Environmental factors structuring fish composition and assemblages in a small macrotidal estuary (eastern English Channel)

Estuarine, Coastal and Shelf Science 79 (2008) 507–517

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Environmental factors structuring fish composition and assemblages in a small macrotidal estuary (eastern English Channel) Jonathan Selleslagh*, Rachid Amara ˆte d’Opale, 32 avenue Foch, 62930 Wimereux, France Laboratoire d’Oce´anologie et de Ge´osciences, UMR 8187 LOG CNRS, Universite´ du Littoral Co

a r t i c l e i n f o

a b s t r a c t

Article history: Received 25 February 2008 Accepted 9 May 2008 Available online 21 May 2008

The fish assemblage structure was analyzed along an estuarine gradient of a small macrotidal estuary (the Canche, France). Fishes were collected every two months between May 2006 and July 2007 from 12 sampling stations using a 1.5-m beam trawl with a 5 mm mesh size in the cod end. To complement this information, sampling was also performed using 15-m fyke nets (8 mm mesh size in the cod end). For each sample, abiotic (temperature, salinity, pH, oxygen, turbidity, river flow, wind speed and depth) and biotic (macro crustacean species abundances) were recorded. Throughout the study, 28 fish species belonging to 20 families were collected. Fish catches were dominated by juveniles, especially Young-Ofthe-Year (YOY) for the majority of the species. According to the Index of Relative Importance (IRI), common goby Pomatoschistus microps, flounder Platichtys flesus, sprat Sprattus sprattus, sea-bass Dicentrarchus labrax and plaice Pleuronectes platessa were the most abundant species, together accounting for 99.2% of the total IRI. Estuarine residents (ER ¼ 66.2%) and marine juvenile migrants species (MJ ¼ 31.4%) were the most important ecological guilds. The structure of the fish assemblage and its relationship to environmental variables was examined using multivariate techniques. Cluster and non-metric multidimensional scaling (nMDS) analysis defined six distinct groups in the Canche estuary, which are discriminated by specific species (SIMPER). Spatio-temporal variations in fish assemblage structure reflect the density peaks of the most abundant species. Spearman rank correlations and canonical correspondence analysis (CCA) showed that among the ten environmental variables examined, temperature, salinity and Crangon crangon (a potential predator for YOY fish or prey for older ones) are the three most important factors influencing fish species richness and abundances. Our observations reinforce the idea that certain fish species may have different life history styles in different geographic areas. The present study highlights the necessity of a better knowledge of the connectivity between estuaries and adjacent marine areas. The Canche constitutes an important ecosystem for fishes and as it is subject to little anthropogenic disturbance; its ichthyofauna can be viewed as a reference or normal assemblage for small temperate macrotidal estuaries. Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: fish assemblage estuarine use ecological guilds environmental factors eastern English Channel

1. Introduction Estuaries are important to humans and marine life. They are widely regarded as among the most productive aquatic systems in the world (McHugh, 1967) and perform a crucial role in the population dynamic of many invertebrate and fish species. They provide a migratory route for anadromous and catadromous fish species, an environment for truly estuarine species and nursery areas for many marine species (McLusky and Elliott, 2004). Several authors have emphasized the importance of estuaries for marine fisheries by demonstrating that a large part of the landings around the world is made up of species that spend part of their life in

* Corresponding author. E-mail address: [email protected] (J. Selleslagh). 0272-7714/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2008.05.006

estuarine waters (Pauly, 1988; Lamberth and Turpie, 2003). Since the adults of many estuarine-dependent species are exploited commercially, the preservation of estuarine habitats is clearly important for maintenance of many marine fisheries (Chambers, 1992). Estuaries are transition zones between seas and freshwater that are occupied by a combination of freshwater and marine species, including many juveniles (Claridge et al., 1986). Compared to marine or freshwater systems, estuaries are abiotically variable and therefore may be rigorous and stressful habitats. Species that inhabit estuaries must be able to tolerate or avoid wide range of salinity, temperature, dissolved oxygen and high level of turbidity. For example, relatively few species are adapted to thrive in conditions such as fluctuating salinity and their resultant physiological demands (Haedrich, 1983). The relationship between environmental factors and the distribution of organisms within estuaries has

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received considerable attention. Because fish are one of the dominant macrofaunal components of estuarine biota, many studies have focused on their distribution patterns (Blaber and Blaber, 1980; Marshall and Elliott, 1998; Whitfield, 1999; Akin et al., 2005). Most of these studies were, however, conducted in large estuaries exposed to important human pressures. Consequently, we currently lack information on both small and less-impacted or nonimpacted estuaries. Estuaries, like many other types of wetland worldwide, are under long-term threat of damage and destruction. While the role of estuarine nursery areas is well known on a qualitative basis (Elliott et al., 1990), the consequences of temporal fluctuations in estuarine environmental variables on the fish populations utilizing estuaries are less well understood. The knowledge of the response of estuarine fishes to changes in environmental conditions will not only enhance our biological understanding of estuarine fish, but will contribute to our understanding of the potential effects of anthropogenic impacts on estuarine fish species. Indeed, there is a growing interest in the use of fish communities in estuarine water quality evaluation and assessments of human impacts (Whitfield and Elliott, 2002; Harrison and Whitfield, 2004). As part of the European Water Framework Directive (WFD; EC, 2000) there is for example a need to determine what is a normal fish assemblage of transitional waters and to assess what deviation there has been from that normality due to human impacts. The study of the structure and functioning of biological communities of least impacted estuaries can be used to generate reference conditions (Harrison and Whitfield, 2004; McLusky and Elliott, 2004). In the present study we analyzed for the first time the fish assemblage of a small macrotidal estuary (the Canche) which is, in contrast to numerous estuaries, less subject to anthropogenic disturbance (Amara et al., 2007). The composition and assemblage of its ichthyofauna can be viewed as a reference or normal assemblage for small temperate estuaries. No information is available about fish assemblages of the English Channel estuaries (Franco et al., 2008). The objectives of the present study were to address this lack of knowledge by describing the fish composition and analyzing the seasonal and spatial patterns in the structure of the fish assemblages of the Canche estuary in relation with various abiotic and biotic factors. 2. Materials and methods 2.1. Study area The study area was the Canche (50 500 50 560 N, 1570 1670 E; Fig. 1), a small estuary, located in northern France along the coast

of the eastern English Channel. The Canche estuary is 12 km in length, 1 km maximum in width and is characterized by a sandymud substratum (Selleslagh, unpublished data). The estuary is characterized by semi-diurnal tide with an average tidal range of about 1 m at neap tides and 6 m at spring tides and can be considered as a macro/hyper-tidal estuary according to the McLusky and Elliott (2004) classification. The water circulation is mainly dependant on the tides and on a small freshwater input of about 13 m3 s1. The Canche estuary can be considered as a little impacted system (Amara et al., 2007) and is classified site under ‘‘Natura 2000’’.

2.2. Sampling and environmental data Fish were collected every two months from May 2006 to July 2007 (except in July 2006) in 12 sampling stations distributed along the estuarine gradient where salinity ranged from 0 in upper reaches to 35 in lower reaches (Fig. 1). Sampling was performed during daytime using a 1.5 m beam trawl, with one tickler chain and 5 mm mesh size in the cod end, towed by a zodiac against the current at 2 knots for 15 min, covering an area of about 1000 m2. All stations were sampled at each survey, except two (stations 7 and 12) in November 2006 due to technical problems. In order to minimize the confounding effects of variations in tidal stage and environmental conditions between each sampling period and to standardize the sampling regime, all sites were sampled at high tide  2 h and with similar tide coefficients for each survey. To complement information on species richness, sampling was also performed using four 15-m fyke nets (8 mm mesh size in the cod end). Two fyke nets were displayed in the middle and upper estuary (Fig. 1) at low tide for a 48 h period at each sampling survey. Prior to trawling, water physico-chemical factors (temperature, salinity, pH, % saturation in dissolved oxygen and turbidity) were recorded using a Tetracon 325 and Cyberscan multiprobes in each sampling station. Depth was recorded at each station and Canche river flow and wind speed data were obtained from the water agency (www.hydro.eaufrance.fr) and ‘‘Me´te´o France Boulogne’’ respectively. The abundance of the brown shrimp Crangon crangon and the green crab Carcinus maenas captured during trawling were also taken into account in the analyses as biotic factors. These two species are considered as potential predator for Young-Of-the-Year (YOY) fish or prey for older ones, and accounted for more than 90% of the total abundance of macro crustaceans.

2.3. Data analysis

Fig. 1. Map of the Canche estuary with location of the beam trawl and fyke net sampling stations.

After each trawl, fishes were identified to species level, weighed (total weight) and measured to the nearest millimeter (total length). If the number of individuals of a species exceeded 30, a representative sub-sample of 30 individuals was measured and weighed and the rest was counted. In order to standardize captures between each trawl and to allow comparisons, fish and macro crustacean abundances were expressed as number of individuals per 1000 m2. The dominant fish species throughout the study period (together contributing >90% of the total Index of Relative Importance (IRI) for each sampling month) were determined using the IRI developed by Pinkas et al. (1971). The IRI aggregate the main evaluation methods (abundance, biomass and frequency of occurrence) within a single index: IRI ¼ (N% þ W%) FO%, where N%, W% and FO% are the relative abundances, biomass and frequency of occurrence, respectively. These indices were calculated on the total 82 samples.

J. Selleslagh, R. Amara / Estuarine, Coastal and Shelf Science 79 (2008) 507–517

2.4. Statistical analyses To test the null hypothesis of no difference between fyke net and beam trawl, ANOSIM was conducted on fish composition (presence/absence). As fyke net data could not be expressed as individuals per 1000 m2 and as sampling was limited to the middle and upper estuary, fish assemblage analyses were performed only on beam trawl data. To compare functional structure of the fish assemblage, species were classified to ecological guilds defined by Elliott and Dewailly (1995): estuarine residents (ER), marine adventitious visitors (MA), diadromous (catadromous/anadromous) migrants (CA), marine seasonal migrants (MS), marine juvenile migrants (nursery species) (MJ) or freshwater adventitious visitors (FW).

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Similarities between samples were computed by a Bray–Curtis similarity matrix using fish species abundances (fourth-root transformed). Similarities were graphically represented by cluster, with distances calculated by group-average sorting and comparison made by similarity profile (SIMPROF test), and by ordination plots using non-metric multidimensional scaling (nMDS). Similarity percentages (SIMPER) were used to determine which species were most responsible for the Bray–Curtis dissimilarity between groups. All these multivariate analyses were performed using the PRIMER software package (version 6.1.9) (Clarke and Warwick, 2001). The identification of the subsets of the eight abiotic (temperature, salinity, pH, % saturation in dissolved oxygen, turbidity, depth, wind speed, river flow) and two biotic parameters (Crangon crangon and Carcinus maenas abundances), which are best correlated to

Fig. 2. Temporal and spatial variations in mean (SD) abiotic environmental variables (temperature, salinity, pH, % saturation in dissolved oxygen and turbidity) in the Canche. Estuarine divisions: L, limnetic; O, oligohaline; M, mesohaline; P, polyhaline; E, euhaline.

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Fig. 3. Temporal and spatial variations in mean (SD) biotic environmental variables (Crangon crangon and Carcinus maenas abundances) in the Canche estuary.

the assemblage structure and which may thus be assumed to greatly affect the communities were examined by CCA (Ter Braak, 1986) using the R package. Analysis was performed on fourth-root transformed fish species abundances. Spearman rank correlation coefficients were used to determine the effect of environmental variables on dominant fish species. A significance level of a minimum of 5% was considered in all statistical analyses.

3. Results 3.1. Environmental conditions Temperature showed seasonal variations (Fig. 2). Highest values were observed in summer months (September and July) with a maximum of 20.7  C and the lowest values during winter (January) with a minimum of 7.6  C. No inter-station variation was observed along the estuarine gradient. Inversely, salinity showed spatial variations, from 0 in the upper part (station 1) to 34.4 in the lower part of the estuary, and no seasonal trends. According to the Venice System (1959), the estuary can be divided into five zones: limnetic L (stations S1, S2), oligohaline O (S3), mesohaline M (S4), polyhaline P (S5, S6) and euhaline E (S7–S12) zones. Salinity was highly variable in the oligo-, meso- and polyhaline zones as indicated by the high standard deviation of the measured values (Fig. 2). Dissolved oxygen and pH

both indicated significant seasonal variations but relatively stable values between stations (Fig. 2), with mean monthly values ranged from 91 to 106 and from 7.8 to 8.6 respectively, but no spatial variations (Fig. 2). Turbidity indicated spatial variations (Fig. 2), with lowest values at station 3 and highest values in central and lower parts of the estuary. On monthly scale, lowest value (2.9 NTU) was obtained in May 2007 and the highest value (110 NTU) in July 2007. River flow was low during the study period (<20 m s1) and depth ranged from 1.5 to 5 m along the estuary. Concerning macro crustaceans, brown shrimp Crangon crangon and green crab Carcinus maenas were clearly the dominant species, as they accounted for more than 90% of the total abundance. Thus, only these two species were retained as biotic factors. C. crangon showed high abundances during the study period (Fig. 3), except in May 2007, and presented the highest density of 321.6 ind. 1000 m2 in July 2007. C. crangon was caught everywhere in the estuary but at lower densities in limnetic zone and at station S7. Carcinus maenas was less abundant during winter months and was absent or at very low abundance in the upper estuary but abundant in the middle (S5, S7, S8) (Fig. 3). 3.2. Fish composition A total of 28 fish species belonging to 20 families were collected in the Canche during the study period (Table 1). Most of the species

Table 1 Families, species, ecological guilds (EG), index of relative importance (IRI), mean length (Lt, mm) and density of fish (ind. 1000 m2), captured in the Canche estuary between May 2006 and July 2007 with beam trawl. Ecological guilds: MA, marine adventitious visitors; CA, catadromous/anadromous migrants; MS, marine seasonal migrants; FW, freshwater adventitious visitors; ER, estuarine residents. The species collected in fyke nets are indicated in bold. : IRI < 0.01 Family

Species (abbreviation)

EG

IRI

mean Lt  SD

Cyprinidae

Blicca bjoerkna (B. bjo) Rutilus rutilus (R. rut) Cottus gobio (C. gob) Lampetra fluviatilis (L. flu) Anguilla anguilla (A. ang) Sprattus sprattus (S. spr) Engraulis encrasicolus (E. enc) Salmo trutta fario (S. far) Salmo trutta trutta (S. tru) Salmo salar (S. sal) Oncorhynchus mykiss (O. myk) Ciliata mustela (C. must) Gadidae larvae (g lar) Liparis montagui (L. mon) Liza aurata (L. aur) Atherina presbyter (A. pre) Dicentrarchus labrax (D. lab) Trachurus trachurus (T. tra) Aphia minuta (A. min) Pomatoschistus lozanoi (P. loz) Pomatoschistus microps (P. mic) Echiichthys vipera (E. vip) Ammodytes tobianus (A. tob) Syngnathus acus (S. acu) Platichtys flesus (P. fle) Pleuronectes platessa (P. pla) Solea solea (S. sol) Scophtalmus rhombus (S. rho)

FW FW FW CA CA MJ MS FW CA CA FW ER MJ MA MA MA MJ MA MA MA ER MA MA ER ER MJ MJ MJ

     17.3   0 0 0     0.2 13.5   0.6 49.7  0.1 0.1 17.6 1.0  

92.0 32.5  3 79.0  9 223.5  155 190.0 58.9  25 100.0 206.0

Cottidae Petromyzontidae Anguillidae Clupeidae Engraulidae Salmonidae

Gadidae Liparidae Mugilidae Atherinidae Moronidae Carangidae Gobiidae

Trachinidae Ammodytidae Syngnathidae Pleuronectidae Soleidae Scophtalmidae

149.5  36 25.6  5 68.0 90.5  8 87.2  6 89.1  18 60.0 58.0 66.1  8 42.7  5 129.0 104.6  19 100.7  26 59.9  36 47.9  18 55.6  5 76.1  73

Mean density (ind. 1000 m2) May 06

Sep 06

Nov 06

Jan 06

Mar 06

May 07

Jul 07

0 0 0 0 0.1 17.6 0 0 0 0 0 0 0.1 0 0 0 1.1 0 0.1 0 43 0.1 0.1 0.2 49.9 20.9 0 0.1

0 0 0 0 0 45.3 0.1 0 0 0 0 0 0 0 0 0 1.9 0 0 0 7.3 0 0.2 0.3 1.2 0.2 0 0

0 0 0 0.1 0 4.9 0 0 0 0 0 0 0 0 0.1 4.5 22.1 0 0 4.5 58.2 0 0.2 0.1 4.4 0.4 0 0

0 0 0 0 0 0.1 0 0 0 0 0 0.1 0 0.1 0.1 1.4 14.4 0 0 3.1 175.7 0 0.2 0 5.0 0.9 0 0

0.1 0 0.2 0.1 0 0.1 0 0.1 0 0 0 0.1 0 0 0 0.2 13.5 0 0 4.7 180.7 0 0.2 0.8 9.8 1.1 0 0.1

0 0 0 0 0 40.2 0 0 0 0 0 0 0.1 0 0 0 4.3 0 0 0 108.8 0 0 0 14.4 0.5 0.1 0

0 0.9 0 0 0.1 151.2 0 0 0 0 0 0 0 0 0 0 0.2 0.1 0.2 4.1 2.3 0 0.8 0.2 37.9 0.5 0.7 0.3

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Fig. 4. Temporal and spatial variations in mean (SD) species richness S, fish density D and biomass B in the Canche.

were occasional, occurring accidentally or during a specific period. Only five species occurred across the seven sampling dates (Table 1). The three most abundant families, based on total abundance, are Gobiidae (56.2%), Clupeidae (24.1%) and Pleuronectidae (13.6%), accounting for 93.9% of the total catch. In terms of IRI, the dominant species were, by respective importance, common goby Pomatoschistus microps (49.7%), flounder Platichtys flesus (17.7%), sprat Sprattus sprattus (17.3%), sea-bass Dicentrarchus labrax (13.5%) and, to a lesser level, plaice Pleuronectes platessa (1%), together accounting for 99.2% of the total IRI. The resident species P. microps clearly dominated the fish assemblages throughout the study period (Table 1). Results showed a strong difference in the species composition according to whether we used beam trawl or fyke net (Table 1). A total of 25 species were captured with the beam trawl whereas only 13 species were collected with the fyke net. In contrast, three Salmonidae species were only captured with the fyke net. Comparison of fish composition between beam trawl and fyke net showed significant difference (ANOSIM; r ¼ 0.633, P ¼ 0.001). In terms of ecological guilds, the fish assemblage was dominated by estuarine residents species ER, which comprised 66.2% of the overall abundance during the study period, followed by marine juvenile migrants MJ (31.4%), marine adventitious visitors MA (2.1%) and marine seasonal migrants MS, catadromous/anadromous migrants CA and freshwater adventitious visitors FW (0.1% each). Each ecological guild was clearly dominated by few species: ER by common goby and flounder, MJ by sprat and sea bass or plaice, CA by European eel, MA by Lozano’s goby Pomatoschistus lozanoı¨ or sand smelt Atherina presbyter and FW by Cyprinidae. According to the lengths of the examined fish, catches were dominated by juveniles (especially YOY) for the majority of the species (Table 1).

salinity (r ¼ 0.76), pH (r ¼ 0.78) and turbidity (r ¼ 0.77) whereas biomass variations were significantly correlated only with salinity (r ¼ 0.96) and turbidity (r ¼ 0.86). Concerning the spatial variations, species richness were significantly correlated with salinity (r ¼ 0.67) and depth (r ¼ 0.82) whereas abundance variations were significantly correlated with depth (r ¼ 0.73). Important temporal and spatial changes were observed in fish abundance per each ecological guild (Fig. 5). Estuarine residents ER clearly dominated the fish assemblage from November to May whereas summer months (September and July) were dominated by marine juvenile migrants MJ. Marine adventitious visitors MA were mainly present during winter months (November to March).

3.3. Temporal and spatial variations in assemblage structure Species richness showed important variations both in time and space with higher values during winter months (November, January and March) and lowest in the upper part of the estuary (Fig. 4). Abundance and biomass both showed spatio-temporal variations (Fig. 4) and were well correlated (r ¼ 0.86). Abundance and biomass were higher in January and March and lower in September. Stations located in the limnetic and lowest part of the euhaline zone had the lowest abundance and biomass (Fig. 4). Temporal variations in species richness were significantly correlated with

Fig. 5. Temporal and spatial variations of the relative composition of each ecological guild. MA, marine adventitious visitors; MS, marine seasonal migrants; MJ, marine juvenile migrants; ER, estuarine residents; CA, catadromous/anadromous migrants; FW, freshwater adventitious visitors.

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Likewise, a clear spatial pattern was observed along the estuarine gradient (Fig. 5). ER clearly dominated the limnetic, oligo- and mesohaline zones (>75%). Freshwater species FW quasi occurred only in the limnetic zone of the estuary. ER species, with MJ species as second principal group, were generally dominant in most of the other stations. MA species were found quasi only in euhaline zone, with an increase importance towards lower stations (Fig. 5). These results suggest the specific functional role played by each haline zone in the Canche estuary toward fish assemblages. 3.4. Temporal and spatial variations in abundance and fish length of dominant species A more or less clear temporal and spatial fluctuation in both abundance and fish length was observed for the dominant species

(Fig. 6). Platichtys flesus and Sprattus sprattus occurred essentially during warm months (May and July) with mean abundances of 40 and 100 ind. 1000 m2 respectively, whereas Dicentrarchus labrax and Pomatoschistus microps where more abundant (20 and 200 ind. 1000 m2 respectively) in cooler months (November to March). Pleuronectes platessa was abundant only during May (21 ind. 1000 m2). Abundance peaks were generally characterized by small individuals as indicated by the temporal fish length variations (Fig. 6). There was significant temporal difference in fish size with an increase in size from the peak abundances. Concerning the spatial distribution, P. microps had a large spatial distribution with a relative low abundance in the limnetic zone whereas D. labrax and S. sprattus were caught everywhere, but with higher abundances in the meso- and euhaline zones, and in the poly- and euhaline zones, respectively. The two flatfish species (P. flesus and P. platessa)

Fig. 6. Temporal and spatial variations in mean (SD) fish length (Lt, mm) and density (D, ind. 1000 m2) for the four dominant species. Fish length was not measured in May and July.

J. Selleslagh, R. Amara / Estuarine, Coastal and Shelf Science 79 (2008) 507–517

showed a clear distribution along the estuarine gradient. The highest abundance of P. flesus were found in the upper part and correspond to the smallest individual (mean size ¼ 50.6 mm). Pleuronectes platessa was never caught in water of salinity <15 and the highest abundance and smallest individuals (mean size ¼ 39.4 mm) were found in the middle of the estuary in polyhaline waters. Pleuronectes platessa, P. flesus and D. labrax clearly showed spatial size decrease from the estuary mouth (Fig. 6).

3.5. Fish assemblages and environmental influence Similarity analysis between samples based on fish abundances was undertaken in order to constitute fish assemblage groupings. Cluster analysis data illustrated a clear division (according to and defined by SIMPROF test) into six distinct groups of samples (Fig. 7a), with a similarity level between groups (Bray–Curtis Similarity, BCS) ranging from 40–50%. Dendrogram pattern was well supported by nMDS results, the six groups found in the cluster analysis being well separated from each other on the 2D nMDS ordination (Fig. 7b; stress value ¼ 0.18). Groups were clearly separated according to seasons and, to a lesser level, to spatial scale, mainly during winter period (groups I and II; Fig. 7a,b).

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Group I consisted of ‘‘Winter’’ samples at upper and middle zones (S1–S7) and was significantly discriminated by Pomatoschistus microps, Platichtys flesus and Dicentrarchus labrax (SIMPER, contribution 90%; Table 2). Group II consisted of ‘‘Winter’’ samples of the lower zone (S8–S12) and was discriminated by P. microps, D. labrax, Pomatoschistus lozanoi, Atherina presbyter, P. flesus and Pleuronectes platessa; group III of ‘‘Autumn’’ samples, discriminated by Sprattus sprattus, P. microps and D. labrax. Group IV consisted of ‘‘Extreme’’ samples, which were characterized by low abundance of fish and only few P. flesus and P. microps. Group V was characterized by ‘‘Spring’’ samples and discriminated by P. microps, P. platessa, S. sprattus and P. flesus, whereas the sixth group consisted of ‘‘Summer’’ samples, which were discriminated by S. sprattus and, to a lesser level, P. flesus, P. microps and D. labrax (Table 2). The CCA analysis (based on species abundances) indicated that variables (abiotic and biotic) explain significantly about 31% of the fish assemblages in the Canche estuary. Although several axes were determined within the analysis, only axes 1 and 2 were plotted as they accounted for 57% of the variability explained by the 11 axes. Fig. 8 indicates the relative environmental preference of fish species. Considering their vector length, temperature (best correlated with axis 1, r ¼ 0.89) and salinity and Crangon crangon abundance (best correlated with axis 2, r ¼ 0.91 and 0.73, respectively) are the three most important environmental variables influencing the fish assemblage (Fig. 8). Axis 1 separates species encounter in warmer period (on the right) to those in cooler period (on the left) whereas axis 2 separates species with low salinity preference (on the top) to euryhaline or marine species (on the bottom). Results showed that biotic variables (abundances of Carcinus maenas and C. crangon, potential predators or prey for fish) have an additional influence to abiotic variables on fish abundances in the Canche estuary. Spearman rank correlations indicated that temperature (and pH) positively affected Sprattus sprattus (0.69 and 0.39 respectively) and negatively Pomatoschistus microps (0.55) and Dicentrarchus labrax (0.55) abundances. Salinity affected flatfish, with a negative effect on flounder (0.69) but a positive one on plaice (0.38). Flow positively affected flounder and common goby and negatively sprat whereas wind intensity only positively affected flounder. Carcinus maenas and C. crangon showed positive correlations with plaice (0.43 and 0.51 respectively) and sprat on a lower level (0.37). The densities of the principal species were not significantly related to oxygen, turbidity or depth. 4. Discussion 4.1. Fish assemblage composition

Fig. 7. Cluster analysis (a) and two-dimensional nMDS ordination plot (b) of the fish assemblages (based on fish abundances) according to Bray–Curtis similarity. Stress value (2D) is given in the top right hand corner of the ordination.

The present study is the first to analyze the fish composition and assemblage of the Canche estuary and more generally of English Channel estuaries. The Canche supported fewer species than most of the European estuaries but in the range of what was recorded: between 16 (Canet–Saint-Nazaire lagoon) and 110 (Thames) species with an average (SD) of 53  20 in 38 European estuaries (Franco et al., 2008). When compared with estuaries which flow in the North Sea, the Canche diversity is lower than the Scheldt estuary (62 species; Maes et al., 2005) and the Elbe Estuary (58 species; Thiel and Potter, 2001), but higher than the Humber estuary (23 species; Marshall and Elliott, 1998). Without mentioning gradients, Elliott and Dewailly (1995) argued that fish composition and assemblage structures reflected major differences in latitude. The diversity of fish species within an area is partly function of the number of available niches and the habitat size (Wootton, 1990), as well as the geographical aspect (Kneib, 1997). Such criteria influence hydrology, salinity, the upstream saltwater penetration limit and the boundary of the external estuary. Thus, as found here, it is not unexpected that small estuaries had smaller species

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Table 2 Discriminating species (% contribution) of each group, defined by SIMPROF test, using SIMPER analysis Average similarity (%)

I (72.6)

II (72.0)

III (67.3)

IV (36.0)

V (68.3)

VI (55.7)

31.5

46.9 48.3

38.5 11.2 19.0

10.7 15.5 62.4 5.2

Contribution (%) P. microps P. flesus S. sprattus D. labrax P. platessa P. lozanoı¨ A. presbyter

52.4 25.9

32.5 8.5

19.8

21.2 3.7 19.1 8.7

Total

98.1

93.7

richness. Species richness is also heavily dependent on both the sampling methods used as well as sampling effort. Whitfield and Marais (1999) recommend that the abundance and catch composition of fishes in estuaries should be determined using different sampling methods that overlap in terms of selectivity. The present study confirmed the utility of using different sampling methods (beam trawl and fyke net) for a better description of the fish composition; only three Salmonidae species were captured with fyke nets. However, the gear selectivity of the fyke nets, which have relatively large mesh size (8 mm), have underestimated the small sized fish classes (Malavasi et al., 2004). Caution is therefore needed to carry out fish composition comparison between estuaries sampled with different methods. Fish assemblages in European estuaries are typically dominated by marine species, either migrants or straggler species, i.e. irregular visitors with no apparent estuarine requirements (Elliott and Dewailly, 1995; Thiel and Potter, 2001; Maes et al., 2005; Franco et al., 2008). Fish assemblage structure of the Canche consisted of approximately the same ecological guilds that are common in European estuaries, although marine adventitious (MA) were low in abundance. Estuarine residents (66.2%) and MJ (31.4%) were the most important ecological guilds of the Canche fish assemblage and

36.6 22.7

25.6

90.8

95.2

94.3

Gobiidae, Clupeidae and Pleuronectidae the most important families. At the species level, the fish fauna is largely dominated by the common goby (54.7%), followed by flounder, sprat and sea-bass. Dominance by a few species is a pattern generally observed in estuaries around the world (Cabral et al., 2001; Akin et al., 2005; Maes et al., 2005; Elliott et al., 2007). Contrary to most other fish species, Pomatoschistus microps benefit from a wider temperature and salinity range tolerance (Dolbeth et al., 2007), allowing the species to occupy different areas in the estuary. When compared with other European estuarine systems (e.g.; Elliott and Dewailly, 1995; Thiel and Potter, 2001; Lobry et al., 2003; Franco et al., 2008), the main difference that can be found is the very low abundance of Mugilidae and Soleidae. The low abundance of Mugillidae in beam trawl sampling was also noted by Martinho et al. (2007) in the Mondego estuary (Portugal). Beam trawling is often considered a suitable method for sampling benthic species, but tends to underestimate pelagic species (Thiel et al., 2003) such as mugilids. However, as shown in other shallow estuaries beam trawling takes a representative pelagic population and Mugilidae are well represented in the sampling (see Elliott et al., 2007). In the present study, because of the low depth of the Canche estuary, the beam trawl samples the quasi-totality of the water column and thus allows pelagic species to be caught in high abundance. Thus the scarcity of Mugilidae in the present study is a characteristic of the Canche estuary. 4.2. Estuary fish use

Fig. 8. CCA ordination diagram based on species abundances, with biotic and abiotic environmental factors represented by vectors. See Table 1 for species abbreviations. Sample codes: number represents the station (1–12) and letter the sampling month (a, May 06; b, September 06; c, November 06; d, January 07; e, March 07; f, May 07; g, July 07).

The low number of ER species encountered reinforces the idea that only few fish species complete their life cycle in estuaries (Claridge et al., 1986; Elliott et al., 2007). As observed in other estuaries, the Canche was mostly used as temporary habitat by fish, as feeding or nursery grounds. Numerous individuals caught were juveniles of euryhaline marine fish species. Nurseries are areas where juveniles aggregate and where fitness is enhanced through better feeding conditions, optimal growth, refuge opportunities and high connectivity with other habitats (Beck et al., 2001). However, despite their recognized importance as nursery areas, some controversy exists as to whether or not marine (juvenile) fish species are really dependent on estuaries or just opportunistically using them in order to achieve higher growth rates and a lower exposure to piscivorous predation than found in other inshore coastal areas (Paterson and Whitfield, 2000). Juveniles of many marine fish found in abundance in the Canche (e.g. plaice, sea-bass or sprat) are commonly found at the same period and developmental stage in marine shallow environments (intertidal sandy beaches or subtidal areas) (Amara and Paul, 2003; Selleslagh and Amara, 2007, 2008). In some geographic areas, sheltered estuarine habitats may offer high densities of prey and other food not encountered in marine areas, and their turbid shallow waters provide protection from predators (McLusky and Elliott, 2004). The simultaneous use of estuarine and shallow marine habitats may be

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a strategy to reduce the intra-and interspecific competition (for food or space) particularly during peak recruitment (Amara et al., 2001). Therefore, these juvenile species can be considered as ‘‘juvenile marine estuarine opportunists’’ since they typically inhabit both estuaries and inshore marine environments (Potter et al., 1997). This result supports the hypothesis that estuarine migration can be considered as facultative migration, with many young fish remaining at the coastal nurseries (Guelinckx et al., 2006). Individual fish may quickly respond to climatic constraints or increased mortality risk and rapidly shift between coastal and estuarine nursery areas in order to increase their individual state and fitness (Childs et al., 2008). Under this hypothesis, estuaries remain crucial, although not necessary, habitats in the life history of fish species. In this work, three species were identified as estuarine resident fish although there is some disagreement in the literature about the designation of different estuarine fish species to life history categories (Maes et al., 2005; Elliott et al., 2007). The seasonality observed in the fluctuations of dominant estuarine resident fish species such as Pomatoschistus microps and Platichthys flesus parallels the patterns found in the shallow marine waters, suggesting that these species were able to spawn or complete their life cycles in marines waters (Maes et al., 2004). Many authors recognized only P. microps and Syngnathus rostellatus as ER species with populations that permanently reside and spawn in estuaries (Thiel and Potter, 2001; Lobry et al., 2003; Maes et al., 2004). In a recent study on life strategies of fishes in European estuaries, Franco et al. (2008), among others, described flounder as marine migrant’s species and typically spawning offshore in the continental shelf. In the present study smallest individual’s flounder (about 10 mm) were exclusively collected in the upper part of the estuary (stations S1, S2). In addition, ichthyoplankton sampling, performed on eight stations distributed along the estuary in spring and summer, revealed that flounder larvae were very abundant and only present in the upper stations of the estuary (personal observation). These observations suggest that flounder may also spawn inside the estuary and can be considered as an ER species. Although juveniles of the common sole, Solea solea are common in European estuaries (Amara et al., 1994; Malavasi et al., 2004; Cabral et al., 2007; Franco et al., 2008) and abundant in the shallow waters of the eastern English Channel (Amara, 2003), they rarely enter the Canche estuary. The factors which determine sole nursery colonization are poorly understood (Horwood, 1993; Amara et al., 2000). The role of attractants (mainly glycine-betain) in the sediment and in food has been mentioned (Marchand, 1992). It has been shown that the distribution of juvenile sole depends on habitat suitability which can vary significantly at local scales (Le Pape et al., 2007; Nicolas et al., 2007). Recent studies (Vinagre et al., 2006; Nicolas et al., 2007) showed that the presence of prey was a major factor affecting soles’ distribution. The absence or scarcity of S. solea in the Canche estuary may be explained by the fact that this species is opportunist and feeds on a wide range of bottomliving organisms and thus find suitable condition for their optimal growth in the shallow marine coastal areas (Amara et al., 2001). Our observations reinforce the idea that certain fish species may have different life history styles in different geographic areas, e.g. the cosmopolitan flathead mullet (Mugil cephalus, Mugilidae) may be catadromous in one region, an estuarine migrant in another and marine in a third (Elliott et al., 2007). 4.3. Spatial and temporal variations in relation to environmental variables The fish assemblage and species composition of the Canche is influenced by a variety of factors, both seasonal and spatial. Spatiotemporal variations in fish assemblage structure reflect the density

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peaks of the most abundant species. Most of these peaks correspond to recruitment events and occur predominantly during spring and summer. Winter months are characterized by a clear domination by ER species (mainly Pomatoschistus microps). The five dominant fish species followed seasonal patterns of occurrence, had distinctive seasonal abundance peaks and demonstrated only minimal temporal or spatial overlap. The same pattern has been already described for the fish communities which use the subtidal and intertidal sandy beach of the studied area (Amara and Paul, 2003; Selleslagh and Amara, 2008). As in many other estuaries, temperature and salinity are the two most important environmental variables influencing species richness, abundance and fish assemblage in the Canche. Thiel et al. (1995) found temperature to be the best predictor of temporal changes in fish abundance and species composition in the Elbe estuary (Germany), while salinity correlated with the spatial distribution of estuarine fish communities. For example, in the Humber, UK (Marshall and Elliott, 1998) and the Zeeschelde, Belgium (Maes et al., 1998), salinity influenced species richness, abundance and biomass. Temperature has been identified as the primary abiotic factor controlling key physiological, biochemical and life-history processes of fish (Beitinger and Fitzpatrick, 1979), and has been found to influence the utilization of estuaries by fishes worldwide (Thiel et al., 1995; Harrison and Whitfield, 2006). Generally, fish have a thermal preference that optimizes physiological processes. Although turbidity has been shown to influence the utilization of estuaries by fishes (Blaber and Blaber, 1980; Cyrus and Blaber, 1992; Akin et al., 2005), this was not the case within the Canche. The importance of turbidity to the distribution of fish species has been attributed to providing either protection from visual predators or an increased food supply (Blaber and Blaber, 1980; Cyrus and Blaber, 1992). The Canche is characterized by relative low turbidity (<60 NTU) comparatively to other European estuaries (e.g. Humber; Marshall and Elliott, 1998). Other environmental factors (freshwater flow, pH, wind intensity, oxygen and depth) were minor determinants of fish abundance, except some significant correlations. Contrary to most previous studies, in the present study both biotic and abiotic variables were used to explain the spatio-temporal fish assemblages. The CCA results indicate that fish assemblages were explained at 31% by biotic and abiotic variables; this is higher or comparable to results obtained in other studies with only abiotic variables. For example, five environmental variables accounted for only 18.4%, 34% and 29.6% of the fish distribution respectively in the Humber estuary, UK (Marshall and Elliott, 1998), Mondego estuary, Portugal (Martinho et al., 2007) and Koycegiz lagoon-estuary, Turkey (Akin et al., 2005). As in many studies on the influence of environmental factors on the utilization of estuaries by fishes (Marshall and Elliott, 1998; Martino and Able, 2003; Akin et al., 2005), the proportion of unexplained variation in the analysis was high (approximately 70–80%). A portion of this unexplained variation is likely the result of other abiotic (e.g. sediment characteristics; Prista et al., 2003) or biotic factors such as food availability, competition and predation (Lankford and Targett, 1994; Islam et al., 2006). It has been suggested that competitive interactions play a role in determining spatial, as well as temporal, partitioning in estuarine fish (Weinstein et al., 1980; Ogburn-Matthews and Allen, 1993). Even though the lower part of the euhaline zone had abundant prey resources (Selleslagh, unpublished data), this area of the estuary was not preferred by fish according to low values of biomass and abundance. Inversely, few species are adapted to thrive in low salinity, explaining the low biomass and abundance also observed in the limnetic zone. Time and energy spent locating and capturing prey in rough waters is greater than in calm waters, which may be a factor, together with salinity,

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contributing to spatial repartition of fish abundance and biomass. The high abundance of the brown shrimp Crangon crangon underlines its important role in the functioning of the estuarine ecosystem. Several studies have concluded that C. crangon is one of the major predators of shallow marine and estuarine areas and exerts a major impact on the infaunal community (Van der Veer and Bergman, 1987). For example, C. crangon predation has been postulated as a controlling factor in juvenile flounder (Van der Veer et al., 1991) and plaice abundance (Van der Veer and Bergman, 1987) and is known to influence larval plaice settling behavior (Wennhage and Gibson, 1998). In estuaries, fishes coexist with mobile invertebrates, such as crabs (Carcinus maenas) and shrimps (C. crangon) which feed on the same bottom fauna. In spring and summertime the small fish have to compete with these invertebrate for their food, and this may serve to limit the numbers of fish in an estuary (McLusky and Elliott, 2004). In the Canche estuary, C. crangon, potential predator for YOY fish (Van der Veer et al., 1991) or prey of several larger fishes (Amara et al., 2001) affected fish abundances or assemblage variability. 5. Conclusions In addition to the fact that the Canche estuary seems to be a temporary habitat for most fish species, the present study underlines the importance of small estuaries as nursery areas and their role for the maintenance of coastal stocks. Due to the limited number of truly estuarine fish, fish assemblage and annual variability in the abundance of the different species of the Canche estuary is determined mainly by marine estuarine opportunist species and recruitment processes at sea (larval and juvenile supplies). Our observations reinforce the idea that certain fish species may have different life history styles in different geographical areas and therefore, as underlined by other recent studies, create further difficulties in the standardization of fish guild definitions. A variety of factors have been showed to influence the utilization of European estuaries by fishes. Weak associations of fish assemblages with environmental factors have, however, been demonstrated in other estuaries. The relative importance of biotic and abiotic factors in driving the spatial and temporal patterns of occurrence of fish in estuaries is still poorly known. The study of the influence of habitat diversity within estuarine systems and more information on biotic interactions such as predator–prey interactions and prey distributions are required to enhance our understanding of estuarine use and dependence. This work highlights the necessity for a better knowledge of the connectivity between estuaries and adjacent marine areas. Acknowledgements This work was done as part of the CPER ‘‘Estuaire’’ project with the support of Fond Europe´en FEDER and Conseil Re´gional Nord Pas de Calais. The authors would like to thank Vincent Cornille, Eric Lecuyer and many students for their assistance with the field sampling and laboratory work. We are also grateful to Pascal Laffargue for his help with R statistical analysis. The authors wish to thank the three anonymous reviewers for providing useful comments on the manuscript. References Akin, S., Buhan, E., Winemiller, K.O., Yilmaz, H., 2005. Fish assemblage structure of Koycegiz lagoon-estuary, Turkey: spatial and temporal distribution patterns in relation to environmental variation. Estuarine, Coastal and Shelf Science 64, 671–684. Amara, R., 2003. Seasonal ichthyodiversity and growth patterns of juvenile flatfish on a nursery ground in the southern bight of the North Sea (France). Environmental Biology of Fishes 67, 191–201.

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