Lake size and fish diversity determine resource use and trophic position of a top predator in high‐latitude lakes

Prey preference of top predators and energy flow across habitat boundaries are of fundamental importance for structure and function of aquatic and terrestrial ecosystems, as they may have strong effects on production, species diversity, and food‐web stability. In lakes, littoral and pelagic food‐web compartments are typically coupled and controlled by generalist fish top predators. However, the extent and determinants of such coupling remains a topical area of ecological research and is largely unknown in oligotrophic high‐latitude lakes. We analyzed food‐web structure and resource use by a generalist top predator, the Arctic charr Salvelinus alpinus (L.), in 17 oligotrophic subarctic lakes covering a marked gradient in size (0.5–1084 km²) and fish species richness (2–13 species). We expected top predators to shift from littoral to pelagic energy sources with increasing lake size, as the availability of pelagic prey resources and the competition for littoral prey are both likely to be higher in large lakes with multispecies fish communities. We also expected top predators to occupy a higher trophic position in lakes with greater fish species richness due to potential substitution of intermediate consumers (prey fish) and increased piscivory by top predators. Based on stable carbon and nitrogen isotope analyses, the mean reliance of Arctic charr on littoral energy sources showed a significant negative relationship with lake surface area, whereas the mean trophic position of Arctic charr, reflecting the lake food‐chain length, increased with fish species richness. These results were supported by stomach contents data demonstrating a shift of Arctic charr from an invertebrate‐dominated diet to piscivory on pelagic fish. Our study highlights that, because they determine the main energy source (littoral vs. pelagic) and the trophic position of generalist top predators, ecosystem size and fish diversity are particularly important factors influencing function and structure of food webs in high‐latitude lakes.     

Seasonal dietary shifts enhance parasite transmission to lake salmonids during ice cover

Changes in abiotic and biotic factors between seasons in subarctic lake systems are often profound, potentially affecting the community structure and population dynamics of parasites over the annual cycle. However, few winter studies exist and interactions between fish hosts and their parasites are typically confined to snapshot studies restricted to the summer season whereas host‐parasite dynamics during the ice‐covered period rarely have been explored. The present study addresses seasonal patterns in the infections of intestinal parasites and their association with the diet of sympatric living Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta) in Lake Takvatn, a subarctic lake in northern Norway. In total, 354 Arctic charr and 203 brown trout were sampled from the littoral habitat between June 2017 and May 2018. Six trophically transmitted intestinal parasite taxa were identified and quantified, and their seasonal variations were contrasted with dietary information from both stomachs and intestines of the fish. The winter period proved to be an important transmission window for parasites, with increased prevalence and intensity of amphipod‐transmitted parasites in Arctic charr and parasites transmitted through fish prey in brown trout. In Arctic charr, seasonal patterns in parasite infections resulted mainly from temporal changes in diet toward amphipods, whereas host body size and the utilization of fish prey were the main drivers in brown trout. The overall dynamics in the community structure of parasites chiefly mirrored the seasonal dietary shifts of their fish hosts.     

Reliance of brown trout on terrestrial prey varies with season but not fish density

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Climate and productivity shape fish and invertebrate community structure in subarctic lakes

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Changing gull diet in a changing world: A 150‐year stable isotope (δ13C, δ15N) record from feathers collected in the Pacific Northwest of North America

The world's oceans have undergone significant ecological changes following European colonial expansion and associated industrialization. Seabirds are useful indicators of marine food web structure and can be used to track multidecadal environmental change, potentially reflecting long‐term human impacts. We used stable isotope (δ¹³C, δ¹⁵N) analysis of feathers from glaucous‐winged gulls (Larus glaucescens) in a heavily disturbed region of the northeast Pacific to ask whether diets of this generalist forager changed in response to shifts in food availability over 150 years, and whether any detected change might explain long‐term trends in gull abundance. Sampled feathers came from birds collected between 1860 and 2009 at nesting colonies in the Salish Sea, a transboundary marine system adjacent to Washington, USA and British Columbia, Canada. To determine whether temporal trends in stable isotope ratios might simply reflect changes to baseline environmental values, we also analysed muscle tissue from forage fishes collected in the same region over a multidecadal timeframe. Values of δ¹³C and δ¹⁵N declined since 1860 in both subadult and adult gulls (δ¹³C, ~ 2–6‰; δ¹⁵N, ~4–5‰), indicating that their diet has become less marine over time, and that birds now feed at a lower trophic level than previously. Conversely, forage fish δ¹³C and δ¹⁵N values showed no trends, supporting our conclusion that gull feather values were indicative of declines in marine food availability rather than of baseline environmental change. Gradual declines in feather isotope values are consistent with trends predicted had gulls consumed less fish over time, but were equivocal with respect to whether gulls had switched to a more garbage‐based diet, or one comprising marine invertebrates. Nevertheless, our results suggest a long‐term decrease in diet quality linked to declining fish abundance or other anthropogenic influences, and may help to explain regional population declines in this species and other piscivores.     

Lipid‐rich zooplankton subsidise the winter diet of benthivorous Arctic charr (Salvelinus alpinus) in a subarctic lake

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Seasonal and annual differences in the foraging ecology of two gull species breeding in sympatry and their use of fishery discards

Niche segregation between similar species will result from an avoidance of competition but also from environmental variability, including nowadays anthropogenic activities. Gulls are among the seabirds with greater behavioural plasticity, being highly opportunistic and feeding on a wide range of prey, mostly from anthropogenic origin. Here, we analysed blood and feather stable isotopes combined with pellet analysis to investigate niche partitioning between Audouin's gull Larus audouinii and yellow‐legged gull Larus michahellis breeding in sympatry at Deserta Island, southern Portugal, during 2014 and 2015. During the breeding season there was considerable overlap in the adults’ diet, as their stable isotope values of blood and primary feather (P1) did not differ, and their pellets were comprised mainly by marine fish species. However, Audouin's gulls presented higher occurrences of pelagic fish, while yellow‐legged gulls fed more on demersal fish, insects, and refuse. SIAR mixing models also estimated a higher proportion of demersal fish in the diet of yellow‐legged gulls. We also found differences between the two gull species in chicks’ feathers, suggesting that Audouin's gull adults selected prey with lower carbon isotope values to feed their young. Secondary feather (S8) of Audouin's gull presented higher isotope values compared to yellow‐legged gulls, indicating different foraging areas (δ¹³C) and/ or trophic levels (δ¹⁵N) between the two species in the non‐breeding season. During both the all‐year and non‐breeding periods the yellow‐legged gull showed a broader isotopic niche width than Audouin's gull in 2013, and in 2014 the two gull species exhibited different isotopic niche spaces. Our study suggests that both gull species foraged in association with fisheries during the breeding season. In this sense, a discard ban implemented under the new European Union Common Fisheries Policy may lead to a food shortage, therefore future research should closely monitor the population dynamics of Audouin's and yellow‐legged gulls.     

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.     

Seasonal depletion of resources intensifies trophic interactions in subarctic freshwater fish communities

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Dietary ontogeny and niche shift to piscivory in lacustrine brown trout Salmo trutta revealed by stomach content and stable isotope analyses

The feeding ecology and ontogeny of a large size range of brown trout Salmo trutta in Lake Fyresvatnet, southern Norway, were examined by stomach content and stable isotope analyses. According to the stomach contents, the S. trutta changed their diet at c. 30 cm total length (L_T). The smaller size classes fed on benthic invertebrates and surface insects, whereas larger S. trutta (>30 cm) fed mainly on whitefish Coregonus lavaretus. A similar, but more gradual shift to piscivory in the size range 25–30 cm was found when using the stable isotope mixing model SIAR to reveal dietary ontogeny. The δ¹³C isotopic signature confirmed that S. trutta independent of size predominantly relied upon benthic energy sources, suggesting that the littoral zone was the primary foraging habitat for both invertebrate and piscivorous feeders. The δ¹⁵N values and trophic position increased with predator length, ranging from an average of 3·60 for small‐sized S. trutta (<15 cm) to 4·15 for large‐sized fish (>35 cm). The S. trutta exhibited a relatively slow growth rate during the predominant invertebrate feeding stages up to 7 years of age and 28 cm L_T, whereas fish above this size and age displayed a rapid growth rate of 9–11 cm year^?1, demonstrating the profitability of piscivorous feeding.     

From autochthonous to allochthonous resources: seasonal shifts in food use by stream‐dwelling YOY Arctic charr Salvelinus alpinus through the ice‐free season

Substantial seasonal changes in resource use associated with enhanced water‐column use were revealed in stream‐living YOY Arctic charr Salvelinus alpinus during the ice‐free season. In July, YOY individuals showed a diet dominated by aquatic invertebrates (mainly Chironomidae larvae), but despite the small size of the fish, the abundance of terrestrial insects in their diet increased markedly from July to September (from 1·9 to 62·8%). Similarly, the frequency of surface drifting foragers, i.e. individuals feeding on allochthonous resources, increased from July to September (from 20·6 to 80%); allochthonous resources thus constituting an important energy subsidy for YOY S. alpinus during the late sub‐Arctic summer.     

Difference in diet and size‐related trophic level in two sympatric fish species,the red mullets Mullus barbatus and Mullus surmuletus,in the Gulf of Lions (north‐west Mediterranean Sea)

Stable‐isotope ratios (δ¹⁵N and δ¹³C) and diet of the red mullets Mullus barbatus and Mullus surmuletus were analysed in two zones differently subjected to the Rhône River runoff in the Gulf of Lions (north‐west Mediterranean sea) in May and October 2004. δ¹⁵N and δ¹³C increased significantly with fish size in M. barbatus in both zones and seasons, whereas no significant trend was evidenced in M. surmuletus. A clear size‐related shift in diet was observed in M. barbatus, with an increase in polychaete and shrimp consumption with size and a decrease in small crustacean consumption. In M. surmuletus, a diet shift was observed only between medium and large individuals. Large M. surmuletus preyed on shrimps, polychaetes, bivalves, ophiurids and amphipods, and ingested prey of lower mean mass than M. barbatus of similar size. Difference in size‐related increase in δ¹⁵N between the two mullid fish species were related to difference of trophic level of their main prey. Sub‐surface deposit‐feeding polychaetes, carnivorous polychaetes, shrimps and brachyurans presented higher δ¹⁵N values than bivalves, small crustaceans and ophiurids. The lower δ¹³C values observed in M. barbatus compared to M. surmuletus were related to a higher consumption of sub‐surface polychaetes in the former species. Significantly, lower δ¹³C were recorded in fishes collected off the Rhône River, particularly in spring, suggesting an influence of river inputs as a source of particular organic matter for mullids in this zone after the flooding season. Thus, these closely related sympatric fish species displayed diet divergences that were reflected in their stable isotopic signatures.     

Stable isotopes indicate that zebra mussels (Dreissena polymorpha) increase dependence of lake food webs on littoral energy sources

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Prey composition and ontogenetic shift in coastal populations of longnose gar Lepisosteus osseus

Longnose gar Lepisosteus osseus were collected from May 2012 to July 2013 in the Charleston Harbor and Winyah Bay estuaries (SC, U.S.A.). This study examined trends in stomach fullness, described major prey components and their importance in the diet of L. osseus, compared stomach content‐based trophic level estimates with the stable‐isotope‐based proxy: δ¹⁵N and tested for the occurrence of an ontogenetic diet shift using stomach content analysis and stable C and N isotopes (δ¹³C and δ¹⁵N). Dominant prey families were Clupeidae, Sciaenidae, Penaeidae, Fundulidae and Mugilidae, with the highest consumption rates in autumn. Trophic levels calculated using stomach contents did not correspond to δ¹⁵N (P > 0·05). Stomach contents and stable‐isotope signatures indicate ontogenetic prey composition shifts from low trophic level benthic prey (fundulids) to higher trophic level pelagic prey (clupeids) as the fish grow between 400 and 600 mm in standard length. Due to their biomass, abundance and top predator status, L. osseus play a significant ecological role in the estuarine community composition, although this effect has often been overlooked by past researchers and should be considered in future estuarine community studies.     

Consistency of elemental and isotope‐ratio patterns across multiple scales from individual fish

Assays of elemental and stable‐isotope ratios across growth increments of scales have the potential to provide a non‐lethal alternative to otolith chemistry for identifying migration and ontogenetic trophic shifts. A central assumption when employing scales as otolith analogues is that any scale from an individual will provide equivalent information about the chemical history of that fish. This assumption was investigated with multiple scales from wild and captive euryhaline Atlantic tarpon Megalops atlanticus from the north‐west Gulf of Mexico. Elemental (Sr:Ca) and isotope‐ratio (δ¹³C and δ¹⁵N) life‐history profiles were compared among multiple scales from each fish. All three chemical proxies showed highly consistent patterns among non‐regenerated scales, while patterns in regenerated scales diverged, indicating rapid regrowth of interior scale material at the onset of regeneration. Patterns of Sr:Ca and δ¹³C covaried, supporting their use as salinity proxies, while δ¹⁵N patterns were consistent with ontogenetic diet shifts. Water samples taken from aquaria holding captive fish were used to calculate partition coefficients for a suite of elements in M. atlanticus scales for future quantification of migratory movements in the region. Together, these results support the assumption that non‐regenerated scales from individual M. atlanticus provide equivalent chemical histories, further validating their use as a viable non‐lethal alternative to otoliths.     

The effects of tissue type and body size on δ13C and δ15N values in parrotfish (Labridae) from Zanzibar,Tanzania

Differences between the stable isotopic ratios (δ¹³C and δ¹⁵N) of two tissues (blood and muscle) from four species of East African coral reef parrotfishes (family: Labridae, tribe: Scarini) were analysed across a broad spectrum of body sizes. Comparison of isotopic ratios between the tissues allowed the assessment of using blood as an alternative tissue to muscle. In 2010–2011, constant differences between tissues (δ_blood minus δ_muscle) were found across a broad range of sampled fish lengths. Linear relationships between the tissues, specific for an isotope, indicate that constants could be generated for converting blood isotope into muscle isotope values. Only one species, Chlorurus sordidus, displayed an inconsistent difference between tissues in δ¹⁵N, indicating that this ratio was dependent on fish length. The δ¹³C of both tissues was positively related linearly to fish length for three species, while δ¹⁵N showed no relationship with body length. The results are interpreted as indicating dietary consistency over days to weeks, the time of tissue turnover for blood and muscle, respectively. Lastly, differences among the species, even closely related species, show that the generation of tissue conversion constants is species‐specific.     

Within-lake variability in carbon and nitrogen stable isotope signatures

1. We assessed spatial and temporal variation in carbon and nitrogen isotopic signatures in different compartments of a single lake ecosystem. Stable isotope analyses were made on samples of particulate organic matter (POM), zooplankton, periphyton, macrophytes, macroinvertebrates and fish collected from several locations throughout the ice‐free period. 2. No spatial variation in δ¹³C or δ¹⁵N values was found for pelagic samples of POM and zooplankton. However, pelagic δ¹⁵N signatures increased steadily through the summer resulting in an almost 6‰ average increase in POM and zooplankton. A concurrent decrease in epilimnetic nitrate concentrations suggested that the increase in δ¹⁵N of POM and zooplankton could have resulted from a progressive ¹⁵N‐enrichment of the available inorganic nitrogen pool as the size of this pool was reduced. 3. Significant spatial variation in isotopic ratios was observed within littoral and profundal communities. Some spatial differences were likely related to lake‐specific characteristics, such as a major inlet and a small harbour area and some were interconnected with temporal events. 4. Marked differences between spring and autumn δ¹⁵N and δ¹³C values of fish at one site probably reflected a spring spawning immigration from a larger downstream lake and also indicated limited dispersal of these immigrants. 5. Our results indicate that restricted sampling of ecosystem components from lakes may provide misleading single values for the isotope end members needed for quantitative uses of stable isotopes in mixing models and for estimating trophic position. Hence we strongly advise that studies of individual lakes, or multiple lake comparisons, that utilise stable isotope analyses should pay more attention to potential within lake spatial and temporal variability of isotope ratios.     

Changes in diets of individual Baltic ringed seals (Phoca hispida botnica) during their breeding season inferred from stable isotope analysis of multiple tissues

The stable isotope ratios (δ¹³C and δ¹⁵N) of three tissues with different metabolic rates (plasma, liver, and muscle) were used to investigate temporal variation in diet among nine individual Baltic ringed seals (Phoca hispida botnica Gmelin) from the Bothnian Bay, northeast Baltic Sea. The isotope values from plasma should reflect the most recent diet, values from liver the diet of the past weeks prior to sampling, and values from muscle should integrate diet over almost the entire breeding season of the ringed seals. In general, δ¹³C values of liver were more enriched in ¹³C than were those of either muscle or plasma, suggesting that the diet of the seals may have included a higher proportion of ¹³C‐enriched benthic prey in April. Females showed more variable δ¹³C values than males, suggesting possible gender differences in diet or in foraging locations. The differences that were apparent between females possibly reflect individual variation in the onset and duration of parturition and lactation, both of which likely restrict female foraging. Previous data from parasite infections and from alimentary tract contents of the same seals were linked to the isotope data to assist in drawing inferences about changes in the diets of individual seals.     

A trophic pathway from biogenic methane supports fish biomass in a temperate lake ecosystem

Although some primary consumers such as chironomid larvae are known to exploit methane‐derived carbon via microbial consortia within aquatic food webs, few studies have traced the onward transfer of such carbon to their predators. The ruffe Gymnocephalus cernuus is a widespread benthivorous fish which feeds predominantly on chironomid larvae and is well adapted for foraging at lower depths than other percids. Therefore, any transfer of methanogenic carbon to higher trophic levels might be particularly evident in ruffe. We sampled ruffe and chironomid larvae from the littoral, sub‐littoral and profundal areas of Jyväsjärvi, Finland, a lake which has previously been shown to contain chironomid larvae exhibiting the very low stable carbon isotope ratios indicative of methane exploitation. A combination of fish gut content examination and stable isotope analysis was used to determine trophic linkages between fish and their putative prey. Irrespective of the depth from which the ruffe were caught, their diet was dominated by chironomids and pupae although the proportions of taxa changed. Zooplankton made a negligible contribution to ruffe diet. A progressive decrease in δ¹³C and δ¹⁵N values with increasing water column depth was observed for both chironomid larvae and ruffe, but not for other species of benthivorous fish. Furthermore, ruffe feeding at greater depths were significantly larger than those feeding in the littoral, suggesting an ontogenetic shift in habitat use, rather than diet, as chironomids remained the predominant prey item. The outputs from isotope mixing models suggested that the incorporation of methane‐derived carbon to larval chironomid biomass through feeding on methanotrophic bacteria increased at greater depth, varying from 0% in the littoral to 28% in the profundal. Using these outputs and the proportions of littoral, sub‐littoral or profundal chironomids contributing to ruffe biomass, we estimated that 17% of ruffe biomass in this lake was ultimately derived from chemoautotrophic sources. Methanogenic carbon thus supports considerable production of higher trophic levels in lakes.     

Trophic behaviour of juvenile reef fishes inhabiting interlinked mangrove–seagrass habitats in offshore mangrove islets

Stable isotope (δ¹³C and δ¹⁵N) and gut content analyses were used to investigate size‐related feeding habits of four reef fishes (the beaugregory Stegastes leucostictus, the french grunt Haemulon flavolineatum, the schoolmaster snapper Lutjanus apodus and the yellowtail snapper Ocyurus chrysurus) inhabiting an offshore (non‐estuarine) mangrove islet off Belize, Central America. Comparisons of isotopic niche space and Schoener diet similarity index suggested a low to moderate degree of niche overlap between fish size groups. The δ¹³C gradient between mangrove and seagrass prey as well as results of Bayesian mixing models revealed that sampled fishes relied mostly on seagrass prey items. Only small and large juveniles of the carnivorous species L. apodus derived a part of their diet from mangroves by targeting mangrove‐associated Grapsidae crabs and fish prey, respectively. Isotopic niche shifts were particularly obvious for carnivorous fishes that ingested larger prey items (Xanthidae crabs and fishes) during their ontogeny. The utilization of mangrove food resources is less than expected and depends on the ecology and life history of the fish species considered. This research highlights that mangrove‐derived carbon contributed relatively little to the diets of four fish taxa from an offshore mangrove islet.