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Collection locations of bone samples from Steller sea lions, northern fur seals and harbor seals, 1951-1997
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Sea lion and seal populations in Alaskan waters underwent various degrees of decline during the latter half of the twentieth century and the cause(s) for the declines remain uncertain. The stable carbon (13C/12C) and nitrogen (15N/14N) isotope ratios in bone collagen from wild Steller sea lions (Eumetopias jubatus), northern fur seals (Callorhinus...
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... Metabolically active tissues integrate the isotopic composition of resources at turnover rates that depend on the tissue type and organism characteristics (del Rio et al., 2009). A comprehensive understanding of diet-tissue discrimination factors and isotopic turnover rates allows for the quantitative analysis of dietary composition and foraging patterns on a range of spatial and temporal scales (Arnould et al., 2011;Martínez del Rio et al., 2009;Hirons et al., 2001). However, the issues that affect diet-tissue discrimination factors and isotopic turnover rates within and between consumer species include the age and body size of sampled individuals, their diet composition, the tissues analyzed and the sample preparations completed prior to analysis (Britton and Busst, 2018;Caut et al., 2008). ...
Stable isotope analysis is robust tool to elucidate the diet, trophic position, and migration of typically large, highly mobile marine predators such as elasmobranchs. However, it is necessary to understand the diet–tissue discrimination factors and isotopic turnover rates of target animals. In this study, diet-switching experiments were conducted on the mottled skate (Beringraja pulchra (Liu, 1932)), caught off Sarufutsu, Hokkaido, Japan, to elucidate the diet–tissue discrimination factors and isotopic turnover rates for carbon and nitrogen stable isotopes. Ninety juvenile skates were fed Euphausia superba (C:N ratio = 3.9 ± 0.06, δ15N = 3.7±0.26‰ and δ13C = –25.9±0.15‰) to satiation at intervals of 2–3 days, and their muscle and liver tissues were serially sampled during 400 experimental days and used for stable isotope analysis. Both carbon and nitrogen stable isotopes reached steady state within the experimental days, and the estimated diet–tissue discrimination factors based on the fitting models were Δ13C = 1.5‰ and Δ15N = 2.3‰ for liver tissues and Δ13C = 3.4‰ and Δ15N = 3.5‰ for muscle tissues. The estimated turnover rates were 0.034 day–1 for δ13C and 0.039 day–1 for δ15N for liver tissues and were higher than those for muscle tissues (0.021 day–1 for δ13C and 0.019 day–1 for δ15N). In addition, the growth-based isotopic turnover rate model comprising juvenile skates revealed that the contribution of growth rate to the isotopic turnover rate was low.
... Carbon isotope values reflect phytoplankton productivity in aquatic environments (DeNiro and Epstein, 1978;France, 1995;Hobson, 1999). Declines in δ 13 C values have been associated with those in primary productivity, and hence with the carrying capacity of ecosystems (Hirons et al., 2001;O'Reilly et al., 2003;Schell, 2000), and ultimately with declines of penguin (Spheniscidae) populations, for example, in the sub-Antarctic region (Hilton et al., 2006;Jaeger and Cherel, 2011). In the South Atlantic Ocean, a 1.38 ‰ decline in δ 13 C values was observed in muscle of tuna species between 2000 and 2015, suggesting a global shift in phytoplankton community structure (Lorrain et al., 2020). ...
Mercury (Hg) is a highly toxic metal that adversely impacts human and wildlife health. The amount of Hg released globally in the environment has increased steadily since the Industrial Revolution, resulting in growing contamination in biota. Seabirds have been extensively studied to monitor Hg contamination in the world's oceans. Multidecadal increases in seabird Hg contamination have been documented in polar, temperate and subtropical regions, whereas in tropical regions they are largely unknown. Since seabirds accumulate Hg mainly from their diet, their trophic ecology is fundamental in understanding their Hg exposure over time. Here, we used the sooty tern (Onychoprion fuscatus), the most abundant tropical seabird, as bioindicator of temporal variations in Hg transfer to marine predators in tropical ecosystems in response to trophic changes and other potential drivers. Body feathers were sampled from 220 sooty terns, from museum specimens (n = 134) and free-living birds (n = 86) from Ascension Island, in the South Atlantic Ocean, over 145 years (1876-2021). Chemical analyses included (i) Hg (total- and methyl-Hg), and (ii) carbon (δ1³C) and nitrogen (δ15N) stable isotopes, as proxies of foraging habitat and trophic position, respectively, to investigate the relationship between trophic ecology and Hg contamination over time. Despite current regulations on its global emissions, mean Hg concentrations were 58.9% higher in the 2020s (2.0 μg g-1, n = 34) than in the 1920s (1.2 μg g-1, n = 107). Feather Hg concentrations were negatively and positively associated with δ1³C and δ15N values. The sharp decline of 2.9‰ in δ1³C values over time indicates ecosystem-wide changes (shifting primary productivity) in the tropical South Atlantic Ocean and can help explain the observed increase in tern's feather Hg concentrations. Overall, this study provides invaluable information on how ecosystem-wide changes can increase Hg contamination of tropical marine predators and reinforces the need for long-term regulations of harmful contaminants at the global scale.
... Reconstructing time series of δ 13 C and δ 15 N. In whiskers, the most recent growth is located at the base of the whisker, and an individual whisker can represent several years' growth [52][53][54]. Otariid whisker growth rate estimated from live wild South American fur seals of 0.08 mm/day [40] was globally applied to this study. ...
Determining trophic habits of predator communities is essential to measure interspecific interactions and response to environmental fluctuations. South American fur seals, Arctocephalus australis (SAFS) and sea lions Otaria byronia (SASL), coexist along the coasts of Peru. Recently, ocean warming events (2014–2017) that can decrease and impoverish prey biomass have occurred in the Peruvian Humboldt Current System. In this context, our aim was to assess the effect of warming events on long-term inter- and intra-specific niche segregation. We collected whisker from SAFS (55 females and 21 males) and SASL (14 females and 22 males) in Punta San Juan, Peru. We used δ ¹³ C and δ ¹⁵ N values serially archived in otariid whiskers to construct a monthly time series for 2005–2019. From the same period we used sea level anomaly records to determine shifts in the predominant oceanographic conditions using a change point analysis. Ellipse areas (SIBER) estimated niche width of species-sex groups and their overlap. We detected a shift in the environmental conditions marking two distinct periods (P1: January 2005—October 2013; P2: November 2013—December 2019). Reduction in δ ¹⁵ N in all groups during P2 suggests impoverished baseline values with bottom-up effects, a shift towards consuming lower trophic level prey, or both. Reduced overlap between all groups in P2 lends support of a more redundant assemblage during the colder P1 to a more trophically segregated assemblage during warmer P2. SASL females show the largest variation in response to the warming scenario (P2), reducing both ellipse area and δ ¹⁵ N mean values. Plasticity to adapt to changing environments and feeding on a more available food source without fishing pressure can be more advantageous for female SASL, albeit temporary trophic bottom-up effects. This helps explain larger population size of SASL in Peru, in contrast to the smaller and declining SAFS population.
... Stable isotopes have been used to reconstruct historical differences in diet and trophic position in Alaskan pinnipeds (Hobson et al. 1997, Hirons et al. 2001, Brennan et al. 2019). These previous studies utilized bulk stable isotope analysis exclusively and were therefore limited in their inferential strength. ...
... We apply hierarchical Bayesian analyses to 70 yr of trophic position data derived from CSIA from pinnipeds (harbor seal and Steller sea lion) in the Gulf of Alaska and Bristol Bay, and freshwater harbor seals in Iliamna Lake. We build on previous research examining pinniped nitro gen stable isotope composition (Hobson et al. 1997, Hirons et al. 2001, Misarti et al. 2009, Brennan et al. 2019) by adding 2 decades of data to the record (2000s and 2010s) and incorporating a broad spatial scope (from latitude 55°2' 60" N to 61°24' 3" N and from longitude 131°6' 45" W to 162°19' 00" W). Additionally, by analyzing nitrogen stable isotopes de rived from amino acids, we were able to control for known changes in nitrogen resources and phytoplankton composition at the base of the food web that can confound trophic position interpretations from bulk stable isotope data collected over decadal scales (Feddern et al. 2021). ...
... Both Steller sea lions and harbor seals exhibit generalist foraging patterns (Lance et al. 2012, Geiger et al. 2013. Diets of Alaskan pinnipeds consist of simi-lar prey species but vary between species, population, and local availability of prey (Iverson et al. 1997, Hirons et al. 2001. Bulk stable isotope studies in the Gulf of Alaska have shown that Steller sea lions feed lower in the food web compared to harbor seals (Iverson et al. 1997). ...
Over the past century, Alaskan pinnipeds have experienced dramatic changes in abundance, but these changes have been highly variable across species and regions. In recent decades, changes in atmospheric forcing and sea surface temperature have been particularly pronounced in the Gulf of Alaska and eastern Bering Sea, impacting the food webs in which Alaskan pinnipeds forage. We used compound-specific stable isotope analysis of nitrogen in amino acids
to estimate historic and modern trophic positions of harbor seals (Phoca vitulina) and Steller sea lions (Eumetopias jubatus) in the Gulf of Alaska and Bristol Bay. We applied a Bayesian hierarchical
framework to determine whether shared trends through time exist across pinnipeds (classified by region and species) on decadal scales. Model results identified both shared trends through time
and classification-specific decadal changes in pinniped trophic position. The largest change in trophic position occurred in the 2000s and 2010s and was observed in both Steller sea lions (median: 2.8) and harbor seals (median: 3.1) in the Gulf of Alaska, but not harbor seals in Bristol Bay or Iliamna Lake. Divergent trophic position patterns in the 2000s were identified in the western stock of Steller sea lions, which increased in trophic position, and sympatric harbor seals in the
northern Gulf of Alaska, which decreased in trophic position. Our results indicate that these species have been experiencing unique food web conditions in recent decades in the Gulf of Alaska, likely in response to recent climate-induced ecological change in the region.
... Carbon isotope values reflect phytoplankton productivity in aquatic environments (DeNiro and Epstein, 1978;France, 1995;Hobson, 1999). Declines in δ 13 C values have been associated with those in primary productivity, and hence with the carrying capacity of ecosystems (Hirons et al., 2001;O'Reilly et al., 2003;Schell, 2000), and ultimately with declines of penguin (Spheniscidae) populations, for example, in the sub-Antarctic region (Hilton et al., 2006;Jaeger and Cherel, 2011). In the South Atlantic Ocean, a 1.38 ‰ decline in δ 13 C values was observed in muscle of tuna species between 2000 and 2015, suggesting a global shift in phytoplankton community structure (Lorrain et al., 2020). ...
... The most recent growth is located at the base of the whisker, and an individual whisker can represent several years' growth (Ginter et al., 2012;Hirons, 2001;Hirons et al., 2001 ...
Comprendre comment des espèces sympatriques ayant des besoins similaires coexistent est une question majeure en écologie. Une communauté où le partage des ressources ou le chevauchement des niches est plus important accueillera plus d'espèces qu'une autre où il l'est moins. À cet égard, le principe d'exclusion compétitive prédit que les espèces doivent avoir des mécanismes de ségrégation pour coexister. Dans le système du courant de Humboldt (HCS) au Pérou, les lions de mer sud-américains (SASL, Otaria byronia) coexistent avec les otaries à fourrure sud-américaines (SAFS, Arctocephalus australis). Cependant, le partitionnement trophique, temporel et spatial lors de la recherche alimentaire reste largement inconnu. Cette étude se déroule dans la réserve nationale de Punta San Juan (PSJ) (15° 22'S, 75° 12'W) au Pérou, où se trouvent d'importantes colonies de reproduction des deux espèces d'otariidés, ce qui en fait un cadre idéal pour étudier les mécanismes de coexistence. L'objectif principal de cette thèse est décrire et de comparer les niches écologiques des espèces d'otariidés sympatriques au Pérou. Ceci sera abordé à travers trois objectifs spécifiques qui incluent décrire et de comparer (i) l'écologie trophique des pinnipèdes sympatriques; (ii) les variables environnementales qui caractérisent les niches écologiques et (iii) les stratégies de recherche de nourriture (dimensions spatiales et temporelles) au sein des niches écologiques des pinnipèdes sympatriques ; selon l'espèce et le sexe. Dans le Chapitre 1, l'analyse des trajectoires de la population montre comment sur une période de 20 ans, les deux populations de pinnipèdes sont maintenant en déclin. Une diminution des juvéniles dans la colonie, suggère que la limitation des ressources est le principal facteur contribuant au déclin actuel des populations. Dans le Chapitre 2, la ségrégation alimentaire interspécifique a été détectée, grâce à l'analyse des parties dures dans les fécès. Les SAFS se nourrissent principalement d'anchois du Pérou (Engraulis ringens) et de céphalopodes tandis que les SASL consomment surtout des galathées (Pleuroncodes monodon) et des anchois du Pérou, en plus petites proportions. Au cours de cette période d'étude, un chevauchement trophique a été détecté pendant un événement El Niño extraordinaire, ce qui suggère que les changements climatiques peuvent exacerber la compétition. Dans le Chapitre 3, nous avons analysé les localisations de 35 otariidés (18 SASL, 17 SAFS) équipés de balises satellites pour déterminer les stratégies de recherche de nourriture. Les mâles se séparent dans l'espace et dans le temps; tandis que les femelles présentent un chevauchement spatial mais disposent de mécanismes de ségrégation temporelle. Les variables environnementales associées suggèrent des caractéristiques d'habitat pélagique et côtier chez les otaries à fourrure et les lions de mer femelles, respectivement. Par contre, les mâles présentent une plus grande variabilité interindividuelle qui devrait être exploré davantage. Quoi qu'il en soit, les résultats démontrent que les stratégies de recherche de nourriture multiples à différentes échelles contribuent à la répartition des ressources. Au Chapitre 4, la différenciation de niche à long terme a été étudiée en examinant les signatures isotopiques archivées en série dans les vibrisses SAFS et SASL. Les otariidés ont étendu la largeur de leur niche (à l'exception des femelles SASL) en réponse à l'augmentation du niveau moyen de la mer et au réchauffement des températures de surface de la mer. Le déclin général des signaux δ15N suggère un appauvrissement de la base du réseau alimentaire, avec des effets bottom-up qui ont impacté les consommateurs tertiaires. L'ensemble des résultats aident à expliquer la diminution actuelle et aide à comprendre la réponse des prédateurs supérieurs aux changements de l'environnement marin.
... A wild animal's trophic discrimination factor varies according to the species' diet and body condition, both of which would be potentially altered during ENSO periods. The comparison of consumer tissue δ 13 C values over time provides information regarding ocean production in foraging grounds throughout fluctuating ENSO conditions (France and Peters, 1997;Hirons et al., 2001;Kurle and Worthy, 2001). From 2014 through 2016 as SSTA increased, declines in primary production were expected, reflected as lower δ 13 C values. ...
... The δ 15 N in consumer tissues relative to diet provide information regarding potential food web linkages (France and Peters, 1997;Hirons et al., 2001;Kurle and Worthy, 2001). The adult Peruvian fur seals all showed a similar pattern in δ 15 N values through time, a long-term gradual decline followed by a quick increase. ...
Peru’s coastal waters are characterized by significant environmental fluctuation due to periodic El Niño- La Niña- Southern Oscillation (ENSO) events. This variability results in ecosystem-wide food web changes which are reflected in the tissues of the Peruvian fur seal (Arctocephalus australis). Stable isotope ratios (δ¹³C and δ¹⁵N) in Peruvian fur seal vibrissae (whiskers) are used to infer temporal primary production and dietary variations in individuals. Sea surface temperature anomaly (SSTA) recordings from the Niño 1+2 Index region captured corresponding ENSO conditions. Fluctuations in δ¹⁵N values were correlated to SSTA records, indicating that ENSO conditions likely impact the diet of these apex predators over time. Anomalous warm phase temperatures corresponded to decreased δ¹⁵N values, whereas cold phase anomalous conditions corresponded to increased δ¹⁵N values, potentially from upwelled, nutrient-rich water. Vibrissae δ¹³C values revealed general stability from 2004 to 2012, a moderate decline during 2013 (La Niña conditions) followed by a period of increased values concurrent with the 2014–2016 El Niño event. Both δ¹³C and δ¹⁵N values were inversely correlated to each other during the strongest El Niño Southern Oscillation event on record (2014–2016), possibly indicating a decline in production leading to an increase in food web complexity. Lower δ¹³C and δ¹⁵N values were exhibited in female compared to male fur seal vibrissae. Findings suggest ENSO conditions influence resource availability, possibly eliciting changes in pinniped foraging behavior as well as food web of the endangered Peruvian fur seal.
... Teeth contain mineralised and soft-tissue components that can preserve a timeline of their chemical composition during growth, and therefore allow retrospective studies of diet and contaminant ex posure of individuals (e.g. Hirons et al. 2001, Zhao et al. 2004, Aubail et al. 2010, Juarez-Rodriguez et al. 2020. Teeth have therefore been used as quantitative monitoring tools to detect and investigate long-term ecological changes and anthropogenic threats to the environment (Boyd & Roberts 1993, Newsome et al. 2007, Outridge et al. 2009, Hanson et al. 2018. ...
As sentinels of ecosystem health, high trophic level predators integrate information through all levels of the food web. Their tissues can be used to investigate spatiotemporal variability in foraging behaviour, and with the appropriate analytical methods and tools, archived samples can be used to reconstruct past trophic interactions. Harp seal Pagophilus groenlandicus teeth collected in the 1990s from the Northwest Atlantic were analysed for bulk stable carbon and nitrogen isotopes (δ ¹³ C bulk and δ ¹⁵ N bulk ), and compound-specific stable nitrogen isotopes of amino acids (δ ¹⁵ N AA ) for the first time. We developed a fine-scale, annual growth layer group (GLG) dentine sub-sampling method corresponding to the second and third year of life. In accordance with previous diet studies, while there was individual variability in δ ¹⁵ N bulk , δ ¹³ C bulk and δ ¹⁵ N AA measurements, we did not detect significant differences in isotopic niche widths between males and females, or between GLGs. Relative trophic position was calculated as the baseline-corrected δ ¹⁵ N AA values using trophic (glutamic acid) and source (phenylalanine and glycine) amino acids. Variability was measured between individuals in their relative trophic position, but within-individual variability was low, suggesting that they fed at the same trophic level over these 2 yr of life. These novel δ ¹⁵ N AA data may therefore suggest individual, specialist harp seal foraging behaviour in sub-adults. Our findings show that compound-specific stable isotope signatures of archived, inert predator tissues can be used as tools for the retrospective reconstruction of trophic interactions on broad spatiotemporal scales.
... Continual dentine deposition [57] in whole-tooth samples analysed here integrates long-term diet that would attenuate isotopic signals related to seasonal consumption of prey. After adjustment for collagen-specific trophic enrichment (~3‰; [58]) to allow for direct, tissue-specific comparison with potential prey, the three ME killer whales with the highest adjusted values (16.8 to 17.5‰) are considerably higher than bulk bone collagen δ 15 N values of both gray and minke whales in the ENP (14.2 ± 0.7 and 14.4 ± 0.8‰, respectively; [46,58], but fall within the range of bone collagen and dentine δ 15 N of ENP pinniped (15.7 to 18.6‰; [59][60][61] and harbor porpoise (15.7 ± 0.7‰; [62]). ...
Ecotypes are groups within a species with different ecological adaptations than their conspecifics. Eastern North Pacific (ENP) killer whale ( Orcinus orca ) ecotypes differ in their diet, behavior, and morphology, but the same is not known for this species in the eastern Canadian Arctic (ECA) and Northwest Atlantic (NWA). Using compound-specific stable isotope analysis (CSIA) of amino acids (AAs), we compared δ ¹⁵ N patterns of the primary trophic and source AA pair, glutamic acid/glutamine (Glx) and phenylalanine (Phe), in dentine collagen of (1) sympatric ENP killer whale ecotypes with well-characterized diet differences and (2) ECA/NWA killer whales with unknown diets. δ ¹⁵ N Glx-Phe was significantly higher in the ENP fish-eating (FE) than mammal-eating (ME) ecotype (19.2 ± 0.4‰ vs. 13.5 ± 0.7‰, respectively). Similar bimodal variation in δ ¹⁵ N Glx-Phe indicated analogous dietary divisions among ECA/NWA killer whales, with two killer whales having higher δ ¹⁵ N Glx-Phe (16.5 ± 0.0‰) than the others (13.5 ± 0.6‰). Inferences of dietary divisions between these killer whales were supported by parallel differences in threonine δ ¹⁵ N (–33.5 ± 1.6‰ and –40.4 ± 1.1‰, respectively), given the negative correlation between δ ¹⁵ N Thr and TP across a range of marine consumers. CSIA-AA results for ECA/NWA whales, coupled with differences in tooth wear (a correlate for diet), are consistent with ecotype characteristics reported in ENP and other killer whale populations, thus adding to documented ecological divergence in this species worldwide.
... Douglas et al. (2004) used the d 15 N values from pond sediment cores to identify when the area was occupied by the Thule because they subsisted primarily on marine animals (e.g. bowhead whales or seals) that are enriched in 15 N (Fry 1988;Hobson and Schell 1998;Hirons et al. 2001). Greater values of d 15 N coincided with archeologically estimated dates of Thule occupation and they concluded that d 15 N could be used to estimate dates of Thule occupation in sediment cores that had insufficient 14 C from sedimented terrestrial vegetation to generate reliable dates, a common problem in the High Arctic (Hadley et al. 2010a, b). ...
We conducted a systematic review of 89 paleolimnological studies applied to archeological questions. Where we discuss the physical, chemical and biological sediment variables used in these studies in terms of their advantages and disadvantages as paleolimnological proxies for archeological studies. We make four key observations: 1) This field is rapidly growing, 2) More research is needed, 3) More standardization is required for future integrative analyses, and 4) More robust studies with multiple proxies are needed as the field grows. To address these challenges, we developed a framework to help researchers design paleolimnological studies in support of archeology. The framework includes standardized terminology of proxy characteristics and definition of a new term: orthogonality. This framework was then integrated with decision matrix analysis to build study scores that can be used to help researchers optimize their study design. This approach will help future researchers build more robust paleolimnology studies to more effectively complement independent archeological work. We also summarized new areas of archeology and chemistry that could be integrated with paleolimnology in the future.
