Long-term species, sexual and individual variations in foraging strategies of fur seals revealed by stable isotopes in whiskers

Background

Individual variations in the use of the species niche are an important component of diversity in trophic interactions. A challenge in testing consistency of individual foraging strategy is the repeated collection of information on the same individuals.

Methodology/Principal Findings

The foraging strategies of sympatric fur seals (Arctocephalus gazella and A. tropicalis) were examined using the stable isotope signature of serially sampled whiskers. Most whiskers exhibited synchronous δ¹³C and δ¹⁵N oscillations that correspond to the seal annual movements over the long term (up to 8 years). δ¹³C and δ¹⁵N values were spread over large ranges, with differences between species, sexes and individuals. The main segregating mechanism operates at the spatial scale. Most seals favored foraging in subantarctic waters (where the Crozet Islands are located) where they fed on myctophids. However, A. gazella dispersed in the Antarctic Zone and A. tropicalis more in the subtropics. Gender differences in annual time budget shape the seal movements. Males that do not perform any parental care exhibited large isotopic oscillations reflecting broad annual migrations, while isotopic values of females confined to a limited foraging range during lactation exhibited smaller changes. Limited inter-individual isotopic variations occurred in female seals and in male A. tropicalis. In contrast, male A. gazella showed large inter-individual variations, with some males migrating repeatedly to high-Antarctic waters where they fed on krill, thus meaning that individual specialization occurred over years.

Conclusions/Significance

Whisker isotopic signature yields unique long-term information on individual behaviour that integrates the spatial, trophic and temporal dimensions of the ecological niche. The method allows depicting the entire realized niche of the species, including some of its less well-known components such as age-, sex-, individual- and migration-related changes. It highlights intrapopulation heterogeneity in foraging strategies that could have important implications for likely demographic responses to environmental variability.     

Analysis of growth and stable isotopes in teeth of male Australian fur seals reveals interannual variability in prey resources

To detect and monitor long‐term ecosystem responses to environmental variability, managers must utilize reliable and quantitative techniques to predict future ecosystem responses. Canine teeth from 67 male Australian fur seals (aged 2–19 yr), collected at Seal Rocks, between 1967 and 1976, were measured for relative growth within the dentine growth layer groups (GLGs), as an index of body growth. Fluctuations in relative growth were apparent during 1956–1971, suggesting interannual variation in prey resources within Bass Strait. These were positively correlated with the Southern Oscillation Index and negatively with the Indian Ocean Subtropical Dipole, both on a 2 yr lag. The observed delay may reflect the time required for the nutrient cascade to filter through to the predominantly benthic prey of Australian fur seals. Stable isotope analysis (δ¹⁵N/δ¹³C) was also used to investigate whether fluctuations in growth were associated with differences in diet. Relative growth was found to be negatively correlated with δ¹⁵N, suggesting years of greater resource availability may be associated with individuals consuming proportionally more prey biomass of lower isotopic value. This study demonstrates that fluctuations in the dentine GLGs of male Australian fur seals are related to environmental parameters, suggesting variation in body growth is mediated by changes in prey resources.     

Holocene changes in the ecology of northern fur seals: insights from stable isotopes and archaeofauna

The remains of northern fur seals (Callorhinus ursinus) are among the most abundant of pinniped elements recovered from mainland coastal archaeological sites in both California and Oregon. This is surprising as all contemporary northern fur seals breed exclusively on offshore islands, primarily at high latitudes, and the species is otherwise pelagic. The vulnerability of these animals to human predation suggests that either humans were foraging much further offshore than has been presumed or alternatively that the ecology of these animals has shifted during the late Holocene. We used isotopic and archaeofaunal analysis of the remains of pinnipeds from the middle to late Holocene of central and northern California to clarify the breeding and foraging behavior, and migration patterns of these ancient animals. The carbon and nitrogen isotope compositions of ancient northern fur seals reveal that these animals fed as far offshore as they do today, and that they remained at middle latitudes throughout the year. From an archaeological site at Moss Landing, California, we identified 16 skeletal elements from at least 12 very small northern fur seal pups. From another site near Mendocino, California, we identified the remains of at least 6 pups. We estimate the size and age of 5 of the young animals using sex-specific regressions of body length on the short dentary length derived from measurements of modern specimens. Our estimates indicate these ancient pups were substantially smaller, and therefore younger, than modern 3-month-old northern fur seal pups from similar latitudes and their nitrogen isotope compositions suggest they had not been weaned. As present-day northern fur seals do not leave their rookeries until they are at least 4 months old, we consider it highly unlikely that these ancient pups swam to these mainland locations from some distant island rookery. While there are numerous nearshore rocky outcrops along the Mendocino Coast, which may have supported small breeding colonies, the Moss Landing site is centered on a 40-km-long sandy beach, and is more than 120 km from what at the time were the nearest offshore islands. We conclude that northern fur seal adult females, subadults, and pups whose remains were recovered at the Moss Landing archaeological site must have been taken at a mainland rookery. Evidence that northern fur seals once bred on the mainland at this central California location suggests that the abundant remains of these animals at numerous other archaeological sites along the California coast also reflect the presence of nearby mainland rookeries. Based on the relative abundance of their remains in ancient human occupation sites and the widespread distribution of sites where their remains have been found, it appears that northern fur seals were once the predominant pinniped throughout a region where they now only rarely occur. Furthermore, their presence along the central and northern California coasts appears to have once severely limited the distribution of other pinnipeds, which are now common to the region.     

Interannual variation in pup production and the timing of breeding in benthic foraging Australian fur seals

Large interannual variations in reproductive success caused by fluctuations in oceanography and prey availability are common to many species of air breathing epipelagic predators. In contrast, little is known about variation in benthic foragers such as Australian fur seals ( Arctocephalus pusillus doriferus ). Between 1997 and 2007, pup production was assessed in 9 yr, while the timing of breeding and adult female condition was assessed in 5 yr at Kanowna Island in Bass Strait, southeastern Australia. Pup production was variable (     = 1,726 ± 42, range = 1,386–2,301), but without temporal trend, as was median birth date (     = 23 November ± 1, range = 21–25 November) and pupping synchrony (period of 90% births:     = 28 ± 2 d, range = 23–31 d). Pup production was negatively correlated with median birth date and positively correlated with female condition, winter sea-surface temperature (SST) and zonal wind strength within Bass Strait. Pup production was also negatively correlated with SST in the previous summer within Bass Strait and in the eastern Great Australian Bight upwelling region. The results suggest that the reproductive success of Australian fur seals is influenced by oceanography but less so than in otariids foraging epipelagically in major upwellings. Despite spanning several El Niño events, no correlation between pup production and the Southern Oscillation Index was observed.     

Phenotypic determinants of individual fitness in female fur seals: larger is better

Inter-individual differences in fitness in female vertebrates have often been related to phenotypic discrepancies, suggesting that bigger individuals exhibit greater fitness. However, the use of the temporally variable indices of quality, such as body mass/condition, may not represent the most reliable index over longer time intervals. Few studies have assessed the direct influence of body size (BS) on individual fitness. We addressed this knowledge gap using data from long-term monitoring of individually marked female subantarctic fur seals. The females of higher quality (i.e. higher lifetime reproductive success) were larger in BS than their counterparts, which correlated with their ability to provision their pup with greater and more regular energy supply, possibly through the maximization of foraging performance and body fat storage. We accordingly found that our study population could be divided into three contrasted categories of maternal quality, with 33% of the females producing over 71% of the viable offspring constituting the next generation. We suggest that a larger BS represents a crucial selective advantage for a central place forager, especially when exploiting remotely available resources.     

Investigation of mercury concentrations in fur of phocid seals using stable isotopes as tracers of trophic levels and geographical regions

Recent studies have shown that the complementary analysis of mercury (Hg) concentrations and stable isotopic ratios of nitrogen (δ¹⁵N) and carbon (δ¹³C) can be useful for investigating the trophic influence on the Hg exposure and accumulation in marine top predators. In this study, we propose to evaluate the interspecies variability of Hg concentrations in phocids from polar areas and to compare Hg bioaccumulation between both hemispheres. Mercury concentrations, δ¹⁵N and δ¹³C were measured in fur from 85 individuals representing 7 phocidae species, a Ross seal (Ommatophoca rossii), Weddell seals (Leptonychotes weddellii), crabeater seals (Lobodon carcinophagus), harbour seals (Phoca vitulina), grey seals (Halichoerus grypus), ringed seals (Pusa hispida) and a bearded seal (Erignathus barbatus), from Greenland, Denmark and Antarctica. Our results showed a positive correlation between Hg concentrations and δ¹⁵N values among all individuals. Seals from the Northern ecosystems displayed greater Hg concentrations, δ¹⁵N and δ¹³C values than those from the Southern waters. Those geographical differences in Hg and stable isotopes values were likely due to higher environmental Hg concentrations and somewhat greater number of steps in Arctic food webs. Moreover, dissimilarities in feeding habits among species were shown through δ¹⁵N and δ¹³C analysis, resulting in an important interspecific variation in fur Hg concentrations. A trophic segregation was observed between crabeater seals and the other species, resulting from the very specific diet of krill of this species and leading to the lowest observed Hg concentrations.     

The influence of diet on foraging habitat models: a case study using nursing Antarctic fur seals

Predictable sources of food underpin lifetime reproductive output in long lived animals. The most important foraging areas of top marine predators are therefore likely to be related to environmental features that enhance productivity in predictable spatial and temporal patterns. Even so, although productive areas within the marine environment are distributed patchily in space and time, most studies assess the relationships between feeding activity and proximate, not long term, environmental characteristics. In addition, individuals within a population may exploit different prey types, and these are often associated with different hydrographic features. Until now, models attempting to associate core foraging areas (CFAs) of marine predators with the environmental characteristics of those areas have not considered the diet of individual animals, despite the influence this could have on these relationships. We used bathymetry and multi‐year (n=24) mean sea surface temperature and variability as predictors of CFAs of lactating Antarctic fur seals Arctocephalus gazella at Heard Island. The effect of prey types on the predictability of these models was explored by matching diet and foraging trip data of individual seals (n=40 seals, n=1 trip each). Differences in diet between seals were mirrored by their spatial behaviour. Foraging strategies differed both between and within groups of seals consuming different diets. Long‐term environmental parameters were useful for predicting the foraging activity of seals that consumed a single prey type with relatively specific habitat preferences, but not for those that consumed single or multiple prey types associated with more varied habitats. Ignoring individual variation in predator diet probably contributes to the poor performance of foraging habitat models. These findings highlight the importance of incorporating individual specialization in foraging behaviour into ecological models and management of predator populations.     

From food to offspring down: tissue-specific discrimination and turn-over of stable isotopes in herbivorous waterbirds and other avian foraging guilds

Isotopic discrimination and turn-over are fundamental to the application of stable isotope ecology in animals. However, detailed information for specific tissues and species are widely lacking, notably for herbivorous species. We provide details on tissue-specific carbon and nitrogen discrimination and turn-over times from food to blood, feathers, claws, egg tissues and offspring down feathers in four species of herbivorous waterbirds. Source-to-tissue discrimination factors for carbon (δ¹³C) and nitrogen stable isotope ratios (δ¹⁵N) showed little variation across species but varied between tissues. Apparent discrimination factors ranged between −0.5 to 2.5‰ for δ¹³C and 2.8 to 5.2‰ for δ¹⁵N, and were more similar between blood components than between keratinous tissues or egg tissue. Comparing these results with published data from other species we found no effect of foraging guild on discrimination factors for carbon but a significant foraging-guild effect for nitrogen discrimination factors.Turn-over of δ¹³C in tissues was most rapid in blood plasma, with a half-life of 4.3 d, whereas δ¹³C in blood cells had a half-life of approximately 32 d. Turn-over times for albumen and yolk in laying females were similar to those of blood plasma, at 3.2 and 6.0 d respectively. Within yolk, we found decreasing half-life times of δ¹³C from inner yolk (13.3 d) to outer yolk (3.1 d), related to the temporal pattern of tissue formation.We found similarities in tissue-specific turn-over times across all avian species studied to date. Yet, while generalities regarding discrimination factors and tissue turn-over times can be made, a large amount of variation remains unexplained.     

Age-specific survival and reproductive performances in fur seals: evidence of senescence and individual quality

Life history theory hypothesises that breeding events induce reproductive costs that may vary among individuals. However, the growing number of studies addressing this question are taxonomically biased, therefore impeding the generalisation of this hypothesis, especially with regard to marine top predators. This study investigated age‐related survival and breeding performances in subantarctic fur seal (Arctocephalus tropicalis) females from Amsterdam Island, southern Indian Ocean. Using multistate capture–recapture models on data obtained from known‐age tagged females over eight consecutive years, we tested for evidence of senescence, individual quality, and reproductive costs in terms of future survival and fecundity. Adult female yearly survival appeared high and constant throughout time. While a two age‐class model was preferred in non‐breeders, breeding females exhibited three age classes with a maximum survival for the prime‐age class (7–12 years). Survival and reproductive probabilities decreased from 13 years onward, suggesting senescence in this population. Survival was lower for non‐breeders than for breeders, among both prime‐aged (0.938 vs 0.982) and older (0.676 vs 0.855) females. Furthermore, non‐breeders exhibited higher probabilities of being non‐breeders the following year than did breeders (0.555 vs 0.414). Such results suggest consistency in female breeding performance over years, supporting the hypothesis that non‐breeding tend to occur among lower quality individuals rather than representing an alternative strategy to enhance residual reproductive value. However, the high proportion of females that did not breed during two consecutive years, and the lower probability of being a successful breeder after a greater reproductive effort confirmed the existence of reproductive costs, especially during the second half of the lactation. These results also suggest that younger age‐classes included a higher proportion of lower quality individuals, which are likely to face higher costs of reproduction. Such hypotheses lead to consider the first breeding event as a filter generating a within‐cohort selection process in females.     

Using stable isotopes to understand changes in ringed seal foraging ecology as a response to a warming environment

Trends toward increased temperatures, reduced sea ice extent, and longer open water seasons have resulted in changing Arctic ecosystem dynamics. Expected changes include shifts in distribution and abundance of prey species for seabirds and marine mammals. Using stable isotope analysis, we studied spatial and interannual variation in ringed seal (Pusa hispida) feeding ecology in Hudson Bay in relation to environmental variables, between 2003 and 2010. Ringed seal muscle and hair samples collected from Arviat and Sanikiluaq, Nunavut, were analyzed for stable isotope ratios of nitrogen (δ¹⁵N) and carbon (δ¹³C). Seals from western Hudson Bay (Arviat) had higher δ¹⁵N and lower δ¹³C than seals from eastern Hudson Bay (Sanikiluaq), and stable isotope ratios varied interannually within each region. Peak δ¹⁵N occurred in years with spring air temperatures between approximately ?5°C and ?2°C. This temperature range was characteristic of warm years in western Hudson Bay and cool years in eastern Hudson Bay. We hypothesize that the high δ¹⁵N observed in ringed seals is indicative of greater importance of capelin (Mallotus villosus) in ringed seal diet. A comparison of ringed seal isotopic niche widths indicated greater dietary differences between western and eastern Hudson Bay with warming, suggesting a possible ecological divergence related to climate change.     

Proteome dynamics in complex organisms: using stable isotopes to monitor individual protein turnover rates

The complete definition of changes in a proteome requires information about dynamics and specifically the rate at which the individual proteins are turned over intracellularly. Whilst this can be achieved in single-cell culture using stable isotope precursors, it is more challenging to develop methods for intact animals. In this study, we show how dietary administration of stable isotope-labelled amino acids can obtain information on the relative rates of synthesis and degradation of individual proteins in a proteome. The pattern of stable isotope-labelling in tryptic peptides can be deconstructed to yield a highly reliable measure of the isotope abundance of the precursor pool, a parameter that is often difficult to acquire. We demonstrate this approach using chickens fed a semisynthetic diet containing [(2)H(8)]valine at a calculated relative isotope abundance (RIA) of 0.5. When the labelling pattern of gel-resolved muscle proteins was analyzed, the intracellular precursor isotope abundance was 0.35, consistent with dilution of the amino acid precursor pool with unlabelled amino acids derived from degradation of pre-existing proteins. However, the RIA was stable over an extended labelling window, and permitted calculation of the rates of synthesis and degradation of individual proteins isolated by gel electrophoresis. For the first time, it is feasible to contemplate the analysis of turnover of individual proteins in intact animals.     

From individual behaviour to population pattern: weather-dependent foraging and breeding performance in black kites

The links between weather and animal behaviour in population processes have received relatively little attention. I studied the effect of weather conditions on foraging and breeding performance of a medium-sized raptor, the black kite, Milvus migrans. The frequency of prey capture attempts and their likelihood of success increased with temperature and declined with rainfall. Kites used flight styles involving a higher energy expenditure in less favourable weather. Nestling provisioning rates declined during rain spells. More kites hunted during periods of favourable weather and after periods with a high frequency of successful prey capture attempts by conspecifics; this result suggested that individuals may fine-tune their foraging effort to the expected foraging reward. Such compensatory behavioural adjustments may increase species resilience to climate change. The behaviourally mediated effects of weather on prey availability translated into population effects. Yearly weather conditions during the last stage of the prelaying period affected population-level productivity, probably through an effect on female body condition mediated by male provisioning capability and hunting yield. The predicted effects of climate change on kites may already be occurring, with progressively earlier laying and northward range expansion. These results confirm the need to pay greater attention to behaviourally mediated effects of climate on populations, particularly when individuals make compensatory adjustments that may enhance resilience to climate change. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Autotrophy in maize husk leaves : evaluation using natural abundance of stable isotopes

The natural abundance of carbon and hydrogen isotopic composition, expressed as a δ¹³C value of plant dry matter and cellulose in the hypsophylls (husk leaves) of maize (Zea mays L.) was measured and compared with that of leaves and cobs. The δ¹³C values of outer hypsophylls were usually 2 to 3%‰ more negative than leaves or other tissues, and became more negative with increasing chlorophyll content, indicating significant local C₃ pathway fixation of CO₂ in the outer hypsophylls. The δD values indicated a significant part of hypsophyll cellulose was derived from heterotrophic sources (sucrose from C₄ photosynthesis in other tissues). Isotopic mass balance calculations allowed quantitative estimation of these carbon sources and, in the samples examined, about 16% of hypsophyll cellulose was derived from local C₃ photosynthesis, about 62% from local C₄ photosynthesis, and about 22% from sucrose imported from other leaves.     

Multiple origins of vagrant Subantarctic fur seals: a long journey to the Brazilian coast detected by molecular markers

In this study, we present the first data about putative source populations of the vagrant Subantarctic fur seal, Arctocephalus tropicalis, found on the Brazilian coast, through the comparison of their mitochondrial DNA control sequences to exclusive haplotypes from the main breeding colonies of the species. The results indicated that, despite the majority of the vagrant individuals are from Gough Island (the closest breeding site to the Brazilian coast), they also come from other reproductive colonies, such as Crozet Island, a distance around 16,500 km from the Brazilian coast. Furthermore, the molecular data identified three possible management units: (1) Gough, (2) Amsterdam, and (3) Marion, Macquarie and Crozet. This significant genetic subdivision must be taken into account in any future management plan for the species conservation, including rehabilitation and even reintroduction of vagrant fur seals. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Diet,individual specialisation and breeding of brown skuas (<Emphasis Type="Italic">Catharacta antarctica lonnbergi</Emphasis>): an investigation using stable isotopes

The diet of brown skuas (Catharacta antarctica lonnbergi) on Bird Island, South Georgia was assessed using a combination of stable isotope analysis (SIA) and mixing model techniques. We found evidence that individual specialisation in diet of adult brown skuas was related to timing of breeding, which may reflect differences in intrinsic quality. Adults with more enriched ¹³C values hatched chicks earlier than those with depleted ¹³C values. Individuals with enriched ¹³C fed predominantly on Antarctic fur seal (Arctocephalus gazella) carrion and placenta while those with lower ratios appeared to rely more on burrowing petrels (e.g. Antarctic prions Pachyptila desolata). Individual foraging differences clearly influenced timing of breeding and potentially the reproductive output of breeding pairs. We confirmed that the main components of the diet of brown skuas during incubation are, in decreasing order of importance, Antarctic fur seal placenta, burrowing petrels and fur seal muscle. In addition, we identified fur seal faeces in the diet during this stage, which had not been detected previously by traditional sampling methods. Finally we identified a correlation in δ¹³C values between pair members, attributable to the influence of courtship feeding of females by males, or assortative mating according to foraging preference or intrinsic quality.     

Coexistence of a locally undifferentiated foraging guild: avian snatchers in a southeastern Australian forest

Three species of sexually dichromatic, insectivorous birds (Golden Whistler, Pachycephala pectoralis; Rufous Whistler, Pa. rufiventris; Rose Robin, Petroica rosea) employ a characteristic foraging manoeuvre (snatching or sally‐striking) disproportionately often, leading several studies to group them together in one foraging guild. The three species synchronously co‐occupy an extensive eucalypt forest east of Melbourne, Australia (Olinda State Forest). All assemble in relatively high densities in late winter and through spring and early summer to breed. Log‐linear modelling of use of foraging techniques, substrate, plant species and heights within the forest indicate that all six species–gender groups virtually do not differ from one another: a situation in which very similar species coexist at high densities. The results are considered in the context of interspecific competition among ecologically similar species and it is suggested how such a situation might arise and be sustained. The absence of gender‐specific differentiation within species is also addressed.     

Substrate limitation of sediment methane flux,methane oxidation and use of stable isotopes for assessing methanogenesis pathways in a small arctic lake

Among predicted impacts of climate change in the Arctic are greater thaw depth and shifts in vegetation patterns and hydrology that are likely to increase organic carbon and nutrient loading to lakes. We measured substrate limitation of sediment methane (CH₄) flux, examined pathways of methanogenesis, and potential CH₄ oxidation using stable isotope labeled acetate in intact sediment cores from arctic lake GTH 112 (68°40′20″N, 149°14′57″W). We hypothesized that the acetoclastic pathway would dominate methanogenesis, reflecting dissolved organic carbon supply from the surrounding landscape, and that sediment CH₄ flux would be stimulated by addition of acetate. Experiments demonstrated acetate limitation of sediment CH₄ flux with short-term CH₄ flux response to availability of acetate, high rates of CH₄ oxidation, and strong dominance of the acetoclastic over the hydrogenotrophic methanogenic pathway. The experiments also indicated that isotopic fractionation effects during isotope enrichment experiments are large during methanogenesis and can alter the methanogenic pathways being investigated. Under oxic conditions, CH₄ oxidation at the sediment–water interface or in the water column is likely to account for much of diffusive CH₄ flux, but under anoxic hypolimnetic conditions and increased substrate availability, conditions that are likely to occur with climate change, sediment CH₄ flux will likely increase, with oxidation utilizing a smaller portion of sediment CH₄ production.