ontogeny of movements and foraging ranges in the australian sea lion

MARINE MAMMAL SCIENCE, 23(3): 598–614 (July 2007)C© 2007 by the Society for Marine MammalogyDOI: 10.1111/j.1748-7692.2007.00134.x

ONTOGENY OF MOVEMENTS AND FORAGINGRANGES IN THE AUSTRALIAN SEA LION

SHANNON L. FOWLER

DANIEL P. COSTA

Department of Ecology and Evolutionary Biology,University of California at Santa Cruz,Santa Cruz, California 95064, U.S.A.

E-mail: [email protected]

JOHN P. Y. ARNOULD

School of Biological and Chemical Sciences,Deakin University,

221 Burwood Highway,Victoria 3125, Australia

ABSTRACT

This study tracked the movements of Australian sea lion (Neophoca cinerea) pups,juveniles, and adult females to identify home ranges and determine if young sealions 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 Australiansea lions at Seal Bay Conservation Park, Kangaroo Island, South Australia. Femalesdid not travel with their offspring at sea, suggesting young Australian sea lionslearn foraging behaviors independently. Although home ranges increased with age,23-mo-old juveniles had not developed adult movement capacity and their rangewas 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 meanlocations were 48 ± 7 m for juveniles and 74 ± 2 m for females. Restricted to shallowcoastal waters, pups and juveniles are more likely to be disproportionately impactedby human activities. With limited available foraging habitat, young Australiansea lions appear particularly vulnerable to environmental alterations resulting fromfisheries or climate change.

Key words: development, foraging ecology, home ranges, learning, Neophoca cinerea,Australian sea lion, PTT, satellite telemetry.

The transition for young mammals from dependence on milk to independentforaging can lead to increased mortality (Hayssen 1993). To improve survival rates ofjuveniles, many species demonstrate protracted dependency periods with extensivematernal instruction (Lee 1986, Symington 1990, Estes et al. 2003). Lessons may notinvolve active pedagogy, but offspring can learn through observation or by exposure to

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FOWLER ET AL.: AUSTRALIAN SEA LION MOVEMENTS 599

foraging areas. As precocial progeny commonly ingest solid food well before weaning,the increased opportunities for learning foraging techniques may be more importantfor some species than the energetic and nutritional benefits of continued nursing(Hayssen 1993).

Mimicry of maternal behavior has been hypothesized to be an important mechanismin the development of foraging habits of young moose (Alces alces; Kossak 1992).Gopukumar et al. (2003) suggested young short-nosed fruit bats, Cynopterus sphinx,learn locations of profitable food patches by accompanying their mothers on foragingflights during late lactation and weaning. Observational learning of maternal foragingtechniques has also been implicated in nonhuman primates (Watts 1985, van Schaiket al. 2003).

Young mammals in aquatic environments must deal with the constraint of theseparation between air at the surface and prey at depth, and pinnipeds must ad-ditionally shift from terrestrial nursing to marine foraging (Bonner 1984). Marinespecies demonstrate a wide range of dependency periods and maternal guidance.Bottlenose dolphins, Tursiops truncatus, remain with their mothers for 3–10 yr, wellbeyond the 18-mo lactation interval (Shane et al. 1986, Wells et al. 1987). In bot-tlenose dolphins at Shark Bay, Australia, the technique of using marine sponges asforaging tools is passed down exclusively from mother to daughter (Krutzen et al.2005). In the Crozet islands, female killer whales, Orcinus orca, teach their offspringthe difficult technique of intentional stranding (Guinet and Bouvier 1995). Sea otter(Enhydra lutris) pups inherit dietary patterns matrilineally, developing the specifictool-using strategy of their mothers (Estes et al. 2003). Walruses (Odobenus rosmarus)nurse their pups aquatically during a protracted 2-year lactation period (Fay 1981).

Although most phocid pups are abandoned onshore after a brief lactation interval,some species enter the water before weaning: e.g., bearded seals (Erignathus barbatus;Lydersen et al. 1994), harbor seals (Phoca vitulina; Lawson and Renouf 1985), ringedseals (Phoca hispida; Lydersen and Hammill 1993), and Weddell seals (Leptonychotesweddellii; Kooyman 1967). Studies have been limited due to logistical difficulties, butdiving behavior in nursing pups has been studied in three of these four phocids andevidence of maternal guidance has been found in all three species. Bearded seal pupsaccompany their mothers during foraging trips at sea (Gjertz et al. 2000). Harbor sealpups also accompany their mothers on many foraging trips (Bowen, et al. 1999), andmother/pup pairs often start diving simultaneously (Bekkby and Bjørge 2003). Satoet al. (2003) found synchronous shallow diving by Weddell seal mother/pup pairsduring lactation.

Otariids have longer dependency periods and, therefore, increased opportunitiesfor maternal transfer of knowledge. Although some researchers have assumed moth-ers and their dependent young dive and forage together (Pitcher and Calkins 1981,Loughlin et al. 2003, Frost et al. 2006) and others have assumed they do not (Atkin-son 1997, Trillmich and Weissing 2006), no prior studies have directly investi-gated otariid mother-pup associations at sea. The Australian sea lion, Neophoca cinerea,demonstrates one of the longest lactation periods in pinnipeds (17.6 mo: Higginsand Gass 1993), and pups begin diving before they are weaned (Fowler et al. 2006).Australian sea lion adults work hard to forage benthically, demonstrating high fieldmetabolic rates, and spending 58% of time at sea diving and 35% of time at seaon or near the bottom (Costa and Gales 2003). Juveniles spend 67% of time at seadiving and 44% of time at sea on or near the bottom (Fowler et al. 2006). Althoughmany air-breathing vertebrates dive well within their estimated limit of oxygen stores(Kooyman et al. 1980, Dolphin 1988, Butler and Jones 1997), Australian sea lion

600 MARINE MAMMAL SCIENCE, VOL. 23, NO. 3, 2007

adults and juveniles appear to operate close to their physiological maximum (Costaet al. 2001, Fowler 2005). The prolonged dependency period could provide exten-sive opportunities for foraging lessons, while the extreme diving behavior requiredin the Australian sea lions’ environment might necessitate it. Alternatively, it hasbeen hypothesized that female harbor seals accompanying pups demonstrate reducedforaging efficiency, and hence, the metabolic demands of foraging for Australian sealions may preclude lactating females from performing suboptimal dives with theiryoung (Bowen et al. 1999).

As a result of small population size, small breeding colony size, low reproductiverate, exposure to human activities, and evidence of population declines in some areas,Australian sea lions have recently been listed as threatened and vulnerable (Environ-mental Protection and Biodiversity Conservation Act 1999). A number of fisheriesoperate near Australian sea lion colonies (Page et al. 2004). Fisheries may competefor the same resources, alter foraging habitat, or directly impact sea lion populationsthrough entanglements, drownings, bycatch, and harassment. The entanglement ratefor Australian sea lions (1.3%) is the third highest reported for any pinniped and be-lieved to be increasing (Page et al. 2004). Potential biological removal (PBR) modelsare non-age structured and can be applied across species to predict the maximumallowable bycatch rate that enables a population to maintain or reach optimum size;they have been used extensively in the United States to calculate allowable levelsof human-induced mortality in marine mammals (Barlow et al. 1995, Wade 1998).Currently, reported levels of Australian sea lion bycatch exceed PBR values (Camp-bell et al. 2006). Satellite tracking of different age classes is needed to determinethe extent of spatial overlap with Australian sea lion foraging effort and commercialfisheries (Page et al. 2004).

The objectives of this study were two-fold: (1) to identify foraging ranges forAustralian sea lion pups, juveniles, and adult females; and (2) to establish if there wasevidence of maternal assistance in the development of foraging skills by determiningwhether pups accompanied their mothers at sea.

METHODS

Fieldwork was conducted between June 2001 and August 2003 at Seal Bay Conser-vation Park, Kangaroo Island, South Australia (35◦41′S, 136◦53′E). A known-agedcohort of 55 pups (28 males and 27 females) was flipper-tagged in 2001 (see Fowleret al. 2006). To ensure individuals were only measured once, pups and adult femalesreceived a subcutaneous passive microtransponder chip (Destron Fearing Corporation,South St. Paul, MN, USA).

Mother/pup pairs were captured simultaneously, sedated with Isoflurane gas anes-thesia (Gales and Mattlin 1998), and weighed (±0.1 kg; Dyna-Link MSI-7200,Measurement Systems International, Seattle, WA, USA). Pairs were captured dur-ing three different field seasons: 6-mo pups (March 2002), 15-mo pups (November2002), and 23-mo juveniles (July 2003). Ten mother/pup pairs were captured eachseason, with the exception of two 15-mo pups and five 23-mo juveniles, which werenever observed suckling. These individuals were captured alone and adult femalessuckling young pups were captured in place of their mothers. The remaining 23-mojuveniles were observed suckling at least once during the field season, despite thefact that average weaning occurs at 17.6 mo (Higgins and Gass 1993). In July 2003,only six known-age juveniles (that had not been sampled in March or November


2002) could be located. Therefore, age was estimated for four juveniles using pelagecondition and growth curves constructed from data on mass and standard length(Fowler 2005).

Satellite Locations

All animals were equipped with time/depth recorders (TDRs: Mark 5, 6, 8, or9; Wildlife Computers, Redmond, WA, USA), VHF radios (Sirtrack Ltd, Havelock,New Zealand), and, with the exception of 6-mo old pups, with platform terminaltransmitters (PTTs: Telonics, Mesa, AZ, USA; Wildlife Computers). Devices weresecured with epoxy (Polystrate 5-min epoxy, Devcon, Danvers, MA, USA) to a neo-prene patch, which was then glued to the dorsal pelage. Six-month-old pups were notequipped with PTTs because radio signals indicated pups did not leave the colony.Visual observations verified pups were either with their mothers, on the beach, or inshallow rock pools directly in front of the colony. Six-month-old pups also demon-strated minimal diving activity (Fowler et al. 2006) and there were concerns aboutthe size of PTTs relative to smaller body sizes.

Data Analyses

Location data (ARGOS system, Toulouse, France) were filtered using the IKNOStoolkit developed in MATLAB (7.0.4 2005, The MathWorks, Natick, MA, USA),which filters based on maximum travel speed (≤3 m/s: Feldkamp et al. 1989, Ponganiset al. 1990), ARGOS location class, time elapsed between two consecutive locations(≥10 min), and whether a location was on land or at sea (Tremblay et al. 2006).Filtered locations were mapped and analyzed in ArcView GIS (3.2 1999, ESRI, Inc.,Redlands, CA, USA). A foraging trip was defined as the time from an animal’sdeparture until its return to the colony based on TDR records. Distance traveled wasmeasured as the maximum straight-line distance from the departure site for eachforaging trip. Following Bradshaw et al. (2004), we calculated the compass bearingto this position of maximum distance. Home ranges were created using the AnimalMovement Extension of ArcView (Hooge et al. 2000), which computes a fixed kernelrange (KR) as a grid. We determined KRs for 75% of all locations per sea lion usingsmoothing factors calculated via least squares cross-validation (Silverman 1986).Following Chilvers et al. (2005), a central point was taken from within each individualKR and direct-line distances to the colony were calculated. Travel rates were defined asmean rates between all at-sea locations. Mean locations were determined to calculatemean sea floor depths where sea lions were diving. Movements of mothers and theiryoung were analyzed using ArcView dynamic interaction pairs function, which teststhe degree to which simultaneous movements of two individuals interact. Straight-line distances were determined between all locations of mothers and their respectiveoffspring that occurred within 30-min time intervals.

Dive behavior recorded from these Australian sea lions is presented in detail else-where (Fowler et al. 2006). Corresponding TDR records of mothers and pups (ninepairs in March 2002, seven pairs in November 2002) and mothers and juveniles (fourpairs in July 2003) were aligned to identify if synchronized diving occurs. The meanTDR deployment was less than 9 days, so given the accuracy of the clock, any clockdrift over this time interval would be insignificant. Percentages of total deploymenttime that mothers and their pups were at sea concurrently were also calculated.


Figure 1. Seal Bay Conservation Park on Kangaroo Island, South Australia. Satellite lo-cations for adult female Australian sea lions (n = 9), 4–20 March 2002, are shown as blackdots. Kernel home range for 75% of all locations is represented as black lines.

RESULTS

Satellite tracks were obtained for 47 Australian sea lions. During March 2002, ninerecords were downloaded for adult females, with a mean ± SE deployment periodof 12.7 ± 0.5 d (SigmaStat 3.1 2004, Systat Software, Inc., Chicago, IL, USA). InNovember 2002, ten adult female records (9.2 ± 2.2 d) and nine 15-mo-old puprecords (9.6 ± 0.4 d) were obtained; eight mother/pup pairs were recorded. DuringJuly 2003, ten adult female records (7.6 ± 0.7 d) and nine 23-mo juvenile records(6.9 ± 0.7 d) were downloaded; four mother/juvenile pairs recorded. Deploymentswere short to allow for retrieval of instruments, but multiple trips to sea were recordedfor most animals: 1.6 ± 0.6 trips for 6-mo-old pups, 5.9 ± 1.1 trips for 15-mo-oldpups, 4.5 ± 0.8 trips for 23-mo-old juveniles, and 3.0 ± 0.4 trips for adult females.The number of locations recorded per unit time was not significantly different betweenage classes (Kruskal-Wallis: H2 = 3.80, P = 0.15).

Mean and maximum distances traveled increased with both age (mean: r2 = 0.59,P < 0.001; max: r2 = 0.50, P < 0.001) and mass (mean: r2 = 0.46, P < 0.001; max:r2 = 0.41, P < 0.001). There were no significant differences between sexes withinage classes (pups: mean t6 = –1.81, P = 0.12; max t6 = −1.27, P = 0.25; juveniles:mean t7 = 0.16, P = 0.88; max t7 = 0.43, P = 0.68); these data were combined.

Adult females headed south to the continental shelf edge (Fig. 1, 2b, 3b). Distancestraveled by adult females were not significantly different between seasons (ANOVA:


Figure 2. Satellite locations for Australian sea lion mothers and pups off Kangaroo Island,10–25 November 2002. Locations for 15-mo-old pups (n = 9) are represented by white dots;locations for adult females (n = 10) are shown as black dots. Kernel ranges for 75% of locationsare represented as black lines.

F2,25 = 0.02, P = 0.98). Compared to adults, 15-mo-old pups stayed much closer tothe colony (Fig. 2a). Both mean and maximum distances traveled by 15-mo old pupswere significantly shorter than distances traveled by their mothers (mean: t16 = 6.07,P < 0.001; max: t16 = 4.89, P < 0.001; Table 1). Twenty-three-month-old juvenilesheaded farther out from the colony than pups but did not reach the continental

Figure 3. Satellite locations for Australian sea lions off Kangaroo Island, 14–31 July 2003.Locations for 23-mo-old juveniles (n = 9) are shown as black Xs; locations for adult females(n = 10) are shown as black dots. Kernel ranges for 75% of locations are shown as black lines.


Tabl

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75%

KR

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(kg)

(km

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KR

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(km

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14.5

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29

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(13.

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36.5

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835

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(22.

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167

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76.6

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374

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shelf edge (Fig. 3a). Mean and maximum distances traveled by juveniles were stillsignificantly shorter than distances traveled by adult females in July 2003 (mean:t17 = 3.77, P = 0.002; max: t17 = 4.90, P < 0.001; Table 1).

Direct-line distances from Seal Bay to KR centers were also significantly shorter forpups and juveniles, indicating central foraging areas closer to the colony for youngeranimals (pups: t35 = 5.96, P < 0.001; juveniles: t36 = −4.81, P < 0.001; Table 1).In November 2002 the KR of 15-mo-old pups was 38.9% of the adult female range(Fig. 2). By July 2003, 23-mo-old juveniles had only expanded their KR to 40.6%of the female range (Fig 3).

Mean azimuthal bearing to positions of maximum distance for adult females was187.2◦ ± 48.2◦ in March (range 78.2◦–246.2◦), 213.4◦ ± 35.2◦ in November (range169.4◦–272,7◦), and 225.5◦ ± 39.8◦ in July (range 152.7◦—269.5◦). Althoughthere were no significant differences between seasons (F2,26 = 2.12, P = 0.14), thestatistical power to detect differences was low (0.22). However, pups and juvenilesheaded in significantly different directions (Mann-Whitney: T = 36.00, P = 0.02);the mean bearing for 15-mo-old pups in November was 178.5◦ ± 55.7◦ (range111.5◦–247.7◦) compared to 244.1◦ ± 18.3◦ for 23-mo-old juveniles in July (range213.6◦–264.5◦). There were no significant differences within seasons between adultfemales and young sea lions (November: t15 = 1.59, P = 0.13; July: t17 = 1.28,P = 0.22).

Statistical power to detect differences between seasons for the maximum trip du-rations of adult females (F2,25 = 3.37, P = 0.051) was low (0.42). There was asignificant difference between mean trip durations (F2,25 = 6.60, P = 0.01), withmothers of the youngest age class (in March 2002) demonstrating the shortest du-ration trips (Tukey post hoc test: P < 0.04). Trip durations of 15-mo-old pups weresignificantly shorter than trip durations of both their mothers (mean: t16 = 6.91, P< 0.001; max: t16 = 3.90, P = 0.001) and 23-mo-old juveniles (mean: t15 = 3.92,P = 0.001; max: t15 = −2.22, P = 0.04; Table 1). The mean trip duration for pupswas only half the mean trip duration for adults. Twenty-three-month-old juvenilesdemonstrated longer trip durations than adult females in July 2003, although thesedifferences were not significant (mean: T = 101.00, P = 0.39; max: t17 = 0.33,P = 0.75).

Mean travel rates of adult females were not significantly different between seasons(F2,25 = 0.60, P = 0.56). Females traveled significantly faster than 15-mo-old pups inNovember 2002 (t15 = 4.28, P < 0.001) and 23-mo-old juveniles in July 2003 (t17 =−3.00, P = 0.008; Table 1). Juveniles traveled at a mean rate that was approximatelyhalf the speed traveled by adult females.

Satellite locations of mother-pup (Fig. 4) and mother-juvenile pairs (Fig. 5) indicateyoung sea lions dived and foraged in different locations than their mothers. Insteadof heading south, many pups and juveniles traveled east or west along the coast,staying in shallow nearshore waters (Fig. 4). Mean locations for 15-mo-old pups and23-mo-old juveniles were in significantly shallower waters than adult females (pups:T = 39.50, P = 0.001; juveniles: T = 53.50, P = 0.003; Table 1).

Although there were spatial overlaps with the tracks of young sea lions and theirmothers, these overlaps were not coincident temporally. Furthermore, many locationsfor mothers and pups occurred at similar times but were separated by considerabledistances. Dynamic interaction pairs analyses determined that mothers and their15-mo-old pups were separated by a mean distance of 50.8 ± 7.4 km within 30-min time intervals; only 3.6% of 140 paired locations were within the range of anadult otariid traveling at maximum measured speeds (3 m/s, or 5.4 km/30 min:


Figure 4. Satellite locations and dive records for an Australian sea lion mother-pup pair,November 2002. Satellite locations for the 15-mo-old pup are represented by white dots;locations for its mother are represented by black dots. Axes are identical for both dive records.Pups and mothers dived in different locations and did not dive together.

Feldkamp et al. 1989, Ponganis et al. 1990). Mothers and their 23-mo-old juvenileswere separated by 38.4 ± 13.5 km; 9.6% of 52 paired locations were within the rangeof an adult otariid traveling at maximum measured speeds. Synchronized animatedtracks provided further verification that mothers did not travel with their offspring.

There was also no indication of mothers and pups diving synchronously in TDRrecords (Fig. 4–6). Although adult females and their offspring sometimes enteredthe water together, they would immediately begin diving independently. Mothersand their 6-mo-old pups were at sea concurrently for only 2.5% ± 0.5% of totaldeployment time, mothers and their 15-mo-old pups were at sea concurrently for19.2% ± 3.5%, and mothers and their 23-mo-old juveniles were at sea concurrentlyfor 12.2% ± 2.2% of deployment time. Data indicate that these Australian sea lionmothers and their young did not associate at sea.

DISCUSSION

Australian sea lions appear to utilize different foraging grounds at different agesand expand ranges throughout development. However, the home range for 23-mo-old juveniles was less than half of the adult female home range. Data indicate youngsea lions are restricted to shallow nearshore waters. In addition, mother-pup pairsdid not travel together, suggesting Australian sea lions do not teach their offspringto dive and forage. Both of these factors may have negative impacts on juvenilerecruitment.


Figure 5. Satellite locations and dive records for an Australian sea lion mother-juvenilepair, July 2003. Satellite locations for the juvenile are represented by black Xs; locations forits mother are represented by black dots. Axes are identical for both dive records. AlthoughAustralian sea lions typically wean at 17.6 mo (Higgins and Gass 1993), this juvenile wasstill observed suckling at 23 mo.

Ontogeny of Foraging

Australian sea lion pups and juveniles traveled shorter distances at slower speedsthan adult females. Of the 2,310 filtered locations, the maximum distance traveledby a young sea lion was 67.3 km, (compared to 132.4 km for an adult female). Thisyoung sea lion, which appeared to have been weaned, also demonstrated the longestforaging trip duration—10.2 d. Of the remaining pups and juveniles, the maximumdistance traveled was only 44.9 km during a trip that lasted 6.8 d.

Although immature Australian sea lions did not reach adult distances or achieveadult depths and durations, dive records indicate pups and juveniles forage benthically(Fowler et al. 2006). We found a close correlation between sea floor depths of meanlocations and mean dive depths, further indicating benthic diving (Table 1). Dataon oxygen stores and oxygen consumption rates suggest young Australian sea lionsmay be physiologically unable to dive deeper or longer (Fowler 2005). So, althoughpups and juveniles were not traveling as far or as fast as adult females, this does notnecessarily mean they do not have the ability to do so. Instead, lower dive capacitymay restrict pups to shallow, coastal environments where they can reach the benthos.

Separation of foraging areas for different age classes also has the potential ben-efit of reducing intraspecific competition. This may be particularly important foryoung pinnipeds facing disadvantages due to physiological limitations. Field et al.(2005) found that younger southern elephant seals, Mirounga leonina, utilized smaller


Figure 6. Dive records for an Australian sea lion mother-pup pair, March 2002. Axes areidentical for both records. Satellite locations were not recorded for 6-mo-old Australian sealions, but dive records suggest young pups did not dive with their mothers.

foraging areas and stayed closer to land than older animals. Juveniles of different agesappeared to avoid competition through temporal and spatial oceanic segregationsthat allowed resource partitioning (Field et al. 2005). Although intraspecific com-petition has not been documented in Australian sea lions, spreading foraging effortover larger areas and minimizing overlap between age classes provide a theoreticalecological advantage in an environment where prey have a low biomass and patchydistribution (Shuntov 1969, Pearce 1991, Kloser et al. 1998).

In November, 15-mo-old Australian sea lion pups traveled in a different direction(south) than 23-mo-old juveniles in July (southwest). Although differences werenot significant between seasons for adults, females also headed in a more westerlydirection in July. Little data are available concerning the distribution of likely preyitems off Kangaroo Island, but rock lobsters, which have been identified as part ofthe Australian sea lion diet, have been documented moving off the west coast, andoffshore aggregations of male lobsters peak in July (Gales and Cheal 1992, Linnaneet al. 2005). Coastal upwelling during summer and fall may also cause seasonalchanges in foraging areas (Kampf et al. 2004, Ward et al. 2006).

Protracted development and dependency in Australian sea lions is in contrast tosome of the other pinnipeds that enter the water before weaning. Young beardedseal pups travel farther than their mothers and wean after just 24 d (Gjertz et al.


2000). Harbor seal juveniles demonstrate larger home ranges than adults; pups weanafter 21–28 d (Lowry et al. 2001). Although Steller sea lion (Eumetopias jubatus)mother-pup pairs have not been studied at sea, trip distance and duration increasethroughout development (Raum-Suryan et al. 2004). Steller sea lions typically wean at12 mo (Calkins and Pitcher 1982) and movement patterns suggest juvenile swimmingability is comparable to adults (Loughlin et al. 2003).

Maternal Transfer of Information

Although deployments were short, there was no indication of maternal supervisionat sea in the satellite records of twenty-four Australian sea lions. There was also noindication of synchronized diving in forty TDR records. This has many potentialconsequences for young Australian sea lions. A mother’s presence is believed to providesome protection from predation (Bowen et al. 1999, Peaker 2002). Factors causingseparation of harbor seal mothers and pups, such as storms, have been shown to lead toincreased pup mortality (Boness et al. 1992, Bekkby and Bjørge 2003). Bowen et al.(1999) suggested harbor seal pups may also receive indirect benefits by observingforaging locations and preferable prey types. Learning to forage independently maynot only decrease chances of survival, but also delay acquisition of adult hunting skills.

Given the extended development and dependency in Australian sea lions, the dis-association of foraging between females and their young could be seen as surprising.It seems intuitive that lactation length would correlate to the degree to which off-spring learn survival skills from their mothers (Delpietro and Russo 2002, Esteset al. 2003, Grellier et al. 2003). Whether this holds true for pinnipeds is unclear.Four studies of phocids found evidence of maternal instruction or supervision at sea(Bowen et al. 1999, Gjertz et al. 2000, Bekkby and Bjørge 2003, Sato et al. 2003).These species (bearded, harbor, and Weddell seals) demonstrate lactation periods ofaverage duration or longer compared to other phocids (Kooyman 1967, Lawson andRenouf 1985, Gjertz et al. 2000). Our study is the first to examine otariids. Althoughotariids have longer lactation intervals than phocids, and Australian sea lions haveone of the longest dependency periods in pinnipeds, ours is also the first study to findno evidence of mother-pup associations at sea.

It is possible that Australian sea lions are the only otariids that do not accompanytheir offspring at sea. Instead of necessitating maternal guidance, the extreme divingbehavior required in the Australian sea lion’s environment may actually prevent it.Bowen et al. (1999) found female harbor seals diving with pups had significantlyshorter diving bouts than females diving without pups. This led to the specula-tion that foraging efficiency of females accompanied by pups was lower than that ofunaccompanied females. Adult female Australian sea lions already dive almost con-tinuously while at sea and operate at or near their physiological maximum (Costa et al.2001, Costa and Gales 2003). Shorter diving bouts and lower foraging efficiency maynot be viable options for Australian sea lion mothers dealing with increased demandsof lactation.

It is also possible that some otariids accompany their pups at sea and others donot. Pups that enter the water at a very early age to avoid tidal flooding or predationby terrestrial carnivores (Lydersen et al. 1994, Bowen et al. 1999) may need to beaccompanied by their mothers. If this were the case, we would expect to see otariidpups in similar environments supervised at sea. Pups that do not have to avoidterrestrial threats, such as Australian sea lions, may be able to wait on land until theyare mature enough to enter the water independently.


A third possibility is that otariids do not teach their young to dive and forage.This could be a consequence of different ontogenetic strategies. Phocids typicallyutilize what is known as capital breeding or the fasting strategy; adult females fast oreat little food during lactation (Costa 1991, Boyd 1998). Larger body size and lowermass-specific metabolism may allow phocid mothers the reserve capacity necessaryto either forego food altogether or to accommodate the lower dive capabilities ofpups and dive with reduced foraging efficiency. Otariids utilize income breeding orthe foraging cycle strategy where mothers alternate suckling periods ashore withforaging bouts at sea (Costa 1991, Boyd 1998). Otariids may not have the reservecapacities required to accommodate the physiological limitations of pups. Futureresearch addressing maternal transfer of foraging information in other otariids wouldbe instructive.

Demographic Implications

Our results suggest young Australian sea lions are restricted to nearshore waterssurrounding the colony, which are more likely to become depleted of prey (Ashmole1963) and more liable to be disproportionately impacted by human activities. Indeed,Campbell et al. (in press) recorded incidental captures of Australian sea lions inwestern rock lobster pots between 1983 and 2004: Pups and juveniles (5–20 mo old)were the only age classes caught and catches occurred exclusively in waters less than20-m deep and within 25 km of a breeding colony. The catch rate (33 voluntarilyreported mortalities) was higher than any previously reported between pinnipeds androck lobster fisheries and appeared to be increasing (Campbell et al., in press). Pageet al. (2004) reported Australian sea lion pups on Kangaroo Island were the mostfrequently entangled age class and the majority of entangling material originatedfrom nearby fisheries. In addition to being restricted to coastal waters, the fact thatyoung Australian sea lions forage without maternal supervision may make them moresusceptible to these interactions.

Our results can be used to identify practical distances for fisheries to operatearound Australian sea lion colonies. Young Australian sea lions may be unable toavoid fisheries interactions close to colonies because they cannot move away from thecoast or expand foraging grounds by diving deeper. For a threatened species with alow reproductive rate, small population, and isolated breeding colonies, successfuljuvenile recruitment is critical. Given the exposure to coastal fisheries, restrictedavailable foraging habitat, limited behavioral options, and susceptibility to resourcelimitation, juvenile Australian sea lions appear particularly vulnerable.

ACKNOWLEDGMENTS

Research protocols were approved by South Australian Department for Environment andHeritage (G24475-2), Wildlife Ethics Committee (4/2001), Prevention of Cruelty to AnimalsAct 1985, and UCSC Chancellor’s Animal Research Committee (Cost01.01). This work wassupported by UC MEXUS, NSF AAAS WISC, JEB Traveling Fellowship, ONR, WildlifeComputers, National Geographic, Myers Oceanographic and Marine Biology Trust, Amer-ican Museum of Natural History Lerner Grey, American Cetacean Society, Friends of LongMarine Lab, PADI AWARE, Sigma Xi, Sealink, Clairol, and South Australia National Parksand Wildlife. The following people provided invaluable assistance in the field: Seal BayConservation Park staff, N. Gales, D. Higgins, N. Rourke, D. Needham, Melbourne ZooPinniped Team (S. Blanchard, G. McDonald), Z. Boland, C. Farber, J. Gibbens, H. Mostman,


S. Sataar, S. Simmons, Y. Tremblay, and M. Weise. P. Robinson and Y. Tremblay assisted withanalyses. J. Estes, H. Fowler, K. J. Fowler, G. Kooyman, and T. Williams provided helpfulcomments on early drafts.

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Received: 28 July 2006Accepted: 26 January 2007

ontogeny of movements and foraging ranges in the australian sea lion

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