Shannon L. Fowler, Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064, USA. E-mail: email@example.com
1Foraging 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.
2Time/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.
3Dive 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.
4Although 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.
5Juveniles 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.
In the marine environment, air-breathing vertebrates face a unique constraint – the separation between air at the surface and prey at depth. While many factors affect the availability of prey, position in the water column is an important variable relative to the rate of oxygen utilization and time available to search (Costa, Gales & Goebel 2001). Air-breathing marine predators generally exhibit three distinct foraging strategies: epipelagic, mesopelagic and benthic diving (Costa 1991; Gremillet et al. 1998; Tremblay & Cherel 2000; Costa et al. 2004).
The utilization of a particular foraging strategy may have demographic implications. Otariids that hunt on the benthos spend > 40% of their time at sea diving compared to < 30% for epipelagic foragers (Costa et al. 2004). Costa & Gales (2003) postulated that increased foraging effort may explain why many pinnipeds and penguins that feed benthically have stable or declining populations, while the majority of epipelagic divers are experiencing substantial population growth. One of the rarest pinnipeds is the benthic-feeding Australian sea lion (Neophoca cinerea Péron 1816), with a stable or declining population (Gales, Shaughnessy & Dennis 1994; Gales, Haberley & Collins 2000). Meanwhile, sympatric epipelagic-foraging New Zealand fur seals (Arctocephalus forsteri) have an exponentially increasing population (Shaughnessy et al. 1994; Gales et al. 2000).
The Australian sea lion demonstrates a unique non-annual, non-synchronous breeding season (Gales et al. 1994; Gales & Costa 1997). Pups are suckled for approximately 17·6 months, one of the longest lactation periods in pinnipeds (Higgins 1993; Higgins & Gass 1993). This reproductive strategy may have evolved as an adaptation to a stable marine environment where resources are limited and show little seasonal fluctuation (Rochford 1980; Pearce 1991; Gales et al. 1994; Gales & Costa 1997). Our study addresses the hypothesis that extended dependency allows pups time to develop the demanding benthic foraging skills required in their environment. Specifically, we wanted to determine if young Australian sea lions are capable of adult benthic diving or if, as in many species, pups and juveniles utilize alternative foraging strategies.
Materials and methods
Fieldwork was conducted between June 2001 and August 2003 at Seal Bay Conservation Park, Kangaroo Island, South Australia (35°41′ S, 136°53′ E). Three-quarters of the Australian sea lion population resides in South Australia and Seal Bay contains the third largest colony (Gales et al. 1994).
establishing a known-aged cohort
Censuses of the colony were carried out twice per day and newborns were identified by direct observation of births or presence of fresh afterbirth. Once the mother left for her first foraging trip after 7–10 days, pups were marked with bleach, sexed and weighed. Fifty-five pups (28 males and 27 females) from a single cohort were identified and marked over a 5-month period in 2001.
Before the first moult at approximately 4 months of age, bleach-marked pups were recaptured and tagged on the trailing edge of each foreflipper (Leader Products Pty Ltd, Melbourne, VIC, Australia). Pups and adult females were injected in the gluteal region with a subcutaneous passive microtransponder (Destron Fearing Corporation, South St Paul, MN, USA) to ensure that individuals were sampled once during the study.
Mothers were identified when they were observed suckling tagged pups. Mother/pup pairs were captured simultaneously using specially designed hoop nets (Fuhrman Diversified, Seabrook, TX, USA). The general anaesthetic gas Isoflurane was delivered, with medical oxygen, from a field portable machine (Gales & Mattlin 1998). Individuals were weighed using a hanging electronic balance (± 0·1 kg; Dyna-Link MSI-7200, Measurement Systems International, Seattle, WA, USA) and a tripod.
Mothers and their pups were captured during three different field seasons: 6-month-old pups (March 2002), 15-month-old pups (November 2002) and 23-month-old juveniles (July 2003). Ten mother/pup pairs were captured each season for a total of 60 different animals over the entire study. Two 15-month-old pups and five 23-month-old juveniles were never observed suckling during the season, so these individuals were captured alone and adult females suckling young pups were captured in place of their mothers. The remaining 23-month-old juveniles were observed suckling at least once during the season, despite the fact that average weaning occurs at 17·6 months. In July 2003, only six known-age juveniles (that had not been sampled during previous seasons) could be located. Therefore, age was estimated for the others using pelage condition and growth curves constructed from data on mass and standard length (Higgins 1990; this study). In addition, one independent juvenile from the previous cohort (aged approximately 3 years) was captured and sampled in July 2003.
All animals were equipped with electronic time/depth recorders (TDR) to measure diving behaviour. Wildlife Computers (Redmond, WA, USA) mark 5, 6 or 8 TDRs were deployed on adult females and mark 5 or 9 TDRs were deployed on pups and juveniles. Devices were secured with epoxy to a neoprene patch the size of the instrument's base (polystrate 5 min epoxy, Devcon, Danvers, MA, USA). The neoprene was attached to a larger foot of netting using cable ties and glued to the dorsal pelage with epoxy. The TDRs were programmed to sample water depth and temperature every 2 or 4 s while the animals were in the water.
To aid in relocation, VHF transmitters were attached in the same manner (Sirtrack Ltd, Havelock, New Zealand). Transmitters were detected by a hand-held receiver (Telonics, Mesa, AZ, USA) and recaptures occurred after 4–15 days.
Data were downloaded and decoded using Wildlife Computers software (hex convert 1·0·0). A custom-built software package programmed in labview 4 (National Instruments, Austin, TX, USA) was used for zero-offset correction, analyses and graphical presentation (Arnould & Hindell 2001).
A dive was defined by a minimum depth of 4 m. Bottom time was determined by inflection points (from descent to flat and flat to ascent) in the deepest 20 m of each dive in which more than 5% of total dive time was spent. Foraging efficiency (FE) was calculated by dividing bottom time by total dive cycle time (dive duration + post-dive surface interval: Ydenberg & Clark 1989). Surface intervals were defined as the time between the first 0 m reading after a dive and the last 0 m reading before the next dive. Time at sea was calculated from the time the animal entered the water until it hauled out. A foraging trip was characterized by almost continuous diving, with very few surface intervals exceeding 30 min. Costa & Gales (2003) defined the percentage of time diving as the proportion of time at sea spent at depths = 6 m. For the purpose of comparison, we used the same criteria for this calculation. Mean and maximum values were determined per animal and averaged across age classes.
Dive records were recovered from nine 6-month-old pups, seven 15-month-old pups, nine 23-month-old juveniles, one 3-year-old and 25 adult females. The mean (± SE) deployment period for 6-month-old pups in March 2002 was 11·8 ± 0·6 days, with 81 ± 19 mean dives recorded per animal. In November 2002, 15-month-old pups had a mean deployment of 9·2 ± 0·5 days, with 1158 ± 113 mean dives per animal. Mean deployment for 23-month-old juveniles was 7·0 ± 0·7 days, with 696 ± 101 mean dives. For the 3-year old, 970 dives were recorded over 6·2 days. Adult females had a mean deployment period of 10·0 ± 0·7 days, with 1110 ± 125 mean dives over three field seasons. There were no significant differences between sexes within age classes; these data were combined (t-test, t6 = −0·60, P = 0·57). Mean water temperatures recorded by the instruments attached to adult females were 18·5 °C in March 2002, 20·6 °C in November 2002 and 16·4 °C in July 2003. Dive behaviours for females were similar to published records (Costa et al. 2001; Costa & Gales 2003).
Six-month-old pups demonstrated minimal diving activity, exhibiting the shallowest dive depths, shortest dive durations and spending the vast majority of time onshore. By 15 months pups were diving deeper, diving for longer durations and taking short foraging trips. Twenty-three-month-old juveniles achieved even deeper depths, longer durations and longer foraging trips. However, even by 23 months of age juveniles were still not exhibiting the depths, dive durations or foraging trip durations typical of adult females (Fig. 1). There was no diel pattern in dive records from any age class.
Maximum dive depths and durations are likely to reflect the absolute abilities of animals at different ages better than other parameters and these increased throughout development (Table 1). Maximum depth and duration were significantly different across age classes (depth: one-way anova, F3,37 = 41·63, P < 0·001; duration: Kruskal–Wallis non-parametric anova, H3 = 12·82, P = 0·01), except between 15 and 23 months (depth: Tukey's test, P = 0·23; duration: Dunn's post-hoc test, P = 0·79). Mean depth and duration also increased significantly with age (depth: F3,37 = 44·38, P < 0·001; duration: F3,37 = 38·97, P < 0·001), except between 15 and 23 months (depth: P = 0·54; duration: P = 0·13). The 3-year-old juvenile demonstrated dive behaviour that was more advanced than animals at 23 months, but still below adult levels.
Table 1. Summary of dive data for different age classes of Australian sea lions. Values are presented as means ± SE. *Values that are significantly different from adult values. The range of individual ages is reported in parentheses below the mean values. Age was estimated for the 3-year-old based on growth curves for this species (Higgins 1990; this study). Maximum and mean depth, maximum and mean duration and maximum bottom time all increased significantly throughout development (max. depth: F3,37 = 41·63, P < 0·001; mean depth: F3,37 = 44·38, P < 0·001; max. duration: H3 = 12·82, P = 0·005; mean duration: F3,37 = 38·97, P < 0·001; max. bottom time: H3 = 15·27, P = 0·002)
Younger age classes concentrated larger percentages of their diving in shallower depths (Fig. 2). Adult females dived most frequently to 81–90 m: 6-month-old pups never reached these depths, 15-month-old pups dived to these depths on 1% of dives and 23-month-old juveniles reached these depths on only 8% of dives.
Adult females had significantly higher maximum bottom times than younger animals (H3 = 15·27, P = 0·002; Table 1). However, mean bottom times were not significantly different between 15-month-old pups, 23-month-old juveniles and adults (F2,31 = 2·21, P = 0·13; Fig. 3). By spending a larger proportion of each dive and total time at sea on the bottom than adults (Fig. 4), 15- and 23-month-old sea lions demonstrated higher FE at shallow depths (Fig. 5). There was no significant correlation between depth and FE for 6-month-old pups (Pearson's product–moment correlation, R = 0·99, P = 0·08). Depth and FE were correlated positively for 15- and 23-month-old animals up to 40 m (15: R = 0·96, P = 0·04; 23: R = 0·97, P = 0·03), but correlated negatively beyond 40 m (15: R = −0·98, P = 0·01; 23: R = −0.096, P = 0·01). For adult females, depth and FE were correlated positively across all depths (R = 0·63, P = 0·002).
The mean surface interval for 6-month-old pups was 12·95 ± 3·73 min, compared to 1·36 ± 0·17 min at 15-month-old pups, 1·37 ± 0·18 min at 23-month-old pups and 2·58 ± 0·15 min for females. Adult mean surface intervals were significantly greater than mean surface intervals for 15- and 23-month-old sea lions (H3 = 21·32, P < 0·001). Dive duration and post-dive surface interval were correlated inversely in 6-month-old pups (R = –0·09, P = 0·03), 15-month-old pups (R = –0·07, P < 0·001) and 23-month-old juveniles (R = –0·04, P = 0·001), but there was no correlation in adult females (R = –0·01, P = 0·44).
Six-month-old pups spent the least amount of time at sea (mean = 10·3 ± 4·8%), while adult females spent the greatest (mean = 49·3 ± 4·0%). Fifteen-month-old pups spent 39·9 ± 2·6% of time at sea, 23-month-old juveniles spent 27·8 ± 2·6% and the 3-year-old spent 47%.
Six-month-old pups also demonstrated the lowest rates of diving (dives h−1, percentage of time diving). However, 15- and 23-month-old sea lions dived more frequently and spent a higher percentage of time at sea diving than adults (Fig. 6).
Instead of adopting a distinctly different foraging strategy, young Australian sea lions appear to develop adult benthic diving skills slowly. Although young sea lions did not achieve adult depths or durations, dive records for 15-month-old pups and 23-month-old juveniles indicate benthic foraging. Young sea lions dived to consecutively similar depths (with no deeper dives within a series, suggesting that the sea floor limited depth), demonstrated no diurnal pattern and maximized bottom time. Because the local maritime environment surrounding Kangaroo Island consists of relatively shallow on-shelf waters (marine chart AUS 346 dated 1997, Australian Hydrographic Office, Wollongong, New South Wales, Australia) pups and juveniles were able to dive and forage benthically, but at shallower depths than adults.
ontogeny of diving behaviours
Results support the hypothesis that extended dependency in Australian sea lions is necessary to allow pups time to develop the diving skills required to forage benthically in their environment (Gales et al. 1994; Gales & Costa 1997; Costa & Gales 2003). In typical otariids pups wean at 10–12 months, but Australian sea lion females normally suckle their pups for 17·6 months (Higgins 1993). Fifteen-month-old Australian sea lions reached a mean depth that was 56% of adult mean depth. The mean depth for 23-month-old juveniles had increased to only 62% of adult mean depth, although colder water temperatures may have partially constrained dive behaviour. A 3-year-old (1·5 years after assumed weaning) achieved a mean dive depth that was 79% of adult mean depth. Developing adult foraging patterns, instead of utilizing alternative techniques, may be a factor in the delayed weaning of Australian sea lions, as has been found in other species (Yoerg 1998).
The Galápagos fur seal (Arctocephalus galapagoensis) also has an extended period of diving development and is, in fact, the only pinniped with a typical dependency interval longer than Australian sea lions (Trillmich 1986). The Galápagos fur seal is also the smallest pinniped, so although it forages epipelagically (Gentry et al. 1986), it must deal with the constraints of smaller body size on diving ability. The youngest Galápagos fur seals that were weaned successfully were 2 years old; at weaning, they were still not capable of adult dive performance (Horning & Trillmich 1997a). Interestingly, both Galápagos fur seals and Australian sea lions show a similar progression of diving behaviours, although Australian sea lions appear to develop slightly faster and wean earlier (Fig. 7).
This prolonged development is in contrast to other otariids, where pups forage epipelagically and are weaned at a younger age. Antarctic fur seals (Arctocephalus gazella) develop epipelagic diving skills early. By the time they are weaned at 4 months, Antarctic fur seal pups have the diving ability to exploit prey similar to those taken by adults (McCafferty, Boyd & Taylor 1998). Baker & Donohue (2000) found that at weaning, 4-month-old northern fur seal (Callorhinus ursinus) pups began abruptly diving deeper and switching to the nocturnal epipelagic foraging patterns typical of adults. Steller sea lions (Eumetopias jubatus) also showed a change in epipelagic dive characteristics that coincided with the assumed onset of weaning at 11–12 months (Loughlin et al. 2003). Steller yearlings were found to be capable of adult dive behaviour (Loughlin et al. 2003).
However, as air-breathing predators feeding in the marine environment pups must develop adequate diving skills to forage successfully. In all otariids studied to date, species that develop these skills earlier are weaned at a younger age.
An important component of the Australian sea lion's benthic foraging strategy is to maintain bottom time independent of depth. In contrast to epipelagic divers, foraging does not occur in transit to and from the surface, so foraging success is dependent upon bottom time. Adults maintain bottom time by increasing dive duration as the animal forages deeper and not extending surface intervals, even when approaching maximum durations (Costa & Gales 2003). Fifteen- and 23-month-old sea lions not only maintained bottom time by using these approaches, but maximized bottom time to a greater extent (Fig. 4).
By spending more time at sea diving, immature sea lions spent a higher proportion of total time at sea on or near the bottom. Although adults may have to travel further to reach foraging grounds, dive records indicate almost continuous benthic diving from the moment females leave the colony (Costa & Gales 2003; this study). Therefore, lower dive rates of adult females were not the result of longer travel times but due to longer surface intervals.
Young sea lions were also able to spend a larger proportion of each dive on the bottom due to the shorter transit times required when diving to shallower depths. Given that breath-hold durations are limited by physiological capabilities, pups can either increase depth while decreasing bottom time or decrease depth to maintain bottom time. The results of the present study suggest that immature Australian sea lions sacrificed depth for bottom time (Fig. 3).
By reducing surface intervals and dive depth, pups and juveniles were able to increase FE. Although FE was higher at 15 and 23 months, these results do not mean that pups and juveniles were more capable foragers than adults. On the contrary, young sea lions most probably had to maximize bottom time to a greater extent due to inexperience and undeveloped hunting skills. Additionally, FE defines an animal's ability to exploit the environment at depth and only adults appeared capable of exploiting depths over 100 m (Fig. 5). Young sea lions may avoid deeper depths because they cannot afford the costs of lower FE.
The Australian sea lion population is currently estimated to be approximately 10 000 and is thought to be stable or decreasing (Gales et al. 1994). As a result of small population size, exposure to human activities and evidence of population declines in some areas, it was listed recently as threatened under Australian legislation (Environmental Protection and Biodiversity Conservation Act 1999, Commonwealth of Australia). The Australian sea lion's range overlaps with that of the New Zealand fur seal and both species have colonies on Kangaroo Island. Australian sea lions and New Zealand fur seals were hunted during the commercial sealing era and there is evidence that both species were once considerably more abundant and widespread (Gales et al. 1994; Shaughnessy et al. 1994). However, the New Zealand fur seal population is currently estimated to be more than 85 000 and has been increasing exponentially for at least three decades (Shaughnessy et al. 1994).
Unlike the Australian sea lion, dive records for New Zealand fur seal adult females indicate predominantly epipelagic foraging (Harcourt et al. 1995). In areas without high productivity, larger body size may make epipelagic feeding on small prey unviable for adult Australian sea lions, as manoeuvrability is inversely proportional to body length (Fish, Hurley & Costa 2003). It should, however, be a feasible option for smaller pups and juveniles. Fifteen-month-old Australian sea lion pups, which are similar in size to adult female New Zealand fur seals, demonstrated longer mean dive durations (3·2 ± 0·2 min: this study vs. 1·4 ± 1·1 min in New Zealand: Mattlin, Gales & Costa 1998), which would indicate that they are capable of similar foraging behaviour. However, despite the apparent success of the New Zealand fur seal foraging strategy and the potential benefit of reduced competition with older conspecifics, young Australian sea lions seem to be hardwired to forage benthically. A lack of plasticity in the foraging behaviours of Australian sea lions could be one factor contributing to current population dynamics.
One limitation of benthic foraging is restricted available foraging habitat due to the finite extent of the continental shelf. This limitation is even more severe for pups that cannot or do not reach adult foraging depths, such as young Australian sea lions. As sea floor depth gradually increases with distance from shore, shallow dives are conducted in near-shore waters closer to the colony, which are more likely to become depleted of prey (‘Ashmole's halo’: Ashmole 1963). If juveniles are not capable of diving deeper, young sea lions may not be able to expand foraging grounds in response to reductions in prey.
Given that Australian sea lion adults operate at or near their physiological maximum (Costa & Gales 2003) and juveniles have reduced diving abilities, young sea lions may be limited in their capacity to increase dive depth, duration or foraging effort. Juvenile Australian sea lions would therefore be particularly vulnerable to resource limitation. Indeed, high mortality rates in young Galápagos fur seals during periods of food scarcity, such as El Niño events, are believed to result from lower juvenile diving abilities (Trillmich & Dellinger 1991; Horning & Trillmich 1997a).
Despite the apparent costs a number of otariids forage benthically, including southern sea lions (Otaria flavenscens: Werner & Campagna 1995), New Zealand sea lions (Phocarctos hookeri: Gales & Mattlin 1997; Costa & Gales 2000) and Australian fur seals (Arctocephalus pusillus doriferus: Arnould & Hindell 2001). Benthic foraging may be advantageous because benthic prey are less influenced by seasonal fluctuations and oceanographic perturbations than epipelagic prey (Miller & Sydeman 2004). However, benthic foragers are particularly sensitive to human-induced disturbances and recently modified environments may suddenly become unsuitable. For example, demersal and benthic fishery trawls disrupt the habitat and remove the larger size classes of prey benthic foragers depend on (Thrush et al. 1998). Juveniles restricted to shallower near-shore waters are even more likely to be impacted by commercial and recreational fisheries. Recent environmental modifications, anthropogenic reductions in benthic prey and fisheries interactions could be impacting seriously juvenile survival and recruitment. These issues should be taken into consideration for conservation and management of benthic foragers and may be an important factor as to why many of these populations are currently at risk.
This work was supported by UC MEXUS, NSF WISC, JEB Travelling Fellowship, ONR (no. N00014-02-1-1012-005), Wildlife Computers, National Geographic Society, Myers Oceanographic and Marine Biology Trust, American Museum of Natural History Lerner Grey Fund, American Cetacean Society, Friends of Long Marine Laboratory, Project AWARE, Sigma Xi, Sealink, Clairol and South Australia National Parks and Wildlife. The following people provided invaluable field assistance: Seal Bay Conservation Park staff, D. Higgins, N. Rourke, D. Needham, Melbourne Zoo (S. Blanchard, G. McDonald), Z. Boland, C. Farber, J. Gibbens, A. Martinez, H. Mostman, S. Sataar, S. Simmons, Y. Tremblay and M. Weise. J. Estes, H. Fowler, K. J. Fowler, G. Kooyman and the Costa laboratory group provided helpful comments on drafts. Research was carried out under South Australian Department for Environment and Heritage permit no. G24475-2 and Wildlife Ethics Committee permit no. 4/2001. Protocols were approved by the Prevention of Cruelty to Animals Act 1985 and the Chancellor's Animal Research Committee (no. Cost01·01).