Otolith chemistry of prey fish consumed by a fish predator: does digestion hinder Russian doll techniques?

The effect of digestion by a predatory fish (largemouth bass Micropterus salmoides) on stable isotopic (δ¹³C and δ¹⁸O) and trace elemental (Sr:Ca and Ba:Ca) compositions of prey fish (bluegill Lepomis macrochirus) otoliths was investigated in a laboratory experiment. Trace element and stable‐isotopic signatures of L. macrochirus otoliths were not significantly altered for up to 16 h after L. macrochirus were consumed by M. salmoides. Prey fish otoliths recovered from predator digesta can retain environmental stable isotopic and trace elemental signatures, suggesting that determination of environmental history for prey fishes by stable‐isotope and trace‐element analysis of otoliths recovered from stomachs of piscivorous fishes will be feasible.     

The role of local adaptation in shaping fish‐mussel coevolution

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Movement,connectivity and population structure of the intertidal fish Lipophrys pholis as revealed by otolith oxygen and carbon stable isotopes

The shanny Lipophrys pholis is an intertidal fish commonly found in Portuguese coastal waters. Spawning takes place from early autumn to mid spring, after which demersal eggs hatch and larvae disperse along the coast. Two to three months later, young juveniles return to the tide pools to settle. However, information on fish movement, habitat connectivity and population structure is scarce for this species. One hundred and twenty early juveniles (16–35?mm) were collected in April 2014 from six rocky beaches along the western and south Portuguese coasts (Agudela, Cabo do Mundo, Boa Nova, Peniche, Sines and Olhos de Água). δ¹⁸O and δ¹³C were determined by isotope-ratio mass spectrometry. Data were analysed to determine whether isotopic signatures could be used to assess the degree of separation between individuals collected from different locations. Mean δ¹³C and δ¹⁸O values ranged from ?0.02‰ to 1.14‰ and ?7.77‰ to ?6.62‰, respectively. Both seawater temperature and salinity caused differences in otolith δ¹⁸O among the four main sampling areas. The variation among areas in δ¹³C was most likely related to slight differences in the diet, growth and metabolism of fish. The distinct isotopic signatures, at least for the northern and central areas, suggested low levels of connectivity across large spatial scales during the juvenile stage. Furthermore, similar isotopic signatures within the same area indicated some degree of larval oceanic retention at short spatial scales. This study suggests that stable isotope records in otoliths could provide information about the home residency, movements and habitat connectivity of intertidal fishes.     

A multi‐basin approach determines variability in host fish suitability for unionids in tributaries of the Laurentian Great Lakes

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Trophic consequences of non‐native species for commercial fish in a backwater bay of the Three Gorges Reservoir,Southwest China

Trophic niche overlap in native and alien fish species can lead to competitive interactions whereby non‐native fishes outcompete indigenous individuals and eventually affect the viability of natural populations. The species Erythroculter mongolicus and Erythroculter ilishaeformis (belonging to the Culterinae), which are two commercially important fish species in the backwater bay of the Pengxi River in the Three Gorges Reservoir (TGR), were threatened by competition from the non‐native Coilia ectenes (lake anchovy). The latter is an alien species introduced into the lower reaches of the Yangtze River in China and now widespread in the TGR. The trophic consequences of non‐native lake anchovy invasion for E. mongolicus and E. ilishaeformis were assessed using stable isotope analysis (δ¹³C and δ¹⁵N) and associated metrics including the isotopic niche, measured as the standard ellipse area. The trophic niche of native E. mongolicus had little overlap (<15%) with the alien fish species and was significantly reduced in size after invasion by lake anchovy. This suggests that E. mongolicus shifted to a more specialized diet after invasion by lake anchovy. In contrast, the trophic niche overlap of native fish E. ilishaeformis with the alien fish species was larger (>50%) and the niche was obviously increased, implying that fish in this species exploited a wider dietary base to maintain their energetic requirements. Thus, marked changes for the native E. mongolicus and E. ilishaeformis were detected as the trophic consequences of invasion of non‐native lake anchovy.     

Comparative trophic impacts of two globally invasive cyprinid fishes reveal species‐specific invasion consequences for a threatened native fish

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Impacts of zebra mussels (Dreissena polymorpha) on isotopic niche size and niche overlap among fish species in a mesotrophic lake

Zebra mussels (Dreissena polymorpha) filter feed phytoplankton and reduce available pelagic energy, potentially driving fish to use littoral energy sources in lakes. However, changes in food webs and energy flow in complex fish communities after zebra mussel establishment are poorly known. We assessed impacts of zebra mussels on fish littoral carbon use, trophic position, isotopic niche size, and isotopic niche overlap among individual fish species using δ¹³C and δ¹⁵N data collected before (2014) and after (2019) zebra mussel establishment in Lake Ida, MN. Isotope data were collected from 11 fish species, and from zooplankton and littoral invertebrates to estimate baseline isotope values. Mixing models were used to convert fish δ¹³C and δ¹⁵N into estimates of littoral carbon and trophic position, respectively. We tested whether trophic position, littoral carbon use, isotopic niche size, and isotopic niche overlap changed from 2014 to 2019 for each fish species. We found few effects on fish trophic position, but 10 out of 11 fish species increased littoral carbon use after zebra mussel establishment, with mean littoral carbon increasing from 43% before to 67% after establishment. Average isotopic niche size of individual species increased significantly (2.1-fold) post zebra mussels, and pairwise-niche overlap between species increased significantly (1.2-fold). These results indicate zebra mussels increase littoral energy dependence in the fish community, resulting in larger individual isotopic niches and increased isotopic niche overlap. These effects may increase interspecific competition among fish species and could ultimately result in reduced abundance of species less able to utilize littoral energy sources.

     

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

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Physiological and ecological hosts of Popenaias popeii (Bivalvia: Unionidae): laboratory studies identify more hosts than field studies

1. Freshwater mussels are critically endangered in North America, making it important to understand their environmental requirements at all life stages. As glochidia (larvae), they attach to fish hosts where they undergo substantial mortality, making this transition important in their life cycle. Larval host fish requirements have typically been described using data from laboratory infestations to determine suitable hosts. 2. Laboratory infestations circumvent many natural barriers that prevent infestation of physiologically compatible fishes by mussel larvae. While such methods are invaluable for identifying ‘physiological hosts,’ they cannot fully describe realised ‘ecological hosts’ in the field. 3. We studied Popenaias popeii in the Black River in New Mexico, because it is of conservation concern and it is the only mussel species present, facilitating identification of glochidial infestation. To explore the difference between physiological hosts and ecological hosts, we conducted a 3‐year field study of fishes infested by P. popeii glochidia. 4. Substantially fewer fish species were infested by P. popeii in the wild (10 of 20 observed) than had been identified as physiological hosts in laboratory trials (24 of 31). We combined data on fish abundance, proportion of fish hosts infested (prevalence) and the number of glochidia per fish (intensity) and identified three fish species that probably contributed substantially more to mussel recruitment by carrying more glochidia than other host species. 5. Similarities in behaviour among these fishes allowed us to hypothesise routes of infestation, such as benthos‐feeding by catostomids, that allow glochidia to infest these hosts at higher rates than other suitable hosts. Overall, this approach provides a method of quantifying the relative importance of different species of host fish in the mussel lifecycle.     

Trophodynamics of Southern Ocean pteropods on the southern Kerguelen Plateau

Pteropods are a group of small marine gastropods that are highly sensitive to multiple stressors associated with climate change. Their trophic ecology is not well studied, with most research having focused primarily on the effects of ocean acidification on their fragile, aragonite shells. Stable isotopes analysis coupled with isotope‐based Bayesian niche metrics is useful for characterizing the trophic structure of biological assemblages. These approaches have not been implemented for pteropod assemblages. We used isotope‐based Bayesian niche metrics to investigate the trophic relationships of three co‐occurring pteropod species, with distinct feeding behaviors, sampled from the Southern Kerguelen Plateau area in the Indian Sector of the Southern Ocean—a biologically and economically important but poorly studied region. Two of these species were gymnosomes (shell‐less pteropods), which are traditionally regarded as specialist predators on other pteropods, and the third species was a thecosome (shelled pteropod), which are typically generalist omnivores. For each species, we aimed to understand (a) variability and overlap among isotopic niches; and (b) whether there was a relationship between body size and trophic position. Observed isotopic niche areas were broadest for gymnosomes, especially Clione limacina antarctica, whose observed isotopic niche area was wider than expected on both δ¹³C and δ¹⁵N value axes. We also found that trophic position significantly increased with increasing body length for Spongiobranchaea australis. We found no indication of a dietary shift toward increased trophic position with increasing body size for Clio pyramidata f. sulcata. Trophic positions ranged from 2.8 to 3.5, revealing an assemblage composed of both primary and secondary consumer behaviors. This study provides a comprehensive comparative analysis on trophodynamics in Southern Ocean pteropod species, and supports previous studies using gut content, fatty acid and stable isotope analyses. Combined, our results illustrate differences in intraspecific trophic behavior that may be attributed to differential feeding strategies at species level.     

Parasite infection alters host stable‐isotope composition under controlled feeding

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Trophic structure of a coastal fish community determined with diet and stable isotope analyses

A combination of dietary guild analysis and nitrogen (δ¹⁵N) and carbon (δ¹³C) stable‐isotope analysis was used to assess the trophic structure of the fish community in Rhode Island and Block Island Sounds, an area off southern New England identified for offshore wind energy development. In the autumn of 2009, 2010 and 2011, stomach and tissue samples were taken from 20 fish and invertebrate species for analysis of diet composition and δ¹⁵N and δ¹³C signatures. The food chain in Rhode Island and Block Island Sounds comprises approximately four trophic levels within which the fish community is divided into distinct dietary guilds, including planktivores, benthivores, crustacivores and piscivores. Within these guilds, inter‐species isotopic and dietary overlap is high, suggesting that resource partitioning or competitive interactions play a major role in structuring the fish community. Carbon isotopes indicate that most fishes are supported by pelagic phytoplankton, although there is evidence that benthic production also plays a role, particularly for obligate benthivores such as skates Leucoraja spp. This type of analysis is useful for developing an ecosystem‐based approach to management, as it identifies species that act as direct links to basal resources as well as species groups that share trophic roles.     

Stable isotope enrichment in laboratory ant colonies: effects of colony age,metamorphosis, diet,and fat storage

Ecologists use stable isotopes to infer diets and trophic levels of animals in food webs, yet some assumptions underlying these inferences have not been thoroughly tested. We used laboratory‐reared colonies of Solenopsis invicta Buren (Hymenoptera: Formicidae: Solenopsidini) to test the effects of metamorphosis, diet, and lipid storage on carbon and nitrogen stable isotope ratios. Effects of metamorphosis were examined in ant colonies maintained on a control diet of domestic crickets and sucrose solution. Effects of a diet shift were evaluated by adding a tuna supplement to select colonies. Effects of lipid content on stable isotopes were tested by treating worker ants with polar and non‐polar solvents. δ¹³C and δ¹⁵N values of larvae, pupae, and workers were measured by mass spectrometry on whole‐animal preparations. We found a significant effect of colony age on δ¹³C, but not δ¹⁵N; larvae, pupae, and workers collected at 75 days were slightly depleted in ¹³C relative to collections at 15 days (Δδ¹³C = ?0.27‰). Metamorphosis had a significant effect on δ¹⁵N, but not δ¹³C; tissues of each successive developmental stage were increasingly enriched in ¹⁵N (pupae, +0.5‰; workers, +1.4‰). Availability of tuna resulted in further shifts of about +0.6‰ in isotope ratios for all developmental stages. Removing fat with organic solvents had no effect on δ¹³C, but treatment with a non‐polar solvent resulted in enriched δ¹⁵N values of +0.37‰. Identifying regular patterns of isotopic enrichment as described here should improve the utility of stable isotopes in diet studies of insects. Our study suggests that researchers using ¹⁵N enrichment to assess trophic levels of an organism at different sites need to take care not to standardize with immature insect herbivores or predators at one site and mature ones at another. Similar problems may also exist when standardizing with holometabolous insects at one site and spiders or hemimetabolous insects at another site.     

The diverse dietary profiles of MIS 3 cave bears from the Romanian Carpathians: insights from stable isotope (δ13C and δ15N) analysis

Late Pleistocene European cave bears (Ursus spelaeus ) have been considered to be largely vegetarian, although stable isotope data (δ¹³C and δ¹⁵N values) from the Romanian Carpathians has suggested considerable dietary variation. Here we evaluate previous and additional adult cave bear isotopic data from four Marine Isotope Stage 3 (MIS 3) sites in the Carpathians. Pe?tera Ur?ilor (N  =  35), Pe?tera Cioclovina (N  =  32), Pe?tera Muierilor (N  =  8), and Pe?tera cu Oase (N  =  72) provide both a dichotomy between samples suggesting vegetarian diets (from Cioclovina and Muierilor) and more omnivorous diets (from Ur?ilor and Oase), and considerable isotopic variation within samples from each site. While an inference of a strictly vegetarian diet may apply to groups that lived in ecosystems which restricted the available animal protein for these large ursids, the within and between sample isotopic variation among the Carpathian cave bears indicates considerable flexibility in their sources of protein and hence in their dietary regimes. In addition, developmental assessment of Cioclovina isotopic profiles (neonates, juveniles, sub‐adults and adults) provides patterns of transfer of stable isotope signatures throughout immature life for both δ¹³C and δ¹⁵N (increase and decrease, respectively), whereas those from Ur?ilor show little developmental shift.     

Utility of fish scales from stock assessment surveys in stable isotope analysis for initial assessments of trophic relationships in riverine fish communities

The utility of using fish scales collected during stock assessment exercises to assess the trophic relationships of riverine fishes using their stable isotopes of d¹³C and d¹⁵N was tested using three riverine fish communities in England (Rivers Great Ouse, Ivel and Goyt). In each river, European barbel Barbus barbus was an important species, with other cyprinid species, including chub Squalius cephalus, present. Stable isotope analyses was completed using relatively small sample sizes per species (<11) from fish samples collected in 2001, 2005 and 2006 when up to 5 scales were collected from each fish. The calculation of standard ellipse areas (as a measure of trophic niche size) revealed that relative to other fishes, B. barbus occupied high trophic positions with minimal overlap in their trophic niche with other species, especially S. cephalus. As the analysed fish samples comprised species of various length ranges and as length has strong ontogenetic consequences for fish diet composition, generalized linear models were developed in which length was the covariate; model outputs included length‐adjusted mean δ¹³C and δ¹⁵N for each species. In each fish community, significant differences in δ¹³C and δ¹⁵N were apparent between B. barbus and S. cephalus, but were less apparent between B. barbus and other fishes. Thus, whilst the utility of using fish scales from stock assessments in stable isotope analyses are limited due to the differing length ranges of the sampled fishes, they can be useful in identifying trophic differences between species when methods such as stomach content analyses are unavailable.     

Identification of the maternal source of young‐of‐the‐year Arctic charr in Lake Hazen,Canada

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Duration of the parasitic phase determines subsequent performance in juvenile freshwater pearl mussels (Margaritifera margaritifera)

Host–parasite systems have been useful in understanding coevolutionary patterns in sympatric species. Based on the exceptional interaction of the long‐lived and highly host‐specific freshwater pearl mussel (FPM; Margaritifera margaritifera) with its much shorter‐lived host fish (Salmo trutta or Salmo salar), we tested the hypotheses that a longer duration of the parasitic phase increases fitness‐related performance of mussels in their subsequent post parasitic phase, and that temperature is the main factor governing the duration of the parasitic phase. We collected juvenile mussels from naturally and artificially infested fish from eight rivers in Norway. Excysted juvenile mussels were maintained separately for each collection day, under similar temperature and food regimes, for up to 56 days. We recorded size at excystment, post excystment growth, and survival as indicators of juvenile fitness in relation to the duration of the parasitic phase. We also recorded the daily average temperatures for the entire excystment period. We observed strong positive relationships between the length of the parasitic phase and the post parasitic growth rate, size at excystment and post parasitic survival. Temperature was identified as an important factor governing excystment, with higher temperatures decreasing the duration of the parasitic phase. Our results indicate that juvenile mussels with the longest parasitic phase have better resources (larger size and better growth rate) to start their benthic developmental phase and therefore to survive their first winter. Consequently, the parasitic phase is crucial in determining subsequent survival. The temperature dependence of this interaction suggests that climate change may affect the sensitive relationship between endangered FPMs and their fish hosts.     

Stable isotopes and trophic positions of littoral fishes from a Mediterranean marine protected area

Stable isotope analyses were employed to explore feeding and foraging habitats and trophic levels of littoral fishes in a western Mediterranean Marine Protected Area (Egadi Islands, Sicily, Italy). Carbon and nitrogen stable isotope ratios were measured in primary producers, invertebrates and fishes collected in December 2001 and January 2002. Fishes of the littoral region of the Egadi Islands had isotopic signatures that fell into a wider range for δ ¹³C (about 6‰) than for δ ¹⁵N (about 3‰). Carbon isotope ratios were consistent with a food web based on mixed sources and two trophic pathways leading to different fish species. Differences in the isotopic composition between islands were higher for benthivorous than for planktivorous fishes. The overall picture gained from this study is of a isotopic distinction between planktivorous and benthivorous fishes, resource partitioning facilitating the coexistence of similar species within the same ecosystem, and spatial variability in the isotopic signatures and trophic level of fishes. Asymmetrical analysis of variance showed that estimated trophic levels were lower in the area with the highest level of protection (Zone A) for only two out of the nine fishes analysed. As a consequence, overall spatial differences do not seem to be a consequence of protection, since in most cases trophic levels did not change significantly between zone A and zones C where professional fishing (trawling apart) is permitted, but of natural sources of variation (e.g. variability in food availability and site-specific food preferences of fishes). However, the results of this study suggest a different response at the species compared to the community level.     

Trophic redundancy among fishes in an East African nearshore seagrass community inferred from stable‐isotope analysis

Stable‐isotope analysis supplemented with stomach contents data from published sources was used to quantify the trophic niches, trophic niche overlaps and potential trophic redundancy for the most commonly caught fish species from an East African nearshore seagrass community. This assessment is an important first step in quantifying food‐web structure in a region subject to intense fishing activities. Nearshore food webs were driven by at least two isotopically distinct trophic pathways, algal and seagrass, with a greater proportion of the sampled species feeding within the seagrass food web (57%) compared with the algal food web (33%). There was considerable isotopic niche overlap among species (92% of species overlapped with at least one other species). Narrow isotopic niche widths of most (83%) species sampled, low isotopic similarity (only 23% of species exhibited no differences in δ¹³C and δ¹⁵N) and low predicted trophic redundancy among fishes most commonly caught by fishermen (15%), however, suggest that adjustments to resource management concerning harvesting and gear selectivity may be needed for the persistence of artisanal fishing in northern Tanzania. More detailed trophic studies paired with information on spatio‐temporal variation in fish abundance, especially for heavily targeted species, will assist in the development and implementation of management strategies to maintain coastal food‐web integrity.     

Predicting the contributions of novel marine prey resources from angling and anadromy to the diet of a freshwater apex predator

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