Ontogeny of oxygen stores and physiological diving capability in Australian sea lions

1.For air-breathing animals in aquatic environments, foraging behaviours are often constrained by physiological capability. The development of oxygen stores and the rate at which these stores are used determine juvenile diving and foraging potential.
2. We examined the ontogeny of dive physiology in the threatened Australian sea lion Neophoca cinerea. Australian sea lions exploit benthic habitats; adult females demonstrate high field metabolic rates (FMR), maximize time spent near the benthos, and regularly exceed their calculated aerobic dive limit (cADL). Given larger animals have disproportionately greater diving capabilities; we wanted to determine the extent physiological development constrained diving and foraging in young sea lions.
3. Ten different mother/pup pairs were measured at three developmental stages (6, 15 and 23 months) at Seal Bay Conservation Park, Kangaroo Island, South Australia. Hematocrit (Hct), haemoglobin (Hb) and plasma volume were analyzed to calculate blood O2 stores and myoglobin was measured to determine muscle O₂. Additionally, FMR's for nine of the juveniles were derived from doubly-labelled water measurements.
4. Australian sea lions have the slowest documented O₂ store development among diving mammals. Although weaning typically occurs by 17·6 months, 23-month juveniles had only developed 68% of adult blood O₂. Muscle O₂ was the slowest to develop and was 60% of adult values at 23 months.
5. We divided available O₂ stores (37·11 ± 1·49 mL O₂ kg−1) by at-sea FMR (15·78 ± 1·29 mL O₂ min−1 kg−1) to determine a cADL of 2·33 ± 0·24 min for juvenile Australian sea lions. Like adults, young sea lions regularly exceeded cADL's with 67·8 ± 2·8% of dives over theoretical limits and a mean dive duration to cADL ratio of 1·23 ± 0·10.
6. Both dive depth and duration appear impacted by the slow development of oxygen stores. For species that operate close to, or indeed above their estimated physiological maximum, the capacity to increase dive depth, duration or foraging effort would be limited. Due to reduced access to benthic habitat and restricted behavioural options, young benthic foragers, such as Australian sea lions, would be particularly vulnerable to resource limitation.

Validating the relationship between 3-dimensional body acceleration and oxygen consumption in trained Steller sea lions

We tested the ability of overall dynamic body acceleration (ODBA) to predict the rate of oxygen consumption ([Formula: see text]) in freely diving Steller sea lions (Eumetopias jubatus) while resting at the surface and diving. The trained sea lions executed three dive types-single dives, bouts of multiple long dives with 4-6 dives per bout, or bouts of multiple short dives with 10-12 dives per bout-to depths of 40 m, resulting in a range of activity and oxygen consumption levels. Average metabolic rate (AMR) over the dive cycle or dive bout calculated was calculated from [Formula: see text]. We found that ODBA could statistically predict AMR when data from all dive types were combined, but that dive type was a significant model factor. However, there were no significant linear relationships between AMR and ODBA when data for each dive type were analyzed separately. The potential relationships between AMR and ODBA were not improved by including dive duration, food consumed, proportion of dive cycle spent submerged, or number of dives per bout. It is not clear whether the lack of predictive power within dive type was due to low statistical power, or whether it reflected a true absence of a relationship between ODBA and AMR. The average percent error for predicting AMR from ODBA was 7-11 %, and standard error of the estimated AMR was 5-32 %. Overall, the extensive range of dive behaviors and physiological conditions we tested indicated that ODBA was not suitable for estimating AMR in the field due to considerable error and the inconclusive effects of dive type.

Ontogeny of diving behaviour in the Australian sea lion: trials of adolescence in a late bloomer

1.Foraging behaviours of the Australian sea lion (Neophoca cinerea) reflect an animal working hard to exploit benthic habitats. Lactating females demonstrate almost continuous diving, maximize bottom time, exhibit elevated field metabolism and frequently exceed their calculated aerobic dive limit. Given that larger animals have disproportionately greater diving capabilities, we wanted to examine how pups and juveniles forage successfully.
2.Time/depth recorders were deployed on pups, juveniles and adult females at Seal Bay Conservation Park, Kangaroo Island, South Australia. Ten different mother/pup pairs were equipped at three stages of development (6, 15 and 23 months) to record the diving behaviours of 51 (nine instruments failed) animals.
3. Dive depth and duration increased with age. However, development was slow. At 6 months, pups demonstrated minimal diving activity and the mean depth for 23-month-old juveniles was only 44 ± 4 m, or 62% of adult mean depth.
4. Although pups and juveniles did not reach adult depths or durations, dive records for young sea lions indicate benthic diving with mean bottom times (2·0 ± 0·2 min) similar to those of females (2·1 ± 0·2 min). This was accomplished by spending higher proportions of each dive and total time at sea on or near the bottom than adults. Immature sea lions also spent a higher percentage of time at sea diving.
5. Juveniles may have to work harder because they are weaned before reaching full diving capability. For benthic foragers, reduced diving ability limits available foraging habitat. Furthermore, as juveniles appear to operate close to their physiological maximum, they would have a difficult time increasing foraging effort in response to reductions in prey. Although benthic prey are less influenced by seasonal fluctuations and oceanographic perturbations than epipelagic prey, demersal fishery trawls may impact juvenile survival by disrupting habitat and removing larger size classes of prey. These issues may be an important factor as to why the Australian sea lion population is currently at risk.

Ontogeny of movements and foraging ranges in the Australian sea lion

This study tracked the movements of Australian sea lion (Neophoca cinerea) pups, juveniles, and adult females to identify home ranges and determine if young sea lions accompanied their mothers at sea. Satellite tags were deployed on nine 15- mo-old pups, nine 23-mo-old juveniles, and twenty-nine adult female Australian sea lions at Seal Bay Conservation Park, Kangaroo Island, South Australia. Females did not travel with their offspring at sea, suggesting young Australian sea lions learn foraging behaviors independently. Although home ranges increased with age,  23-mo-old juveniles had not developed adult movement capacity and their range was only 40.6% of the adult range. Juveniles traveled shorter distances (34.8 ± 5.5 km) at slower speeds (2.0 ± 0.3 km/h) than adults (67.9 ± 3.5 km and 3.9 ± 0.3 km/h). Young sea lions also stayed in shallower waters; sea floor depths of mean locations were 48±7m for juveniles and 74±2m for females. Restricted to shallow coastal waters, pups and juveniles are more likely to be disproportionately impacted by human activities. With limited available foraging habitat, young Australian sea lions appear particularly vulnerable to environmental alterations resulting from fisheries or climate change.

Accuracy of ARGOS locations of pinnipeds at-sea estimated using Fastloc GPS

Background: ARGOS satellite telemetry is one of the most widely used methods to track the movements of free-ranging marine and terrestrial animals and is fundamental to studies of foraging ecology, migratory behavior and habitat-use. ARGOS location estimates do not include complete error estimations, and for many marine organisms, the most commonly acquired locations (Location Class 0, A, B, or Z) are provided with no declared error estimate.
Methodology/Principal Findings: We compared the accuracy of ARGOS locations to those obtained using Fastloc GPS from the same electronic tags on five species of pinnipeds: 9 California sea lions (Zalophus californianus), 4 Galapagos sea lions (Zalophus wollebaeki), 6 Cape fur seals (Arctocephalus pusillus pusillus), 3 Australian fur seals (A. p. doriferus) and 5 northern elephant seals (Mirounga angustirostris). These species encompass a range of marine habitats (highly pelagic vs coastal), diving behaviors (mean dive durations 2–21 min) and range of latitudes (equator to temperate). A total of 7,318 ARGOS positions and 27,046 GPS positions were collected. Of these, 1,105 ARGOS positions were obtained within five minutes of a GPS position and were used for comparison. The 68^th percentile ARGOS location errors as measured in this study were LC-3
0.49 km, LC-2 1.01 km, LC-1 1.20 km, LC-0 4.18 km, LC-A 6.19 km, LC-B 10.28 km.
Conclusions/Significance: The ARGOS errors measured here are greater than those provided by ARGOS, but within the range of other studies. The error was non-normally distributed with each LC highly right-skewed. Locations of species that make short duration dives and spend extended periods on the surface (sea lions and fur seals) had less error than species like elephant seals that spend more time underwater and have shorter surface intervals. Supplemental data (S1) are provided allowing the creation of density distributions that can be used in a variety of filtering algorithms to improve the quality of ARGOS tracking data.

Assessing the use of milk fatty acids to infer the diet of the Australian sea lion (Neophoca cinerea)

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 ± 4.8 m) and ‘offshore’ regions characterised by comparatively deep bathymetry (60.5 ± 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 ± 1.2% compared with 16.5 ± 1.9% respectively), 20 : 4n-6 (6.1 ± 0.7 compared with 2.5 ± 0.7 respectively) and 22 : 4n-6 (2.4 ± 0.2% compared with 0.8 ± 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.

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.

Regional variability in diving physiology and behavior in a widely distributed air-breathing marine predator, the South American sea lion Otaria byronia

Our understanding of how air-breathing marine predators cope with environmental variability is limited by our inadequate knowledge of their ecological and physiological parameters. Due to their wide distribution along both coasts of the sub-continent, South American sea lions (Otaria byronia) provide a valuable opportunity to study the behavioral and physiological plasticity of a marine predator in different environments. We measured the oxygen stores and diving behavior of South American sea lions throughout most of its range, allowing us to demonstrate that diving ability and behavior vary across its range. We found no significant differences in mass-specific blood volumes of sea lions among field sites and a negative relationship between mass-specific oxygen storage and size, which suggests that exposure to different habitats and geographical locations better explains oxygen storage capacities and diving capability in South American sea lions than body size alone. The largest animals in our study (individuals from Uruguay) were the most shallow and short duration divers, and had the lowest mass-specific total body oxygen stores, while the deepest and longest duration divers (individuals from Southern Chile) had significantly larger mass-specific oxygen stores, despite being much smaller animals.Our study suggests that the physiology of air-breathing diving predators is not fixed, but that it can be adjusted, to a certain extent, depending on the ecological setting and or habitat. These adjustments can be thought of as a "training effect" as the animal continues to push its physiological capacity through greater hypoxic exposure, its breath holding capacity increases.

Sexual segregation in habitat use is smaller than expected in a highly dimorphic marine predator, the southern sea lion

Sexual segregation in habitat use is widely reported in many taxa and can profoundly influence the distribution and behaviour of animals. However, our knowledge of the mechanisms driving sexual segregation is still in its infancy (particularly in marine taxa) and the influence of extrinsic factors in mediating the expression of sex differences in foraging behaviour is underdeveloped. Here, we combine data from biologging tags, with stable isotope analysis of vibrissae, to assess sexual segregation in southern sea lions (SSL) (Otaria flavescens) breeding at the Falkland Islands in the South Atlantic. We found evidence to support segregation, most notably in δ13C and δ15N values. However, in spite of extreme sexual size dimorphism and differing constraints related to female-only parental care, adult male and adult female SSL overlapped considerably in isotopic niches and foraging area, and shared similar foraging trip characteristics (such as distance and duration). This is in contrast to SSL breeding in Argentina, where prior studies report sexual differences in foraging locations and foraging trip characteristics. We posit that sexual segregation in SSL is influenced by habitat availability (defined here as the width of the Patagonian Shelf) and individual foraging preferences, rather than commonly invoked individual-based limiting factors per se.

Variation in the fatty acid composition of the 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%; t20=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, t20 = 5.31, P<0.001) and polyunsaturated fatty acids (PUFA, 35.5±0.7% and 34.5±0.7%, respectively, t20 = 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 18:1ω9c 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.

Evolution of Pinnipedia lactation strategies: a potential role for α-lactalbumin?

Despite the considerable variation in milk composition found among mammals, a constituent common across all groups is lactose, the main sugar and osmole in most eutherians milk. Exceptions to this are the families Otariidae (fur seals and sea lions) and Odobenidae (walruses), where lactose has not been detected. We investigated the molecular basis for this by cloning α-lactalbumin, the modifier protein of the lactose synthase complex. A mutation was observed which, in addition to preventing lactose production, may enable otariids to maintain lactation despite the extremely long inter-suckling intervals during the mother's time at sea foraging (more than 23 days in some species).

Effect of proximity to the shelf edge on the diet of female Australian fur seals

The Australian fur seal Arctocephalus pusillus doriferus is a temperate latitude species with a breeding distribution restricted to Bass Strait, Australia. Recent studies of the foraging behaviour of female Australian fur seals indicated that they feed demersally in the shallow continental shelf waters, a behaviour that is in contrast to the epipelagic foraging of females of most other arctocephaline (Southern Hemisphere fur seals) species and akin to that observed in sea lions. These studies, however, were conducted at one colony (Kanowna Island) located in central northern Bass Strait, and it was suggested that the observed foraging behaviour may have been due to the distance of this colony from the continental shelf edge (180 km), making it inefficient to forage beyond it. Here, the diet of lactating Australian fur seals was compared between 2 colonies to test if differing proximity to the continental shelf edge resulted in differences in foraging behaviour. The 2 breeding colonies studied, Kanowna Island and The Skerries, were 180 and 25 km from the nearest shelf edge, respectively. We analysed a total of 917 scat samples collected at the 2 colonies between 1997 and 2001. From faecal analysis, 45 primarily demersal on-shelf species of fishes and cephalopods were identified. Only 4 species had a frequency of occurrence greater than 10%: redbait Emmelichthys nitidus, jack mackerel Trachurus sp., red rock cod Pseudophycis bachus, and Gould’s squid Nototodarus gouldi. No seasonal, annual or spatial differences were found between the 2 colonies, indicating that proximity to the shelf edge does not influence diet.

Individual variation in the pup attraction call produced by female Australian fur seals during early lactation

Otariid seals (fur seals and sea lions) are colonial breeders with large numbers of females giving birth on land during a synchronous breeding period. Once pups are born, females alternate between feeding their young ashore and foraging at sea. Upon return, both mother and pup must relocate each other and it is thought to be primarily facilitated by vocal recognition. Vocalizations of thirteen female Australian fur seals (Arctocephalus pusillus doriferus) were recorded during the breeding seasons of December 2000 and 2001, when pups are aged from newborns to one month. The pup attraction call was examined to determine whether females produce individually distinct calls which could be used by pups as a basis for vocal recognition. Potential for individual coding, discriminant function analysis (DFA), and classification and regression tree analysis were used to determine which call features were important in separating individuals. Using the results from all three analyses: F0, MIN F and DUR were considered important in separating individuals. In 76% of cases, the PAC was classified to the correct caller, using DFA, suggesting that there is sufficient stereotypy within individual calls, and sufficient variation between them, to enable vocal recognition by pups of this species.