Fortuitous Encounters between Seagliders and Adult Female Northern Fur Seals (Callorhinus ursinus) off the Washington (USA) Coast: Upper Ocean Variability and Links to Top Predator Behavior

Behavioral responses by top marine predators to oceanographic features such as eddies, river plumes, storms, and coastal topography suggest that biophysical interactions in these zones affect predators' prey, foraging behaviors, and potentially fitness. However, examining these pathways is challenged by the obstacles inherent in obtaining simultaneous observations of surface and subsurface environmental fields and predator behavior. In this study, migratory movements and, in some cases, diving behavior of 40 adult female northern fur seals (NFS; Callorhinus ursinus) were quantified across their range and compared to remotely-sensed environmental data in the Gulf of Alaska and California Current ecosystems, with a particular focus off the coast of Washington State (USA) – a known foraging ground for adult female NFS and where autonomous glider sampling allowed opportunistic comparison of seal behavior to subsurface biophysical measurements. The results show that in these ecosystems, adult female habitat utilization was concentrated near prominent coastal topographic, riverine, or inlet features and within 200 km of the continental shelf break. Seal dive depths, in most ecosystems, were moderated by surface light level (solar or lunar), mirroring known behaviors of diel vertically-migrating prey. However, seal dives differed in the California Current ecosystem due to a shift to more daytime diving concentrated at or below the surface mixed layer base. Seal movement models indicate behavioral responses to season, ecosystem, and surface wind speeds; individuals also responded to mesoscale eddies, jets, and the Columbia River plume. Foraging within small scale surface features is consistent with utilization of the inner coastal transition zone and habitats near coastal capes, which are known eddy and filament generation sites. These results contribute to our knowledge of NFS migratory patterns by demonstrating surface and subsurface behavioral responses to a spatially and temporally dynamic ocean environment, thus reflecting its influence on associated NFS prey species.

[1]  R. Davis,et al.  Mixing in the Transition Layer during Two Storm Events , 2011 .

[2]  Nicholas A. Bond,et al.  The Sun, Moon, Wind, and Biological Imperative–Shaping Contrasting Wintertime Migration and Foraging Strategies of Adult Male and Female Northern Fur Seals (Callorhinus ursinus) , 2014, PloS one.

[3]  A. Trites,et al.  Broad thermal capacity facilitates the primarily pelagic existence of northern fur seals (Callorhinus ursinus) , 2014 .

[4]  P. Strub,et al.  Altimeter-derived variability of surface velocities in the California Current System: 2. Seasonal circulation and eddy statistics , 2000 .

[5]  R. Towell,et al.  DECLINE IN NORTHERN FUR SEAL (CALLORHINUS URSINUS) PUP PRODUCTION ON THE PRIBILOF ISLANDS , 2006 .

[6]  B. Worton Using Monte Carlo simulation to evaluate kernel-based home range estimators , 1995 .

[7]  Carey E Kuhn,et al.  Evidence of localized resource depletion following a natural colonization event by a large marine predator. , 2014, The Journal of animal ecology.

[8]  R. Brodeur,et al.  Association of predators and prey at frontal features in the California Current: competition, facilitation, and co-occurrence , 2009 .

[9]  Mary Jane Perry,et al.  Seaglider observations of variability in daytime fluorescence quenching of chlorophyll-a in Northeastern Pacific coastal waters , 2008 .

[10]  David M. Checkley,et al.  Patterns and processes in the California Current System , 2009 .

[11]  J. Haney,et al.  AGGREGATIONS OF CORY'S SHEARWATERS (CALONECTRIS DIOMEDEA) AT GULF STREAM FRONTS , 1985 .

[12]  Dynamics of Large Mammal Populations , 1983 .

[13]  Daniele Iudicone,et al.  Mixed layer depth over the global ocean: An examination of profile data and a profile-based climatology , 2004 .

[14]  D. Costa,et al.  Chapter 15. Synthesis and Conclusions , 1986 .

[15]  F. Chavez,et al.  The California Current system off Monterey, California: physical and biological coupling , 2003 .

[16]  R. Schusterman,et al.  AERIAL AND UNDERWATER VISUAL ACUITY IN THE CALIFORNIA SEA LION (ZALOPHUS CALIFORNIANUS) AS A FUNCTION OF LUMINANCE * , 1971, Annals of the New York Academy of Sciences.

[17]  H. Freeland,et al.  An examination of historical mixed layer depths along Line P in the Gulf of Alaska , 2005 .

[18]  J. Packard Fur Seals: Maternal Strategies on Land and at Sea, R.L. Gentry, G.L. Kooyman (Eds.). Princeton University Press, Princeton (1986), xviii , 1987 .

[19]  B. Sackmann Remote Assessment of 4-D Phytoplankton Distributions off the Washington Coast , 2007 .

[20]  Boris Dewitte,et al.  Eddy activity in the four major upwelling systems from satellite altimetry (1992-2007) , 2009 .

[21]  W. C. Leggett,et al.  Bias in Hydroacoustic Estimates of Fish Abundance due to Acoustic Shadowing: Evidence from Day–Night Surveys of Vertically Migrating Fish , 1992 .

[22]  Mary-Anne Lea,et al.  Extreme weather events influence dispersal of naive northern fur seals , 2009, Biology Letters.

[23]  G. Kooyman,et al.  Chapter 4. Feeding and Diving Behavior of Northern Fur Seals , 1986 .

[24]  M. Bigg ARRIVAL OF NORTHERN FUR SEALS, CALWRHINUS URSINUS, ON S'I PAUL ISLAND, ALASKA , 1986 .

[25]  F. Trillmich,et al.  The Effects of El Niño on Galapagos Pinnipeds , 1991 .

[26]  J. Baker Post-weaning migration of northern fur seal Callorhinus ursinus pups from the Pribilof Islands, Alaska , 2007 .

[27]  M. Ashton,et al.  Synthesis and Conclusions , 2012 .

[28]  K. Sherman,et al.  The Large Marine Ecosystem Concept: Research and Management Strategy for Living Marine Resources. , 1991, Ecological applications : a publication of the Ecological Society of America.

[29]  J. Paduan,et al.  Structure of Velocity and Temperature in the Northeast Pacific as Measured with Lagrangian Drifters in Fall 1987 , 1993 .

[30]  C. C. Eriksen,et al.  Seaglider: a long-range autonomous underwater vehicle for oceanographic research , 2001 .

[31]  Brian C. Battaile,et al.  Foraging habitats of lactating northern fur seals are structured by thermocline depths and submesoscale fronts in the eastern Bering Sea , 2013 .

[32]  C. Ladd Interannual variability of the Gulf of Alaska eddy field , 2007 .

[33]  Patrick F. Cummins,et al.  Argo : A new tool for environmental monitoring and assessment of the world's oceans, an example from the N. E. Pacific , 2005 .

[34]  Ian D. Jonsen,et al.  ROBUST STATE-SPACE MODELING OF ANIMAL MOVEMENT DATA , 2005 .

[35]  P. Stabeno,et al.  Observations from a Yakutat eddy in the northern Gulf of Alaska , 2005 .

[36]  Tony R. Walker,et al.  Dispersal of male and female Antarctic fur seals (Arctocephalus gazella) , 1998 .

[37]  A. Mahadevan,et al.  Comment on "Eddy/Wind Interactions Stimulate Extraordinary Mid-Ocean Plankton Blooms" , 2008, Science.

[38]  G. Antonelis,et al.  Impact of the 1982-1983 el niño on the northern fur seal population at San Miguel Island, California , 1991 .

[39]  W. Large,et al.  Upper Ocean Thermal Response to Strong Autumnal Forcing of the Northeast Pacific , 1986 .

[40]  James C. McWilliams,et al.  Eddy properties in the California Current System , 2011 .

[41]  L. Washburn,et al.  Patterns of coastal eddy circulation and abundance of pelagic juvenile fish in the Santa Barbara Channel, California, USA , 2002 .

[42]  P. Stabeno,et al.  Dynamics of the Bering Sea , 1999 .

[43]  P. Harrison,et al.  Physical processes that enhance nutrient transport and primary productivity in the coastal and open ocean of the subarctic NE Pacific , 2005 .

[44]  D. Mackas,et al.  Zooplankton distribution and dynamics in a North Pacific Eddy of coastal origin: II. Mechanisms of eddy colonization by and retention of offshore species , 2005 .

[45]  J. Koslow,et al.  Abundance and community composition of micronekton across a front off Southern California , 2012 .

[46]  A. Trites,et al.  Physical growth of northern fur seals (Callorhinus ursinus): seasonal fluctuations and migratory influences , 1996 .

[47]  R. Merrick,et al.  Diving behavior of immature Steller sea lions (Eumetopias jubatus) , 2003 .

[48]  B. Hickey,et al.  Influences of the Juan de Fuca Eddy on circulation, nutrients, and phytoplankton production in the northern California Current System , 2008 .

[49]  Andrew C. Thomas,et al.  A census of oceanic anticyclonic eddies in the Gulf of Alaska , 2008 .

[50]  Ian D. Jonsen,et al.  META‐ANALYSIS OF ANIMAL MOVEMENT USING STATE‐SPACE MODELS , 2003 .

[51]  T. Weingartner,et al.  Satellite and hydrographic observations of eddy‐induced shelf‐slope exchange in the northwestern Gulf of Alaska , 2003 .

[52]  T. Loughlin,et al.  Diving Patterns and Foraging Locations of Female Northern Fur Seals , 2008 .

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

[54]  E. Sinclair Fur seal investigations, 1992 , 1992 .

[55]  C. Simenstad,et al.  Nearshore fish and macroinvertebrate assemblages along the Strait of Juan de Fuca including food habits of the common nearshore fish , 1980 .

[56]  J. Baker,et al.  Relative influence of climate variability and direct anthropogenic impact on a sub-tropical Pacific top predator, the Hawaiian monk seal , 2012 .

[57]  B. Efron,et al.  Bootstrap confidence intervals , 1996 .

[58]  Giulio Boccaletti,et al.  Mixed Layer Instabilities and Restratification , 2007 .

[59]  B. Hickey,et al.  Influence of wind stress and ambient flow on a high discharge river plume , 2002 .

[60]  F. Trillmich,et al.  Pinnipeds and El Niño : responses to environmental stress , 1991 .

[61]  F. Trillmich Chapter 11. Attendance Behavior of Galapagos Fur Seals , 1986 .

[62]  William J. Sydeman,et al.  Spring-time distributions of migratory marine birds in the southern California Current: Oceanic eddy associations and coastal habitat hotspots over 17 years , 2006 .

[63]  P. Brickley,et al.  Impact of Haida Eddies on chlorophyll distribution in the Eastern Gulf of Alaska , 2005 .

[64]  F. Trillmich,et al.  Pinnipeds and El Niño , 1991, Ecological Studies.

[65]  P. Niiler On the Ekman divergence in an oceanic jet , 1969 .

[66]  Thomas R. Loughlin,et al.  Oceanographic features related to northern fur seal migratory movements , 2005 .

[67]  David A. S. Rosen,et al.  Thermal limits in young northern fur seals, Callorhinus ursinus , 2014 .

[68]  Toshio Suga,et al.  The North Pacific climatology of winter mixed layer and Mode waters , 2004 .

[69]  K. Kenyon,et al.  Migration of the Northern Fur Seal, Callorhinus ursinus , 1953 .

[70]  J. Barth Short‐wave length instabilities on coastal jets and fronts , 1994 .

[71]  Roger L. Gentry,et al.  Northern Fur Seal Behavior and Ecology@@@Behavior and Ecology of the Northern fur Seal , 1998 .

[72]  M. Reed,et al.  POTENTIAL IMPACT OF ENTANGLEMENT IN MARINE DEBRIS ON THE POPULATION DYNAMICS OF THE NORTHERN FUR SEAL, CALLORHINUS URSINUS , 1990 .

[73]  I. Staniland,et al.  Segregation between the sexes: Antarctic fur seals, Arctocephalus gazella, foraging at South Georgia , 2008, Animal Behaviour.

[74]  Robert L. Smith,et al.  A separating coastal upwelling jet at Cape Blanco, Oregon and its connection to the California Current System , 2000 .

[75]  John A. Barth,et al.  Physical and biological variables affecting seabird distributions during the upwelling season of the northern California Current , 2005 .

[76]  Genshiro Kitagawa,et al.  Selected papers of Hirotugu Akaike , 1998 .

[77]  Michelle E. Lander,et al.  CAUSES OF MORTALITY IN NORTHERN FUR SEALS (CALLORHINUS URSINUS), ST. PAUL ISLAND, PRIBILOF ISLANDS, ALASKA, 1986–2006 , 2010, Journal of wildlife diseases.

[78]  C. Guinet,et al.  Mesoscale eddies as foraging area of a deep-diving predator, the southern elephant seal , 2010 .

[79]  W. Geyer,et al.  Response of a river plume during an upwelling favorable wind event , 2001 .

[80]  James C. McWilliams,et al.  Equilibrium structure and dynamics of the California Current System , 2003 .

[81]  John Horne,et al.  Mesoscale Eddies Are Oases for Higher Trophic Marine Life , 2012, PloS one.

[82]  Barbara M. Hickey,et al.  Coastal oceanography of Washington and Oregon , 1989 .

[83]  W. Crawford Physical Characteristics of Haida Eddies , 2002 .

[84]  Craig M. Lee,et al.  Subthermocline Eddies over the Washington Continental Slope as Observed by Seagliders, 2003–09 , 2013 .

[85]  John A. Barth,et al.  Mesoscale structure and its seasonal evolution in the northern California Current System , 2005 .

[86]  D. Kobayashi,et al.  The transition zone chlorophyll front, a dynamic global feature defining migration and forage habitat for marine resources , 2001 .

[87]  William N. Venables,et al.  GLMs, GAMs and GLMMs: an overview of theory for applications in fisheries research , 2004 .

[88]  B. Hickey Chapter 2 Patterns and Processes of Circulation over the Washington Continental Shelf and Slope , 1989 .

[89]  A. W. Mantyla,et al.  Physical, chemical and biological structure of a coastal eddy near Cape Mendocino , 1990 .

[90]  Ian D. Jonsen,et al.  Identifying leatherback turtle foraging behaviour from satellite telemetry using a switching state-space model , 2007 .

[91]  D. Chelton,et al.  Global observations of nonlinear mesoscale eddies , 2011 .

[92]  K. M. Schaefer,et al.  Tracking apex marine predator movements in a dynamic ocean , 2011, Nature.

[93]  T. Zeppelin,et al.  Stable isotope and scat analyses indicate diet and habitat partitioning in northern fur seals Callorhinus ursinus across the eastern Pacific , 2010 .

[94]  Deborah Austin,et al.  Stomach temperature telemetry reveals temporal patterns of foraging success in a free-ranging marine mammal. , 2006, The Journal of animal ecology.

[95]  H. Akaike,et al.  Information Theory and an Extension of the Maximum Likelihood Principle , 1973 .

[96]  D. Costa,et al.  Chapter 5. Free-Ranging Energetics of Northern Fur Seals , 1986 .

[97]  Kenneth H. Brink,et al.  The global coastal ocean : regional studies and syntheses , 1998 .

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

[99]  Barbara M. Hickey,et al.  The Columbia River plume as cross-shelf exporter and along-coast barrier , 2009 .

[100]  Ken Yoda,et al.  Foraging spots of streaked shearwaters in relation to ocean surface currents as identified using their drift movements , 2014 .

[101]  J. L. Harrison,et al.  The Government Printing Office , 1968, American Journal of Pharmaceutical Education.

[102]  T. Gelatt,et al.  Diving ontogeny and lunar responses in a highly migratory mammal, the northern fur seal Callorhinus ursinus , 2010 .

[103]  Mary Jane Perry,et al.  Seaglider observations of blooms and subsurface chlorophyll maxima off the Washington coast , 2008 .

[104]  S. Philander,et al.  El Niño Southern Oscillation phenomena , 1983, Nature.

[105]  F. Trillmich Attendance behavior of Galápagos fur seals , 1986 .

[106]  W. K. Johnson,et al.  A synoptic survey of young mesoscale eddies in the Eastern Gulf of Alaska , 2009 .

[107]  Martin Wæver Pedersen,et al.  State-space models for bio-loggers: A methodological road map , 2013 .

[108]  Michael J. Weise,et al.  Movement and diving behavior of male California sea lion (Zalophus californianus) during anomalous oceanographic conditions of 2005 compared to those of 2004 , 2006 .

[109]  A. York,et al.  Pup Production Following Harvest of Female Northern Fur Seals , 1981 .

[110]  Helen Bailey,et al.  Large‐scale movements and high‐use areas of western Pacific leatherback turtles, Dermochelys coriacea , 2011 .

[111]  J. Paduan,et al.  Variability of the near‐surface eddy kinetic energy in the California Current based on altimetric, drifter, and moored current data , 1998 .

[112]  Nicholas R. Bates,et al.  Eddy/Wind Interactions Stimulate Extraordinary Mid-Ocean Plankton Blooms , 2007, Science.

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

[114]  R. Ream,et al.  At-sea behavior of juvenile male northern fur seals (Callorhinus ursinus) , 2004 .

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

[116]  J. Wallace,et al.  A Pacific Interdecadal Climate Oscillation with Impacts on Salmon Production , 1997 .

[117]  R. H. Lander A life table and biomass estimate for Alaskan fur seals , 1981 .

[118]  Paul E. Smith,et al.  Mesoscale eddies and survival of late stage Pacific sardine (Sardinops sagax) larvae , 2001 .

[119]  D. G. Chapman,et al.  A population study of the Alaska fur-seal herd , 1954 .

[120]  U. S. Fish,et al.  Special scientific report--wildlife / , 1949 .

[121]  Sophie Bertrand,et al.  Schooling behaviour and environmental forcing in relation to anchoveta distribution: An analysis across multiple spatial scales , 2008 .

[122]  Jiayi Pan,et al.  River Influences on Shelf Ecosystems: Introduction and synthesis , 2010 .

[123]  Robert L. Smith,et al.  The structure of the transition zone between coastal waters and the open ocean off northern California, winter and spring 1987 , 1991 .

[124]  T. Williams,et al.  Sequential megafaunal collapse in the North Pacific Ocean: An ongoing legacy of industrial whaling? , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[125]  P. Stabeno,et al.  Northern Gulf of Alaska eddies and associated anomalies , 2007 .

[126]  Brian Hoover,et al.  Prey Patch Patterns Predict Habitat Use by Top Marine Predators with Diverse Foraging Strategies , 2013, PLoS ONE.