Food Resource Use in Sympatric Juvenile Plaice and Flounder in Estuarine Habitats Stefano Mariani, Ciara Boggan & David Balata

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Marine Ecology. ISSN 0173-9565

ORIGINAL ARTICLE Food resource use in sympatric juvenile plaice and flounder in estuarine habitats Stefano Mariani, Ciara Boggan & David Balata

Marine Biodiversity, Ecology & Evolution, UCD School of Biology & Environmental Science, University College Dublin, Belfield, Dublin, Ireland

Keywords Abstract A daptation; coastal habitats; flatfish; Irish Sea; Platichthys flesus; Pleuronectes platessa; Environmental conditions in estuarine habitats can vary greatly and influence trophic niche. the composition of fish assemblages and their trophic interrelationships. We investigated feeding habits and patterns of diet overlap in juvenile plaice ( Pleu Correspondence ronectes platessa) and flounder (Platichthys flesus) from two estuarine habitats Stefano Mariani, Marine Biodiversity, Ecology in the Irish Sea. Plaice was found to vary its diet significantly across environ & Evolution, UCD School of Biology & ments, whereas flounder exhibited a more consistent and homogeneous feeding Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland. pattern. Importantly, sympatric fish sampled at the same station were shown to E-mail: [email protected] reduce diet overlap. The results support the view that environmental hetero geneity in estuaries maintains a wide range of selective forces, the net outcome Accepted: 17 November 2010 of which can produce a diverse array of feeding adaptations among interacting species. doi:10.1111/j.1439-0485.2010.00419.x

inhabiting coastal ecosystems (Beyst et aí 1999; Darna- Introduction ude et aí 2001; Mariani et aí 2002; Platell et aí 2006; Despite extensive habitat destruction, pollution and long Russo et aí 2008). Juveniles of flatfish species (Order term irresponsible exploitation regimes (Lotze et aí Pleuronectiformes) are found in abundance in estuarine 2006), estuarine and coastal areas still retain a pivotal role and coastal fish assemblages worldwide, making them in aquatic production processes, conservation, resource good candidates for studies of resource partitioning. In use, economy and commerce. Most of such ‘transitional’ particular, European flounder ( Platichthys flesus L.) and habitats represent vital ‘nurseries’ for the juvenile stages plaice (Pleuronectes platessa L.) represent key species in of several commercially important fish (Beck et aí 2001; cold temperate areas in the Northeast Atlantic and the Kraus & Secor 2005), providing abundant food resources, latter especially sustains a very valuable commercial fish shelter and favourable conditions for rapid growth ery. After hatching, juvenile flounder and plaice use (Haedrich 1983). Yet, estuaries, lagoons and tidal flats are shallow nursery grounds during the first months of life, also characterised by an unparalleled spatial and temporal between March and October (Russell 1976; Gibson 1994; environmental heterogeneity (Elliott & Quintino 2007), Raffaelli & Hawkins 1996), exhibiting at this time a high which necessarily poses severe adaptive challenges to the degree of spatial overlap. organisms that spend at least part of their life cycle Despite the reported similarity in diet (Gibson 1994; therein. Piet et aí 1998), most studies suggest that sympatric pla One main ecological challenge is to be able to parti ice and flounder segregate trophic niches (Aarnio et aí tion resources in a densely populated and variable envi 1996; Beyst et al. 1999; Amezcua et al. 2003; Andersen ronment. Similar species that occupy the same habitat at et al. 2005; Russo et al. 2008). Most comparative studies the same time will likely consume slightly different prey emphasise inter-specific variation and competition in a to minimise niche overlap (Schoener 1974), and a num specific spatial context - sometimes going as far as pro ber of studies have shown this to be the case for fish viding mechanistic explanations for the observed variation

96 Marine Ecology32 (Suppl. 1 ) (2011 ) 96-101 © 2011 Blackwell Verlag GmbH Mariani, Boggan & Balata Food resource use in plaice and flounder in diet (Bels & Davenport 1996; Gronkjaer et al. 2007; Sampling Russo et al. 2008) - but tend to overlook the overall role of coastal environmental heterogeneity in influencing the Juveniles of plaice and flounder were collected using a adaptive responses of species. 10-m long, 4-m high, hand-dragged seine (2-mm mesh), Here we compare the feeding habits of sympatric between June and July 2008, which corresponds to the flounder and plaice in two different estuarine environ period of maximum abundance and activity of 0-group ments in the Irish Sea and we test the hypothesis that flatfishes in inshore tidal areas in the Northeast Atlantic local conditions will affect the dietary patterns in these (Gibson 1994; Raffaelli 8c Hawkins 1996). In each locality, species, resulting in spatial variations in their trophic specimens were collected once a week, over 4 weeks, dur inter-relationships. ing daytime, at high and low tide, to maximize the repre sentation of the sample for both species. Specimens were counted each time, and a random subsample was sacri Material and Methods ficed using an overdose of phenoxyethanol and later Study area placed in a 5% formalin solution for preservation and identification. The study was carried out in two inshore tidal inlets in the Irish Sea: North Bull Island (53°22' N, 6°07' W), in Dublin Bay, and Wexford Harbour (52°20' N, 6°27' W), Data processing and analysis at the southernmost end of the Irish Sea basin (Fig. 1). All preserved individuals were measured with a calliper North Bull Island has previously been shown to have (fork length, LF, to the nearest mm) and their stomach higher average salinity (37 psu) and lower average tem contents emptied into a Petri dish and observed under a perature (17 °C) than Wexford Harbour (27 psu and stereomicroscope. Prey items were classified to the lowest 19 °C) throughout the year (Craig et al. 2008). Both taxonomic level possible and recorded as present or localities are characterized by sandy/muddy bottoms, absent. which remain completely exposed during low tide. Within The multivariate dataset was explored and represented each location, two stations ~500 m apart were chosen for using a two-dimensional unconstrained principal coordi sampling.

North Bull ¿*£7 r / C Island

IRELAND Dublin

N. Bull Island

Plaice S1 Plaice S2 Flounder S1 Flounder S2

Wexford H

Wexford Fig. 1. Map of study areas with bar plots Harbour representing the recorded numbers of plaice and flounder (annotations S1 and S2 refer to Plaice S1 Plaice S2 Flounder S1 Flounder S2 the two stations within each location).

Marine Ecology32 (Suppl. 1) (2011) 96-101 © 2011 Blackwell Verlag GmbH 97 Food resource use in plaice and flounder Mariani, Boggan & Balata nate ordination (PCO) based on Gower’s dissimilarity Results measure (Gower 1966). Permutational multivariate analy sis of variance (PERMANOVA; Anderson 2001) was then A total of 1144 flounder and 810 plaice were collected. used to analyse the variation in feeding habits of plaice Llounder were dominant in Wexford Harbour (975 versus and flounder between and within the two different estua 184) and plaice in North Bull Island (626 versus 169) rine habitats. The experiment consisted of a three-way (Fig- !)• design with ‘Species’ (‘Spe’, two levels) as a fixed factor, A total of 202 fish were examined for stomach con ‘Locality’ (‘Loc’, two levels) as a random and crossed fac tents: 50 flounder (31 + 19) and 50 plaice (30 + 20) from tor, and ‘Station’ (‘Sta’, two levels) as a random factor two stations in North Bull Island, 50 flounder (30 + 20) nested in ‘Locality’. Pairwise tests were also conducted to and 52 plaice (36 + 16) from the two stations in Wexford pinpoint the levels responsible for significant interactions. Harbour. Pish size ranged between 22 and 127 m m and Leeding was also examined by comparing the variation no differences were observed between species and loca of most abundant taxa, which were ‘pooled’ into taxo- tions (ANOVA: F = 1.42, df = 3, P = 0.24) and none of nomical/ecological guilds as follows: ‘Copepods’ (com them had an empty stomach. Twenty-one different prey prising Harpacticoida, Cyclopoida and Calanoida), items were identified, with mysids being generally the pri ‘Worms’ (comprising Polychaeta, Oligochaeta and Nema mary resource for flounder and polychaetes being the toda), ‘Amphipoda + Isopoda’, and ‘Other Malacostraca’ most abundant prey in plaice (Table 1). (comprising Mysidacea, Brachyura and Caridea). These PCO ordination of sample centroids showed a more data were analysed by univariate ANO VA, applying the clumped distribution for flounder and a greater scattering same design described for PERMANOVA, and after test of the plaice data points (Pig. 2). PERMANOVA detected ing for homogeneity of variance using the Cochran’s significant differences for both the interactions: Spe*Loc C-test (Underwood 1997). Student-Newman-Keuls and Spe>fSta(Loc), as well as for the effect ‘Station(Loc)’, (SNK) tests were used for post hoc multiple pairwise revealing the dependence of locality-specific variation in comparisons. governing feeding interactions between these species

Table 1. Frequency of occurrence of all prey Items found In the stomach contents of plaice (P) and flounder (F) from Bull Island (B) and Wexford Harbour (W) at stations 1 and 2.

FB1 (19) FB2 (31) FW1 (30) FW2 (20) PB1 (30) PB2 (20) PW1 (16) PW2 (36)

Harpacticoida 0.11 0.19 0.2 0.65 0.9 0.2 0 0.06 Cyclopoida 0 0.1 0 0 01 0.2 0 0 C alanoida 0 0 0 0 0.03 0 0 0 Polychaeta Err. 0.05 0.1 0 0.15 0.47 0.55 0.75 0.56 Polychaeta Sed. 0.21 0.03 0.2 0.25 0.03 0.35 0.18 0 A m phipoda 0.53 0.48 0.07 0.2 0.27 0.25 0.19 0.31 Isopoda 0.1 0.1 0.03 0 0.03 0.1 0 0.08 Bivalvia 0 0.6 0.03 0 0.2 0.4 0 0 O stracoda 0 0.3 0.13 0 0.03 0 0 0.17 eggs 0 0.3 0.03 0.5 0.07 0.1 0 0.06 N em atoda 0 0 0 0 0 0 0 0.06 Brachyura 0.16 0.03 0.03 0.25 0 0 0 0 Caridea 0 0 0.03 0 0.50 0 0 0 Mysidacea 0.63 0.23 0.57 0.6 0.1 0 0 0 Oligochaeta 0 0 0 0 0.03 0.05 0 0 Holoturldae 0 0 0 0 0 0 0.06 0 algae 0.1 0.13 0.03 0 0.27 0.2 0.12 0 Hydrozoa 0.05 0 0 0 0 0 0 0.06 Cirripedia 0 0 0 0 0 0 0.06 0 fish 0 0.03 0 0 0 0 0 0 Tunicata 0 0 0.03 0 0 0 0 0 unidentified 0 0 0.03 0 0 0 0 0

Numbers In brackets In the column headers refer to sample size. Values In bold represent 'Important' (>25%) or 'dominant' (>50%) prey Items, according to Albertlne-Berhaut (1973).

40 1.2 Copepods Amphipoda + Isopoda

1.0 T

0.8

A FB1 0.6 PW1 • F W 1 0.4 O O PW2

0.2 0 FB2 FW2 0.0 1 i B-1 B-2 W-1 W-2 B-1 B-2 W-1 W-2 PB2 1.2 - 1,21 Other malacostraca “Worm s”

û - - 2 0 1.0 1.0 -

0.8 0.8-

A PB1 0.6 0 .6 - -4 0 -4 0 -20 0 20 40 0.4 0.4- PC01 (51.3% of total variation) 0.2 0 .2 -

Fig. 2. Ordination plot of sample centroids Inferred with Principal 0.0 0 .0 - i i i coordinate analysis. F is for flounder (black), P is for plaice (grey), B is B-1 B-2 W-1 W-2 B-1 B-2 W-1 I W-2 for 'North Bull Island' (triangles) and W is for 'Wexford Harbour' Flounder = i Plaice (circles). Fig. 3. Frequencies of four main food categories In plaice and floun der from two estuaries. Results of univariate ANOVA tests are In the Table 2. Results summary table for PERMANOVA procedure con text. ducted on presence/absence stomach content data. Values in bold are significant with a = 0.05. source df MS pseudo-F P-value Discussion Spe 1 68,768 2.215 0.114 The study of the feeding habits and resource partitioning Loc 1 20,513 2.073 0.081 in closely related fish can be very useful to understand Sta (Loc) 2 9171.8 3.400 0.001 Spe*Loc 1 31,029 2.612 0.041 the flows of energy across the food web (Darnaude, 2005) Spe*Sta(Loc) 2 11,756 4.358 0.001 and provide important insights into the trophic flexibility residual 191 2697.5 of interacting species (Mariani et aí 2002; Platell et aí total 198 2006; Russo et al. 2008). Yet, the quantification of diet overlap or niche segregation - even when supported by (Table 2). Pairwise tests conducted on both interactions robust explanations of the processes underlying the pat showed consistent significant differences between species terns - may still only provide a very narrow picture of within stations but only plaice was shown to vary its diet the true flexibility of a species’ trophic ecology. significantly between locations. This study expands the analysis of resource partitioning Univariate analyses were also informative in describing between two common flatfish, plaice and flounder, by diet variation between and within species (Fig. 3). Signifi taking into consideration the naturally high environmen cant differences between species were detected in the cate tal heterogeneity of estuarine habitats, and performing gory ‘Worms’ (F = 32.5, P = 0.01). The interactions diet comparisons in two different estuarine habitats. Spe*Loc for ‘Other Malacostraca’ (F = 42.9, P = 0.02) and Wexford Harbour was found to be dominated by Spe*Sta (Loc) for ‘Copepods’ (F = 4.3, P = 0.01) were also flounder, whereas North Bull Island showed a predomi significant, and the Spe*Loc interaction for both ‘Cope nance of plaice. This is probably linked to the lower salin pods’ (F = 10.7, P = 0.08) and ‘Amphipoda + Isopoda ities observed year-round in Wexford (Craig et aí 2008) (F = 14.4, P = 0.06) were only marginally above the proba and the well-known pronounced preference of flounder bility threshold. SNK tests confirmed significant differences for brackish environments. This species appeared to exhi between plaice and flounder across all stations in terms of bit a more spatially homogeneous food spectrum ‘Copepods’, but only in Wexford for ‘Other Malacostraca’. (clumped scatter of data in Fig. 2) relative to plaice,

Marine Ecology32 (Suppl. 1 ) (2011 ) 96-101 © 2011 Blackwell Verlag GmbH 99 Food resource use in plaice and flounder Mariani, Boggan & Balata which exhibits remarkable diet changes between the two Conclusions study locations (wider distribution of data in Fig. 2). Univariate tests on the most abundant prey items We have shown that the patterns of niche overlap and (Fig. 3) illustrate well the extent and nature of diet varia resource partitioning between plaice and flounder in estu tion between and within plaice and flounder. Plaice seems arine habitats vary depending on the specific system stud to be the most efficient forager of polychaetes and other ied. This strengthens the view that estuaries, lagoons and worm-like prey, whereas flounder consistently consumes a other transitional habitats may represent a heterogeneous greater amount of malacostraca, particularly mysids ‘mosaic’ of selective forces (Weinig & Schmit 2004), (Table 1). The frequency of different preys across floun which is crucial to the evolution of the life-histories of der samples is much more even than in plaice: for coastal marine fish (Mariani 2006) and perhaps influences instance, considerable frequencies of copepods, decapods the functioning of more ‘extended’ phenotypic traits and bivalves are found in the stomachs of plaice from (sensu Dawkins 1982), such as trophic interactions and North Bull Island, whereas virtually only polychaetes and community structure. amphipods are consumed in Wexford. One explanation Future studies should attempt to evaluate whether the may reside in the fact that Wexford is a flounder-domi observed trophic flexibility results entirely from pheno nated habitat, which might drive the less numerous plaice typic plasticity (Gronkjaer et aí 2007) or also to some to select only preys, such as polychaetes and amphipods, extent from genomic adaptation. that are not ‘preferred’ by flounder, as indeed appears to be the case in Wexford Harbour. Intra-specific competi Acknowledgements tion may also play a role, prompting plaice to select a wider range of prey in the location where it is more fre The study was based on data collected as part of CB’s quent and dominant {i.e. North Bull Island). final year project, internally funded by the UCD School On the other hand, flounder does not seem to go of Biology and Environmental Science. We would like to through the same ‘diet switch’, when the two estuaries thank Debbi Pedreschi for help during sampling and the are compared. The only prey categories affected are am editors and two anonymous reviewers for their valuable phipods and isopods, which show a low frequency in suggestions. Wexford (Fig. 3), although this is counterbalanced by the intense consumption of other malacostraca (espe References cially mysids). Without a parallel investigation on the abundance of potential prey (Wouters & Cabral 2009), Aarnio K., Bonsodorff E., Rosenback N. (1996) Food and feed it remains difficult to assess to what extent the results ing habits of juvenile flounder Platichthys flesus (L.) and may be influenced by differential availabilities of turbot Scophthalmus maximus (L.) in the Aland archipelago, resources; however, the present data unambiguously northern Baltic Sea. 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