Age-specific growth, survival, and population dynamics of female ...

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Age-specific growth, survival, and population dynamics of female Australian fur seals J. Gibbens and J.P.Y. Arnould

Abstract: Postsealing population recovery rates of fur seals and sea lions have differed markedly, perhaps owing to habitat type. Australian fur seals (Arctocephalus pusillus doriferus Wood Jones, 1925) employ a benthic foraging mode similar to sea lions, and have exhibited similarly slow population recovery. Nonetheless, the population doubled in recent decades, suggesting a recent change in demographic rates. In the present study, the frequency and size of known-age females (n = 297) were used to create body growth and survivorship models. These were compared with models obtained in the 1970s before the recent population increase. Body growth, which is relatively rapid in comparison to other fur seal species, remains unchanged since the 1970s, suggesting that density-dependent effects are absent despite the population increases. Adult survival rates (weighted mean: 0.885) have increased greatly since the 1970s and are the likely mechanism of the recent increases. Total population abundance was estimated to be 4.5 times that of pups. Australian fur seals display high survivorship, rapid body growth, low fecundity, and low population growth rates; all are characteristics typical of benthic foraging sea lions rather than other fur seals. Re´sume´ : Les taux de rećupe´ration chez les otaries a` fourrure et les lions de mer depuis la fermeture de la chasse diffe`rent conside´rablement, peut-eˆtre a` cause de leurs types d’habitat. Les otaries a` fourrure d’Australie (Arctocephalus pusillus doriferus Wood Jones, 1925) utilisent un mode de recherche de nourriture semblable a` celui des lions de mer et connaissent une rećupe´ration de´mographique aussi lente. Neánmoins, la population a double´ au cours des dećennies rećentes, ce qui laisse croire a` un changement dans les taux de´mographiques. Dans notre e´tude, la fre´quence et la taille de femelles d’aˆge connu (n = 297) nous ont servi a` e´laborer des mode`les de croissance corporelle et de survie. Ces mode`les ont e´te´ compare´s a` des mode`les reálise´s dans les anneés 1970 avant l’accroissement rećent de la population. La croissance corporelle, qui est relativement rapide en comparaison de celles des autres espe`ces d’otaries a` fourrure, demeure inchangeé depuis les anneés 1970, ce qui fait penser il n’y a pas d’effets de densite´ de´pendance malgre´ l’accroissement de la population. Les taux de survie des adultes (moyenne ponde´reé: 0,885) se sont grandement accrus depuis les anneés 1970 et sont vraisemblablement les mećanismes explicatifs des accroissements rećents. L’abondance totale de la population est estimeé a` 4,5 fois celle des petits. Les otaries a` fourrure d’Australie posse`dent une survie e´leveé, un croissance corporelle rapide, une fećondite´ basse et des taux de croissance de´mographique bas, des caracte´ristiques plus typiques des lions de mer, qui recherchent leur nourriture dans le benthos, que des autres otaries a` fourrure. [Traduit par la Re´daction]

Introduction During the commercial sealing era of 1790–1850, many populations of otariids were hunted to very low numbers (Bonner 1994). Since then, the recovery rates of fur seal and sea lion populations have differed markedly (Costa et al. 2006). It has recently been suggested that these divergent population dynamics are in fact associated with habitat type rather than phylogeny (Arnould and Costa 2006). Epipelagic foragers (most fur seals) exploit the upper portion of upwellings and frontal structures, which are typically rich in nutrients, and their populations recovered rapidly to large sizes. In contrast, benthic foragers (most sea lions) hunt near the benthos of continental shelves, which are typically of lower productivity. Their populations are an order of magnitude smaller and most are stable or declining (Arnould and Costa 2006; Costa et al. 2006).

Australian fur seals (Arctocephalus pusillus doriferus Wood Jones, 1925) are one of the few exceptions to this pattern and are the only fur seal species known to use benthic foraging exclusively (Arnould and Hindell 2001; Arnould and Kirkwood 2008). Their status as conspecific to epipelagic foraging Cape fur seals (Arctocephalus pusillus pusillus (Schreber, 1775)), from which they separated some 12 000 years ago (Wynen et al. 2001; Deme´re´ et al. 2003), makes them an ideal candidate in which to investigate the effects of habitat type on population dynamics while controlling for phylogeny. The Cape fur seal population forages in the nutrient-rich Benguela upwelling off southwestern Africa (Kooyman and Gentry 1986) and recovered rapidly to a size of approximately 2 million individuals (Butterworth et al. 1995). In contrast, the Australian fur seal population exploits the nutrient-poor continental shelf of Bass Strait (Gibbs 1992; Ar-

Received 24 February 2009. Accepted 2 July 2009. Published on the NRC Research Press Web site at cjz.nrc.ca on 24 September 2009. J. Gibbens.1 Department of Zoology, University of Melbourne, Parkville, Victoria 3010, Australia. J.P.Y. Arnould. School of Life and Environmental Sciences, Deakin University, 221 Burwood Highway, Burwood, Victoria 3125, Australia. 1Corresponding

author (e-mail: [email protected]).

Can. J. Zool. 87: 902–911 (2009)

doi:10.1139/Z09-080

Published by NRC Research Press

Gibbens and Arnould

nould and Hindell 2001; Arnould and Kirkwood 2008) and recovered relatively slowly to approximately 100 000 animals (Kirkwood et al. 2005). Curiously, half of the abundance of the Australian fur seal population was attained in the last 2 decades (Kirkwood et al. 2005). Prior to this, no growth had been observed from 1945 to 1986 and the population was thought to have stabilized at a quarter of its estimated presealing size (Pearse 1979; Warneke and Shaughnessy 1985; Warneke 1988). The population’s recovery is presumably constrained by its fecundity, which is the lowest observed in fur seals and instead is similar to that recorded in sea lions (Gibbens et al. 2010). Yet, the current reproductive rate is similar to that reported in the 1970s so that the recent doubling in population abundance cannot be attributed to increased fecundity (Arnould et al. 2003). The recent population increases have been inferred from trends in pup production because unquantifiable numbers of adults and juveniles spend time at sea during which they are invisible to counters (Berkson and DeMaster 1985). Pup production estimates have also been extrapolated to estimate population abundance; however, such conversions depend on the proportion of pups in the population (Wickens and Shelton 1992), which has not been quantified in Australian fur seals. Previously, pup to population conversion factors observed in other pinniped species (e.g., Harwood and Prime 1978) have been used as proxies (Pemberton and Kirkwood 1994; Shaughnessy et al. 2002; Pemberton and Gales 2004; Kirkwood et al. 2005). However, the conversion factor is influenced by the fecundity rate, and because fecundity is relatively low in Australian fur seals, factors derived from species may be unsuitable (Wickens and Shelton 1992; Gibbens et al. 2010). The Australian fur seal population now represents the largest marine predator biomass in the Bass Strait ecosystem, raising concerns about increased rates of conflict with the local commercial fishing industry (Pemberton and Shaughnessy 1993; Goldsworthy et al. 2003). However, the current lack of demographic information hinders understanding of its dynamics, abundance, and management requirements. Demographic information obtained for other fur seals is extensive (Wickens and York 1997), but may not be appropriate for modelling the dynamics of benthic foraging populations for which demographic information is scarce and largely limited to the Steller sea lion (Eumetopias jubatus (Schreber, 1776)) (Holmes and York 2003; Eberhardt et al. 2005). To better understand the Australian fur seal population and the effects of a benthic foraging mode on population dynamics, there is a need for the basic parameters of survival and body growth rates to be determined. Therefore, the aims of this study were to (i) determine female age structure, (ii) derive a survivorship model from the age structure, (iii) model female body growth, (iv) compare the models with ones obtained prior to the recent population increase, and (v) investigate the abundance and dynamics of the Australian fur seal population.

Materials and methods The study was conducted between 2003 and 2005 at Kanowna Island (39810’S, 146818’E), northern Bass Strait, the site of an Australian fur seal colony with annual pup pro-

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duction of approximately 3550 and median birth date of 23 November (Gibbens and Arnould 2009). Breeding occurs all around the island but is concentrated in two main areas comprising >75% of the colony (J. Gibbens, unpublished data). Captures of juvenile and adult females (‡1 year old) were conducted in the main breeding areas from March to October, with 84% of captures occurring in winter (June– August). Female pups (10 years, and a similar agespecific decline in pregnancy rates (but not birth rates) was observed in a concurrent study, perhaps indicative of senescence (Gibbens et al. 2010). High survival rates have not always been observed in Australian fur seals. A 1970s study reported an adult female age structure with relatively low frequencies in the middle age classes (5–11 years; Fig. 4; Arnould et al. 2003). Survival rates were substantially lower than those of the present study (weighted adult mean = 0.498, compared with 0.885), and a rapid population decline of 8%–24% per year was projected (Arnould et al. 2003). The matrix elasticities of the present study (Fig. 3) indicate that the population growth rate is up to 7 times more sensitive to changes in adult survival rates than fecundity rates, which is a general feature of fur seals and other large mammals (Wickens and York 1997; Oli and Dobson 2003). Therefore, the 0.387 increase in mean survival rates over the last 3 decades is the likely mechanism of the observed doubling in population abun-

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dance. In the same period, body growth and fecundity rates remained unchanged, suggesting that increased survivorship has resulted from the relaxation of an exogenous source of mortality rather than increased resource availability (Arnould and Warneke 2002; Arnould et al. 2003; Gibbens et al. 2010; this paper). It has previously been suggested that fishers routinely culled seals because they were perceived as competitors and that this was particularly intense during the 1960s (Arnould et al. 2003). Australian seals were not protected from hunting until 1975 (Shaughnessy 1999). Until 1983, fishers in Victorian waters (northern Bass Strait) could legally shoot ‘‘nuisance seals’’ interfering with fishing operations, and anecdotal evidence suggests that this was common (R.M. Warneke, unpublished data). At least 8% of tagged juveniles retrieved as carcasses during the 1970s had gunshot wounds (Warneke 1975). Introduction of protective legislation therefore coincides with increased survival and population growth. Population abundance The survivorship model indicated that total female abundance was 6.0 times greater than that of female pups. This is a greater difference than the 3.5–4.5 range estimated for grey seals (Halichoerus grypus (Fabricius, 1791); Harwood and Prime (1978)) and frequently used as a conversion factor in both sexes of Australian fur seals (Pemberton and Kirkwood 1994; Shaughnessy et al. 2002; Pemberton and Gales 2004; Kirkwood et al. 2005). It is also higher than the 3.95 factor estimated by scaling the demographic rates of female northern, Antarctic, and South American fur seals to the maximum observed ages of male and female Australian fur seals (Goldsworthy et al. 2003). The conversion factor is influenced by the fecundity rate used to estimate N0 (Wickens and Shelton 1992), which was estimated to be 0.45 by Harwood and Prime (1978) and 0.39 by Goldsworthy et al. (2003) (calculated from Barlow and Boveng 1991 and Lima and Paez 1997). These are higher fecundity rates than used in the present study (0.266), and accordingly, pups were estimated to comprise a smaller proportion of the female Australian fur seal population. However, a conversion factor of 6.0 may not be suitable for the whole population because breeding male otariids experience additional mortality risks (e.g., fighting and fasting) and, consequently, have substantially lower survivorship than females (Butterworth et al. 1995; Wickens and York 1997). Reports of male survivorship are scarce, but in Steller sea lions and northern fur seals, female to male sex ratios in the nonpup component of the population were estimated as 2.13:1 and 2.77, respectively (Lander 1981; Calkins and Pitcher 1982; Trites and Larkin 1996). Applying the mean of these ratios to the survivorship model of the present study results in a pup to population conversion factor of 4.5. In the absence of survivorship data in male Australian fur seals, this factor is suggested for converting pup production to a population abundance estimate. The factor is comparable with ones previously used for the Australian fur seal population (Harwood and Prime 1978; Goldsworthy et al. 2003), which although based on inappropriately high fecundity, ignored the potential for a highly female-biased sex ratio in nonpups. Published by NRC Research Press

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Population dynamics Stable population growth was projected rapidly (in 2 years) by the matrix model, although this could be somewhat overestimated owing to modeled values for N1–3 being used in the initial age structure. Nonetheless, the projection infers a largely stable adult age structure as would result from a period of constant survival and fecundity and survival rates (Caughley 1980). Survival rates were adjusted for the trend at the study site from 1997 to 2005, as information prior to this was unavailable. Slightly higher trends were observed at some colonies in the 1990s (Shaughnessy et al. 2002; Kirkwood et al. 2005), and if this was the case at the study site, the survival rates of older age classes (8+ years) could be negatively biased. The similar survival rates of adult otariids suggests that fecundity is the characteristic distinguishing rapidly and slowly recovering populations. In benthic foraging Steller sea lions, late-gestation pregnancy rates of 0.63–0.55 have been recorded (Pitcher et al. 1998), similar to the late-gestation and birth rates of 0.55 and 0.53, respectively, recorded in Australian fur seals (Arnould et al. 2003; Gibbens et al. 2010) and the 0.48 birth rate recorded in Australian sea lions (when converted to an annual rate; Higgins and Gass 1993). These rates are lower than birth rates recorded in epipelagic foraging New Zealand fur seals (0.699; McKenzie 2006), Antarctic fur seals (0.68; Lunn et al. 1994; Wickens and York 1997), and subantarctic fur seals (Arctocephalus tropicalis (J.E. Gray, 1872)) (0.84; Hes and Roux 1983), suggesting that epipelagic foragers achieve higher rates of birth and, consequently, population growth. Accordingly, Australian fur seals are unlikely to recover at the rates of 10%–15% per year reported in other fur seal populations (Wickens and York 1997). Species-wide pup censuses conducted in 2002 and 2007 observed a similar trend to that obtained by the present study (2.0% per year; R. Kirkwood, personal communication (2009)). Using this growth rate, a 4.5 pup to population conversion factor, and the 2007 pup production estimate of 21 882 (R. Kirkwood, personal communication (2009)), the estimated presealing population size of 200 000 (Ling 2002) is projected to be reached in 2043. However, growth generally slows as a population becomes density-dependent (Sinclair et al. 2006) and, furthermore, the current environmental carrying capacity is unknown. The commercial fishing industry may have decreased carrying capacity by altering trophic dynamics since the presealing era (Goldsworthy et al. 2003). However, fishing has caused concurrent declines in predator populations, particularly that of the great white shark (Carcharodon carcharias (L., 1758)) (Malcolm et al. 2001), and their roles in regulating the prehistoric seal population are unknown. Furthermore, a sympatric population of New Zealand fur seals is currently recovering at up to 11% per year and recolonising Bass Strait, which could introduce competition for prey and breeding sites (Arnould et al. 2000; McKenzie 2006). The prey, body condition, and pup production of Australian fur seals are influenced by local oceanography (Kirkwood et al. 2008; Gibbens and Arnould 2009); however, it is difficult to predict how this may affect future population dynamics (Harley et al. 2006). Local oceanography is linked

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to the Southern Oscillation (Middleton and Bye 2007) and extremes of the oscillation (El Ninõ – La Ninã events) may increase in strength and frequency with climate change (Trenberth and Hoar 1997). However, while El Ninõ is associated with catastrophic prey depletion and reproductive failure for many epipelagic foragers (Trillmich and Ono 1991), no such association has been found in Australian fur seals (Kirkwood et al. 2008; Gibbens and Arnould 2009). Unless an oceanic regime shift occurs, like that implicated in the decline of the Steller sea lion population (Trites and Donnelly 2003), the near-future population dynamics of Australian fur seals may be more influenced by interactions with humans than by environmental change. In summary, Australian fur seals display rapid body growth, low fecundity, and low population recovery rates. These characteristics resemble those of benthic foraging sea lions and contrast with the slower body growth, higher fecundity, and higher population recovery rates observed in epipelagic foraging fur seals. Additional studies of benthic foraging sea lions would be useful for understanding the effects of habitat type on population dynamics, and the population model in the present study could be improved with information on juvenile and male survivorship in Australian fur seals.

Acknowledgements Research was conducted under Department of Sustainability and Environment (Victoria) Wildlife Research permit 10003856. Funding was provided by the Holsworth Wildlife Research Endowment, University of Melbourne Department of Zoology, and the Australian Research Council. Material support and personnel were provided by Melbourne Zoo, Parks Victoria (Wilsons Promontory), University of Melbourne, and Deakin University. R. Kirkwood provided advice on recent population trends. Field assistance provided by A. Hoskins, P. Day, M. Sale, N. Fuller, S. Thompson, L. Bamforth, and R. Web.

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