Environmental biology of fishes, tập 93, số 1, 2012

Environ Biol Fish (2012) 93:1–12 DOI 10.1007/s10641-011-9881-4 Feeding ecology and prey preferences of a piscivorous fish in the Lagoa Peixe National Park, a Biosphere Reserve in Southern Brazil Fabiano Corrêa & Marlucy Coelho Claudino & Rodrigo Ferreira Bastos & Sônia Huckembeck & Alexandre Miranda Garcia Received: 17 June 2010 / Accepted: 27 June 2011 / Published online: 13 July 2011 # Springer Science+Business Media B.V 2011 Abstract We investigated the diet, feeding strategy, size-related dietary shifts and prey preferences of South American Hoplias aff malabaricus in an internationally recognized but poorly investigated Biosphere Reserve in southern Brazil Fish were caught between April 2008 and March 2009 using a variety of fishing gear The analysis of 113 individuals revealed a diet essentially composed of fish (16 species), particularly characid species (9) The diet became more diverse and contained larger fish prey with increasing predator size Feeding strategy analysis revealed a clear specialization towards the consumption of fish However, individuals did not prey upon particular prey species, instead opportunistically consuming many different fish species, which could be a strategy to avoid intraspecific competition Characid species were the most important prey, followed by poecillids A multi-gear sampling of the ichthyofauna revealed that these prey species were the most abundant (Characidae: 61.3%, Poeciliidae 18.8%) of the 14 fish families occurring at the study site, suggesting that the predator exploits the most abundant fish resources available rather than the rarer F Corrêa (*) : M C Claudino : R F Bastos : S Huckembeck : A M Garcia (*) Instituto de Oceanografia, Laboratório de Ictiologia, Universidade Federal de Rio Grande, Campus Carreiros, Caixa Postal 474, CEP 96.201-900 Rio Grande, RS, Brazil e-mail: correafecologia@yahoo.com.br e-mail: amgarcia@mikrus.com.br fish prey These findings suggest that potential topdown controls exerted by H aff malabaricus in this system follow specific food web pathways that seem to be mediated by the abundance of prey resources Keywords Diet Feeding strategy Size-related dietary shift Trahira Food niche Characins Introduction Piscivorous fish play an important role in the array of ecosystem services provided by ichthyofauna due to their regulation of prey populations and, therefore, their impact on trophic cascades (Helfman et al 2009) Such influences can have crucial effects on the functioning of aquatic ecosystems and the levels of biodiversity they sustain (Polis and Winemiller 1996; Mazzeo et al 2010) Temporal variations in predator abundance have a profound impact on not only the abundance of aquatic prey but also on adjacent terrestrial ecosystems via indirect interactions with terrestrial consumers (Hebert et al 2008) Studying the feeding ecology of piscivorous fish is, therefore, a key step towards understanding the processes driving biodiversity in aquatic ecosystems Such knowledge is critically relevant in conservation areas to guide managers and decision makers to cope with anthropogenic impacts, such as when exotic species threaten native ones (Zaret and Paine 1973) Lagoa Peixe National Park (LPNP) is a poorly investigated conservation area in the coastal plain of southern Brazil which harbors many diverse and productive aquatic fauna, including endangered fish species such as the annual fish Austrolebias minuano (Corrêa et al 2009) It was recognized as a Ramsar Site and a UNESCO Biosphere Reserve in 1993, largely due to its important ecological role as a stopover site for migratory shorebirds in South America (Tagliani 1995) Despite the importance of the LPNP importance for conservation, no prior information on fish trophic ecology or aquatic food web structure is available for this unique ecosystem The most abundant piscivorous fish in the freshwater wetlands of the LPNP is the South American Hoplias aff malabaricus (Bloch, 1794) (Loebmann and Vieira 2005) This perch-like piscivore of the Erythrinidae family is distributed from Costa Rica (Central America) to Southern South America (Argentina) and is well known for having a strong top-down structuring role on trophic food webs of lentic aquatic systems (Winemiller 1989; Mazzeo et al 2010) Although it is well adapted to lentic environments, it is also found in small and large rivers, especially in pools with abundant marginal vegetation It is cryptically colored and captures its prey by ambush and is active mainly at night (Loureiro and Hahn 1996) It is considered a top predator with trophic levels ranging from 2.4 to (Garcia et al 2006; Rodríguez-Graña et al 2008) Mesocosm experiments revealed that H aff malabaricus can exert a strong control on planktivorous fish with cascading effects on chlorophyll a, water turbidity and zooplankton abundance (Mazzeo et al 2010) These authors recommended, however, that additional studies be carried out in whole-lake systems because the simplified conditions and small scale of mesocosm experiments hinder direct extrapolation Also, the high complexity of the food web and spatial heterogeneity of natural aquatic systems in subtropical and tropical regions represent additional constraints and should be investigated However, prior studies on the diet and feeding behavior of H aff malabaricus have been restricted to streams and river flood plains, with no known studies on subtropical freshwater wetlands For example, field studies conducted on streams and river flood plains have shown that small fish usually comprise the main prey of H aff malabaricus, although invertebrates, especially insects, vegetation remains and organic detritus can also be found in the stomach contents of H aff Environ Biol Fish (2012) 93:1–12 malabaricus (Loureiro and Hahn 1996; Carvalho et al 2002; Peretti and Andrian 2008; Corrêa and Piedras 2009) Size-related diet shifts also occur, with small juveniles feeding primarily on invertebrates, while subadults and adults are piscivorous (Winemiller 1989) However, these prior studies did not unambiguously show the fish prey preferences of the H aff malabaricus under natural conditions because the authors did not carry out a concomitant evaluation of fish prey availability in the study site Considering the crucial role that H aff malabaricus can have on aquatic food webs and the lack of information about its feeding ecology on subtropical wetlands, the present study investigates its diet, feeding strategy and size-related dietary shifts in a wetland located within an important conservation area in southern Brazil Also, based on a concomitant multi-gear sampling of the ichthyofauna in the study site, our work reveals the prey preferences of this top predator under natural field conditions Material and methods Study area The LPNP was created in 1986 to protect crucial feeding and resting sites for migratory birds along the coast of Rio Grande Sul state in southern Brazil (Fig 1) The LPNP has a humid subtropical climate, with mean temperatures ranging from 14.6°C in winter to 22.2°C in summer, and a mean annual temperature of 17.5°C The annual precipitation ranges from 1150 to 1450 mm yr−1, with an annual mean of 1250 mm yr−1 (Tagliani 1995) The main lagoon (locally known as ‘Lagoa Peixe’) consists primarily of shallow areas (200 mm) During the afternoon (from 1400 to 1700), one to two beach seine (9 m long, 2.4 m high, mesh size 13 mm wings and mm center) hauls were conducted in the open margins of the wetland, and three beam trawl (mouth of 1×1 m and size mesh of mm) hauls were employed in the vegetated margins of the wetland in each field trip The hauls conducted in the shallower waters (< 1.5 m) targeted mainly smaller individuals (< 200 mm) Some cryptic species were caught by dip net, which was used for approximately 15 in each field collection Aside from H aff malabaricus specimens, all fish species collected in the freshwater wetland using the previously mentioned types of fishing gear had their total size and numerical abundance recorded in order to assess the general relative abundance patterns of the ichthyofauna at the study site Such concomitant surveys of the abundance of the piscivorous fish and its fish prey populations were used to infer prey availability and patterns of resource exploitation by the H aff malabaricus population Immediately after their collection, individuals were euthanized and placed on ice Later, they were transported to the laboratory and stored in a freezer After thawing, each individual was weighed (Wt, g) and measured (total length, TL, mm) and, after being surgically dissected, had their stomach contents analyzed Food items were weighed on an analytical balance with an accuracy of 0.0001 g Food items found in the stomachs were identified to the lowest possible taxonomic level using a stereoscopic microscope When a food item was intact, its weight (g) and total length (TL, mm) were measured Food resources found in non-empty stomachs were quantified using the following parameters (Hyslop 1980): a) frequency of occurrence (%F), which represented the percentage of the total number of stomachs in which a particular food item was found, b) numerical abundance (%N), which represented the abundance in the percentage of a food item in relation to the total abundance of all stomachs c) weight (%W) of the item, which represented the weight (g) in percentage of a food item in relation to the total weight of all stomachs These parameters (%F,%N,% W) were combined into the Index of Relative Importance of Pinkas et al (1971) with the following formula: IRI ¼ %F»ð%N þ %WÞ, which was computed for each food item In order to assess the influence of hydrological changes in the study area, we analyzed diet and feeding ecology during periods of lower and higher precipitation In order to accomplish this, monthly mean values of rainfall (square root transformed) were analyzed with the Bray-Curtis similarity index in order to distinguish temporal rainfall patterns during the studied period Data were obtained in two meteorological stations located in cities (Rio Grande and Mostardas) near the study area (Fig 1) Differ- Environ Biol Fish (2012) 93:1–12 ences in diet composition between rainfall periods revealed by the cluster analysis were evaluated by MDS (Multi-Dimensional Scaling) and ANOSIM analyses using the Primer software package (Clarke and Gorley 2006) The feeding strategy of H aff malabaricus and the characteristics of their food niche were evaluated by the graphical method proposed by Amundsen et al (1996) In this approach, prey-specific abundance is defined as the percentage a prey taxon comprises of all prey items in only those predators in which the actual prey occurs according to the formula Pi =(∑Si/ ∑Sti) x 100, where Pi is the prey-specific abundance of prey i, Si the stomach content (weight) comprised of prey i, and Sti the total stomach content in only those predators with prey i in their stomach (Amundsen et al 1996) In the resulting diagram,% F values are arranged in the x-axis and Pi values on the y-axis The feeding strategy (generalist-specialist dichotomy) and the contribution of each individual to the food niche structure is obtained by analyzing the distribution of points (each one representing a food item) along a graph The population as a whole can be considered a specialist when the prey points are positioned at the top right of the graph, whereas their placement in the bottom half of the graph suggests a population with a generalist feeding behavior When points are located in the upper left corner of the diagram (i.e., with low%F and high Pi) they indicate individual opportunistic or specialist feeding behavior of some individuals within the predator population The relationship between the weight (g) and total length (TL, mm) of fish prey consumed and the total length (TL, mm) of the predator was evaluated with a nonlinear regression In the model calculation (PreyTL = a * exp b * PredatorTL), the algorithm of GaussNewton was used based on an iterative process using a convergence criterion of 1.0−6 and baseline values (‘seeds’) for the regression constant (a) and the regression coefficient (b) of and 0.01, respectively (Haimovici and Velasco 2000; Cantanhêde et al 2009) Size-related dietary shifts were also analyzed based on three size classes: 0–100, 101–200 and 201–350 mm TL, with 16, 20 and 18 individuals in each one, respectively Differences in the average total weight (g) of the food found in the stomach content of these three size classes were evaluated by the Kruskal-Wallis test (Zar 1994) Environ Biol Fish (2012) 93:1–12 Results Seasonal changes in rainfall Rainfall showed strong variation across months, with values ranging from 12.4 mm in November 2008 to 129.15 mm in August 2008 In general, the average rainfall was higher during the winter and summer (70.9 and 80.7 mm, respectively) than in the spring and autumn (19.9 and 38.3 mm, respectively) Cluster analysis applied to monthly rainfall values revealed (at 75% of similarity) two main groups (Fig 2a) The former were comprised of months with low precipitation (< 25 mm), whereas the later by months with moderate to high (25–100 mm) values (Fig 2b) Diet composition and seasonal changes A total of 113 individuals with sizes (TL) ranging from 26 to 364 mm had their stomach contents Fig Dendogram showing the similarity (Bray-Curtis index) among mean values of rainfall (square root transformed) in each month from April 2008 to March 2009 Data obtained from two meteorological stations located in the cities of Rio Grande and Mostardas (see map on Fig 1) The horizontal line denotes similarity at 75% (a) Mean values of rainfall during the low and moderate-high periods obtained in the cluster analysis (b) analyzed, and nearly half of them (52.1%) were empty The analysis of the food content of the nonempty stomachs revealed 20 items (Table 1) Fish were the most conspicuous items in the diet of H aff malabaricus and included 15 species belonging to distinct fish families Fragments of insects and plants were also found in the stomach contents, but they had comparatively lower contributions in terms of numerical abundance (%N) and biomass (%W) (Table 1) Characins were the most frequent and abundant prey found in the diet, with Cheirodon interruptus being the fish prey with the highest numerical abundance The spotted livebearer Phalloceros caudimaculatus (Poeciliidae) was the second most numerous fish in the diet of H aff malabaricus The numerical abundance patterns of these two main fish prey (characins and poecilids) matched the relative abundance of the two most abundant fish families at the study site closely The multi-gear sampling of the ichthyofauna revealed that Characi- Table Frequency of occurrence (%F), numerical abundance (%N), weight (%W) and index of relative importance (%IRI) of the food items found in the stomach content of Hoplias aff malabaricus in the ‘Lagoa Peixe’ National Park (LPNP), southern Brazil Environ Biol Fish (2012) 93:1–12 Food items Code %Fo %N %W IRI% Actinopterygii Characiformes Characidae Astyanax eigenmanniorum (Cope, 1894) Asteig 1.85 0.95 0.77 0.08 Astyanax jacuhiensis (Cope, 1894) Astjac 3.7 1.9 4.07 0.58 Astyanax sp Astspp 7.41 4.76 3.26 1.56 Characins not identified Charac 12.96 7.62 3.45 3.78 Cheirodon interruptus (Jenyns, 1842) Cheint 11.11 9.52 1.97 3.37 Hyphessobrycon bifasciatus Ellis, 1911 Hypbif 1.85 0.95 0.8 0.09 Hyphessobrycon luetkenii (Boulenger, 1887) Hyplue 1.85 1.9 Hyphessobrycon sp Hypspp 1.85 1.9 Pseudocorynopoma doriae Perugia, 1891 Psedor 1.85 0.95 0.95 1,00 0.11 0.14 0.14 0.05 Erythrinidae Hoplias aff malabaricus (Bloch, 1794) Hopmal 1.85 0.95 0.55 0.07 Siluriformes Heptapteridae Heptapterus sympterygium Buckup, 1988 Hepsyp 1.85 0.95 1.53 Pimelodella australis Eigenmann, 1917 Pimaus 3.7 1.9 2.17 0.12 0.40 Rhamdia quelen (Quoy & Gaimard, 1824) Ranque 1.85 0.95 30.07 1.52 Phacau 12.96 6.67 0.57 2.48 Cynmel 1.85 0.95 0.11 0.05 Ausfac 1.85 0.95 10.18 0.54 Cyprinodontiformes Poeciliidae Phalloceros caudimaculatus (Hensel, 1868) Cyprinodontiformes Rivulidae Cynopoecilus melanotaenia (Regan, 1912) Perciformes Cichlidae Australoheros facetus (Jenyns, 1842) Others Organic matter Orgmat Plant remains not identified Plant 9.26 4.76 0.53 20.37 22.86 0.93 1.29 12.8 Insect remains not identified Resins 5.56 2.86 0.03 0.42 Fishes remains not identified Resfis 42.59 25.71 36.96 70.49 dae (61.3%) and Poeciliidae (18.8%) were the most abundant of the 14 fish families occurring at the study site (Fig 3) Other fish prey found in the diet belonged to the Heptapteridae and Cichlidae families In contrast, these families were more important in terms of their %W than their %N contribution (Table 1) Accordingly, these prey were not abundant in the study site but were characterized by their greater sizes (especially cichlids), when compared to characins and poecillids (Fig 3) The other eight fish families that occurred in small proportions (< 5%) at the study site were not found in the diet of H aff malabaricus (Table 1) No differences were observed in the diet composition of individuals caught during low and moderate-high rainfall periods (Fig 4) This pattern was corroborated by the ANOSIM, which did not reveal statistically significant differences between the periods (Global R=0.49, p=−0.006) Therefore, we pooled our dataset for the subsequent data analysis on feeding strategy and size-related dietary shifts Environ Biol Fish (2012) 93:1–12 Feeding strategy and size related dietary shift The feeding strategy analysis revealed that, as a whole, the studied population had a specialist feeding strategy towards the consumption of fish (Fig 5a), resulting in a narrow niche width as depicted by the box inserted in Fig 5a However, when the feeding strategy was analyzed considering only fish prey, Fig a Numerical abundance (%) and number of species in each family (parentheses) and b average total length (TL, mm) of fish species in the study site based on a multi-gear survey conducted concomitantly with the collection of the species studied here (Hoplias aff malabaricus) Fig MDS ordination of the composition of the diet of Hoplias aff malabaricus during periods of low (L) and moderate-high (M-H) rainfall periods Data values were square-root transformed, and the Bray-Curtis similarity was used Fig Feeding strategy diagram for individuals of the Hoplias aff malabaricus in the Lagoa Peixe National Park with fish prey pooled as a single food category (a) or separately by species (b) Prey-specific abundance (Pi) is plotted against frequency of occurrence (%F) of food items in the diet of Hoplias aff malabaricus The inserted box represents a conceptual diagram of a resource niche width characterized by a high between-phenotype component (sensu Amundsen et al 1996) to the niche width contribution The following food items were considered: Heptapterus sympterygium (Hepsyp), Cynopoecilus melanotaenia (Cynmel), Hoplias aff malabaricus (Hopmal), Rhamdia quelen (Ranque), organic matter (OrgMat), fish remains (FisRem), Phalloceros caudimaculatus (Phacau), Astyanax jacuhiensis (Astjac), Cheirodon interruptus (Cheint), Astyanax spp (Astspp), Pimelodella australis (Pimaus), Characidae (Charac), Plant fragments (Plant), Insects (Insect) there was a high variability in prey consumption between individuals (phenotypes) Some individuals preyed upon certain fish prey, such as the catfishes Heptapterus sympterygium and Rhamdia quelen, the annual fish Cynopoecilus melanotaenia and juveniles of the H aff malabaricus, resulting in low frequency of occurrence (%F) and higher prey-specific abundance values (Pi) in the diagram (Fig 5b) This pattern revealed a higher between-phenotype component to the niche width of the studied species and, consequently, greater partitioning of the food resources (mainly fish) between individuals of the predator population, as depicted by the box inserted in Fig 5b There were conspicuous size-related dietary shifts in terms of diet composition and prey sizes consumed by H aff malabaricus; with increasing predator size, the diet became more diverse (Table 2, Fig 6) and comprised larger fish prey (Fig 7) There was a significant increase in prey diet richness with the increase in size (TL, mm) (Kruskal-Wallis, H: 6.61, df: 2, p[...]... A Pfeiffenberger (*) : P J Motta Department of Integrative Biology, University of South Florida, 4202 E Fowler Avenue, Tampa, FL 33620, USA e-mail: jpfeiff2@mail.usf.edu Present Address: J A Pfeiffenberger Department of Biological Sciences, Florida Institute of Technology, 150 W University Boulevard, Melbourne, FL 329 01, USA feeding with increasing levels of competition in order to outcompete conspecifics... and Wainwright 1995) can affect the prey capture kinematics of fishes, and that higher stocking densities and competition reduce the growth and survival rate of fishes (Houde 1977; Anderson et al 2002) The goal of this study is to examine the effects of intraspecific competition on the prey capture kine- Environ Biol Fish (2012) 93:13–21 matics of bluegill sunfish Specifically, it is hypothesized that:... is thought to be increasing in Environ Biol Fish (2012) 93:31–41 occurrence worldwide including the Gulf of Mexico (Diaz and Rosenburg 2008) The Gulf of Mexico supports a variety of economically and ecologically important species that may be impacted by declining DO levels The seasonal presence of a large dead zone in the Gulf of Mexico at the mouth of the Mississippi river is well documented and also... patterns of estuarine fishes The goal of this study was to assess the relative importance of biotic and abiotic factors on habitat selection Specifically, we compared the relative importance of predator density, substrate, and food availability with varying levels of DO concentration to assess ecological impacts of declining oxygen concentrations on habitat selection patterns We used a series of replicated... backward movement of the pelvic and pectoral girdles and a forward movement of the second pterygiophore of the anal fin Still it is not clear which sound production mechanisms apply for the acoustic signalling in the rock-dwelling cichlids of Lake Malawi Sounds produced by cichlids appear to act in a variety of social interaction Variations in acoustic signals may be used for identification of conspecific... Proceedings of the National Academy of Sciences of the United States of America 96:5107–5110 Almeida OG, Miranda A, Frade P, Hubbard PC, Barata EN, Canário AVM (2005) Urine as a social signal in the Mozambique Tilapia (Oreochromis mossambicus) Chem Senses 30(Suppl 1):1309–1310 Amorim MCP (2006) Diversity of sound production in fish In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes,. .. the observed high degree of individual-level food niche variation in H aff malabaricus is an outcome of its ambush feeding strategy and its potential role in avoiding conspecific competition The analysis of the stomach contents of the studied species revealed a clear size-related dietary shift between diet composition and richness and the size Environ Biol Fish (2012) 93:1–12 of the prey consumed Dietary... moved in the time from reaching 20% of the peak gape while opening the mouth until the prey disappeared in the mouth of the predator were determined by tracking a spot on the opercle of the fish and the head of the Artemia sp during the prey capture sequence In addition, the velocities of the predator and the prey (VPredator and VPrey) were determined for the duration of the prey capture event (TPrey),... wetlands of Dulce River (Cordoba, Argentina) Hydrobiology 316:103–107 Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization Am Nat 161:1–20 Cantanhêde GS, Fugi R, Hahn NS (2009) Variation in prey selection of a piscivorous fish after the impoundment of a neotropical reservoir: prey size and type... which is determined as the time from when the mouth reaches 20% of the peak gape while opening the mouth until the prey disappears in the mouth of the predator In addition, the running average for the change in velocity of the predator (AInstantaneous) was determined for each field of 10 sequential fields before the prey entered the mouth of the predator and used to determine if the predator maintained,