Community structure affects trophic ontogeny in a predatory fish

While most studies have focused on the timing and nature of ontogenetic niche shifts, information is scarce about the effects of community structure on trophic ontogeny of top predators. We investigated how community structure affects ontogenetic niche shifts (i.e., relationships between body length, trophic position, and individual dietary specialization) of a predatory fish, brown trout (Salmo trutta). We used stable isotope and stomach content analyses to test how functional characteristics of lake fish community compositions (competition and prey availability) modulate niche shifts in terms of (i) piscivorous behavior, (ii) trophic position, and (iii) individual dietary specialization. Northern Scandinavian freshwater fish communities were used as a study system, including nine subarctic lakes with contrasting fish community configurations: (i) trout‐only systems, (ii) two‐species systems (brown trout and Arctic charr [Salvelinus alpinus] coexisting), and (iii) three‐species systems (brown trout, Arctic charr, and three‐spined sticklebacks [Gasterosteus aculeatus] coexisting). We expected that the presence of profitable small prey (stickleback) and mixed competitor–prey fish species (charr) supports early piscivory and high individual dietary specialization among trout in multispecies communities, whereas minor ontogenetic shifts were expected in trout‐only systems. From logistic regression models, the presence of a suitable prey fish species (stickleback) emerged as the principal variable determining the size at ontogenetic niche shifts. Generalized additive mixed models indicated that fish community structure shaped ontogenetic niche shifts in trout, with the strongest positive relationships between body length, trophic position, and individual dietary specialization being observed in three‐species communities. Our findings revealed that the presence of a small‐sized prey fish species (stickleback) rather than a mixed competitor–prey fish species (charr) was an important factor affecting the ontogenetic niche‐shift processes of trout. The study demonstrates that community structure may modulate the ontogenetic diet trajectories of and individual niche specialization within a top predator.     

Marine-freshwater transitions are associated with the evolution of dietary diversification in terapontid grunters (Teleostei: Terapontidae)

The ecological opportunities associated with transitions across the marine-freshwater interface are regarded as an important catalyst of diversification in a range of aquatic taxa. Here, we examined the role of these major habitat transitions and trophic diversification in a radiation of Australasian fishes using a new molecular phylogeny incorporating 37 Terapontidae species. A combined mitochondrial and nuclear gene analysis yielded a well-supported tree with most nodes resolved. Ancestral terapontids appear to have been euryhaline in habitat affiliation, with a single transition to freshwater environments producing all Australasian freshwater species. Mapping of terapontid feeding modes onto the molecular phylogeny-predicted carnivorous dietary habits was displayed by ancestral terapontids, which subsequently diversified into a range of additional carnivorous, omnivorous, herbivorous and detritivorous dietary modes upon transition to freshwater habitats. Comparative analyses suggested that following the freshwater invasion, the single freshwater clade has exhibited an increased rate of diversification at almost three times the background rate evident across the rest of the family. The marine-freshwater transition within Terapontidae appears to have resulted in substantial dietary radiation in freshwater environments, as well as increased lineage diversification rates relative to euryhaline-marine habitats.     

Riparian contributions to the diet of terapontid grunters (Pisces: Terapontidae) in wet–dry tropical rivers

The diets of terapontid assemblages in 22 catchments across Australia's wet–dry tropics were investigated in relation to the direct use of terrestrial‐riparian inputs, as well as the role of ontogeny and morphology in mediating consumption of allocthonous material. The diet of several species was restricted almost entirely to instream trophic resources throughout their life history. In contrast, ontogenetic diet shifts towards increasing consumption of terrestrial prey types were a prominent feature of the dietary ecology of some terapontids, with collective allocthonous dietary items making a significant contribution (up to 42%) to diet in larger size classes of several species. For those species consuming terrestrial‐riparian material in their diet, terrestrial invertebrates were the most common prey item; however, terrestrial vegetation, principally riparian fruits, and terrestrial vertebrates were also important dietary inclusions in the larger size classes of particular species. A large mouth gape was the morphological feature most strongly associated with consumption of terrestrial food resources within the Terapontidae. Results indicate that the direct consumption of terrestrially derived food sources in northern Australian aquatic systems may be more important than previously asserted, and that additional research is required to better clarify the role of terrestrial subsidies to these ecosystems.     

Comparing the diet of two sympatric urolophid elasmobranchs (Trygonoptera testacea Müller & Henle and Urolophus kapalensis Yearsley & Last): evidence of ontogenetic shifts and possible resource partitioning

The diets of two urolophids, the common stingaree Trygonoptera testacea and the kapala stingaree Urolophus kapalensis were analysed and compared to examine resource partitioning between these two morphologically similar sympatric Australian batoids. The diet of T. testacea was polychaete-based, while that of U. kapalensis was dominated by crustaceans (mostly carid shrimps and amphipods). Intraspecific dietary compositions were examined amongst size classes within each of the two species to identify ontogenetic shifts in diet. Differences in the dietary compositions of the smaller total-length classes of T. testacea suggest that their diet shifts as they increase in size, from one dominated by carids to one almost entirely comprising polychaetes. Significant ontogenetic dietary shifts were not identified in U. kapalensis . Although the two species shared eight broad dietary categories, their overall dietary compositions were found to be significantly different. The limited overlap in the dietary compositions of these two sympatric stingarees suggests the possibility of resource partitioning, with interspecific competition being implicated as a possible cue. Possible mechanisms for the partitioning of resources within and between these two species are discussed.     

Evidence for a multi‐peak adaptive landscape in the evolution of trophic morphology in terapontid fishes

Using the Australian marine‐freshwater terapontid fishes as a model system, we examined the role of dietary phenotypic optima in an adaptive macro‐evolutionary landscape. Comparative modelling relying on both a priori and data‐driven identification of selective regimes suggested multi‐peak models as best describing much of the dietary phenotypic landscape of terapontids. Both approaches identified common phenotypic optima for different lineages of marine and freshwater herbivores, and minimal differentiation between carnivores and omnivores, irrespective of their phylogenetic relationships, as the model best describing morphological evolution. Significant correlations also existed between these phenotypic axes and proportions of non‐animal dietary items in species’ diets. While simulation results provided evidence for a multi‐peak adaptive landscape in the evolution of trophic morphology in terapontids, they could not rule out chance convergence in these adaptive peaks. However, they do provide scope for identifying areas for more detailed, functionally specific study of phenotypic convergence in herbivorous terapontid trophic habits. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 623–634.     

Guild structure of carnivorous intertidal fishes of the Chilean coast: implications of ontogenetic dietary shifts

Although ontogenetic changes in resource use within species are common in animals, these changes have not been widely considered in studies of guild structure within communities. The occurrence of one or more shifts in resource use in an individual of a given species during its life should mean that it would also belong to different guilds at different life stages. We specifically addressed this issue by describing the feeding habits of ten species of carnivorous fishes occurring in tidepools in rocky intertidal areas along the coast of central Chile. Most of these species undergo clear ontogenetic dietary shifts and a feeding guild structure of this group of fishes was established that takes these dietary shifts into account. Each species was divided into a number of size classes. Dietary overlap values between both intraspecific and interspecific size-class pairs in the entire group of ten species were used to construct a phenogram of dietary similarity through an UPGMA cluster analysis. Numbers of guilds and their memberships were established objectively by applying a bootstrapping procedure. Four “ontogenetic” feeding guilds (OFGs), each consisting of size-classes of species, were recognized. The majority of species belonged to more that one guild. Interestingly, when the bootstrapping procedure was applied to a phenogram based on the diets of “taxonomic” or complete species, only one significant guild was found. The implications of these ontogenetic dietary shifts for interspecific interactions are substantial because the identity of the species with which each fish species shares resources change through their lives. The usefulness of taxonomic species for investigating potential competitive interactions in this assemblage is greatly undermined. Received: 26 September 1997 / Accepted: 15 December 1997     

Gut content and stable isotope analyses provide complementary understanding of ontogenetic dietary shifts and trophic relationships among fishes in a tropical river

1. Despite widespread recognition of the role of body size in fish trophic ecology, little attention has been focused on this issue in isotopic studies, particularly in tropical systems. 2. We used analyses of stomach contents and stable isotopes to examine size‐related shifts in diet in a terapontid fish assemblage in the Australian wet–dry tropics. Stomach content analysis identified substantial ontogenetic dietary shifts in all species, corresponding to changes in body size–isotope trajectories for two species. Shifts away from relatively specialised diets of heavily ¹³C‐depleted insect larvae to consumption of a range of items across multiple basal carbon sources appeared to be the proximate cause of observed isotopic changes. 3. Allochthonous organic matter in the form of C3 riparian vegetation was particularly important to smaller terapontids before larger fish shifted to a broad range of dietary items and similarly broad range of basal carbon sources. 4. While there was general agreement between δ¹³C and stomach content analysis, there was minimal concurrence between the latter and δ¹⁵N isotopic derivation of estimates of trophic position. Due to factors such as omnivory, isotopically overlapping basal sources and uncertainties about rates of isotopic fractionation in both predator and prey species, stomach content analysis provides an essential complement to isotopic methodologies in tropical systems. 5. Given that basal sources supporting any individual species can change markedly with ontogeny, consideration of intraspecific, size‐related variation is necessary in isotopic studies of food web structure.     

Ontogenetic niche shifts and resource partitioning in a subarctic piscivore fish guild

The feeding ecology of three piscivorous fish species (perch (Perca fluviatilis), pike (Esox lucius) and burbot (Lota lota)), was studied in the subarctic Pasvik watercourse (69 °N), northern Norway and Russia. All three species primarily occupied the benthic habitats in the watercourse. Perch and burbot exhibited distinct ontogenetic niche shifts in food resource use, perch changing from a dominance of zooplankton to zoobenthos to fish, and burbot from zoobenthos to fish. Fish prey dominated the diet of all the investigated size-classes of pike, but small-sized pike (<20 cm) were not represented in the sample. Fish prey size was positively related to predator size in all three species. Whitefish (Coregonus lavaretus) was the dominant prey of pike and large-sized burbot and perch. Nine-spined sticklebacks (Pungitius pungitius) was also an important prey and appeared to be a dietary stepping-stone enhancing the transition from invertebrate feeding to consumption of large-sized whitefish prey for all three predators. A cluster analysis separated the different size groups of the three predator species into five functional feeding groups, most of them containing two or all three species. Within these feeding groups, and especially among the piscivorous size-classes, there was a strong and significant interspecific overlap in prey selection, and the dietary similarities between the species were in general much larger than the intraspecific similarities between ontogenetic stages. All three piscivorous species are important top predators in the aquatic food web of the watercourse, and their ontogenetic diet shifts and resource partitioning patterns generate a substantial food web complexity in this subarctic ecosystem.     

Ontogenetic niche shifts matter in community ecology: a review and future perspectives

Almost all organisms on Earth exhibit ontogenetic niche shifts, which causes great phenotypic variation among individuals and is thus considered to critically mediate community structure and dynamics. In contrast, community ecology has traditionally assumed that species are composed of identical individuals with invariant traits and ignored the potentially important ecological roles of ontogenetic niche shifts. To bridge the gap, here I briefly review ecologically relevant examples which show that basic insights of species-based community theories can be revised by including the ontogenetic perspective. Specifically, I focus on the most representative animals in the study of ontogenetic niche shifts, i.e., fish, insects, and amphibians. Notably, their ontogenetic niche shifts create novel views of community structure: (1) ontogenetic diet shifts of predatory fish couple pelagic and benthic food webs in aquatic systems, (2) ontogenetic shifts in interaction types of pollinating insects couple herbivory and pollination networks in terrestrial systems, and (3) ontogenetic habitat shifts of amphibians and aquatic insects couple aquatic and terrestrial metacommunities at interface areas. Dynamic models of such stage-structured communities suggest that their ontogenetic niche shifts may affect the community resilience and disturbance responses. Exploring more complex systems (e.g., where many species undergo ontogenetic niche shifts several times or continuously) is a future direction, for which describing body size relationships between interacting organisms would be a promising approach. I conclude that both theoretical and empirical advances are needed to facilitate the ontogenetic perspective for better understanding mechanisms underlying biodiversity and ecosystem functioning which are increasingly threatened by anthropogenic disturbance.     

Trophic niche and habitat shifts of sympatric Gerreidae

The diet and mouth growth rates of three Gerreidae species (Eugerres brasilianus, Eucinostomus melanopterus and Diapterus rhombeus) were assessed at different ontogenetic phases (juveniles, sub‐adults and adults) in order to detect allometric growth, and whether they are related to habitat and seasonal changes in the Goiana Estuary, north‐east Brazil. The importance of each prey for each ontogenetic phase was described using the index of relative importance. The three species showed seasonal ontogenetic shifts in diet and allometric growth of mouth morphology. They also had an exclusively zoobenthic diet, comprising mainly Polychaeta, Copepoda, Ostracoda, Gastropoda and Bivalvia. Mouth development showed a possible influence on diet changes for E. melanopterus. Significant interactions (P < 0·01) were detected among seasons, areas and ontogenetic phases for the most important prey for E. brasilianus and E. melanopterus. Diet overlaps are evidence of intra and interspecific competition among gerreids for specific prey. A conceptual model of the competition and seasonal diet shifts among ontogenetic phases of gerreids is given. The sediment ingested due to the feeding mechanisms of Gerreidae species could also partially explain the ingestion of synthetic items observed for all ontogenetic phases, which indicates one of a myriad effects of human activities (e.g. artisanal fishery) in this estuary.     

Do sharks exhibit heterodonty by tooth position and over ontogeny? A comparison using elliptic Fourier analysis

Tooth morphology is often used to inform the feeding ecology of an organism as these structures are important to procure and process dietary resources. In sharks, differences in morphology may facilitate the capture and handling of prey with different physical properties. However, few studies have investigated differences in tooth morphology over ontogeny, throughout the jaws of a single species, or among species at multiple tooth positions. Bull (Carcharhinus leucas), blacktip (Carcharhinus limbatus), and bonnethead sharks (Sphyrna tiburo) are coastal predators that exhibit ontogenetic dietary shifts, but differ in their feeding ecologies. This study measured tooth morphology at six positions along the upper and lower jaws of each species using elliptic Fourier analysis to make comparisons within and among species over their ontogeny. Significant ontogenetic differences were detected at four of the six tooth positions in bull sharks, but only the posterior position on the lower jaw appeared to exhibit a functionally relevant shift in morphology. No ontogenetic changes in morphology were detected in blacktip or bonnethead sharks. Intraspecific comparisons found that most tooth positions significantly differed from one another across all species, but heterodonty was greatest in bull sharks. Additionally, interspecific comparisons found differences among all species at each tooth position except between bull and blacktip sharks at two positions. These morphological patterns within and among species may have implications for prey handling efficiency, as well as in providing insight for paleoichthyology studies and reevaluating heterodonty in sharks.     

Ontogenetic dietary shifts and feeding ecology of the rasptail skate Raja velezi and the brown smoothhound shark Mustelus henlei along the Pacific coast of Costa Rica,Central America

Stomachs from 511 Raja velezi and 340 Mustelus henlei captured as by‐catch in the commercial trawling fishery (2010–2012) were analysed to examine diet composition, ontogenetic shifts and degree of dietary overlap between species life stages in the Pacific Ocean of Costa Rica. Shrimps were the most important prey categories in the diet of R. velezi, while teleosts and cephalopods dominated the diet of M. henlei. Diet comparisons between different stages of R. velezi and M. henlei revealed clear ontogenetic dietary shifts: crustaceans (mainly shrimps, crabs and stomatopods) dominated the diet of immature individuals, and adults had a higher proportion of teleosts. The results suggest that R. velezi is an epibenthic predator that specializes in shrimps during early life stages, and to a lesser extent, teleosts as it matures, while M. henlei is an opportunistic predator with a highly diverse diet consisting of teleosts, cephalopods, shrimps and stomatopods. This study also found little evidence of dietary overlap between species or life stages and suggests that intra‐ and interspecific competition between R. velezi and M. henlei may be reduced by: (1) diet specialization in immature stages of R. velezi, (2) ontogenetic dietary shifts between immature and mature individuals, (3) prey‐size selectivity in larger individuals of R. velezi and (4) differences in depth utilization in overlapping geographical regions.     

Stable isotope analysis indicates a lack of inter- and intra-specific dietary redundancy among ecologically important coral reef fishes

Parrotfish are critical consumers on coral reefs, mediating the balance between algae and corals, and are often categorised into three functional groups based on adult morphology and feeding behaviour. We used stable isotope analysis (δ¹³C, δ¹⁵N) to investigate size-related ontogenetic dietary changes in multiple species of parrotfish on coral reefs around Zanzibar. We compared signatures among species and functional groups (scrapers, excavators and browsers) as well as ontogenetic stages (immature, initial and terminal phase) within species. Stable isotope analysis suggests that ontogenetic dietary shifts occurred in seven of the nine species examined; larger individuals had enriched δ¹³C values, with no relationship between size and δ¹⁵N. The relationship between fish length and δ¹³C signature was maintained when species were categorised as scrapers and excavators, but was more pronounced for scrapers than excavators, indicating stronger ontogenetic changes. Isotopic mixing models classified the initial phase of both the most abundant excavator (Chlorurus sordidus) as a scraper and the immature stage of the scraper Scarus ghobban (the largest species) as an excavator, indicating that diet relates to size rather than taxonomy. The results indicate that parrotfish may show similar intra-group changes in diet with length, but that their trophic ecology is more complex than suggested by morphology alone. Stable isotope analyses indicate that feeding ecology may differ among species within functional groups, and according to ontogenetic stage within a species.     

Prey use of wetland benthivorous sunfishes: ontogenetic, interspecific and seasonal variation

The intensity of competitive interactions between fishes is partly determined by prey use and ontogenetic niche shifts. In a wetland where distinct habitat shifts are missing we compared prey use of three generalist benthivorous sunfishes to look for evidence of ontogenetic, interspecific, and “seasonal” variation in prey composition. Diet analysis revealed evidence of diet ontogeny in warmouth (Lepomis gulosus, 30–152 mm standard length, SL), but not in bluespotted sunfish (Enneacanthus gloriosus, 30–47 mm SL) or dollar sunfish (Lepomis marginatus, 30–60 mm SL). Bluespotted and dollar sunfishes consumed small dipteran and amphipod prey and had similar diets in both seasons suggesting a potential for strong interspecific competition. In the dry season, warmouth shifted from using smaller insect prey to larger decapod and fish prey with increasing size. This shift to prey types that were little used by the other species reduced dietary niche overlap with the other sunfishes. After drought and re-flooding (in the wet season), decapods and small fish were less abundant in the wetland and the warmouth ontogenetic shift was less distinct. When matched for gape width, prey composition differed between warmouth and both dollar and bluespotted sunfishes in the wet season, suggesting differences in sunfish foraging modes, but prey use differences were less clear in the dry season when prey were abundant. Both warmouth ontogenetic diet shifts and seasonal variation in prey use (probably mediated by prey abundance) had strong influences on diet overlap and therefore the potential for intra- and interspecific competition between sunfishes in this wetland ecosystem.     

Temporal consistency of ontogenetic shifts in habitat use by coral reef fishes in the northernmost coral ecosystem in the world (Kudaka Island, Japan)

The prevalence of major habitat shifts in tropical fishes between juvenile and adult stages (ontogenetic shifts) in one of the northernmost coral reefs in the world (Kudaka Island, Japan) is given. The comparative analysis of spatial distribution of juveniles v . adults highlighted four ontogenetic patterns: no change in habitat use between juveniles and adults (five species), a decrease in the number of habitats used by adults compared to juveniles (three species), an increase in the number of habitats used during the adult stage (four species) and use of nursery areas by juveniles followed by extensive movements to different adult habitats (three species). The comparative analysis of fish distribution over time ( i.e. during three consecutive settlement months) showed that 84% of species had temporal consistency in ontogenetic patterns of habitat use.     

Sequence and expression of an α-amylase gene in four related species of prickleback fishes (Teleostei: Stichaeidae): ontogenetic,dietary, and species-level effects

Partial α-amylase gene sequences were determined and α-amylase gene expression was quantified in four species of carnivorous, omnivorous, and herbivorous prickleback fishes (family Stichaeidae) to assess the effects of ontogeny, diet, and species on expression of this gene. Pairwise comparison of α-amylase nucleotide sequences revealed 96–98 % identity, and comparison of amino acid portions revealed 93–95 % similarity among the four prickleback species. Expression was determined using in situ hybridization and intensity of expression quantified using image analysis. Alpha-amylase expression level was compared in three feeding categories of the four species: (1) small, wild-caught carnivorous juveniles; (2) larger, wild-caught juveniles of the carnivorous species and the three that had shifted to herbivory or omnivory; and (3) larger, juveniles produced by feeding a low-starch artificial diet to small juveniles until they reached the size of the larger wild-caught juveniles. The results showed no dietary effect in any species but significant ontogenetic and species-level effects in Cebidichthys violaceus, as well as in the sister species Xiphister mucosus and X. atropurpureus. Based on a phylogeny for the Stichaeidae produced for this study using two mtDNA genes and one nuclear gene, the ontogenetic dietary shifts to herbivory/omnivory evolved independently in C. violaceus and in the clade containing the two species of Xiphister. All three of these species increased α-amylase gene expression with increase in size and had higher expression than Anoplarchus purpurescens, which is a member of a third, stichaeid clade comprising carnivores. These results show the importance of α-amylase in the herbivores and omnivores.     

Ontogenetic diet shifts and interrupted piscivoryin introduced largemouth bass (Micropterus salmoides)

The ecology of largemouth bass (Micropterus salmoides) is one of the best known for freshwater fish, though largely through studies within its native range (North America). I studied the habitat and diet of a bass population introduced into a Mediterranean lake. The bass displayed strong ontogenetic diet shifts as follows: young‐of‐the‐year <25 mm fed on microcrustaceans; fish 25–75 mm, on amphipods and insects; fish 100–225 mm, on a freshwater shrimp, small fish and insects; fish 250–300 mm, on shrimp or crayfish; and fish >300 mm, on crayfish and large fish. The diet showed several differences from most previous studies: importance of freshwater shrimp instead of insects, low piscivory, and a delay in the ontogenetic shift to piscivory. Moreover, the ontogenetic shift to piscivory was interrupted at 250–300 mm, with consumption of shrimp and crayfish. This interruption of piscivory has been largely unreported and seems a consequence of the size‐structure and species composition of the fish assemblage. A review of the literature suggests that piscivory by largemouth bass might be generally lower in populations introduced outside North America.     

Competition during early ontogeny: Effects of native and invasive planktivores on the growth,survival, and habitat use of bluegill

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Ontogenetic diet shifts produce trade‐offs in elemental imbalance in bluegill sunfish

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Trophic niche ontogeny and palaeoecology of early Toarcian Stenopterygius (Reptilia: Ichthyosauria)

Reconstructing ecological niche shifts during ontogeny in extinct animals with no living analogues is difficult without exceptional fossil collections. Here we demonstrate how a previously identified ontogenetic shift in the size and shape of the dentition in the early Toarcian ichthyosaur Stenopterygius quadriscissus accurately predicts a particular dietary shift. The smallest S. quadriscissus fed on small, burst‐swimming fishes, with a steady shift towards faster moving fish and cephalopods with increasing body size. Larger adult specimens appear to have been completely reliant on cephalopods, with fish completely absent from gut contents shortly after onset of sexual maturity. This is consistent with a previously proposed ontogenetic niche shift based on tooth shape and body size, corroborating the idea that dental ontogeny may be a useful predictor of dietary shifts in marine reptiles. Applying the theoretical framework used here to other extinct species will improve the resolution of palaeoecological reconstructions, where appropriate sample sizes exist.