Dynamic oceanography determines fine scale foraging behavior of Masked Boobies in the Gulf of Mexico

During breeding, foraging marine birds are under biological, geographic, and temporal constraints. These contraints require foraging birds to efficiently process environmental cues derived from physical habitat features that occur at nested spatial scales. Mesoscale oceanography in particular may change rapidly within and between breeding seasons, and findings from well-studied systems that relate oceanography to seabird foraging may transfer poorly to regions with substantially different oceanographic conditions. Our objective was to examine foraging behavior of a pan-tropical seabird, the Masked Booby (Sula dactylatra), in the understudied Caribbean province, a moderately productive region driven by highly dynamic currents and fronts. We tracked 135 individuals with GPS units during May 2013, November 2013, and December 2014 at a regionally important breeding colony in the southern Gulf of Mexico. We measured foraging behavior using characteristics of foraging trips and used area restricted search as a proxy for foraging events. Among individual attributes, nest stage contributed to differences in foraging behavior whereas sex did not. Birds searched for prey at nested hierarchical scales ranging from 200 m—35 km. Large-scale coastal and shelf-slope fronts shifted position between sampling periods and overlapped geographically with overall foraging locations. At small scales (at the prey patch level), the specific relationship between environmental variables and foraging behavior was highly variable among individuals but general patterns emerged. Sea surface height anomaly and velocity of water were the strongest predictors of area restricted search behavior in random forest models, a finding that is consistent with the characterization of the Gulf of Mexico as an energetic system strongly influenced by currents and eddies. Our data may be combined with tracking efforts in the Caribbean province and across tropical regions to advance understanding of seabird sensing of the environment and serve as a baseline for anthropogenic based threats such as development, pollution, and commercial fisheries.

[1]  J. Short,et al.  Bird mortality from the Deepwater Horizon oil spill. II. Carcass sampling and exposure probability in the coastal Gulf of Mexico , 2014 .

[2]  Y. Ropert‐Coudert,et al.  Relationship between reversed sexual dimorphism, breeding investment and foraging ecology in a pelagic seabird, the masked booby , 2009, Oecologia.

[3]  C. Amante,et al.  ETOPO1 arc-minute global relief model : procedures, data sources and analysis , 2009 .

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

[5]  K. Dugger,et al.  Foraging strategies of Adélie penguins: adjusting body condition to cope with environmental variability , 2010 .

[6]  L. Breaker,et al.  Mapping and Monitoring Large-Scale Ocean Fronts Off the California Coast Using Imagery from the GOES-10 Geostationary Satellite , 2005 .

[7]  J. Parrish,et al.  Modeled distribution and abundance of a pelagic seabird reveal trends in relation to fisheries , 2013 .

[8]  J. Hare,et al.  Mesoscale, cyclonic eddies as larval fish habitat along the southeast United States shelf: a Lagrangian description of the zooplankton community , 2010 .

[9]  T. Patterson,et al.  Deep Sea Research Part II: Topical Studies in Oceanography , 2013 .

[10]  G. Visser,et al.  Does food availability affect energy expenditure rates of nesting seabirds? A supplemental-feeding experiment with Black-legged Kittiwakes (Rissa tridactyla) , 2002 .

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

[12]  Ian R. Cleasby,et al.  Long-term individual foraging site fidelity--why some gannets don't change their spots. , 2015, Ecology.

[13]  R. Dirzo,et al.  Resource partitioning by species but not sex in sympatric boobies in the central Pacific Ocean , 2010 .

[14]  W. Sturges,et al.  Circulation in the Gulf of Mexico: Observations and Models: Sturges/Circulation in the Gulf of Mexico: Observations and Models , 2005 .

[15]  R. W. Russell,et al.  Physical processes , prey abundance , and the foraging ecology of seabirds , 2013 .

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

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

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

[19]  Graham H. Pyke,et al.  Optimal Foraging: A Selective Review of Theory and Tests , 1977, The Quarterly Review of Biology.

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

[21]  Robert M. Suryan,et al.  Foraging destinations and marine habitat use of short-tailed albatrosses: A multi-scale approach using first-passage time analysis , 2006 .

[22]  S. Salas,et al.  Dynamics of Fishing Gear and Spatial Allocation of Fishing Effort in a Multispecies Fleet , 2010 .

[23]  H. Weimerskirch,et al.  Foraging strategy of a tropical seabird, the red- footed booby, in a dynamic marine environment , 2005 .

[24]  S. Garthe,et al.  Foraging plasticity in a pelagic seabird species along a marine productivity gradient , 2010 .

[25]  B. Congdon,et al.  Day-to-day variation in sea-surface temperature reduces sooty tern Sterna fuscata foraging success on the Great Barrier Reef, Australia , 2007 .

[26]  Philip W. Stevens,et al.  Flyingfish Spawning (Parexocoetus brachypterus) in the Northeastern Gulf of Mexico , 2003, Environmental Biology of Fishes.

[27]  Leo Breiman,et al.  Random Forests , 2001, Machine Learning.

[28]  William J. Sydeman,et al.  Marine bird and cetacean associations with bathymetric habitats and shallow-water topographies: impl , 2004 .

[29]  S. Wanless,et al.  Brood neglect and contingent foraging behavior in a pelagic seabird , 2004, Behavioral Ecology and Sociobiology.

[30]  H. Weimerskirch,et al.  Seasonal variation in oceanographic habitat and behaviour of white-chinned petrels Procellaria aequinoctialis from Kerguelen Island , 2010 .

[31]  M. Short,et al.  Sensitivity of tropical seabirds to El Niño precursors. , 2009, Ecology.

[32]  S. Garthe,et al.  Tracking seabirds to identify ecologically important and high risk marine areas in the western North Atlantic , 2012 .

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

[34]  Y. Naito,et al.  A fine-scale time budget of Cape gannets provides insights into the foraging strategies of coastal seabirds , 2004, Animal Behaviour.

[35]  M. Hindell,et al.  Flexible foraging behaviour in a marine predator, the Masked booby (Sula dactylatra), according to foraging locations and environmental conditions , 2015 .

[36]  E. Chávez,et al.  Los arrecifes coralinos del Caribe noroccidental y Golfo de México en el contexto socioeconómico , 1988 .

[37]  J. Kruskal.  Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis , 1964 .

[38]  Steffen Oppel,et al.  Using an algorithmic model to reveal individually variable movement decisions in a wintering sea duck. , 2009, The Journal of animal ecology.

[39]  C. Calenge.  Analysis of Animal Movements in R : the adehabitatLT Package , 2011 .

[40]  M. Hindell,et al.  The individual counts: within sex differences in foraging strategies are as important as sex-specific differences in masked boobies Sula dactylatra , 2013 .

[41]  S. Benhamou,et al.  Are Cape gannets dependent upon fishery waste? A multi-scale analysis using seabird GPS-tracking, hydro-acoustic surveys of pelagic fish and vessel monitoring systems , 2013 .

[42]  W. Walker,et al.  Foraging dynamics of seabirds in the Eastern tropical pacific ocean , 2007 .

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

[44]  Andréa Thiebault,et al.  Bird-Borne Video-Cameras Show That Seabird Movement Patterns Relate to Previously Unrevealed Proximate Environment, Not Prey , 2014, PloS one.

[45]  R. Silver,et al.  Parental Care in an Ecological Perspective: A Quantitative Analysis of Avian Subfamilies , 1985 .

[46]  W. J. Smith,et al.  The Sulidae: Gannets and Boobies , 1979 .

[47]  Ashutosh Kumar Singh,et al.  The Elements of Statistical Learning: Data Mining, Inference, and Prediction , 2010 .

[48]  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 .

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

[50]  David S. Lee,et al.  Foraging over Sargassum by Western North Atlantic Seabirds , 2012 .

[51]  Torkild Tveraa,et al.  Hierarchical patch dynamics and animal movement pattern , 2006, Oecologia.

[52]  H. Weimerskirch,et al.  Variability of resource partitioning in sympatric tropical boobies , 2011 .

[53]  J. Kelly,et al.  The Parental Dilemma Under Variable Predation Pressure: Adaptive Variation in Nest Attendance by Great Egrets , 2012 .

[54]  Elena B. Sachs,et al.  Seabird use of discards from a nearshore shrimp fishery in the South Atlantic Bight, USA , 2011 .

[55]  Wei-Yin Loh,et al.  Classification and regression trees , 2011, WIREs Data Mining Knowl. Discov..

[56]  J. Graves,et al.  Distribution and Habitat Associations of Billfish and Swordfish Larvae across Mesoscale Features in the Gulf of Mexico , 2012, PloS one.

[57]  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.

[58]  H. Weimerskirch,et al.  The regular alternation of short and long foraging trips in the blue petrel Halobaena caerulea: a previously undescribed strategy of food provisioning in a pelagic seabird , 1994 .

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

[60]  A. Barth,et al.  The Surface Circulation of the Caribbean Sea and the Gulf of Mexico as Inferred from Satellite Altimetry , 2009 .

[61]  N. B. Kotliar,et al.  Multiple scales of patchiness and patch structure: a hierarchical framework for the study of heterogeneity , 1990 .

[62]  D. Costa,et al.  Effects of El Niño-driven changes in wind patterns on North Pacific albatrosses , 2016, Journal of The Royal Society Interface.

[63]  J. Santora,et al.  New approach for using remotely sensed chlorophyll a to identify seabird hotspots , 2012 .

[64]  Peter Cornillon,et al.  Fronts in Large Marine Ecosystems , 2009 .

[65]  D. Grémillet,et al.  Overlap between vulnerable top predators and fisheries in the Benguela upwelling system: implications for marine protected areas , 2009 .

[66]  Robert F. Chen,et al.  Natural Variability of Surface Oceanographic Conditions in the Offshore Gulf of Mexico , 2015 .

[67]  S. Weeks,et al.  Oceanography and seabird foraging: within-season impacts of increasing sea-surface temperature on the Great Barrier Reef , 2013 .

[68]  Ole Martin Smedstad,et al.  Variational Data Assimilation for the Global Ocean , 2013 .

[69]  S. Garthe,et al.  Influence of water flow velocity, water depth and colony distance on distribution and foraging patterns of terns in the Wadden Sea , 2009 .

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

[71]  A. Longhurst.  Ecological Geography of the Sea , 1998 .

[72]  Kurt M. Fristrup,et al.  Geometry of visual recruitment by seabirds to ephemeral foraging flocks , 1992 .

[73]  D. Leipper.  A sequence of current patterns in the Gulf of Mexico , 1970 .

[74]  G. Davoren,et al.  Differences in prey selection and behaviour during self-feeding and chick provisioning in rhinoceros auklets , 1999, Animal Behaviour.

[75]  C. Ribic,et al.  Distribution of seabirds in the northern Gulf of Mexico in relation to mesoscale features: Initial observations , 1997 .

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

[77]  L. Prieur,et al.  Analysis of variations in ocean color1 , 1977 .

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

[79]  H. Weimerskirch,et al.  Tracking seabirds to identify potential Marine Protected Areas in the tropical western Indian Ocean , 2012 .

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

[81]  Simon N Ingram,et al.  Mesoscale fronts as foraging habitats: composite front mapping reveals oceanographic drivers of habitat use for a pelagic seabird , 2014, Journal of The Royal Society Interface.

[82]  Marti J. Anderson,et al.  Distance‐Based Tests for Homogeneity of Multivariate Dispersions , 2006, Biometrics.

[83]  H. Weimerskirch,et al.  Foraging strategy of masked boobies from the largest colony in the world: relationship to environmental conditions and fisheries , 2008 .

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

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

[86]  Daniel C. Dunn,et al.  Marine Geospatial Ecology Tools: An integrated framework for ecological geoprocessing with ArcGIS, Python, R, MATLAB, and C++ , 2010, Environ. Model. Softw..

[87]  M. Hindell,et al.  Foraging Parameters Influencing the Detection and Interpretation of Area-Restricted Search Behaviour in Marine Predators: A Case Study with the Masked Booby , 2013, PloS one.

[88]  W. J. Grecian,et al.  Inter- and intra-year variation in foraging areas of breeding kittiwakes (Rissa tridactyla) , 2014, Marine biology.

[89]  C. Santos,et al.  Foraging habitat choice of White-tailed Tropicbirds revealed by fine-scale GPS tracking and remote sensing , 2019, PeerJ.

[90]  R. Pitman,et al.  A TEST FOR BIAS ATTRIBUTABLE TO SEABIRD AVOIDANCE OF SHIPS DURING SURVEYS CONDUCTED IN THE TROPICAL PACIFIC , 2006 .

[91]  J. Short,et al.  Bird mortality from the Deepwater Horizon oil spill. I. Exposure probability in the offshore Gulf of Mexico , 2014 .

[92]  O. Håstad,et al.  Ultraviolet vision and foraging in dip and plunge diving birds , 2005, Biology Letters.

[93]  Prieur,et al.  Analysis of variations in ocean color’ , 2000 .

[94]  Mohi Kumar.  Circulation in the Gulf of Mexico: Observations and Models , 2006 .

[95]  O. Lindén,et al.  Ixtoc I; a case study of the world's largest oil spill , 1981 .

[96]  D. R. Cutler,et al.  Utah State University From the SelectedWorks of , 2017 .

[97]  G. Nevitt,et al.  The influence of developmental environment on the evolution of olfactory foraging behaviour in procellariiform seabirds , 2008, Journal of evolutionary biology.

[98]  Y. Ropert‐Coudert,et al.  Foraging behaviour and energetics of Cape gannets Morus capensis feeding on live prey and fishery discards in the Benguela upwelling system , 2007 .

[99]  H. Drummond,et al.  Effect of El Niño on the diet of a specialist seabird, Sula nebouxii, in the warm eastern tropical Pacific , 2012 .

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

[101]  Andy Liaw,et al.  Classification and Regression by randomForest , 2007 .

[102]  Marc Lavielle,et al.  Using penalized contrasts for the change-point problem , 2005, Signal Process..

[103]  PARENTAL PROVISIONING PATTERNS OF WEDGE-TAILED SHEARWATERS AND THEIR RELATION TO CHICK BODY CONDITION , 2002 .