Creatures of habit: foraging habitat fidelity of adult female Australian sea lions

We examined the movement characteristics and seasonality of feeding behaviour for an endemic Australian otariid, the Australian sea lion Neophoca cinerea. By combining tracking data and stable isotope analysis of serially subsampled vibrissae from 20 adult females at 7 colonies, we were able to characterise individual foraging specialisation across 80% of the species range. Adult females expressed long-term temporal consistency in both foraging site (offshore vs. inshore) and prey selection. When seasonality in foraging behaviour was detected (n = 7), there was no consistency in variation of isotope ratios between individuals or colonies. Offshore-foraging sea lions fed at higher trophic levels than inshore foragers. Potentially, inshore foragers could be subdivided into those which targeted heterogeneously distributed seagrass meadows or calcarenite reef sys tems for different payoffs. This data highlights the importance of understanding individual specialisation and the dangers of generalising behaviour at the colony level. Individual specialisation in foraging behaviour may be a mechanism that reduces intra-specific competition, but its effectiveness will be a function of the temporal stability of individual differences. The present study is the first to identify multi-season consistency of individual foraging behaviour for any otariid. Given the long-term stability of adult female foraging behaviour, categorising individuals using a proxy measure such as whisker isotopic signature appears robust, economical, and appropriate. Such data is critical to mod- elling population response to anthropogenically driven fine-scale habitat modification.

[1]  K. Hobson,et al.  Isotopic (δ15N and δ13C) evidence for intersexual foraging differences and temporal variation in habitat use in waved albatrosses , 2007 .

[2]  A. Klimley,et al.  School fidelity and homing synchronicity of yellowfin tuna, Thunnus albacares , 1999 .

[3]  Gwilym M. Jenkins,et al.  Time series analysis, forecasting and control , 1972 .

[4]  M. Hindell,et al.  Fine-scale three-dimensional spatial use by diving, lactating female Weddell seals Leptonychotes weddellii , 2002 .

[5]  S. Bearhop,et al.  Applications of stable isotope techniques to the ecology of mammals , 2008 .

[6]  K. Hobson,et al.  Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals , 1996 .

[7]  M. Willson,et al.  Vertebrate exploitation of pulsed marine prey: a review and the example of spawning herring , 2006, Reviews in Fish Biology and Fisheries.

[8]  Mirtha Lewis,et al.  Sex-specific foraging strategies and resource partitioning in the southern elephant seal (Mirounga leonina) , 2006, Proceedings of the Royal Society B: Biological Sciences.

[9]  B. L. Boeuf,et al.  DIFFERENCES IN FORAGING LOCATION OF MEXICAN AND CALIFORNIA ELEPHANT SEALS: EVIDENCE FROM STABLE ISOTOPES IN PUPS , 2006 .

[10]  L. Halsey,et al.  Monitoring Prey Availability via Data Loggers Deployed on Seabirds: Advances and Present Limitations , 2008 .

[11]  D. Crocker,et al.  Swimming speed and foraging strategies of New Zealand sea lions (Phocarctos hookeri) , 2001 .

[12]  D. Schneider,et al.  A spatial and temporal perspective on research and management of groundfish in the northwest Atlantic , 1995 .

[13]  Clifford M. Hurvich,et al.  Regression and time series model selection in small samples , 1989 .

[14]  D. Noakes,et al.  Adaptive peaks and alternative foraging tactics in brook charr: evidence of short-term divergent selection for sitting-and-waiting and actively searching , 1999, Behavioral Ecology and Sociobiology.

[15]  C. Adams,et al.  Temporal stability of niche use exposes sympatric Arctic charr to alternative selection pressures , 2011, Evolutionary Ecology.

[16]  D. Pauly,et al.  Mapping world-wide distributions of marine mammal species using a relative environmental suitability (RES) model , 2006 .

[17]  C. Guinet,et al.  Foraging habitat and diving activity of lactating Subantarctic fur seals in relation to sea-surface temperatures at Amsterdam Island , 2000 .

[18]  R. Tibshirani,et al.  Generalized Additive Models , 1991 .

[19]  R. Phillips,et al.  Central place foraging by breeding Cook’s petrel Pterodroma cookii: foraging duration reflects range, diet and chick meal mass , 2010 .

[20]  Andrew Harvey,et al.  An Algorithm for Exact Maximum Likelihood Estimation of Autoregressive–Moving Average Models by Means of Kaiman Filtering , 1980 .

[21]  D. Post.  USING STABLE ISOTOPES TO ESTIMATE TROPHIC POSITION: MODELS, METHODS, AND ASSUMPTIONS , 2002 .

[22]  M. Kimura,et al.  The Stepping Stone Model of Population Structure and the Decrease of Genetic Correlation with Distance. , 1964, Genetics.

[23]  Lenore Fahrig,et al.  Response of predators to loss and fragmentation of prey habitat: a review of theory. , 2006, Ecology.

[24]  Steven C. Wheelwright,et al.  Forecasting methods and applications. , 1979 .

[25]  J. Arnould,et al.  Bathymetry and frontal system interactions influence seasonal foraging movements of lactating subantarctic fur seals from Marion Island , 2009 .

[26]  K. Hobson,et al.  Using stable isotopes of nitrogen and carbon to study seabird ecology: applications in the Mediterranean seabird community* , 2003 .

[27]  C. Bradshaw,et al.  Foraging ecology of a generalist predator the female New Zealand fur seal , 2002 .

[28]  V. Lesage,et al.  Spherical First Passage Time: A tool to investigate area-restricted search in three-dimensional movements , 2010 .

[29]  Torkild Tveraa,et al.  USING FIRST‐PASSAGE TIME IN THE ANALYSIS OF AREA‐RESTRICTED SEARCH AND HABITAT SELECTION , 2003 .

[30]  S. Goldsworthy,et al.  Dietary analysis of regurgitates and stomach samples from free-living Australian sea lions , 2006 .

[31]  B. Worton.  Kernel methods for estimating the utilization distribution in home-range studies , 1989 .

[32]  I. Nagelkerken,et al.  How important are mangroves and seagrass beds for coral-reef fish? The nursery hypothesis tested on an island scale , 2002 .

[33]  T. Loughlin,et al.  Deep genetic subdivision within a continuously distributed and highly vagile marine mammal, the Steller's sea lion (Eumetopias jubatus) , 2006, Molecular ecology.

[34]  C. Kendall,et al.  Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur , 2003 .

[35]  K. Hobson,et al.  Stable isotopes document seasonal changes in trophic niches and winter foraging individual specialization in diving predators from the Southern Ocean. , 2007, The Journal of animal ecology.

[36]  Jenkins,et al.  Evaluating the impact of predation by fish on the assemblage structure of fishes associated with seagrass (Heterozostera tasmanica) (Martens ex Ascherson) den Hartog, and unvegetated sand habitats. , 2000, Journal of experimental marine biology and ecology.

[37]  S. Goldsworthy,et al.  Effect of seasonal changes in upwelling activity on the foraging locations of a wide-ranging central-place forager, the New Zealand fur seal , 2008 .

[38]  D. Schell,et al.  Growth rates of vibrissae of harbor seals (Phoca vitulina) and Steller sea lions (Eumetopias jubatus) , 2001 .

[39]  Corey J A Bradshaw,et al.  Measurement error causes scale-dependent threshold erosion of biological signals in animal movement data. , 2007, Ecological applications : a publication of the Ecological Society of America.

[40]  I. Boyd,et al.  Comparing individual and spatial influences on foraging behaviour in Antarctic fur seals Arctocephalus gazella , 2004 .

[41]  Birgitte I. McDonald,et al.  Effects of maternal traits and individual behavior on the foraging strategies and provisioning rates of an income breeder, the Antarctic fur seal , 2009 .

[42]  A. Carlini,et al.  Geographical variation in the diet of the Antarctic fur seal Arctocephalus gazella , 2003, Polar Biology.

[43]  S. Garthe,et al.  Fine-scale foraging behaviour of a medium-ranging marine predator. , 2009, The Journal of animal ecology.

[44]  W. Karesh,et al.  Movements and location at sea of South American sea lions (Otaria flavescens) , 2001 .

[45]  C. Bost,et al.  Foraging behaviour of satellite-tracked king penguins in relation to sea-surface temperatures obtained by satellite telemetry at Crozet Archipelago, a study during three austral summers , 1997 .

[46]  D. Schneider.  Seabirds and fronts: a brief overview , 1990 .

[47]  G. Jenkins,et al.  The influence of habitat structure on nearshore fish assemblages in a southern Australian embayment: Comparison of shallow seagrass, reef-algal and unvegetated sand habitats, with emphasis on their importance to recruitment , 1998 .

[48]  J. Fryxell,et al.  Are there general mechanisms of animal home range behaviour? A review and prospects for future research. , 2008, Ecology letters.

[49]  David Pinaud,et al.  Quantifying search effort of moving animals at several spatial scales using first‐passage time analysis: effect of the structure of environment and tracking systems , 2007 .

[50]  W. J. Nichols,et al.  Satellite telemetry suggests high levels of fishing-induced mortality in marine turtles , 2003 .

[51]  Michael F. Sigler,et al.  Persistence of forage fish ‘hot spots’ and its association with foraging Steller sea lions (Eumetopias jubatus) in southeast Alaska , 2006 .

[52]  W. Sydeman,et al.  Spatio-temporal variability in prey harvest and reproductive ecology of a piscivorous seabird, Cerorhinca monocerata, in an upwelling system , 2007 .

[53]  M. Hindell,et al.  Foraging strategies of southern elephant seals (Mirounga leonina) in relation to frontal zones and water masses , 2001, Antarctic Science.

[54]  P. Nichols,et al.  Assessing the use of milk fatty acids to infer the diet of the Australian sea lion (Neophoca cinerea) , 2009 .

[55]  G. Box,et al.  On a measure of lack of fit in time series models , 1978 .

[56]  Pierre Fréon,et al.  Review of fish associative behaviour: Toward a generalisation of the meeting point hypothesis , 2000, Reviews in Fish Biology and Fisheries.

[57]  C. D. Duck,et al.  Foraging behaviour and diet of lactating female southern sea lions (Otaria flavescens) in the Falkland Islands , 1998 .

[58]  D. Olson,et al.  The concentrating of organisms at fronts: a cold-water fish and a warm-core Gulf Stream ring , 1985 .

[59]  Gwilym M. Jenkins,et al.  Time series analysis, forecasting and control , 1971 .

[60]  A. Lowther,et al.  Detecting alternate foraging ecotypes in Australian sea lion (Neophoca cinerea) colonies using stable isotope analysis , 2011 .

[61]  S. Votier,et al.  Inter-colony movements, at-sea behaviour and foraging in an immature seabird: results from GPS-PPT tracking, radio-tracking and stable isotope analysis , 2011 .

[62]  D. Costa,et al.  ENERGETICS OF A BENTHIC DIVER: SEASONAL FORAGING ECOLOGY OF THE AUSTRALIAN SEA LION, NEOPHOCA CINEREA , 2003 .

[63]  U. Ellenberg,et al.  Consistent foraging routes and benthic foraging behaviour in yellow-eyed penguins , 2007 .

[64]  J. Arnould,et al.  Stable isotopes reveal inter-annual and inter-individual variation in the diet of female Australian fur seals , 2011 .

[65]  N. Bax,et al.  A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen , 2002 .

[66]  Flavio Quintana,et al.  Diving behaviour and foraging location of female southern elephant seals from Patagonia , 1995 .

[67]  P. Boveng,et al.  Provisioning strategies of Antarctic fur seals and chinstrap penguins produce different responses to distribution of common prey and habitat , 2007 .

[68]  I. Newton,et al.  Ecologically justified charisma: preservation of top predators delivers biodiversity conservation , 2006 .

[69]  G. Antonelis,et al.  Diving patterns of California sea lions, Zalophus californianus , 1989 .

[70]  D. Simberloff,et al.  Ecological Specialization and Susceptibility to Disturbance: Conjectures and Refutations , 2002, The American Naturalist.

[71]  D. Costa,et al.  Behavioural estimation of blue whale movements in the Northeast Pacific from state-space model analysis of satellite tracks , 2009 .

[72]  R. Hedges,et al.  Isotopic Comparison of Hair and Bone: Archaeological Analyses , 1999 .

[73]  J. Arnould,et al.  Habitat selection by female Australian fur seals (Arctocephalus pusillus doriferus) , 2007 .

[74]  A. Trites.  Fetal growth of northern fur seals: life-history strategy and sources of variation , 1991 .

[75]  J. M. Burnsa,et al.  Fine-scale habitat selection of crabeater seals as determined by diving behavior , 2008 .

[76]  M. Hindell,et al.  Age and Reproductive Maturity of New Zealand Fur Seals (Arctocephalus forsteri) in Southern Australia , 2007 .

[77]  J. Hindell.  Assessing the trophic link between seagrass habitats and piscivorous fishes , 2006 .

[78]  S. Goldsworthy,et al.  Colony-specific foraging areas of lactating New Zealand fur seals , 2008 .

[79]  S. Goldsworthy,et al.  A risk-assessment approach to evaluating the significance of seal bycatch in two Australian fisheries , 2007 .

[80]  R. A. Campbell,et al.  Islands in the sea: extreme female natal site fidelity in the Australian sea lion, Neophoca cinerea , 2008, Biology Letters.

[81]  M. Mateo,et al.  Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies , 1996 .

[82]  M. Collins,et al.  Linking predator and prey behaviour: contrasts between Antarctic fur seals and macaroni penguins at South Georgia , 2010 .

[83]  L. Giraldeau,et al.  Experimental evidence for the maintenance of foraging specializations by frequency-dependent choice in flocks of spice finches , 1997 .

[84]  N. Gales,et al.  Estimating diet composition of the Australian sea lion (Neophoa cinerea) from scat analysis: an unrliable technique , 1992 .

[85]  I. Boyd,et al.  Distribution of foraging by female Antarctic fur seals , 2002 .

[86]  C. Campagna,et al.  Diving behaviour of lactating southern sea lions (Otaria flavescens) in Patagonia , 1995 .

[87]  Louie H. Yang,et al.  The Ecology of Individuals: Incidence and Implications of Individual Specialization , 2002, The American Naturalist.

[88]  P. Richard,et al.  Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals , 2009, Biology Letters.

[89]  B. McConnell,et al.  SMS seal: A new technique to measure haul-out behaviour in marine vertebrates , 2008 .

[90]  Bernie J. McConnell,et al.  Foraging ecology of southern elephant seals in relation to the bathymetry and productivity of the Southern Ocean , 1992, Antarctic Science.

[91]  M. Hindell,et al.  Dive behaviour, foraging locations, and maternal-attendance patterns of Australian fur seals (Arctocephalus pusillus doriferus) , 2001 .

[92]  N. Gemmell,et al.  Summer foraging areas for lactating New Zealand sea lions Phocarctos hookeri , 2005 .

[93]  I. Boyd,et al.  An energy–distance trade-off in a central-place forager, the Antarctic fur seal (Arctocephalus gazella) , 2007 .

[94]  R. Phillips,et al.  Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds , 2006 .

[95]  Daniel P Costa,et al.  Ontogeny of diving behaviour in the Australian sea lion: trials of adolescence in a late bloomer. , 2006, The Journal of animal ecology.

[96]  W. Montevecchi,et al.  The foraging decisions of a central place foraging seabird in response to fluctuations in local prey conditions , 2009 .

[97]  Bruce E. Lyon,et al.  Individual variation in prey selection by sea otters: patterns, causes and implications , 2003 .

[98]  D. Costa,et al.  Multiple foraging strategies in a marine apex predator, the Galapagos Sea Lion , 2008 .