1).

From 160 species registered, 28% appeared in only one height zone. The base of the

trunk zone (Z1) had 18 (44%) species that were indicators of Z1 zone. The species with

the highest indicator value for the trunk base height zone were: Calypogeia tenax,

Cololejeunea diaphana, Monodactylopsis monodactyla, Plagiochila sp1, Prionolejeunea

mucronata, Symphyogyna brasiliensis, Syrropodon xanthophyllus and Xylolejeunae

crenata. The indicator species with a significant association to the outer canopy zone (Z6)

Chapter 4 89

were: Cololejeunea cardiocarpa, Colura greig-smithii, Colura tenuicornis, Diplasiolejeunea

brunnea, Diplasiolejeunea buckii, Drepanolejeuneae sp1. and Verdoornianthus griffinii

(Appendix 2). The remaining 115 species were found in more than one height zone and

had a low and non-significant indicator value. The fidelity index calculated from the

indicator species analysis allowed us to separate the species in two groups: understory

specialists (18 species and 3 families), and canopy specialists (12 species and 3 families)

(Appendix 2).

4.4 Discussion Most of the 160 epiphytic bryophyte species recorded in the Colombian Amazon have

been reported previously from other Amazonian studies in countries such as Brazil,

Colombia, French Guiana, Guyana, and Ecuador (Benavides et al., 2006, 2004; Churchill,

1994; Mota de Oliveira et al., 2009; Mota de Oliveira & ter Steege, 2013; Zartman & Ilkiu-

Borges, 2007).

The most recent study on the Amazon region (Mota de Oliveira & ter Steege, 2013) is

consistent with our results concerning the most abundant families and the most common

species. In addition, our results are supported by the description of the characteristic

flora in the Amazon region with a high dominance of liverworts (Gradstein et al., 2001).

The higher richness of liverworts compared with mosses in our study has been observed

across tropical lowland forests in South America and Asia (Cornelissen & ter Steege,

1989; Florschütz-de Waard & Bekker, 1987; Gradstein et al., 2001; Mota de Oliveira & ter

Steege, 2013; Sporn et al., 2010). It is mainly due to the high percentage of a single

genera of Lejeuneaceae that drives the species richness. Several studies have shown

that in tropical lowland forests, Lejeuneaceae can make up 70% of all liverwort species

present (Cornelissen & ter Steege, 1989; Gradstein, 2006; Zartman, 2003).

Lejeuneaceae is not only a rich and very abundant family in the tropical lowland forest

where they are an important component of the cryptogamic flora, but also contributes to

the temperate liverwort flora (Gradstein, 2006). For that reason, the species from this

Chapter 4 90

family are good candidates for inferring the origin of tropical diversity and their

contribution to the non-tropical diversity (Wilson et al., 2007). Most of the species from

this family are epiphytic and occur on trunks and branches, twigs, or living leaves in the

rain forest (Gradstein et al., 2001). In our study, we found an increase in the number of

Lejeuneaceae species with the height zone in contrast to the other families. This can be

related to the fact that this family is highly specialized among the leafy liverworts, and with

the good capacity to have long-distance dispersal (Heinrichs et al., 2014; Mizutani, 1961;

Schuster, 1983).

The height zone with the highest species richness was the upper trunk (Z3), a zone

where branches and trunk converge. It is possible that the high number of species

observed is due to the combination of canopy and trunk communities are overlapping at

the top of the trunk. In the lower part of the tree, the establishment of epiphytic bryophytes

may be limited by the reduced light intensity (Sporn et al., 2010). Our results differ from

the findings by Mota de Oliveira (2009), where the richness peak was in the inner canopy

(Z4). The difference could be related to the type of canopy (more or less closed),

specifically with the leaf area index (LAI) (Xiao et al., 2014; Caldararu et al., 2012; Mu et

al., 2007), because this factor changes the environmental conditions inside the forest,

especially the availability of light and moisture (Sillett & Antoine, 2004). In general, the

abundance of epiphytic bryophytes was higher in the inner canopy, the upper trunk as

well as the tree bases. This is similar to the observations in other neotropical rain forests

(e.g. Cornelissen & ter Steege 1989).

Several studies have established that there is a clear differentiation in the vertical

stratification of bryophytic and phanerogamic epiphytic species. Vertical stratification is

related to environmental conditions such as atmospheric humidity, temperature, light

intensity, and wind velocity (Cardelús, 2007; Cornelissen & ter Steege, 1989; Gentry &

Dodson, 1987; Hietz et al., 1964; Barkman, 1958; Proctor, 1981).

The vertical stratification observed in the epiphytic bryophytes is probably driven by the

specificity of several species to particular forest strata. For example, Cheilolejeunea

urubuensis, Cololejeunea cardiocarpa, Colura greig–smithii, Colura tenuicornis,

Diplasiolejeunea brunnea, Diplasiolejeunea buckii, Verdoornianthus griffinii, and V.

Chapter 4 91

marsupifolious are creeping epiphytic bryophytes mostly found in the upper canopy (sun

epiphytes). The creeping growth (xerotolerant life–form) in the canopy is associated with

the strategy to retain water and humidity for extended periods after precipitation events

(Zots et al., 2000). Particularly the genera Colura and Diplasolejeunea have

morphological unique characteristics to tolerate the exposure of the canopy. Colura

species have extremely modified leaves that form an apical sac. This genus grows

exclusively in the canopy, avoiding the shaded forest understory, while Diplasiolejeunea

species have extremely imbricate underleaves that provides an additional layer of

protection to the lobules (1 to each lateral leaf). This genus can grow also in forest

understory but in a smaller proportion, (Gradstein et al., 2001; Gradstein & Costa, 2003).

Sun epiphytes and generalists are adapted to relatively dry habitats and predictably have

better survival chances. They may descend from the high canopy of the primary forest

and establish themselves nearer to the ground in gaps (Gradstein & Ilkiu-Borges, 2009).

The upper section of the trunk in the rain forest is occupied by shade-tolerant and

drought-tolerant species, mainly appressed mats of liverworts from the Lejeuneaceae

family (Gradstein & Pócs, 1989). In our study these species, including Ceratolejeunea

desciscens, Cheilolejeunea holostipa, Drepanolejeunea anoplantha, Lejeunea

laetevirens, and Prionolejeunea scaberula, were indicators for this part of the tree. The

species diversity of the lower trunk although was lower than the upper and middle

sections of the tree had a highest number of unique bryophyte families such as

Plagiochilaceae, Lejeuneaceae, Fissidentaceae, Leucobryaceae, Calymperaceae and

Leucophanaceae. The presence of those families that normally found in the understory or

even exposed soil of the rainforest was allowed by the steadily high degree of humidity

(Richards, 1954).

The sun and understory epiphytes differ in their reproduction strategy and dispersal

range. Our findings agree with the fact that shade epiphyte dispersibility is constrained

and that short distance dispersal is caused mainly by vegetative reproduction (Löbel et

al., 2009; Cleavitt, 2002). For example, we found that understory specialists such as

Anomoclada portoricensis, Calypogeia laxa, C. tenax, Cyclolejeuneae luteola, Mnioloma

paralellogramum, Prionolejeunea scaberula, Riccardia amazonica, and Xylolejeunea

crenata were frequently producing vegetative gemmae and caducous leaves.

Chapter 4 92

In the case of sun epiphytes spore dispersal was common, and the species were

predominantly monoicous (Gradstein & Ilkiu-Borges, 2009). The predominance of

monoicouos species was supported by our observations, where most of the canopy

specialists were monoicous such as Cheilolejeunea urubuensis, Cololejeunea

cardiocarpa, Colura tenuicornis, Leptolejeunea elliptica, Verdoornianthus griffinii, V.

marsupifolious.

In general, we found more similarity in the species assemblages of one height zone

between different localities than in the different height zones in one locality. The strong

influence of height zones on species assemblages reveals the importance of the

environmental differences across the vertical gradient within a single tree. In this way the

vertical distribution reflects the underlying moisture gradient, where the communities are

strongly stratified through the height zones in the forest (McCune, 1993). Temperature

gradients within forests have also shown influence on the abundance of epiphytic

bryophytes (Sillett & Antoine, 2004). Changes in microclimatic conditions to epiphytic

bryophytes include decreasing humidity and increasing exposure to desiccating wind with

increasing height in the canopy (Campbell & Coxson, 2001).

Epiphytes are recognized to have high dispersal ability. As a consequence, they can

colonize rapidly available sites that fall within their dispersal range (Nieder et al., 1999).

Under this premise, we assume the idea that the high similarity in the community

composition in the different zones is explained by the easiness of dispersion across

localities. Epiphytic bryophytes from the base of the tree showed a higher similarity in

their composition among localities. This is because of the presence of species from

genera with widespread distribution such as Leucobryum, Leucophanes, Plagiochilla,

Sematophyllum, Symphyogyna (Pócs, 1982). A possible explanation for this high

similarity is that the continuous distribution of the bryophytes from the tree base to the

adjacent soil facilitates dispersal.

We found a clear separation between species from the tree base and species from the

upper canopy, probably explained by the fact that those forest strata correspond to the

extremes of a micro-environmental continuous gradient. In the upper canopy the

Chapter 4 93

epiphytes are exposed to high temperatures and low levels of humidity due to the solar

radiation intensity and high wind velocity. In contrast, in the lower part of the tree, the air

humidity is higher, and the light penetration is lower (Kessler, 2000). The clear separation

between Zones 1 and 6 in our observations matches the results in a recent study in the

Amazon basin (Mota de Oliveira et al., 2009).

According to Hubbell’s neutral theory, the similarity in the species composition between

sites should decrease with increasing geographical distance. The decrease of community

similarity with geographical distance can be accounted for by 1- a more different

environment with distance, 2- dispersal limitations due to the spatial configuration of the

environment, and 3- inherent dispersal limitations that prevents free mixing of the

metacommunity (Soininen et al., 2007; Hubbell, 2001). Based on our results, the variation

in plant composition did not show a strong relationship between the geographical gradient

and ecological distance matrices. In short, similarity decay between communities across

the Colombian Amazon was not directly related to geographic distance most probably due

to the environmental similarities among all the sites. In contrast, similarity between

communities was primarily explained by the niche theory, where the different species

have adapted to different and specific environmental conditions.

In conclusion, contrary to the communities of the seed plants, where the structure of the

community is addressed mainly by dispersal limitation (Gehrig-Downie, 2013), the niche

assembly gave us the confidence to explain the stratification of the epiphytic bryophytes

at local and regional scales. The presence of a high percentage of indicator species

across the Colombian Amazon is evidence to further support a high specificity of species

for a particular microhabitat around the forest.

In our study we found the species Monodactylopsis monodactyla, Colura greig-smithii,

Colura cylindrica and Thysananthus amazonicus, which were considered vulnerable (VU),

according to the IUCN categories due to presence of a unique record in Colombia

(Linares & Uribe, 2002). After our research we found new records of those species in

Amazonas, Caqueta, Putumayo and Vaupes departments. This increase in the number of

localities and records effectively changes the category from Vulnerable (VU) to Near

Threatened (NT).

Chapter 4 94

We found a high number of shade epiphytes across the Colombian Amazon. These

species can be more strongly affected by a disturbed forest than sun epiphytes or

generalists due to restricted ability to reestablish themselves in secondary forest with less

dense canopy (Gradstein & Ilkiu-Borges, 2009). A conservation strategy designed to

preserve the rainforest needs to take into account that the epiphytic bryophytes are highly

sensitive to variation in the environmental conditions.

Puerto Colombia, Putumayo

Chapter 5 96

5. Genetic population structure of Cheilolejeunea rigidula (Nees & Mont.) R.M.

Schust. in the Amazon region

5.1 Introduction The dispersal of organisms among habitats is the fundamental basis of modern ecological

theory, connecting population dynamics, biogeography, and community structure (Shurin

et al., 2009). Dispersal can have important repercussions on populations and

communities at local and regional scales, increasing or not increasing connectivity

(Debinski & Holt, 2000). The structure within populations at different spatial scales and

the levels of gene flow within a population can be estimated through the distribution of the

genetic variation (Vekemans & Hardy, 2004; Wright, 1943).

Plant populations are often highly spatially structured (Ennos, 2001), related to the fact

that plants are static, and that genetic dispersal is by means of pollen and seeds, or in the

case of bryophytes by spores, sperm and vegetative fragments. In this way the gene flow

may be limited, and genetic isolation by distance occurs within populations. The small

size of the spores, however, is a convenient condition for travel across long distances,

and the production of vegetative propagules suggests that bryophytes display high

dispersal ability (Laenen, 2009).

Molecular studies of data have been increasing in recent years; these have been used for

biogeographic inferences and to determine patterns in the distribution of the species in

bryophytes (De Queiroz, 2005). New evolutionary history information has led to a re-

evaluation of the theory of dispersal, changing the previous belief that dispersal can

generate patterns with regular distribution and the idea that continental drift is the

principal cause of shaping intercontinental distribution (De Queiroz, 2005). The duality

between the vicariance and dispersal theories is part of a debate in evolutionary biology

Chapter 5 97

(Frey et al., 2010; Heinrichs et al., 2013; Laenen, 2009; Lewis et al., 2014), and

bryophytes are not an exception in the debate.

In this study, we used the species Cheilolejeunea rigidula as a model to study the genetic

population structure of a species, broadly distributed in the lowland rain forest of tropical

America. It can grow as an epiphyte across the complete vertical gradient of the trees,

from the base of the trunk to the top of the canopy (Campos et al., 2015; Mota de Oliveira

& ter Steege, 2013). This species has been found in every floristic inventory that includes

epiphytic liverworts in the Amazon (Mota de Oliveira et al., 2011).

We hypothesized that the distribution of Cheilolejeunea rigidula across the Amazon

region has been shaped by the events of long-distance dispersal. In this work we used

molecular distance and population genetics to test this hypothesis. In particular, we

addressed the following question: Is there a genetic population structure, considering

populations by sites, height zones or sections of the tree? Is there a correlation between

genetic distance and geographic distance?

5.2 Materials and Methods

5.2.1 Target Species

In the present study, Cheilolejunea rigidula (Nees & Mont.) R. M. Schust., was selected

as a model to analyze the genetic population structure of a common bryophyte in the

Amazon region. The genus Cheilolejeunea Spruce (Steph.) is part of the largest family of

liverworts, with more than a thousand species in some 68 genera, Lejeuneaceae

(Gradstein, 2013; Wang al., 2014). This family abounds in humid tropical forests, and

occupy different epiphytic niches, ranging from large tree trunks to tiny twigs and surfaces

of living leaves (Gradstein, 1994). Cheilolejeunea contains an estimated 80-100 species

and is pantropical in distribution (Ye et al., 2015) and is part of the subtribe

Cheilolejeuneinae Gradst. This genus is characterized by distal hyaline papilla, which is

distal to the apical tooth (second tooth), creeping to ascending growth (Figure 5-1), thin

stems with a 2(‒4) cell-wide ventral merophyte and enlarged epidermis cells, leaf lobules

with 1(‒2) teeth and leaf cells with 1‒3(‒5) large, coarsely granular oil bodies, bifid

Chapter 5 98

underleaves and an inflated perianth with 3‒5 smooth keels, rarely pluriplicate or without

keels (Ye & Zhu, 2010).

Cheilolejunea rigidula is the most common species of Cheilolejeunea in tropical America

(Gradstein et al., 2001) and it is also the most common bryophyte in the Amazon (Mota

de Oliveira, 2010) primarily growing on the bark of trees in the canopy and the understory

of lowland rain forest (Campos et al., 2015; Mota de Oliveira & ter Steege, 2013).

C. rigidula is a dioicous plant. The species can be recognized by leaves with a flat and

rounded leaf apex, and by the rather small, distant, obovate underleaves (2‒3.5 times

stem width) with cuneate to slightly rounded bases (Figure 5-1). Trigones are

conspicuous and well delimited. The cells have 1‒2 very large oil bodies, very coarsely

segmented and almost filling the lumen (Gradstein & Costa, 2003). The plants rarely

produce sporophytes. Out of 80 plants examined for the present study, only six had

perianths in different stages of decay.

Figure 5-1. Cheilolejeunea rigidula (Nees & Mont.) R. M. Schust., showing characteristic

underleaves with cuneate bases.

Chapter 5 99

5.2.2 Sampling A total of 80 shoot samples of Cheilolejeunea rigidula from four upland forests in the

Colombian Amazon were analyzed. They were collected according to standard

procedures, using plots of 40cm2 on phorophytes at different height zones and sections

(Figure 5-2).

Figure 5-2. Schematic full-grown tree showing the two sections (canopy and trunk) and

six height zones, Z1: tree base; Z2: lower trunk; Z3: upper trunk; Z4: inner canopy; Z5:

middle canopy; Z6: outer canopy.

Figure 5-3. Study sites in the Amazon basin where the shoot samples were collected: 1. Pto. Colombia (Putumayo); 2. La Gamitana (Caquetá); 3. Macaquiño (Vaupés); 4. El

Zafire (Amazonas), all Colombia; 5. Mabura Hill (Guiana); 6. Manaus (Brazil) and 7. Tapajos (Brazil).

Chapter 5 100

Six samples of C. rigidula from central and eastern of the Amazon and the Guiana Shield

were included (Mota de Oliveira et al., 2011): one from Mabura Hill (Guiana), four from

Manaus (Brazil), and one from Tapajos (Brazil), (Figure 5-3).

5.2.3 Molecular methods

All samples were air-dried and DNA was extracted using the Macherey-Nagel NucleoMag

96 Plat kit on the Thermo Scientific KingFisher Flex extraction robot. Final elution was

carried out in 150µl. Two chloroplast markers (partial atpB gene and partial psbA

gene/psbA-trnH spacer (hereafter named psbA) well as the nuclear ribosomal internal

transcribed spacers (ITS) 1 and 2 were amplified (Stech & Quandt, 2014), using primers

from Table 5-1 PCR amplification of atpB, ITS1 and ITS2 was carried out in a reaction volume of 25µl,

containing 2.5µl 10x Qiagen PCR buffer CL, 2.5µl 25mM MgCl2, 0.25µl 100mM BSA,

1.0µl of each 10µM primer, 1.5µl 2.5mM dNTP, 1.25 units of Qiagen Taq and 1.0µl

template DNA. PCR was performed through three minutes of initial denaturation at 94°C,

followed by 40 cycles of 30 seconds denaturation at 94°C, 40 seconds annealing at 50°C

and one minute extension at 72°C. Final extension was done for five minutes at 72°C. For

amplification of psbA, a reaction volume of 25µl was used, containing 2.5µl 10x Qiagen

PCR buffer CL, 2.0µl 25mM MgCl2, 1.0µl of each 10µM primer, 1.0µl 2.5mM dNTP, 1.25

units of Qiagen Taq and 1.0µl template DNA. PCR was performed by three minutes of

initial denaturation at 95°C followed by 35 cycles of 20 seconds denaturation at 95°C, 20

seconds annealing at 53°C and 1.30 minute extension at 72°C. Final extension was done

for 10 minutes at 72°C. Final bidirectional sequencing was performed as BaseClear B.V.

in Leiden, the Netherlands, using the amplification primers. Sequence editing and

alignment, raw data was edited manually using Sequencher 4.10.1 (Gene Codes

Corporation, Ann Arbor, MI, USA) and aligned using BioEdit 7.0.5.3 (Hall, 1999). Every

variable site was checked, and ambiguous symbols conforming to IUPAC code were

inserted when the signal was unclear.

Chapter 5 101

Table 5-1. Primers used in this study.

Primer Marker Sequence M13F-672F atpB 5'-TTGATACGGGAGCYCCTCTWAGTGT-3' M13R-910R atpB 5'-TTCCTGYARAGANCCCATTTCTGT-3' M13F-501F psbA 5'-TTTCTCAGACGGTATGCC-3' M13R-trnHR psbA 5'-GAACGACGGGAATTGAAC-3' M13F-Bryo-18SF ITS1 5'-GGTGAAGTTTTCGGATCGCG-3' M13R-Bryo-5.8SR ITS1 5'-TGCGTTCTTCATCGTTGC-3' M13F-Bryo-5.8SF ITS2 5'- GACTCTCAGCAACGGATA-3' M13R-Bryo-26SR ITS2 5'-AGATTTTCAAGCTGGGCT-3'

5.2.4 Population genetic analysis

The total number of specimens of Cheilolejeunea rigidula, collected and used for DNA

extraction, including successful and unsuccessful samples sequenced was 80. The

chloroplast markers atpB and psbA were successfully sequenced in 65 and 50 samples

respectively, and with the nuclear marker ITS we had 55 samples sequenced (Table 5-2).

Table 5-2. Samples of Cheilolejeunea rigidula, with locations, zone of the tree where they

were collected, and markers successfully sequenced. Amazonas (AM), Caquetá (CA),

Putumayo (PU), Vaupés (VA), Manaus (MAN), Mabura Hill (MAB), and Tapajos (TAP).

Trunk zone (1, 2, 3) and canopy zone (4, 5, 6).

Site Samples Zone Elevation Latitude Longitude atpB psbA ITS AM AM0AZ3 3 129 -3,9856 -69,8906 + + + AM AM0AZ4 4 129 -3,9856 -69,8906 + + + AM AM0DZ2 2 118 -3,9859 -69,8906 + + + AM AM0DZ3 3 118 -3,9859 -69,8906 + + + AM AM0DZ4 4 118 -3,9859 -69,8906 + + + AM AMODZ5 5 118 -3,9859 -69,8906 + + + AM AM0EZ3 3 140 -3,9875 -69,8906 + + + AM AM0EZ4 4 140 -3,9875 -69,8906 + + + AM AM0GZ3 3 139 -3,9880 -69,8916 + + + AM AM0GZ4 4 139 -3,9880 -69,8916 + + - AM AM0GZ5 5 139 -3,9880 -69,8916 + - + AM AM0HZ3 3 117 -3,9883 -69,8910 + + + AM AM0HZ4 4 117 -3,9883 -69,8910 + + +

Chapter 5 102

Site Samples Zone Elevation Latitude Longitude atpB psbA ITS AM AM0HZ5 5 117 -3,9883 -69,8910 + + + AM AM0LZ3 3 132 -3,9971 -69,8921 + + + AM AMOLZ4 4 132 -3,9971 -69,8921 + + - AM AM0LZ5 5 132 -3,9971 -69,8921 + + + AM AM0OZ5 5 114 -3,9991 -69,8935 + + + AM AM0PZ3 3 115 -3,9992 -69,8931 + + + AM AM0PZ4 4 115 -3,9992 -69,8931 + - + AM AM0PZ5 5 115 -3,9992 -69,8931 + - + AM AM0PZ6 6 115 -3,9992 -69,8931 + - + CA CA0AZ5 5 125 -0,2478 -72,4206 + - + CA CA0BZ3 3 126 -0,2475 -72,4202 + + + CA CA0BZ5 5 126 -0,2475 -72,4202 + + + CA CA0CZ2 2 138 -0,2482 -72,4204 + + + CA CA0CZ4 4 138 -0,2482 -72,4204 + + + CA CA0CZ5 5 138 -0,2482 -72,4204 + - - CA CA0DZ5 5 136 -0,2480 -72,4198 + + + CA CA0EZ2 2 130 -0,2478 -72,4180 + + + CA CA0EZ3 3 130 -0,2475 -72,4162 + + + CA CA0EZ4 4 130 -0,2473 -72,4144 + + + CA CA0FZ2 2 130 -0,2473 -72,4180 + + + CA CA0FZ3 3 139 -0,2473 -72,4180 + + + CA CA0FZ4 4 139 -0,2473 -72,4180 + - + CA CA0FZ5 5 139 -0,2473 -72,4180 + + + CA CA0JZ3 3 118 -0,2417 -72,4086 + + + CA CA0LZ3 3 118 -0,2417 -72,4080 + + + CA CA0OZ5 5 143 -0,2398 -72,4064 + + + PU PU0BZ3 3 210 -0,6134 -74,3399 + - - PU PU0CZ4 4 212 -0,6129 -74,3400 + + + PU PU0FZ3 3 197 -0,6113 -74,3399 + + - PU PU0FZ5 5 197 -0,6113 -74,3399 + + + PU PU0FZ6 6 197 -0,6113 -74,3399 + + - PU PU0IZ4 4 186 -0,6056 -74,3483 + - + PU PU0JZ5 5 182 -0,6058 -74,3486 + - - PU PU0KZ4 4 181 -0,6057 -74,3491 + + + PU PU0LZ1 1 183 -0,6053 -74,3488 + + - PU PU0LZ4 4 183 -0,6053 -74,3488 + + - PU PU0MZ2 2 225 -0,6043 -74,3503 + - + PU PU0MZ3 3 225 -0,6043 -74,3503 + + + PU PU0OZ1 1 208 -0,6043 -74,3511 + + + PU PU0PZ1 1 205 -0,6039 -74,3506 + + + PU PU0PZ3 3 205 -0,6039 -74,3506 + + +

Chapter 5 103

Site Samples Zone Elevation Latitude Longitude atpB psbA ITS PU PU0PZ5 5 205 -0,6039 -74,3506 + + + VA VA0CZ4 4 202 1,2730 -70,1082 + + + VA VA0CZ5 5 202 1,2730 -70,1082 + + + VA VA0DZ5 4 192 1,2734 -70,1077 + + + VA VA0HZ3 3 187 1,2745 -70,1056 + - - MAN 1_Manaus 3 101 -2,9280 -59,9690 + + + MAN 2_Manaus 4 101 -2,9280 -59,9690 + + + MAN 3_Manaus 3 101 -2,9280 -59,9690 + + + MAN 4_Manaus 4 101 -2,9280 -59,9690 + - + MAB Mabura 3 76 5,2940 -58,6940 + - + TAP Tapajos 6 100 -2,5090 -54,9630 + - +

Distance genetic analysis

Cheilolejeunea rigidula is a species that can be easily confused with C. aneogyna, which

shares its small size, brown coloration, creeping habitat, rounded leaf apex and

underleaves with arched insertion line. Both are very common in lowland rain forests and

areas of tropical South America (Campos et al., 2015; Mota de Oliveira & ter Steege,

2013; Schäfer-Verwimp et al., 2013). However, Cheilolejeunea aneogyna has a lobule

apex with two teeth positioned very closed together, whereas C. rigidula has a lobule

apex with only one tooth (Gradstein & Costa, 2003), (Figure 5-4).

Figure 5-4. A - Lobule of Cheilolejeunea aneogyna (Spruce) A. Evans, showing paired

lobule teeth. B - Lobule of Cheilolejeunea rgidula (Nees & Mont.) R. M. Schust., showing

lobule apex with one tooth.

Chapter 5 104

Because of the similarities between these species, from the GenBank database we used

13 sequences of species related to C. rigidula (Table 5-3) in order to clarify the

relationship between samples and define the monophyly of C. rigidula. In this case,

distance analyses were performed on sequences based on ITS marker with Neighbor

Joining (NJ) techniques in PAUP* version 4.0a179 (Swofford, 2003). The NJ tree

produced was edited with the program FigTree, version 1.4.0 (Rambaut & Drummond,

2014), (Figure 5-5).

Table 5-3. Species used to realize the distance analyses based on the Neighbor Joining

(NJ) algorithm (Sequences from GenBank) and geographinc origin of the sample.

Haplotype composition and distribution The individuals displaying a specific and identical DNA sequence in the analysis were

assigned to one haplotype of Cheilolejeunea rigidula. For each marker, ITS, atpB and

psbA, we performe certain analyses for haplotypes shared among geographical areas. In

order to examine relationships among samples across the Amazon, statistical parsimony

networks were constructed using TCS 1.21 (Clement et al., 2000), (Figure 5-6, Figure 5-7, Figure 5-8).

Species Geographic origin

1 Cheilolejeunea aneogyna (Nees & Mont.) R. M. Schust. Suriname 2 Cheilolejeunea rigidula-1 (Nees & Mont.) R. M. Schust. Guyana 3 Cheilolejeunea rigidula-2 (Nees & Mont.) R. M. Schust. Belize 4 Cheilolejeunea trifaria (Reinw. et al.) Mizut. Colombia 5 Cheilolejeunea clausa (Nees & Mont.) Steph. Colombia 6 7

Cheilolejeunea revoluta (Herzog) Gradst. & Grolle Cheilolejeunea neblinensis Ilk.-Borg. & Gradst.

Costa Rica Colombia

8 Cheilolejeunea meyeniana (Gottsche, Lindenb. & Nees) R.M. Schust. & Kachroo

Indonesia

9 Cheilolejeunea holostipa (Spruce) Grolle & R.L. Zhu Colombia 10 Cheilolejeunea lineata (Lehm. & Lindenb.) Steph. Guadalupe 11 Cheilolejeunea acutangula (Nees) Grolle Mexico 12 Trocholejeunea sandvicensis (Gottshe) Mizut. - Out group* China 13 Lejeunea flava (Sw.) Nees - Out group* Brazil

Chapter 5 105

Genetic diversity analysis

In order to assess the partitioning of genetic variation among and within populations of

Cheilolejeunea rigidula, from the Amazon region (Table 5-2), Analysis of Molecular

Variance AMOVA (Excoffier, 1995) was used. For this analysis we used a molecular

distance matrix to realize pairwise comparisons. The results are expressed as the

percentage of variance explained by intra and inter population differentiation and give an

appreciation of the general genetic pattern describing the data (Laenen, 2009), (Table 5-4, Table 5-5, Table 5-6). The haplotype (h) and nucleotide (π) diversity was calculated

based on haplotype frequencies. Haplotypic diversity (h) describes the relative diversity of

haplotypes considering their frequencies, while nucleotidic diversity (π) shows the

divergence existing among haplotypes (Laenen, 2009), (Table 5-7, Table 5-8, Table 5-9).

These analyses were performed using Arlequin 3.5 (Excoffier & Lischer, 2010).

In order to test the genetic similarity among samples, we carried out all the analyses for

each marker (ITS, atpB and pbsA) in different cases by localities (Amazonas, Caquetá,

Putumayo, Vaupés, Manaus, Mabura Hil and Tapajos), by sections of the tree (canopy

and trunk) and by height zones in the tree (1 to 6).

Population differentiation In order to investigate the genetic population structure, evaluating the overall level of

genetic divergence among subpopulations, the fixation index Fst was calculated (Table 5-4, Table 5-5, Table 5-6). This index has a theoretical minimum (Fst = 0) indicating no

genetic divergence, and theoretical maximum (Fst = 1) indicating fixation for alternative

alleles in different subpopulations (Hamilton, 2011). First, a Fst (Weir & Cockerham,

1984) was calculated by localities for each marker, followed by an Fst by sections of the

tree, and finally, by height zones in the tree.

Using the distance method of Tamura Nei, we calculated the genetic distance between

groups of samples over all combined loci for pairwise genetic differentiation in Arlequin

3.5 (Excoffier & Lischer, 2010). In order to test the presence of correlation and

Chapter 5 106

significance between genetic distance and geographical distance, we used a Mantel test

(Figure 5-9)

5.3 Results Population genetic analysis The final dataset of Cheilolejeunea rigidula consisted of 65 samples successfully

sequenced (atpB 65, psbA 50 and ITS 55), distributed in the geographic areas as follows:

22 samples from Amazonas, 17 samples from Caquetá, 16 from Putumayo, four from

Vaupés, four from Manaus, one from Mabura Hill and one from Tapajos (Table 5-2). The

other 15 samples of the pool collected were not successfully sequenced, because the

sequenced obtained where not good enough.

Distance genetic analysis The identity of the samples from Colombia used in this study was clearly determined. The

phenogram (Figure 5-5) shows a large green clade with samples of Cheilolejeunea

rigidula that were used for the present study. It was morphologically corroborated. The

other samples located in the blue clade were excluded from the analyses because they

correspond to Cheilolejeunea aneogyna.

Chapter 5 107

Figure 5-5. NJ tree derived from a Neighbor joining analysis of Cheilolejeunea rigidula

and Cheilolejeunea aneogyna, including 11 taxa related to those species and two

outgroup species.

Chapter 5 108

Haplotype composition and distribution The chloroplast markers produced less haplotype diversity than the nuclear marker. Using

the chloroplast marker psbA (Figure 5-6), from 6 haplotypes, we found one haplotype

with widespread distribution in the Amazon region. This haplotype (Hap. 1) was present in

Amazon with 42% frequency, in Caquetá with 30%, in Putumayo with 21% and in Vaupés

with 7% from 43 specimens included. Haplotype 6 was restricted to Manaus with three

specimens included; haplotype 2 was restricted to Caquetá, and the haplotypes 3, 4, and

5 to Putumayo.

When the haplotype distribution was analyzed with the chloroplast marker atpB (Figure 5-7), from 11 haplotypes, we also found haplotype 1 as the most widespread in the

region. It was present in Amazon with 40% frequency, Caquetá with 30%, Putumayo with

20% and Vaupés with 10% from 54 specimens included. Haplotypes 7, 8 and 9 were

restricted to Manaus (the haplotype 7 with two specimens included), haplotype 11 was

restricted to Tapajos, haplotypes 2 - 6 to Putumayo, and haplotype 10 to Mabura Hill.

In the case of haplotype distribution based on the nuclear marker ITS (Figure 5-8), we

found a higher diversity of haplotypes with less frequency. From 41 haplotypes, we

obtained 30 haplotypes containing only one specimen (73%), 9 haplotypes with two

specimens (22%), 1 haplotype with three specimens (2.5%), and 1 haplotype with four

specimens (2.5%). Haplotypes 6, 9, and 26 were distributed in two geographic regions;

the other haplotypes were restricted to one site. Haplotype 6 corresponded to Putumayo

50% and Caquetá 50%, haplotype 9 corresponded to Putumayo 33.3% and Caquetá

66%, and haplotype 26 corresponded to Amazonas 50% and Caquetá 50%.

Chapter 5 109

Figure 5-6. Haplotype network of Cheilolejeunea rigidula using the chloroplast marker

(psbA). Dashes correspond to non-sampled or extinct haplotypes. Haplotypes are


proportional to the haplotype frequency.

Figure 5-7. Haplotype network of Cheilolejeunea rigidula using the chloroplast marker

(atpB). Dashes correspond to non-sampled or extinct haplotypes. Haplotypes are


proportional to the haplotype frequency.

Chapter 5 110

Figu

re 5

-8.

Hap

loty

pe n

etw

ork

of C

heilo

leje

unea

rig

idul

a us

ing

the

nucl

ear m

arke

r (IT

S).

Each

ste

p co

rresp

onds

to a

mut

atio

n an

d th

e do

ts c

orre

spon

d to

non

-sam

pled

or

extin

ct h

aplo

type

s. H

aplo

type

s ar

e re

pres

ente

d by

colo

red

area

s (g

eogr

aphi

c re

gion

s) a

nd b

y pi

e di

agra

ms

who

se s

ize

is p

ropo

rtion

al to

the

hapl

otyp

e fre

quen

cy.

Chapter 5 111

Genetic diversity analysis

According to the AMOVA analyses, in the case of the geographical regions the genetic

variation is present within sites (72.55%), more than among sites (27.45%). The same

patterns were determined within height zones (97.13%), more than among height zones

(2,87%) and in the case of the sections on the tree, within sections (101%) and among

sections (-1.16%), (Table 5-4, Table 5-5, Table 5-6).

Fixation indices estimated from the variance components, showed a fixation index of

Fst=0.028 in the height zones and Fst=0.01 in the sections on the tree. According to the

qualitative guidelines proposed by Wright (1978), these values may be considered as

indicating little genetic differentiation among populations. In the case of geographical

regions, the value of the fixed index was Fst=0.27 indicating very large genetic

differentiation.


observed at seven Localities: Amazonas, Caquetá, Putumayo, Vaupés, Manaus, Mabura

Hill and Tapajos. The p-value represents the result of a test consisting of 1023

permutations.

Source of variation

d.f. Sum of squares

Variance components

Percentage of variation

Among sites 6 50.367 0.8895 27.45 Within sites 48 12.833 2.35069 72.55 Total 54 163.200 3.24027

Fixation Index Fst: 0.27454 P-value = <0.05


observed at six groups (height zone in the tree, zone 1 to zone 6).

Source of variation d.f. Sum of squares

Variance components


Among height zones 5 18.418 0.08746 Va 2.87 Within height zones 49 144.782 2.95473 Vb 97.13 Total 54 163.200 3.04219

Fixation Index Fst: 0.02875 P-value = <0.05

Chapter 5 112

Table 5-6. Molecular variance analysis AMOVA and Fixation index Fst, in Cheilolejeunea

rigidula from the variation observed at two groups (sections in the tree, canopy and trunk).

The p-value represents the result of a test consisting of 1023 permutations.

Source of variation

d.f. Sum of squares

Variance components


Among sections 1 2.094 -0.03496 Va -1.16 Within sections 53 161.106 3.03974 Vb 101.16 Total 54 163.200 3.00478

Fixation Index Fst: -0.01164 P-value = <0.05

Haplotype (h) and nucleotide (π) diversity indices within geographical regions in the

Amazon (Table 5-7) showed that the most of the genetic diversity is found in the

Amazonas, Caquetá, Putumayo and Manaus. Mabura Hill and Tapajos had a nucleotype

and haplotype diversity of 0.0 due to the presence of only one haplotype in those regions.

Table 5-7. Haplotypic (h) and nucleotidic (π), diversity of the geographical regions with

their corresponding standard deviation (SD).

Site Nb of haplotypes

Haplotype Diversity

SD Nucleotide Diversity

SD

Amazonas 13 0.9421 0.0340 0.0149 0.0078

Caquetá 12 0.9750 0.0295 0.0107 0.0061

Putumayo 9 0.9778 0.0540 0.0080 0.0050

Vaupés 2 0.6667 0.3143 0.0122 0.0100

Manaus 3 0.8333 0.2224 0.0068 0.0053

Mabura Hill 1 0 0 0 0

Tapajos 1 0 0 0 0

The indices within height zones of the tree (Table 5-8) indicate that the highest genetic

diversity is located in zones 3 and 4, followed by zones 5 and 2, and the lowest indexes

were registered in zones 1 and 6, where the presence of the haplotypes was one per

zone. Finally, the indexes within sections of the tree (Table 5-9) were higher in the

canopy than in the trunk. This was expected due to the high genetic diversity in the zones

4 and 5; these zones correspond to the canopy section.

Chapter 5 113

Table 5-8. Haplotypic (h) and nucleotidic (π), diversity of the height zones in the tree, with


Height Zones in the tree

Nb of haplotypes

Haplotype Diversity


SD

One 1 0 0 0 0

Two 6 0.9286 0.0844 0.0152 0.0091

Three 12 0.9780 0.0345 0.0113 0.0065

Four 11 0.9848 0.0403 0.0140 0.0810

Five 14 0.9673 0.0298 0.0148 0.0821

Six 1 0 0 0 0

Table 5-9. Haplotypic (h) and nucleotidic (π), diversity of the sections in the tree, with


Sections Nb of haplotypes

Haplotype Diversity


SD

Canopy 26 0.9871 0.0122 0.0147 0.0079

Trunk 18 0.9746 0.0199 0.0125 0.0069

Population differentiation The results from the analyses in the Mantel Test of the relationship between genetic

distance (Tamura Nei) based on ITS marker and geographical distance showed a weak

yet significant correlation: When the geographic distance increase the genetic distance

increase (P<0.001), (r=0.516, Permutations = 999), (Figure 5-9).

Chapter 5 114

Figure 5-9. Mantel test showing the relationship between genetic distance (Tamura Nei)

and geographical distance (Degrees) of pairs of shoots from different localities

5.4 Discussion

The dendrogram developed using molecular and morphological data for the specimens of

Cheilolejeunea rigidula and C. aneogyna provided us with reliable identifications despite

the difficulty of identifying the species using traditional morphological characters

(Heinrichs et al., 2009). Specimens previously erroneously identified as C. rigidula were

properly identified due to their position in the C. aneogyna branch. The evidence from the

phylogenetic analysis strongly suggests that all individual but one from Mabura Hill are in

fact C. aneogyna. The reliability of correct taxonomic identifications in the analysis of

bryophytes is a permanent concern in phylogenetic analyses. The specimens from

Mabura Hill in our dataset were assigned to either C. aneogyna or to C. rigidula only after

carefully checking that all the other specimens were accurately identified and belonged to

different clades in the phylogenetic analysis. The C. rigidula specimens sampled covered

an area of 1.6 M km2 and were located from 50 m to 2.319 km apart covering nearly 50%

of the area of the Amazon basin (SINCHI, 2010).

Chapter 5 115

The haplotype network for the chloroplast markers (atpB, psbA) showed little variation

between the analyzed samples. However, in atpB there is some structure, the haplotypes

from Manaus and Tapajos are close together and separated from the Colombian and

Guiana ones. The nuclear marker (ITS) showed a clear spatial structure, we could

differentiate haplotypes of the most eastern populations from the most western

populations.

Liverworts are considered to be widely distributed with few limitations to their dispersal

(Laaka-Lindberg et al., 2003). The small size and viability of the spores allows them to

travel large distances once the spores reach the winds above the canopy (Miller &

McDaniel, 2004; Sundberg et al., 2006). The epiphytic bryophytes are not limited by

substrate availability and spore germination, bryophytes requires only of bark with some

moisture to germinate (Hallingbäck, 2002). The spatial structure of haplotypes in

bryophytes has been found to be stronger in dioecious species where sexual reproduction

is somehow limited (Laenen, 2009). The evidence of long-distance dispersal can be

observed in the presence of unique haplotypes in regions that are more related to

common haplotypes in locations thousands of kilometers away than to individuals located

a few hundred meters away.

The genetic diversity of C. rigidula using the ITS marker was highly variable within the

populations despite the strong spatial structure. The high variability in each site was due

to a large number of unique haplotypes. From the 41 haplotypes identified, only 11 had

more than one sequence. The high proportion of unique haplotypes might indicate some

degree of subpopulation structure within the geographic regions (Laenen, 2009). Even

species with cosmopolitan distribution such as the moss Physcomitrella patens show a

high within-site variability; however the high within-site variability of P. patens has been

related to the small size of the populations in ephemeral habitats (Hooper, 2008).

Cheilolejunea rigidula is the most common liverwort in western and central Amazonia

(Campos et al., 2015; Mota de Oliveira & ter Steege, 2013), indicating that the high

variability observed within the populations is most probably due to incipient geographical

isolation of subpopulations in each locality. The lack of a genetic differentiation of C.

rigidula along the height of the trees is reflected in the absence of an ecological

specialization for a particular height zone. This species can grow as an epiphyte across

Chapter 5 116

the complete vertical gradient of the trees from the base of the trunk to the top of the

canopy (Campos et al., 2015; Mota de Oliveira & ter Steege, 2013).

Remarkably, the west-to-east gradient is supported by the relationship between genetic

distance and geographic distance. In average, the further apart the individuals are, the

more different their genetic structure is, indicating the limitations not in the dispersal but in

sexual reproduction of C. rigidula. Our study shows that bryophytes have a spatially

structured genetic variation although this variation occurs at larger spatial scales than

previously considered (over 2000 km). Our results also show that tropical liverworts

should not be considered as evolutionary dead ends but as part of a network of

evolutionary entities interacting with their environment (Heinrichs et al., 2013). Moreover,

the spatial structure of the subpopulations of C. rigidula in the Amazon is consistent with

the fact that current distribution of liverworts is not random, and that the distribution

patterns result from events such as occasional long distance dispersal, frequent dispersal

over short distances, local extinction, and local diversification (Heinrichs et al., 2013).

Macaquiño community, Vaupés

Chapter 6 118

6. Conclusions and recommendations

6.1 Conclusions

This thesis presented a comprehensive study of the epiphytic bryophytes in four localities

in the Colombian Amazon. We addressed several different research fields: taxonomy,

floristics, ecology, and population genetics. In this way, we contributed to the knowledge

and understanding of the structure, dynamics, and diversity of the community of this

group of plants in the lowland rain forests.

From the study new records of epiphytic bryophytes were reported from Colombia: one

moss species (Bryophyta) and eighteen liverworts (Marchantiophyta) including seventeen

members of Lejeuneaceae and one of Lepidoziaceae. We also reported new records for

the departments of Amazonas, Caquetá, Putumayo, and Vaupés: 82 species of liverworts

and 27 species of mosses. The sampling produced 2827 records contained in 160

species and distributed in 26 families and 64 genera. As we had expected, the epiphytic

bryophyte flora was dominated by liverworts, and the Lejeuneaceae family was clearly the

most dominant in the Colombian Amazon. The most common species in the Amazon

region were Archilejeunea fuscescens, Ceratolejeunea cornuta, Cheilolejeunea rigidula,

Sematophyllum subsimplex and Octoblepharum albidum. Overall, the species richness

was rather similar except for Putumayo where the number of species was slightly higher

due to the influence of the northern Andes.

Our study in the Amazon region showed a clear differentiation in the composition of the

epiphytic bryophytes communities across the vertical gradient in the forest. We were able

to establish that some species are specialists, showing preferences for a particular zone

of the trees. The specificity of several species to particular strata was evidenced in both

habitats, in the canopy and in the base of the trunks. We found species in the upper

canopy adapted to dry habitats, with a xerotolerant life form, associated with strategies

that favor the retention of water and humidity. However, at the base of the trees we found

species exhibiting more exposed growth forms because of the high humidity. The clear

differentiation between the communities of the upper canopy and tree base are explained

Chapter 6 119

most likely by the fact that these forest strata correspond to the extremes of a micro-

environmental continuous gradient.

We found more similarity among species assemblages of the same height zone among

the different localities across the Amazon region than in the different height zones in the

same locality. The importance of the environmental differences along the vertical gradient

in the host tree was evidenced by the strong influence of height zones on species

assemblages, providing evidence of the strong niche effect on the epiphytic bryophytes

communities in the phorophytes throughout the Amazon region. In short, the similarity

among communities was primarily explained by the niche theory, according to which

different species adapt to specific environmental conditions. The presence of a high

percentage of indicator species across the Colombian Amazon is further evidence to

support a high specificity of species for a particular microhabitat within the forest.

The molecular techniques used in the analyses of the populations of Cheilolejeunea

rigidula allowed us to understand the level of connectivity for this species across seven

localities in the Amazon region. We found a spatial structure, using the nuclear marker

ITS. This structure indicated an east-to-west and north-to-south gradient with a gradual

differentiation of subpopulations from the western limits of the Amazon with the Andes

towards the more eastern Manaus. Cheilolejunea rigidula is one of the most common

liverworts in western and central Amazonia, indicating that the high variability observed

within the populations is most probably due to incipient geographical isolation of

subpopulations in each locality. The lack of a genetic differentiation among the height

zones of the trees reflects the absence of an ecological specialization for a particular zone

in this species. The evidence of long-distance dispersion was observed in the presence of

unique haplotypes in regions that are more related to common haplotypes in locations

thousands of kilometers away than to individuals located a few hundred meters away.

However, the long-distance dispersal events are not strong enough to obscure the spatial

structure of the subpopulations.

Chapter 6 120

6.2 Recommendations

Our principal recommendation is related to the study of the genetic population structure of

Cheilolejeunea rigidula. We believe that including more individuals from different localities

across the Amazon could provide insights into the genetic networks produced and could

provide a better differentiation of populations and connectivity across the Amazon region.

In general, the floristic studies on epiphytic bryophytes in the Colombian Amazon have

been restricted to the epiphytes from the understory. We consider that any ecological

study of tropical epiphytes require the inclusion of the canopy microhabitat. The high

number of new records to Colombia in this study evidenced the lack of properly

conducted studies of tropical epiphytic bryophytes.

A. Appendix 1: Species - Chapter 3

Appendix. Species of bryophytes recorded in the four localities of the Colombian Amazon

showing the distribution, Amazonas: AM, Caquetá: CA, Putumayo: PU and Vaupés: VA

Species AM CA PU VA Archilejeunea crispistipula (Spruce) Steph. X X X X

Archilejeunea fuscescens (Hampe ex Lehm.) Fulford X X X X

Archilejeunea parviflora (Ness) Schiffn. X X X X

Bazzania aurescens Spruce X X X X

Bazzania diversicuspis Spruce X X X X

Bazzania hookeri (Lindenb.) Trevis. X X X X

Calypogeia laxa Gottsche & Lindenb. X X X X

Calypogeia tenax (Spruce) Steph. X X X X

Ceratolejeunea cornuta (Lindenb.) Schiffn. X X X X

Ceratolejeunea cubensis (Mont.) Schiffn. X X X X

Cheilolejeunea aneogyna (Spruce) A. Evans X X X X

Cheilolejeunea neblinenesis Ilk.-Borg. & Gradst. X X X X

Cheilolejeunea rigidula (Mont.) R.M. Schust. X X X X

Cheilolejeunea trifaria (Reinw. et al.) Mizut. X X X X

Cheilolejeunea urubuensis (Zartman & Ackerman) R.L.Zhu &

Y.M.Wei

X X X X

Cololejeunea cardiocarpa (Mont.) A. Evans X X X X

Cololejeunea microscopica (Taylor) Schiffn. X X X X

Colura greig - smithii Jovet-Ast X X X X

Colura sagittistipula (Spruce) Grolle X X X X

Cyclolejeunea luteola (Spruce) Grolle X X X X

122

Species AM CA PU VA Drepanolejeunea anoplantha (Spruce) Steph. X X X X

Fissidens steerei Grout X X X X

Harpalejeunea oxyphylla (Nees & Mont.) Steph. X X X X

Lejeunea boryana Mont. X X X X

Leptolejeunea elliptica (Lehm. & Lindenb.) Schiffn. X X X X

Leptoscyphus porphyrius (Nees) Grolle X X X X

Leucobryum martianum (Hornsch.) Müll. Hal. X X X X

Leucophanes molleri Müll. Hal. X X X X

Metalejeunea cucullata (Reinw. et al.) Grolle X X X X

Microlejeunea bullata (Tayl.) Steph. X X X X

Micropterygium leiophyllum Spruce X X X X

Micropterygium parvistipulum Spruce X X X X

Monodactylopsis monodactyla (Spruce) R.M. Schust. X X X X

Octoblepharum albidum Hedw. X X X X

Octoblepharum pulvinatum (Dozy & Molk.) Mitt. X X X X

Odontoschisma variabile (Lindenb. & Gottsche) Trev. X X X X

Pilosium chlorophyllum (Hornsch.) Broth. X X X X

Plagiochila montagnei Ness X X X X

Plagiochila subplana Lindenb. X X X X

Pycnolejeunea contigua (Ness) Grolle. X X X X

Pycnolejeunea macroloba (Ness & Mont.) Schiffn. X X X X

Rectolejeunea emarginuliflora (Gottsche) A. Evans X X X X

Sematophyllum subsimplex (Hedw.) Mitt. X X X X

Syrrhopodon cryptocarpus Dozy & Molk. X X X X

Syrrhopodon fimbriatus Mitt. X X X X

Syrrhopodon leprieurii Mont. X X X X

Syrrhopodon simmondsii Steere X X X X

Verdoornianthus griffinii Gradst. X X X X

Verdoornianthus marsupiifolius (Spruce) Gradst. X X X X

Xylolejeunea crenata (Nees & Mont.) X.L. He & Grolle X X X X

Amblystegium species 01 X

Callicostella pallida (Hornsch.) Ångstr. X

123

Species AM CA PU VA Cheilolejeunea adnata (Kunze) Grolle X

Harpalejeunea tridens (Besch. & Spruce) Steph. X

Pictolejeunea picta (Gottsche ex Steph.) Grolle X

Plagiochila species 01 X

Radula mammosa Spruce X

Calymperes rubiginosum (Mitt.) W.D. Reese X

Drepanolejeunea orthophylla (Nees & Mont.) Bischl. X

Frullania apiculata (Reinw. et al.) Nees X

Lejeunea species 03 X

Acroporium pungens (Hedw.) Broth. X

Calymperes lonchophyllum Schwägr. X

Cololejeunea gracilis (Jovet-Ast) Pócs & Bernecker X

Cryphaea species 01 X

Fissidens prionodes Mont. X

Frullanoides liebmanniana (Lindenb. & Gottsche) van Slag X

Holomitrium arboreum Mitt. X

Lejeunea adpressa Nees X

Lejeunea caespitosa Lindenb. X

Lejeunea reflexistipula (Lehm. & Lindenb.) Gottsche X

Lejeunea species 02 X

Leptolejeunea exocellata (Spruce) A. Evans X

Lophocolea bidentata (L.) Dumort X

Lopholejeunea nigricans (Lindenb.) Schiffn. X

Pelekium schistocalix (Müll. Hal.) Touw X

Pilotrichum bippinatum (Schwägr.) Brid. X

Prionolejeunea aemula (Gottsche) A. Evans X

Prionolejeunea mucronata (Sande Lac.) Steph. X

Prionolejeunea scaberula (Spruce) Steph. X

Radula javanica Gottsche X

Schlotheimia torquata (Hedw.) Brid. X

Syrrhopodon parasiticus Paris X

Syrrhopodon prolifer Schwägr. X

124

Species AM CA PU VA Vesicularia vesicularis (Schwägr.) Broth. X

Archilejeunea ludoviciana (Lehm.) Geissler & Gradst. X

Cololejeunea diaphana A. Evans X

Colura cylindrica Herzog X

Cyclolejeunea peruviana (Lehm. & Lindenb.) A. Evans X

Drepanolejeunea crucianella (Tayl.) A. Evans X

Microlejeunea aphanella (Spruce) Steph. X

Odontoschisma portoricensis (Hampe & Gottsche) Steph. X

Rectolejeunea berteroana (Gottsche ex Steph.) A. Evans X

Syrrhopodon africanus (Mitt.) Paris X

Telaranea nematodes (Gottsche ex Austin) M.A Howe X

Ceratolejeunea coarina (Gottsche) Steph. X X

Syrrhopodon rigidus Hook. & Grev. X X

Ceratolejeunea laetefusca (Austin) R.M. Schust. X X

Ceratolejeunea species 01 X X

Cheilolejeunea clausa (Nees & Mont.) R.M. Schust. X X

Groutiella obtusa (Mitt.) Florsch. X X

Microlejeunea epiphylla Bischl. X X

Mniomalia viridis (Mitt.) Müll. Hal. X X

Neckeropsis undulata (Hedw.) Reichardt X X

Rhacopilopsis trinitensis (Müll. Hal.) E. Britton & Dixon X X

Symbiezidium barbiflorum (Lindenb. & Gottsche) A. Evans X X

Syrrhopodon lanceolatus (Hampe) W.D. Reese X X

Acrolejeunea torulosa (Lehm. & Lindenb.) Schiffn. X X

Acroporium guianense (Mitt.) Broth. X X

Bazzania cuneistipula (Gottsche & Lindenb.) Trevis. X X

Ceratolejeunea ceratantha (Nees & Mont.) Steph. X X

Drepanolejeunea species 01 X X

Diplasiolejeunea brunnea Steph. X X

Diplasiolejeunea buckii Grolle X X

Drepanolejeunea palmifolia (Nees) Steph. X X

Frullania caulisequa (Nees) Nees X X

125

Species AM CA PU VA Frullania kunzei (Lehm. & Lindenb.) Lehm. & Lindenb. X X

Riccardia amazonica (Spruce) Gradst. X X

Telaranea pecten (Spruce) J.J Engel & G.L. Merr. X X

Diplasiolejeunea cavifolia Steph. X X

Harpalejeunea stricta (Lindenb. & Gottsche) Steph. X X

Lejeunea laetevirens Nees & Mont. X X

Schiffneriolejeunea amazonica Gradst. X X

Trichosteleum papillosum (Hornsch.) A. Jaeger X X

Calymperes erosum Müll. Hal. X X X

Calymperes othmeri Herzog X X X

Cheilolejeunea holostipa (Spruce) Grolle & R.-L. Zhu X X X

Cheilolejeunea oncophylla (Ångstr.) Grolle & M.E. Reiner X X X

Drepanolejeunea bidens (Steph.) A. Evans X X X

Hyophila involuta A. Jaeger X X X

Lejeunea flava (Sw.) Ness X X X

Lejeunea species 01 X X X

Plagiochila species 02 X X X

Prionolejeunea denticulata (Weber) Schiffn. X X X

Sematophyllum subpinnatum (Brid.) E. Britton X X X

Syrrhopodon hornschuchii Mart. X X X

Syrrhopodon incompletus Schwägr. X X X

Syrrhopodon ligulatus Mont. X X X

Lejeunea phyllobola Nees & Mont. X X X

Micropterygium trachyphyllum Reimers X X X

Mnioloma parallelogramum (Spruce) R.M. Schust. X X X

Octoblepharum stramineum Mitt. X X X

Drepanolejeunea araucariae Steph. X X X

Lopholejeunea eulopha (Tayl.) Schiffn. X X X

Lopholejeunea subfusca (Nees) Schiffn. X X X

Symbiezidium dentatum Herzog X X X

Syrrhopodon flexifolius Mitt. X X X

Telaranea diacantha (Mont.) J.J. Engel & Merrill X X X

126

Species AM CA PU VA Thysananthus amazonicus (Spruce) Schiffn. X X X

Anoplolejeunea conferta (Meissn.) A. Evans X X X

Ceratolejeunea confusa R.M. Schust. X X X

Ceratolejeunea desciscens (Sande Lac.) Steph. X X X

Ceratolejeunea guianensis (Ness & Mont.) Steph. X X X

Colura tenuicornis (A. Evans) Steph. X X X

Drepanolejeunea lichenicola (Spruce) Steph. X X X

Lepidolejeunea involuta (Gottsche) Grolle X X X

Micropterygium pterygophyllum (Nees) Trevis. X X X

Plagiochila disticha (Lehm. & Lindenb.) Lindenb. X X X

Symphyogyna brasiliensis (Nees) Nees & Mont. X X X

Syrrhopodon xanthophyllus Mitt. X X X

B. Appendix 2: Species indicator analysis - Chapter 4

Z1-Z6: Number of occurrences per zone; N: Total number of occurrences per species;

WA: Mid-point of zonation for the species as calculated by weighted average for the

species; IV: Indicator value for each species to its maximum class (P<0.05); IS: Zone for

which the species is indicative Bold names are the indicators species. (*) Specialist for the

understory, (**) specialist for the canopy.

ESPECIE Z1 Z2 Z3 Z4 Z5 Z6 N WA IV IS Cololejeunea cardiocarpa ** 17 17 6 0.25 6

Colura greig – smithii ** 6 6 6 0.09 6

Colura tenuicornis ** 3 3 6 0.04 6

Diplasiolejeunea brunnea ** 5 5 6 0.07 6

Diplasiolejeunea buckii ** 6 6 6 0.09 6

Drepanolejeunea sp. ** 4 4 6 0.06 6

Leptolejeunea elliptica ** 3 13 16 5.8 0.16 6

Metalejeunea cucullata 1 4 3 1 13 22 5 0.12 6

Microlejeunea bullata 2 15 35 52 5.6 0.36 6

Pycnolejeunea macroloba 1 10 21 28 29 30 119 4.4 0.11 6

Rectolejeunea emarginuliflora ** 6 11 17 5.6 0.11 6

Verdoornianthus griffinii ** 13 13 6 0.20 6

Verdoornianthus marsupiifolius ** 5 37 42 5.9 0.50 6

Cheilolejeunea urubuensis ** 2 24 26 5.9 0.34 6

Archilejeunea fuscescens 3 12 29 37 44 37 162 4.3 0.18 5

Ceratolejeunea confusa 1 2 7 1 11 4.6 0.07 5

Drepanolejeunea araucariae 2 3 6 1 12 4.5 0.04 5

Octoblepharum stramineum 1 13 14 4.9 0.18 5

128

ESPECIE Z1 Z2 Z3 Z4 Z5 Z6 N WA IV IS Ceratolejeunea coarina 1 5 2 1 9 4.3 0.04 4

Cheilolejeunea aneogyna 6 18 20 26 24 9 103 3.7 0.10 4

Cheilolejeunea neblinensis 1 2 11 19 11 44 3.8 0.12 4

Leptoscyphus porphyrius 3 8 15 12 38 3.9 0.09 4

Octoblepharum pulvinatum 1 7 13 24 8 53 3.6 0.17 4

Odontoschisma variabile 13 20 21 10 64 3.4 0.10 4

Syrrhopodon fimbriatus 1 5 8 11 4 1 30 3.5 0.06 4

Syrrhopodon flexifolius 4 6 2 12 3.8 0.04 4

Anomoclada portoricensis * 3 3 3 0.04 3

Bazzania aurescens 8 8 19 4 39 2.5 0.14 3

Ceratolejeunea desciscens 2 8 14 7 2 33 3 0.09 3

Cheilolejeunea holostipa 2 14 13 6 1 36 3.7 0.08 3

Drepanolejeunea anoplantha 2 9 17 16 13 57 3.5 0.07 3

Lejeunea laetevirens 3 3 3 0.04 3

Octoblepharum albidum 6 23 25 20 15 1 90 3.2 0.10 3

Prionolejeunea scaberula * 3 3 3 0.04 3

Syrrhopodon cryptocarpos 3 7 18 5 33 2.8 0.15 3

Archilejeunea crispistipula 15 16 11 5 47 2.1 0.08 2

Bazzania hookeri 6 17 5 12 10 50 3.1 0.09 2

Syrrhopodon hornschuchii 2 7 3 2 14 2.4 0.05 2

Trichosteleum papillosum 5 1 6 2.2 0.06 2

Calypogeia laxa * 12 3 15 1.2 0.15 1

Calypogeia tenax * 7 7 1 0.10 1

Cololejeunea microscopica 9 1 1 11 1,6 0.1 1

Cololejeunea diaphana * 3 3 1 0.04 1

Cyclolejeunea luteola * 30 8 38 1.2 0.37 1

Fissidens steerei 7 1 1 9 1.6 0.08 1

Lejeunea boryana 9 7 3 1 20 1.8 0.06 1

Leucobryum martianum 57 32 25 11 3 128 2 0.39 1

Leucophanes molleri 42 25 15 7 89 1.9 0.31 1

Micropterygium leiophyllum 17 3 1 21 1.2 0.21 1

Micropterygium trachyphyllum 11 3 1 15 1.3 0.12 1

Mnioloma parallelogramum * 15 7 22 1.3 0.16 1

Monodactylopsis monodactyla * 12 12 1 0.18 1

Pilosium chlorophyllum 20 4 1 25 1.2 0.25 1

129

ESPECIE Z1 Z2 Z3 Z4 Z5 Z6 N WA IV IS Plagiochila sp.1 * 6 6 1 0.09 1

Prionolejeunea mucronata * 3 3 1 0.04 1

Riccardia amazonica * 5 1 6 1.2 0.06 1

Sematophyllum subsimplex 42 15 22 29 11 1 120 2.6 0.23 1

Symphyogyna brasiliensis * 5 5 1 0.07 1

Syrrhopodon leprieurii * 12 10 22 1.5 0.10 1

Syrrhopodon simmondsii 18 9 5 1 2 35 1.9 0.13 1

Syrrhopodon xanthophyllus * 4 4 1 0.06 1

Telaranea diacantha * 10 10 1 0.15 1

Xylolejeunea crenata * 8 8 1 0.12 1

Acrolejeunea torulosa 1 3 4 5.5

Acroporium guianense 1 1 1 1 4 3.5

Acroporium pungens 1 1 2 2.5

Amblystegium sp. 1 1 1 5

Anoplolejeunea conferta 2 3 5 5 1 16 4

Telaranea pecten 2 2 1

Archilejeunea ludoviciana 1 1 2 1.5

Archilejeunea parviflora 6 6 1 1 2 3 19 2.8

Bazzania cuneistipula 7 4 4 4 19 2.9

Bazzania diversicuspis 7 8 9 11 35 3.7

Callicostella pallida 1 1 1

Calymperes erosum 1 4 2 7 4.1

Calymperes lonchophyllum 2 2 1 5 1.8

Calymperes othmeri 1 2 4 7 3.4

Calymperes rubiginosum 1 1 2 2.5

Ceratolejeunea ceratantha 3 4 4 11 2.1

Ceratolejeunea cornuta 6 16 19 22 21 19 103 3.9

Ceratolejeunea cubensis 4 8 5 3 9 1 30 3.3

Ceratolejeunea guianensis 1 4 2 7 4.4

Ceratolejeunea laetefusca 2 3 2 1 8 3.3

Ceratolejeunea sp. 1 1 2 4

Cheilolejeunea adnata 1 1 5

Cheilolejeunea clausa 1 2 1 4 4

Cheilolejeunea oncophylla 2 5 3 4 14 3.6

Cheilolejeunea rigidula 2 6 18 18 18 9 71 4

130

ESPECIE Z1 Z2 Z3 Z4 Z5 Z6 N WA IV IS Cheilolejeunea trifaria 1 1 4 3 9 3.3

Chiloscyphus coadunatus 2 2 1

Cololejeunea gracilis 1 1 6

Colura cylindrica 1 1 6

Colura sagittistipula 1 2 7 8 4 22 3.5

Cryphaea sp1. 1 1 2 4 3.8

Cyclolejeunea peruviana 1 1 6

Cyrto-hypnum schistocalix 1 1 1

Diplasiolejeunea cavifolia 1 1 2 3.5

Drepanolejeunea crucianella 1 1 5

Drepanolejeunea fragilis 1 2 4 2 2 11 4.2

Drepanolejeunea lichenicola 1 1 3 5 5.2

Drepanolejeunea orthophylla 1 1 2 5.5

Drepanolejeunea palmifolia 5 8 6 3 22 2.3

Fissidens prionodes 1 1 1

Frullania apiculata 1 1 1 3 4

Frullania caulisequa 1 1 3 5 5.2

Frullania kunzei 2 5 6 13 4.3

Frullanoides liebmanniana 1 1 2 5

Groutiella obtusa 1 1 2 4 3.8

Haplolejeunea cucullata 1 1 1

Harpalejeunea oxyphylla 1 5 1 2 2 11 3.9

Harpalejeunea stricta 1 3 2 6 4

Harpalejeunea tridens 1 1 2 2.5

Holomitrium arboreum 1 1 2 4.5

Lejeunea caespitosa 1 1 4

Lejeunea flava 1 1 5 2 3 4 16 4.1

Lejeunea phyllobola 1 3 1 5 3

Lejeunea reflexistipula 1 1 2 3.5

Lejeunea sp.1 2 1 3 5.3

Lejeunea sp.2 1 1 2 3.5

Lejeunea sp.3 1 1 6

Lepidolejeunea involuta 3 1 1 2 7 3

Leptolejeunea exocellata 1 1 4

Lopholejeunea eulopha 3 1 4 3.8

131

ESPECIE Z1 Z2 Z3 Z4 Z5 Z6 N WA IV IS Lopholejeunea nigricans 1 1 2 2.5

Lopholejeunea subfusca 3 2 1 6 4.7

Microlejeunea aphanella 1 1 2

Microlejeunea epiphylla 1 1 1 2 5 4.8

Micropterygium parvistipulum 3 4 4 2 13 2.4

Micropterygium pterygophyllum 4 2 1 7 1.7

Mniomalia viridis 2 2 4 3 11 3.7

Neckeropsis undulata 1 1 2 1.5

Pictolejeunea picta 1 1 1

Pilotrichum bippinatum 1 1 2

Plagiochila disticha 3 1 4 8 2.8

Plagiochila montagnei 2 7 7 1 2 1 20 2.9

Plagiochila subplana 8 9 5 7 3 32 2.6

Plagiochila sp.2 1 2 3 2.3

Prionolejeunea aemula 1 1 5

Prionolejeunea denticulata 3 3 4 10 3.1

Pycnolejeunea contigua 17 23 12 19 26 19 116 3.6

Radula javanica 1 1 4

Radula mammosa 1 1 3

Rectolejeunea berteroana 1 1 6

Rhacopilopsis trinitensis 2 2 4 1.5

Schlotheimia torquata 1 1 1 3 4

Sematophyllum subpinnatum 3 1 1 1 6 4

Shiffneriolejeunea amazonica 1 1 2 5

Symbiezidium barbiflorum 1 1 4 5 11 4.9

Symbiezidium transversale 1 3 2 6 3.2

Syrrhopodon graminicola 1 1 6

Syrrhopodon incompletus 1 2 1 4 2.5

Syrrhopodon incompletus var.

lanceolatus 3 1 4 1.3

Syrrhopodon ligulatus 3 5 5 6 19 3.7

Syrrhopodon parasiticus 1 1 1 3 2.7

Syrrhopodon prolifer 1 1 6

Syrrhopodon rigidus 1 1 2 2.5

Telaranea nematodes 1 1 1

132

ESPECIE Z1 Z2 Z3 Z4 Z5 Z6 N WA IV IS Thysananthus amazonicus 2 1 4 3 10 4.8

Vesicularia vesicularis 2 2 1

Appendix 2. Zonation of epiphytic bryophyte families in the Colombian Amazon. Z1-Z6:

Number of occurrences per zone; N: Total number of occurrences per species; WA: Mid-

point of zonation for the species as calculated by weighted average for the species; IV:

Indicator value for each species to its maximum class (P<0.05); IS: Zone for which the

species is indicative. Bold names are the indicators families. (*) Specialist for the

understory, (**) specialist for the canopy.

FAMILIA Z1 Z2 Z3 Z4 Z5 Z6 N WA IV IS Aneuraceae * 5 1 6 1.2 0.06 1

Calypogeiaceae * 34 10 44 1.2 0.35 1

Fissidentaceae 8 1 1 10 1.5 0.1 1

Lepidoziaceae 81 44 42 32 25 224 2.4 0.27 1

Leucobryaceae 64 62 63 56 39 1 285 2.8 0.2 1

Leucophanaceae 42 25 15 7 89 1.9 0.30 1

Plagiochilaceae 20 16 15 12 5 1 69 2.6 0.08 1

Sematophyllaceae 42 22 28 31 13 2 138 2.7 0.19 1

Stereophyllaceae 20 4 1 25 1.2 0.25 1

Calymperaceae 48 49 48 39 18 3 205 2.7 0.15 2

Cephaloziaceae 13 23 21 10 67 3.4 0.10 3

Hypnaceae * 4 2 6 1.3 0.04 4

Lejeuneaceae 153 189 274 285 298 362 1561 3.9 0.23 6

Amblystegiaceae 1 1 5

Callicostaceae 1 1 2 1.5

Cryphaeaceae 1 1 2 4 3.8

Dicranaceae 1 1 2 4.5

Frullaniaceae 4 6 8 3 21 4.5

Lophocoleaceae 2 3 8 15 12 40 3.8

Macromitriaceae 1 2 1 3 7 3.9

133

FAMILIA Z1 Z2 Z3 Z4 Z5 Z6 N WA IV IS Neckeraceae 1 1 2 1.5

Phyllodrepaniaceae 2 2 4 3 11 3.7

Radulaceae 1 1 2 3.5

Thuidiaceae 1 1 1

References Acebey, A., Gradstein, S. R., & Krömer, T. (2003). Species richness and habitat

diversification of bryophytes in submontane rain forest and fallows of Bolivia.

Journal of Tropical Ecology, 19(01), 9–18.

Allee, W. C. (1926). Measurement of environmental factors in the tropical rain-

forest of Panama. Ecology, 7(3), 273–302.

Barkman, J. J. (1958). Phytosociology and ecology of cryptogamic epiphytes.

Benavides, J. C., Duque M, A. J., Duivenvoorden, J. F., & Cleef, A. M. (2006).

Species richness and distribution of understorey bryophytes in different forest

types in Colombian Amazonia. Journal of Bryology, 28(3), 182–189.

Benavides, J. C., Idarraga, A., & Alvarez, E. (2004). Bryophyte diversity patterns

in flooded and tierra firme forests in the Araracuara Region, Colombian

Amazonia. Tropical Bryology, 117–126.

Benitez, A., Gradstein, R., Prieto, M., Aragón, G., León-Yánez, S., Moscoso, A., &

Burghardt, M. (2012). Additions to the bryophyte flora of Ecuador 2 Adiciones

a la Flora de Briofitas del Ecuador 2. Tropical Bryology, 3106–3499.

Benitez, A., & Gradstein, S. R. (2011). Adiciones a la Flora de Briófitas del

Ecuador. Cryptogamie, Bryologie, 32(1), 65–74.

Caldararu, S., Palmer, P. I., & Purves, D. W. (2012). Inferring Amazon leaf

demography from satellite observations of leaf area index. Biogeosciences,

9(4), 1389–1404.

Campbell, J., & Coxson, D. S. (2001). Canopy microclimate and arboreal lichen

loading in subalpine spruce-fir forest. Canadian Journal of Botany, 79(5),

537–555.

Campos, L. V, ter Steege, H., & Uribe, J. (2015). The epiphytic bryophyte flora of

References 136

the Colombian Amazon. Caldasia, 37(1), 47–59.

Campos, L. V., Gradstein, S. R., Uribe, J., & ter Steege, H. (2014). Additions to

the Catalogue of Hepaticae of Colombia II. Cryptogamie, Bryologie, 35(1),

77–92.

Cardelús, C. L. (2007). Vascular Epiphyte Communities in the Inner‐Crown of

Hyeronima alchorneoides and Lecythis ampla at La Selva Biological Station,

Costa Rica. Biotropica, 39(2), 171–176.

Chao, A., Chazdon, R. L., Colwell, R. K., & Shen, T. (2005). A new statistical

approach for assessing similarity of species composition with incidence and

abundance data. Ecology Letters, 8(2), 148–159.

Churchill, S. (1994). The mosses of Amazonian Ecuador. Aarhus University Press.

Churchill, S. (2009). Moss diversity and endemism of the tropical Andes. Annals of

the Missouri Botanical Garden, 96(3), 434–449.

Churchill, S. (2016). Bryophyta. In Bernal, R., Gradstein, S. R. & Celis, M. [eds.].

Catalogue of plants of Colombia. Universidad Nacional de Colombia.

Churchill, S. P., Sanjines A, N. N., & Aldana M, C. (2009). Catálogo de las

briófitas de Bolivia: diversidad, distribución y ecología. Missouri Botanical

Garden & Museo Noel Kempff Mercado. La Rosa Editorial, Santa Cruz de la

Sierra Bolivia.

Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to

estimate gene genealogies. Molecular Ecology, 9(10), 1657–1659.

Cleavitt, N. L. (2002). Stress tolerance of rare and common moss species in

relation to their occupied environments and asexual dispersal

potential. Journal of Ecology, 90(5), 785-795.

Cornelissen, J. H. C., & ter Steege, H. (1989). Distribution and ecology of

epiphytic bryophytes and lichens in dry evergreen forest of Guyana. Journal

of Tropical Ecology, 5(02), 131–150.

Cortés, C., Ibarra, J., Morelo, J., Briceño, J., De Motta, B., Luna, C., Garavito, F.,

& Pulido, C. (1979). Suelos. En: La Amazonia colombiana y sus recursos.

References 137

PRORADAM. Instituto Geográfico Agustín Codazzi., 101–207.

Dauphin, G. (2003). Ceratolejeunea. Flora Neotropica, 1–86.

Dauphin, G. (2005). Catalogue of Costa Rican Hepaticae and Anthocerotae.

Bryophyte Diversity and Evolution, 26(1), 141–218.

De Queiroz, A. (2005). The resurrection of oceanic dispersal in historical

biogeography. Trends in Ecology & Evolution, 20(2), 68–73.

Debinski, D. M., & Holt, R. D. (2000). A survey and overview of habitat

fragmentation experiments. Conservation Biology, 14(2), 342–355.

Dufrêne, M., & Legendre, P. (1997). Species assemblages and indicator species:

the need for a flexible asymmetrical approach. Ecological Monographs, 67(3),

345–366.

Engel, J. J., & Merrill, G. L. (2004). Austral Hepaticae. 35. A taxonomic and

phylogenetic study of Telaranea (Lepidoziaceae), with a monograph of the

genus in temperate Australasia and commentary on extra-Australasian taxa.

Fieldiana Botany, 1–261.

Ennos, R. A. (2001). Inferences about spatial processes in plant populations from

the analysis of molecular markers. Special Publication - British Ecological

Society, 14, 45–72.

Estébanez, B., Draper, I., & Medina, R. (2011). Briófitos: una aproximación a las

plantas terrestres más sencillas. Memorias de La Real Sociedad Española de

Historia Natural. Segunda Época, (IX), 19–73.

Eva, H. D., Huber, O., Achard, F., Balslev, H., Beck, S., Behling, H., …

Colchester, M. (2005). A proposal for defining the geographical boundaries of

Amazonia. Office for Official Publications of the European Communities.

Excoffier, L. (1995). AMOVA 1.55 (analysis of molecular variance). University of

Geneva, Geneva.

Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of

programs to perform population genetics analyses under Linux and Windows.

Molecular Ecology Resources, 10(3), 564–567.

References 138

Florschütz-de Waard, J., & Bekker, J. M. (1987). A comparative study of the

bryophyte flora of different forest types in West Suriname. Cryptogamie.

Bryologie, Lichénologie, 8(1), 31–45.

Frahm, J.-P., & Gradstein, S. R. (1991). An altitudinal zonation of tropical rain

forests using byrophytes. Journal of Biogeography, 669–678.

Frahm, J.-P., Pócs, T., O’Shea, B., Koponen, T., Piipo, S., Enroth, J., … Fang, Y.

(2003). Manual of tropical bryology. Frahm.

Frego, K. A. (2007). Bryophytes as potential indicators of forest integrity. Forest

Ecology and Management, 242(1), 65–75.

Frey, W., Pfeiffer, T., & Stech, M. (2010). Geomolecular divergence patterns of

Gondwanan and Palaeoaustral bryophytes–An overview Studies in austral

temperate rain forest bryophytes 34. Nova Hedwigia, 91(3-4), 317–348.

Frey, W., & Stech, M. (2009). Bryophyta (Musci, mosses). In Frey, W. [ed.].

Syllabus of plant families A. Engler’s Syllabus der Pflanzenfamilien. Part 3.

Bryophytes and seedless vascular plants. 13th ed. Gebr. Borntraeger

Verlagsbuchhandlung, Stuttgart, Germany, 116–257.

Fulford, M. (1945). Studies on American hepaticae—VI. Ceratolejeunea. Brittonia,

5(4), 368–403.

Fulford, M., Crandall, B., & Stotler, R. (1970). Ecology of an elfin forest in Puerto

Rico. 11. The leafy Hepaticae of Pico del Oeste. Journal of the Arnold

Arboretum.

Fulford, M. (1968). Manual of the leafy Hepaticae of Latin America.

Gehrig-Downie, C. (2013). Epiphyte diversity and microclimate of the tropical

lowland cloud forest in French Guiana. Niedersächsische Staats-und

Universitätsbibliothek Göttingen.

Gentry, A. H., & Dodson, C. H. (1987). Diversity and biogeography of neotropical

vascular epiphytes. Annals of the Missouri Botanical Garden, 74(2), 205–233.

Gimingham, C. H., & Birse, E. M. (1957). Ecological studies on growth-form in

bryophytes: I. Correlations between growth-form and habitat. The Journal of

References 139

Ecology, 533–545.

Goffinet, B., & Shaw, J. (2009). Bryophyte Biology. Cambridge University Press.

Gradstein, S. R. (1992). vanishing tropical rain forest and environment for

bryophytes and lichens. In Bryophytes and Lichens in a Changing

Environment, edited by Jeffrey W. Bates and Andrew M. Farmer.

Gradstein, S. R. (1994). Lejeuneaceae: Ptychantheae, Brachiolejeuneae. Flora

Neotropica, 1–216.

Gradstein, S. R. (2006). The lowland cloud forest of French Guiana: a liverwort

hotspot. Cryptogamie. Bryologie, 27(1), 141–152.

Gradstein, S. R. (2013). A classification of Lejeuneaceae (Marchantiophyta) based

on molecular and morphological evidence. Phytotaxa, 100(1), 6–20.

Gradstein, S. R., Churchill, S. P., Balslev, H., Forero, E., & Luteyn, J. L. (1995).

Diversity of Hepaticae and Anthocerotae in montane forests of the tropical

Andes. In Biodiversity and conservation of Neotropical montane forests.

Proceedings of a symposium, New York Botanical Garden, 21-26 June 1993.

(pp. 321–334). New York Botanical Garden.

Gradstein, S. R., Churchill, S. P., & Salazar Allen, N. (2001). Guide to the

bryophytes of tropical America. New York Botanical Garden Press.

Gradstein, S. R., & da Costa, D. P. (2003). Hepaticae and anthocerotae of Brazil.

New York Botanical Garden Press.

Gradstein, S. R., & Ilkiu-Borges, A. L. (2009). Guide to the Plants of Central

French Guiana, Part IV. Liverworts.

Gradstein, S. R., Montfoort, D., & Cornelissen, J. H. C. (1990). Species richness

and phytogeography of the bryophyte flora of the Guianas, with special

reference to the lowland forest. Tropical Bryology, 2, 117–126.

Gradstein, S. R., & Pócs, T. (1989). Bryophytes. In Lieth, H. & Werger M.J.A.

(eds.). Tropical rain forest ecosystems, 311–325.

Gradstein, S. R., & Schäfer-Verwimp, A. (2011). A new species of Harpalejeunea

(Spruce) Schiffn.(Lejeuneaceae) from montane cloud forest of Colombia and

References 140

Costa Rica. Cryptogamie, Bryologie, 32(2), 101–106.

Gradstein, S. R., & Uribe, J. (2016). Marchantiophyta. In Bernal, R., Gradstein,

S.R. & Celis, M. [ed.]. Catalogue of plants of Colombia.

Grolle, R. (1992). Zwei neue Arten der Lebermoosgattung Diplasiolejeunea aus

der Neotropis. Friedrich-Schiller-Universitat.

Grolle, R., & Reiner–Drehwald, M. E. (1999). Review of the genus Harpalejeunea

(Lejeuneaceae) including the description of H. grandis, a new species from

the p{á}ramos of Colombia. Journal of Bryology, 21(1), 31–45.

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor

and analysis program for Windows 95/98/NT.

Hallingbäck, T. (2002). Globally widespread bryophytes, but rare in Europe.

Portugaliae Acta Biologica, 20(1), 11–24.

Hamilton, M. (2011). Population genetics. John Wiley & Sons.

Heinrichs, J., Dong, S., Schaefer-Verwimp, A., Peralta, D. F., Feldberg, K.,

Schmidt, A. R., & Schneider, H. (2014). Towards a monophyletic classification

of Lejeuneaceae II: subtribes Pycnolejeuneinae and Xylolejeuneinae subtr.

nov., transfer of Otolejeunea to Lepidolejeuninae, and generic refinements.

Phytotaxa, 163(2), 61–76.

Heinrichs, J., Dong, S., Schafer-Verwimp, A., Pocs, T., Feldberg, K., Czumaj, A.,

… Schneider, H. (2013). Molecular Phylogeny of the Leafy Liverwort

Lejeunea (Porellales): Evidence for a Neotropical Origin, Uneven Distribution

of Sexual Systems and Insufficient Taxonomy. PLoS ONE, 8(12), e82547.

Heinrichs, J., Hentschel, J., Wilson, R., Feldberg, K., & Schneider, H. (2007).

Evolution of leafy liverworts (Jungermanniidae, Marchantiophyta): estimating

divergence times from chloroplast DNA sequences using penalized likelihood

with integrated fossil evidence. Taxon, 31–44.

Heinrichs, J., Klugmann, F., Hentschel, J., & Schneider, H. (2009). DNA

taxonomy, cryptic speciation and diversification of the Neotropical-African

liverwort, Marchesinia brachiata (Lejeuneaceae, Porellales). Molecular

References 141

Phylogenetics and Evolution, 53(1), 113–121.

Hietz, P., & Hietz‐Seifert, U. (1995). Structure and ecology of epiphyte

communities of a cloud forest in central Veracruz, Mexico. Journal of

Vegetation Science, 6(5), 719–728.

Holz, I., Gradstein, S. R., Heinrichs, J., & Kappelle, M. (2002). Bryophyte diversity,

microhabitat differentiation, and distribution of life forms in Costa Rican upper

montane Quercus forest. The Bryologist, 105(3), 334–348.

Hooper, E. J. (2008). Ecological genetics of the moss Physcomitrella patens.

(Doctoral dissertation, The University of Leeds). The University of Leeds.

Hoorn, C., & Wesselingh, F. (2011). Amazonia, landscape and species evolution:

a look into the past. John Wiley & Sons.

Hosokawa, T., Odani, N., & Tagawa, H. (1964). Causality of the distribution of

corticolous species in forests with special reference to the physio-ecological

approach. The Bryologist, 67(4), 396–411.

Hubbell, S. P. (2001). The unified neutral theory of biodiversity and biogeography

(MPB-32) (Vol. 32). Princeton University Press.

Ilkiu-Borges, A. L., & Gradstein, S. R. (2008). A new species of Cheilolejeunea

(Spruce) Schiffn.(Lejeuneaceae) from Cerro de la Neblina, Venezuela. Nova

Hedwigia, 87(3-4), 521–528.

Kessler, M. (2000). Altitudinal zonation of Andean cryptogam communities.

Journal of Biogeography, 27(2), 275–282.

Kumagai, T., Kuraji, K., Noguchi, H., Tanaka, Y., Tanaka, K., & Suzuki, M. (2001).

Vertical profiles of environmental factors within tropical rainforest, Lambir Hills

National Park, Sarawak, Malaysia. Journal of Forest Research, 6(4), 257–

264.

Laaka-Lindberg, S., Korpelainen, H., & Pohjamo, M. (2003). Dispersal of sexual

propagules in bryophytes. Journal of the Hattori Botanical Laboratory, 93,

319–330.

Laenen, B. (2009). Role of Sexual Determinism in the Genetic Structure and

References 142

Diversity in Bryophytes: A Model Based on Two Sister Taxa in the Genus

Radula. Université de Liège. Liège, Belgium. [iv] 47. (Master’s thesis; treats

R. complanata and R. lindenbergiana).

Legendre, P., & Legendre, L. (1998). Numerical ecology: second English edition.

Developments in Environmental Modelling, 20.

Lesica, P., McCune, B., Cooper, S. V, & Hong, W. S. (1991). Differences in lichen

and bryophyte communities between old-growth and managed second-growth

forests in the Swan Valley, Montana. Canadian Journal of Botany, 69(8),

1745–1755.

Lewis, L. R., Rozzi, R., & Goffinet, B. (2014). Direct long‐distance dispersal

shapes a New World amphitropical disjunction in the dispersal‐limited dung

moss Tetraplodon (Bryopsida: Splachnaceae). Journal of Biogeography,

41(12), 2385–2395.

Linares, E. L., & Uribe-Meléndez, J. (2002). Libro rojo de briófitas de Colombia.

Instituto de Ciencias Naturales, Universidad Nacional de Colombia.

Lisboa, R. C. L. (1976). Estudos sobre a vegetacao das campinas amazônicas 5.

Brioecología de uma campina amazônica. Acta Amazonica, 6, 171–191.

Lloret, F. (1994). Gap colonization by mosses on a forest floor: an experimental

approach. Lindbergia.

Löbel, S., Snäll, T., & Rydin, H. (2009). Mating system, reproduction mode and

diaspore size affect metacommunity diversity. Journal of ecology, 97(1), 176-

185.

Magurran, A. E. (2013). Measuring biological diversity. John Wiley & Sons.

McCune, B. (1993). Gradients in epiphyte biomass in three Pseudotsuga-Tsuga

forests of different ages in western Oregon and Washington. Bryologist, 405–

411.

McCune, B., Grace, J. B., & Urban, D. L. (2002). Analysis of ecological

communities (Vol. 28). MjM software design Gleneden Beach, OR.

Miller, N. G., & McDaniel, S. F. (2004). Bryophyte dispersal inferred from

References 143

colonization of an introduced substratum on Whiteface Mountain, New York.

American Journal of Botany, 91(8), 1173–1182.

Mizutani, M. (1961). A revision of Japanese Lejeuneaceae. Journal of the Hattori

Botanical Laboratory, 24, 115– 302.

Montfoort, D., & Ek, R. C. (1990). Vertical distribution and ecology of epiphytic

bryophytes and lichens in a lowland rain forest in French Guiana. Institute of

Systematic Botany. Utrecht

Mota de Oliveira, S. (2010). Diversity of epiphytic bryophytes across the amazon.

Mota de Oliveira, S., Temme, A., Erkens, R. H. J., & ter Steege, H. (2011).

Dispersal and connectivity of populations of Cheilolejeunea rigidula

(Lejeuneaceae) in Amazonian forests: a pilot study. Boletim Do Instituto de

Botânica (São Paulo), 21, 133–139.

Mota de Oliveira, S., & ter Steege, H. (2013). Floristic overview of the epiphytic

bryophytes of terra firme forests across the Amazon basin. Acta Botanica

Brasilica. SciELO Brasil.

Mota de Oliveira, S., & ter Steege, H. (2015). Bryophyte communities in the

Amazon forest are regulated by height on the host tree and site elevation.

Journal of Ecology, 103, 441–450.

Mota de Oliveira, S., ter Steege, H., Cornelissen, J. H. C., & Gradstein, S. R.

(2009). Niche assembly of epiphytic bryophyte communities in the Guianas: a

regional approach. Journal of Biogeography, 36(11), 2076–2084.

Mouillot, D. (2007). Niche‐assembly vs. dispersal‐assembly rules in coastal fish

metacommunities: implications for management of biodiversity in brackish

lagoons. Journal of Applied Ecology, 44(4), 760–767.

Mu, Q., Heinsch, F. A., Zhao, M., & Running, S. W. (2007). Development of a

global evapotranspiration algorithm based on MODIS and global meteorology

data. Remote Sensing of Environment, 111(4), 519–536.

Nadkarni, N. M. (1986). The nutritional effects of epiphytes on host trees with

special reference to alteration of precipitation chemistry. Selbyana, 44–51.

References 144

Nieder, J., Engwald, S., & Barthlott, W. (1999). Patterns of neotropical epiphyte

diversity. Selbyana, 66–75.

Perry, D. R. (1978). A method of access into the crowns of emergent and canopy

trees. Biotropica, 155–157.

Pócs, T. (1982). Tropical forest bryophytes. In Bryophyte ecology (pp. 59–104).

Springer.

Pohjamo, M., Laaka-Lindberg, S., Ovaskainen, O., & Korpelainen, H. (2006).

Dispersal potential of spores and asexual propagules in the epixylic hepatic

Anastrophyllum hellerianum. Evolutionary Ecology, 20(5), 415–430.

Proctor, M. C. F. (1981). Diffusion resistances in bryophytes. In Symposium-

British Ecological Society.

Quesada, C. A., Lloyd, J., Anderson, L. O., Fyllas, N. M., Schwarz, M., &

Czimczik, C. I. (2011). Soils of Amazonia with particular reference to the

RAINFOR sites. Biogeosciences, 8(6).

Rambaut, A., & Drummond, A. J. (2014). FigTree version 1.4, available at. http.

tree.bio.ed.ac.uk/software/figtree.

Rangel, O. (2008). La vegetación de la región amazónica de Colombia –

Aproximación inicial. En: Colombia Diversidad Biótica VII. Vegetación,

palinología y paleoecología de la amazonía colombiana. Instituto de Ciencias

Naturales, Universidad Nacional de Colombia. 1-53.

Reese, W. D. (1993). Calymperaceae. Flora Neotropica, 1–101.

Rhoades, F. M., Lowman, M. D., & Nadkarni, N. M. (1995). Nonvascular epiphytes

in forest canopies: worldwide distribution, abundance, and ecological roles.

Forest Canopies., 353–408.

Ribeiro, J. E. L. da S. (1999). Flora da reserva ducke. INPA; DFID.

Richards, P. W. (1954). Notes on the bryophyte communities of lowland Tropical

Rain Forest, with special reference to Moraballi Creek, British Guiana.

Vegetatio, 5(1), 319–328.

Richards, P. W. (1984). The ecology of tropical forest bryophytes. New Manual of

References 145

Bryology, 1233–1270.

Rudas, A., & Prieto, A. (2005). Flora of the Amacayacu Amazonas National

Natural Park, Colombia. Missouri Botanical Garden Press.

Ruiz, C. A., & Aguirre, J. (2004). Distribución de la brioflora en el gradiente vertical

(suelo-dosel) y la selectividad de habitats en Tarapaca (Amazonas,

Colombia). Tropical Bryology, 81–96.

Schäfer-Verwimp, A., Lehnert, M., & Nebel, M. (2013). Contribution to the

knowledge of the bryophyte flora of Ecuador. Phytotaxa, 128(1), 1–63.

Shurin, J. B., Cottenie, K., & Hillebrand, H. (2009). Spatial autocorrelation and

dispersal limitation in freshwater organisms. Oecologia, 159(1), 151–159.

Schuster, R. M. (1983). Phytogeography of bryophyte. In: R.M. Schuster (ed.),

New Manual of bryology. Vol. 1. Hattori Botanical Laboratory, Nichinan., 463–

626.

Schuster, R. M. (2001). Revisionary studies on austral Acrobolbaceae, I. J. Hattori

Bot. Lab., 90, 97–166.

Sillett, S. C., & Antoine, M. E. (2004). Lichens and bryophytes in forest canopies.

Forest Canopies. Elseiver Academic Press, MA, 151–174.

SINCHI. (2010). Monitoreo de los bosques y otras coberturas de la Amazonia

colombiana, periodo 2002. Instituto Amazónico de Investigaciones

Científicas.

Soininen, J., McDonald, R., & Hillebrand, H. (2007). The distance decay of

similarity in ecological communities. Ecography, 30(1), 3–12.

Sporn, S. G., Bos, M. M., Kessler, M., & Gradstein, S. R. (2010). Vertical

distribution of epiphytic bryophytes in an Indonesian rainforest. Biodiversity

and Conservation, 19(3), 745–760.

Stech, M., & Quandt, D. (2014). 20,000 species and five key markers: the status

of molecular bryophyte phylogenetics. Phytotaxa, 9(1), 196–228.

Stropp, J. (2011). Towards an understanding of tree diversity in Amazonian

forests. University of Utrecht, CNPq, IEB, Gordon & Betty Moore Foundation,

References 146

Utrecht.

Subramaniam, A., Yager, P. L., Carpenter, E. J., Mahaffey, C., Björkman, K.,

Cooley, S., … Shipe, R. (2008). Amazon River enhances diazotrophy and

carbon sequestration in the tropical North Atlantic Ocean. Proceedings of the

National Academy of Sciences, 105(30), 10460–10465.

Sundberg, S., Hansson, J., & Rydin, H. (2006). Colonization of Sphagnum on land

uplift islands in the Baltic Sea: time, area, distance and life history. Journal of

Biogeography, 33(8), 1479–1491.

Swofford, D. L. (2003). Phylogenetic analysis using parsimony. Version 4. Sinauer

Associates, Sunderland, Massachusetts.

Szövényi, P., Hock, Z. S., & Tóth, Z. (2004). Phorophyte preferences of epiphytic

bryophytes in a stream valley in the Carpathian Basin. Journal of Bryology,

26(2), 137–146.

Tan, B. C., & Pócs, T. (2000). Bryogeography and conservation of bryophytes.

Bryophyte Biology, 1, 403–476.

Team, R. C. (2014). R: A language and environment for statistical computing.

Vienna, Austria: R Foundation for Statistical Computing; 2013.

ter Steege, H. (1998). Single Rope Techniques in Tropical Rain Forest Trees:

Going Down Safe and Sound1. Biotropica, 30(3), 496–497.

ter Steege, H., & Cornelissen, J. H. C. (1988). Collecting and studying bryophytes

in the canopy of standing rain forest trees. Methods in Bryology. Hattori

Botanical Laboratory, Nichinan, 285, 290.

ter Steege, H., Pitman, N. C. A., Sabatier, D., Baraloto, C., Salomão, R. P.,

Guevara, J. E., … Molino, J.-F. (2013). Hyperdominance in the Amazonian

tree flora. Science, 342(6156), 1243092.

ter Steege, H., Sabatier, D., Castellanos, H., van Andel, T., Duivenvoorden, J., de

Oliveira, A., … Mori, S. (2000). An analysis of the floristic composition and

diversity of Amazonian forests including those of the Guiana Shield. Journal

of Tropical Ecology, 16(06), 801–828.

References 147

Uribe, J. (2006). Type studies on Frullania subgenus Meteoriopsis (Hepaticae). V.

Frullania dulimensis sp. nov. from Colombia. Cryptogamie. Bryologie, 27(3),

309–312.

Uribe, J. M., & Gradstein, S. R. (1998). Catalogue of the Hepaticae and

Anthocerotae of Colombia.

Vanderpoorten, A., & Goffinet, B. (2009). Introduction to bryophytes. Cambridge

University Press.

Vekemans, X., & Hardy, O. J. (2004). New insights from fine‐scale spatial genetic

structure analyses in plant populations. Molecular Ecology, 13(4), 921–935.

Veneklaas, E. J., & Van Ek, R. (1990). Rainfall interception in two tropical

montane rain forests, Colombia. Hydrological Processes, 4(4), 311–326.

Wang, J., Gradstein, S. R., Shi, X.-Q., & Zhu, R. L. (2014). Phylogenetic position

of Trocholejeunea and a new infrageneric classification of Acrolejeunea

(Lejeuneaceae, Marchantiophyta). Bryophyte Diversity and Evolution, 36(1),

31–44.

Wei, Y.-M., He, Q., Gradstein, S. R., Campos, L. V, & Zhu, R.-L. (2013). Notes on

Early Land Plants Today. 46. Transfer of Vitalianthus urubuensis

(Marchantiophyta, Lejeuneaceae) to Cheilolejeunea. Phytotaxa, 152(1), 50–

52.

Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of

population structure. Evolution, 1358–1370.

Wilson, R., Gradstein, S. R., Schneider, H., & Heinrichs, J. (2007). Unravelling the

phylogeny of Lejeuneaceae (Jungermanniopsida): evidence for four main

lineages. Molecular Phylogenetics and Evolution, 43(1), 270–282.

Wilson, R., Heinrichs, J., Hentschel, J., Gradstein, S. R., & Schneider, H. (2007).

Steady diversification of derived liverworts under Tertiary climatic fluctuations.

Biology Letters, 3(5), 566–569.

Wolf, J. H. D. (1993). Diversity patterns and biomass of epiphytic bryophytes and

lichens along an altitudinal gradient in the northern Andes. Annals of the

References 148

Missouri Botanical Garden, 928–960.

Wright, S. (1943). Isolation by distance. Genetics, 28(2), 114.

Wright, S. (1978). Evolution and the genetics of populations: a treatise in four

volumes: Vol. 4: variability within and among natural populations. University of

Chicago Press.

Xiao, Z., Liang, S., Wang, J., Chen, P., Yin, X., Zhang, L., & Song, J. (2014). Use

of general regression neural networks for generating the GLASS leaf area

index product from time-series MODIS surface reflectance. IEEE

Transactions on Geoscience and Remote Sensing, 52(1), 209-223.

Ye, W., Gradstein, S.R., Show, B., Ho, B.C., Schafer-Verwimp, A., Pocs, T.,

Heinrichs, J. & Zhu, R.-L. (2015). Phylogeny and classification of

Lejeuneaceae subtribe Cheilolejeuneinae (Marchantiophyta) based on

nuclear and plastid molecualr markers. Cryptogamie, Bryologie, 36(4), 313–

373.

Zartman, C. (2003). Habitat fragmentation impacts on epiphyllous bryophyte

communities in central Amazonia. Ecology, 84(4), 948–954.

Zartman, C. E., & Ackerman, I. L. (2002). A new species of Vitalianthus

(Lejeuneaceae, Hepaticae) from the Brazilian Amazon. The Bryologist,

105(2), 267–269.

Zartman, C., & Ilkiu-Borges, A. L. (2007). Guia para as briófitas epífilas da

Amazônia Central. Fundação de Amparo à Pesquisa do Estado do

Amazonas.

Zotz, G., Schweikert, A., Jetz, W., & Westerman, H. (2000). Water relations and

carbon gain are closely related to cushion size in the moss Grimmia

pulvinata. New Phytologist, 148(1), 59–67.

Diversity of epiphytic bryophytes of the Colombian … · Diversity of epiphytic bryophytes of the...

Documents

Transcript of Diversity of epiphytic bryophytes of the Colombian … · Diversity of epiphytic bryophytes of the...