Palaeoclimatic changes resulted in range expansion and subsequent divergence in brown fur seals, Arctocephalus pusillus.

Past climatic change as a driving force of marine diversification is still largely unclear, particularly for Southern Hemisphere species. Here, we present a case using the brown fur seal, Arctocephalus pusillus, assessing the geographical structure and demographic history using mitochondrial and nuclear data. Results show the two previously defined subspecies (one from Australia and the other from southern Africa) are phylogeographically distinct. Migration analyses based on nuclear data suggest the absence of migrants among the two genetically close assemblages. The demographic history of A. pusillus is characterized by a glacial population expansion (approx. 18 kya) in the southern African lineage, which coincides with time estimates of population expansion of prey species of seals. Approximate Bayesian calculations support an eastward dispersal event during the Last Glacial Maximum when sea levels were lower, followed by a postglacial divergence event, approximately 13 kya. The demographic history of the brown fur seal in the Southern Oceans provides support that recent palaeoclimatic changes could have facilitated expansions in some marine species and that postglacial sea-level rise may have acted as a dispersal barrier for species mostly confined to continental shelves.

Quantity over quality? Prey-field characteristics influence the foraging decisions of little penguins (Eudyptula minor).

Quantifying prey characteristics is important for understanding the foraging behaviour of predators, which ultimately influence the structure and function of entire ecosystems. However, information available on prey is often at magnitudes which cannot be used to infer the fine-scale behaviour of predators, especially so in marine environments where direct observation of predator-prey interactions is rarely possible. In the present study, animal-borne video data loggers were used to determine the influence of prey type and patch density on the foraging behaviour of the little penguin (Eudyptula minor), an important predator in southeastern Australia. We found that numerical density positively influenced time spent foraging at a patch. However, when accounting for calorific value in density estimates, individuals spent longer at dense patches of low-quality prey. This may reflect a trade-off between capture effort and calorific gain as lower quality prey were captured at higher rates. During the breeding season, foraging trip distance and duration is constrained by the need to return to the colony each day to feed offspring. The results of the study suggest that, under these spatio-temporal constraints, little penguins maximize foraging performance by concentrating efforts at larger quantities of prey, irrespective of their calorific quality.

Interspecific and intraspecific foraging differentiation of neighbouring tropical seabirds.

BACKGROUND: Social interactions, reproductive demands and intrinsic constraints all influence foraging decisions in animals. Understanding the relative importance of these factors in shaping the way that coexisting species within communities use and partition resources is central to knowledge of ecological and evolutionary processes. However, in marine environments, our understanding of the mechanisms that lead to and allow coexistence is limited, particularly in the tropics. METHODS: Using simultaneous data from a suite of animal-borne data loggers (GPS, depth recorders, immersion and video), dietary samples and stable isotopes, we investigated interspecific and intraspecific differences in foraging of two closely-related seabird species (the red-footed booby and brown booby) from neighbouring colonies on the Cayman Islands in the Caribbean. RESULTS: The two species employed notably different foraging strategies, with marked spatial segregation, but limited evidence of interspecific dietary partitioning. The larger-bodied brown booby foraged within neritic waters, with the smaller-bodied red-footed booby travelling further offshore. Almost no sex differences were detected in foraging behaviour of red-footed boobies, while male and female brown boobies differed in their habitat use, foraging characteristics and dietary contributions. We suggest that these behavioural differences may relate to size dimorphism and competition: In the small brown booby population (n < 200 individuals), larger females showed a higher propensity to remain in coastal waters where they experienced kleptoparasitic attacks from magnificent frigatebirds, while smaller males that were never kleptoparasitised travelled further offshore, presumably into habitats with lower kleptoparasitic pressure. In weakly dimorphic red-footed boobies, these differences are less pronounced. Instead, density-dependent pressures on their large population (n > 2000 individuals) and avoidance of kleptoparasitism may be more prevalent in driving movements for both sexes. CONCLUSIONS: Our results reveal how, in an environment where opportunities for prey diversification are limited, neighbouring seabird species segregate at-sea, while exhibiting differing degrees of sexual differentiation. While the mechanisms underlying observed patterns remain unclear, our data are consistent with the idea that multiple factors involving both conspecifics and heterospecifics, as well as reproductive pressures, may combine to influence foraging differences in these neighbouring tropical species.

Validating accelerometry-derived proxies of energy expenditure using the doubly labelled water method in the smallest penguin species.

Understanding energy use is central to understanding an animal's physiological and behavioural ecology. However, directly measuring energy expenditure in free-ranging animals is inherently difficult. The doubly labelled water (DLW) method is widely used to investigate energy expenditure in a range of taxa. Although reliable, DLW data collection and analysis is both financially costly and time consuming. Dynamic body acceleration (e.g. VeDBA) calculated from animal-borne accelerometers has been used to determine behavioural patterns, and is increasingly being used as a proxy for energy expenditure. Still its performance as a proxy for energy expenditure in free-ranging animals is not well established and requires validation against established methods. In the present study, the relationship between VeDBA and the at-sea metabolic rate calculated from DLW was investigated in little penguins (Eudyptula minor) using three approaches. Both in a simple correlation and activity-specific approaches were shown to be good predictors of at-sea metabolic rate. The third approach using activity-specific energy expenditure values obtained from literature did not accurately calculate the energy expended by individuals. However, all three approaches were significantly strengthened by the addition of mean horizontal travel speed. These results provide validation for the use of accelerometry as a proxy for energy expenditure and show how energy expenditure may be influenced by both individual behaviour and environmental conditions.

Dive behaviour and foraging effort of female Cape fur seals Arctocephalus pusillus pusillus.

While marine top predators can play a critical role in ecosystem structure and dynamics through their effects on prey populations, how the predators function in this role is often not well understood. In the Benguela region of southern Africa, the Cape fur seal (Arctocephalus pusillus pusillus) population constitutes the largest marine top predator biomass, but little is known of its foraging ecology other than its diet and some preliminary dive records. Dive information was obtained from 32 adult females instrumented with dive recorders at the Kleinsee colony (29°34.17' S, 16°59.80' E) in South Africa during 2006-2008. Most dives were in the depth range of epipelagic prey species (less than 50 m deep) and at night, reflecting the reliance of Cape fur seals on small, vertically migrating, schooling prey. However, most females also performed benthic dives, and benthic diving was prevalent in some individuals. Benthic diving was significantly associated with the frequency with which females exceeded their aerobic dive limit. The greater putative costs of benthic diving highlight the potential detrimental effects to Cape fur seals of well-documented changes in the availability of epipelagic prey species in the Benguela.

Early-life sexual segregation: ontogeny of isotopic niche differentiation in the Antarctic fur seal.

Investigating the ontogeny of niche differentiation enables to determine at which life-stages sexual segregation arises, providing insights into the main factors driving resource partitioning. We investigated the ontogeny of foraging ecology in Antarctic fur seals (Arctocephalus gazella), a highly dimorphic species with contrasting breeding strategies between sexes. Sequential δ(13)C and δ(15)N values of whiskers provided a longitudinal proxy of the foraging niche throughout the whole life of seals, from weaning, when size dimorphism is minimal to the age of 5. Females exhibited an early-life ontogenetic shift, from a total segregation during their first year at-sea, to a similar isotopic niche as breeding females as early as age 2. In contrast, males showed a progressive change in isotopic niche throughout their development such that 5-year-old males did not share the same niche as territorial bulls. Interestingly, males and females segregated straight after weaning with males appearing to feed in more southerly habitats than females. This spatial segregation was of similar amplitude as observed in breeding adults and was maintained throughout development. Such early-life niche differentiation is an unusual pattern and indicates size dimorphism and breeding constraints do not directly drive sexual segregation contrary to what has been assumed in otariid seals.

Mating success and body condition not related to foraging specializations in male fur seals.

Individual specialization is widespread among wild populations. While its fitness consequences are central in predicting the ecological and evolutionary trajectories of populations, they remain poorly understood. Long-term individual foraging specializations occur in male Antarctic (Arctocephalus gazella) and Australian (A. pusillus doriferus) fur seals. Strong selective pressure is expected in these highly dimorphic and polygynous species, raising the question of the fitness payoffs associated with different foraging strategies. We investigated the relationship between individual isotopic niche (a proxy of foraging specialization), body size and condition, and an index of reproductive success (harem size) in territorial males. Individuals varied greatly in their skin and fur isotopic values reflecting a range of foraging strategies within the two populations. However, in both species, isotopic niche was not correlated to body size, condition or mating success (R (2)/ρ < 0.06). Furthermore, no foraging niche was predominant in either species, which would have indicated a substantial long-term fitness benefit of a particular strategy via a higher survival rate. These results suggest that the fitness consequences of a foraging strategy depend not only on the quality of prey and feeding habitat but also on an individual's hunting efficiency and skills.

Changes in behaviour drive inter-annual variability in the at-sea distribution of northern gannets.

The at-sea distribution of seabirds primarily depends on the distance from their breeding colony, and the abundance, distribution and predictability of their prey, which are subject to strong spatial and temporal variation. Many seabirds have developed flexible foraging strategies to deal with this variation, such as increasing their foraging effort or switching to more predictable, less energy dense, prey, in poor conditions. These responses may vary both within and between individuals, and understanding this variability is vital to predict the population-level impacts of spatially explicit environmental disturbances, such as offshore windfarms. We conducted a multi-year tracking study in order to investigate the inter-annual variation in the foraging behaviour and location of a population of northern gannets breeding on Alderney in the English Channel. To do so, we investigated the link between individual-level behaviour and population-level behaviour. We found that a sample of gannets tracked in 2015 had longer trip durations, travelled further from the colony and had larger core foraging areas and home range areas than gannets tracked in previous years. This inter-annual variation may be associated with oceanographic conditions indexed by the North Atlantic Oscillation (NAO). Our findings suggest that this inter-annual variation was driven by individuals visiting larger areas in all of their trips rather than individuals diversifying to visit more, distinct areas. These findings suggest that, for gannets at least, if prey becomes less abundant or more widely distributed, more individuals may be required to forage further from the colony, thus increasing their likelihood of encountering pressures from spatially explicit anthropogenic disturbances.

Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion.

Despite global declines in the abundance of marine predators, knowledge of foraging ecology, necessary to predict the ecological consequences of large changes in marine predator abundance, remains enigmatic for many species. Given that populations suffering severe declines are of conservation concern, we examined the foraging ecology of southern sea lions (SSL) (Otaria flavescens)-one of the least studied otariids (fur seal and sea lions)-which have declined by over 90% at the Falkland Islands since the 1930s. Using a combination of biologging devices and stable isotope analysis of vibrissae, we redress major gaps in the knowledge of SSL ecology and quantify patterns of individual specialization. Specifically, we revealed two discrete foraging strategies, these being inshore (coastal) and offshore (outer Patagonian Shelf). The majority of adult female SSL (72% or n = 21 of 29 SSL) foraged offshore. Adult female SSL that foraged offshore travelled further (92 ± 20 vs. 10 ± 4 km) and dived deeper (75 ± 23 vs. 21 ± 8 m) when compared to those that foraged inshore. Stable isotope analysis revealed long-term fidelity (years) to these discrete foraging habitats. In addition, we found further specialization within the offshore group, with adult female SSL separated into two clusters on the basis of benthic or mixed (benthic and pelagic) dive behavior (benthic dive proportion was 76 ± 9 vs. 51 ± 8%, respectively). We suggest that foraging specialization in depleted populations such as SSL breeding at the Falkland Islands, are influenced by foraging site fidelity, and could be independent of intraspecific competition. Finally, the behavioral differences we describe are crucial to understanding population-level dynamics, impediments to population recovery, and threats to population persistence.

Factors affecting the foraging behaviour of the European shag: implications for seabird tracking studies.

Seabird tracking has become an ever more popular tool to aid environmental procedures such as the designation of marine protected areas and environmental impact assessments. However, samples used are usually small and little consideration is given to experimental design and sampling protocol. European shags Phalacrocorax aristotelis were tracked using GPS technology over three breeding seasons and the following foraging trip characteristics: trip duration, trip distance, maximum distance travelled from the colony, size of area used and direction travelled from colony were determined for each foraging trip. The effect of sex, year of study, breeding site, number and age of chicks and the timing of tracking on foraging behaviour were investigated using a General Estimation Equation model. A range of sampling scenarios reflecting likely field sampling were also tested to compare how foraging behaviour differed depending on composition of the sample of birds tracked. Trip distance, trip duration, maximum distance travelled and size of area used were all significantly affected by the breeding site, and the number of chicks a tracked adult was raising. The effect of sex was also seen when examining trip distance, trip duration and the maximum distance travelled. The direction travelled on a foraging trip was also significantly affected by breeding site. This study highlights the importance of sampling regime and the influence that year, sex, age, number of chicks and breeding site can have on the foraging trip characteristics for this coastal feeding seabird. Given the logistical and financial constraints in tracking large numbers of individuals, this study identifies the need for researchers to consider the composition of their study sample to ensure any identified foraging areas are as representative as possible of the whole colony's foraging area.

Plasma cortisol and thyroid hormone concentrations in pre-weaning Australian fur seal pups.

The hormonal factors that influence development from birth to weaning in otariid seals is still largely unknown. In the present study, a suite of thyroid hormones and cortisol were measured in Australian fur seal pups in order to determine baseline concentrations as well as to describe their endocrinology over this critical developmental period. A cross-section of newborn pups from a breeding colony located on Kanowna Island, Australia were sampled at six different times over the course of the 10 month lactation period. Sample times were designed to correspond to periods of heightened physiological change during pre-weaning development: post-natal, pre-molt, the initiation of molt, mid-molt, period of peak milk intake and weaning. Results indicate that the greatest hormonal changes were associated with the post-natal stage and molt, with molt showing the greatest changes, as has been reported for several species of pinnipeds. Two forms of thyroid hormones analyzed (Total T(4), and Free T(3)), increased with the initiation of the molt, and Free T(3) exhibited a second increase that was associated with the period of peak milk intake. The T(3):T(4) ratio was significantly lower during the initiation of molt than either pre- or mid-molt. The study was able to describe physiological change during the first year of life in Australian fur seals as well as document basal concentrations of thyroid hormones and cortisol in pups of this species.

Terrestrial apnoeas and the development of cardiac control in Australian fur seal (Arctocephalus pusillus doriferus) pups.

The development of cardiac control in association with terrestrial respiration patterns was examined throughout the period of maternal dependence in Australian fur seal pups. Resting eupnoic heart rate and respiration rate were significantly correlated (r (2) = 0.49) and both decreased with age (P < 0.05 in both cases). From an early age (1 month), pups displayed terrestrial apnoeas (18.1 +/- 0.5 s) accompanied by substantial bradycardia (127 beats min(-1), a 13% decrease from eupnoic HR). Terrestrial apnoea duration increased significantly with age reaching a mean of 41 s just prior to weaning, slightly lower than the mean dive duration (52 s) previously recorded for pups of the same age. Correspondingly, mean apnoic heart rate decreased with age to 74 beats min(-1) just prior to weaning, representing a 25% decrease on eupnoic heart rate. Importantly, concomitant with the decrease in mean apnoic heart rate with age, an increase in the control of bradycardia was evident with the variability in instantaneous apnoic heart decreasing such that older pups were able to maintain a low steady heart rate for the duration of the apnoea. The changes seen in these parameters are similar to those reported during postnatal development in elephant seals (Mirounga spp.) and harbour seals (Phoca vitulina), and are considered indicative of the development of cardiac control. These findings suggest a common strategy for the development of bradycardia control in both otariid and phocid seals.

Acoustic features involved in the neighbour-stranger vocal recognition process in male Australian fur seals.

Many territorial species have the ability to recognise neighbours from stranger individuals. If the neighbouring individual is assumed to pose less of a threat, the territorial individual responds less and avoids unnecessary confrontations with familiar individuals at established boundaries, thus avoiding the costly energy expenditure associated with fighting. Territorial male Australian fur seals respond more to strangers than to neighbouring males. The present study evaluated which acoustic features were important in the neighbour-stranger recognition process in male Australian fur seals. The results reveal that there was an increase in response strength or intensity from males when they heard more bark units, indicating the importance of repetition to detect a caller. However, lengthening and shortening the inter-unit spaces, (i.e. changing the rhythm of the call) did not appear to significantly affect an animal's response. In addition, the whole frequency spectrum was considered important to recognition with results suggesting that they may vary in their importance. A call containing the dominant and surrounding harmonics was considered important to a male's ability to recognise its neighbour. Furthermore, recognition occurs even with a partial bark, but males need to hear between 25 and 75% of each bark unit from neighbouring seals. Our study highlights which acoustic features induce stronger or weaker responses from territorial males, decoding the important features in neighbour-stranger recognition.

The physiological and behavioural development of diving in Australian fur seal (Arctocephalus pusillus doriferus) pups.

The physiological and behavioural development of diving was examined in Australian fur seal (Arctocephalus pusillus doriferus) pups to assess whether animals at weaning are capable of exploiting the same resources as adult females. Haematocrit, haemoglobin and myoglobin contents all increased throughout pup development though total body oxygen stores reached only 71% of adult female levels just prior to weaning. Oxygen storage components, however, did not develop at the same pace. Whereas blood oxygen stores had reached adult female levels by 9 months of age, muscle oxygen stores were slower to develop, reaching only 23% of adult levels by this age. Increases in diving behaviour corresponded to the physiological changes observed. Pups spent little time (<8%) in the water prior to moulting (age 1-2 months) whereas following the moult, they spent >27% of time in the water and made mid-water dives (maximum depth 35.7 +/- 2.9 m) with durations of 0.35 +/- 0.03 min. By 9 months (just prior to weaning), 30.5 +/- 9.3% of all dives performed were U-shaped benthic dives (maximum depth 65.0 +/- 6.0 m) with mean durations of 0.87 +/- 0.25 min, significantly shorter than those of adult females. These results suggest that while Australian fur seal pups approaching the age of weaning are able to reach similar depths as adult females, they do not have the physiological capacity to remain at these depths for sufficient durations to exploit them to the same efficiency.

Variation in the fatty acid composition of blubber in Cape fur seals (Arctocephalus pusillus pusillus) and the implications for dietary interpretation.

Analysis of the fatty acid (FA) composition of blubber is a valuable tool in interpreting the diet of marine mammals. This technique is based on the principle that particular FA present in prey can be incorporated largely untransformed into predator adipose tissue stores, thereby providing biochemical signatures with which to identify prey species. Several studies of phocid seals and cetaceans have documented vertical stratification in the FA composition of blubber such that inferences about diet may vary greatly depending on the layer of the blubber that is analysed. It is not known whether blubber in otariid seals (fur seals and sea lions) also displays vertical stratification in FA composition. Furthermore, it is not known whether the FA composition of blubber is uniform in these species. In the present study, the vertical and regional variation in FA composition of blubber was investigated in seven adult female Cape fur seals (Arctocephalus pusillus pusillus). The proportion of monounsaturated fatty acids (MUFA) was greater in the outer (43.6+/-1.3%) than inner portion (40.9+/-1.2%; t(20)=5.59, P<0.001) whereas the proportions were greater in the inner than outer portions for saturated fatty acids (23.6+/-0.5% and 21.9+/-0.6%, respectively, t(20) = 5.31, P<0.001) and polyunsaturated fatty acids (PUFA, 35.5+/-0.7% and 34.5+/-0.7%, respectively, t(20) = 3.81, P < 0.001). There was an inverse relationship between MUFA and PUFA in the blubber, independent of sampling location. In addition, with the exception of the inner portion from non-lactating females, blubber from the mammary area had the highest proportions of 18:1omega9c and total MUFA, followed by blubber from the rump and neck, suggesting that the deposition and mobilisation of blubber lipids may not be uniform around the body in otariid seals. These results support the need for blubber tissue to be sampled from the same site on animals, and to the full depth of the blubber layer, to minimise variation in FA profiles that could occur if different sites and depths were sampled. Such standardisation of sampling will further aid in interpreting diet in otariid seals using the FA Signature Analysis approach.

Characterisation of proteins in the milk of fur seals.

Milk protein composition was investigated throughout the lactation periods of the Australian fur seal (Arctocephalus pusillus doriferus) and Antarctic fur seal (Arctocephalus gazella). The mean protein content of the milk was found to be 10.9% and 10.6% respectively. The concentration of total protein did not change during lactation, although a decline in casein content of the milk in late lactation was apparent. Milk protein concentration during a foraging/suckling cycle of the Antarctic fur seal analysed at the time of arrival on shore, and 24 h and 72 h after arrival was 12.8%, 11.4% and 12.5% respectively. Re-feeding animals at 72 h resulted in a significant increase in milk protein content to 14.9%. Characterisation of milk protein by SDS-PAGE analysis revealed 5 casein and 10 major whey protein bands. Amino-terminal sequencing indicated that the majority of the whey fraction of the milk is beta-lactoglobulin (beta-LG). The limited amino acid sequence indicated 3 different beta-LGs were secreted in the milk. Subsequently, RT-PCR was used to extend the sequence of one of the beta-LGs and translation of the 464 bp fragment indicated that it shared 79% sequence identity with feline beta-LG II.

The comparative energetics and growth strategies of sympatric Antarctic and subantarctic fur seal pups at Iles Crozet.

The period of maternal dependence is a time during which mammalian infants must optimise both their growth and the development of behavioural skills in order to successfully meet the demands of independent living. The rate and duration of maternal provisioning, post-weaning food availability and climatic conditions are all factors likely to influence the growth strategies of infants. While numerous studies have documented differences in growth strategies at high taxonomic levels, few have investigated those of closely related species inhabiting similar environments. The present study examined the body composition, metabolism and indices of physiological development in pups of Antarctic fur seals (Arctocephalus gazella) and subantarctic fur seals (Arctocephalus tropicalis), congeneric species with different weaning ages (4 months and 10 months, respectively), during their overlap in lactation at a sympatric breeding site in the Iles Crozet. Body lipid reserves in pre-moult pups were significantly greater (t28=2.73, P<0.01) in subantarctic (26%) than Antarctic fur seals (22%). Antarctic fur seal pups, however, had significantly higher (t26=3.82, P<0.001) in-air resting metabolic rates (RMR; 17.1 +/- 0.6 ml O2 kg(-1) min(-1)) than subantarctic fur seal pups (14.1 +/- 0.5 ml O2 kg(-1) min(-1)). While in-water standard metabolic rate (SMR; 22.9 +/- 2.5 ml O2 kg(-1) min(-1)) was greater than in-air RMR for Antarctic fur seal pups (t9=2.59, P<0.03), there were no significant differences between in-air RMR and in-water SMR for subantarctic fur seal pups (t12=0.82, P>0.4), although this is unlikely to reflect a greater ability for pre-moult pups of the latter species to thermoregulate in water. Pup daily energy expenditure was also significantly greater (t27=2.36, P<0.03) in Antarctic fur seals (638 +/- 33 kJ kg(-1) day(-1)) than in subantarctic fur seals (533 +/- 33 kJ kg(-1) day(-1)), which corroborates observations that pups of the former species spend considerably more time actively learning to swim and dive. Consistent with this observation is the finding that blood oxygen storage capacity was significantly greater (t9=2.81, P<0.03) in Antarctic (11.5%) than subantarctic fur seal (8.9%) pups. These results suggest that, compared with subantarctic fur seals, Antarctic fur seal pups adopt a strategy of faster lean growth and physiological development, coupled with greater amounts of metabolically expensive behavioural activity, in order to acquire the necessary foraging skills in time for their younger weaning age.