Diet and food partitioning between juveniles of mutton ... fileDiet of juvenile mutton Lutjanus...

Journal of Fish Biology (2010) 76, 2299–2317

doi:10.1111/j.1095-8649.2010.02586.x, available online at www.interscience.wiley.com

Diet and food partitioning between juveniles of muttonLutjanus analis, dog Lutjanus jocu and lane Lutjanus

synagris snappers (Perciformes: Lutjanidae)in a mangrove-fringed estuarine environment

C. R. Pimentel* and J.-C. Joyeux

Departamento de Oceanografia e Ecologia, Universidade Federal do Espírito Santo,Av. Fernando Ferrari, 514 Goiabeiras, 29075-910 Vitoria, Espírito Santo, Brazil

(Received 25 July 2009, Accepted 19 January 2010)

Diet of juvenile mutton Lutjanus analis, dog Lutjanus jocu and lane Lutjanus synagris snapperswere studied in the tropical Brazilian estuarine system of the Piraque-acu and Piraque-mirim Riversto determine how these species share the resources in this restricted space. The three species preyprincipally upon Peracarida (L. synagris: relative importance index IRIc = 29%), Natantia (L. analisand L. synagris: IRIc = 39 and 38%, respectively), Reptantia (L. analis and L. jocu: IRIc = 28and 43%, respectively) and Teleostei (L. jocu: IRIc = 24%). The three species use estuaries asnursery habitats but food overlap was not biologically significant due to a combination of inter-specific differences in size, spatial distribution, microhabitat preferences and seasonal patterns ofabundance and prey choice. Large marine protected areas incorporating essential habitats for alllife stages are suggested to be the best tool for the management of these economically importantspecies. © 2010 The Authors

Journal compilation © 2010 The Fisheries Society of the British Isles

Key words: diet overlap; estuary; nursery areas; south-western Atlantic Ocean.

INTRODUCTION

Many tropical fish species use mangrove-fringed estuaries as nursery areas. Theyreside in these environments while juveniles; the complex three-dimensional struc-ture provides higher availability of food resources and minimizes the incidence ofpredation (Laegdsgaard & Johnson, 1995, 2001; Nagelkerken et al., 2000a, 2001).This pattern of utilization of these environments is shown by several snapper speciesin Brazil (Andreata et al., 1997; Chagas et al., 2006) and elsewhere (Sheaves, 1995;Sierra & Popova, 1997; Nagelkerken et al., 2000b; Cocheret de la Moriniere et al.,2002, 2003). Before recruiting into adult stocks over reefs, shelf or continental slopeareas (Costa et al., 2005; Fredou & Ferreira, 2005; Klippel et al., 2005; Fredouet al., 2006), the mutton snapper Lutjanus analis (Cuvier), the dog snapper Lutjanusjocu (Bloch & Schneider) and the lane snapper Lutjanus synagris (L.) commonly

*Author to whom correspondence should be addressed. Tel.: +55 27 4009 7791; fax: + 55 4009 2500;email: [email protected]

2299© 2010 The AuthorsJournal compilation © 2010 The Fisheries Society of the British Isles

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use estuaries during their juvenile phase. Only L. jocu, however, is considered atruly estuarine-dependent species, whereas the other two are considered estuarine-facultative or independent species (Lindeman et al., 2000; Martinez-Andrade, 2003).

Most snapper species are considered important fishing resources in their areaof occurrence, principally because the excellent quality of their meat generateshigh demand and considerable economic value (Fredou et al., 2006). As elsewhere(Martinez-Andrade, 2003) L. analis, L. jocu and L. synagris show slow growth(growth coefficient of the von Bertalanffy equation k < 1·5 year−1) and mediumto high longevity (generally >10 years) on the Brazilian coast (Rezende & Fer-reira, 2004; Klippel et al., 2005; Leite et al., 2005). These characteristics make themvulnerable to overfishing and all three species show moderate to high levels of over-exploitation by hand-line commercial fisheries (Klippel et al., 2005; Fredou et al.,2009a, b). Lutjanus analis was listed as ‘vulnerable’ in the first edition of the Brazil-ian red list (IBAMA, 2004) before being lowered to the category ‘overfished or underrisk of overfishing’ in later editions.

On the central coast of Brazil, juveniles of these three species of snappers [meantotal length (LT) at maturity: 488, 437 and 241 mm, respectively; Martinez-Andrade,2003] are sympatric in estuaries and embayments (Chagas et al., 2006; Araujo et al.,2008). This raises both the concern about the preservation of these coastal areasand the interest in determining how these species share the niches available in thatrestricted space. In this context, knowledge of the trophodynamics of key speciesallows the building of a functional model of the ecosystem, which can help inits management (Duarte & García, 1999a, b) and consequently in its conservation.Therefore, the study of feeding habits and partitioning of food resources are importanttools for resource managers to evaluate natural community structures and then tryto understand how human disturbances can affect them. Moreover, considering thatfood overlap can lead to competition, this information is essential for understandingthe actual mechanisms that allow the coexistence of several species.

Thus, the primary objectives of the study were to determine the feeding ecology ofthe three snapper species and to estimate the degree of food overlap between them.The study was conducted in the estuarine system of the Piraque-acu and Piraque-mirim Rivers (a small area where illegal fishing is not so widespread or intenseas elsewhere) under the hypothesis that the diets of such congeneric species arebiologically similar. In addition, the hypothesis that there is no intraspecific dietvariation between the two estuaries, since they are connected environments, wastested.

MATERIALS AND METHODS

S T U DY A R E AThe estuarine system of the Piraque-acu and Piraque-mirim Rivers (17◦ 58′ S; 40◦ 00′ W)

is located in the municipality of Aracruz, state of Espírito Santo, Brazil (Fig. 1). It has a‘Y’ shape with the northern estuary Piraque-acu (PA) joining the southern estuary Piraque-mirim (PM) c. 1·5 km west of the system mouth. The open water area covers 5·1 km2.The geographic setting and hydrology of the system have been studied by Barroso (2004),and most of the following information is extracted from this source unless stated otherwise.The climate is tropical, characterized by a dry and mild winter and a hot and rainy sum-mer. Most of the rain is concentrated between October and March [1947 to 2007 historical

© 2010 The AuthorsJournal compilation © 2010 The Fisheries Society of the British Isles, Journal of Fish Biology 2010, 76, 2299–2317

D I E T A N D F O O D PA RT I T I O N I N G B E T W E E N T H R E E L U T JA N U S S P P. 2301

40° 15′ 20′′ W19° 53′ 31′′ S

40° 07′ 53′′ W19° 58′ 56′′ S

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AtlanticOcean

Piraquê-mirim Estuary

Piraquê-açú Estuary

Fig. 1. The Piraque-acu–Piraque-mirim Estuaries, Brazil (modified from Barroso, 2004) showing the eightsampling stations ( ) and the fringe mangrove forest ( ).

series for precipitation, with 57 complete years; Hydrographical Information System of theNational Agency of Waters (http://hidroweb.ana.gov.br/) for the station 1940002 (19◦ 57′23′ S; 40◦ 09′ 17′′ W)]. Due to an El Nino southern oscillation episode (+1·2 sigma peak;http://www.cdc.noaa.gov/people/klaus.wolter/MEI/), however, the study period was atypicalin terms of rainfall. The rainy season immediately before sampling (October 2002 to March2003) showed only about half the normal rainfall on the lowlands (312 mm v. median =773 mm; n = 52), a situation that occurs about once every 10 years on average. During thesampling period, precipitation was low to moderate and the 2003 to 2004 rainy season startedlate with heavier rainfall starting in December 2003. The estuarine system is weakly strat-ified and the freshwater flow is much smaller than the tidewater volume. The tidal regimeis microtidal (1·4 to 1·5 m maximum variation in height) with semi-diurnal mixed tides.Salinity is lower in the PA (mean ± s.d. 28·1 ± 9·6 at 1 m depth during the period sampled;n = 124) than in the PM (mean ± s.d. 30·2 ± 8·6; n = 120). Barroso (2004) consideredthe upper section of PA a mesohaline estuary (5 < salinity < 18) subjected to oligohaline(0·5 < salinity < 5) and freshwater (salinity < 0·5) events, whereas its lower section andthe entire PM as a polyhaline environment (18 < salinity < 30). Euhaline conditions (30 <salinity < 40) predominate from the confluence of the two estuaries to the system mouth.Temperatures tend to be warmer in summer (mean ± s.d. 27·9 ± 1·0◦ C at 1 m depth duringthe period sampled; n = 48) and slightly cooler in the winter (mean ± s.d. 23·5 ± 0·5◦ C;n = 48). The PA upper section shows higher turbidity than the lower section and the PM. Thisprobably occurs because the PA receives a much greater freshwater input from a drainagearea 5·4 times larger (376 v. 69 km2) than the PM. In general, the PA is shallower thanthe PM (mean ± s.d. 4·3 ± 1·8 and 5·7 ± 2·0 m in the PA and PM, respectively, duringthe period and at the stations sampled; n = 120 and 122) and its depth increases seawards,whereas the opposite occurs in the PM. At present, the native vegetation is restricted to theintertidal zone and the slopes of the low-altitude plateau within which is inserted the estuarinesystem. The mangrove forest still occupies 12·3 km2 and comprises red mangrove Rhizophoramangle, black mangrove Avicennia schaueriana and white mangrove Laguncularia racemosa.Despite fragile law enforcement, trawling is limited (trawling is illegal in Brazilian estuaries).Most fishing is recreational or for subsistence.



Table I. Grouping of sampling dates within seasons

Season Sampling date

Autumn 2003 10 April, 7 May, 7 JuneWinter 2003 5 July, 4 August, 2 SeptemberSpring 2003 2 October, 1 November, 30 NovemberSummer 2003–2004 21 December, 31 January, 29 FebruaryAutumn 2004 3 April, 30 April, 27 May, 27 June

S A M P L I N G D E S I G N

Monthly replicated samples (n = 244) were collected in the PA and in the PM betweenApril 2003 and June 2004, in diurnal sessions (c. from 0700 to 1700 hours) during neap tideperiods. The eight stations sampled were approximately equidistantly distributed, with fourstations in each estuary (Fig. 1). The wing trawl had an 8·62 m head rope and a 10·43 mground rope, stretched mesh of 13 mm in the wings and belly and 5 mm in the cod end.The tows lasted 5 min (mean ± s.d. = 4·96 ± 0·25 min) and the position of the boat wasgeoreferenced using a GPS (Garmin 12; www.garmin.com) at the beginning and at eachpassing minute of the tow until its completion. Salinity and temperature were measured ateach station before towing (n = 244 for both) at a depth of 1 m with a multiparameter meter(YSI-85; www.ysi.com). Depth at sampling was measured with a depth meter (SpeedtechSM-5; www.speedtech.com) at the beginning of each tow (n = 242). The fishes capturedwere immediately put on ice and later frozen.

L A B O R ATO RY P RO C E D U R E S

In the laboratory, the fishes were thawed and identified to species level according toMenezes & Figueiredo (1980). Standard length (LS) was measured to the nearest millimetreand the total mass (MT) with precision of ±0·01 g. Neither sex nor maturity status wasassessed routinely. The guts (from oesophagus to anus) were extracted and stored in 70%ethanol. The identification of food items was done under binocular microscope (Leica MZ75;www.leica-microsystem.com) to the lowest taxonomic level possible, according to Figueiredo& Menezes (1978, 2000) and Menezes & Figueiredo (1980, 1985) for fishes, Melo (1996,1999) for Reptantia, Kensley & Schotte (1989) for Isopoda and Tavares (2002) for Natantia.The food items were enumerated and later grouped in food categories. The eight categorieswere (1) infraclass Teleostei (otolith pairs, scales and vertebrae were considered one individ-ual); (2) suborder Reptantia (isolated claws were considered as one individual); (3) suborderNatantia; (4) superorder Peracarida; (5) other invertebrates (classes Gastropoda and Poly-chaeta); (6) animal material (unidentified animals remains); (7) vegetal material (leaves andbranches); (8) inorganic material. To analyse the spatial and seasonal variations of the dietof each species, the categories were segregated by estuaries (PA and PM) and by season(Table I), oven-dried at 60◦ C during 24 h and weighted with precision of ±0·0001 g.

S TAT I S T I C A L A NA LY S E S

Differences in LS between the two species (interspecific) or between estuaries for thesame species (intraspecific) were tested by a Mann–Whitney non-parametric U -test (MW )for two independent samples (with Monte-Carlo resampling, 10 000 runs; n = 43, 48 and90 for L. analis, L. jocu and L. synagris, respectively). The differences in LS between allthree species (n = 181) and the seasonal variation in LS for the three species (n = 43, 48and 90 for L. analis, L. jocu and L. synagris, respectively) were tested by the non-parametricKruskal–Wallis test (KW ) for k independent samples (with Monte-Carlo resampling, 10 000runs). The tests were carried out using SPSS for Windows, version 12 (www.spss.com).



Food analyses were done using data from either the food items (i; not grouped) or the foodcategories (c; grouped). The Shannon–Wiener diversity index (H ′

i ; using ln) of the diet, thefrequency of occurrence (%Fi) and the numerical frequency (%Ni) of items were computedusing food-item data. The frequency of occurrence (%Fc) and the numerical frequency (%Nc)were calculated from the food-category data and the mass frequency (%Mc) from the dry-mass data. Animal, vegetal and inorganic material categories were not included in %Nc [northe absolute importance index (IAc) or relative importance index (IRc); see below] due tothe impossibility of enumeration. The IAc of each category George & Hadley, 1979 and theIRc (George & Hadley, 1979) were calculated from: IAc = %Fc + %Nc + %Mc and IRc =100IAc(

∑nc=1 IAc)

−1.Non-metric multidimensional scaling (nMDS) was used to explore the spatial and seasonal

variation in the diets of the three species, using IRc, Bray–Curtis similarity and fourth-rootdata transformation (Clarke & Warwick, 1994). Matrices were either five food categories ×6 (three species × two estuaries) or five food categories × 15 (three species × five seasons)and were analysed in Primer for Windows, version 5·2·4. Diet overlap was calculated usingthe Schoener’s index (T ; Schoener, 1970): T = 1 − 0·5 ∑n

i=1 |Pxi − Pyi | where Pxi and Pyi

are the proportions by number of item i for species x and y, respectively. The index variesfrom 0, when the two diets contain no item in common, to 1 when they are identical. A valueof T ≥ 0·6 was considered biologically significant (Scrimgeour & Winterbourn, 1987).

RESULTS

VA R I AT I O N I N LS

The three species differed in LS (KW ; P ≤ 0·001) and L. synagris was sig-nificantly smaller (mean ± s.d. = 77 ± 33 mm; range 18 to 162 mm) than theother species (MW ; P ≤ 0·001 for both tests). Differences were also detected (MW ;P < 0·05) between L. analis (122 ± 60 mm; range 20 to 249 mm) and L. jocu (143± 49 mm; range 17 to 237 mm). The three species had a larger mean LS in thePM (130 ± 57, 165 ± 45 and 82 ± 36 mm for L. analis, L. jocu and L. synagris)than in the PA (113 ± 64, 122 ± 44 and 74 ± 30 mm for L. analis, L. jocu andL. synagris). The difference between estuaries, however, was only significant forL. jocu (MW ; P < 0·001). The mean length of L. jocu considerably decreased dur-ing summer (Fig. 2). The lowest mean LS for L. analis and L. synagris occurredduring the autumn of 2003. The LS increased later to decrease again in the autumnof 2004. Seasonal variation in LS was only significant for L. jocu and L. synagris(KW ; P < 0·01 and <0·05, respectively).

C O M P O S I T I O N O F D I E T

Food was found in 93% (n = 40), 94% (n = 45) and 90% (n = 81) of the stom-achs of L. analis, L. jocu and L. synagris. Many fragile items were in advancedstages of digestion at the time of capture, indicating that opportunistic feeding in thetrawl was unlikely. In addition, hauls were short (5 min), limiting the time avail-able for the individuals to feed (or swallow) potential prey in the net. Among the28 taxonomic categories consumed by L. analis, the most important were Natantia(IRc = 39·11%), principally from the infraorder Penaeidea (%Ni = 11·21) and Rep-tantia (IRc = 28·48%), mainly from the family Xanthidae (%Ni = 10·31) (Table II).This was the only species that preyed on the food category other invertebrates(IRc = 5·38%), which was composed basically by the class Gastropoda (%Ni =



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Fig. 2. Seasonal variation in mean ± s.d. standard length (LS) of Lutjanus analis ( ), Lutjanus jocu ( ) andLatjanus synagris ( ) in the Piraque-acu and Piraque-mirim Estuaries during 2003 to 2004.

1·79). For L. jocu, 26 taxonomic categories were identified, including primarilyReptantia (IRc = 43·81%), also numerically dominated by the family Xanthidae(%Ni = 17·31), and Teleostei (IRc = 24·30%), mostly from the family Gerreidae(%Ni = 2·88) (Table II). For L. synagris, 24 taxonomic categories were identified,with Natantia (IRc = 38·41%), predominantly from the infraorder Penaeidea (%Ni =5·87), and Peracarida (IRc = 29·18%), predominantly from the order Mysidacea(%Ni = 24·86), being the most important (Table II). None of the three snapperspecies preyed upon the other, and cannibalism was not registered.

The three snapper species consumed a wide variety of invertebrates and fishes, butfeeding was clearly bottom-oriented. Thus, the majority of the organisms consumedwere typically epibenthic, sometimes demersal (Gerreidae of the genera Eucinosto-mus and Diapterus), rarely pelagic (Engraulidae). A single fish prey (a SiluriformesCallichthyidae taken by L. jocu) was characteristic of continental waters and all oth-ers were marine or brackish species. Except for Grapsidae consumed by L. jocu, theBrachyura crustaceans belonged to species that do not typically live in the intertidalzone, in mud burrows (e.g. Oxypodidae) or on vegetation roots but are found on opensandy–muddy areas (i.e. Portunidae) and hard-bottom substrata (i.e. Xanthidae). Insome cases, these prey were represented by a single isolated claw that, occasionally,filled every available space in the gut. The Anomura were represented by speciesthat do not use gastropod shells for protection (squat lobsters) and species that do(hermit crabs). In the latter case, no associated shells were found. Penaeidea shrimpswere the Natantia crustaceans most consumed by L. analis and L. synagris, whereasCaridea, mainly from the family Alpheidae (crack-pistol shrimp), were the mostcommon Natantia preyed by L. jocu. Vegetal and inorganic materials were probablyconsumed while snappers were capturing prey that live on the bottom. The gastropodconsumed by L. analis were extremely small (<2 mm length) compared with thefish (113, 184 and 196 mm LS) and were probably ingested by accident.



Table II. Frequency of occurrence (%Fi) and numerical frequency (%Ni) of the dietaryitems identified in digestive tracts of juveniles of Lutjanus analis, Lutjanus jocu and Lutjanussynagris (n, number of guts with food) from the Piraque-acu and Piraque-mirim Estuaries,

Brazil. Families and species within families are listed alphabetically

L. analis (n = 40) L. jocu (n = 45) L. synagris (n = 81)

Food item %Fi %Ni %Fi %Ni %Fi %Ni

Teleostei 30·00 6·28 15·56 4·33 12·35 3·91Callichthyidae 0 0 2·22 0·48 0 0Cynoglossidae 0 0 2·22 0·48 0 0Engraulidae 2·50 0·90 0 0 1·23 0·28Gerreidae — — — — — —Diapterus sp. 0 0 2·22 0·48 0 0Eucinostomus sp. 5·00 0·90 6·67 2·40 1·23 0·28Gobiidae 7·50 1·35 0 0 1·23 0·28Ctenogobius boleosoma 2·50 0·45 0 0 0 0Ophichthidae — — — — — —Myrophis punctatus 2·50 0·45 0 0 0 0Paralichthyidae 2·50 0·90 0 0 0 0Triglidae 2·50 0·45 0 0 0 0Reptantia — — — — — —Brachyura 35·00 8·07 37·78 12·50 14·81 3·63Goneplacidae 0 0 0 0 1·23 0·28Grapsidae 0 0 13·33 4·33 0 0Goniopsis sp. 0 0 6·67 3·37 0 0Pachygrapsus sp. 0 0 2·22 0·48 0 0Portunidae–Polybiinae — — — — — —Ovalipes trimaculatus 2·50 0·45 0 0 0 0Portunidae–Portuninae 10·00 2·24 13·33 2·88 4·94 1·12Callinectes sp. 7·50 1·79 4·44 0·96 3·70 0·84Portunus anceps 5·00 1·35 0 0 0 0Xanthidae 15·00 8·97 13·33 4·81 2·47 0·56Hexapanopeus sp. 5·00 1·35 24·44 12·02 9·88 2·23Panopeus sp. 0 0 2·22 0·48 1·23 0·28Anomura 2·50 0·90 11·11 5·29 2·47 0·56Petrolisthes armatus 0 0 2·22 0·48 0 0Thalassinidea 0 0 0 0 2·47 0·84Natantia 50·00 39·91 24·44 13·94 43·21 24·86Caridea 10·00 2·24 4·44 0·96 3·70 0·84Alpheidae 20·00 4·93 11·11 3·37 4·94 1·12Penaeidea 30·00 11·21 8·89 3·85 17·28 5·87Peracarida 0 0 0 0 6·17 24·30Amphipoda 2·50 0·45 6·67 1·44 6·17 1·96Isopoda 5·00 0·90 11·11 2·88 3·70 1·12Mysidacea 2·50 1·35 6·67 17·79 27·16 24·86Other invertebrates — — — — — —Gastropoda 10·00 1·79 0 0 0 0Polychaeta 2·50 0·45 0 0 0 0Animal material 22·50 — 15·56 — 29·93 —Vegetal material 12·50 — 22·22 — 19·75 —Inorganic material 7·50 — 6·67 — 12·35 —



S PAT I A L VA R I AT I O N O F D I E T

The diet of L. analis was dominated by Natantia followed by Reptantia in bothestuaries (Fig. 3). Reptantia dominated the diet of L. jocu in both estuaries. Teleostei,in the PA, and Natantia, in the PM, were second in importance. The diet of L. synagriswas dominated by Peracarida and Natantia in the PA and Natantia followed byReptantia in the PM. Two categories were more important in the PM than in thePA: Natantia for L. synagris and Reptantia for L. jocu. Peracarida (for L. jocu andL. synagris) and Teleostei (for L. jocu), however, were consumed more in the PA thanin the PM. Overall, the diets of the three snappers were species specific and showedlower spatial variation in L. analis and L. synagris than in L. jocu [Fig. 4(a)]. In thelatter case, the larger individuals present in the PM consumed a higher proportionof Reptantia than the smaller individuals in the PA.

S E A S O NA L VA R I AT I O N O F D I E T

Overall, the diets were species specific and showed low (L. synagris), medium(L. jocu) and high (L. analis) seasonal variation. Latjanus analis and L. jocu dietswere on occasion (in autumn) extremely similar due to high consumption of Teleosteiand absence of Peracarida [Fig. 4(b)]. Winter, spring and summer L. analis diet[Fig. 4(b)] differed by including other invertebrates and, in spring, by excludingTeleostei. Thus, the clearest seasonal pattern was presented by L. analis in whichthe relative importance of Natantia, Peracarida and other invertebrates increased fromautumn to spring to decrease later in inverse proportion to the larger prey Teleosteiand Reptantia (Fig. 5). For the others species, the IRc of food categories variedapparently haphazardly around an average diet (Fig. 5). The diet of L. jocu wasdominated by Reptantia in all seasons but most notably in winter. Natantia tendedto dominate in the diet of L. synagris from autumn 2003 to spring and Peracaridato dominate in the other seasons.

D I E T D I V E R S I T Y

The more diverse diet was that of L. jocu (H ′ = 2·62), followed by L. analis(H ′ = 2·26) and L. synagris (H ′ = 2·02). The diets of all species were more diversein the PM than in the PA (H ′ = 2·75 and 1·87 for L. analis, respectively; 2·74and 2·26 for L. jocu; 2·29 and 2·06 for L. synagris). The seasonal variation in dietdiversity did not present a common interspecific pattern (Fig. 6). The diet was morediverse in summer for L. analis and in the autumn 2003 for L. jocu and L. synagris.The lowest diversities occurred in autumn 2004 for L. analis, in the spring for L. jocuand in the summer for L. synagris.

D I E T OV E R L A P

In none of the analysed situations was diet overlap biologically significant, i.e.≥0·60. The highest interspecific value occurred between L. jocu and L. synagris(T = 0·53). T -values for overlap between L. analis and its two congeneric specieswere equal (T = 0·48). This general pattern could still be detected in the PA afterfishes were segregated by estuaries (Table III). In the PM, however, the highest over-lap value occurred between L. analis and L. synagris and the lowest was between



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Fig. 3. Variation between estuaries [Piraque-acu and Piraque-mirim (PM) Estuary] of the relative importance

index (IRc) for the food categories [Teleostei ( ), Reptantia ( ), Natantia ( ), Peracarida ( ) and otherinvertebrates ( )] in (a) Lutjanus analis, (b) Lutjanus jocu and (c) Lutjanus synagris diets.



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Fig. 4. Non-metric multidimensional scaling analyses for (a) spatial and (b) seasonal variation in snapper[Lutjanus analis (La), Lutjanus jocu (Lj) and Lutjanus synagris (Ls)] diets using the relative importanceindex (IRc). The estuary [Piraque-acu (PA) or Piraque-mirim (PM)] or the season (A1, Autumn 2003; W,Winter; Sp, Spring; Su, Summer; A2, Autumn 2004) are furnished beside the snappers species.

L. jocu and L. synagris. Seasonal comparisons indicated that the overlap betweenL. analis and L. jocu varied from a maximum in autumn 2004 and a minimum inwinter. In the two other cases (L. analis v. L. synagris and L. jocu v. L. synagris), thehighest overlaps were registered in winter and autumn 2003 and the lowest in sum-mer. Note that many seasonal overlaps between species are based on a relatively smallnumber of values (Table IV). Intraspecific comparisons between estuaries showed thehighest T -value for L. analis (T = 0·56), followed by L. synagris (T = 0·53) andL. jocu (T = 0·50).

DISCUSSION

The region between Abrolhos Bank (c. 18◦ S) and Cape of Sao Tome (22◦ 22′ S),where the PA–PM estuarine system is located, is a faunistic transition zone between



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Fig. 5. Seasonal variation in relative importance index (IRc) of the food categories [Teleostei ( ), Reptantia( ), Natantia ( ), Peracarida ( ) and other invertebrates ( )] in (a) Lutjanus analis, (b) Lutjanus jocuand (c) Lutjanus synagris diets.



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1·0

Fig. 6. Seasonal variation of Lutjanus analis ( ), Lutjanus jocu ( ) and Lutjanus synagris ( ) diet diversity(Shannon–Wiener index). The vertical axis starts at 1·0 to emphasize the interspecific differences.

the northern (i.e. tropical oceanic domain) and the southern (i.e. subtropical to tem-perate oceanic domain) areas of the Brazilian coast (Joyeux et al., 2001; Ferreiraet al., 2004; Chagas et al., 2006). This transition seems to be generated by regionaloceanographic processes, like permanent or intermittent upwelling events, and bylatitude (i.e. temperature gradient related). Both marine (Floeter et al., 2001, 2004)and estuarine (Vieira & Musick, 1993, 1994) organisms and communities have beenfound to gradually shift along this transition zone. It appears that the utilization ofestuarine areas by the snappers varies regionally. Estuaries show an increase in snap-per species richness and numerical abundance north of this zone and a low diversityand low abundance south of it (Teixeira & Falcao, 1992; Vieira & Musick, 1994;Araujo et al., 2002; Vendell et al., 2003; Chagas et al., 2006; Monteiro-Neto et al.,2008). Differences in estuary typology between the northern and southern domainsmay play a role but the observed changes in richness and abundance also fit with the

Table III. Spatial and seasonal variation in diet overlap (Schoener’s index, T ) between Lut-janus analis, Lutjanus jocu and Lutjanus synagris in the Piraque-acu and Piraque-mirim

Estuaries, Brazil

Snapper pair Piraque-acu Piraque-mirim

L. analis v. L. jocu 0·40 0·56L. analis v. L. synagris 0·35 0·57L. jocu v. L. synagris 0·58 0·44

Autumn (2003) Winter Spring Summer Autumn (2004)

L. analis v. L. jocu 0·37 0·28 0·30 0·31 0·45L. analis v. L. synagris 0·35 0·57 0·39 0·16 0·35L. jocu v. L. synagris 0·53 0·48 0·39 0·14 0·15



Table IV. Number of guts with food analysed to assess the diet of Lutjanus analis, Lutjanusjocu and Lutjanus synagris in the Piraque-acu and Piraque-mirim Estuaries, Brazil

Species Piraque-acu Piraque-mirim

L. analis 21 19L. jocu 23 22L. synagris 45 36

Autumn (2003) Winter Spring Summer Autumn (2004)

L. analis 8 7 4 15 6L. jocu 11 10 7 11 6L. synagris 12 29 21 11 8

reported importance of the snapper species in the commercial fisheries, i.e. negligiblesouth of the Cape of Sao Tome (Bernardes et al., 2005; Claro & Lindeman, 2008)but important northward (Costa et al.; 2003, 2005; Fredou & Ferreira, 2005; Klippelet al., 2005; Fredou et al., 2006).

Within the transition zone, only L. analis, L. jocu and L. synagris use estuar-ine environments (Chagas et al., 2006; Araujo et al., 2008; R. M. Macieira, pers.comm.) even though other snapper species are present on the coast, e.g. Lutjanusalexandrei Moura & Lindeman, Lutjanus chrysurus (Bloch), Lutjanus cyanopterus(Cuvier) and Lutjanus purpureus (Poey). The mean total length (LT) at 50% maturitycomputed by Martinez-Andrade (2003) from published sources for these species are448 mm for L. analis, 437 mm for L. jocu and 241 mm for L. synagris, i.e. c. 362,365 and 200 mm LS, respectively. These lengths are well above the maximum sizerecorded in the present study or in the nearby Baía de Vitoria. There, L. analis were≤246 mm LS (n = 551), L. jocu ≤189 mm LS (n = 44) and L. synagris ≤180 mmLS (n = 1673) [unpubl. data; Chagas et al. (2006) provide a full analysis of spatialand temporal abundance patterns for the three species in that estuary]. Thus, juvenilesnappers probably use estuaries as nursery areas in an opportunistic manner becausethey can also be commonly found in non-estuarine ecosystems such as tidepools,embayments and shallow coastal areas (Sierra & Popova, 1997; Araujo et al., 2008;Claro & Lindeman, 2008; pers. obs.). Contrary to adults that are mainly nocturnal,juveniles of L. analis principally feed during daylight hours (Mueller et al., 1994).For their part, L. jocu forages under daylight conditions while L. synagris is report-edly nocturnal (Claro & Lindeman, 2008). The low vacuity coefficient found for allspecies, however, tends to indicate that their rhythms of feeding activity are similarand diurnal in the estuarine system.

G E N E R A L C O M P O S I T I O N O F D I E T

Overall, adults of snapper species are classified as generalist and opportunisticcarnivores (Randall, 1967; Duarte & García, 1999a, b; Rojas-Herrera et al., 2004).Correspondingly, high prey diversity was observed in the diet of the juveniles ofall species. Most prey were epibenthic organisms, which indicate that these fishesforage near the bottom. There are, however, some indirect indications that in theestuarine system the three species occupy distinct microhabitats at the same locale



(sampling station). For example, L. jocu is frequently found near mangrove prop-roots, occasional rock drop-offs and the slope that links the mangrove forest mudfloor to the bottom of the river channel while the two other species are not encoun-tered there (pers. obs.). Moreover, L. synagris was especially abundant in trawlscarried out over shallow algae-covered flats in open areas (unpubl. data), a featurethat corresponds to the bathymetric distribution of the species (and L. analis) in anearby estuary (Chagas et al., 2006). Extremely shallow areas (e.g. beaches), man-grove creeks and mangrove forest mud floor do not seem commonly visited by eitherspecies because the fishes Atherinidae, Eleotridae [e.g. Guavina guavina (Valenci-ennes) that lives in intertidal crab burrows], Hemiramphidae and Poeciliidae and thecrab Ucides cordatus (whose open burrows, as opposed to the closed burrows ofUca spp., are located in the intertidal area of the forest floor) and Aratus pisonis(that lives on mangrove prop-roots and trunks) were conspicuously absent from thestomachs analysed (Vergara-Filho et al., 1997; Vendell et al., 2003). Only L. jocuconsumed semi-terrestrial crabs (Grapsidae, Goniopsis sp. and Pachygrapsus sp.),which confirms the strong affinity of this species to the estuarine shores. Thus, abouttwo-thirds of the total surface area of the system (c. 12 km2 mangrove v. 5 km2 openwater; Barroso, 2004) may not be directly used by the snappers but, possibly, for afew metres into the mangrove fringe (Vance et al., 1996; Ronnback et al., 1999).

Three incidental observations shed some light on the opportunistic behaviour ofthese predators and illustrate some elaborate feeding habits. For example, hermitcrabs are apparently ingested without their gastropod shells (Randall, 1967; Duarte& García, 1999a; present study) indicating that fishes either suck the crab out of theshell or exclusively and opportunistically prey upon unshelled individuals. [Duarte& García (1999a) suggested that predated hermit crabs were in the moult stage.]The latter hypothesis is more probable because the snapper feeding apparatus is notappropriate for extraction by suction. Also, the presence of isolated (apparently auto-tomized) single and large crab claws in the stomachs of several L. jocu seems toindicate that these fish purposely consume parts of organisms that are too large tobe swallowed whole (i.e. sublethal predation on regenerable parts). Possibly, largerprey are easier to spot than small ones while providing a high food volume at amodest energetic cost. Finally, microgastropoda ingested by L. analis were probablyconsumed unintentionally during winnowing to capture larger infaunal prey (Muelleret al., 1994) such as the Polychaeta to which they were strongly associated. Win-nowing is unusual in snappers and remains unreported in L. jocu and L. synagris(Claro & Lindeman, 2008).

The taxon list (Table II) fits with those of Randall (1967), Rivera-Arriaga et al.(1996), Sierra & Popova (1997), Duarte & García (1999a, b) and Claro & Lindeman(2008). A number of food items previously cited for the central and north-westernAtlantic Ocean, such as algae, Asteroidea, Bivalvia, Bryozoa, Cephalopoda, Cope-poda, Nematoda, Ophiuroidea and Palinura, were not observed in the present study.Differences in diet observed between the present study and others are derived fromcomparing juveniles foraging in estuaries (present study) and adults foraging incoastal and coral reef areas. Juvenile snappers feed mainly on benthic and planktoniccrustaceans while coastal adults will mostly prey upon fishes or fishes and benthicinvertebrates (Claro & Lindeman, 2008).



S PAT I A L VA R I AT I O N O F D I E T

Overall, the three species consumed larger (i.e. Reptantia and Teleostei v. Per-acarida and Natantia) and more diverse prey in the PM than in the PA. One of severalpossible reasons for this difference would be that the diet composition closely reflectsthe local fauna (Duarte & García, 1999a, b). Under this hypothesis, faunistic vari-ations would be principally generated through differences in morphological (depthand habitat complexity) and water (turbidity, temperature and salinity) characteris-tics between estuaries. The PA actually has stronger estuarine characteristics (lowerdepth, higher turbidity and larger vertical and horizontal variations in salinity) thanthe PM, which is much less influenced by river inflow (Barroso, 2004). In support ofthe hypothesis, there are unpublished data on the fish community (n = 10 815 fishes;including the three snappers species) collected during the sampling programme thatindicate such faunistic differences between the two estuaries (R. M. Macieira, pers.comm.). In particular it appears that the PA has higher fish diversity (93 v. 78species), significantly higher total abundance (133 v. 59 individuals per 1000 m2)and biomass (2285 v. 1590 g per 1000 m2) and lower mean size (83 v. 90 mm LT)than the PM. Also, in species where significant differences in abundance (n = 13,including L. synagris) or biomass (n = 6) between estuaries exist, the higher valueof either variable is always found for the PA. These features are totally in agreementwith the observation by Vidy (2000) that estuaries are good nursery habitats if theyreceive sufficient, or adequate, freshwater inputs. The contrast between the PA andthe PM, with respect to salinity, ichthyofauna and snapper size, distribution or dietwould probably be higher in ‘normal’ La Nina years (Barroso, 2004) than under ElNino conditions (i.e. present study).

S E A S O NA L VA R I AT I O N O F D I E T

In L. analis, seasonal changes in the relative importance of food categories donot reflect ontogenetic shifts in diet. Therefore, in all three snapper species, seasonalvariation in diet is probably caused by the overlay of the opportunistic and generalistfeeding mode upon a seasonal oscillation in the abundance and availability of prey(Platell et al., 1997; Duarte & García, 1999a, b). The apparent absence of synchronywith an expected seasonal pattern of productivity of the environment (Pianka, 1974)may have resulted from the overall dryness of 2003, the sampling period directlyfollowing a very weak rainy season (2002 to 2003) and finishing during a rainyseason (2003 to 2004) that started 3 month later than usual.

D I E T OV E R L A P

High levels of diet overlap between coexistent fish species have been occasionallyreported (Sierra & Popova, 1997; Cocheret de la Moriniere et al., 2003) but this doesnot necessarily mean that competition for food occurs (Pianka, 1974; Cocheret de laMoriniere et al., 2003). Resources can be diverse and abundant enough as to permittheir sharing among species and thus to allow the coexistence of various species hav-ing a relatively similar diet. In the present study, however, interspecific differences insize, spatial distribution and microhabitat preferences probably are the main factorsresponsible for the low diet overlap, counterbalancing the enormous ecological sim-ilarity between these three congeneric and sympatric snapper species. Ontogenetic



changes towards larger preys as fishes grow (Platell et al., 1997; Cocheret de laMoriniere et al., 2003) also play a fundamental role to reduce inter and intraspecificcompetition. Overall, interspecific overlaps were of the same order of magnitudethat intraspecific overlaps between estuaries. The former, however, were extremelylow when estimated on a seasonal basis and such low overlap can be reinforced byseasonal or specific divergences in estuarine system use. For example, Chagas et al.(2006) demonstrated distinct abundance patterns between L. analis (most abundantduring the rainy season) and L. synagris (most abundant during the dry season) in theBaía de Vitoria that would reduce any given overlap to insignificance. In addition,in that same estuary L. jocu was, respectively, seven and 50 times less abundantoverall than L. analis and L. synagris. In such a situation, competition would beone-sided against the rarest species although the very exclusive microhabitat usedby L. jocu would considerably lower it. Therefore, the three species use estuaries asnursery habitat but food overlap between species is not biologically significant dueto a combination of interspecific differences in size, spatial distribution, differingmicrohabitat preferences and distinctive seasonal patterns of abundance and preychoice.

In estuaries, juvenile snappers suffer diverse anthropogenic effects of direct, indi-rect and competitive influence. Examples of such threats are artisanal, recreationaland professional fishing, change in community structure, habitat destruction or waterpollution and competition with humans for several food items (i.e. fisheries exploita-tion of shrimps, crabs and fishes) (Barroso, 2004). Isolated management of the adultstocks is surely insufficient to maintain their productivity since the biological andbehavioural characteristics of the snappers (e.g. slow growth rate, late sexual matu-rity, medium to high longevity and asymptotic sizes, low rates of natural mortalityand predictable spawning aggregations; Claro & Lindeman, 2008) confer to theirpopulations low rates of regeneration and productive capacity. The creation of largemarine protected areas covering these essential habitats and other critical environ-ments (e.g. rocky shores, tidepools, sand beaches, calcareous algae and coral reefs,algae and seagrass banks) is perhaps the best management and conservation strategyfor these species of great economic and ecological interest.

The study was funded through PACT – Projeto do Milenio – Uso e Apropriacao de Recur-sos Costeiros, Grupo Biodiversidade e Qualidade Ambiental financed by the Brazilian Min-istry of Science and Technology. The authors thank L. Neves, C. E. Stein, E. R. S. deAlmeida, K. Matuchack, L. P. Chagas, M. G. Moura and R. M. Macieira for assistance infield collections and laboratory analyses and the Brazilian National Council for Research(CNPq) for financial support.

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Diet and food partitioning between juveniles of mutton ... fileDiet of juvenile mutton Lutjanus...

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