•There wasn’t significant partition of resources between males and females of vaquita.•Matures individuals showed a more selective feeding spectrum than immatures.•The niche analysis results ...suggested changes in the vaquita’s habitat and prey composition.•The vaquita had a high trophic level and feeding mainly on benthic prey.
The worldwide smallest cetacean, the vaquita (Phocoena sinus), is on the verge of extinction with fewer than 20 individuals left as of summer 2018. The main cause of mortality is bycatch by entanglement in illegal gillnets and environmental changes. Habitat disturbances have negatively impacted prey diversity, and therefore, the vaquita’s feeding success. We investigated the trophic niche of the vaquita and its variability from 1985 to 1993 by quantifying δ13C and δ15N values from bone samples (n = 33). We reconstructed part of vaquita’s refuge food web and identified some prey items. Between 1985 and 1993 the vaquita’s isotopic ellipses shifted moderately, δ13C and δ15N without significant differences, suggesting variations in habitat baseline values and probably prey composition. We observed a high overlap in the ellipses between males and females, suggesting that both sexes were feeding in the same geographic area over several years and with similar prey composition. Together, our results indicate that the vaquita is a generalist high-TL consumer, feeding on benthic and small pelagic prey it maintained similar mean δ15N values for years. Given these results, conservation efforts should intensify to protect the biodiversity of the Upper Gulf of California and the surviving vaquita.
The use of amino acid (AA) nitrogen stable isotopes (δ15N) from consumer tissues aims to provide precise estimates of trophic position (TP), but the drivers of AA isotope fractionation remain ...unclear. In particular, the main factors driving the variability in TEFAA among taxonomic groups and trophic levels remain largely unexplained, which challenges the application of universal values for TEFs. While the relationship between protein content and quality and TEFs has been examined, studies have yielded inconsistent results, and the role of protein and lipid nutritional requirements as well as feeding regime have not been considered. Likewise, drivers that influence physiological and nutritional processes have not been examined relative to TEFAA variation. We conducted a meta‐analysis of controlled feeding experiments within a single group, teleosts fishes, to evaluate the relationship between five nutritional factors (protein and lipid content, protein and lipid content relative to nutritional requirements, and feeding regime) and three ecological drivers (diet type, life stage, and habitat type) on TEFAA. We considered a broad range of protein levels (8–71%) in diets and found no relationship between source TEFAAs and percent protein relative to nutritional requirements, whereas lipid content relative to nutrient requirements, feeding regime and habitat type partially explain the variability in TEFs of Lys, but not for Phe and Met TEFs. The variability for the latter was representative of robust source AAs. Among trophic AAs, Asp, Ile, Pro, and Leu TEFs were significantly higher in species from brackish than marine habitats possibly due to osmoregulation involvement. TEFGlu was sensitive to protein content and feeding regime within teleosts, but relatively constant when comparing TEFs among teleosts, non‐teleosts, and all taxa. Our results indicate that TEFAA is less variable within a single taxon than among multiple taxa and that such variation is not negligible. Our results indicate that δ15NAA values could provide better TP estimates if using taxon‐specific values, and highlights the need to explain the mechanisms of AA fractionation and quantify the variability in TEFs used during error propagation for TP estimates.
Compound-specific isotope analysis (CSIA) of amino acids (AAs) in consumer tissues is a developing technique with wide-ranging applications for identifying nitrogen (N) sources and estimating animal ...trophic level. Controlled experiments are essential for determining which dietary conditions influence variability in N stable isotopes (δ
N) trophic enrichment factors in bulk tissue (TEF
) and AAs (TEF
). To date, however, studies have not independently evaluated the effect of protein quantity and quality (digestibility) on TEFs, complicating the application of AA-δ
N values for estimating trophic levels. We conducted a 98-d feeding experiment using five formulated isoenergetic feeds prepared with a high-quality protein source to evaluate the effect of protein quantity and quality on TEFs of liver and muscle tissues of juvenile Pacific yellowtail (
), a carnivorous fish species. We decreased protein digestibility using well-established protocols that do not change AA profiles. Growth rates were higher in diets with higher protein content, and isotopic equilibrium was reached for both fish tissues and all treatments. Protein quantity and quality influenced isotope discrimination depending on tissue type and AA. In liver tissue, bulk TEFs showed a limited but significant relationship with protein quality, but did not differ with protein quantity or quality in muscle. None of the pre-established source AAs (Lys, Met, Phe, and Gly) TEFs varied significantly with protein quantity or quality in liver tissue. However, in muscle tissue, TEF
increased significantly with protein content and decreased in response to reduced digestibility, indicating it may not serve as proxy for baseline isotopic values used to calculate trophic level. Among trophic AAs, TEF
decreased significantly with increasing protein quantity in liver tissue, while both Leu and Ile TEFs decreased with lower protein digestibility in muscle tissue. Our results indicate that CSIA-AA in liver tissue provides more robust source and trophic AA-δ
N values than in muscle.
Compound‐specific isotope analysis (CSIA) of amino acids (AAs) in consumer tissues is a developing technique with wide‐ranging applications for identifying nitrogen (N) sources and estimating animal ...trophic level. Controlled experiments are essential for determining which dietary conditions influence variability in N stable isotopes (δ15N) trophic enrichment factors in bulk tissue (TEFbulk) and AAs (TEFAA). To date, however, studies have not independently evaluated the effect of protein quantity and quality (digestibility) on TEFs, complicating the application of AA‐δ15N values for estimating trophic levels. We conducted a 98‐d feeding experiment using five formulated isoenergetic feeds prepared with a high‐quality protein source to evaluate the effect of protein quantity and quality on TEFs of liver and muscle tissues of juvenile Pacific yellowtail (Seriola lalandi), a carnivorous fish species. We decreased protein digestibility using well‐established protocols that do not change AA profiles. Growth rates were higher in diets with higher protein content, and isotopic equilibrium was reached for both fish tissues and all treatments. Protein quantity and quality influenced isotope discrimination depending on tissue type and AA. In liver tissue, bulk TEFs showed a limited but significant relationship with protein quality, but did not differ with protein quantity or quality in muscle. None of the pre‐established source AAs (Lys, Met, Phe, and Gly) TEFs varied significantly with protein quantity or quality in liver tissue. However, in muscle tissue, TEFPhe increased significantly with protein content and decreased in response to reduced digestibility, indicating it may not serve as proxy for baseline isotopic values used to calculate trophic level. Among trophic AAs, TEFLeu decreased significantly with increasing protein quantity in liver tissue, while both Leu and Ile TEFs decreased with lower protein digestibility in muscle tissue. Our results indicate that CSIA‐AA in liver tissue provides more robust source and trophic AA‐δ15N values than in muscle.
We show that protein quantity and quality influence isotope discrimination depending on the AA and tissue type, probably due to tissue‐specific energetic requirements and metabolism. Our results support the use of the isotopic composition of liver tissue as robust source and trophic amino acids. Some AA in muscle tissue (Phe, Leu, and Ile) may be more sensitive to variations in dietary protein quantity and quality, and may not serve as proxies for baseline isotopic values or trophic level.
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 δ15N and δ13C 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) δ15N and δ13C values was observed from 1993 to 2005 (a decrease of ∼4‰ for δ15N source-AAs and 3‰ for δ13C essential-AAs), while the trophic position of whales was variable over time and it did not exhibit directional trends. The baseline δ15N and δ13C 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.
Understanding the effect of stage‐specific traits on species feeding habits can reveal how natural selection shapes life strategies. Amino acid (AA) nitrogen stable isotopes (δ15N) provide multiple ...proxies of habitat baseline values and diet that can improve our understanding of species feeding strategies relative to their animal metabolism. We evaluated the effect of body length as a proxy for life stage and sex on the feeding habits of the common dolphin Delphinus delphis delphis using δ13C and δ15N in bulk tissue and AAs δ15N from skin samples collected for almost two decades.
For bulk δ13C and δ15N data, we used SIBER analysis to compare isotopic niches by sex and life stage. For AA δ15N data, we developed a hierarchical Bayesian model (HBM) to estimate indices of trophic status (Δ15N and trophic position). The model reflected the natural hierarchical structure of AA data by partitioning variability into three sources: between laboratory replicates, within dolphins and among dolphins.
Estimates of Δ15N based on all trophic and source AAs were more precise for each dolphin, less variable among dolphins and on average 2.4‰ higher than indices based on single trophic (Glx) and source (Phe) AAs. Precision was further increased when information was shared among individuals through random effects or regression models. Estimates of trophic position showed similar patterns. Both Δ15N and δ15Nbulk isotopic niches showed no difference by sex, suggesting that males and females have similar feeding habits and may not segregate. However, lower Δ15N values for weaning calves and smaller juveniles discriminate them from adults, whereas δ15N bulk isotopic niches do not. A trophic discrimination factor (TDFTro‐Src) of 3.1‰ was required for reasonable estimates of trophic position for these dolphins.
Together, the lack of δ15N differences between sexes, low variation between juveniles and adults and knowledge of common dolphins' social organization support intraspecific feeding cooperation as an important strategy to feed in the highly dynamic marine environment. Our study also presents an efficient way to analyse complex AA δ15N data using HBM to investigate foraging behaviour in long‐lived marine species difficult to study in the wild.
Our long‐term study provides insights about the ontogeny of common dolphin feeding strategies using δ13C and δ15N values from skin, and amino acid δ15N values analyzed with Bayesian statistics. The latter included development of a hierarchical Bayesian model for analyses of complex amino acid δ15N data. Photo: NOAA Fisheries, SWFSC under permit 774‐1714‐10.
Understanding the effect of stage-specific traits on species feeding habits can reveal how natural selection shapes life strategies. Amino acid (AA) nitrogen stable isotopes (δ
N) provide multiple ...proxies of habitat baseline values and diet that can improve our understanding of species feeding strategies relative to their animal metabolism. We evaluated the effect of body length as a proxy for life stage and sex on the feeding habits of the common dolphin Delphinus delphis delphis using δ
C and δ
N in bulk tissue and AAs δ
N from skin samples collected for almost two decades. For bulk δ
C and δ
N data, we used SIBER analysis to compare isotopic niches by sex and life stage. For AA δ
N data, we developed a hierarchical Bayesian model (HBM) to estimate indices of trophic status (Δ
N and trophic position). The model reflected the natural hierarchical structure of AA data by partitioning variability into three sources: between laboratory replicates, within dolphins and among dolphins. Estimates of Δ
N based on all trophic and source AAs were more precise for each dolphin, less variable among dolphins and on average 2.4‰ higher than indices based on single trophic (Glx) and source (Phe) AAs. Precision was further increased when information was shared among individuals through random effects or regression models. Estimates of trophic position showed similar patterns. Both Δ
N and δ
N
isotopic niches showed no difference by sex, suggesting that males and females have similar feeding habits and may not segregate. However, lower Δ
N values for weaning calves and smaller juveniles discriminate them from adults, whereas δ
N bulk isotopic niches do not. A trophic discrimination factor (TDF
) of 3.1‰ was required for reasonable estimates of trophic position for these dolphins. Together, the lack of δ
N differences between sexes, low variation between juveniles and adults and knowledge of common dolphins' social organization support intraspecific feeding cooperation as an important strategy to feed in the highly dynamic marine environment. Our study also presents an efficient way to analyse complex AA δ
N data using HBM to investigate foraging behaviour in long-lived marine species difficult to study in the wild.
•Isotope analysis and DA measurements are a novel method to study DA transfer.•Foraging characteristics contribute to a population's capacity to accumulate toxins.•Anchovies are better sentinel ...species for coastal-pelagic regions than mussels.•Prey size selectivity explains the capacity for anchovies to accumulate DA.•DA accumulation and δ13C gradients reflect spatial mismatches.•Baseline isotope values of C and N differ among habitats.
Given the effects of harmful algal blooms (HABs) on human and wildlife health, understanding how domoic acid (DA) is accumulated and transferred through food webs is critical for recognizing the most affected marine communities and predicting ecosystem effects. This study combines stable isotopes of carbon (δ13C) and nitrogen (δ15N) from bulk muscle tissue with DA measurements from viscera to identify the foraging strategies of important DA vectors and predators in Monterey Bay, CA. Tissue samples were collected from 27 species across three habitats in the summer of 2018 and 2019 (time periods without prominent HABs). Our results highlight an inshore-offshore variation in krill δ13C values and DA concentrations (DA; ppm) in anchovies indicating differences in coastal productivity and DA accumulation. The narrow overlapping isotopic niches between anchovies and sardines suggest similar diets and trophic positions, but striking differences in DA indicate a degree of specialization, thus, resource partitioning. In contrast, krill, market squid, and juvenile rockfish accumulated minimal DA and had comparatively broad isotopic niches, suggesting a lower capacity to serve as vectors because of potential differences in diet or feeding in isotopically distinct locations. Low DA in the liver of stranded sea lions and their generalist foraging tendencies limits our ability to use them as sentinels for DA outbreaks in a specific geographic area. Collectively, our results show that DA was produced a few kilometers from the coastline, and anchovies were the most powerful DA vector in coastal-pelagic zones (their DA loads exceeded the 20 ppm FDA regulatory limits for human consumption), while mussels did not contain detectable DA and only reflect in situ DA, δ13C, and δ15N values. Our study demonstrates the efficacy of combining multiple biogeochemical tracers to improve HAB monitoring efforts and identify the main routes of DA transfer across habitats and trophic levels.
In a wide range of sexually reproducing marine organisms, males and females coexist through niche separation to reduce intraspecific competition and maximize survival; however, sexual segregation in ...mesopelagic cephalopods is poorly understood. To evaluate ontogenetic differences in diet and habitat partitioning between juvenile female and male jumbo squid Dosidicus gigas, we determined age and maturity, quantified stable isotope ratios along gladii bulk tissue and individual amino acids (AAs), and analyzed morphometrics of feeding apparatuses. D. gigas of 24 to 33 cm gladius length (GL) were collected in the northern Humboldt Current. Results showed that females had larger feeding apparatuses than males and higher δ15N values in bulk tissue and trophic AAs, but relatively similar source-AA δ15N values at same GLs. These results indicate that females catch prey of higher trophic position at earlier maturing stages than males, but tend to share similar habitat. This behavior likely reduces intraspecific competition, promotes ontogeny of sexual niche partitioning, and maximizes energy intake. Our study reveals that sexual segregation in feeding habits occurs in juvenile D. gigas during ontogenesis in the northern Humboldt Current, a strategy that can help elucidate its complex population dynamics and adaptation to fluctuating environmental conditions.
Compound-specific stable isotope analysis (CSIA) of amino acids (AAs) has been rapidly incorporated in ecological studies to resolve consumer trophic position (TP). Differential
N fractionation of ..."trophic" AAs, which undergo trophic
N enrichment, and "source" AAs, which undergo minimal trophic
N enrichment and serve as a proxy for primary producer δ
N values, allows for internal calibration of TP. Recent studies, however, have shown the difference between source and trophic AA δ
N values in higher marine consumers is less than predicted from empirical studies of invertebrates and fish. To evaluate CSIA-AA for estimating TP of cetaceans, we compared source and trophic AA δ
N values of multiple tissues (skin, baleen, and dentine collagen) from five species representing a range of TPs: bowhead whales, beluga whales, short-beaked common dolphins, sperm whales, and fish-eating (FE) and marine mammal-eating (MME) killer whale ecotypes. TP estimates (TP
) using several empirically derived equations and trophic discrimination factors (TDFs) were 1-2.5 trophic steps lower than stomach content-derived estimates (TP
) for all species. Although TP
estimates using dual TDF equations were in better agreement with TP
estimates, our data do not support the application of universal or currently available dual TDFs to estimate cetacean TPs. Discrepancies were not simply due to inaccurate TDFs, however, because the difference between consumer glutamic acid/glutamine (Glx) and phenylalanine (Phe) δ
N values (δ
N
) did not follow expected TP order. In contrast to pioneering studies on invertebrates and fish, our data suggest trophic
N enrichment of Phe is not negligible and should be examined among the potential mechanisms driving "compressed" and variable δ
N
values at high TPs. We emphasize the need for controlled diet studies to understand mechanisms driving AA-specific isotopic fractionation before widespread application of CSIA-AA in ecological studies of cetaceans and other marine consumers.
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