Isotopic niche reflects stress-induced variability in physiological status.
ABSTRACT: The isotopic niche has become an established concept in trophic ecology. However, the assumptions behind this approach have rarely been evaluated. Evidence is accumulating that physiological stress can affect both magnitude and inter-individual variability of the isotopic signature in consumers via alterations in metabolic pathways. We hypothesized that stress factors (inadequate nutrition, parasite infestations, and exposure to toxic substances or varying oxygen conditions) might lead to suboptimal physiological performance and altered stable isotope signatures. The latter can be misinterpreted as alterations in isotopic niche. This hypothesis was tested by inducing physiological stress in the deposit-feeding amphipod Monoporeia affinis exposed to either different feeding regimes or contaminated sediments. In the amphipods, we measured body condition indices or reproductive output to assess growth status and ?13C and ?15N values to derive isotope niche metrics. As hypothesized, greater isotopic niche estimates were derived for the stressed animals compared to the control groups. Moreover, the ?15N values were influenced by body size, reproductive status and parasite infestations, while ?13C values were influenced by body size, oxygen conditions and survival. Using regression analysis with isotope composition and growth variables as predictors, we were able to discriminate between the amphipods exposed to nutritionally or chemically stressful conditions and those in the control groups. Thus, interpretation of isotopic niche can be confounded by natural or anthropogenic stressors that may induce an apparent change in isotopic niche. These findings stress the importance of including measures of growth and health status when evaluating stable isotope data in food web studies.
Project description:The isotopic composition of baleen whales' epidermis structural layers can give information about dietary change over time. This study investigated if epidermis layers integrated isotopic values that record physiological changes from gestation to lactation. Epidermis tissues (n = 43) were collected from free ranging lactating female gray whale and calves during the beginning of three breeding seasons. Modelling of ?13C and ?15N values show intra- and inter-individual differences based on epidermal layers, age class and year of sampling. The isotopic composition of mother-calf pairs is correlated, and the estimates of the maximum mother-to-calf isotopic difference was ~1.4‰ for ?13C and between 1 and 1.5‰ for ?15N values. Change in ?15N values among epidermal layers in calves was associated with the transition from fetus to consumption of maternal milk. It is here proposed when lactation influences calf epidermis, ?15N values decrease consistently from the outermost to the innermost layer. However, if a calf was born only few days before collection, epidermis integrates more variable ?15N patterns because gestation still affects the isotopic composition of the layers. The possibility of calculating mother-to-calf nitrogen isotope fractionation, and the regularity of changes between calf layer ?15N values, allowed results of an isotopic clock model to predict the age of each calf when sampled with its mother. This model has the potential to be a straightforward method to estimate the beginning of lactation, therefore calf birth date when direct observations are not feasible. The non-lethal remote collection of epidermis appears to be an effective tool for the study of the physiology of reproduction of baleen whales. The parallel study of the three epidermal structural layers highlighted the importance of considering the unique mother-calf pair physiological status at the time of sampling time when stable isotope results are interpreted.
Project description:Stable isotope analysis (SIA) is an important tool for investigation of animal dietary habits for determination of feeding niche. Ideally, fresh samples should be used for isotopic analysis, but logistics frequently demands preservation of organisms for analysis at a later time. The goal of this study was to establish the best methodology for preserving forest litter-dwelling crickets for later SIA analysis without altering results. We collected two cricket species, Phoremia sp. and Mellopsis doucasae, from which we prepared 70 samples per species, divided among seven treatments: (i) freshly processed (control); preserved in fuel ethanol for (ii) 15 and (iii) 60 days; preserved in commercial ethanol for (iv) 15 and (v) 60 days; fresh material frozen for (vi) 15 and (vii) 60 days. After oven drying, samples were analyzed for ?15N, ?13C values, N(%), C(%) and C/N atomic values using continuous flow isotope ratio mass spectrometry. All preservation methods tested, significantly impacted ?13C and ?15N and C/N atomic values. Chemical preservatives caused ?13C enrichment as great as 1.5‰, and ?15N enrichment as great as 0.9‰; the one exception was M. doucasae stored in ethanol for 15 days, which had ?15N depletion up to 1.8‰. Freezing depleted ?13C and ?15N by up to 0.7 and 2.2‰, respectively. C/N atomic values decreased when stored in ethanol, and increased when frozen for 60 days for both cricket species. Our results indicate that all preservation methods tested in this study altered at least one of the tested isotope values when compared to fresh material (controls). We conclude that only freshly processed material provides adequate SIA results for litter-dwelling crickets.
Project description:Scat is frequently used to study animal diets because it is easy to find and collect, but one concern is that gross fecal analysis (GFA) techniques exaggerate the importance of small-bodied prey to mammalian mesopredator diets. To capitalize on the benefits of scat, we suggest the analysis of scat carbon and nitrogen isotope values (?13C and ?15N). This technique offers researchers a non-invasive method to gather short-term dietary information. We conducted three interrelated studies to validate the use of isotopic values from coyote scat: 1) we determined tissue-to-tissue apparent C and N isotope enrichment factors (?13* and ?15*) for coyotes from road kill animals (n = 4); 2) we derived diet-to-scat isotope discrimination factors for coyotes; and 3) we used field collected coyote scats (n = 12) to compare estimates of coyote dietary proportions from stable isotope mixing models with estimates from two GFA techniques. Scat consistently had the lowest ?13C and ?15N values among the tissues sampled. We derived a diet-to-scat ?13C value of -1.5‰ ± 1.6‰ and ?15N value of 2.3‰ ± 1.3‰ for coyotes. Coyote scat ?13C and ?15N values adjusted for discrimination consistently plot within the isotopic mixing space created by known dietary items. In comparison with GFA results, we found that mixing model estimates of coyote dietary proportions de-emphasize the importance of small-bodied prey. Coyote scat ?13C and ?15N values therefore offer a relatively quick and non-invasive way to gain accurate dietary information.
Project description:Stable isotope analysis in mysticete skin and baleen plates has been repeatedly used to assess diet and movement patterns. Accurate interpretation of isotope data depends on understanding isotopic incorporation rates for metabolically active tissues and growth rates for metabolically inert tissues. The aim of this research was to estimate isotopic incorporation rates in blue whale skin and baleen growth rates by using natural gradients in baseline isotope values between oceanic regions. Nitrogen (?15N) and carbon (?13C) isotope values of blue whale skin and potential prey were analyzed from three foraging zones (Gulf of California, California Current System, and Costa Rica Dome) in the northeast Pacific from 1996-2015. We also measured ?15N and ?13C values along the lengths of baleen plates collected from six blue whales stranded in the 1980s and 2000s. Skin was separated into three strata: basale, externum, and sloughed skin. A mean (±SD) skin isotopic incorporation rate of 163±91 days was estimated by fitting a generalized additive model of the seasonal trend in ?15N values of skin strata collected in the Gulf of California and the California Current System. A mean (±SD) baleen growth rate of 15.5±2.2 cm y-1 was estimated by using seasonal oscillations in ?15N values from three whales. These oscillations also showed that individual whales have a high fidelity to distinct foraging zones in the northeast Pacific across years. The absence of oscillations in ?15N values of baleen sub-samples from three male whales suggests these individuals remained within a specific zone for several years prior to death. ?13C values of both whale tissues (skin and baleen) and potential prey were not distinct among foraging zones. Our results highlight the importance of considering tissue isotopic incorporation and growth rates when studying migratory mysticetes and provide new insights into the individual movement strategies of blue whales.
Project description:The measurement of bulk tissue nitrogen (?15N) and carbon isotope values (?13C) chronologically along biologically inert tissues sampled from offspring can provide a longitudinal record of their mothers' foraging habits. This study tested the important assumption that mother-offspring stable isotope values are positively and linearly correlated. In addition, any change in the mother-offspring bulk tissues and individual amino acids that occurred during gestation was investigated. Whiskers sampled from southern elephant seal pups (Mirounga leonina) and temporally overlapping whiskers from their mothers were analyzed. This included n?=?1895 chronologically subsampled whisker segments for bulk tissue ?15N and ?13C in total and n?=?20 whisker segments for amino acid ?15N values, sampled from recently weaned pups (n?=?17), juvenile southern elephant seals (SES)?<?2 years old (n?=?23) and adult female SES (n?=?17), which included nine mother-offspring pairs. In contrast to previous studies, the mother-offspring pairs were not in isotopic equilibrium or linearly correlated during gestation: the ?15N and ?13C mother-offspring offsets increased by 0.8 and 1.2‰, respectively, during gestation. The foetal bulk ?15N values were 1.7?±?0.5‰ (0.9-2.7‰) higher than mothers' ?15N values before birth, while the foetal ?13C increased by ~1.7‰ during gestation and were 1.0?±?0.5‰ (0.0-1.9‰) higher than their mothers' ?13C at the end of pregnancy. The mother-offspring serine and glycine ?15N differed by ~4.3‰, while the foetal alanine ?15N values were 1.4‰ lower than that of their mothers during the third trimester of pregnancy. The observed mother-offspring ?15N differences are likely explained by shuttling of glutamate-glutamine and glycine-serine amongst skeletal muscle, liver, placenta and foetal tissue. Foetal development relies primarily on remobilized endogenous maternal proteinaceous sources. Researchers should consider foetal physiology when using offspring bulk tissue isotope values as biomarkers for the mother's isotopic composition as part of monitoring programmes.
Project description:Stable isotope analysis of commercially and ecologically important fish can improve understanding of life-history and trophic ecology. However, accurate interpretation of stable isotope values requires knowledge of tissue-specific isotopic turnover that will help to describe differences in the isotopic composition of tissues and diet. We performed a diet-switch experiment using captive-reared parasite-free Eurasian perch (Perca fluviatilis) and wild caught specimens of the same species, infected with the pike tapeworm Triaenophorus nodulosus living in host liver tissue. We hypothesize that metabolic processes related to infection status play a major role in isotopic turnover and examined the influence of parasite infection on isotopic turn-over rate of carbon (?13C), nitrogen (?15N) and sulphur (?34S) in liver, blood and muscle. The ?15N and ?13C turnovers were fastest in liver tissues, followed by blood and muscle. In infected fish, liver and blood ?15N and ?13C turnover rates were similar. However, in infected fish, liver and blood ?13C turnover was faster than that of ?15N. Moreover, in infected subjects, liver ?15N and ?13C turnover rates were three to five times faster than in livers of uninfected subjects (isotopic half-life of ca.3-4 days compared to 16 and 10 days, respectively). Blood ?34S turnover rate were about twice faster in non-infected individuals implying that parasite infection could retard the turnover rate of ?34S and sulphur containing amino acids. Slower turnover rate of essential amino acid could probably decrease individual immune function. These indicate potential hidden costs of chronic and persistent infections that may have accumulated adverse effects and might eventually impair life-history fitness. For the first time, we were able to shift the isotope values of parasites encapsulated in the liver by changing the dietary source of the host. We also report variability in isotopic turnover rates between tissues, elements and between infected and parasite-free individuals. These results contribute to our understanding of data obtained from field and commercial hatcheries; and strongly improve the applicability of the stable isotope method in understanding life-history and trophic ecology of fish populations.
Project description:The sea otter (Enhydra lutris) is a marine mammal hunted to near extinction during the 1800s. Despite their well-known modern importance as a keystone species, we know little about historical sea otter ecology. Here, we characterize the ecological niche of ancient southern sea otters (E. lutris nereis) using ?13C analysis and ?15N analysis of bones recovered from archaeological sites spanning ~7,000 to 350 years before present (N = 112 individuals) at five regions along the coast of California. These data are compared with previously published data on modern animals (N = 165) and potential modern prey items. In addition, we analyze the ?15N of individual amino acids for 23 individuals to test for differences in sea otter trophic ecology through time. After correcting for tissue-specific and temporal isotopic effects, we employ nonparametric statistics and Bayesian niche models to quantify differences among ancient and modern animals. We find ancient otters occupied a larger isotopic niche than nearly all modern localities; likely reflecting broader habitat and prey use in prefur trade populations. In addition, ancient sea otters at the most southerly sites occupied an isotopic niche that was more than twice as large as ancient otters from northerly regions. This likely reflects greater invertebrate prey diversity in southern California relative to northern California. Thus, we suggest the potential dietary niche of sea otters in southern California could be larger than in central and northern California. At two sites, Año Nuevo and Monterey Bay, ancient otters had significantly higher ?15N values than modern populations. Amino acid ?15N data indicated this resulted from shifting baseline isotope values, rather than a change in sea otter trophic ecology. Our results help in better understanding the contemporary ecological role of sea otters and exemplify the strength of combing zooarchaeological and biological information to provide baseline data for conservation efforts.
Project description:Competition for resources within a population can lead to niche partitioning between sexes, throughout ontogeny and among individuals, allowing con-specifics to co-exist. We aimed to quantify such partitioning in Antarctic fur seals, Arctocephalus gazella, breeding at South Georgia, which hosts ~95% of the world's population. Whiskers were collected from 20 adult males and 20 adult females and stable isotope ratios were quantified every 5?mm along the length of each whisker. Nitrogen isotope ratios (?15N) were used as proxies for trophic position and carbon isotope ratios (?13C) indicated foraging habitat. Sexual segregation was evident: ?13C values were significantly lower in males than females, indicating males spent more time foraging south of the Polar Front in maritime Antarctica. In males ?13C values declined with age, suggesting males spent more time foraging south throughout ontogeny. In females ?13C values revealed two main foraging strategies: 70% of females spent most time foraging south of the Polar Front and had similar ?15N values to males, while 30% of females spent most time foraging north of the Polar Front and had significantly higher ?15N values. This niche partitioning may relax competition and ultimately elevate population carrying capacity with implications for ecology, evolution and conservation.
Project description:Climatic variation alters biochemical and ecological processes, but it is difficult both to quantify the magnitude of such changes, and to differentiate long-term shifts from inter-annual variability. Here, we simultaneously quantify decade-scale isotopic variability at the lowest and highest trophic positions in the offshore California Current System (CCS) by measuring ?15N and ?13C values of amino acids in a top predator, the sperm whale (Physeter macrocephalus). Using a time series of skin tissue samples as a biological archive, isotopic records from individual amino acids (AAs) can reveal the proximate factors driving a temporal decline we observed in bulk isotope values (a decline of ?1 ‰) by decoupling changes in primary producer isotope values from those linked to the trophic position of this toothed whale. A continuous decline in baseline (i.e., primary producer) ?15N and ?13C values was observed from 1993 to 2005 (a decrease of ?4‰ for ?15N source-AAs and 3‰ for ?13C essential-AAs), while the trophic position of whales was variable over time and it did not exhibit directional trends. The baseline ?15N and ?13C shifts suggest rapid ongoing changes in the carbon and nitrogen biogeochemical cycling in the offshore CCS, potentially occurring at faster rates than long-term shifts observed elsewhere in the Pacific. While the mechanisms forcing these biogeochemical shifts remain to be determined, our data suggest possible links to natural climate variability, and also corresponding shifts in surface nutrient availability. Our study demonstrates that isotopic analysis of individual amino acids from a top marine mammal predator can be a powerful new approach to reconstructing temporal variation in both biochemical cycling and trophic structure.
Project description:Golden and Blueline Tilefish (Lopholatilus chamaeleonticeps and Caulolatilus microps) are keystone taxa in northwest (NW) Atlantic continental shelf-edge environments due to their biotic (trophic-mediated) and abiotic (ecosystem engineering) functional roles combined with high-value fisheries. Despite this importance, the ecological niche dynamics (i.e., those relating to trophic behavior and food-web interactions) of these sympatric species are poorly understood, knowledge of which may be consequential for maintaining both ecosystem function and fishery sustainability. We used stable isotope ratios of carbon (?13C) and nitrogen (?15N) to build realized ecological niche hypervolumes to serve as proxies for diet and production use patterns of L. chamaeleonticeps and C. microps. We hypothesized that: (a) species exhibit ontogenetic shifts in diet and use of production sources; (b) species acquire energy from spatially distinct resource pools that reflect a sedentary life-history and differential use of the continental shelf-edge; and (c) species exhibit differentiation in one or more measured niche axes. We found evidence for ontogenetic shifts in diet (?15N) but not production source (?13C) in both species, suggesting a subtle expansion of measured ecological niche axes. Spatial interpolation of stable isotope ratios showed distinct latitudinal gradients; for example, individuals were 13C enriched in northern and 15N enriched in southern regions, supporting the assertion that tilefish species acquire energy from regional resource pools. High isotopic overlap was observed among species (?82%); however, when hypervolumes included depth and region of capture, overlap among species substantially decreased to overlap estimates of 15%-77%. This suggests that spatial segregation could alleviate potential competition for resources among tilefish species inhabiting continental shelf-edge environments. Importantly, our results question the consensus interpretation of isotopic overlap estimates as representative of direct competition among species for shared resources or habitats, instead identifying habitat segregation as a possible mechanism for coexistence of tilefish species in the NW Atlantic.