Size- and depth-dependent variation in habitat and diet of the common carp (Cyprinus carpio)
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1 Aquat.sci.63 (2001) /01/ $ /0 Birkhäuser Verlag, Basel, 2001 Aquatic Sciences Size- and depth-dependent variation in habitat and diet of the common carp (Cyprinus carpio) Emili García-Berthou Departament de Ciències Ambientals and Institut d Ecologia Aquàtica, Universitat de Girona, E Girona, Catalonia, Spain, caegb@fc.udg.es Key words: Exotic fish, common carp, Cyprinus carpio, diet, Lake Banyoles, Spain. ABSTRACT The habitat and diet variation of the common carp (Cyprinus carpio) were studied in Lake Banyoles (Catalonia, Spain). Carp was the second most abundant species offshore and used more the littoral in spring and deep bottoms in winter. The diet of carp was based on detritus, amphipods (Echinogammarus sp.), phantom midge larvae (Chaoborus flavicans), diatom mucilages, and plant debris. Amphipods and phantom midge larvae were much more important in diet than previous studies found, because of their greater availability in this lake. Among the carp inhabiting deep waters, there was size-dependent variation in diet, with smaller carp selecting more meiobenthos (cladocerans, ostracods, and small chironomids) and larger carp preying on profundal macrobenthos (phantom midge larvae and large chironomids). Roach (Rutilus rutilus) and carp dominated in abundance the non-littoral zone of the lake and showed resource partitioning, with roach being a more efficient zooplanktivore and carp being more able to prey on hard material (plant seeds, mollusks, and ostracods). Introduction The common carp (Cyprinus carpio) is probably the first fish species whose distribution was widely extended by human introduction, since it was introduced by the Romans from the River Danube throughout Europe (Balon, 1995). It is the third most frequently introduced species world-wide (Welcomme, 1992) and is almost cosmopolitan nowadays. The common carp also accounts for the world s second highest farmed fish production, mainly from polyculture in Asia (Milstein, 1992), and the production of ornamental varieties is even more important in monetary value (Balon, 1995). Despite the common carp s ubiquity and economic importance, little is known of its ecology in natural systems (Crivelli, 1981). The functional morphology of its feeding apparatus (Sibbing, 1982; Sibbing et al., 1986; Sibbing, 1988) and the impact of this cyprinid species on macrophytes and water quality (Crivelli, 1983; Richardson et al., 1990; Wilcox and Hornbach, 1991; Lougheed et al., 1998) have been well
2 Diet of common carp 467 documented. Yet most diet studies have been done on fish culture ponds or rice fields (Crivelli, 1981; Sibbing, 1982; Chapman and Fernando, 1994; Michel and Oberdorff, 1995). Diet studies in deep, natural lakes, in western Europe, and of large carp are almost non-existent (see synopses of carp diet studies in Sarig, 1966; Michel and Oberdorff, 1995). I studied such a population of carp in Lake Banyoles, the second largest lake in the Iberian Peninsula. This study is part of comprehensive research into the feeding ecology of the entire fish assemblage of the lake (García-Berthou, 1994, 1999a, 1999b; García- Berthou and Moreno-Amich, 2000b, 2000c). The lake is dominated by exotic species, particularly largemouth bass (Micropterus salmoides) and pumpkinseed sunfish (Lepomis gibbosus) in the littoral zone and roach (Rutilus rutilus) and carp offshore (García-Berthou and Moreno-Amich, 2000a). The goal of the research is to assess the ecological role of the exotic species. In this paper, I analyse the habitat and diet of a carp population introduced into a Mediterranean lake and compare it with previous studies. Largely unknown patterns of sizeand depth-dependent variation in habitat and diet of carp are reported. The resource partitioning between roach and carp, the most common fish offshore, is described. Materials and methods Study area Lake Banyoles, situated at 42 7 N, 2 45 E and 172 m above sea level in Catalonia (Spain), is a karstic lake consisting of six basins (see bathymetric map in Moreno- Amich and García-Berthou, 1989; García-Berthou, 1999a). The mainly subterranean water sources and high calcium concentration restrict the lake s productivity. Although usually considered oligotrophic because of the low nutrient concentration and phytoplankton biomass, it is rather mesotrophic based on its primary production and its benthic community. Information is available on its morphometry (Moreno-Amich and García-Berthou, 1989), hydrology (Roget et al., 1993), bacterioplankton (Garcia-Gil et al., 1996), phytoplankton (Planas, 1973), zooplankton (Miracle, 1976), and non-littoral zoobenthos (Rieradevall, 1991). Selected features of the lake are: surface area, ha; mean depth, 14.8 m; water temperature, 7 26 C; and conductivity, ms cm 1. The history of introductions and the structure and habitat partitioning of the current fish assemblage are described by García-Berthou and Moreno- Amich (2000a). The littoral zone of Lake Banyoles is dominated in abundance by largemouth bass and pumpkinseed sunfish, and the rest of the lake by roach and common carp. The most common native species are the freshwater blenny (Salaria (= Blennius) fluviatilis) and chub (Leuciscus cephalus). I have published elsewhere the habitats and diets of roach (García-Berthou, 1999a), pumpkinseed sunfish (García-Berthou and Moreno-Amich, 2000b), mosquitofish (Gambusia holbrooki) (García-Berthou, 1999b), and rudd (Scardinius erythrophthalmus) (García-Berthou and Moreno-Amich, 2000c) in the lake during the same period.
3 468 García-Berthou Field and laboratory methods Fish from Lake Banyoles were sampled quarterly from December 1990 to November Sampling was by boat electrofishing in the littoral zone and with trammel nets (stretched mesh size: inner net, 2 cm; outer, 12.5 cm). Constant sampling effort was used in different seasons and depths. Most of the carp were captured with trammel nets (see Results). Trammel net sizes were 6 2 m in the littoral (i.e. set at 0 2 m deep) and m in the rest of the lake. Limnetic trammel nets were placed at 5, 10, and 15 m of depth and bottom trammel nets at 10 and 20 m (or 15 m for shallower basins). Nets were set for 24 h on six consecutive days. All captured fish were stored immediately on ice and later frozen. Resource availability was not directly measured because the zooplankton (Miracle, 1976) and benthos (Rieradevall, 1991) had already been studied. Our sampling points (limnetic and bottom trammel nets) matched those of the previous benthos study and are detailed elsewhere (García-Berthou, 1994, 1999a). In the laboratory, fish were measured (fork length to the nearest mm), eviscerated, and weighed (to the nearest 0.1 kg). The entire gut was preserved in 70% ethanol until analysis. The gut contents of all carp (n = 50) were examined under a dissecting microscope. Prey were sorted usually to the species or genus level. First, I tried to identify all food categories present and, in particular, to detect rare larger prey, which were separated. A subsample of about 10% was then taken, after homogenisation, for more precise analysis. Prey were counted and weighed to the nearest 0.1 mg after excess moisture was removed by blotting. Data analyses Percent number (% number), percent biomass (hereafter, % B), and frequency of occurrence were used to estimate the dietary importance of each food category. Percent number is the number of individuals of a prey type divided by the total number of individuals and expressed as a percentage, after pooling the gut contents of all fish. Percent B is the equivalent measure for biomass data. Frequency of occurrence is the percentage of guts where a food category was present. To describe prey importance and feeding strategy, I used Costello s (1990) graphical method, i.e. a plot of % number or % B with frequency of occurrence. The most important prey are closer to the top right corner. The other diagonal corresponds to feeding strategy; prey with low occurrence but dominant by number or biomass correspond to some sort of specialisation and are closer to the top left corner. Correspondence analysis (CA) was used to describe the main sources of diet variation (ter Braak, 1987). This technique has two main advantages over the conventional procedures of dietary data analysis: (1) instead of pooling food categories a priori (often according to taxonomic rather than ecological criteria), CA groups similar food categories based on common occurrence (Graham and Vrijenhoek, 1988); and (2) relevant factors are not selected a priori by the researcher; instead, CA identifies the dimensions explaining the highest proportion of variation, including measured and unmeasured factors (see also García-Berthou, 1999a). Although CA is not generally used for dietary data, it is common in the analysis of
4 Diet of common carp 469 community ecology data (ter Braak, 1987). CA generally performs better than factor analysis (principal component analysis) for community data sets, particularly for long gradients (Gauch, 1982; ter Braak, 1987). Four food categories were excluded from the CA because they dominated the first solutions as outliers due to very low occurrence but relatively high number or biomass. Empty guts (only 3 fish) are intrinsically excluded by CA. The matrix analysed thus consisted of 46 fish and 66 food categories. Analysis of covariance (ANCOVA) was used to interpret the dimensions in terms of the measured characteristics of the samples (see e.g., ter Braak, 1987: 132). The fish CA scores were the response variables, season and basin were factors, and fish length and capture depth were covariates. The homogeneity-of-slopes assumption of the standard ANCOVA (García-Berthou and Moreno-Amich, 1993) was satisfied for both dimensions (P > 0.05). Variation in carp catches was analysed with G-tests for goodness of fit and for independence. Size structure was analysed by ANCOVA. Fish length was log-transformed because homoscedasticity and linearity were clearly improved. All data analyses were performed with SPSS for Windows 7.5. Results Habitat use and size structure Of the 1,403 individuals of 11 fish species captured, only 50 were carp. However, its relative abundance increased with depth and it was the second most abundant species offshore (Fig. 1). There was no significant seasonal variation in total catches of carp (Fig. 2; G 3 = 2.8, P = 0.42). Carp were captured at all depths, ranging from 0 to 20 m, but significantly more in the littoral in spring and in deep waters in winter (Fig. 2; G 6 = 13.3, P = 0.04). Mean fork length was 476 mm (SE = 7.7 mm, n = 50), with a range of mm. Although most carp were large, there was a significant Figure 1. Relative abundance (percentage of catches) of common carp, roach, and the rest of fish species by depth in Lake Banyoles. Total fish catches by depth are given on the right
5 470 García-Berthou Figure 2. Length-frequency distribution of common carp in Lake Banyoles by season and depth tendency of larger individuals to use deeper habitats, mostly in winter (ANCOVA test of homogeneity of slopes of fork length with depth and season, depth season: F 3, 42 = 3.4, P = 0.03) (Fig. 2). There was also some seasonal variation in mean length (ANCOVA, season: F 3, 42 = 4.1, P = 0.01). Most of the carp (45 of 50) were captured with trammel nets and constant sampling effort was used throughout the different depths and seasons, so these patterns were not due to differential sampling selectivity.
6 Diet of common carp 471 Carp food Carp food mainly consisted of detritus, plant material (including debris, diatoms, and seeds), amphipods (Echinogammarus sp.), and phantom midge larvae (Chaoborus flavicans) (Table 1, Fig. 3). The relationship between % B and frequency of occurrence already distinguished a few food categories, namely amphipods, phantom midge larvae, and diatom mucilages, which were more important by biomass because they were larger than most other prey (Fig. 3). Phantom midge larvae were mostly consumed by carp from basin IV (see map in Moreno-Amich and García- Berthou, 1989; García-Berthou, 1999a), where they are more common because of greater summer anoxia (Rieradevall, 1991). Diet variation For correspondence analysis of prey number, the first two dimensions were considered because they were easy to interpret and globally explained 26.1% of the variance (eigenvalues = and 0.926). Most of the littoral prey (such as the freshwater shrimp Atyaephyra desmaresti, amphipods, trichopteran larvae, and snails) had positive scores for the first dimension (hereafter, D1), whereas prey with negative scores mainly consisted of profundal benthos, namely phantom midge larvae, and chironomid larvae (Chironomus spp., Procladius sp., and Stictochironomus maculipennis) (Fig. 4). Chironomus and Procladius are the most abundant chirono- Table 1. Diet of common carp in Lake Banyoles: percent number, percent biomass (% B), and frequency of occurrence of the main food components. Number of guts analysed = 50; total number of prey in the gut contents = 255,977; total biomass = g Food category Percent % B Frequency of number occurrence Detritus Algae Plant debris Dicotyledoneae leaves Plant seeds Digested material Alona affinis Candona sp Echinogammarus sp Other Crustacea Chaoborus flavicans larvae Procladius sp. larvae Chironomus spp. larvae Other nematoceran larvae Other Insecta Mollusca Other invertebrates Fish eggs
7 472 García-Berthou Figure 3. Relationship between % Biomass and frequency of occurrence of the food categories in carp diet. Plot based on Costello s (1990) method. The most important food categories are detailed. l. = larvae Figure 4. Correspondence analysis of gut contents (prey number) of common carp: food category scores for the first and second dimensions. l. = larvae, p. = pupae, a. = adults
8 Diet of common carp 473 mids in the profundal benthos of Lake Banyoles and phantom midge larvae dominate the most hypoxic basins (Rieradevall, 1991). D1 scores were not significantly related to fish length (F 1, 27 = 0.51, P = 0.48) or season (F 3, 27 = 1.35, P = 0.28) but to capture depth (F 1, 27 = 13.0, P = 0.001), so D1 showed depth-dependent variation in diet. Prey with positive scores for the second dimension (hereafter D2) also consisted of profundal benthos but were smaller, corresponding to meiobenthos such as cladocerans (Leydigia acanthocercoides) and ostracods (Cypria ophtalmica and Candona sp.) (Fig. 4). Small chironomid species (Cryptochironomus sp., Cladotanytarsus sp., Microchironomus tener, and Tanypus sp.) displayed intermediate D2 scores. Unlike D1, D2 was not significantly related to capture depth (F 1, 27 = 2.28, P = 0.14) or season (F 3, 27 = 0.68, P = 0.58) but to fish length (F 1, 27 = 16.8, P < ). Therefore, D2 showed size-dependent variation in diet, with smaller carp selecting more meiobenthos and larger carp preying on profundal macrobenthos. Discussion Diet of carp Common carp are considered omnivorous fish that feed on chironomids, tubificids, larger zooplankton and zooperiphyton (Sibbing, 1988) but the bulk of its diet consists of detritus (Chapman and Fernando, 1994; Michel and Oberdorff, 1995). Michel and Oberdorff (1995) reported that chironomids and mollusks generally are the most important animal prey of carp (see also Prejs, 1973; Guziur, 1976). In Lake Banyoles, detritus was also dominant but chironomids and mollusks were less important. In contrast, amphipods and phantom midge larvae were by far the most consumed invertebrates, due to their higher availability in the lake (Rieradevall, 1991). The consumption of plant material (including fresh plants and debris) by carp in Lake Banyoles (% B = 10.0) was lower than by rudd (% B = 31.6) and chub (% B = 17.5). This agrees with the low efficiency of carp feeding on macrophytes (Sibbing, 1988) and supports the view that carp s impact on macrophytes is not through direct predation but through uprooting (Crivelli, 1983; Powles et al., 1983). Carp captured in deep bottoms of Lake Banyoles showed size-dependent variation in diet, with smaller individuals preying on meiobenthos (cladocerans, ostracods) and the largest carp preying on macrobenthos (phantom midge larvae and large chironomids). As far as I know, this pattern has not been reported before but is consistent with ecomorphological studies. Carp of cm standard length are able to retain algae and large zooplankton and detritus (> 250 µm) with their branchial sieve (Sibbing et al., 1986), but the efficiency of this retention diminishes with carp size (Sibbing, 1988). Therefore, carp feeding is more selective, even in deep waters, than is usually realised (see also Sibbing, 1988) and the knowledge of carp size structure is essential to understand its impact on benthic communities.
9 474 García-Berthou Figure 5. Relationship between the % Biomass of the different food categories in roach and carp diets in Lake Banyoles. l. = larvae Resource partitioning with roach Roach and carp dominate in abundance the non-littoral zone of Lake Banyoles (Fig. 1). There is a significant similarity between the diets of roach (see García- Berthou, 1999a) and carp (this study) (r = 0.966, n = 119, p < ; Fig. 5). The diets of both fish species are mainly based on detritus, plant material, and amphipods but show a clear resource partitioning. In contrast to carp, roach are quite zooplanktivorous, mostly preying on the cladoceran Daphnia longispina (Fig. 5). Other prey more linked to the water surface such as nematoceran pupae (including C. flavicans) and exuviae are also less important in carp than in roach. Large carp (> 30 cm), such as those of Lake Banyoles, are less efficient zooplanktivores due to the larger mesh width of their branchial sieve (Sibbing, 1988). Zooplankton seems to be more consumed by carp in artificial, eutrophic ponds (Sarig, 1966) or reservoirs. Another difference with roach is that hard material (plant seeds and debris, mollusks such as Physella acuta and Pisidium spp., and ostracods such as Candona sp. and C. ophtalmica) are more important in carp diet (Fig. 5). This is consistent with the high efficiency of carp processing this kind of food with their powerful pharyngeal jaws (Sibbing, 1988; Tucker et al., 1996). The high occurrence of seeds is characteristic of carp diet (Sarig, 1966; Crivelli, 1981; Chapman and Fernando, 1994; Michel and Oberdorff, 1995).
10 Diet of common carp 475 ACKNOWLEDGEMENTS I am grateful to everybody who assisted in field and laboratory work, especially Q. Paredes and D. Boix. Several people kindly helped with taxonomic identification, namely F. Còrdoba, X. Espadaler, D. García de Jalón, N. Prat, M. Rieradevall, and N. Vicens. The manuscript greatly benefited from the comments by three anonymous reviewers. This study was financially supported by the Autonomous Government of Catalonia (FI fellowship and CIRIT grant AR89) and the Town Council of Banyoles, and received an award (Àngel Arisó) from the Institute of Catalan Studies. REFERENCES Balon, E.K., Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers. Aquaculture 129: Chapman, G. and C.H. Fernando, The diets and related aspects of feeding of Nile tilapia (Oreochromis niloticus L.) and common carp (Cyprinus carpio L.) in lowland rice fields in northeast Thailand. Aquaculture 123: Costello, M.J., Predator feeding strategy and prey importance: a new graphical analysis. J. Fish Biol. 36: Crivelli, A.J., The biology of the common carp, Cyprinus carpio L. in the Camargue, southern France. J. Fish Biol. 18: Crivelli, A.J., The destruction of aquatic vegetation by carp. A comparison between southern France and the United States. Hydrobiologia 106: García-Berthou, E., Ecologia alimentària de la comunitat de peixos de l Estany de Banyoles, Ph.D. dissertation, Univ. of Girona, Girona, Spain, 288 p. García-Berthou, E., 1999a. Spatial heterogeneity in roach (Rutilus rutilus) diet among contrasting basins within a lake. Arch. Hydrobiol. 146: García-Berthou, E., 1999b. Food of introduced mosquitofish: ontogenetic diet shift and prey selection. J. Fish Biol. 55: García-Berthou, E. and R. Moreno-Amich, Multivariate analysis of covariance in morphometric studies of the reproductive cycle. Can. J. Fish. Aquat. Sci. 50: García-Berthou, E. and R. Moreno-Amich, 2000a. Introduction of exotic fish into a Mediterranean lake over a 90-year period. Arch. Hydrobiol. 149: García-Berthou, E. and R. Moreno-Amich, 2000b. Food of introduced pumpkinseed sunfish: ontogenetic diet shift and seasonal variation. J. Fish Biol. 57: García-Berthou, E. and R. Moreno-Amich, 2000c. Rudd (Scardinius erythrophthalmus) introduced to the Iberian peninsula: feeding ecology in Lake Banyoles. Hydrobiologia 436: Garcia-Gil, L.J., X. Casamitjana and C.A. Abella, Comparative study of two meromictic basins of Lake Banyoles (Spain) with sulphur phototrophic bacteria. Hydrobiologia 319: Gauch, H.G., Multivariate analysis in community ecology, Cambridge Univ. Press, Cambridge, 298 pp. Graham, J.H. and R.C. Vrijenhoek, Detrended correspondence analysis of dietary data. Trans. Amer. Fish. Soc. 117: Guziur, J., The feeding of two year old carp (Cyprinus carpio L.) in a vendance Lake Klawój. Ekol. pol. 24: Lougheed, V.L., B. Crosbie and P. Chow-Fraser, Predictions on the effect of common carp (Cyprinus carpio) exclusion on water quality, zooplankton, and submergent macrophytes in a Great Lakes wetland. Can. J. Fish. Aquat. Sci. 55: Michel, P. and T. Oberdorff, Feeding habits of fourteen European freshwater fish species. Cybium 19: Milstein, A., Ecological aspects of fish species interactions in polyculture ponds. Hydrobiologia 231: Miracle, M.R., Distribución en el espacio y en el tiempo de las especies del zooplancton del lago de Banyoles. Monografías ICONA 5:
11 476 García-Berthou Moreno-Amich, R. and E. García-Berthou, A new bathymetric map based on echo-sounding and morphometrical characterization of the Lake of Banyoles (NE-Spain). Hydrobiologia 185: Planas, D., Composición, ciclo y productividad del fitoplancton del lago de Banyoles. Oecologia aquatica 1: Powles, P.M., H.R. MacCrimmon and D.A. MacRae, Seasonal feeding of carp, Cyprinus carpio, in the bay of Quinte Watershed, Ontario. Canadian Field-Naturalist 97: Prejs, A., Experimentally increased fish stock in the pond type Lake Warniak. IV. Feeding of introduced and autochthonous non-predatory fish. Ekol. pol. 21: Richardson, W.B., S.A. Wickham and S.T. Threlkeld, Foodweb response to the experimental manipulation of a benthivore (Cyprinus carpio), zooplanktivore (Menidia beryllina) and benthic insects. Arch. Hydrobiol. 119: Rieradevall, M., Ecologia i producció del bentos del llac de Banyoles, Ph.D. dissertation, Univ. of Barcelona, Barcelona, Spain, 223 pp. Roget, E., J. Colomer, X. Casamitjana and J.E. Llebot, Bottom currents induced by baroclinic forcing in Lake Banyoles. Aquat. sci. 55: Sarig, S., Synopsis of biological data on common carp Cyprinus carpio (Linnaeus), 1758 (Near East and Europe). FAO Fish. Synops Sibbing, F.A., Pharingeal mastication and food transport in the carp (Cyprinus carpio L.): a cineradiographic and electromiographic study. J. Morph. 172: Sibbing, F.A., Specializations and limitations in the utilization of food resources by the carp, Cyprinus carpio: a study of oral food processing. Env. Biol. Fish. 22: Sibbing, F.A., J.W.M. Osse and A. Terlouw, Food handling in the carp (Cyprinus carpio): its movement patterns, mechanisms and limitations. J. Zool. 210: ter Braak, C.J.F., Ordination. In: R.H.G. Jongman, C.J.F. ter Braak and O.F.R. van Tongeren (eds), Data analysis in community and landscape ecology. Pudoc, Wageningen, pp Tucker, J.K., F.A. Cronin and D.W. Soergel, Predation on zebra mussels (Dreissena polymorpha) by common carp (Cyprinus carpio). J. Freshwater Ecol. 11: Welcomme, R.L., A history of international introductions of inland aquatic species. ICES mar. Sci. Symp. 194: Wilcox, T.P. and D.J. Hornbach, Macrobenthic community response to carp (Cyprinus carpio L.) foraging. J. Freshwat. Ecol. 6: Received 5 July 2000; revised manuscript accepted 13 November 2000.
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