Habitat preference, accessibility, and competition limit the global distribution of breeding Black-browed Albatrosses

Telemetry methods and remote sensing now make it possible to record the spatial usage of wide-ranging marine animals and the biophysical characteristics of their pelagic habitats. Furthermore, recent statistical advances mean that such data can be used to test ecological hypotheses and estimate species' distributions. Black-browed Albatrosses Thalassarche melanophrys are highly mobile marine predators with a circumpolar breeding and foraging distribution in the Southern Hemisphere. Although they remain relatively abundant, increased fisheries bycatch has led to their listing as endangered by conservation bodies. We satellite-tracked 163 breeding Black-browed Albatrosses and eight closely related Campbell Albatrosses T. impavida from nine colonies. We then quantified habitat usage, and modeled population-level spatial distribution at spatiotemporal scales >50 km and 1 month, as a function of habitat accessibility, habitat preference, and intraspecific competition, using mixed-effects generalized additive models (GAMM). During incubation, birds foraged over a wider area than in the post-brood chick-rearing period, when they are more time constrained. Throughout breeding, the order of habitat preference of Black-browed Albatrosses was for neritic (0-500 m), shelf-break and upper shelf-slope (500 1000 m), and then oceanic (>1000 m) waters. Black-browed Albatrosses also preferred areas with steeper (>3 degrees) bathymetric relief and, in addition, during incubation, warmer sea surface temperatures (peak preference similar to 16 degrees C). Although this suggests specialization in neritic habitats, incubation-stage Black-browed Albatrosses from South Georgia also foraged extensively in oceanic waters, preferring areas with high eddy kinetic energy (>250 cm(2)/s(2)), especially the Brazil-Malvinas Confluence, a region of intense mesoscale turbulence. During chick-rearing, this species had a more southerly distribution, and following the seasonal retreat of sea ice, birds from some populations utilized neritic polar waters. Campbell Albatrosses showed similar bathymetric preferences but also preferred positive sea level anomalies. Black-browed Albatross foraging areas were partially spatially segregated with respect to colony and region, with birds preferring locations distant from neighboring colonies, presumably in order to reduce competition between parapatric conspecifics. At the global scale, the greatest concentrations of breeding Black-browed Albatrosses are in southern South American neritic, shelf-break, and shelf-slope waters. These regions also hold large fisheries and should therefore be a priority for introduction of bycatch mitigation measures.

[1]  P. Heil,et al.  The pattern and variability of Antarctic sea-ice drift in the Indian Ocean and western Pacific sectors , 1999 .

[2]  G. Robertson,et al.  The Evangelistas Islets, Chile: a new breeding site for black-browed albatrosses , 2003, Polar Biology.

[3]  Matthew D. Johnson,et al.  MEASURING HABITAT QUALITY: A REVIEW , 2007 .

[4]  P. A. Prince,et al.  Food, feeding ecology and ecological segregation of seabirds at South Georgia , 1980 .

[5]  S. Iverson,et al.  Stable isotopes and fatty acid signatures reveal age- and stage-dependent foraging niches in tufted puffins , 2008 .

[6]  J. Le Fèvre,et al.  Aspects of the Biology of Frontal Systems , 1987 .

[7]  D. Gordon,et al.  Optimization, Conflict, and Nonoverlapping Foraging Ranges in Ants , 2003, The American Naturalist.

[8]  H. Weimerskirch,et al.  Foraging ranges and partitioning of feeding zones in three species of southern albatrosses , 1988 .

[9]  O. Ovaskainen,et al.  State-space models of individual animal movement. , 2008, Trends in ecology & evolution.

[10]  V. Afanasyev,et al.  SUMMER DISTRIBUTION AND MIGRATION OF NONBREEDING ALBATROSSES: INDIVIDUAL CONSISTENCIES AND IMPLICATIONS FOR CONSERVATION , 2005 .

[11]  Henri Weimerskirch,et al.  Are seabirds foraging for unpredictable resources , 2007 .

[12]  W. Tickell.  The Distribution of Black-browed and Grey-headed Albatrosses , 1976 .

[13]  R. Furness,et al.  Seabird colony distributions suggest competition for food supplies during the breeding season , 1984, Nature.

[14]  Bernie J. McConnell,et al.  ASSESSMENT OF ARGOS LOCATION ACCURACY FROM SATELLITE TAGS DEPLOYED ON CAPTIVE GRAY SEALS , 2002 .

[15]  M. Collins,et al.  Spatial and temporal operation of the Scotia Sea ecosystem: a review of large-scale links in a krill centred food web , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  H. Weimerskirch,et al.  Effect of environmental variability on habitat selection, diet, provisioning behaviour and chick growth in yellow-nosed albatrosses , 2005 .

[17]  Andrew P. Martin,et al.  Bumblebee flight distances in relation to the forage landscape. , 2008, The Journal of animal ecology.

[18]  Atle Mysterud,et al.  FUNCTIONAL RESPONSES IN HABITAT USE: AVAILABILITY INFLUENCES RELATIVE USE IN TRADE-OFF SITUATIONS , 1998 .

[19]  R. Kirkwood,et al.  Comparison of census methods for black-browed albatrosses breeding at the Ildefonso Archipelago, Chile , 2007, Polar Biology.

[20]  M. Austin.  Species distribution models and ecological theory: A critical assessment and some possible new approaches , 2007 .

[21]  R. H. Woodward,et al.  An Assessment of SeaWiFS and MODIS Ocean Coverage , 1998 .

[22]  L. Ballance,et al.  Response of seabirds to thermal boundaries in the tropical Pacific: the thermocline versus the Equatorial Front , 2001 .

[23]  Henri Weimerskirch,et al.  Scale‐dependent habitat use in a long‐ranging central place predator , 2005 .

[24]  S. Wanless,et al.  Spatial match–mismatch in the Benguela upwelling zone: should we expect chlorophyll and sea-surface temperature to predict marine predator distributions? , 2008 .

[25]  P. A. Prince,et al.  The foraging behaviour and energetics of wandering albatrosses brooding chicks , 1996, Antarctic Science.

[26]  H. Pulliam.  On the relationship between niche and distribution , 2000 .

[27]  W. Esaias,et al.  Annual cycles of phytoplankton chlorophyll concentrations in the global ocean: A satellite view , 1993 .

[28]  S. Wanless,et al.  Stage-dependent foraging in breeding black-legged kittiwakes Rissa tridactyla: distinguishing behavioural responses to intrinsic and extrinsic factors , 2006 .

[29]  H. Pulliam,et al.  Sources, Sinks, and Population Regulation , 1988, The American Naturalist.

[30]  D. Oro,et al.  Oceanographic habitat of an endangered Mediterranean procellariiform: implications for marine protected areas. , 2006, Ecological applications : a publication of the Ecological Society of America.

[31]  Mirtha Lewis,et al.  Southern elephant seal trajectories, fronts and eddies in the Brazil/Malvinas Confluence , 2006 .

[32]  P. Wilson,et al.  GEOGRAPHIC STRUCTURE OF ADÉLIE PENGUIN POPULATIONS: OVERLAP IN COLONY-SPECIFIC FORAGING AREAS , 2004 .

[33]  P. Fauchald,et al.  Foraging in a Hierarchical Patch System , 1999, The American Naturalist.

[34]  D. Costa,et al.  Fast and fuel efficient? Optimal use of wind by flying albatrosses , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  G. Marshall,et al.  Wind field and sex constrain the flight speeds of central‐place foraging albatrosses , 2009 .

[36]  H. Neil,et al.  Subantarctic oceanography around New Zealand: Preliminary results from an ongoing survey , 2001 .

[37]  D. Kramer,et al.  The effect of competitors and distance on central place foraging eastern chipmunks, Tamias striatus , 1994, Animal Behaviour.

[38]  S. Wanless,et al.  Spatial match-mismatch across four trophic levels of the Benguela upwelling zone during an ecosystem shift. , 2008 .

[39]  P. A. Prince,et al.  Quantifying habitat use in satellite-tracked pelagic seabirds : application of kernel estimation to albatross locations , 2000 .

[40]  J. Croxall,et al.  Interannual variation in the diets of two albatross species breeding at South Georgia: implications for breeding performance , 2003 .

[41]  S. Fretwell,et al.  On territorial behavior and other factors influencing habitat distribution in birds , 1969 .

[42]  D. K. Cairns,et al.  The Regulation of Seabird Colony Size: A Hinterland Model , 1989, The American Naturalist.

[43]  Scott A. Shaffer,et al.  Analytical approaches to investigating seabird-environment interactions: a review , 2009 .

[44]  B. McConnell,et al.  Movements and foraging areas of naïve, recently weaned southern elephant seal pups , 2002 .

[45]  H. Weimerskirch,et al.  Foraging and provisioning strategies of black-browed albatrosses in relation to the requirements of the chick: natural variation and experimental study , 1997 .

[46]  James G. Richman,et al.  Location and dynamics of the Antarctic Polar Front from satellite sea surface temperature data , 1999 .

[47]  C. Bock,et al.  Avian habitat evaluation: should counting birds count? , 2004 .

[48]  Satoru Taguchi,et al.  Primary production and standing crop of phytoplankton along the ice-edge in the Weddell Sea , 1981 .

[49]  A. Terauds,et al.  Foraging areas of black-browed and grey-headed albatrosses breeding on macquarie island in relation to marine protected areas , 2006 .

[50]  Douglas H. Johnson.  THE COMPARISON OF USAGE AND AVAILABILITY MEASUREMENTS FOR EVALUATING RESOURCE PREFERENCE , 1980 .

[51]  B. Raymond,et al.  Preferred foraging areas of Heard Island albatrosses during chick raising and implications for the management of incidental mortality in fisheries , 2008 .

[52]  P. A. Prince,et al.  The energy expenditure of free-ranging black-browed albatross , 1995 .

[53]  George L. Hunt,et al.  Foraging ecology of short-tailed shearwaters near the Pribilof Islands, Bering Sea , 1996 .

[54]  Luis Thayer.  Genetic affinities of newly sampled populations of Wandering and Black-browed Albatross , 2005 .

[55]  D. Costa,et al.  Foraging effort in relation to the constraints of reproduction in free‐ranging albatrosses , 2003 .

[56]  C. Ribic,et al.  Species-habitat relationships among Antarctic seabirds: a function of physical or biological factors? , 1993 .

[57]  S. Wood.  Stable and Efficient Multiple Smoothing Parameter Estimation for Generalized Additive Models , 2004 .

[58]  Pierre Jouventin,et al.  Foraging Strategy of Wandering Albatrosses Through The Breeding Season: A Study Using Satellite Telemetry , 1993 .

[59]  Timothy J. Smyth,et al.  Movements of migrating green turtles in relation to AVHRR derived sea surface temperature , 2001 .

[60]  R. Phillips,et al.  Status and distribution of wandering, black-browed and grey-headed albatrosses breeding at South Georgia , 2006, Polar Biology.

[61]  G. Beauchamp,et al.  Time and energy constraints and the relationships between currencies in foraging theory , 1994 .

[62]  L. Ballance,et al.  Oceanographic influences on seabirds and cetaceans of the eastern tropical Pacific: A review , 2006 .

[63]  R. Hucke‐Gaete,et al.  Artisanal longline fisheries in Southern Chile: Lessons to be learned to avoid incidental seabird mortality , 2006 .

[64]  Joel s. Brown,et al.  A guide to central place effects in foraging. , 2008, Theoretical population biology.

[65]  J. Croxall,et al.  Global relationships amongst black‐browed and grey‐headed albatrosses: analysis of population structure using mitochondrial DNA and microsatellites , 2001, Molecular ecology.

[66]  R. Phillips,et al.  Seasonal sexual segregation in two Thalassarche albatross species: competitive exclusion, reproductive role specialization or foraging niche divergence? , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  D. Irons,et al.  PREY RESOURCES, COMPETITION, AND GEOGRAPHIC STRUCTURE OF KITTIWAKE COLONIES IN PRINCE WILLIAM SOUND , 2003 .

[68]  P. Ryan,et al.  Exploitation of mesoscale oceanographic features by grey-headed albatross Thalassarche chrysostoma in the southern Indian Ocean , 2001 .

[69]  Greg A Breed,et al.  Sex-specific, seasonal foraging tactics of adult grey seals (Halichoerus grypus) revealed by state-space analysis. , 2009, Ecology.

[70]  Scarla J. Weeks,et al.  Offshore diplomacy, or how seabirds mitigate intra-specific competition: a case study based on GPS tracking of Cape gannets from neighbouring colonies , 2004 .

[71]  J. Croxall,et al.  Interannual variations in cephalopod consumption by albatrosses at South Georgia: implications for future commercial exploitation of cephalopods , 2007 .

[72]  H. Weimerskirch,et al.  Ultimate and proximate factors affecting the breeding performance of a marine top-predator , 2002 .

[73]  John P. Croxall,et al.  EFFECTS OF SATELLITE TRANSMITTERS ON ALBATROSSES AND PETRELS , 2003 .

[74]  Gilles Reverdin,et al.  Global high-resolution mapping of ocean circulation from TOPEX/Poseidon and ERS-1 and -2 , 2000 .

[75]  Antoine Guisan,et al.  Predictive habitat distribution models in ecology , 2000 .

[76]  A. Hedenström,et al.  OPTIMAL FLIGHT SPEED OF BIRDS , 1995 .

[77]  Michael L. Morrison,et al.  The habitat concept and a plea for standard terminology , 1997 .

[78]  C. Bost,et al.  Foraging strategies of incubating and brooding king penguins Aptenodytes patagonicus , 1998, Oecologia.

[79]  Á. Felicísimo,et al.  Ocean Surface Winds Drive Dynamics of Transoceanic Aerial Movements , 2008, PloS one.

[80]  Bernie J. McConnell,et al.  Estimating space‐use and habitat preference from wildlife telemetry data , 2008 .

[81]  P. A. Prince,et al.  Exploitation of the marine environment by two sympatric albatrosses in the Pacific Southern Ocean , 1999 .

[82]  Laurent Dubroca,et al.  Spatial distribution of foraging in female Antarctic fur seals Arctocephalus gazella in relation to oceanographic variables: a scale-dependent approach using geographic information systems , 2001 .

[83]  G. Pierce,et al.  Remotely sensed mesoscale oceanography and the distribution of Illex argentinus in the South Atlantic , 2001 .

[84]  K. R. Thompson.  Quantitative analysis of the use of discards from squid trawlers by Black‐browed Albatrosses Diomedea melanophris in the vicinity of the Falkland Islands , 2008 .

[85]  R. Phillips,et al.  Quantifying habitat use and preferences of pelagic seabirds using individual movement data: a review , 2009 .

[86]  K. Hyrenbach,et al.  Oceanographic habitats of two sympatric North Pacific albatrosses during the breeding season , 2002 .

[87]  P. Moore.  Abundance and population trends of mollymawks on Campbell Island , 2004 .

[88]  Michael P. Meredith,et al.  Antarctic Circumpolar Current frontal system in the South Atlantic: Monitoring using merged Argo and animal-borne sensor data , 2008 .

[89]  D. Simberloff.  The Guild Concept and the Structure of Ecological Communities , 1991 .

[90]  Hermes Mianzan,et al.  Marine fronts at the continental shelves of austral South America: Physical and ecological processes , 2004 .

[91]  H. Higuchi,et al.  Foraging activity and submesoscale habitat use of waved albatrosses Phoebastria irrorata during chick-brooding period , 2005 .

[92]  P. A. Prince,et al.  Dead or alive, night or day: how do albatrosses catch squid? , 1994, Antarctic Science.

[93]  S. Wanless,et al.  Evidence of intra-specific competition for food in a pelagic seabird , 2001, Nature.

[94]  Rory P. Wilson,et al.  Black-browed albatrosses, international fisheries and the Patagonian Shelf , 2000 .

[95]  R. Gray,et al.  Can ecological theory predict the distribution of foraging animals? A critical analysis of experiments on the ideal free distribution , 1993 .

[96]  Guillermo Blanco,et al.  CONSPECIFIC FOOD COMPETITION EXPLAINS VARIABILITY IN COLONY SIZE: A TEST IN MAGELLANIC PENGUINS , 2002 .

[97]  N. Ashmole.  THE REGULATION OF NUMBERS OF TROPICAL OCEANIC BIRDS , 2008 .

[98]  Thomas M. Smith,et al.  An Improved In Situ and Satellite SST Analysis for Climate , 2002 .

[99]  L. Bugoni,et al.  Seabird mortality on factory trawlers in the Falkland Islands and beyond , 2006 .

[100]  L. Underhill,et al.  Albatross overlap with fisheries in the Benguela Upwelling System: implications for conservation and management , 2008 .

[101]  N. Huin.  Foraging distribution of the black-browed albatross, Thalassarche melanophris, breeding in the Falkland Islands , 2002 .

[102]  H. Higuchi,et al.  Foraging of royal albatrosses, Diomedea epomophora, from the Otago Peninsula and its relationships to fisheries , 2005 .

[103]  Henri Weimerskirch,et al.  At-sea distribution and scale-dependent foraging behaviour of petrels and albatrosses: a comparative study. , 2007, The Journal of animal ecology.

[104]  D. Gordon,et al.  How resources and encounters affect the distribution of foraging activity in a seed-harvesting ant , 2000, Behavioral Ecology and Sociobiology.

[105]  M. Boyce,et al.  Evaluating resource selection functions , 2002 .

[106]  H. Weimerskirch,et al.  Dietary evidence for spatial foraging segregation in sympatric albatrosses (Diomedea spp.) rearing chicks at Iles Nuageuses, Kerguelen , 2002 .

[107]  C. J. Thomas,et al.  The spatial distribution and size of rook (Corvus frugilegus) breeding colonies is affected by both the distribution of foraging habitat and by intercolony competition , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[108]  A distance-dependent estimation of foraging ranges of neighbouring bird colonies , 2005 .

[109]  B. V. Horne,et al.  DENSITY AS A MISLEADING INDICATOR OF HABITAT QUALITY , 1983 .

[110]  Jason Matthiopoulos,et al.  The use of space by animals as a function of accessibility and preference , 2003 .

[111]  M. Hindell,et al.  Colony-based foraging segregation by Antarctic fur seals at the Kerguelen Archipelago , 2008 .

[112]  K. Hyrenbach,et al.  Albatross response to survey vessels: implications for studies of the distribution, abundance, and prey consumption of seabird populations , 2001 .