Sea cucumber habitat differentiation and site retention as determined by intraspecific stable isotope variation

Stable carbon and nitrogen isotope ratios (δ¹³C/δ¹⁵N) were assessed as a means to ascertain the recent in situ feeding history of the common New Zealand sea cucumber Australostichopus mollis in relation to nutrient enrichment from a longline green‐lipped mussel (Perna canaliculus) farm in Northern New Zealand. δ¹³C and δ¹⁵N isotopic signatures and the ratios of sea cucumbers sampled from within the impact footprint of the mussel farm were compared with those of sea cucumbers residing on adjacent natural reefs. Sea cucumbers from beneath mussel farming longlines had significantly different δ¹³C stable isotope signatures in comparison with sea cucumbers collected from neighbouring natural reef habitats. This difference supports the hypothesis that sea cucumbers in the same bay maintain distinctly different feeding histories, with those residing beneath mussel farming longlines deriving tissue carbon from sediment impacted by farming activities. This hypothesis is further supported by the finding that the isotope signature of sediment collected from beneath the mussel farm is consistent with the expectation that sea cucumbers were feeding on and consuming sediment enriched with bivalve waste (faeces and pseudo‐faeces). In contrast, the nitrogen stable isotope signature (δ¹⁵N) was found to be similar between sites for both sea cucumbers and assumed food sources. Both findings lend support to the viability of future sea cucumber/green‐lipped mussel farm polyculture systems. Sea cucumbers in different locations (mussel farm, natural reef) possessed distinctly different isotope signatures, suggesting that mixing of sea ranched sea cucumbers with natural reef populations would be negligible or non‐existent. Similarities between the isotope signatures in low metabolic tissue of sea cucumbers residing at the mussel farm site to that of mussel farm‐impacted sediment suggest that cucumbers beneath mussel farms appear to have high rates of retention at the farm site.     

Ecological influences on the difference in δ15N and δ13C values between fish tissues: implications for studies of temporal diet variation

Temporal diet changes can be detected by comparing δ¹³C and δ¹⁵N values between tissues with different isotopic turnover times. However, other factors contribute to disparities in δ¹³C and δ¹⁵N signatures between tissues and could confound the interpretation of stable isotope data. We examined the effects of ecological factors on differences in muscle and liver δ¹³C and δ¹⁵N signatures of Arctic charr [Salvelinus alpinus, (L.)] to determine whether their effects were large enough to influence studies of diet change. In addition, we examined whether differences in lipid content accounted for a significant portion of the differences in δ¹³C values between tissues. Results indicated that life history, diet, reproductive status and gender had significant effects on the differences in δ¹³C values between tissues, while gender and diet significantly affected differences in δ¹⁵N values. Differences in % lipid content between tissues also explained approximately 74% of the observed variation in the difference in δ¹³C values between tissues. The differences in δ¹³C values observed between muscle and liver tissues may be partially explained by physiological differences in lipid storage and use between tissues associated with ecological factor effects. These results demonstrate that ecological factors other than a change in diet can influence the differences in δ¹³C and δ¹⁵N signatures between muscle and liver tissues. However, the impact of ecological factors on studies of diet change depends on how the magnitude of the factor effects compared with a biologically meaningful change in diet.     

Using stable isotope data to quantify niche overlap and diets of muskellunge,northern pike and walleye in a deep Minnesota lake

Muskellunge (Esox masquinongy Mitchill), northern pike (Esox lucius L.) and walleye (Sander vitreus Mitchill) often coexist in lake communities, yet uncertainty exists about the potential for interspecific competition among these top predators. Stable isotope data were used to assess niche overlap and diets of these predators in Elk Lake (Minnesota, U.S.A). δ¹³C indicated primary production sources (e.g. pelagic v. littoral) and δ¹⁵N indicated trophic position; the bivariate distribution of these isotopes defined the species’ isotopic niche. Niche overlap probabilities were calculated and stable isotope mixing models were used to quantify diet proportions. Muskellunge and northern pike niches overlapped little (<10%), while walleye overlapped muskellunge (15%–60%) and northern pike (33%–53%) more extensively. Muskellunge diets focused (50%) on cisco (Coregonus artedi Lesueur), walleye primarily assimilated non-cisco prey fish (80%), and northern pike diets were dominated by non-cisco prey fish (45%) and invertebrates (40%). The presence of a cisco population and the flexibility of northern pike to use invertebrate resources may decrease potential competition among these predators. However, cisco are threatened by climate change and eutrophication, and our results suggest that extirpation of cisco may cause major changes in potential competitive interactions among these top predators. Moreover, cisco were unique among prey species in their ability to exploit pelagic energy, such that loss of cisco will likely alter energy flow in lake food webs where they currently exist.     

Stable carbon (δ13C) and nitrogen (δ15N) isotopes as natural indicators of live and dry food in Piaractus mesopotamicus (Holmberg, 1887) larval tissue

This study proposed the use of the stable isotope technique to track the type of food utilized by pacu Piaractus mesopotamicus larvae during their development, and to identify the moment when the larvae start using nutrients from the dry diet by retaining its carbon and nitrogen atoms in their body tissues. Five‐day‐old pacu larvae at the onset of exogenous feeding were fed Artemia nauplii or formulated diet exclusively; nauplii+formulated diet during the entire period; or were weaned from nauplii to a dry diet after 3, 6 or 12 days after the first feeding. δ¹³C and δ¹⁵N values for Artemia nauplii were ?15.1‰ and 4.7‰, respectively, and ?25.0‰ and 7.4‰ for the dry diet. The initial isotopic composition of the larval tissue was ?20.2‰ and 9.5‰ for δ¹³C and δ¹⁵N respectively. Later, at the end of a 42‐day feeding period, larvae fed Artemia nauplii alone reached values of ?12.7‰ and 7.0‰ for δ¹³C and δ¹⁵N respectively. Larvae that received the formulated diet alone showed values of ?22.7‰ for δ¹³C and 9.6‰ for δ¹⁵N. The stable isotope technique was precise, and the time at which the larvae utilized Artemia nauplii, and later dry diet as a food source could be clearly defined.     

Uncertainties associated with trophic discrimination factor and body size complicate calculation of δ15N-derived trophic positions in Arapaima sp.

Stable isotope ratios of nitrogen (δ¹⁵N) have been used to estimate trophic position (TP) of organisms due to the predictable enrichment of nitrogen-15 in consumer tissues relative to their diet. We explored estimates of trophic position using liver and muscle δ¹⁵N and stomach content analysis in a broad size range of Arapaima sp. from Amazonian floodplain lakes. Estimates of TP based on liver δ¹⁵N were more closely related to the stomach content data than estimates based on muscle δ¹⁵N, possibly because of the higher turnover of nitrogen in liver. Total length and season explained most of the variation in TP values estimated from δ¹⁵N, showing that they have more effect than prey trophic position on δ¹⁵N values. The TP estimated by identification of stomach content was 3.6 and was unrelated to the size of the arapaima. This highlights the need for a better understanding of the factors that affect values of δ¹⁵N and stomach content analysis is still needed to unravel the trophic ecology of predatory fishes.     

Tissue‐specific stable isotope ratios of shortfin mako (Isurus oxyrinchus) and white (Carcharodon carcharias) sharks as indicators of size‐based differences in foraging habitat and trophic level

We evaluated whether the trophic level and feeding grounds (coastal versus offshore) of white and shortfin mako sharks captured in the northern Mexican Pacific varied as a function of size using carbon (δ¹³C values) and nitrogen (δ¹⁵N values) stable isotope analysis of soft tissues. A step increase in δ¹⁵N values was observed at approximately 85 cm TL and 150–170 cm TL for shortfin mako and white sharks, respectively, consistent with the dilution of the maternal isotopic signal following the incorporation of exogenous food. Shortfin mako and white shark muscle tissue and whole blood were enriched in ¹⁵N as a function of size, which is consistent with increasing trophic level, but this pattern may be confounded by differences in habitat. To infer differences in foraging habitat throughout life, we compared isotope ratios of liver and blood fractions with those of white muscle tissue; these tissues have relatively faster and slower isotope turnover rates, respectively. Whole blood and muscle δ¹³C values of small white sharks (<200 cm total length) caught near the coast suggested benthic foraging. Very limited differences between δ¹³C values of muscle tissue and whole blood from small and medium mako (<196 cm TL) and small white sharks indicated equilibrium to local feeding grounds. In contrast, differences in the δ¹³C values of liver tissue from small and medium mako and small white sharks indicated changes in diet or feeding grounds. The δ¹³C values of plasma and muscle tissue of large white sharks (>350 cm total length) caught offshore indicate feeding in coastal and oceanic areas and are consistent with recent migration to pelagic feeding grounds. Our study provides insight into size‐based habitat use and migration patterns of two species of migratory sharks for which there is limited information, particularly in their nursery grounds in Mexican waters.     

Sympatric walleye Sander vitreus and sauger Sander canadensis in large reservoirs: Variable isotopic niche size and overlap across multiple time scales

Walleye Sander vitreus (Mitchill) and sauger Sander canadensis (Griffith & Smith) may occupy similar niches in sympatric populations, but their long‐term resource use is poorly studied. Multi‐tissue (liver, muscle and bone) isotopic niche analyses were used to compare resource use by these species in two large reservoirs in Saskatchewan, Canada. Population isotopic niches were larger for sauger (1.73‰²–3.60‰²) than walleye (0.51‰²–2.61‰²) in Lake Diefenbaker, but opposite in Tobin Lake (sauger = 0.54‰²–2.57‰²; walleye = 1.30‰²–2.94‰²). Analyses of population overlap suggest that these species co‐exist via niche partitioning, but partitioning was more pronounced in Lake Diefenbaker (overlap = 6%–38%; Tobin Lake overlap = 18%–62%). The size of individual niches and levels of intra‐ and interspecific overlap among individual fish also varied with reservoir. This study shows that walleye and sauger use different resources across different time scales, but the degree of partitioning can vary markedly with environment.     

Identifying female foraging ecotype and fisheries impacts through pup whisker stable isotopes

1. Individual specialization in the foraging behaviour of marine predators can affect the ecology, evolution, and ability of a population to respond to environmental variability and human impacts.
2. Here, blood serum and whisker stable isotope values from New Zealand (NZ) sea lion pups (Phocarctos hookeri) are compared with their mother’s values to identify whether they can be used as proxies to identify their mother’s isotopic niche and foraging strategy.
3. Female NZ sea lions have been identified, both through telemetry and stable isotope research of blood serum and whiskers, to have two distinct foraging ecotypes (mesopelagic or benthic), consistent across their adult life. Females who are mesopelagic foragers have higher overlap and a greater risk of harmful interactions with fisheries.
4. Stable isotope analysis of adult females can be used to determine the proportion of the female population exposed to these detrimental interactions. However, the capture, restraint, and removal of a whisker or blood from an adult female NZ sea lion is an expensive, time-consuming, and invasive undertaking. Instead, by comparing the blood serum and whisker δ¹³C and δ¹⁵N values of 12 NZ sea lion mother-and-pup pairs, for whom the foraging behaviour of the female is known, the question as to whether a pup’s blood serum or whisker isotope value can be used as a proxy to identify female foraging ecotype was investigated.
5. The δ¹³C and δ¹⁵N values for the blood serum and whiskers of pups and their mothers were correlated and differed significantly between foraging ecotypes. This research validates that pup blood serum and whisker stable isotope values from 1-month-old pups can be used as indicators of female isotopic niche and therefore foraging ecotype.
6. This tool can be used across all NZ sea lion colonies to indicate female NZ sea lion foraging ecotypes. For the Auckland Islands, it could determine the proportion of breeding females exposed to negative interactions with fisheries, leading to a better understanding of the level of these effects and helping to implement appropriate management to mitigate impacts.

     

Seasonal and spatial variations of the food web structure in a shallow eutrophic lake assessed by stable isotope analysis

Stable isotope analysis was used to investigate seasonal and spatial variations of the food web structure in a large eutrophic lake ecosystem (Lake Taihu, China). Basal food sources, invertebrates and fish were sampled in two lake regions with different environmental conditions and spatial variations in the isotopic composition of lake food webs were found. Overall, more depleted δ¹³C and enriched δ¹⁵N isotope values of organic matter sources and consumers were found in the phytoplankton-dominated lake region than in the macrophyte-dominated region. Wide seasonal variations in the isotopic ratios were also observed in the lake biota, with a general trend towards enriched δ¹³C and δ¹⁵N values in summer and depleted values in winter. This pattern could be explained by a combination of environmental (e.g., irradiance and nutrient inputs) and biotic (e.g., availability of food sources and plasticity in prey item choice) features. Results of isotope mass balance suggest that macrophytes provide some trophic support in the macrophyte-dominated area, but in both lake regions it is more likely that aquatic food webs are phytoplankton based rather than macrophyte based under eutrophic conditions.     

Stock structure of blue threadfin Eleutheronema tetradactylum across northern Australia as inferred from stable isotopes in sagittal otolith carbonate

Abstract Stable isotopes of δ¹⁸O and δ¹³C in sagittal otolith carbonates were used to determine the stock structure of the polynemid Eleutheronema tetradactylum (Shaw) across tropical northern Australia, where this species is an important component of inshore commercial and recreational fisheries. Stable isotopes from the sagittal otolith carbonate of 470 fish from 11 discrete locations across western, northern and eastern Australia were sampled between 2007 and 2009. Analysis of these stable isotopes revealed different location‐specific signatures, indicating strong population subdivision. The significant differences in the isotopic signatures of E. tetradactylum demonstrated that there is unlikely to be substantial movement of fish between these locations. The spatial separation of these populations indicates a complex fine spatial scale stock structure across northern Australia, with at least 11 stocks or management units present. The population subdivision of E. tetradactylum was evident along expansive stretches of open beach systems and within coastal embayments with no physical barriers such as headlands. These results indicate that optimal fisheries management will require a review of the current spatial arrangements, particularly the potential for localised depletion of stocks on small spatial scales.     

Using stable isotope analysis to assess the relationship among dietary protein sources,growth, nutrient turnover and incorporation in Nile tilapia (Oreochromis niloticus)

Nile tilapia (1.20 g) were fed for 56 days in five treatments (FM100 containing only fish meal [FM] as a protein source; soybean meal (SBM) replace 25%, 50%, 75% and 100% of FM protein in the diets of FM75, FM50, FM25 and FM0, respectively) to assess the effects of dietary protein sources on growth, turnover half‐life of nitrogen and carbon stable isotopes (δ¹³C and δ¹⁵N) in muscle, isotope discrimination factors (Δ¹⁵N and Δ¹³C), and the relative contribution of protein sources to muscle growth. Results showed that the final body weight, weight gain and specific growth rate of fish fed diet FM25 were significantly higher than other treatments (p < .05). By day 35, fish under all treatments reached isotopic equilibrium, and the equilibrium values consistently increase as a function of stable isotope values in diets. Growth accounted for most isotopic changes in muscle and resulted in significantly shorter half‐lives of nitrogen and carbon in FM25 (p < .05). The Δ¹⁵N of FM25 and Δ¹³C of FM0 were significantly lower than other treatments (p < .05). The proportional contributions of SBM protein were significantly higher than their respective levels in FM75 and FM25 (p < .05), indicating a preferential incorporation of nitrogen from the SBM in muscle tissue.     

A comparison of changes in stable isotope ratios in the epidermal mucus and muscle tissue of slow‐growing adult catfish

Although stable isotope analysis is a powerful tool for determining diet, migration patterns and the structure of food webs in aquatic systems, the slow response of isotopic ratios in the widely used muscle tissue often hampers this approach, particularly in slow‐growing or adult fishes. We conducted a diet‐switch experiment to compare the changes in the stable carbon isotope ratio (δ¹³C values) in the epidermal mucus and muscle tissue of five‐year‐old catfish (Silurus asotus). The isotope ratios in noninvasively sampled mucus changed more rapidly than those in the muscle tissue. As isotopic change in mucus was relatively rapid, this technique can be used over a finer timescale than traditional isotopic analyses using the muscle tissue. The isotopic change half‐life in our experimental condition was 200 days, which would not be short enough for some research purposes. Examining mucus along with the muscle would enable food habits of slow‐growing fishes to be determined over different timescales. However, the rate of isotopic change in the mucus was negatively affected by the size of fish and was slower than the previously reported rates in juvenile steelhead. These findings suggest that mucus turnover rates need to be determined prior to the field data interpretation.     

Stable isotope evaluation of population‐ and individual‐level diet variability in a large,oligotrophic lake with non‐native lake trout

Non‐native piscivores can alter food web dynamics; therefore, evaluating interspecific relationships is vital for conservation and management of ecosystems with introduced fishes. Priest Lake, Idaho, supports a number of introduced species, including lake trout Salvelinus namaycush, brook trout S. fontinalis and opossum shrimp Mysis diluviana. In this study, we used stable isotopes (δ¹³C and δ¹⁵N) to describe the food web structure of Priest Lake and to test hypotheses about apparent patterns in lake trout growth. We found that isotopic niches of species using pelagic‐origin carbon did not overlap with those using more littoral‐origin carbon. Species using more littoral‐origin carbon, such as brook trout and westslope cutthroat trout Oncorhynchus clarki lewisi, exhibited a high degree of isotopic niche overlap and high intrapopulation variability in resource use. Although we hypothesised that lake trout would experience an ontogenetic diet shift, no such patterns were apparent in isotopic signatures. Lake trout growth rates were not associated with patterns in δ¹⁵N, indicating that variation in adult body composition may not be related to adult diet. Understanding trophic relationships at both the individual and species levels provides a more complete understanding of food webs altered by non‐native species.     

Stable isotope ratios of egg albumen of three waterbird species nesting in the Colorado River Delta indicate differences in foraging ground and isotopic niche breadth

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Investigation of geographic origin,salinity and feed on stable isotope profile of Pacific white shrimp (Litopenaeus vannamei)

Increasing numbers of mislabelled seafood products in the globalized market underline the need for approaches to identify the origin of these products. Pacific white shrimp cultured in different salinities (Litopenaeus vannamei) from 16 locations in China and USA were collected and differentiated based on δ¹³C and δ¹⁵N values. The δ¹³C and δ¹⁵N values of 16 commercial feeds used in shrimp culture were measured and effects of feed on C and N stable isotope composition in shrimp were investigated. Carbon and nitrogen isotopic analysis of the shrimp did not provide means to discriminate farmed shrimp from China and USA. However, the shrimp cultured in water with high salinity were enriched in ¹³C compared to shrimp cultured in freshwater and this provided another basis for discrimination. The correlation between δ¹³C in feed and shrimp was not significant, while the δ¹⁵N in feed and shrimp showed a trend of positive correlation.     

Influences of ocean conditions and feeding ecology on the survival of juvenile Chinook Salmon (Oncorhynchus tshawytscha)

Recruitment variability in many fish populations is postulated to be influenced by climatic and oceanographic variability. However, a mechanistic understanding of the influence of specific variables on recruitment is generally lacking. Feeding ecology is one possible mechanism that more directly links ocean conditions and recruitment. We test this mechanism using juvenile Chinook Salmon (Oncorhynchus tshawytscha) collected off the west coast of Vancouver Island, British Columbia, Canada, in 2000–2009. Stable isotopes of carbon (δ¹³C), an indicator of temperature or primary productivity, and nitrogen (δ¹⁵N), an indicator of trophic position, were taken from muscle tissues of genetically stock‐identified salmon. We also collated large‐scale climate indices (e.g., Pacific Decadal Oscillation, North Pacific Gyre Oscillation), local climate variables (e.g., sea surface temperature) and copepod community composition across these years. We used a Bayesian network to determine how ocean conditions influenced feeding ecology, and subsequent survival rates. We found that smolt survival of Chinook Salmon is predicted by their δ¹³C value, but not their δ¹⁵N. In turn, large‐scale climate variability determined the δ¹³C values of salmon, thus linking climate to survival through feeding ecology, likely through qualities propagated from the base of the food chain.     

Stable isotope ratios in archived striped bass scales suggest changes in trophic structure

Stable carbon isotope ratios were measured in archived striped bass, Morone saxatilis (Walbaum), scales to identify changes in the feeding behaviour of this species over time. Striped bass tissue and scale samples were collected from Rhode Island coastal waters during 1996 and archived scale samples (1982–1997) were obtained from Chesapeake Bay. Known striped bass prey items were also collected from Chesapeake Bay and analysed for δ¹³C. A significant correlation was observed between carbon isotope ratios in striped bass scales and muscle tissue (r² = 0.52; P < 0.05). Carbon isotope ratios were enriched (less negative) in scales relative to muscle tissue by about 3‰. Carbon isotope ratios in archived striped bass scales from Chesapeake Bay increased significantly from ?16.7 ± 0.2‰ in 1982 to ?15.1 ± 0.3‰ in 1997. Benthic species, especially invertebrates, were isotopically enriched relative to pelagic fish species collected from the main‐stem of Chesapeake Bay. Prey samples collected from riverine locations within Chesapeake Bay were isotopically depleted relative to those collected in the open portion of the Bay. The changes in the carbon isotope ratios of the striped bass scales could be related to changes in the relative proportions of pelagic and benthic food items in the diet of striped bass or to changes in the feeding locations of this species. In either case, there have been changes in the feeding behaviour and/or relationships of the striped bass between 1982 and 1997. Such changes may be related to changing ecological conditions within the estuary, which could influence the health of Chesapeake Bay striped bass.     

Feeding on the edge: δ13C analysis of a macrofauna food web from disappearing seagrass beds in a polluted urban harbour – implications for biomonitoring and restoration efforts

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Assessing the food web impacts of an anadromous Arctic charr introduction to a sub‐Arctic watershed using stable isotopes

Anadromous Arctic charr, Salvelinus alpinus (L.), was introduced to a sub‐Arctic river–lake system near the village of Kujjuuaq, Nunavik, and the stable isotope values and diets of key resident fish species were used to assess changes in feeding patterns. Stable isotope values for most species did not differ significantly between the pre‐ and post‐introduction periods, with observed shifts being within the bounds of expected natural variation. Lake chub, Couesius plumbeus (Agassiz), were the single species to show a difference between study periods, with a small but significant increase in δ¹⁵N. No significant post‐introduction changes were seen in lake trout, Salvelinus namaycush (Walbaum), omnivory or in any of the assessed quantitative food web metrics. Gut contents of major fish species similarly showed significant temporal overlap between the pre‐ and post‐introduction periods, and there was no significant change in species' weight–length relationships. The minor ecological impact was interpreted in relation to the availability of open niches exploitable by ecological generalists such as Arctic charr. The explanation accords with the known habitat and feeding flexibility of Arctic charr and the ecological immaturity of sub‐Arctic lakes known to have driven adaptive variation among Arctic charr. Findings suggest that anadromous Arctic charr may be introduced at moderate densities to other sub‐Arctic watersheds without major negative food web consequences for other resident fish species.