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Identifying foraging habitats of adult female long-nosed fur seal Arctocephalus forsteri based on vibrissa stable isotopes
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We investigated how foraging ecotypes of female long-nosed fur seals (Arctocephalus forsteri) could be identified from vibrissa stable isotopes. We collected regrowths of vibrissae from adult females (n = 18) from Cape Gantheaume, Kangaroo Island, South Australia from two breeding seasons (2016, 2017). The period represented by the regrowth was known and 8 individuals were administered with 15N-enriched glycine as a biomarker to mark the start date of the regrowth. Non-glycine marked and glycine marked vibrissae were used to estimate the rate of the individual vibrissa regrowth. Using individual growth rates (0.18 ± 0.04 mm d-1), we reconstructed a stable isotope (δ13C and δ15N) time series for each regrowth and allocated them to corresponding at-sea locations either based on geolocation tracks (n = 14) or foraging habitat type (shelf or oceanic) based on diving data (n = 2) of the sampled seals. Mean δ15N from vibrissa segments was higher when females foraged on the continental shelf region (16.1 ± 0.7, n = 29) compared to oceanic waters (15.1 ± 0.7, n = 106) in 2017, whereas it was similar in both regions in 2016 (shelf: 15.3 ± 0.4, n = 13; oceanic: 15.4 ± 0.4, n = 15). Based on the stable isotope signatures of vibrissa segments, model-based clustering analysis correctly classified 79.8% of them into shelf or oceanic foraging habitats. This demonstrates the potential of using vibrissa stable isotopes for studying the foraging ecology of an important top marine predator.
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... Furthermore, although detailed taxonomic resolution is poor, stable isotope ratios can inform about diet composition if the appropriate trophic discrimination factor (TDF) is known (Drago et al. 2010(Drago et al. , 2015Stricker et al. 2015;Beltran et al. 2016). As a result, the stable isotope analysis of whiskers has become a standard method in the study of eared seal ecology (e.g., Kernaléguen et al. 2012;Franco-Trecu et al. 2014;Baylis et al. 2015;Scherer et al. 2015;Vales et al. 2015;Chilvers 2019;Foo et al. 2019). ...
Detailed knowledge of marine mammal diet is critical to understand their ecological roles and for the adequate management of marine resources. Antarctic fur seals (Arctocephalus gazella) in the Southern Atlantic Ocean rely largely on Antarctic krill (Euphausia superba) during the summer months, but their winter diet remains largely unknown. Here, stable carbon and nitrogen isotope ratios in whiskers and blood of young (2-3 years old) and subadult (4-7 years old) Antarctic fur seal males from the South Shetland Islands were used to assess the seasonal and interannual changes in the krill contribution to their diet. The stable isotope ratios revealed that krill dominated the diet of young and subadult male Antarctic fur seals year-round, with penguins, and not fish, as the second major prey, regardless of year and season. The year-round reliance of young and subadult male Antarctic fur seals on krill should be considered for ecosystem-based fisheries management, as they represent the bulk of the fur seal population remaining off Antarctica during the winter months.
... C Glucose levels at birth had a significant impact on survival, even after controlling for the effect of the maternal foraging group, with pups born in the highest glucose quartile with almost 9 times higher chances of survival compared to pups born in the lowest glucose quartile (CPHM, HR = 8.92 ± 0.67, 95% CI = 2.3-33.3, Z = 3.3, P = 0.001) more frequent and/or longer resting periods in land during pregnancy (Baylis et al. 2016(Baylis et al. , 2018Jeanniard-Du-dot et al. 2017;Foo et al. 2019a), potentially favoring energy transfer to the foetus. This hypothesis is also supported by the impact of foraging strategies on foetal BUN levels. ...
The success of maternal foraging strategies during the rearing period can greatly impact the physiology and survival of dependent offspring. Surprisingly though, little is known on the fitness consequences of foraging strategies during the foetal period. In this study, we characterized variation in maternal foraging strategy throughout pregnancy in a marine top predator (South American fur seal, Arctocephalus australis), and asked if these shifts predicted neonatal health and postnatal survival. We found that during early pregnancy all pregnant females belonged to a single, homogenized foraging niche without evident clusters. Intriguingly though, during late pregnancy, individual fur seal mothers diverged into two distinct foraging niches characterized by a benthic-nearshore and a pelagic-offshore strategy. Females that shifted towards the benthic-nearshore strategy gave birth to pups with greater body mass, higher plasmatic levels of glucose and lower levels of blood urea nitrogen. The pups born to these benthic females were eight times more likely to survive compared to females using the pelagic-offshore foraging strategy during late pregnancy. These survival effects were mediated primarily by the impact of foraging strategies on neonatal glucose independent of protein metabolic profile and body mass. Benthic-nearshore foraging strategies during late pregnancy potentially allow for the greater maternal transfer of glucose to the foetus, leading to higher chances of neonatal survival. These results call for a deeper understanding of the balance between resource acquisition and allocation provided by distinct foraging polymorphisms during critical life-history periods, and how this trade-off may be adaptive under certain environmental conditions.
... Indeed, an increased presence of barracouta (Thyristes atun), red cod (Pseudophysis bachus), redbait, and pilchard were observed in the diet of AUFS during years with high winter sea-surface height anomalies in the Bass Strait region 81 . Sea-surface height anomalies have also been associated with changes in foraging behaviour in southern elephant seals (Mirounga leonina) and New Zealand fur seals (Arctocephalus forsteri), likely due to increased eddy activity 82,83 . Both the trip duration and dive duration observed in the present study decreased under stronger (i.e. more easterly or more westerly) 1-year lagged spring zonal winds in Bass Strait. ...
Understanding the factors which influence foraging behaviour and success in marine mammals is crucial to predicting how their populations may respond to environmental change. The Australian fur seal (Arctocephalus pusillus doriferus, AUFS) is a predominantly benthic forager on the shallow continental shelf of Bass Strait, and represents the greatest biomass of marine predators in south-eastern Australia. The south-east Australian region is experiencing rapid oceanic warming, predicted to lead to substantial alterations in prey diversity, distribution and abundance. In the present study, foraging effort and indices of foraging success and efficiency were investigated in 138 adult female AUFS (970 foraging trips) during the winters of 1998–2019. Large scale climate conditions had a strong influence on foraging effort, foraging success and efficiency. Foraging effort and foraging success were also strongly influenced by winter chlorophyll-a concentrations and sea-surface height anomalies in Bass Strait. The results suggest increasing foraging effort and decreasing foraging success and efficiency under anticipated environmental conditions, which may have population-level impacts.
Individual variation in habitat and resource use has been reported for many top predators. This variation becomes important when comparing individuals taking into account sex, size, or age classes, since it can influence population dynamics and stability. We evaluated the individual variation and sexual/geographical isotopic niche overlap of the South American fur seal (SAFS) from the western South Atlantic. Whiskers of adult individuals from Brazil (n = 19), Uruguay (n = 29), and Argentina (n = 5) collected between 2005 and 2016 were serially sampled, resulting in 1001 samples, and their carbon and nitrogen isotopic ratios were analyzed longitudinally. According to its length, time integrated by whiskers ranged between 1.4 and 5.6 years. Males had δ¹³C (− 14.5 ± 0.6‰) and δ¹⁵N (18.9 ± 1.2‰) values significantly higher than females (δ¹³C = − 15.2 ± 0.5‰, δ¹⁵N = 17.8 ± 1.2‰). Females from Uruguay and Brazil were isotopically similar, displaying a large isotopic niche overlap (65.2–84%). Contrary, moderate isotopic niche overlaps were observed between males from Uruguay and Brazil (40.1–48.4%), and Uruguay and Patagonia (22.3–27.8%), indicating the use of different prey and/or feeding grounds. The WIC/TNW index of individual specialization pointed a significant specialization in males (0.38 for δ¹⁵N and 0.39 for δ¹³C). Females, on the other hand, are more generalists compared to males (0.53 and 0.71, for δ¹⁵N and δ¹³C, respectively). Differences in the ecological opportunity between sexes can account for these variations. Our study points out that trophic generalist populations of SAFS are composed of specialist and generalist individuals.
Determining the foraging strategies for top marine predators is fundamental to understanding their role in the marine ecosystem and essential to gain insight into how species and populations may respond to environmental variability and human impacts. The long-term foraging strategies of individuals can be studied using stable isotope analysis of whiskers, which archive keratinous tissue. Here, stable isotope analysis (Δ ¹³ C and Δ ¹⁵ N) along the length of whiskers from female New Zealand (NZ) sea lions Phocarctos hookeri was used to investigate individuals' long-term foraging strategies. Previous telemetry studies showed that individual female NZ sea lions have one of 2 distinct foraging strategies that are habitual within and between years. Furthermore, past stable isotope research showed that these 2 distinct foraging strategies, i.e. benthic (foraging on the sea floor) or mesopelagic (foraging at various depths in the water column), can be identified through Δ ¹³ C and Δ ¹⁵ N stable isotope values from blood and whiskers. In the present study, chronological serial stable isotope sampling of female NZ sea lion whiskers confirmed long-term consistency of individual foraging strategies. Thirty-one of 35 individuals showed constant benthic (n = 13) or mesopelagic (n = 18) isotopic values along the length of their whiskers. The remaining 4 individuals showed mesopelagic foraging strategies but with slight oscillations. Serial stable isotope analysis of whiskers is a powerful tool for investigating the ecological niche of top marine predators throughout their adult life. This tool can be used within the Auckland Islands' NZ sea lion population to determine the proportion of the female population that are exposed to detrimental interactions with fisheries.
ABSTRACT: Accurately estimating predators’ diets at relevant spatial and temporal scales is key to understanding animals’ energetics and fitness, particularly in populations whose decline might be related to their diet such as northern fur seals Callorhinus ursinus. Our goals were to improve the accuracy of diet estimates and extend understanding of feeding ecology by combining 2 scat-based methods of diet determination (hard-part identification and DNA-metabarcoding) with stable isotope measurements and individual behavioural data. We collected 98 scats on a northern fur seal breeding colony. We also tracked 20 females with biologgers, and took blood samples to determine δ13C and δ15N values as proxies for seal foraging habitat and diet. Results show that diet composition from hard-parts analysis corresponded well with DNA results, with DNA yielding a greater diversity of prey species at a finer taxonomic level. Overall, scat-based methods showed that seals mostly fed on neritic shelf-associated prey. Cluster analyses of combined hard-parts and DNA results however identified 2 diet groups, one mostly neritic and the other mostly pelagic. Stable isotopes and behavioural data revealed that 40% of seals fed in oceanic waters on pelagic prey. This is more than indicated by scat-based analyses, which are likely biased towards animals foraging closest to the colony and underestimate some dietary specializations within the population. Consequently, the combination of multiple methods for diet identification with at-sea tracking of individuals can help identify and quantify specialist groups within a population and provide a wider spatial and temporal ecological context for dietary analysis.
King penguins make up the bulk of avian biomass on a number of sub-Antarctic islands where they have a large functional effect on terrestrial and marine ecosystems. The same applies at Marion Island where a substantial proportion of the world population breeds. In spite of their obvious ecological importance, the at-sea distribution and behavior of this population has until recently remained entirely unknown. In addressing this information deficiency, we deployed satellite-linked tracking instruments on 15 adult king penguins over 2 years, April 2008 and 2013, to study their post-guard foraging distribution and habitat preferences. Uniquely among adult king penguins, individuals by and large headed out against the prevailing Antarctic Circumpolar Current, foraging to the west and southwest of the island. On average, individuals ventured a maximum distance of 1,600 km from the colony, with three individuals foraging close to, or beyond, 3,500 km west of the colony. Birds were mostly foraging south of the Antarctic Polar Front and north of the southern boundary of the Antarctic Circumpolar Current. Habitat preferences were assessed using boosted regression tree models which indicated sea surface temperate, depth, and chorophyll a concentration to be the most important predictors of habitat selection. Interestingly, king penguins rapidly transited the eddy-rich area to the west of Marion Island, associated with the Southwest Indian Ocean Ridge, which has been shown to be important for foraging in other marine top predators. In accordance with this, the king penguins generally avoided areas with high eddy kinetic energy. The results from this first study into the behavioral ecology and at-sea distribution of king penguins at Marion Island contribute to our broader understanding of this species.
Stable isotope analysis (SIA) of whiskers is increasingly used to investigate the foraging ecology of pinnipeds. An understanding of whisker growth dynamics is lacking for most species yet is necessary for study design and interpretation of isotope data. Here we present measurements of whisker growth obtained using photogrammetry in 5 California sea lions Zalophus californianus and 2 spotted seals Phoca largha. Data were collected from captive individuals for at least 1 yr, resulting in serial measurements of 321 sea lion and 153 spotted seal whiskers. The sea lion whiskers exhibited linear growth, with growth rates that ranged from <0.01 to 0.18 mm d⁻¹. In contrast, spotted seal whiskers exhibited asymptotic growth characterized by rapid initial growth of up to 1.40 mm d⁻¹; whiskers reached 75 and 95% of their asymptotic length after an average of 48 and 105 d, respectively. Over half of the spotted seal whiskers were lost annually during a period that coincided with the annual pelage molt, whereas the maximum estimated lifespan of sea lion whiskers was 10+ yr. Our data indicate that sea lion whisker growth rates can be used to reliably determine time periods of tissue deposition and link isotope values with ecological events over multiple years. In contrast, spotted seal whiskers archive dietary information over a period of months, and interpretation of isotope values is complicated by growth and shedding patterns of whiskers, and physiological changes associated with the annual pelage molt.
Individuals within populations often differ substantially in habitat use, the ecological consequences of which can be far reaching. Stable isotope analysis provides a convenient and often cost effective means of indirectly assessing the habitat use of individuals that can yield valuable insights into the spatiotemporal distribution of foraging specialisations within a population. Here we use the stable isotope ratios of southern sea lion (Otaria flavescens) pup vibrissae at the Falkland Islands, in the South Atlantic, as a proxy for adult female habitat use during gestation. A previous study found that adult females from one breeding colony (Big Shag Island) foraged in two discrete habitats, inshore (coastal) or offshore (outer Patagonian Shelf). However, as this species breeds at over 70 sites around the Falkland Islands, it is unclear if this pattern is representative of the Falkland Islands as a whole. In order to characterize habitat use, we therefore assayed carbon (δ13C) and nitrogen (δ15N) ratios from 65 southern sea lion pup vibrissae, sampled across 19 breeding colonies at the Falkland Islands. Model-based clustering of pup isotope ratios identified three distinct clusters, representing adult females that foraged inshore, offshore, and a cluster best described as 'intermediate'. A significant difference was found in the use of inshore and offshore habitats between West and East Falkland and between the two colonies with the largest sample sizes, both of which are located in East Falkland. However, habitat use was unrelated to the proximity of breeding colonies to the Patagonian Shelf, a region associated with enhanced biological productivity. Our study thus points towards other factors, such as local oceanography and its influence on resource distribution, playing a prominent role in inshore and offshore habitat use.
Multiple factors, including limitation in food resources, have been proposed as possible
causes for the lack of recovery of the endangered western segment of the Steller sea lion
population in the United States. Because maternal body condition has important consequences on
fetal development and neonatal survival, the diets of pregnant females may be particularly important
in regulating population sizes. We used the stable carbon and nitrogen isotope values of
vibrissae from Steller sea lion pups as an indirect indicator of maternal diets during gestation.
Combining these data with isotope data from potential prey species in a Bayesian mixing model,
we generated proportional estimates of dietary consumption for key prey. Our analysis indicated
that females in the most westerly metapopulations relied heavily on Atka mackerel and squid,
whereas females inhabiting the Gulf of Alaska region had a fairly mixed diet, and the metapopulation
of Southeast Alaska showed a strong reliance on forage fish. These results are similar to
previous data from scat collections; however, they indicate a possible under-representation of softbodied
prey (squid) or prey with fragile skeletons (forage fish) from analyses of data from scats.
This study supports the utility of stable isotope modeling in predicting diet composition in gestating
adult female Steller sea lions during winter, using pup vibrissae.
This study assessed ontogenetic dietary changes in male South American fur seals Arctocephalus australis in northern and central Patagonia (Argentina) using stable isotope ratios (δ15N and δ13C) in vibrissae and bones. Sucking pups were characterised by higher δ15N values and lower δ13C values than older specimens. Weaning was associated with a marked drop of δ15N values, both in bone and vibrissae. Such a drop was inconsistent with the consumption of local prey and may reveal movement to distant foraging grounds or physiological changes associated with either fasting or rapid growth. Stable isotope ratios indicated that juveniles fed more pelagically than subadults and adults, but that there were no major differences between the 2 latter age categories. As subadults and adults are rather similar in body mass and are much larger than juveniles, body mass may play a role in the ontogenetic dietary changes reported. Nevertheless, demersal benthic prey were always scarce in the diet of male fur seals, which relied primarily on Argentine shortfin squid and small pelagic fish throughout life, though adults also consumed large amounts of decapod crustaceans available at shallow depths. Vibrissae did not reveal regular oscillations of δ15N or δ13C, except in 1 individual. Thus, male fur seals from northern and central Patagonia do not appear to migrate regularly between isotopically distinct areas, although nomadic displacements cannot be ruled out.
Strategies employed by wide-ranging foraging animals involve consideration of habitat quality and predictability and should maximise net energy gain. Fidelity to foraging sites is common in areas of high resource availability or where predictable changes in resource availability occur. However, if resource availability is heterogeneous or unpredictable, as it often is in marine environments, then habitat familiarity may also present ecological benefits to individuals. We examined the winter foraging distribution of female Antarctic fur seals, Arctocephalus gazelle, over four years to assess the degree of foraging site fidelity at two scales; within and between years. On average, between-year fidelity was strong, with most individuals utilising more than half of their annual foraging home range over multiple years. However, fidelity was a bimodal strategy among individuals, with five out of eight animals recording between-year overlap values of greater than 50%, while three animals recorded values of less than 5%. High long-term variance in sea surface temperature, a potential proxy for elevated long-term productivity and prey availability, typified areas of overlap. Within-year foraging site fidelity was weak, indicating that successive trips over the winter target different geographic areas. We suggest that over a season, changes in prey availability are predictable enough for individuals to shift foraging area in response, with limited associated energetic costs. Conversely, over multiple years, the availability of prey resources is less spatially and temporally predictable, increasing the potential costs of shifting foraging area and favouring long-term site fidelity. In a dynamic and patchy environment, multi-year foraging site fidelity may confer a long-term energetic advantage to the individual. Such behaviours that operate at the individual level have evolutionary and ecological implications and are potential drivers of niche specialization and modifiers of intra-specific competition.
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.
Isotopic analysis of serially sampled vibrissae (whiskers) is a powerful method to investigate changes in an individual's resource and habitat use over time, which is difficult or impossible to accomplish using traditional dietary proxies such as observation or scat analysis. A vibrissae-based isotopic approach is limited by knowledge of vibrissae growth rates, which are required to determine the time period represented by each subsampled segment. Likewise, determining the magnitude of, and variation in, isotopic differences between a consumer and its diet, commonly referred to as trophic discrimination factors (TDFs), is a crucial step in quantifying diet composition using stable isotopes. TDF estimates are available only for a few mammalian taxa. We measured vibrissae growth rates and δ 13 C and δ 15 N TDFs in captive southern sea otters (Enhydra lutris nereis). Sea otters were administered 15 N-enriched glycine intravenously and vibrissae were collected periodically and serially sampled for carbon (δ 13 C) and nitrogen (δ 15 N) isotope analysis. Growth of adult sea otter vibrissae was linear with a mean (±SD) rate of 7.7 (± 1.2) cm/year. Mean (±SD) whole diet—vibrissae TDFs were 2.8‰ (±0.2‰) for δ 13 C and 5.5‰ (±0.2‰) for δ 15 N. Mean (±SD) lipid-extracted diet—vibrissae TDFs were 2.4‰ (±0.2‰) for δ 13 C and 4.9‰ (±0.3‰) for δ 15 N. δ 13 C TDFs were similar to previously reported values for mammalian carnivores, but δ 15 N TDFs were higher than expected. These results will increase the accuracy of isotopic diet analyses of mustelids and other carnivores for which there are few estimates of TDFs and no estimates of vibrissae growth rates.
Development in foraging behaviour and dietary intake of many vertebrates are age-structured. Differences in feeding ecology may correlate with ontogenetic shifts in dispersal patterns, and therefore affect foraging habitat and resource utilization. Such life-history traits have important implications in interpreting tropho-dynamic linkages. Stable isotope ratios in the whiskers of sub-yearling southern elephant seals (Mirounga leonina; n = 12) were used, in conjunction with satellite telemetry and environmental data, to examine their foraging habitat and diet during their first foraging migration. The trophic position of seals from Macquarie Island (54°30'S, 158°57'E) was estimated using stable carbon (δ(1) (3)C) and nitrogen (δ(15)N) ratios along the length of the whisker, which provided a temporal record of prey intake. Satellite-relayed data loggers provided details on seal movement patterns, which were related to isotopic concentrations along the whisker. Animals fed in waters south of the Polar Front (>60°S) or within Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR) Statistical Subareas 88.1 and 88.2, as indicated by both their depleted δ(1) (3)C (
The southern coastline of Australia forms part of the worlds' only northern boundary current system. The Bonney Upwelling occurs every austral summer along the south-eastern South Australian coastline, a region that hosts over 80% of the worlds population of an endangered endemic otariid, the Australian sea lion. We present the first data on the movement characteristics and foraging behaviour of adult male Australian sea lions across their South Australian range. Synthesizing telemetric, oceanographic and isotopic datasets collected from seven individuals enabled us to characterise individual foraging behaviour over an approximate two year time period. Data suggested seasonal variability in stable carbon and nitrogen isotopes that could not be otherwise explained by changes in animal movement patterns. Similarly, animals did not change their foraging patterns despite fine-scale spatial and temporal variability of the upwelling event. Individual males tended to return to the same colony at which they were tagged and utilized the same at-sea regions for foraging irrespective of oceanographic conditions or time of year. Our study contrasts current general assumptions that male otariid life history strategies should result in greater dispersal, with adult male Australian sea lions displaying central place foraging behaviour similar to males of other otariid species in the region.
Highly dimorphic species like southern ele-phant seals (Mirounga leonina, SES hereafter) frequently exhibit resource partitioning according to sex and/or age classes. We measured carbon and nitrogen stable isotopes (d 13 C and d 15 N) of 404 blood samples (136 males and 268 females from Kerguelen Islands, 49°21 0 S, 70°18 0 E) from 2004 to 2011. Assuming that the distribution of carbon isotopes (d 13 C value) reflects the two main foraging grounds (Polar Frontal and Antarctic Zones), we quantified the proportion of SES foraging within each zone in relation with size, a proxy for their age. We found a clear shift from Polar Frontal to Antarctic waters as male SES aged, but no relation as far as females is concerned. We also observed a widening range of nitrogen isotopic (d 15 N) values, sug-gesting that both males and females expanded their diet spectra with age. Whereas males increased their trophic level, females remained constant on average, with some adult females feeding both at lower and at higher trophic levels than juveniles.
Growth rates of vibrissae (whiskers), which act as a temporal record of feeding in harbor seals (Phoca vitulina) and Steller sea lions (Eumetopias jubatus), were estimated using (13)C- and (15)N-labeled glycine followed by stable-isotope analysis. The labeled glycine was incorporated into keratin and served as a temporal marker for growth-rate calculation. One captive harbor seal received two doses 147 days apart, while a second seal received one dose; vibrissae were analyzed after 86 and 154 days. The peak positions indicated that growth began in the fall, continued into spring, but ceased in June, with active growth rates of 0.33 mm/day. Two adult captive Steller sea lions each received two labeled doses during a 308-day period. After 427 days vibrissae in both sea lions showed two peaks corresponding to the markers; growth rates were calculated as 0.05-0.07 mm/day. Growth rates in captive juvenile and wild adult Steller sea lions, 0.10-0.17 mm/day, supported the assumption that major isotopic oscillations in vibrissae of wild sea lions were annual. The multiyear records imply that Steller sea lions retain their vibrissae; harbor seal vibrissae, in contrast, have periods of rapid growth and appear to be shed, at least in part, annually.
Trophic interactions between organisms are the main drivers of ecosystem dynamics, but scant dietary information is available for wide-ranging predators during migration. We investi- gated feeding habits of a key consumer of the Southern Ocean, the southern elephant seal Miroun- gia leonina, by comparing its blood δ13C and δ15N values with those of various marine organisms, including crustaceans, squid, fishes, seabirds and fur seals. At the end of winter, δ13C values (-23.1 to -20.1‰) indicate that female elephant seals forage mainly in the vicinity of the Polar Front and in the Polar Frontal Zone. Trophic levels derived from δ15N values (trophic level = 4.6) show that the southern elephant seal is a top consumer in the pelagic ecosystem that is dominated by colossal squid. The mean δ15N value of seals (10.1 ± 0.3‰) indicates that they are not crustacean eaters, but instead feed on crustacean-eating prey. Surprisingly, most of the previously identified prey species have isotope δ13C and δ15N values that do not fit with those of potential food items. The most singular pattern to emerge from δ15N values of predators and prey is that female seals are likely to feed on myctophid fishes, not squid or Patagonian toothfish. We therefore suggest that they occupy a unique trophic niche amongst the guild of air-breathing, diving vertebrates by feeding on mesopelagic fish at great depths. In turn, this finding emphasizes the role of myctophids in oceanic waters and will help to quantify and model fluxes of matter and energy within the pelagic ecosystem of the Southern Ocean.
Lactating New Zealand fur seals (Arctocephalus forsteri (Lesson. 1828)) that breed at Cape Gantheaume. South Australia, experience broad-scale seasonal changes in ocean productivity. To assess how seasonal changes in ocean productivity influenced foraging behaviour. 18 lactating New Zealand fur seals were fitted with satellite transmitters and time-depth recorders (TDRs). Using temperature and depth data from TDRs. we used the presence of thermoclines as a surrogate measure of upwelling activity in continental-shelf waters. During the austral autumn 80% of lactating fur seals foraged on the continental shelf (114 +/- 44 km from the colony), in a region associated with the Bonney upwelling. In contrast, during winter months seals predominantly foraged in oceanic waters (62%), in a region associated with the Subtropical Front (460 +/- 138 km from the colony). Our results indicate that lactating New Zealand fur seals shift their foraging location from continental-shelf to oceanic waters in response to a seasonal decline in productivity over the continental shelf, attributed to the cessation of the Bonney upwelling. This study identified two regions used by lactating New Zealand fur seals: (1) a nearby and seasonally productive upwelling system and (2) a distant and permanent oceanic front.
Adult male, female and juvenile New Zealand and Australian fur seals Arctocephalus forsteri and A. pusillus doriferus regularly return to colonies, creating the potential for intra- and inter-specific foraging competition in nearby waters. We hypothesise that the fur seals in this study utilise different prey, thereby reducing competition and facilitating coexistence. We analysed scats and regurgitates from adult male, female and juvenile New Zealand fur seals and adult male Australian fur seals and compared prey remains found in the samples. Most prey consumed by adult male and female fur seals occur over the continental shelf or shelf break, less than 200 km from Cape Gantheaume. Adult female fur seals utilised proportionally more low-energy prey such as large squid and medium-sized fish. The adult female diet reflected that of a generalist predator, dictated by prey abundance and their dependant pups' fasting abilities, In contrast, adult male New Zealand and Australian fur seals consumed proportionally more energy-rich prey such as large fish or birds, most likely because they could more efficiently access and/or handle such prey. Juvenile fur seals primarily consumed small fish that occur in pelagic waters, south of the shelf break, suggesting juveniles cannot efficiently utilise prey where adult fur seals forage. The age and sex groups in this study employ dramatically different strategies to maximise their survival and reproductive success and consequently the prey that they utilise reflect their different physiological constraints and metabolic requirements.
ABSTRACT • Stable isotope analysis (SIA) has the potential to become a widespread tool in mammalian ecology, because of its power in resolving the ecological and behavioural characteristics of animals. Although applications of the technique have enhanced our understanding of mammalian biology, it remains underused. Here we provide a review of previous applications to the study of extant mammals, drawing when appropriate on examples from the wider ecological literature, to identify the potential for future development of the approach. • Stable isotope analysis has been applied successfully to understanding the basic foraging decisions of mammals. However, SIA generates quantitative data on a continuous scale meaning that the approach can be particularly powerful in the characterization of community metrics, such as dimensions of resource partitioning within species assemblages or nutrient dynamics in food chains. Resolving spatial and temporal patterns of individual, intraspecific and interspecific resource use is of fundamental importance in animal ecology and evolutionary biology and SIA will emerge as a critical tool in these fields. • Geographical differences in naturally occurring stable isotopes have allowed ecologists to describe large-scale mammal migrations. Several isotopic gradients exist at smaller spatial scales, which can provide finer resolution of spatial ecology. • A combination of foraging and movement decisions is of prime importance in the study of ecotoxicology, since this discipline requires quantitative understanding of exposure risk.
Information on the diet of threatened species is important in devising appropriate management plans to ensure their conservation. The Australian sea lion (Neophoca cinerea) is Australia's only endemic and globally one of the least numerous pinniped species. However, dietary information is currently limited because of the difficulty in using traditional methods (identification of prey hard parts from scats, regurgitates and stomach samples) to reliably provide dietary information. The present study assessed the use of fatty acid (FA) analysis to infer diet using milk samples collected from 11 satellite tracked Australian sea lions from Olive Island, South Australia. Satellite tracking revealed that females foraged in two distinct regions; 'inshore' regions characterised by shallow bathymetry (10.7 AE 4.8 m) and 'offshore' regions characterised by comparatively deep bathymetry (60.5 AE 13.4 m). Milk FA analysis indicated significant differences in the FA composition between females that foraged inshore compared with those that foraged offshore. The greatest differences in relative levels of individual FAs between the inshore and offshore groups were for 22 : 6n-3 (6.5 AE 1.2% compared with 16.5 AE 1.9% respectively), 20 : 4n-6 (6.1 AE 0.7 compared with 2.5 AE 0.7 respectively) and 22 : 4n-6 (2.4 AE 0.2% compared with 0.8 AE 0.2% respectively). Using discriminant scores, crustacean, cephalopod, fish and shark-dominated diets were differentiated. The discriminant scores from Australian sea lions that foraged inshore indicated a mixed fish and shark diet, whereas discriminant scores from Australian sea lions that foraged offshore indicated a fish-dominated diet, although results must be interpreted with caution due to the assumptions associated with the prey FA dataset. FA analysis in combination with satellite tracking proved to be a powerful tool for assessing broad-scale spatial dietary patterns.
A detailed high resolution survey of a small region (68
68 km) of the Subtropical Front south of Australia over a period of 14 days is
used to study the interaction between the mixed layer and the permanent frontal
structure underneath during summer conditions. The front extends through the
mixed layer as a salinity front, while its temperature structure is modified by
seasonal warming. Wind-driven movement of the mixed layer combines with the
short-time development of indentations and filaments in the front to produce
some degree of decoupling between the mixed layer and the underlying structure,
and the front is not always found at the same location in and below the mixed
layer. Intrusions and parcels of distinct water properties are found just below
the mixed layer, produced as a result of the relative movement of the front in
and below the mixed layer. These parcels are typically 10 km in width and 10–50
m in depth. Successive surveys of the front with a time separation of 2 days
showed that these features persist over at least 1 week. Large scale surveys of
the front show that parcels are ubiquitous along the Subtropical Front over a
distance of several hundred kilometres. The results suggest that any study
aimed at understanding the intricate interaction between the mixed layer and
the layers below in oceanic fronts will have to address wind-driven dynamics
and frontal dynamics together.
In the Southern Ocean, mesoscale features, such as fronts and eddies, have been shown to have a significant impact in structuring and enhancing primary productivity. They are therefore likely to influence the spatial structure of prey fields and play a key role in the creation of preferred foraging regions for oceanic top-predators. Optimal foraging theory predicts that predators should adjust their movement behaviour in relation to prey density. While crossing areas with sufficient prey density, we expect predators would change their behaviour by, for instance, decreasing their speed and increasing their turning frequency. Diving predators would as well increase the useful part of their dive i.e. increase bottom-time thereby increasing the fraction of time spent capturing prey. Southern elephant seals from the Kerguelen population have several foraging areas: in Antarctic waters, on the Kerguelen Plateau and in the interfrontal zone between the Subtropical and Polar Fronts. This study investigated how the movement and diving behaviour of 22 seals equipped with satellite-relayed data loggers changed in relation to mesoscale structures typical of the interfrontal zone. We studied the links between oceanographic variables including temperature and sea level anomalies, and diving and movement behaviour such as displacement speed, diving duration and bottom-time. Correlation coefficients between each of the time series were calculated and their significance tested with a parametric bootstrap. We focused on oceanographic changes, both temporal and spatial, occurring during behavioural transitions in order to clarify the connections between the behaviour and the marine environment of the animals. We showed that a majority of seals displayed a specific foraging behaviour related to the presence of both cyclonic and anticyclonic eddies. We characterized mesoscale oceanographic zones as either favourable or unfavourable based on the intensity of foraging activity as identified by the behavioural variables. Our findings highlight the importance of mesoscale features for top-predators’ behaviour and introduce a new approach for evaluating the importance to the seals of the origin and intensity of these features.
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.
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 δ(13)C and δ(15)N oscillations that correspond to the seal annual movements over the long term (up to 8 years). δ(13)C and δ(15)N 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.
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.
1. The stable isotopes of nitrogen (deltaN-15) and carbon (deltaC-13) were analysed in 22 species of marine birds from coastal waters of the northeast Pacific Ocean. Analyses confirm that stable nitrogen isotopes can predict seabird trophic positions. 2. Based on deltaN-15 analyses, seabird trophic-level inferences generally agree with those of conventional dietary studies, but suggest that lower trophic-level organisms are more important to several seabirds than was recognized previously. 3. Stable-carbon isotope analysis may be a good indicator of inshore vs. offshore feeding preference. 4. In general, stable-isotope analysis to determine trophic level offers many advantages over conventional dietary approaches since trophic inferences are based on time-integrated estimates of assimilated and not just ingested foods, and isotopic abundance represents a continuous variable that is amenable to statistical analysis.
Identifying individuals' foraging strategies is critical to understanding the ecology of a species, and can provide the means to predict possible ecological responses to environmental change. Our study combines stable isotope analysis and satellite telemetry to study the variability in individual foraging strategies of adult female southern elephant seals (Mirounga leonina). Our hypothesis is that female elephant seals from the Western Antarctica Peninsula (WAP) display individual specialization in their diets. We captured adult female elephant seals (n = 56, 2005-2009) at Livingston Island (Antarctica), and instrumented them with SMRU-CTD satellite tags. We collected blood, fur, and vibrissae samples for δ(13)C and δ(15)N analyses. The mean values for all vibrissae were -21.0 ± 0.7‰ for δ(13)C, and 10.4 ± 0.8‰, for δ(15)N. The individual variability of δ(13)C (60%) was more important than the within-individual variability (40%) in explaining the total variance observed in our data. For δ(15)N, the results showed the opposite trend, with the within-individual variability (64%) contributing more to the total variance than the individual variability (36%), likely associated with the effect that the fasting periods have on δ(15)N values. Most individuals were specialists, as inferred from the low intra-individual variability of δ(13)C values with respect to the population variability, with half the individuals utilizing 31% or less of their available niche. We found eight different foraging strategies for these animals. Female elephant seals from the WAP are a diverse group of predators with individuals utilizing only a small portion of the total available niche, with the consequent potential to expand their foraging habits to exploit other resources or environments in the Southern Ocean.
Until recently, large apex consumers were ubiquitous across the globe and had been for millions of years. The loss of these
animals may be humankind’s most pervasive influence on nature. Although such losses are widely viewed as an ethical and aesthetic
problem, recent research reveals extensive cascading effects of their disappearance in marine, terrestrial, and freshwater
ecosystems worldwide. This empirical work supports long-standing theory about the role of top-down forcing in ecosystems but
also highlights the unanticipated impacts of trophic cascades on processes as diverse as the dynamics of disease, wildfire,
carbon sequestration, invasive species, and biogeochemical cycles. These findings emphasize the urgent need for interdisciplinary
research to forecast the effects of trophic downgrading on process, function, and resilience in global ecosystems.
Declines in marine predator populations have been attributed to anthropogenic activity and environmental change. Southern elephant seals Mirounga leonina are major consumers of biomass in the eastern region of the Southern Ocean and have been declining in numbers since the 1960s. Previous studies have identified evidence for habitat and diet partitioning over a range of spatial and temporal scales between juveniles and adults in the Macquarie Island population. We first analysed the stable isotopes (SI) of 6 entire vibrissae from a dead adult female southern elephant seal from Kerguelen Islands to determine moult and growth patterns. Secondly we analysed the SI from the vibrissae of 102 juvenile southern elephant seals to investigate diet. The results from the growth pattern analysis indicated that vibrissae do not grow or moult simultaneously. However, it is likely that at least part of the vibrissae will have been produced sometime during the most recent trip to sea and will give a broad indication of diet. The subsequent SI analysis confirmed that juveniles are consuming greater proportions of fish species, and identified myctophids as the primary component of juvenile diet. Myctophids are also consumed by king penguins Aptenodytes patagonicus which have greatly increased in numbers recently in the Macquarie Island area. This may have presented the juvenile southern elephant seals with increased competition and may influence survival.
The sustainable exploitation of the marine environment depends upon our capacity to develop systems of management with predictable outcomes. Unfortunately, marine ecosystems are highly dynamic and this property could conflict with the objective of sustainable exploitation. This book investigates the theory that the population and behavioural dynamics of predators at the upper end of marine food chains can be used to assist with management. Since these species integrate the dynamics of marine ecosystems across a wide range of spatial and temporal scales, they offer new sources of information that can be formally used in setting management objectives. This book examines the current advances in the understanding of the ecology of marine predators and will investigate how information from these species could be used in management.
Central place foragers often change their foraging behaviour in response to changes in prey availability in the environment. Lactating Long-nosed fur seals (LNFS; Arctocephalus forsteri) at Cape Gantheaume in South Australia have been observed to display alternate foraging strategies where they forage on the shelf in summer and switch to oceanic foraging in winter. We investigated the relationship between changes in shelf summertime upwelling and the timing and variability when females switch from predominantly shelf to oceanic foraging. Geolocation tags were deployed on females from summer to winter in 2016 and 2017, giving us longitudinal tracks over the transition period. The timing of switching from shelf to oceanic foraging was primarily driven by seasonal oceanographic changes on the shelf – specifically when the strength of the seasonal localised upwelling began to decline. The individual variability in the timing of the switch was driven by the strength of the coastal upwelling with variability being greater in years when upwelling strength was weaker. By comparing our results to that of previous studies on the same colony, we found qualitative evidence that inter-annual environmental variability likely influences whether individuals display a single or multiple foraging strategies. This further highlights the flexibility in foraging strategies used by LNFS in response to environmental changes. The effect of inter-annual differences in foraging strategies on overall reproductive success warrants further investigation.
We determined the delta N-15 and delta C-13 values of individual amino acids (AAs) isolated from chick blood of 4 penguin species that forage in different oceanic regions (from the subtropics of the Indian Ocean to Antarctica) to test if: (1) the delta N-15 values of phenylalanine (delta N-15(phe)) revealed different foraging areas among the species; (2) the difference between glutamic acid and phenylalanine delta N-15 values (Delta delta N-15(glu-phe)) accurately predicted trophic levels; and (3) the delta C-13 value of AAs could resolve species foraging locations, similar to bulk delta C-13 values. The delta C-13 values of all AAs decreased with latitude, were positively correlated with bulk delta C-13 data, and, therefore, tracked the isotopic baseline. However, we were not able to discern additional ecological information from these delta C-13 values. In contrast, the delta N-15 values of AAs distinguished the isotopic value of the nitrogen at the base of the food web from the trophic level of the consumer, providing new insight for the study of the trophic ecology of seabirds. The difference in the bulk delta N-15 values of northern and southern rockhopper penguins Eudyptes chrysocome ssp. was due to both a difference in their foraging location (different delta N-15(phe)) and their trophic levels (different Delta delta N-15(glu-phe)). The delta N-15(phe) values of king Aptenodytes patagonicus and Adelie penguins Pygoscelis adeliae were higher than those of rockhoppers, which could reflect a foraging on mesopelagic prey for king penguins and, in the highly productive Antarctic shelf waters, for Adelie penguins. The Delta delta N-15(glu-phc) accurately reflected the relative trophic level of penguins, but further work is required to determine the trophic enrichment factors for compound-specific isotope analysis.
The degree of individual specialization in resource use differs widely among wild populations where individuals range from fully generalized to highly specialized. This interindividual variation has profound implications in many ecological and evolutionary processes. A recent review proposed four main ecological causes of individual specialization: interspecific and intraspecific competition, ecological opportunity and predation. Using the isotopic signature of subsampled whiskers, we investigated to what degree three of these factors (interspecific and intraspecific competition and ecological opportunity) affect the population niche width and the level of individual foraging specialization in two fur seal species, the Antarctic and subantarctic fur seals (Arctocephalus gazella and Arctocephalus tropicalis), over several years. Population niche width was greater when the two seal species bred in allopatry (low interspecific competition) than in sympatry or when seals bred in high-density stabilized colonies (high intraspecific competition). In agreement with the niche variation hypothesis (NVH), higher population niche width was associated with higher interindividual niche variation. However, in contrast to the NVH, all Antarctic females increased their niche width during the interbreeding period when they had potential access to a wider diversity of foraging grounds and associated prey (high ecological opportunities), suggesting they all dispersed to a similar productive area. The degree of individual specialization varied among populations and within the annual cycle. Highest levels of interindividual variation were found in a context of lower interspecific or higher intraspecific competition. Contrasted results were found concerning the effect of ecological opportunity. Depending on seal species, females exhibited either a greater or lower degree of individual specialization during the interbreeding period, reflecting species-specific biological constraints during that period. These results suggest a significant impact of ecological interactions on the population niche width and degree of individual specialization. Such variation at the individual level may be an important factor in the species plasticity with significant consequences on how it may respond to environmental variability.
Steller sea lions (SSL; Eumetopias jubatus) grow their vibrissae continually, providing a multiyear record suitable for ecological and physiological studies based on stable isotopes. An accurate age-specific vibrissae growth rate is essential for registering a chronology along the length of the record, and for interpreting the timing of ecologically important events. We utilized four methods to estimate the growth rate of vibrissae in fetal, rookery pup, young-of-the-year (YOY), yearling, subadult, and adult SSL. The majority of vibrissae were collected from SSL live-captured in Alaska and Russia between 2000 and 2013 (n = 1,115), however, vibrissae were also collected from six adult SSL found dead on haul-outs and rookeries during field excursions to increase the sample size of this underrepresented age group. Growth rates of vibrissae were generally slower in adult (0.44 ± 0.15 cm/mo) and subadult (0.61 ± 0.10 cm/mo) SSL than in YOY (0.87 ± 0.28 cm/mo) and fetal (0.73 ± 0.05 cm/mo) animals, but there was high individual variability in these growth rates within each age group. Some variability in vibrissae growth rates was attributed to the somatic growth rate of YOY sea lions between capture events (P = 0.014, r2 = 0.206, n = 29).
Measurements of the 6~3C of total dissolved inorganic carbon (Y:-CO 2) in the world oceans are presented. Most of the samples are from the GEOSECS expeditions which covered the Atlantic, Pacific, and Indian oceans between 1971 and 1978. The results from 2252 samples from 107 hydrographic stations are presented as north-south vertical (depth) sections with 81~C con-toured at intervals of 0.196o. The data show that the distribution of 5~3C is controlled mainly by the input of organically produced material and its subsequent oxidation as it falls through the water column. This covariance can be summarized by the regression equation: 6t3C = 1.5-0.0075. AOU, where AOU represents the oxygen utilization within a water sample after leaving the surface. Other factors influencing the distribution of 8tJC are the dissolution of inorganic carbonate and the addition of anthropogenic CO2 to the oceans. A complex mathematical model was employed to estimate the levels of 12CO 2 and ~'3C in pre-industrial oceanic surface waters. The results suggest that the Y-CO2 of surface waters has increased by 40 ttmole kg -t from a pre-industrial level of approximately 2135 ttmole kg-~. The 6~C of the Y.CO 2 has decreased by 0.5%o from a pre-industrial value of approximately 2.596o.
During a large-scale ecosystem study on the south-east Australian shelf in
spring 1994, we opportunistically sampled a widespread phytoplankton bloom.
Thalassiosira partheneia, a small centric diatom, was
the primary species in the bloom, indicating that we had sampled the early
stage of a typical short-lived spring bloom for the area. Pigment analysis
indicated four distinct communities that were coincident with the regional
oceanography. The bloom was strongest over the northern shelf where the East
Australian Current overlaid uplifted nutrient-rich slope water, but absent at
inner stations on the wide southern shelf, where slope water did not reach.
The bloom was patchy over the southern outer shelf where slope water was
present to the surface and local conditions were influenced by topography.
Pigment and stable isotope data indicated that primary production in this area
was almost entirely oceanic. A slight trend for seaward enrichment of sediment
δ13C is best explained by limited macroalgal
growth in shallow waters. There was little fresh organic matter in the
sediment even for stations under the bloom, suggesting that the bloom did not
reach the seabed directly. The lack of specific zooplankton grazing pigments
suggests that zooplankton grazing was minimal.
Human activities have serious impacts on marine apex predators. Inadequate knowledge of the spatial and trophic ecology of these marine animals ultimately compromises the viability of their populations and impedes our ability to use them as environmental biomonitors. Intrinsic biogeochemical markers, such as stable isotopes, fatty acids, trace elements, and chemical pollutants, are increasingly being used to trace the spatial and trophic ecology of marine top predators. Notable advances include the emergence of the first océanographie "isoscapes" (isotopic geographic gradients), the advent of compound-specific isotopic analyses, improvements in diet reconstruction through Bayesian statistics, and tissue analysis of tracked animals to ground-truth biogeochemical profiles. However, most researchers still focus on only a few tracers. Moreover, insufficient knowledge of the biogeochemical integration in tissues, fractionation and routing processes, and geographic and temporal variability in baseline levels continue to hamper the resolution and potential of these markers in studying the spatial and feeding ecology of top predators.
We have measured the carbon isotopic composition of particulate organic
matter suspended in surface waters (POM) between 59°S and 30°S
in the SW Indian Ocean during the austral summer. In an attempt to
further document the pattern and causes of covariance between
POC-δ13C and [CO2aq], we concurrently
measured surface water pCO2, temperature, salinity, nitrate
concentration, POM concentration, chlorophyll a and the
δ13C of total dissolved inorganic carbon. While we
found the previously reported general negative correlation between
POC-δ13C and [CO2aq], we also observed a
prominent maximum in POC-δ13C in the region immediately
north of the Subtropical Convergence, coinciding with a maximum in [POM]
and chlorophyll a, and with a minimum in pCO2. The increase
in POC-δ13C between 59°S and the Subtropical
Convergence is consistent with the trend expected if [CO2aq]
were the main factor controlling the isotopic composition of POM. In
contrast, data from the region north of the Subtropical Convergence
clearly illustrate that POC-δ13C can also vary
independently of [CO2aq] as a 5 per mil decrease in
POC-δ13C was found in a region characterized by nearly
constant [CO2aq]. We review several physiological factors
which may account for these observations and discuss their implications
for paleoceanographic reconstruction of [CO2aq] from the
carbon isotopic composition of sedimentary organic matter.
The isotopic composition of many elements varies across both land and ocean surfaces in a predictable fashion. These stable-isotope ratios are transferred into animal tissues, potentially providing a powerful natural geospatial tag. To date, most studies using stable isotopes as geolocators in marine settings have focussed on mammals and seabirds conducting large ocean-basin scale migrations. An increasing understanding of isotopic variation in the marine environment, and improved sampling and analytical techniques, however, means that stable isotopes now hold genuine promise as a natural geolocation tag in marine fishes. Here, the theoretical background underpinning the use of stable isotopes of C, N and O in otolith, scale and muscle tissues as geolocation tools in the marine environment is reviewed, and examples of their applications are provided.
Stable isotope analysis (SIA) has emerged as a common tool in ecology and has proven especially useful in the study of animal diet, habitat use, movement, and physiology. SIA has been vigorously applied to the study of marine mammals, because most species live in habitats or undergo large migrations/movements that make them difficult to observe. Our review supplies a complete list of published SIA contributions to marine mammal science and highlights informative case examples in four general research areas: (1) physiology and fractionation, (2) foraging ecology and habitat use, (3) ecotoxicology, and (4) historic ecology and paleoecology. We also provide a condensed background of isotopic nomenclature, highlight several physiological considerations important for accurate interpretation of isotopic data, and identify research areas ripe for future growth. Because it is impossible to conduct controlled laboratory experiments on most marine mammal species, future studies in marine mammal ecology must draw on isotopic data collected from other organisms and be cognizant of key assumptions often made in the application of SIA to the study of animal ecology. The review is designed to be accessible to all audiences, from students unfamiliar with SIA to those who have utilized it in published studies.
Summary1.This study examined the changing status of the marine ecosystem at the island of South Georgia (Southern Ocean) using up to 27 variables measured over 22 years from three upper trophic level predators that specialize in foraging upon krill (Eupuasia superba Dana). These variables included population size, breeding performance, offspring growth rate, foraging behaviour and diet. A method was developed for reducing these multivariate time-series to a single vector, called a combined standardized index (CSI).2.Sensitivity analyses showed that missing values had a large effect upon the accuracy of the CSI but this effect was reduced if the individual variables were highly correlated. The level of correlation and proportion of missing values within the empirical data set were within the acceptable range. Individual variables had widely varying influence upon the CSI but, in general, those with longer time-series had the greatest influence.3.Principal components analysis showed that variables representing offspring growth tended to explain the greatest proportion of the variability in the CSI and this was followed by variables representing diet.4.There were 3 years in which the CSI showed extreme and significantly low values. There was a significant non-linear functional response (similar to the Holling Type II functional response) between the overall CSI and krill biomass and a similar relationship existed when the CSI was calculated for each species individually.5.Separate analysis of variables that were likely to be representative of changing population size showed the presence of a significant decline between 1977 and 1998. There was no trend in the CSI from variables representative of foraging conditions during the summer breeding season. The study has shown that the marine ecosystem at South Georgia shows acute but transient variability that is amplified in the response of upper trophic-level predators. There is less certainty that trends in populations are a consequence of shifts in the degree to which the ecosystem can support krill-feeding seals and penguins.
Stable isotope signatures of lactating females and their nursing offspring were measured on 11 species, including herbivores, carnivores, hibernators, and non-hibernators. We hypothesized that: (1) nursing offspring would have stable isotope signatures that were a trophic level higher than their mothers, and (2) this pattern would be species-independent. The plasma of adult females had a ཋN enrichment over their diets of 4.1ǂ.7, but offspring plasma had a mean ཋN enrichment over maternal plasma of 0.9ǂ.8 and no C enrichment (0.0ǂ.6). The trophic level enrichment did not occur between mother and offspring because milk was depleted in both ཋN (1.0ǂ.5) and ཉC (2.1ǂ.9) relative to maternal plasma. Milk to offspring plasma enrichment was relatively small (ཋN enrichment of 1.9ǂ.7 and ཉC enrichment of 1.9ǂ.8) compared to the trophic level enrichment between the adults and their diets. While some species did have significant differences between the isotope signatures of mother and offspring, the differences were not related to whether they were hibernators or non-hibernators, carnivores or herbivores. Investigators wanting to use stable isotopes to quantify weaning or other lactation processes or diets of predators when both adults and nursing offspring are consumed must first establish the parameters that apply to a particular species/environment/diet combination.
Ratios of stable carbon and nitrogen isotopes were examined in the baleen of 11 southern right whales originating from South Africa, including one neonate, six juveniles and four adults. Oscillations in carbon isotope ratios were marked, and indicated feeding north of or at the Subtropical Convergence (STC) alternating with feeding south of the STC. There was an inverse relationship in juveniles between the periodicity of the oscillations and the length of the baleen plate, indicating a reduction in baleen growth with age. The size of the periodicity predicted for the smallest juvenile plate was equivalent to the length of the baleen at 1 yr of age as estimated from the rate of baleen growth in calves, suggesting that the oscillations in carbon isotope ratios were annual events. On this assumption, the timing of the formation of the most recent carbon enrichment peak could be calculated for each individual, given the date of death and the rate of baleen growth in the preceding year; formation occurred over a period of 100 d from January to April (mean in February). A similar analysis indicated that valleys in the nitrogen isotope ratios were formed between January and June (mean in April), and enrichment peaks between August and May (mean in December). These patterns were not inconsistent with previous scenarios of southern right whale migration, if the enrichment peaks in carbon isotopes were taken to represent feeding just north of the STC, the subsequent decline in enrichment levels to represent feeding south of the STC in autumn, and the persistence of an isotopic signature characteristic of high latitude plankton throughout the winter and early spring to indicate that feeding essentially ceased when the northern migration began, and did not resume until the southern migration was under way. The oscillations in nitrogen isotope ratios would support this interpretation, if they were assumed to represent cycles of starvation and recovery. A comparison with baleen growth rates for bowhead whales allowed the ages of the six juveniles to be assessed. Their size at age, when compared to the lengths and growth rates of calves measured photogrammetrically, suggested that growth in body length of southern right whales slows markedly between weaning and 1 yr, and may be almost negligible from 1 to 4 yr of age.
A review is presented of the ocean circulation along Australia’s southern shelves and slope. Uniquely, the long, zonal shelf is subject to an equatorward Sverdrup transport that gives rise to the Flinders Current – a small sister to the world’s major Western Boundary Currents. The Flinders Current is strongest near the 600 m isobath where the current speeds can reach 20 cm/s and the bottom boundary layer is upwelling favourable. It is larger in the west but likely intermittent in both space and time due to possibly opposing winds, thermohaline circulation and mesoscale eddies. The Flinders Current may be important to deep upwelling within the ubiquitous canyons of the region.
13C contents of total dissolved inorganic carbon (δ13C-DIC) and particulate organic matter (δ13Corg) were determined to examine the factors influencing phytoplankton 13C contents and carbon export from the SOIREE iron-induced algal bloom. Suspended particles sieved into 200, 70, 20, 5, and 1 micrometer (μm) size classes displayed an extremely large range in δ13Corg of 8‰. δ13Corg values increased from −28‰ for the 1–5 μm class to a maximum of −20‰ for the 20–70 μm class, which was dominated by the large pennate diatom Fragilariopsis kerguelensis. Larger particles (70–200 and >200 μm) had similar δ13Corg to the smaller (1–5 and 5–20 μm) particles, reflecting both the presence of long narrow Thalassiothrix antarctica diatoms and zooplankton that grazed on small phytoplankton. Comparison of results inside and outside the bloom identified cell surface/volume ratio (mainly reflecting cell size) as the dominant control of phytoplankton δ13Corg, with subsidiary roles for growth rate and seawater [CO2]aq. The SOIREE iron fertilization provoked an increase in the proportion of large (>20 μm) diatoms. This increased the δ13Corg of the bulk suspended particles within the mixed layer, but there was minimal increase in the δ13Corg of sub-surface suspended particles and negligible change in the δ13Corg of particles obtained with sediment traps suspended below the bloom. This suggests that there was no increase in carbon export over the ∼13 day observation period. However, comparison to δ13Corg results from previous voyages, and to vertical changes in δ13C-DIC, suggests that large diatoms control carbon export from the Antarctic Zone over the summer growth season. This result must be viewed with great caution as it is based on very sparse data and involves several assumptions.
Choices made by foraging animals should maximize energy intake, although ‘irrational’ short-term behaviours are common. One explanation for this is that environmental variation may lead to the evolution of behaviours that benefit individual reproductive output, but only over long timescales. Long-term (multiyear) fidelity to foraging regions in extremely variable environments may confer ecological benefits to individuals, such as familiarity with resources, even when energy gain is not consistently high in all years. We examined the annual foraging ranges (sometimes exceeding 3.5 million km2) of female southern elephant seals, Mirounga leonina, over 4 years and found that individuals used preferred regions year after year. We hypothesized that the degree of fidelity in a particular year was related to the foraging success (as measured by mass gain) in the previous year; however, there was no significant relation between the two. Despite this high variation in annual foraging success, the regions revisited in consecutive years provided higher potential food production as measured by higher variance in sea surface temperatures over two decades (a surrogate measure of ocean productivity). The evolution of long-term fidelity assisted by simple navigational rules may confer energetic advantages over an individual's lifetime and explain the existence of seemingly nonadaptive short-term behaviours.
The Leeuwin Current (LC) is an unusual poleward-flowing eastern boundary current that carries warm, low-salinity water southward along the coast of Western Australia. LC dynamics include the formation of a dynamic mesoscale eddy field whose biological dynamics have not been studied. Satellite altimetry indicates that the eddies studied in the 2003 field programme were dynamically typical of LC eddies, but the warm-core (WC) eddy was relatively large and long-lived. The WC eddy contained relatively elevated chlorophyll a concentrations thought to originate, at least in part, from the continental shelf/shelf break region and to have been incorporated during eddy formation. Primary production per unit volume in the WC eddy was ∼2× higher than in the cold-core (CC) eddy due to an historical accumulation of chlorophyll a over the period since eddy formation (5–6 months), though chlorophyll a-specific daily production was volumetrically ∼50% greater in the CC eddy. In the WC eddy, nitrate uptake rates were 4× greater than in the CC eddy, despite the fact that vertical diffusive fluxes of nitrate into the WC eddy were probably only 50% of those in the CC eddy. We therefore hypothesize that other nitrate sources were important, possibly including isopycnal mixing and/or lateral transport into the eddy from surrounding waters. In addition, a deep mixed layer favoured a large (>5 μm) diatom population within the centre of the WC eddy while the CC eddy was persistently stratified, with a shallower mean mixed-layer depth (∼100 m vs. ∼200 m for the WC eddy) and a well developed deep chlorophyll a maximum at ∼100 m composed of 30% prochlorophytes (not capable of taking up nitrate). Both factors probably contributed to higher f-ratios in the WC and in the >5 μm phytoplankton relative to total phytoplankton.
Explains isotope terminology and fractionation, and summarises isotopic distributions in the C, N and S biogeochemical cycles. Five case studies (delta 15N measures of N2 fixation; the global carbon cycle and the CO2 problem; sulphur and acid deposition; use in archaeology; and detrital organic matter in saltmarshes) show how stable isotope measurements can provide crucial information for ecosystem analysis.-P.J.Jarvis