Anda di halaman 1dari 14

Journal of Fish Biology (2004) 64, 970983 doi:10.1111/j.1095-8649.2004.00365.x, available online at http://www.blackwell-synergy.


Functional groups of lagoon fish species in Languedoc Roussillon, southern France

O. D U M A Y , P. S. T A R I , J. A. T O M A S I N I

D. M O U I L L O T *

Laboratoire Ecosyste`mes Lagunaires, UMR CNRS-UMII 5119, Universite Montpellier II Case 093, 34 095 MONTPELLIER Cedex 5, France (Received 5 April 2003, Accepted 10 January 2004)
Ten functional traits of fish species were related to habitat, diet or food acquisition, to propose a classification of 21 lagoon fishes into 10 functional groups. The selection of traits was based on their functional interest and the ease of measurement. Some groups were taxonomically related containing species belonging to the same genus, e.g. Syngnathus, Atherina or Pomatochistus. Species with a flat body shape constituted another group and three species (Anguilla anguilla, Gambusia affinis and Callionymus pusillus) formed individual groups. These results could be used to constitute functional units and to simplify such complex ecosystems and their # 2004 The Fisheries Society of the British Isles interactions. Key words: allometry; exotic species; functional traits; multivariate analysis.

INTRODUCTION A central aim of ecology is to measure biodiversity. It is not easy to capture this measure as a single number (Chapin et al., 2000; Purvis & Hector, 2000). Numerous facets of biodiversity have been already quantified using specific richness or evenness, taxonomic and phylogenetic indices (Simpson, 1949; Alatalo, 1981; Bulla, 1994; Warwick & Clarke, 1995; Smith & Wilson, 1996; Hill, 1997; Clarke & Warwick, 2001). Nevertheless, the most important question is not whether a proposed statistic satisfies some theoretical criterion, but whether it allows meaningful inquiries about ecosystem functioning or environmental factors. It is now generally accepted that functional diversity, which is the value and range of functional traits of the organisms present in a given ecosystem (Diaz & Cabido, 2001), rather than species diversity per se, is the key (Grime, 1997; Tilman et al., 1997; Chapin et al., 2000; Diaz & Cabido, 2001; Naeem, 2002a, b; Naeem & Wright, 2003). Species richness is practically always used as an explanatory variable for ecosystem function because it is easy to estimate and assumed to be a good estimator for functional diversity (Lawton et al., 1998; Tilman, 1999). Nevertheless, Diaz & Cabido (2001) theoretically showed that species richness (species number per se) will only be an adequate surrogate for functional diversity if there is a linear increase in niche space coverage as species richness
*Author to whom correspondence should be addressed. Tel.: 33 4 67 14 39 26; fax: 33 4 67 14 37 19; email:


2004 The Fisheries Society of the British Isles



Functional diversity

Increasing functional redundancy in fish assemblage

Species richness
FIG. 1. Relation between functional diversity and species richness in fish assemblages. When functional redundancy or similarity increases in a fish community, functional diversity increases at a slower rate than species richness whereas this relation is linear when species are functionally different. Thus, species richness is a good surrogate for functional diversity if new species add new functions or new functional groups.

increases. For Petchey & Gaston (2002), functional diversity could be strongly related to richness only if species traits were equally complementary. These two assumptions are summarized in Fig. 1 with different fish assemblages containing more or less functionally redundant or similar species. When species are added with similar functions in an ecosytem, functional diversity is not linearly related to richness and thus increases at a lower rate than richness. Indeed, many authors argue that functional diversity rather than species richness determines ecosystem functioning and must be estimated (Grime, 1997; Tilman et al., 1997; Chapin et al., 2000; Diaz & Cabido, 2001; Naeem, 2002a, b). The introduction of functional groups was an important step in estimating functional diversity, with species being grouped by similar function, similar effects on ecosystem processes or similar responses to environmental pressures (Diaz & Cabido, 1997; Lavorel et al., 1997, 1999; Walker et al., 1999; Wilson, 1999; Walker & Langridge, 2002). These functional groups or types have been used to investigate the influence of climatic change (Diaz & Cabido, 1997) or species loss (Fonseca & Ganade, 2001; Naeem, 2002b) on ecosystem processes. In functional ecology, classifying species into groups based on similar function is a useful approach to studying assembly or coexistence rules, trophic interactions, species redundancy or similarity and environmental or perturbation influences on the system. Worldwide, lagoon systems represent 13% of the coastline (Knoppers, 1994) and together with other coastal ecosystems contribute a large part of the ecological richness of the biosphere (Costanza et al., 1997). Due to their location between the continent and the sea and their shallow depths, lagoons are among the most productive ecosystems (on average 300 g C m2 year1, Knoppers, 1994) but also very sensitive to both climatic and human impacts. In the Languedoc-Roussillon region (southern France, Mediterranean Sea), lagoons comprise 50% of the coastline. They

2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983



are subject to many human impacts, in particular aquaculture, tourist activities and agriculture in the watershed. For instance, in Languedoc-Roussillon, some lagoons are used intensively for aquaculture (20% of the Thau Lagoon area) (Bacher et al., 1997; Fiandrino et al., 2003). It is important to study the impact of these activities on the different biotic components of the lagoon ecosystem and on the different ecosystem processes, i.e. productivity, stability and resilience (Chapin et al., 1997; Tilman et al., 1997; Loreau, 2000; Loreau et al., 2001; Bond & Chase, 2002). Numerous studies have highlighted the influence of fish communities on ecosystem processes (Angeler et al., 2002; Baldo & Drake, 2002; Carrasson & Cartes, 2002; Davoren et al., 2002; Mancinelli et al., 2002) but these communities remain complex systems with respect to functions and interactions. To simplify these systems or ecological compartments, functionally homogenous units are needed (Simberloff & Dayan, 1991; Austen et al., 1994; Garrison & Link, 2000). Thus the aim of the present study was to propose functional groups for the fish community of the Languedoc-Roussillon lagoons, based on functional traits which were related to diet, habitat or food acquisition methods (Keast & Webb, 1966; Goulding, 1985; Grossman, 1986; Motta et al., 1995; Norton, 1995; Piet, 1998). The limits of this method, its ecological interest and the relation to the guild concept were also investigated.


Fishes were caught in four coastal brackish lagoons of southern France: Thau (43 240 N; 3 360 E), Mauguio (43 340 2800 N; 4 030 0000 E), Saint-Nazaire (42 400 3900 N; 3 000 2400 E) and Salses-Leucate (42 500 4300 N; 2 590 4300 E) lagoons. These lagoons are very different in their characteristics (e.g. surface, topography, depth, salinity and human impact level). Many fish species inhabit these water bodies. For instance, 72 species were recorded in the Mauguio Lagoon, 20 were common and the others rare or very rare (unpubl. data). In order to obtain the best possible representation of the fish community of the lagoons, an active capture method, such as a drawnet, rather than a passive one such de lec, 1991; as capetchade or trammel net seemed more appropriate (George & Ne Harrison & Whitfield, 1995). With a passive method there are always selectivity problems, i.e. some species are more easily caught than others and thus the sampled community can be biased. In addition, as the drawnet covers the entire water column from the bottom to the surface, both pelagic and benthic species were captured.

The definition of functional groups and the classification of species must be done carefully. The selection of which functions are of interest, which traits can be measured as an index of these functions and the multivariate analysis chosen to classify species into these groups all influence the final result. Following Fonseca & Ganade (2001), building functional groups involved the following five main steps.

Defining functional groups

Functional groups can be seen under different facets, depending on whether groups are defined as a set of species exhibiting a similar response to environmental conditions or have similar effects on the dominant ecosystem processes (Blondel, 2003). Here, the
2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983



principal aim was not to measure a response of the community to disturbances such as global change or human impact but to define groups of species acting in the same way in the system.

Species inclusion criteria

Many kinds of communities (e.g. macrophytes, plankton and bacteria) within the lagoon, are all potentially of interest. In this study the fish component was focused on.

Selecting the functions of interest

To define functional groups of fish species based on their influence on the system three functions of interest were selected: diet (e.g. herbivore or carnivore), habitat (e.g. pelagic or benthic) and method of food acquisition.

Choosing the traits

It is necessary to select the traits which reflect the functions of interest but which are still possible to measure on a large number of individuals in a short time. Among all morphological characters available on fish species, those offering a trade-off between their relevant interest and ease of measurement were chosen. Most of the functional traits were relevant for several functions of interest but some others could be associated with diet, habitat and the food acquisition method. Following these criteria, 10 functional traits were selected (Fig. 2): (i) mass (M) was the first trait to be estimated because body size is related to the amount of food intake by individuals and to their impact on the food web (Greenwood et al., 1996; Niklas & Enquist, 2001). In addition, this variable is used to standardize other variables. Mass was measured on each individual with a precision balance; (ii) ratio of standard length

Pos Og pL pd horizontal Bd cd

45 +1 10 0 10 0 1

90 +2 Pro

LS dGr Horiz.

2 45 90

FIG. 2. Different functional traits measured on lagoon fishes including the different classes of the oral gape position (from Sibbing & Nagelkerke, 2001). LS, standard length; Bd, body depth (trait LS : Bd); D, eye diameter; Og, oral gape; Pro, protrusion length; Pos, oral gape position; dGr, gill raker depth; cL, caudal fin length; cd, caudal fin depth (trait cL : cd); pL, pectoral fin length; pd, pectoral fin depth (trait pL : pd).

2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983



(LS) to body depth (Bd; LS : Bd), which is related to the hydrodynamic ability of fish species (Sibbing & Nagelkerke, 2001); (iii) ratio between length (pL) and depth (pd) of the pectoral fin, pectoral fin aspect ratio (pL : pd), which is strongly correlated to swimming performance for labrid species (Walker & Westneat, 2000; Bellwood & Wainwright, 2001; Bellwood et al., 2002; Wainwright et al., 2002). More generally, it appears to be related to manoeuvrability at slow speeds and efficiency of locomotion (Bellwood et al., 2002); (iv) aspect of ratio caudal fin length (cL) to caudal fin depth (cd; cL : cd) decreases as the swimming ability of the fish declines (Sibbing & Nagelkerke, 2001). Benthic fishes tend to have a high ratio whereas high-speed fishes have a low ratio; (v) eye diameter (D) is related to the detection of food and gives information about the visual acuity of the species (Piet, 1998). Hunting fishes need efficient visual acuity; (vi) oral gape position (Pos) is the angle of the oral gap with the body line, giving information about capture mode or benthic character (Sibbing & Nagelkerke, 2001). Five classes were defined (Fig. 2): 10 to 10 ; 1 for 10 to 45 and 2 for 45 to 90 ; (vii) protrusion length (Pro) allows a reduction of the distance between the fishes and their prey to limit energetic cost (Sibbing & Nagelkerke, 2001). An ambush mode of prey capture or a digger activity is usually linked to this protrusion; (viii) gill raker depth (dGr) is high when food acquisition is by filtration which is related to a planktonic diet (Sibbing & Nagelkerke, 2001); (ix) oral gape (Og) is directly related to the maximal size of the prey and influences the impact of the fish on the food web (Sibbing & Nagelkerke, 2001); (x) gut length (GuL) is strongly related to fishs diet (Kramer & Bryant, 1995, Elliott & Bellwood, 2003). The ratio of GuL to LS is between 07 and 10 in carnivorous fishes and >1 in herbivorous fishes. Because of size differences, fish species traits were standardized (Adite & Winemiller, 1997; Winemiller, 1991). The choice was to standardize biomass because recent studies have highlighted the robust relationship between morphological or metabolic rates and body mass (West et al., 1997; Enquist & Niklas, 2001; Niklas & Enquist, 2001). The exception to this was gut length which was standardized by LS (Kramer & Bryant, 1995; Cleveland & Montgomery, 2003). If the allometric relationship between a trait (X) and mass (M) is X aMb and the exponent coefficient is invariant between scales or species, [ln(X 1)][ln(M 1)]1 could be expected to be constant or robust for the same population. So, this transformation was choosen.

Building a classification
Factorial discriminant analysis (FDA) was used to extract variables (functional traits) discriminating fish species. FDA was applied to the original data set: a rectangular matrix crossing fish individuals and functional traits. This analysis is based on linear models such as multiple linear regression to seek linear combinations of variables (here functional traits) that best discriminate among the groups (fish species) (Legendre & Legendre, 1998). The factorial form of this analysis is able to provide factorial axes with inertia defining planes where individuals and species are distributed. When all individuals are perfectly represented by a factorial axis, its inertia is 100%. Thereafter, a cluster analysis based on Euclidean distance and the Ward linkage method was used to build functional groups of fish species. This distance was the best cut-off distance to distinguish 10 relevant functional groups. These analyses were computed with ADE-4 (v 2001) and PC Ord (Mc Cune & Mefford, 1999).


In the four studied lagoons, 21 fish species, from 17 genera, were collected (Table I). All these species were not present in every lagoon; some were temporarily absent and others non-existent. As the common goby Pomatoschistus microps (Kryer), the marbled goby Pomatoschistus marmoratus (Risso) and the

2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983

TABLE I. Mean S.E. of the different functional variables for each lagoon fish species. n, number of individuals measured; M, mass; LS, standard length; Bd, body depth; D, eye diameter; Og, oral gape; Pro, protrusion length; Pos, oral gape position; dGr, gill raker depth; GuL, gut length; cL : cd, aspect of ratio caudal fin (length to depth), pL : pd, ratio between length and depth of pectoral fin or pectoral fin aspect ratio LS (mm) Pro (mm)
00 29 09 52 08 20 38 06 30 00 20 40 19 05 19 09 38 06 13 07 18 05 08 07 00 13 09 25 40 21 05 00 00 00 00 10 20 00 00 10 10 00 10 00 10 20 10 00 20 00 09 05 10 00 20 00 20 03 00 10 00 00 05 08 20 00 20 00 01 1160 20 06 358 31 32 06 496 26 01 660 22 06 3550 53 30 04 543 20 11 750 32 690 14 07 144 18 06 05 728 39 22 04 2972 71 00 00 180 20 00 00 523 43 01 04 306 31 00 400 16 09 2383 66 34 1180 00 2700 12 05 805 37 00 00 286 28 00 00 354 27


2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983

160 107 17 118 11 80 230 12 160 00 340 250 56 11 138 15 175 11 53 05 77 14 75 12 170 303 18 90 120 375 17 34 08 31 07 40 50 09 57 06 15 63 06 60 00 70 50 20 06 51 08 56 06 20 00 37 08 37 08 30 74 08 70 60 91 05 20 05 21 06 45 67 12 75 09 50 73 06 80 00 60 100 24 08 89 12 58 08 30 06 63 11 58 12 30 59 09 160 50 48 05 18 06 24 08

Species code n Pos

M (g)

Bd (mm)

D (mm)

Og (mm)

dGr (mm)

GuL (mm)

cL : cd
05 11 05 11 04 20 16 03 13 03 07 14 15 04 20 06 11 04 25 00 23 06 17 06 12 08 03 11 14 09 03 20 08 24 09

pL : pd
14 22 07 20 05 15 24 08 26 04 24 19 19 04 23 08 24 07 34 09 26 04 19 06 23 21 04 21 25 32 07 13 05 11 05

Anguilla anguilla Atherina boyeri Atherina hepsetus Callionymus pusillus Chelon labrosus Dicentrarchus labrax Diplodus sargus Echiichthys vipera Gambusia affinis Gobus niger Liza aurata Pomatochistus microps Pomatochistus minutus Pomatoschistus sp. Salaria pavo Sarpa salpa Scophthalmus rhombus Solea solea Sparus aurata Syngnathus abaster Syngnathus typhle

Aan Abo Ahe Cpu Cla Dla Dsa Evi Gaf Gni Lau Pmc Pmn Psp Spa Ssa Srh Sso Sau Sab Sty

1 42 19 1 2 3 1 1 4 4 25 4 3 69 1 7 1 1 4 55 16

310 2650 31 13 627 35 51 12 794 28 32 550 148 10 925 08 45 06 650 14 118 650 193 1010 04 04 255 18 69 16 645 29 102 13 907 22 04 02 296 07 18 09 490 25 16 08 467 26 59 700 188 26 899 33 466 1240 566 1580 265 26 1020 29 04 04 928 36 05 05 1036 36




(b) Cpu Sso Srh Ahe Spa Sty Sab Pmc Aan Sau Dla Lau Cla Ssa Gaf Pos D* cL : cd Og* cd* GuL* dGr* Pro pL : pd LS : Bd 1 1 1 -1 1 -1

Dsa Pmn Psp Gni Abo Evi

FIG. 3. Factorial discriminant analysis with the first two axes (total inertia of 69%) (a) for species and (b) for the variables (*, standardized). See Table I for abbreviations.

sand goby Pomatoschistus minutus (Pallas) could not be easily distinguished, they were combined as Pomatoschistus sp. Only four P. microps and three P. minutus specimens, from Mauguio Lagoon, were determined by staining canals, pores and papillae (Sanzo, 1911) by the Iljin method (Iljin, 1930). The FDA discriminated fish species based on functional traits. The first three axes represented 82% of the total inertia (Figs 3 and 4). Axis 1 clearly contrasted the black-striped pipefish Syngnathus abaster Risso and the broad-nosed pipefish Syngnathus typhle L. with the other fish species. The Syngnathus group had high values for the standard length to body depth ratio, caudal fin length to depth ratio, eye diameter and oral gape, oral gape position >45 , and low


Sty Sab

Cpu (b) Cla Spa Ssa Psp Lau Dsa Sau Gni Srh Aan Evi Ahe Dla cL : cd Abo Pmc Sso Pmn Pos LS : Bd Og* D* cd*

1 -1 1 1 1 -1

GuL* pL : pd

Pro* Gaf dGr*

FIG. 4. Factorial discriminant analysis with the first and the third axes (total inertia of 53%) (a) for species and (b) for the variables (*, standardized). See Table I for abbreviations.

2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983


Ward distance

All depths



Atherina hepsetus Dicentrarchus labrax Atherina boyeri Echiichthys vipera Gobus niger Pomatoschistus sp.






Carnivorous/Planctonophagous Filtration/Hunting

Benthic episubstratum Carnivorous (medium prey)


Benthic episubstratum Carnivororous (small prey)


3 Pomatoschistus minutus
Pomatoschistus microps Sarpa salpa

All depths



4 5 6

Liza aurata Chelon labrosus Anguilla anguilla Diplodus sargus Sparus aurata Solea solea

Benthic All depths

Carnivorous Carnivorous

Hunting Hunting




7 Scophthalmus rhombus
Salaria pavo

Benthic Benthic Benthic episubstratum

Carnivorous Planctonophagous Omnivorous

Digger Gulping

8 9

Callionymus pusillus Syngnathus abaster Syngnathus typhle Gambusia affinis

Filtration/Gulping 10

FIG. 5. Dendrogram from cluster analysis showing the habitat, diet and mode of capture similarities between the different functional group of fishes from 1 to 10.

values in pectoral fin length to depth ratio, gut length and protrusion. Axis 2 divided species into two opposite groupings. One group, with the sand smelt Atherina boyeri Risso, the lesser weever Echiichthys vipera (Cuvier) and the gobies Pomatoschistus sp., P. minutus and the black goby Gobius niger L., displayed an oral gape axis >45 while this variable was between 10 and 45 in the group with the sand smelt Atherina hepsetus L., the peacock blenny Salaria pavo (Risso) and the common sole Solea solea (L.) and the brill Scophthalmus rhombus (L.). Axis 3 highlighted the special position of the mosquitofish Gambusia affinis (Baird & Girard). This species had high gill raker depth and protusion values. The same tendency was observed for A. boyeri, A. hepsetus and the European sea bass Dicentrarchus labrax (L.), unlike the gobies and Syngnathus group. To propose functional groups of fish species, a cluster analysis was computed (Fig. 5). A Ward distance of 10 was chosen to discriminate 10 functional groups. Three functional groups had only one species each [group 5: the European eel Anguilla anguilla (L.); group 8: Callionymus pusillus Delaroche; group 10: G. affinis]. Two groups contained only co-generic species (group 3: three Pomatoschistus; group 9: two Syngnathus). Group 6 included two sparidae [the gilthead sea bream Sparus aurata L. and the white sea bream Diplodus sargus (L.)] and group 1 two species of the Atherina genus plus D. labrax. Species with a flat body shape were in the same group 7. Groups 2 and 4 included various species taxonomically unrelated. DISCUSSION This study aimed to test the possibility of using multivariate analyses to separate functional groups based on morphological and anatomical traits in

2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983



fishes. It allowed discrimination of 10 coherent groups based on diet, habitat and food capture abilities. To characterize each group, one main reference (UNESCO, 1986) and the results from Figs 3 and 4 and the data of Table I were used. Some functional traits are common among some groups discriminated by cluster analysis, but each group is characterized by its own and unique combination of traits. Groups 1, 4 and 6 are composed of fish species swimming at all depths. Species from group 1 tend to move far from the bottom and their body shape is more fusiform than fish species from groups 4 and 6 which tend to move nearer the bottom; the standard length to body depth ratio values are higher in the first group than in the other two groups. Fish species (from the Sparidae and Mugilidae) of these two groups (4 and 6) have high pectoral fin aspect ratios, and they are well adapted for manoeuvring between rocks or in dense beds of aquatic plants. Species from groups 1 and 6 are mainly carnivorous, but can eat plants (Rosecchi, 1985) while those of group 6 are omnivorous or herbivorous. The relative size of the gut is often indicative of diet in fishes (Kramer & Bryant, 1995). The gut length to LS ratio values are higher in group 4 than in groups 1 and 6. In group 1, Atherina sp. and juveniles D. labrax eat planktonic food by quert, 1973; Aprahamian filtration and small bottom-living prey (Labourg & Ste & Barr, 1985; Trabelsi et al., 1994; Laffaille et al., 2000). These species show high gill raker depth for filtration and large protrusion length to ingest small prey. A protrusible mouth increases their prey capture ability and efficiency (Helfman et al., 1997). In group 6 species, the mouth is small with flat (D. sargus) or conical (S. aurata) teeth in front to catch and molar-like teeth laterally to crush prey. With the exception of the special case of G. affinis, functional groups 2, 3, 5, 7 and 8 include more or less bottom-living, mainly carnivorous, species. Groups 2 and 3 are close, so in both of them, fishes display an oral gape axis 45 . It can be noticed that G. niger is more linked to E. vipera than to Pomatoschistus sp. Indeed, G. niger and E. vipera show larger body size, protrusion and oral gape than Pomatoschistus sp. The prey spectrum of G. niger and E. vipera is greater than Pomatoschistus sp., the two first species can feed on larger prey such as small fishes (Joyeux et al., 1991). Salaria pavo and the flatfishes are surprisingly placed in the same group (7) and the next group (8) consists of C. pusillus. The species in these two groups display several traits in common: small protrusion and oral gape, and oral gape axis between 45 and 10 . Group 5 consists only of A. anguilla. Body morphology of this carnivorous bottom-living species is particularly well adapted for entering holes, swimming through aquatic plant beds and burrowing into soft bottoms. The Syngnathidae, group (9), stands far apart from the other groups in FDA (Figs 3 and 4) because of the unusual pipefish characteristics. Their colouration and their long and slender body shape mimic aquatic plants among which they live. They did not show protrusion, but their tubelike mouth allows them to ingest tiny prey from some distance, which may compensate for their slow swimming, and the large size of their eyes is well adapted to precisely locate small prey. Gambusia affinis is also clearly separated from the other groups (Fig. 5). It is an exotic species, native in U.S.A. and Mexico but introduced into many

2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983



countries (Courtenay & Meffe, 1989) as a biological control agent for mosquitoes. This species cannot be defined as a bottom-living fish. Typically, it lives close to shore in calm shallow waters, among subsurface vegetation (Hubbs, 1971; Miura et al., 1979; Arthington et al., 1986). This aggressive fish is an opportunistic omnivore feeding on a large range of prey, from plankton, strained by long and closely spaced gill rakers, to small fishes and amphibian larvae (Harrington & Harrington, 1961; Farley, 1980; Walter & Legner, 1980; Bence & Murdoch, 1982; Bence, 1986; Morton et al., 1988). Gambusia affinis morphology is well suited to capture prey from the water surface or in the water column (Moyle & Cech, 1988): the flattened head with an upward-pointing mouth has a large protrusion to ingest prey and the dorsal fin in a posterior position. In this study, the aim was not to examine all functional traits of lagoon fish species. The choice was driven by their relevant interest and the easiness of their estimation (about 1015 min are required to measure all the variables for each individual). This study is in the context of diversity-ecosystem function. Lagoons in Languedoc-Roussillon are highly impacted by humans. The fish component is an important part to study in the functional processes in coastal ecosystems (Mathieson et al., 2000; Angeler et al., 2002; Baldo & Drake, 2002). Before investigations can be undertaken about the influence of the functional diversity of the fish community on lagoon stability, productivity or resilience, the first step was to classify these fish species into functional groups. Many studies have highlighted the complexity of ecological systems and their fundamental unpredictability due to multiple interactions (Huisman & Weissing, 2001). One way to overcome this problem is certainly a simplification of communities through a partitioning of species into a variety of guilds, functional groups or functional types (Simberloff & Dayan, 1991; Mathieson et al., 2000; Blondel, 2003; Jauffret & Lavorel, 2003). If the guild concept has been more often used than functional groups for vertebrates, it refers more to the mechanisms of resource sharing by species in a competitive context. Within the context of biodiversity and ecosystem functions, a wide range of ecosystem functions from the fishes are required and the functional groups seem more appropriate than the guilds. For example, the gill raker depth is directly linked to a resource use (plankton) and thus to the guild concept whereas the swimming abilities (fin variables) are more related to the place in the water column, habitat and capture modes and thus to functional groups. These two concepts are sometimes used synonymously and clarification is needed (Simberloff & Dayan, 1991; Blondel, 2003). The variables proposed in the study are not complete to speculate about fish compartment functioning in lagoon ecosystems and data on reproduction modes, abundances and migratory behaviour and more generally life-history traits are required. Moreover, for seven of the 21 species the various traits are measured in one specimen per species, so these functional groups are far from being a final classification of lagoon fishes within different ecological functional groups.
We wish to thank B.J. Anderson and J.F. Craig, the Editor, for improving this manuscript and for English corrections. Two anonymous reviewers provided helpful comments. This work was supported by the grant 002420 from University of Montpellier II on functional diversity of lagoon fish species.

2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983



Adite, A. & Winemiller, K. O. (1997). Trophic ecology and ecomorphology of fish assemblages in coastal lakes of Benin, West Africa. Ecoscience 4, 623. Alatalo, R. V. (1981). Problems in the measurement of evenness in ecology. Oikos 37, 199204. Angeler, D. G., Rodrigo, M. A., Sanchez-Carrillo, S. & Alvarez-Cobelas, M. (2002). Effects of hydrologically confined fish on bacterioplankton and autotrophic picoplankton in a semiarid marsh. Aquatic Microbial Ecology 29, 307312. Aprahamian, M. W. & Barr, C. D. (1985). The growth, abundance and diet of 0-group sea bass, Dicentrarchus labrax, from the Severn Estuary. Journal of the Marine Biological Association of the United Kingdom 65, 169180. Arthington, A. H., McKay, R. J. & Milton, D. A. (1986). The ecology and management of exotic and endemic freshwater fish in Queensland. In Fisheries Management: Theory and Practice in Queensland (Hundloe, T. J. A., ed.), pp. 224245. Brisbane: Griffith University Press. Austen, D. J., Bayley, P. B. & Menzel, B. W. (1994). Importance of the guild concept to fisheries research and management. Fisheries 19, 1220. Bacher, C., Millet, B. & Vaquer, A. (1997). Modelling the impact of cultivated filter-feeders on phytoplanktonic biomass of the Thau Lagoon (France). Comptes Rendus de lAcademie des Sciences 320, 7381. Baldo, F. & Drake, P. (2002). A multivariate approach to the feeding habits of small fish in the Guadalquivir Estuary. Journal of Fish Biology 61 (Suppl. A), 2132. Bellwood, D. R. & Wainwright, P. C. (2001). Locomotion in labrid fishes: implications for habitat use and cross-shelf biogeography on the Great Barrier Reef. Coral Reefs 20, 139150. Bellwood, D. R., Wainwright, P. C., Fulton, C. J. & Hoey, A. (2002). Assembly rules and functional groups at global biogeographical scales. Functional Ecology 16, 557562. Bence, J. R. (1986). Feeding rate and attack specialization: the role of predator experience and energetic trade-offs. Environmental Biology of Fishes 16, 113121. Bence, J. R. & Murdoch, W. W. (1982). Ecological studies of insect predators and Gambusiain rice field : a preliminary report. Proceedings of the California Mosquito and Vector Control Association 50, 4850. Blondel, J. (2003). Guilds or functional groups: does it matter? Oikos 100, 223231. Bond, E. M. & Chase, J. M. (2002). Biodiversity and ecosystem functioning at local and regional spatial scales. Ecology Letters 5, 467470. Bulla, L. (1994). An index of evenness and its associated diversity measure. Oikos 70, 167171. Carrasson, M. & Cartes, J. E. (2002). Trophic relationships in a Mediterranean deep-sea fish community: partition of food resources, dietary overlap and connections within the benthic boundary layer. Marine Ecology Progress Series 241, 4155. Chapin, F. S., Walker, B. H., Hobbs, R. J., Hooper, D. U., Lawton, J. H., Sala, O. E. & Tilman, D. (1997). Biotic control over the functioning of ecosystems. Science 277, 500504. Chapin, F. S., Zavaleta, E. S., Eviner, V. T., Naylor, R. L., Vitousek, P. M., Reynolds, H. L., Hooper, D. U., Lavorel, S., Sala, O. E., Hobbie, S. E., Mack, M. C. & Diaz, S. (2000). Consequences of changing biodiversity. Nature 405, 234242. Clarke, K. R. & Warwick, R. M. (2001). A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Marine Ecology Progress Series 216, 265278. Cleveland, A. & Montgomey, W. L. (2003). Gut characteristics and assimilation efficiencies in two species of herbivorous damselfishes (Pomacentridae: Stegastes dorsopunicans and S. planifrons). Marine Biology 142, 3544. Costanza, R., Darge, R., Degroot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., Oneill, R. V., Paruelo, J., Raskin, R. G., Sutton, P. & Vandenbelt, M. (1997). The value of the worlds ecosystem services and natural capital. Nature 387, 253260.

2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983



Courtenay, W. R. & Meffe, G. K. (1989). Small fishes in strange places: a review of introduced poeciliids. In Ecology and Evolution of Livebearing Fishes (Poeciliidae) (Meffe, G. K. & Nelson, F. F., Jr, eds), pp. 319331. New Jersey: Prentice Hall. Davoren, G. K., Montevecchi, W. A. & Anderson, J. T. (2002). Scale-dependent associations of predators and prey: constraints imposed by flightlessness of common murres. Marine Ecology Progress Series 245, 259272. Diaz, S. & Cabido, M. (1997). Plant functional types and ecosystem function in relation to global change. Journal of Vegetation Science 8, 463474. Diaz, S. & Cabido, M. (2001). Vive la difference: plant functional diversity matters to ecosystem processes. Trends in Ecology and Evolution 16, 646655. Elliott, J. P. & Bellwood, D. R. (2003). Alimentary tract morphology and diet in three coral reef fish families. Journal of Fish Biology 63, 15981609. Enquist, B. J. & Niklas, K. J. (2001). Invariant scaling relations across tree-dominated communities. Nature 410, 655660. Farley, D. G. (1980). Prey selection by the mosquito fish, Gambusia affinis, in Fresno County rice field. Proceedings of the California Mosquito and Vector Control Association 45, 8794. Fiandrino, A., Martin, Y., Got, P., Bonnefont, J. L. & Troussellier, M. (2003). Bacterial contamination of Mediterranean coastal sea water as affected by riverine inputs: simulation approach applied to a shellfish breeding area (Thau Lagoon, France). Water Research 37, 17111722. Fonseca, C. R. & Ganade, G. (2001). Species functional redundancy, random extinctions and the stability of ecosystems. Journal of Ecology 89, 118125. Garrison, L. P. & Link, J. S. (2000). Dietary guild structure of the fish community in the North-east United States continental shelf ecosystem. Marine Ecology Progress Series 202, 231240. de lec, C. (1991). Dictionnaire des engins de peche. Rennes: IFREMER George, J. P. & Ne (Ouest-France). Goulding, M. (1985). Forest fishes of the Amazon. In Key Environments of Amazonia (Prance, G. T. & Lovejoy, T. E., eds), pp. 267276. New York: Pergamon Press. Greenwood, J. J. D., Gregory, R. D., Harris, S., Morris, P. A. & Yalden, D. W. (1996). Relations between abundance, body size and species number in British birds and mammals. Philosophical Transactions of the Royal Society of London Series B 351, 265278. Grime, J. P. (1997). Biodiversity and ecosystem function: the debate deepens. Science 277, 12601261. Grossman, G. D. (1986). Food resource partitioning in a rocky intertidal fish assemblage. Journal of Zoology, London 1, 317355. Harrington, R. W., Jr & Harrington, E. S. (1961). Food selection among fishes invading a high subtropical saltmarsh : from onset of floading trough the progress of mosquito brood. Ecology 42, 646666. Harrison, T. D. & Whitfield, A. K. (1995). Fish community structure in three temporarily open/closed estuaries on the natal coast. Ichthyological Bulletin of the J. L. B. Smith Institute of Ichthyology 64, 180. Helfman, G. S., Colette, B. B. & Facey, D. E. (1997). The Diversity of Fishes. Oxford: Blackwell Science. Hill, M. O. (1997). An evenness statistic based on the abundance-weighted variance of species proportions. Oikos 79, 413416. Hubbs, C. (1971). Competition and isolation mechanism in the Gambusia affinis Gambusia heterochir hybrid swarm. Bulletin of the Texas Memorial Museum 19, 146. Huisman, J. & Weissing, F. J. (2001). Fundamental unpredictability in multispecies competition. The American Naturalist 157, 488494. ` me des gobiide s. Instituo Espanol de Oceanografia, Trabajos 2, Iljin, B. S. (1930). Le syste 163. Jauffret, S. & Lavorel, S. (2003). Are plant functional types relevant to describe degradation in arid, southern Tunisian steppes? Journal of Vegetation Science 14, 399408.
2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983



gime alimentaire de Gobius Joyeux, J. C., Tomasini, J. A. & Bouchereau, J. L. (1991). Le re , 1758 (Teleostei, Gobiidae) dans la lagune de Mauguio France. niger Linne Annales des Sciences Naturelles, Zoologie 12, 5769. Keast, A. & Webb, D. (1966). Mouth and body form relative to feeding ecology in the fish fauna of a small lake, Lake Opinicon, Ontario. Journal of the Fisheries Research Board of Canada 23, 18451874. Knoppers, B. (1994). Aquatic primary production in coastal lagoons. In Coastal Lagoon Processes (Kjerfve, B., ed.), pp. 243286. Amsterdam: Elsevier Science. Kramer, D. L. & Bryant, M. J. (1995). Intestine length in the fishes of a tropical stream : 2. Relationships to diet the long and short of a convoluted issue. Environmental Biology of Fishes 42, 129141. gime alimentaire du bar Dicentrarchus labrax L. Labourg, P. J. & Stequert, B. (1973). Re servoirs a ` poissons de la re gion dArcachon. Bulletin dEcologie 4, 187194. des re Laffaille, P., Lefeuvre, J. C. & Feunteun, E. (2000). Impact of sheep grazing on juvenile sea bass, Dicentarchus labrax, in tidal salt marshes. Biological Conservation 96, 271277. Lavorel, S., McIntyre, S., Landsberg, J. & Forbes, T. D. A. (1997). Plant functional classifications: from general groups to specific groups based on response to disturbance. Trends in Ecology & Evolution 12, 474478. Lavorel, S., Rochette, C. & Lebreton, J. D. (1999). Functional groups for response to disturbance in Mediterranean old fields. Oikos 84, 480498. Lawton, J. H., Naeem, S., Thompson, L. J., Hector, A. & Crawley, M. J. (1998). Biodiversity and ecosystem function: getting the Ecotron experiment in its correct context. Functional Ecology 12, 848852. Legendre, P. & Legendre, L. (1998). Numerical Ecology. Amsterdam: Elsevier. Loreau, M. (2000). Biodiversity and ecosystem functioning: recent theoretical advances. Oikos 91, 317. Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J. P., Hector, A., Hooper, D. U., Huston, M. A., Raffaelli, D., Schmid, B., Tilman, D. & Wardle, D. A. (2001). Ecology Biodiversity and ecosystem functioning: Current knowledge and future challenges. Science 294, 804808. Mancinelli, G., Costantini, M. L. & Rossi, L. (2002). Cascading effects of predatory fish exclusion on the detritus-based food web of a lake littoral zone (Lake Vico, central Italy). Oecologia 133, 402411. Mathieson, S., Cattrijsse, A., Costa, M. J., Drake, P., Elliott, M., Gardner, J. & Marchand, J. (2000). Fish assemblages of European tidal marshes: a comparison based on species, families and functional guilds. Marine Ecology Progress Series 204, 225242. McCune, B. & Mefford, M. J. (1999). PC-ORD. Multivariate Analysis of Ecological Data, Version 4. Gleneden Beach, Oregon: MjM Software Design. Miura, T., Takahashi, R. M. & Wilder, W. H. (1979). Habitat and food selection by the mosquitofish, Gambusia affinis. Proceedings of the California Mosquito and Vector Control Association 47, 4650. Morton, R. M., Beumer, J. P. & Pollock, B. R. (1988). Fishes of a subtropical Australian saltmarsh and their predation on mosquitoes. Environmental Biology of Fishes 21, 185194. Motta, P. J., Clifton, K. B., Hernandez, P. & Eggold, B. T. (1995). Ecomorphological correlates in ten species of subtropical sea grass fishes : diet and microhabitat utilization. Environmental Biology of Fishes 44, 3760. Moyle, P. B. & Cech, J. J., Jr (1988). Fishes: An Introduction to Ichthyology. New Jersey: Prentice Hall. Naeem, S. (2002a). Disentangling the impacts of diversity on ecosystem functioning in combinatorial experiments. Ecology 83, 29252935. Naeem, S. (2002b). Ecosystem consequences of biodiversity loss: The evolution of a paradigm. Ecology 83, 15371552. Naeem, S. & Wright, J. P. (2003). Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecology Letters 6, 567579.
2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983



Niklas, K. J. & Enquist, B. J. (2001). Invariant scaling relationships for interspecific plant biomass production rates and body size. Proceedings of the National Academy of Sciences of the United States of America 98, 29222927. Norton, S. F. (1995). A functional approach to ecomorphological patterns of feeding in cottid fishes. Environmental Biology of Fishes 44, 6178. Petchey, O. L. & Gaston, K. J. (2002). Functional diversity (FD), species richness and community composition. Ecology Letters 5, 402411. Piet, G. J. (1998). Ecomorphology of a size-structured tropical freshwater fish community. Environmental Biology of Fishes 51, 6786. Purvis, A. & Hector, A. (2000). Getting the measure of biodiversity. Nature 405, 212219. Rosecchi, E. (1985). Lalimentation de Diplodus annularis, Diplodus sargus, Diplodus vulgaris et Sparus aurata (Pisces, Sparidae) dans le golfe du Lion et les lagunes littorales. Revue des Travaux de lInstitut des Peches maritimes 49, 125141. Sanzo, L. (1911). Distributione delle papille cutanee (organi ciatiform) e suo valore sistematico nei Gobi. Mitteilungen aus der Zoologishen Station zu Neapel 20, 251328. Sibbing, F. A. & Nagelkerke, L. A. J. (2001). Resource partitioning by Lake Tana barbs predicted from fish morphometrics and prey characteristics. Reviews in Fish Biology and Fisheries 10, 393437. Simberloff, D. & Dayan, T. (1991). The guild concept and the structure of ecological communities. Annual Review of Ecology and Systematics 22, 115143. Simpson, E. H. (1949). Measurement of species diversity. Nature 163, 688. Smith, B. & Wilson, J. B. (1996). A consumers guide to evenness indices. Oikos 76, 7082. Tilman, D. (1999). The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80, 14551474. Tilman, D., Knops, J., Weldin, D., Reich, P., Ritchie, M. & Siemann, E. (1997). The influence of functional diversity and composition on ecosystem processes. Science 277, 13001302. gime alimentaire Trabelsi, M., Kartas, F. & Quignard, J. P. (1994). Comparaison du re dune population marine et dune population lagunaire dAtherina boyeri des co tes tunisiennes. Vie Milieu 44, 117123. UNESCO (1986). Fishes of the North-eastern Atlantic and the Mediterranean, Vols II & III (Whitehead, P. J. P., Bauchot, M.-L., Hureau, J.-C., Nielsen, J. & Tortonese, E., eds). Paris: UNESCO. Wainwright, P. C., Bellwood, D. R. & Westneat, M. W. (2002). Ecomorphology of locomotion in labrid fishes. Environmental Biology of Fishes 65, 4762. Walker, B. H. & Langridge, J. L. (2002). Measuring functional diversity in plant communities with mixed life forms: a problem of hard and soft attributes. Ecosystems 5, 529538. Walker, B., Kinzig, A. & Langridge, J. (1999). Plant attribute diversity, resilience, and ecosystem function: the nature and significance of dominant and minor species. Ecosystems 2, 95113. Walker, J. A. & Westneat, M. W. (2000). Mechanical performance of aquatic rowing and flying. Proceedings of the Royal Society of London Series B 267, 18751881. Walter, L. L. & Legner, E. F. (1980). Impact of the desert pupfish, Cyprinodon macularis and Gambusia affinis on fauna in pond ecosystems. Hilgardia 4, 18. Warwick, R. M. & Clarke, K. R. (1995). New biodiversity measures reveal a decrease in taxonomic distinctness with increasing stress. Marine Ecology Progress Series 129, 301305. West, G. B., Brown, J. H. & Enquist, B. J. (1997). A general model for the origin of allometric scaling laws in biology. Science 276, 122126. Wilson, J. B. (1999). Guilds, functional types and ecological groups. Oikos 86, 507522. Winemiller, K. O. (1991). Ecomorphological diversification in lowland freshwater fish assemblages from 5 biotic regions. Ecological Monographs 61, 343365.

2004 The Fisheries Society of the British Isles, Journal of Fish Biology 2004, 64, 970983