Journal of Animal Blackwell Publishing Ltd Ecology 2006 Ontogeny of diving behaviour in the Australian sea lion: 75, 358–367 trials of adolescence in a late bloomer

SHANNON L. FOWLER*, DANIEL P. COSTA*, JOHN P. Y. ARNOULD†, NICHOLAS J. GALES‡ and CAREY E. KUHN* *Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064, USA; †School of Life and Environmental Sciences Deakin University, Burwood, VIC 3125, Australia; and ‡Australian Antarctic Division, Channel Highway, Kingston, Tasmania 7001, Australia

Summary 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. Imma- ture 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. Key-words: benthic diving, foraging ecology, Neophoca cinerea, postnatal development, weaning. Journal of Animal Ecology (2006) 75, 358–367 doi: 10.1111/j.1365-2656.2006.01055.x

(Magrath & Lill 1985; Diamond & Bond 1991; Lima & Introduction Moreira 1993; Doroff & DeGange 1994). Juveniles may The acquisition of adult foraging behaviour can follow have different dietary requirements (Sullivan 1988), a variety of paths. In many vertebrates, juveniles utilize insufficient physiological capability (Rolseth, Koehler different foraging techniques from conspecific adults & Barclay 1994; Ponganis et al. 1999; Irvine et al. 2000), incompatible mouthparts for adult prey (Castro & © 2006 The Authors. Journal compilation Correspondence: Shannon L. Fowler, Department of Ecology Hernandezgarcia 1995; Maurer 1996), inadequate © 2006 British and Evolutionary Biology, University of California, Santa experience and associated learning (Heinsohn 1991; Ecological Society Cruz, CA 95064, USA. E-mail: [email protected] Hauser 1993; Bard 1995; Langen 1996) or may be

359 avoiding competition with adults (Milinski & Parker or near its physiological maximum (Costa et al. 2001; Ontogeny of diving 1991). Adult strategies are not necessarily a prerequi- Costa & Gales 2003). Many air-breathing vertebrates in Australian sea site for self-sufficiency and in some cases mastering dive within their limit of estimated oxygen stores lions them may even delay independence (Yoerg 1998). (Kooyman et al. 1980; Dolphin 1988; Kooyman 1989; In the marine environment, air-breathing vertebrates Butler & Jones 1997), but the Australian sea lion exceeds face a unique constraint – the separation between air this limit (calculated aerobic dive limit) on 79% of dives at the surface and prey at depth. While many factors (Costa et al. 2001). Australian sea lions spend 58% of time affect the availability of prey, position in the water at sea diving and demonstrate high field metabolism column is an important variable relative to the rate of (Costa & Gales 2003). To exploit benthic habitats, oxygen utilization and time available to search (Costa, adult females spend 61% of each dive and 35% of total Gales & Goebel 2001). Air-breathing marine predators time at sea on or near the bottom (Costa & Gales 2003). generally exhibit three distinct foraging strategies: Given the extreme diving behaviour of adult Australian epipelagic, mesopelagic and benthic diving (Costa 1991; sea lions, we wanted to examine how pups and juveniles Gremillet et al. 1998; Tremblay & Cherel 2000; Costa forage successfully. Previous studies have shown that et al. 2004). young marine mammals are born with minimal oxygen Although some species utilize an assortment of these stores that develop as they mature (Thorson & Le Boeuf foraging patterns (Loughlin, Bengston & Merrick 1987; 1994; Horning & Trillmich 1997b; Jørgensen et al. Croxall, Davis & O’Connell 1988; Kato, Watanuki & 2001; Noren et al. 2001; Noren et al. 2002). Younger Naito 1998), each strategy is defined by inherent animals also use oxygen stores faster due to allometric functional characteristics. When hunting epipelagically, relationships and costs associated with growth (Brody predators exhibit short dives in the top 50 m of the 1945; Miller & Irving 1975; Ashwell-Erickson & Elsner water column and often capture multiple small prey 1981; Schmidt-Nielsen 1984). Young pups may not (Gentry et al. 1986; Croxall et al. 1988; Costa 1991). have fully developed pulmonary surfactant capabilities Dive records for epipelagic foragers indicate a diel to enable lung collapse during deeper dives (Miller et al. pattern with shallower, more frequent dives during the 2005). Finally, smaller animals experience more drag night as prey in the deep scattering layer migrate verti- per unit mass (Schreer & Kovacs 1997). These factors cally (Gentry et al. 1986; Goebel et al. 1998). Meso- constrain the abilities of young divers. pelagic foragers demonstrate a diel pattern, but take The Australian sea lion demonstrates a unique single large prey during long dives deep in the midwater non-annual, non-synchronous breeding season (Gales column (DeLong & Stewart 1991; Kooyman et al. 1992; et al. 1994; Gales & Costa 1997). Pups are suckled for Hochachka & Foreman 1993). Predators foraging approximately 17·6 months, one of the longest lacta- benthically tend to hunt for single large prey on or near tion periods in pinnipeds (Higgins 1993; Higgins & the substrate bottom (Kooyman et al. 1982; Gentry Gass 1993). This reproductive strategy may have evolved et al. 1986; Croxall et al. 1988). Benthic divers exhibit as an adaptation to a stable marine environment where long dives to consecutively similar depths with no diel resources are limited and show little seasonal fluctu- pattern (Kooyman et al. 1982; Costa 1991; Tremblay & ation (Rochford 1980; Pearce 1991; Gales et al. 1994; Cheryl 2000). Foraging on the benthos restricts avail- Gales & Costa 1997). Our study addresses the hypo- able search space to a two-dimensional area and is thesis that extended dependency allows pups time to limited to the continental shelf or seamounts. For develop the demanding benthic foraging skills required benthic foragers, search time is constrained by bottom in their environment. Specifically, we wanted to deter- time (Wilson & Wilson 1988; Boyd 1996). mine if young Australian sea lions are capable of adult The utilization of a particular foraging strategy may benthic diving or if, as in many species, pups and juve- have demographic implications. Otariids that hunt on niles utilize alternative foraging strategies. the benthos spend > 40% of their time at sea diving compared to < 30% for epipelagic foragers (Costa et al. Materials and methods 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 Fieldwork was conducted between June 2001 and experiencing substantial population growth. One of August 2003 at Seal Bay Conservation Park, Kangaroo the rarest pinnipeds is the benthic-feeding Australian Island, South Australia (35°41′ S, 136°53′ E). Three- sea lion (Neophoca cinerea Péron 1816), with a stable or quarters of the Australian sea lion population resides declining population (Gales, Shaughnessy & Dennis in South Australia and Seal Bay contains the third © 2006 The Authors. 1994; Gales, Haberley & Collins 2000). Meanwhile, largest colony (Gales et al. 1994). Journal compilation sympatric epipelagic-foraging New Zealand fur seals © 2006 British (Arctocephalus forsteri) have an exponentially increasing Ecological Society,   -  Journal of Animal population (Shaughnessy et al. 1994; Gales et al. 2000). Ecology, 75, The Australian sea lion provides a particularly inter- Censuses of the colony were carried out twice per day 358–367 esting model of a benthic diver because it is operating at and newborns were identified by direct observation of

360 births or presence of fresh afterbirth. Once the mother dorsal pelage with epoxy. The TDRs were programmed S. L. Fowler et al. left for her first foraging trip after 7–10 days, pups were to sample water depth and temperature every 2 or 4 s marked with bleach, sexed and weighed. Fifty-five pups while the animals were in the water. (28 males and 27 females) from a single cohort were To aid in relocation, VHF transmitters were attached identified and marked over a 5-month period in 2001. in the same manner (Sirtrack Ltd, Havelock, New Before the first moult at approximately 4 months of Zealand). Transmitters were detected by a hand-held age, bleach-marked pups were recaptured and tagged receiver (Telonics, Mesa, AZ, USA) and recaptures on the trailing edge of each foreflipper (Leader Products occurred after 4–15 days. Pty Ltd, Melbourne, VIC, Australia). Pups and adult females were injected in the gluteal region with a sub-   cutaneous passive microtransponder (Destron Fearing Corporation, South St Paul, MN, USA) to ensure that Data were downloaded and decoded using Wildlife individuals were sampled once during the study. Computers software (  1·0·0). A custom- built software package programmed in  4   (National Instruments, Austin, TX, USA) was used for zero-offset correction, analyses and graphical presen- Mothers were identified when they were observed tation (Arnould & Hindell 2001). suckling tagged pups. Mother/pup pairs were captured A dive was defined by a minimum depth of 4 m. simultaneously using specially designed hoop nets Bottom time was determined by inflection points (from (Fuhrman Diversified, Seabrook, TX, USA). The descent to flat and flat to ascent) in the deepest 20 m of general anaesthetic gas Isoflurane was delivered, with each dive in which more than 5% of total dive time was medical oxygen, from a field portable machine (Gales spent. Foraging efficiency (FE) was calculated by dividing & Mattlin 1998). Individuals were weighed using a bottom time by total dive cycle time (dive duration + hanging electronic balance (± 0·1 kg; Dyna-Link MSI- post-dive surface interval: Ydenberg & Clark 1989). 7200, Measurement Systems International, Seattle, Surface intervals were defined as the time between the WA, USA) and a tripod. first 0 m reading after a dive and the last 0 m reading Mothers and their pups were captured during three before the next dive. Time at sea was calculated from different field seasons: 6-month-old pups (March 2002), the time the animal entered the water until it hauled 15-month-old pups (November 2002) and 23-month- out. A foraging trip was characterized by almost old juveniles (July 2003). Ten mother/pup pairs were continuous diving, with very few surface intervals captured each season for a total of 60 different animals exceeding 30 min. Costa & Gales (2003) defined the over the entire study. Two 15-month-old pups and five percentage of time diving as the proportion of time at 23-month-old juveniles were never observed suckling sea spent at depths = 6 m. For the purpose of com- during the season, so these individuals were captured parison, we used the same criteria for this calculation. alone and adult females suckling young pups were Mean and maximum values were determined per animal captured in place of their mothers. The remaining 23- and averaged across age classes. month-old juveniles were observed suckling at least once during the season, despite the fact that average Results weaning occurs at 17·6 months. In July 2003, only six known-age juveniles (that had not been sampled dur- Dive records were recovered from nine 6-month-old ing previous seasons) could be located. Therefore, age pups, seven 15-month-old pups, nine 23-month-old was estimated for the others using pelage condition and juveniles, one 3-year-old and 25 adult females. The growth curves constructed from data on mass and mean (± SE) deployment period for 6-month-old pups standard length (Higgins 1990; this study). In addition, in March 2002 was 11·8 ± 0·6 days, with 81 ± 19 mean one independent juvenile from the previous cohort dives recorded per animal. In November 2002, 15-month- (aged approximately 3 years) was captured and sampled old pups had a mean deployment of 9·2 ± 0·5 days, in July 2003. with 1158 ± 113 mean dives per animal. Mean deploy- ment 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 All animals were equipped with electronic time/depth deployment period of 10·0 ± 0·7 days, with 1110 ± 125 recorders (TDR) to measure diving behaviour. Wildlife mean dives over three field seasons. There were no sig- Computers (Redmond, WA, USA) mark 5, 6 or 8 nificant differences between sexes within age classes; © 2006 The Authors. − TDRs were deployed on adult females and mark 5 or 9 these data were combined (t-test, t6 = 0·60, P = 0·57). Journal compilation TDRs were deployed on pups and juveniles. Devices Mean water temperatures recorded by the instruments © 2006 British were secured with epoxy to a neoprene patch the size of attached to adult females were 18·5 °C in March 2002, Ecological Society, ° ° Journal of Animal the instrument’s base (polystrate 5 min epoxy, Devcon, 20·6 C in November 2002 and 16·4 C in July 2003. Ecology, 75, Danvers, MA, USA). The neoprene was attached to a Dive behaviours for females were similar to published 358–367 larger foot of netting using cable ties and glued to the records (Costa et al. 2001; Costa & Gales 2003).

361 Ontogeny of diving in Australian sea lions

Fig. 1. Representative dive records for four different age classes of Australian sea lions: (a) 6-month-old pup; (b) 15-month-old pup; (c) 23-month-old juvenile; and (d) adult female. Beyond the age of normal weaning (17·6 months), 23-month-old juveniles were still not exhibiting adult dive behaviour.

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)

Max Mean Max Mean Max Mean Age Mass depth depth duration duration bottom bottom (months) n (kg) (m) (m) (min) (min) time (min) Time (min)

6·1 ± 0·2 (5·4–7·1) 9 30·0 ± 1·7* 29 ± 5* 7 ± 1* 2·7 ± 1·1* 0·4 ± 0·2* 1·2 ± 0·6* 0·3 ± 0·1* 14·5 ± 0·2 (13·4–15·7) 7 44·5 ± 2·0* 68 ± 5* 40 ± 4* 5·8 ± 0·2* 3·2 ± 0·2 4·8 ± 0·2* 2·5 ± 0·2 22·6 ± 0·2 (22·1–22·9) 9 48·3 ± 2·6* 78 ± 6* 44 ± 4* 5·8 ± 0·2* 2·8 ± 0·2* 4·6 ± 0·2* 2·0 ± 0·2 3 years 1 65·0 100 57 ± 5 9·0 2·8 ± 0·0 4·6 1·7 ± 0·1 Adult 25 88·2 ± 2·1 103 ± 7 71 ± 4 7·5 ± 0·8 3·3 ± 0·2 5·3 ± 0·5 2·1 ± 0·2

Six-month-old pups demonstrated minimal diving than other parameters and these increased throughout activity, exhibiting the shallowest dive depths, shortest development (Table 1). Maximum depth and duration dive durations and spending the vast majority of time were significantly different across age classes (depth: one-  onshore. By 15 months pups were diving deeper, diving way , F3,37 = 41·63, P < 0·001; duration: Kruskal– for longer durations and taking short foraging trips. Wallis non-parametric , H3 = 12·82, P = 0·01), Twenty-three-month-old juveniles achieved even deeper except between 15 and 23 months (depth: Tukey’s test, depths, longer durations and longer foraging trips. P = 0·23; duration: Dunn’s post-hoc test, P = 0·79). Mean © 2006 The Authors. However, even by 23 months of age juveniles were still depth and duration also increased significantly with age Journal compilation not exhibiting the depths, dive durations or foraging (depth: F = 44·38, P < 0·001; duration: F = 38·97, © 2006 British 3,37 3,37 trip durations typical of adult females (Fig. 1). There P < 0·001), except between 15 and 23 months (depth: Ecological Society, Journal of Animal was no diel pattern in dive records from any age class. P = 0·54; duration: P = 0·13). The 3-year-old juvenile Ecology, 75, Maximum dive depths and durations are likely to reflect demonstrated dive behaviour that was more advanced 358–367 the absolute abilities of animals at different ages better than animals at 23 months, but still below adult levels. 362 S. L. Fowler et al.

Fig. 3. The relationship between bottom time and dive depth for different age classes of Australian sea lions. Symbols represent mean values for individual animals. Six-month-old pups were not demonstrating extensive diving activity, but 15- month-old pups and 23-month-old juveniles defended bottom time at the cost of depth.

Fig. 2. Frequency plots of dive depth for different age classes of Australian sea lions. (a) Seventy-nine per cent of all dives for 6-month-old pups were to 10 m or less; (b) 15-month-old pups dived most frequently to 41–50 m (26% of all dives); (c) 23-month-old juveniles dived most frequently to 10 m or less (17% of all dives); (d) adult females dived to 81–90 m for 25% of their dives.

Younger age classes concentrated larger percentages Fig. 4. Bottom time for different age groups of Australian sea of their diving in shallower depths (Fig. 2). Adult lions (mean ± SE). Bottom time is expressed as a percentage of females dived most frequently to 81–90 m: 6-month- dive duration and total time at sea. *Values significantly old pups never reached these depths, 15-month-old different from adult values. Six-month pups spent a similar pups dived to these depths on 1% of dives and 23- proportion of each dive on the bottom as adults. However, because of substantially lower rates of diving, 6-month-old month-old juveniles reached these depths on only 8% pups spent only 0·1% of total time at sea on the bottom. In of dives. contrast, 15- and 23-month-old sea lions spent significantly

Adult females had significantly higher maximum higher proportions of each dive (F2,31 = 20·07, P < 0·001) and bottom times than younger animals (H3 = 15·27, P = time at sea on the bottom than adults (H3 = 31·94, P < 0·001). 0·002; Table 1). However, mean bottom times were not significantly different between 15-month-old pups, 23- 23: R = −0.096, P = 0·01). For adult females, depth

month-old juveniles and adults (F2,31 = 2·21, P = 0·13; and FE were correlated positively across all depths Fig. 3). By spending a larger proportion of each dive (R = 0·63, P = 0·002). and total time at sea on the bottom than adults (Fig. 4), The mean surface interval for 6-month-old pups was 15- and 23-month-old sea lions demonstrated higher 12·95 ± 3·73 min, compared to 1·36 ± 0·17 min at 15- FE at shallow depths (Fig. 5). There was no significant month-old pups, 1·37 ± 0·18 min at 23-month-old © 2006 The Authors. correlation between depth and FE for 6-month-old pups and 2·58 ± 0·15 min for females. Adult mean Journal compilation pups (Pearson’s product–moment correlation, R = 0·99, surface intervals were significantly greater than mean © 2006 British P = 0·08). Depth and FE were correlated positively surface intervals for 15- and 23-month-old sea lions Ecological Society, Journal of Animal for 15- and 23-month-old animals up to 40 m (15: (H3 = 21·32, P < 0·001). Dive duration and post-dive Ecology, 75, R = 0·96, P = 0·04; 23: R = 0·97, P = 0·03), but corre- surface interval were correlated inversely in 6-month- 358–367 lated negatively beyond 40 m (15: R = −0·98, P = 0·01; old pups (R = –0·09, P = 0·03), 15-month-old pups 363 Discussion Ontogeny of diving in Australian sea Instead of adopting a distinctly different foraging lions 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 Fig. 5. Foraging efficiency [FE = bottom time/(dive duration + shallow on-shelf waters (marine chart AUS 346 dated post-dive surface interval): Ydenberg & Clark 1989] in relation 1997, Australian Hydrographic Office, Wollongong, to dive depth for Australian sea lions. Mean FE was calculated for 10 m depth bins for different age classes. Peak FE was at New South Wales, Australia) pups and juveniles were 21–30 m for 6-month-old pups, 31–40 m for 15-month-old able to dive and forage benthically, but at shallower pups and 23-month-old juveniles and 191–200 m for adult depths than adults. females.    

Results support the hypothesis that extended depend- ency 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 Fig. 6. Diving rates for different age groups of Australian sea has been found in other species (Yoerg 1998). lions (mean ± SE). *Rates significantly different from adult The Galápagos fur seal (Arctocephalus galapagoensis) values. Six-month-old pups exhibited the lowest diving rates, but 15- and 23-month-old sea lions demonstrated significantly also has an extended period of diving development and −1 higher rates than females (dives h : F3,35 = 40·96, P < 0·001; is, in fact, the only pinniped with a typical dependency percentage of time diving: F3,37 = 87·76, P < 0·001). interval longer than Australian sea lions (Trillmich 1986). The Galápagos fur seal is also the smallest pinniped, so although it forages epipelagically (Gentry (R = –0·07, P < 0·001) and 23-month-old juveniles et al. 1986), it must deal with the constraints of smaller (R = –0·04, P = 0·001), but there was no correlation in body size on diving ability. The youngest Galápagos adult females (R = –0·01, P = 0·44). fur seals that were weaned successfully were 2 years Six-month-old pups spent the least amount of time old; at weaning, they were still not capable of adult dive at sea (mean = 10·3 ± 4·8%), while adult females spent performance (Horning & Trillmich 1997a). Interestingly, the greatest (mean = 49·3 ± 4·0%). Fifteen-month-old both Galápagos fur seals and Australian sea lions show pups spent 39·9 ± 2·6% of time at sea, 23-month-old a similar progression of diving behaviours, although juveniles spent 27·8 ± 2·6% and the 3-year-old spent Australian sea lions appear to develop slightly faster © 2006 The Authors. 47%. and wean earlier (Fig. 7). Journal compilation Six-month-old pups also demonstrated the lowest This prolonged development is in contrast to other © 2006 British rates of diving (dives h−1, percentage of time diving). otariids, where pups forage epipelagically and are weaned Ecological Society, Journal of Animal However, 15- and 23-month-old sea lions dived more at a younger age. Antarctic fur seals (Arctocephalus Ecology, 75, frequently and spent a higher percentage of time at sea gazella) develop epipelagic diving skills early. By the 358–367 diving than adults (Fig. 6). time they are weaned at 4 months, Antarctic fur seal 364 However, as air-breathing predators feeding in the S. L. Fowler et al. 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 Fig. 7. Development of (a) maximum dive depths and (b) longer surface intervals. maximum dive durations for Australian sea lions (AS: this Young sea lions were also able to spend a larger pro- study) and Galápagos fur seals (GFS − *Horning & Trillmich 1997a). Estimated weaning (triangles) for both species occurs portion of each dive on the bottom due to the shorter when pups achieve 68% of adult maximum dive depth and transit times required when diving to shallower depths. 77% of adult maximum dive duration. Given that breath-hold durations are limited by phys- iological capabilities, pups can either increase depth pups have the diving ability to exploit prey similar to while decreasing bottom time or decrease depth to those taken by adults (McCafferty, Boyd & Taylor maintain bottom time. The results of the present study 1998). Baker & Donohue (2000) found that at weaning, suggest that immature Australian sea lions sacrificed 4-month-old northern fur seal (Callorhinus ursinus) depth for bottom time (Fig. 3). pups began abruptly diving deeper and switching to the By reducing surface intervals and dive depth, pups nocturnal epipelagic foraging patterns typical of adults. and juveniles were able to increase FE. Although FE Steller sea lions (Eumetopias jubatus) also showed a was higher at 15 and 23 months, these results do not change in epipelagic dive characteristics that coincided mean that pups and juveniles were more capable with the assumed onset of weaning at 11–12 months foragers than adults. On the contrary, young sea lions (Loughlin et al. 2003). Steller yearlings were found to be most probably had to maximize bottom time to a capable of adult dive behaviour (Loughlin et al. 2003). greater extent due to inexperience and undeveloped The duration of lactation dictates when pinniped hunting skills. Additionally, FE defines an animal’s neonates must be prepared to survive independently ability to exploit the environment at depth and only and is determined most probably by a number of fac- adults appeared capable of exploiting depths over 100 m tors. Australian sea lions wean much later than most (Fig. 5). Young sea lions may avoid deeper depths otariids in an environment with little seasonal fluctu- because they cannot afford the costs of lower FE. ation (Rochford 1980; Pearce 1991). The Galápagos fur seal’s flexibility in the timing of weaning may be a way   to deal with a food supply that varies unpredictably © 2006 The Authors. (Limberger et al. 1983; Trillmich & Limberger 1985; The Australian sea lion population is currently esti- Journal compilation Trillmich & Dellinger 1991). The two subpolar species, mated to be approximately 10 000 and is thought to be © 2006 British Antarctic and northern fur seals, wean much earlier, stable or decreasing (Gales et al. 1994). As a result of Ecological Society, Journal of Animal possibly as an adaptation to their environment’s strong small population size, exposure to human activities Ecology, 75, seasonality (Peterson 1968; Doidge, McCann & Croxall and evidence of population declines in some areas, it 358–367 1986; Gentry et al. 1986; Trites & Antonelis 1994). was listed recently as threatened under Australian 365 legislation (Environmental Protection and Biodiversity sea lions (Phocarctos hookeri: Gales & Mattlin Ontogeny of diving Conservation Act 1999, Commonwealth of Australia). 1997; Costa & Gales 2000) and Australian fur seals in Australian sea The Australian sea lion’s range overlaps with that of the (Arctocephalus pusillus doriferus: Arnould & Hindell lions New Zealand fur seal and both species have colonies on 2001). Benthic foraging may be advantageous because Kangaroo Island. Australian sea lions and New Zealand benthic prey are less influenced by seasonal fluctua- fur seals were hunted during the commercial sealing tions and oceanographic perturbations than epipelagic era and there is evidence that both species were once prey (Miller & Sydeman 2004). However, benthic considerably more abundant and widespread (Gales foragers are particularly sensitive to human-induced et al. 1994; Shaughnessy et al. 1994). However, the New disturbances and recently modified environments may Zealand fur seal population is currently estimated to be suddenly become unsuitable. For example, demersal more than 85 000 and has been increasing exponentially and benthic fishery trawls disrupt the habitat and for at least three decades (Shaughnessy et al. 1994). remove the larger size classes of prey benthic foragers Unlike the Australian sea lion, dive records for New depend on (Thrush et al. 1998). Juveniles restricted to Zealand fur seal adult females indicate predominantly shallower near-shore waters are even more likely to be epipelagic foraging (Harcourt et al. 1995). In areas impacted by commercial and recreational fisheries. without high productivity, larger body size may make Recent environmental modifications, anthropogenic epipelagic feeding on small prey unviable for adult reductions in benthic prey and fisheries interactions Australian sea lions, as manoeuvrability is inversely could be impacting seriously juvenile survival and proportional to body length (Fish, Hurley & Costa recruitment. These issues should be taken into consid- 2003). It should, however, be a feasible option for eration for conservation and management of benthic smaller pups and juveniles. Fifteen-month-old Australian foragers and may be an important factor as to why sea lion pups, which are similar in size to adult female many of these populations are currently at risk. New Zealand fur seals, demonstrated longer mean dive durations (3·2 ± 0·2 min: this study vs. 1·4 ± 1·1 min in Acknowledgements New Zealand: Mattlin, Gales & Costa 1998), which would indicate that they are capable of similar foraging This work was supported by UC MEXUS, NSF WISC, behaviour. However, despite the apparent success of the JEB Travelling Fellowship, ONR (no. N00014-02-1- New Zealand fur seal foraging strategy and the potential 1012-005), Wildlife Computers, National Geographic benefit of reduced competition with older conspecifics, Society, Myers Oceanographic and Marine Biology young Australian sea lions seem to be hardwired to Trust, American Museum of Natural History Lerner forage benthically. A lack of plasticity in the foraging Grey Fund, American Cetacean Society, Friends of behaviours of Australian sea lions could be one factor Long Marine Laboratory, Project AWARE, Sigma Xi, contributing to current population dynamics. Sealink, Clairol and South Australia National Parks One limitation of benthic foraging is restricted avail- and Wildlife. The following people provided invaluable able foraging habitat due to the finite extent of the con- field assistance: Seal Bay Conservation Park staff, D. tinental shelf. This limitation is even more severe for Higgins, N. Rourke, D. Needham, Melbourne Zoo pups that cannot or do not reach adult foraging depths, (S. Blanchard, G. McDonald), Z. Boland, C. Farber, such as young Australian sea lions. As sea floor depth J. Gibbens, A. Martinez, H. Mostman, S. Sataar, S. gradually increases with distance from shore, shallow Simmons, Y. Tremblay and M. Weise. J. Estes, H. Fowler, dives are conducted in near-shore waters closer to the K. J. Fowler, G. Kooyman and the Costa laboratory colony, which are more likely to become depleted of group provided helpful comments on drafts. Research prey (‘Ashmole’s halo’: Ashmole 1963). If juveniles are was carried out under South Australian Department not capable of diving deeper, young sea lions may not for Environment and Heritage permit no. G24475-2 be able to expand foraging grounds in response to and Wildlife Ethics Committee permit no. 4/2001. reductions in prey. Protocols were approved by the Prevention of Cruelty Given that Australian sea lion adults operate at or to Animals Act 1985 and the Chancellor’s Animal near their physiological maximum (Costa & Gales Research Committee (no. Cost01·01). 2003) and juveniles have reduced diving abilities, young sea lions may be limited in their capacity to increase References dive depth, duration or foraging effort. Juvenile Australian sea lions would therefore be particularly Arnould, J.P.Y. & Hindell, M.A. (2001) Dive behaviour, foraging locations, and maternal attendance patterns on vulnerable to resource limitation. Indeed, high mortal- Australian fur seals (Arctocephalus pusillus doriferus). ity rates in young Galápagos fur seals during periods of Canadian Journal of Zoology, 79, 35–48. © 2006 The Authors. food scarcity, such as El Niño events, are believed to Ashmole, N.P. (1963) The regulation of numbers of tropical Journal compilation result from lower juvenile diving abilities (Trillmich & oceanic birds. Ibis, 104, 458–473. © 2006 British Dellinger 1991; Horning & Trillmich 1997a). Ashwell-Erickson, S. & Elsner, R. (1981) The energy cost of Ecological Society, free existence for Bering Sea harbour and spotted seals. The Journal of Animal Despite the apparent costs a number of otariids Eastern Bering Sea Shelf: Oceanography and Resources (eds Ecology, 75, forage benthically, including southern sea lions (Otaria D.W. Hood & J.A. Calder), pp. 869–899. US Department 358–367 flavenscens: Werner & Campagna 1995), New Zealand of Commerce, Washington, DC. 366 Baker, J.D. & Donohue, M.J. (2000) Ontogeny of swimming Gales, N.J., Shaughnessy, P.D. & Dennis, T.E. (1994) Distri- S. L. Fowler et al. and diving in northern fur seal pups. Canadian Journal of bution, abundance, and breeding cycle of the Australian sea Zoology, 78, 100–109. lion, Neophoca cinerea (Mammalia: Pinnipedia). Journal of Bard, K.A. (1995) Sensorimotor cognition in young feral Zoology, 234, 353–370. orangutans (Pongo pygmaeus). Primates, 36, 297–321. Gentry, R.L., Costa, D.P., Croxall, J.P., David, J.H.M., Davis, Boyd, I.L. (1996) Temporal scales of foraging in a marine R.W., Kooyman, G.L., Majluf, P., McCann, T.S. & predator. Ecology, 77, 426–434. Trillmich, F. (1986) Summary and conclusions. Fur Seals: Brody, S. (1945) Bioenergetics and Growth with Special Refer- Maternal Strategies on Land and at Sea (eds R.L. Gentry & ence to the Efficiency Complex in Domestic Animals. Hafner G.L. Kooyman), pp. 220–264. Princeton University Press, Press, New York. Princeton. Butler, P.J. & Jones, D.R. (1997) Physiology of diving birds Goebel, M.E. (1998) Female foraging behaviour: Inter- and and mammals. Physiological Review, 77, 837–899. intra-annual variation in individuals. Behaviour and Ecology Castro, J.J. & Hernandezgarcia, V. (1995) Ontogenetic changes of the Northern Fur Seal (ed. R.H. Gentry), pp. 243–259. in mouth structures, foraging behaviour and habitat use of Princeton University Press, Princeton, New Jersey. Scomber japonicus and Ilex coindetii. Scientia Marina, 59, Gremillet, D., Argentin, G., Schulte, B. & Culik, B.M. (1998) 347–355. Flexible foraging techniques in breeding comorants Costa, D.P. (1991) Reproductive and foraging energetics of Phalacrocorax carbo and shags Phalacrocorax aristotelis: pinnipeds: implications for life history patterns. Behaviour benthic or pelagic feeding? Ibis, 140, 113–119. of Pinnipeds (ed. D. Renouf ), pp. 300–344. Chapman & Harcourt, R.G., Schulman, A.M., Davis, L.S. & Trillmich, F. Hall, London. (1995) Summer foraging by lactating female New Zealand Costa, D.P. & Gales, N.J. (2000) Foraging energetics and fur seals (Arctocephalus forsteri) off Otago Peninsula, New diving behaviour of lactating New Zealand sea lions, Zealand. Canadian Journal of Zoology, 73, 678–690. Phocarctos hookeri. Journal of Experimental Biology, 203, Hauser, M.D. (1993) Ontogeny of foraging behaviour in wild 3655–3665. vervet monkeys, Cercopithecus aethiops, social interactions Costa, D.P. & Gales, N.J. (2003) Energetics of a benthic diver: and survival. Journal of Comparative Psychology, 107, 276– seasonal foraging ecology of the Australian sea lion, 282. Neophoca cinerea. Ecological Monographs, 73, 27–43. Heinsohn, R.G. (1991) Slow learning of foraging skills and Costa, D.P., Gales, N.J. & Goebel, M.E. (2001) Aerobic dive extended parental care in cooperatively breeding white- limit: how often does it occur in nature? Comparative Bio- winged choughs. American Naturalist, 137, 864–881. chemistry and Physiology, Part A, 129, 771–783 [Review]. Higgins, L.V. (1990) Reproductive behaviour and maternal Costa, D.P., Kuhn, C.E., Weise, M.J., Shaffer, S.A. & investment of Australian sea lions. PhD Thesis, University Arnould, J.P.Y. (2004) When does physiology limit the for- of California, Santa Cruz. aging behaviour of freely diving mammals? International Higgins, L.V. (1993) The nonannual, nonseasonal breeding Congress Series, 1275, 359–366. cycle of the Australian sea lion, Neophoca cinerea. Journal Croxall, J.P., Davis, R.W. & O’Connell, M.J. (1988) Diving of Mammalogy, 74, 270–274. patterns in relation to diet of gentoo and macaroni penguins Higgins, L.V. & Gass, L. (1993) Birth to weaning: parturition, at South Georgia. Condor, 90, 157–167. duration, lactation and attendance cycles of the Australian DeLong, R.L. & Stewart, B.S. (1991) Diving patterns of sea lion (Neophoca cinerea). Canadian Journal of Zoology, northern elephant seal bulls. Marine Mammal Science, 7, 71, 2047–2055. 369–384. Hochachka, P.W. & Foreman, R.A. (1993) Phocid and ceta- Diamond, J. & Bond, A.B. (1991) Social-behaviour and the cean blueprints of muscle metabolism. Canadian Journal of ontogeny of foraging in the kea (Nestor notabilis). Ethology, Zoology, 71, 2089–2098. 88, 128–144. Horning, M. & Trillmich, F. (1997a) Ontogeny of diving Doidge, D.W., McCann, T.S. & Croxall, J.P. (1986) Attendance behaviour in the Galápagos fur seal. Behaviour, 134, 1211– behaviour of Antarctic fur seals. Fur Seals: Maternal Strat- 1257. egies on Land and at Sea (eds R.L. Gentry & G.L. Kooyman), Horning, M. & Trillmich, F. (1997b) Development of haemo- pp. 102–114. Princeton University Press, Princeton. globin, haematocrit and erythrocyte values in Galápagos Dolphin, W.F. (1988) Foraging dive patterns of humpback whales, fur seals. Marine Mammal Science, 13, 100–113. Megaptera novaeangliae, in southeast Alaska: a cost–benefit Irvine, L.G., Hindell, M.A., van den Hoff, J. & Burton, H.R. analysis. Canadian Journal of Zoology, 66, 2432–2441. (2000) The influence of body size on dive duration of Doroff, A.M. & DeGange, A.R. (1994) Sea otter, Enhydra underyearling southern elephant seals (Mirounga leonina). lutris, prey composition and foraging success in the northern Journal of Zoology London, 251, 463–471. Kodiak Archipelago. Fisheries Bulletin, 92, 704–710. Jørgensen, C., Lydersen, C., Brix, O. & Kovacs, K.M. (2001) Fish, F.E., Hurley, J. & Costa, D.P. (2003) Manoeuvrability by Diving development in nursing harbour seal pups. Journal the sea lion Zalophus californianus: turning performance of of Experimental Biology, 204, 3993–4004. an unstable body design. Journal of Experimental Biology, Kato, A., Watanuki, Y. & Naito, Y. (1998) Benthic and pelagic 206, 667–674. foraging of two Japanese comorants, determined by simul- Gales, N.J. & Costa, D.P. (1997) The Australian sea lion: a taneous recording of location and diving activity. Journal of review of an unusual life history. Marine Mammal Research Yamashina Institute of Ornithology, 30, 101–108. in the Southern Hemisphere, vol. 1. Status, Ecology and Kooyman, G.L. (1989) Diverse Divers: Physiology and Beha- Medicine (eds M. Hindell & C. Kemper), pp. 78–87. Surrey viour. Springer-Verlag, Berlin. Beatty and Sons, Sydney. Kooyman, G.L., Cherel, Y., Le Maho, Y., Croxall, J.P., Gales, N.J., Haberley, B. & Collins, P. (2000) Changes in the Thorson, P.H. & Ridoux, V. (1992) Diving behaviour and abundance of New Zealand fur seals, Arctocephalus forsteri, Energetics during foraging cycles in King Penguins. Eco- © 2006 The Authors. in Western Australia. Wildlife Research, 26, 165–168. logical Monographs, 62, 143–163. Journal compilation Gales, N.J. & Mattlin, R.H. (1997) Summer diving behaviour Kooyman, G.L. (2002) Evolutionary and ecological aspects © 2006 British of lactating New Zealand sea lions Phocarctos hookeri. of some Antarctic and sub-Antarctic penguin distributions. Ecological Society, Canadian Journal of Zoology, 75, 1695–1706. Oecologia, 130, 485–495. Journal of Animal Gales, N.J. & Mattlin, R.H. (1998) Fast, safe, field-portable Kooyman, G.L., Davis, R.W., Croxall, J.P. & Costa, D.P. Ecology, 75, gas anaesthesia for otariids. Marine Mammal Science, 14, (1982) Diving depths and energy requirements of king 358–367 355–361. penguins. Science, 217, 726–727. 367 Kooyman, G.L., Wahrenbrock, E.A., Castellini, M.A., Peterson, R.S. (1968) Social behaviour in the pinnipeds with Ontogeny of diving Davis, R.W. & Sinnet, E.E. (1980) Aerobic and anaerobic particular reference to the northern fur seal. The Behaviour in Australian sea metabolism during voluntary diving in Weddell seals: and Physiology of Pinnipeds (eds R.J. Harrison, R.C. evidence of preferred pathways from blood chemistry and Hubbard, R.S. Peterson, C.E. Rice & R.J. Schusterman), lions behaviour. Journal of Comparative Physiology B, 138, 335– pp. 3–53. Appleton-Century-Crofts, New York. 346. Ponganis, P.J., Starke, L.N., Horning, M. & Kooyman, G.L. Langen, T.A. (1996) Skill acquisition and the timing of natural (1999) Development of diving capacity in emperor pen- dispersal in the white throated magpie jay, Calocitta formosa. guins. Journal of Experimental Biology, 202, 781–786. Animal Behaviour, 51, 575–588. Rochford, D.J. (1980) Nutrient status of the oceans around Lima, A.P. & Moreira, G. (1993) Effects of prey size and for- Australia. CSIRO Division of Fisheries and Oceanography aging mode on the ontogenetic change in feeding niche of Report, 1977–79, 9–20. Colostethus stepeni, Anura, Dendrobatidae. Oecologica, Rolseth, S.L., Koehler, C.E. & Barclay, R.M.R. (1994) 95, 93–102. Differences in the diets of juvenile and adult hoary bats, Limberger, D., Trillmich, F., Kooyman, G.L. & Majluf, P. Lasiurus cinereus. Journal of Mammalogy, 75, 394–398. (1983) Reproductive failure of fur seals in Galápagos and Schmidt-Nielsen, K. (1984) Scaling: Why Is Body Size So Peru in 1982–83. Tropical Ocean–Atmosphere Newsletter, Important? Cambridge University Press, Cambridge. 21, 16–17. Schreer, J.F. & Kovacs, K.T. (1997) Allometry of diving Loughlin, T.R., Bengston, J.L. & Merrick, R.L. (1987) capacity in air-breathing vertebrates. Canadian Journal of Characteristics of feeding trips of female northern fur seals. Zoology, 75, 339–358. Canadian Journal of Zoology, 65, 2079–2084. Shaughnessy, P.D., Gales, N.J., Dennis, T.E. & Goldsworthy, Loughlin, T.R., Sterling, J.T., Merrick, R.L. & Sease, J.L. S.D. (1994) Distribution and abundance of New Zealand (2003) Diving behaviour of immature Steller sea lions. fur seals, Arctocephalus forsteri, in South Australia and Fishery Bulletin, 101, 566–582. Western Australia. Wildlife Rescue, 21, 667–695. Magrath, R.D. & Lill, A. (1985) Age-related differences in Sullivan, K.A. (1988) Age-specific probability and prey behaviour and ecology of crimson rosellas, Platycercus ele- choice. Animal Behaviour, 36, 613–615. gans, during the non-breeding season. Australian Wildlife Thorson, P.H. & Le Boeuf, B.J. (1994) Developmental aspects Rescue, 12, 299–306. of diving in northern elephant seal pups. Elephant Seals: Mattlin, R.H., Gales, N.J. & Costa, D.P. (1998) Seasonal Population Ecology, Behaviour, and Physiology (eds B.J. Le dive behaviour of lactating New Zealand fur seals (Arc- Boeuf & R.M. Laws), pp. 271–289. University of California tocephalus forsteri). Canadian Journal of Zoology, 76, 350– Press, Berkeley. 360. Thrush, S.F., Hewitt, J.E., Cummings, V.J., Dayton, P.K., Maurer, E.F. (1996) Environmental variation and behaviour: Cryer, M., Turner, S.J., Funnell, G.A., Budd, R.G., Milburn, resource availability during ontogeny and feeding per- C.J. & Wilkinson, M.R. (1998) Disturbance of the marine formance in salamander larvae (Ambystoma texanum). habitat by commercial fishing: impacts at the scale of the Freshwater Biology, 36, 35–44. fishery. Ecological Applications, 8, 866–879. McCafferty, D.J., Boyd, I.L. & Taylor, R.I. (1998) Diving Tremblay, Y. & Cherel, Y. (2000) Benthic and pelagic dives: a behaviour of Antarctic fur seal (Arctocephalus gazella) new foraging behaviour in rockhopper penguins. Marine pups. Canadian Journal of Zoology, 76, 513–520. Ecology Progress Series, 204, 257–267. Milinski, M. & Parker, G.A. (1991) Competition for Trillmich, F. (1986) Maternal investment and sex-allocation in resources. Behavioural Ecology − an Evolutionary Approach the Galápagos fur seal, Arctocephalus galapagoensis. (eds J.R. Krebs & N.B. Davies), pp. 137–168. Blackwell Behavioural Ecology and Sociobiology, 19, 157–164. Scientific Publications, Oxford. Trillmich, F. & Dellinger, T. (1991) The effects of El Niño on Miller, K. & Irving, L. (1975) Metabolism and temperature Galápagos pinnipeds. Pinnipeds and El Niño. Responses regulation in young harbour seals, Phoca vitulina richardsi to Environmental Stress (eds F. Trillmich & K.A. Ono), in water. American Journal of Physiology, 229, 506–511. pp. 66–74. Springer-Verlag, Heidelberg. Miller, N.J., Postle, A.D., Schürch, S., Schoel, W.M., Daniels, Trillmich, F. & Limberger, D. (1985) Drastic effects of El Niño C.B. & Orgeig, S. (2005) The development of the pulmo- on Galápagos pinnipeds. Oecologia, 67, 19–22. nary surfactant system in California sea lions. Comparative Trites, A.W. & Antonelis, G.A. (1994) The influence of cli- Biochemistry and Physiology, Part A, 141, 191–199. matic seasonality on the life cycle of the Pribilof northern Miller, A.K. & Sydeman, W.J. (2004) Rockfish response to fur seal. Marine Mammal Science, 10, 311–324. low-frequency ocean climate change as revealed by the diet Werner, R. & Campagna, C. (1995) Diving behaviour of lac- of a marine bird over multiple time scales. Marine Ecology tating southern sea lions (Otaria flavescens) in Patagonia. Progress Series, 281, 201–216. Canadian Journal of Zoology, 73, 1975–1982. Noren, S.R., Lacave, G., Wells, R.S. & Williams, T.M. (2002) Wilson, R.P. & Wilson, M.P.T. (1988) Foraging behaviour in The development of blood oxygen stores in bottlenose dol- four sympatric cormorants. Journal of Animal Ecology, 57, phins (Tursiops truncatus): implications for diving capacity. 943–955. Journal of Zoology, 258, 105–113. Ydenberg, R.C. & Clark, C.W. (1989) Aerobiosis and anaer- Noren, S.R., Williams, T.M., Pabst, D.A., McLellan, W.A. & obiosis during diving by Western grebes: an optimal forag- Dearolf, J.L. (2001) The development of diving in marine ing approach. Journal of Theoretical Biology, 139, 437–449. endotherms: preparing the skeletal muscles of dolphins, Yoerg, S.I. (1998) Foraging behaviour predicts age at inde- penguins, and seals for activity during submergence. pendence in juvenile Eurasian dippers (Cinclus cinclus). Journal of Comparative Physiology, 171, 127–134. Behavioural Ecology, 9, 471–477. Pearce, A.F. (1991) Eastern boundary currents of the southern hemisphere. Journal of the Royal Society Western Australia, Received 29 June 2005; revised version accepted 24 October © 2006 The Authors. 74, 35–45. 2005 Journal compilation © 2006 British Ecological Society, Journal of Animal Ecology, 75, 358–367