Shadowed by scale: subtle behavioral niche partitioning in two sympatric, tropical breeding albatross species

BackgroundTo meet the minimum energetic requirements needed to support parents and their provisioned offspring, the timing of breeding in birds typically coincides with periods of high food abundance. Seasonality and synchrony of the reproductive cycle is especially important for marine species that breed in high latitudes with seasonal booms in ocean productivity. Laysan and black-footed albatrosses breeding in the northwestern Hawaiian Islands have a dual reliance on both seasonally productive waters of high latitudes and on nutrient-poor waters of low latitudes, because their foraging ranges contract during the short but critical brood-guard stage. Therefore, these species face an additional constraint of having to negotiate nutrient-poor waters during the most energetically-demanding stage of the breeding cycle. This constriction of foraging range likely results in a higher density of foraging competitors. Thus, our aim was to understand how Hawaiian albatross partition resources both between and within species in this highly constrained breeding stage while foraging in less productive waters and simultaneously experiencing increased competition. High-precision GPS dataloggers were deployed on black-footed (Phoebastria nigripes, n=20) and Laysan (Phoebastria immutabilis, n=18) albatrosses during the brood-guard stage of the breeding season in 2006 (n=8), 2009 (n=13), 2010 (n=16) and 2012 (n=1). We used GPS data and movement analyses to identify six different behavioral states in foraging albatrosses that we then used to characterize foraging trips across individuals and species. We examined whether variations in behavior were correlated with both intrinsic factors (sex, body size, body condition) and extrinsic factors (lunar phase, wind speed, year).ResultsBehavioral partitioning was revealed both between and within species in Hawaiian albatrosses. Both species were highly active during chick-brooding trips and foraged across day and night; however, Laysan albatrosses relied on foraging at night to a greater extent than black-footed albatrosses and exhibited different foraging patterns at night. For both species, foraging along direct flight paths and foraging on the water in a “sit-and-wait” strategy were just as prevalent as foraging in a searching flight mode, indicating flexibility in foraging strategies in Hawaiian albatross. Both species strongly increased drift forage at night when the lunar phase was the darkest, suggesting Hawaiian albatross feed on diel vertically-migrating prey to some extent. Black-footed albatrosses showed greater variation in foraging behavior between individuals which suggests a higher level of intra-specific competition. This behavioral variability in black-footed albatrosses was not correlated with sex or body size, but differences in body condition suggested varying efficiencies among foraging patterns. Behavioral variability in Laysan albatrosses was correlated with sex, such that females exhibited greater flight foraging than drift foraging, had longer trip durations and flew farther maximum distances from the breeding colony, but with no difference in body condition.ConclusionFine-scale movement data and an analysis of multiple behavioral states identified behavioral mechanisms that facilitate coexistence within a community of albatross during a critical life-history period when energetic demands are high, resources are limited, and competition for food is greatest.

[1]  H. Fritz,et al.  Scale–dependent hierarchical adjustments of movement patterns in a long–range foraging seabird , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  S. Wanless,et al.  Sex‐specific food provisioning in a monomorphic seabird, the common guillemot Uria aalge: nest defence, foraging efficiency or parental effort? , 2009 .

[3]  Daniel P. Costa,et al.  Fractal landscape method: an alternative approach to measuring area-restricted searching behavior , 2007, Journal of Experimental Biology.

[4]  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 .

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

[6]  J. Croxall,et al.  Sexual dimorphism and sexual segregation in foraging strategies of northern giant petrels, Macronectes halli, during incubation , 2000 .

[7]  S. Garthe,et al.  Sex-specific foraging behaviour in northern gannets Morus bassanus: incidence and implications , 2012 .

[8]  Hidetoshi Shimodaira,et al.  Pvclust: an R package for assessing the uncertainty in hierarchical clustering , 2006, Bioinform..

[9]  J. Granadeiro,et al.  Working the day or the night shift? Foraging schedules of Cory's shearwaters vary according to marine habitat , 2012 .

[10]  Nova Scotia The VFractal: a new estimator for fractal dimension of animal movement paths , 1996 .

[11]  K. R. Clarke,et al.  Non‐parametric multivariate analyses of changes in community structure , 1993 .

[12]  A. Harding,et al.  Foraging Responses of Black-Legged Kittiwakes to Prolonged Food-Shortages around Colonies on the Bering Sea Shelf , 2014, PloS one.

[13]  Christopher M. Perrins,et al.  THE TIMING OF BIRDS‘ BREEDING SEASONS , 2008 .

[14]  W. Montevecchi,et al.  Fishing in the Dark: A Pursuit-Diving Seabird Modifies Foraging Behaviour in Response to Nocturnal Light Levels , 2011, PloS one.

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

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

[17]  D. Lack,et al.  Ecological adaptations for breeding in birds , 1969 .

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

[19]  L. Ballance,et al.  SEABIRD COMMUNITY STRUCTURE ALONG A PRODUCTIVITY GRADIENT: IMPORTANCE OF COMPETITION AND ENERGETIC CONSTRAINT , 1997 .

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

[21]  J. Creech Internet Reviews: IUCN Red List of Threatened Species , 2014 .

[22]  D. Bolnick,et al.  Using delta13C stable isotopes to quantify individual-level diet variation. , 2007, Oecologia.

[23]  R. Phillips,et al.  Post-migratory body condition and ovarian steroid production predict breeding decisions 1 by female gray-headed albatrosses . 2 3 4 , 2013 .

[24]  J. Haney Seabird patchiness in tropical oceanic waters: the influence of Sargassum reefs , 1986 .

[25]  L. Ballance,et al.  S34.4: Foraging ecology of tropical seabirds , 1999 .

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

[27]  D. Costa,et al.  Latitudinal Range Influences the Seasonal Variation in the Foraging Behavior of Marine Top Predators , 2011, PloS one.

[28]  K. Yoda,et al.  Patterns of GPS Tracks Suggest Nocturnal Foraging by Incubating Peruvian Pelicans (Pelecanus thagus) , 2011, PloS one.

[29]  Joanna Burger,et al.  Biology of marine birds , 2001 .

[30]  A. Lescroël,et al.  Working less to gain more: when breeding quality relates to foraging efficiency. , 2010, Ecology.

[31]  R. Suryan,et al.  Post-breeding season distribution of black-footed and Laysan albatrosses satellite-tagged in Alaska: inter-specific differences in spatial overlap with North Pacific fisheries. , 2009 .

[32]  P. D. Abel,et al.  Ecotoxicology and the marine environment , 1991 .

[33]  Márcio S. Araújo,et al.  Using δ13C stable isotopes to quantify individual-level diet variation , 2007, Oecologia.

[34]  A. M. Kaufman,et al.  Variation in Energy Expenditure among Black‐Legged Kittiwakes: Effects of Activity‐Specific Metabolic Rates and Activity Budgets , 2003, Physiological and Biochemical Zoology.

[35]  G. Polis Age Structure Component of Niche Width and Intraspecific Resource Partitioning: Can Age Groups Function as Ecological Species? , 1984, The American Naturalist.

[36]  D. Mackas,et al.  The seasonal cycle revisited: interannual variation and ecosystem consequences , 2001 .

[37]  R. Mundry,et al.  Diving seabirds share foraging space and time within and among species , 2010 .

[38]  M. Begon,et al.  Ecology: From Individuals to Ecosystems , 2005 .

[39]  Ronald K. Pearson,et al.  Mining imperfect data - dealing with contamination and incomplete records , 2005 .

[40]  G. Boehlert,et al.  A Review of the Effects of Seamounts on Biological Processes , 2013 .

[41]  Patricia Fernández,et al.  Foraging destinations of three low‐latitude albatross (Phoebastria) species , 2001 .

[42]  O. Pizarro,et al.  Global climatology of near‐inertial current characteristics from Lagrangian observations , 2008 .

[43]  Michel Potier,et al.  Foraging strategy of a top predator in tropical waters: great frigatebirds in the Mozambique Channel , 2004 .

[44]  Chao Qian,et al.  Population , 1940, State Rankings 2020: A Statistical View of America.

[45]  R. Furness,et al.  REPRODUCTIVE CONSEQUENCES FOR GREAT SKUAS SPECIALIZING AS SEABIRD PREDATORS , 2004 .

[46]  Vsevolod Afanasyev,et al.  At–Sea Behavior Varies with Lunar Phase in a Nocturnal Pelagic Seabird, the Swallow-Tailed Gull , 2013, PloS one.

[47]  Scott A. Shaffer,et al.  Wind, Waves, and Wing Loading: Morphological Specialization May Limit Range Expansion of Endangered Albatrosses , 2008, PloS one.

[48]  M. Sokolowski,et al.  Evolution of foraging behavior in Drosophila by density-dependent selection. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Scott T. Walter,et al.  Factors influencing Brown Pelican (Pelecanus occidentalis) foraging movement patterns during the breeding season , 2014 .

[50]  W. Montevecchi,et al.  Seasonal Sexual Segregation by Monomorphic Sooty Shearwaters Puffinus griseus Reflects Different Reproductive Roles during the Pre-Laying Period , 2014, PloS one.

[51]  K. Kenyon,et al.  Breeding Cycles and Behavior of Laysan and Black-Footed Albatrosses , 1962 .

[52]  W. Montevecchi,et al.  Ashmole's halo : direct evidence for prey depletion by a seabird , 1987 .

[53]  Márcio S Araújo,et al.  The ecological causes of individual specialisation. , 2011, Ecology letters.

[54]  Frederic Bartumeus,et al.  Coupling instantaneous energy-budget models and behavioural mode analysis to estimate optimal foraging strategy: an example with wandering albatrosses , 2014, Movement ecology.

[55]  T. Hothorn,et al.  Simultaneous Inference in General Parametric Models , 2008, Biometrical journal. Biometrische Zeitschrift.

[56]  R. Macarthur,et al.  Population Ecology of Some Warblers of Northeastern Coniferous Forests , 1958 .

[57]  Douglas Nychka,et al.  Bayesian Confidence Intervals for Smoothing Splines , 1988 .

[58]  D. Costa,et al.  Functional significance of sexual dimorphism in wandering albatrosses, Diomedea exulans , 2001 .

[59]  John L. Harper,et al.  Ecology: from individuals to ecosystems. 4th edition , 2006 .

[60]  G. Odell,et al.  Swarms of Predators Exhibit "Preytaxis" if Individual Predators Use Area-Restricted Search , 1987, The American Naturalist.

[61]  Olivier Gimenez,et al.  Quantifying the impact of longline fisheries on adult survival in the black‐footed albatross , 2007 .

[62]  V. Afanasyev,et al.  Foraging behaviour of four albatross species by night and day , 2007 .

[63]  D. Roby,et al.  Diet Composition, Reproductive Energetics, and Productivity of Seabirds Damaged by the Exxon Valdez Oil Spill , 1998 .

[64]  H. Weimerskirch,et al.  Personality, Foraging and Fitness Consequences in a Long Lived Seabird , 2014, PloS one.

[65]  R. Phillips,et al.  Sex-specific foraging strategies throughout the breeding season in a tropical, sexually monomorphic small petrel , 2012, Animal Behaviour.

[66]  Scott A. Shaffer,et al.  Hawaiian albatrosses track interannual variability of marine habitats in the North Pacific , 2010 .

[67]  W. Walker,et al.  POPULATION STATUS, FOODS AND FORAGING OF LAYSAN ALBATROSSES PHOEBASTRIA IMMUTABILIS NESTING ON GUADALUPE ISLAND, MEXICO , 2004 .

[68]  H. Weimerskirch,et al.  Consistency pays: sex differences and fitness consequences of behavioural specialization in a wide-ranging seabird , 2014, Biology Letters.

[69]  Y. Ropert‐Coudert,et al.  Sex-specific foraging behaviour in a seabird with reversed sexual dimorphism: the red-footed booby , 2005, Oecologia.

[70]  H. Weimerskirch,et al.  Evidence for olfactory search in wandering albatross, Diomedea exulans , 2008, Proceedings of the National Academy of Sciences.

[71]  I. Jonsen,et al.  Daily activity budgets reveal a quasi-flightless stage during non-breeding in Hawaiian albatrosses , 2014, Movement ecology.

[72]  S. Wanless,et al.  Space Partitioning Without Territoriality in Gannets , 2013, Science.

[73]  W. Montevecchi,et al.  Activity Budgets and Foraging Ranges of Breeding Common Murres , 1987 .

[74]  C. Harrison Seabirds of Hawaii: Natural History and Conservation , 1990 .

[75]  D. Costa,et al.  Same size--same niche? Foraging niche separation between sympatric juvenile Galapagos sea lions and adult Galapagos fur seals. , 2013, The Journal of animal ecology.

[76]  L. Crowder,et al.  ESTIMATING FISHERY BYCATCH AND EFFECTS ON A VULNERABLE SEABIRD POPULATION , 2003 .

[77]  Henri Weimerskirch,et al.  Top marine predators track Lagrangian coherent structures , 2009, Proceedings of the National Academy of Sciences.

[78]  J. Drazen,et al.  Micronekton abundance and biomass in Hawaiian waters as influenced by seamounts, eddies, and the moon , 2011 .

[79]  Simon Benhamou,et al.  Animal movements in heterogeneous landscapes: identifying profitable places and homogeneous movement bouts. , 2008, Ecology.

[80]  R. Ricklefs Comparative Avian Demography , 1983 .

[81]  Henri Weimerskirch,et al.  Does Prey Capture Induce Area‐Restricted Search? A Fine‐Scale Study Using GPS in a Marine Predator, the Wandering Albatross , 2007, The American Naturalist.

[82]  R. Schreiber,et al.  SEA‐BIRD BREEDING SEASONS ON CHRISTMAS ISLAND, PACIFIC OCEAN* , 2008 .

[83]  P. Sievert,et al.  Status Assessment of Laysan and Black-Footed Albatrosses, North Pacific Ocean, 1923-2005 , 2009 .

[84]  Robert R. Bidigare,et al.  Biological enhancement at cyclonic eddies tracked with GOES Thermal Imagery in Hawaiian waters , 2001 .

[85]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[86]  T. E. Martin Food as a limit on breeding birds: a life-history perspective , 1987 .

[87]  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.

[88]  D. J. Anderson,et al.  NOCTURNAL AND DIURNAL FORAGING ACTIVITY OF HAWAIIAN ALBATROSSES DETECTED WITH A NEW IMMERSION MONITOR , 2000 .

[89]  Y. Watanuki Individual diet difference, parental care and reproductive success in slaty-backed gulls , 1992 .

[90]  M. Corre Breeding seasons of seabirds at Europa Island (southern Mozambique Channel) in relation to seasonal changes in the marine environment , 2001 .

[91]  Daniel I Bolnick,et al.  Intraspecific competition drives increased resource use diversity within a natural population , 2007, Proceedings of the Royal Society B: Biological Sciences.

[92]  Nicolas Mouquet,et al.  Mechanisms of Coexistence in Competitive Metacommunities , 2004, The American Naturalist.

[93]  S. Wanless,et al.  Sex-specific foraging behaviour in a monomorphic seabird , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[94]  J. Haney Seabird affinities for Gulf Stream frontal eddies: Responses of mobile marine consumers to episodic upwelling , 1986 .

[95]  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.

[96]  Rory P. Wilson,et al.  When three per cent may not be three per cent; device-equipped seabirds experience variable flight constraints , 2012 .

[97]  R. Drent,et al.  The Prudent Parent: Energetic Adjustments in Avian Breeding 1) , 1980 .

[98]  I. Owens,et al.  Ancient ecological diversification explains life-history variation among living birds , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[99]  H. Weimerskirch,et al.  INFLUENCE OF BODY CONDITION ON REPRODUCTIVE DECISION AND REPRODUCTIVE SUCCESS IN THE BLUE PETREL , 1995 .

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

[101]  S. Stearns,et al.  The Evolution of Life Histories , 1992 .

[102]  S. Bograd,et al.  Observations of seamount‐attached eddies in the North Pacific , 1997 .

[103]  R. Phillips,et al.  Foraging strategies of grey-headed albatrosses Thalassarche chrysostoma: integration of movements, activity and feeding events , 2004 .

[104]  H. Weimerskirch,et al.  Seasonal changes in the provisioning behaviour and mass of male and female wandering albatrosses in relation to the growth of their chick , 2000, Polar Biology.

[105]  M. Harris Breeding seasons of sea‐birds in the Galapagos Islands , 2009 .

[106]  S. Wood Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models , 2011 .

[107]  M Tim Tinker,et al.  Food limitation leads to behavioral diversification and dietary specialization in sea otters , 2008, Proceedings of the National Academy of Sciences.

[108]  R. Furness,et al.  2 3 At-sea activity patterns of breeding and nonbreeding white-chinned petrels 4 Procellaria aequinoctialis from South Georgia , 2010 .