Pelagic marine protected areas protect foraging habitat for multiple breeding seabirds in the central Pacific

Biological Conservation

Volumn 181, Issue , 2015, Pages 226-235

  Young, Hillary S ^a   Maxwell, Sara M ^b   Conners, Melinda G ^c   Shaffer, Scott A ^c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SAN JOSE STATE UNIVERSITY   (United States)

Author keywords

Central tropical pacific; Facilitated foraging; Gridded utilization distribution; Home range; Pelagic marine protected areas; Seabirds; Sula

Indexed keywords

BREEDING POPULATION; FACILITATION; FORAGING BEHAVIOR; GPS; HABITAT TYPE; HOME RANGE; MARINE PARK; PELAGIC ENVIRONMENT; POPULATION DISTRIBUTION; REPRODUCTIVE BEHAVIOR; SEABIRD;

PACIFIC OCEAN; PACIFIC OCEAN (CENTRAL);

AVES; SULA DACTYLATRA; SULA LEUCOGASTER; SULA SULA SULA; SULIDAE;

EID: 84949115938     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2014.10.027     Document Type: Article

References (88)

1. Agardy T., Di Sciara G.N., Christie P. Mind the gap: addressing the shortcomings of marine protected areas through large scale marine spatial planning. Mar. Policy 2011, 35:226-232.
2. Alpine J., Hobday A. Area requirements and pelagic protected areas: is size an impediment to implementation?. Mar. Freshwater Res. 2007, 58:558-569.
3. Anderson D.J., Ricklefs R.E. Radio-tracking masked and blue-footed boobies (Sula spp.) in the Galapagos Islands. Nat. Geog. Res. 1987, 3:152-163.
4. Angel M.V. Biodiversity of the pelagic ocean. Conserv. Biol. 1993, 7:760-772.
5. Ashmole N., Ashmole M. Comparative feeding ecology of sea bird of a tropical oceanic island. Peabody Museum Nat. Hist. Bull. 1967, 24:1-131.
6. Au D.W., Pitman R.L. Seabird interactions with dolphins and tuna in the eastern tropical Pacific. Condor 1986, 88:304-317.
7. Ballard G., Jongsomjit D., Veloz S.D., Ainley D.G. Coexistence of mesopredators in an intact polar ocean ecosystem: the basis for defining a Ross Sea marine protected area. Biol. Conserv. 2012, 156:72-82.
8. Block B.A., Teo S.L., Walli A., Boustany A., Stokesbury M.J., Farwell C.J., Weng K.C., Dewar H., Williams T.D. Electronic tagging and population structure of Atlantic bluefin tuna. Nature 2005, 434:1121-1127.
9. Block B.A., Jonsen I., Jorgensen S., Winship A., Shaffer S.A., Bograd S., Hazen E., Foley D., Breed G., Harrison A.-L. Tracking apex marine predator movements in a dynamic ocean. Nature 2011, 475:86-90.
10. Boersma P.D., Parrish J.K. Limiting abuse: marine protected areas, a limited solution. Ecol. Econ. 1999, 31:287-304.
11. Bograd S.J., Rabinovich A.B., LeBlond P.H., Shore J.A. Observations of seamount-attached eddies in the north pacific. J. Geophys. Res.-Oceans 1997, 102:12441-12456.
12. Calenge C. Exploring habitat selection by wildlife with adehabitat. J. Stat. Softw. 2007, 22:1-19.
13. Cox S.P., Martell S.J., Walters C.J., Essington T.E., Kitchell J.F., Boggs C., Kaplan I. Reconstructing ecosystem dynamics in the central Pacific Ocean, 1952 1998. I. Estimating population biomass and recruitment of tunas and billfishes. Can. J. Fish. Aquat. Sci. 2002, 59:1724-1735.
14. Croxall J.P., Butchart S.H., Lascelles B., Stattersfield A.J., Sullivan B., Symes A., Taylor P. Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv. Int. 2012, 22:1-34.
15. Davies R.D., Wanless S., Lewis S., Hamer K.C. Density-dependent foraging and colony growth in a pelagic seabird species under varying environmental conditions. Mar. Ecol. Prog. Ser. 2013, 485:287-294.
16. Dawdy D.R., Matalas N.C. Statistical and probability analysis of hydrologic data, part III: analysis of variance, covariance and time series. Handbook of Applied Hydrology, A Compendium of Water-resources Technology 1964, 868-890. McGraw-Hill Book Company, New York. V.T. Chow (Ed.).
17. Depkin, C.D., 2002. Trip report to Palmyra Atoll, 06 August 2001-07. October 2002. U.S. Fish and Wildlife Service, Honolulu, Hawai'i.
18. Dueri S., Bopp L., Maury O. Projecting the impacts of climate change on skipjack tuna abundance and spatial distribution. Global Change Biol. 2014, 20:742-753.
19. Federal Register, 2006. Presidential Proclamation 8031 of June 15, 2006: Establishment of the Northwestern Hawaiian Islands Marine National Monument. pp. 36443-36475. US Federal Register.
20. Federal Register, 2009. Establishment of the Pacific Remote Islands Marine National Monument, Presidential Proclamation 8336. pp. 1565-1575. US Federal Register.
21. Ferretti F., Worm B., Britten G.L., Heithaus M.R., Lotze H.K. Patterns and ecosystem consequences of shark declines in the ocean. Ecol. Lett. 2010, 13:1055-1071.
22. Fieberg J. Utilization distribution estimation using weighted kernel density estimators. J. Wildlife Manage. 2007, 71:1669-1675.
23. Field C.B., Behrenfeld M.J., Randerson J.T., Falkowski P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 1998, 281:237-240.
24. Gaines S.D., Lester S.E., Grorud-Colvert K., Costello C., Pollnac R. Evolving science of marine reserves: new developments and emerging research frontiers. Proc. Natl. Acad. Sci. 2010, 107:18251-18255.
25. Game E.T., Grantham H.S., Hobday A.J., Pressey R.L., Lombard A.T., Beckley L.E., Gjerde K., Bustamante R., Possingham H.P., Richardson A.J. Pelagic protected areas: the missing dimension in ocean conservation. Trends Ecol. Evol. 2009, 24:360-369.
26. Garthe S., Markones N., Mendel B., Sonntag N., Krause J.C. Protected areas for seabirds in German offshore waters: designation, retrospective consideration and current perspectives. Biol. Conserv. 2012, 156:126-135.
27. Grémillet D., Dell'Omo G., Ryan P.G., Peters G., Ropert-Coudert Y., Weeks S.J. Offshore diplomacy, or how seabirds mitigate intra-specific competition: a case study based on GPS tracking of Cape gannets from neighbouring colonies. Mar. Ecol. Prog. Ser. 2004, 268:265-279.
28. Harding A., Paredes R., Suryan R., Roby D., Irons D., Orben R., Renner H., Young R., Barger C., Dorresteijn I. Does location really matter? An inter-colony comparison of seabirds breeding at varying distances from productive oceanographic features in the Bering Sea. Deep Sea Res. Part II: Topical Stud. Oceanogr. 2013, 94:178-191.
29. Harrison C.S., Hida T.S., Seki M.P. Hawaiian seabird feeding ecology. Wildlife Monogr. 1983, 85:3-71.
30. Hartzell, P.L., Youngren, S.M., Rapp, D.C., 2012. Biological status and trends, terrestrial component at French Frigate Shoals, Northwestern Hawaiian Islands (1986-2011). Technical Report, Honolulu, Hawaii.
31. Hazen E.L., Jorgensen S.J., Rykaczewski R., Bograd S.J., Foley D.G., Jonsen I.D., Shaffer S.A., Dunne J., Costa D.P., Crowder L.B., Block B.A. Predicted habitat shifts of Pacific top predators in a changing climate. Nat. Climate Change 2012, 3:234-238.
32. Hobday A.J., Maxwell S.M., Forgie J., McDonald J., Darby M., Seto K., Bailey H., Bograd S.J., Briscoe D.K., Costa D.P., Crowder L.B., Dunn D.C., Fossette S., Halpin P.N., Hartog J.R., Hazen E.L., Lascelles B.G., Lewison R.L., Poulos G., Powers A. Dynamic ocean management: integrating scientific and technological capacity with law, policy and management. Stanford Environ. Law J. 2014, 33:125-165.
33. Hooker S.K., Cañadas A., Hyrenbach K.D., Corrigan C., Polovina J.J., Reeves R.R. Making protected area networks effective for marine top predators. Endangered Species Res. 2011, 13:203-218.
34. Howell E., Kobayashi D., Parker D., Balazs G. TurtleWatch: a tool to aid in the bycatch reduction of loggerhead turtles Caretta caretta in the Hawaii-based pelagic longline fishery. Endangered Species Res. 2008, 5:267-278.
35. Hyrenbach K.D., Forney K.A., Dayton P. Marine protected areas and ocean basin management. Aquat. Conserv.: Mar. Freshwater Ecosyst. 2000, 10:437-458.
36. Hyrenbach K.D., Keiper C., Allen S.G., Ainley D.G., Anderson D.J. Use of marine sanctuaries by far-ranging predators: commuting flights to the California current system by breeding Hawaiian albatrosses. Fish. Oceanogr. 2006, 15:95-103.
37. Itano D.G., Holland K.N. Movement and vulnerability of bigeye (Thunnus obesus) and yellowfin tuna (Thunnus albacares) in relation to FADs and natural aggregation points. Aquat. Living Resour. 2000, 13:213-223.
38. Kai E.T., Rossi V., Sudre J., Weimerskirch H., Lopez C., Hernandez-Garcia E., Marsac F., Garçon V. Top marine predators track Lagrangian coherent structures. Proc. Natl. Acad. Sci. 2009, 106:8245-8250.
39. Kappes M.A., Weimerskirch H., Pinaud D., Le Corre M. Variability of resource partitioning in sympatric tropical boobies. Mar. Ecol. Prog. Series 2011, 441:281-294.
40. Keating K.A., Cherry S. Modeling utilization distributions in space and time. Ecology 2009, 90:1971-1980.
41. Kenyon, J., Maragos, J., Vroom, P., 2012. Monitoring supports establishment of Pacific Remote Islands Marine National Monument. In: Proceedings of the 12th International Coral Reef Symposium. pp. 9-13.
42. Kernohan B., Gitzen R.A., Millspaugh J. Analysis of animal space use and movements. Radio Tracking and Animal Populations 2001, 126-168. Academic Press, San Diego. J. Millspaugh, J. Marzluff (Eds.).
43. Langley, A., Harley, S., Hoyle, S., Davies, N., Hampton, J., Kleiber, P., 2009. Stock assessment of yellowfin tuna in the western and central Pacific Ocean. Western Central Pacific Fisheries Commission, Scientific Committee, 5th Regular Session.
44. Lascelles B.G., Langham G.M., Ronconi R.A., Reid J.B. From hotspots to site protection: identifying marine protected areas for seabirds around the globe. Biol. Conserv. 2012, 156:5-14.
45. Le Corre M., Cherel Y., Lagarde F., Lormée H., Jouventin P. Seasonal and inter-annual variation in the feeding ecology of a tropical oceanic seabird, the red-tailed tropicbird Phaethon rubricauda. Mar. Ecol. Prog. Series 2003, 255:289-301.
46. Lester S.E., Halpern B.S., Grorud-Colvert K., Lubchenco J., Ruttenberg B.I., Gaines S.D., Airamé S., Warner R.R. Biological effects within no-take marine reserves: a global synthesis. Mar. Ecol. Prog. Series 2009, 384:33-46.
47. Lewis S., Schreiber E.A., Daunt F., Schenk G.A., Wanless S., Hamer K.C. Flexible foraging patterns under different time constraints in tropical boobies. Animal Behav. 2004, 68:1331-1337.
48. Lewis S., Schreiber E.A., Daunt F., Schenk G.A., Orr K., Adams A., Wanless S., Hamer K.C. Sex-specific foraging behaviour in tropical boobies: does size matter?. Ibis 2005, 147:408-414.
49. Lormee H., Barbraud C., Chastel O. Reversed sexual size dimorphism and parental care in the Red-footed Booby Sula sula. IBIS 2005, 147:307-315.
50. Lotze H.K., Coll M., Magera A.M., Ward-Paige C., Airoldi L. Recovery of marine animal populations and ecosystems. Trends Ecol. Evol. 2011, 26:595-605.
51. Louzao M., Hyrenbach K.D., Arcos J.M., Abelló P., Sola L.G.D., Oro D. Oceanographic habitat of an endangered Mediterranean procellariiform: implications for marine protected areas. Ecol. Appl. 2006, 16:1683-1695.
52. Louzao M., Pinaud D., Peron C., Delord K., Wiegand T., Weimerskirch H. Conserving pelagic habitats: seascape modelling of an oceanic top predator. J. Appl. Ecol. 2011, 48:121-132.
53. Ludynia K., Kemper J., Roux J.-P. The Namibian Islands' marine protected area: using seabird tracking data to define boundaries and assess their adequacy. Biol. Conserv. 2012, 156:136-145.
54. Martell S.J., Essington T.E., Lessard B., Kitchell J.F., Walters C.J., Boggs C.H. Interactions of productivity, predation risk, and fishing effort in the efficacy of marine protected areas for the central Pacific. Can. J. Fish. Aquat. Sci. 2005, 62:1320-1336.
55. Maxwell S.M., Frank J.J., Breed G.A., Robinson P.W., Simmons S.E., Crocker D.E., Gallo-Reynoso J.P., Costa D.P. Benthic foraging on seamounts: A specialized foraging behavior in a deep-diving pinniped. Mar. Mamm. Sci. 2012, 28:E333-E344.
56. Maxwell S.M., Morgan L.E. Facilitated foraging of seabirds on pelagic fishes: implications for management of pelagic marine protected areas. Mar. Ecol. Prog. Series 2013, 481:289-303.
57. Maxwell S.M., Breed G.A., Nickel B.A., Makanga-Bahouna J., Pemo-Makaya E., Parnell R.J., Formia A., Ngouessono S., Godley B.J., Costa D.P., Witt M.J., Coyne M.S. Using satellite tracking to optimize protection of long-lived marine species: Olive Ridley sea turtle conservation in Central Africa. PLoS ONE 2011, 6:e19905.
58. Maxwell S.M., Hazen E.L., Bograd S.J., Halpern B.S., Breed G.A., Nickel B., Teutschel N.M., Crowder L.B., Benson S., Dutton P.H., Bailey H., Kappes M.A., Kuhn C., Weise M.J., Mate B., Shaffer S.A., Hassrick J.L., Henry R.W., Irvine L., McDonald B.I., Robinson P.W., Block B.A., Costa D.P. Cumulative human impacts on marine predators. Nat. Commun. 2013, 4:1-9.
59. Maxwell S.M., Ban N., Morgan L.E. Pragmatic approaches for effective pelagic marine protected area management. Endangered Species Res. 2014, 26:59-74.
60. McCauley, D., Pinsky, M., Estes, J., Palumbi, S., Joyce, F., Warner, R., in press. Marine defaunation: the past, present, and future of animal loss in the global ocean. Science.
61. Montevecchi W., Hedd A., McFarlane Tranquilla L., Fifield D., Burke C., Regular P., Davoren G., Garthe S., Robertson G., Phillips R. Tracking seabirds to identify ecologically important and high risk marine areas in the western North Atlantic. Biol. Conserv. 2012, 156:62-71.
62. Myers R.A., Worm B. Rapid worldwide depletion of predatory fish communities. Nature 2003, 423:280-283.
63. Norse E. Pelagic protected areas: the greatest parks challenge of the 21st century. Parks 2005, 15:32-39.
64. Pauly D., Christensen V., Guénette S., Pitcher T.J., Sumaila U.R., Walters C.J., Watson R., Zeller D. Towards sustainability in world fisheries. Nature 2002, 418:689-695.
65. Péron C., Grémillet D., Prudor A., Pettex E., Saraux C., Soriano-Redondo A., Authier M., Fort J. Importance of coastal Marine protected areas for the conservation of pelagic seabirds: the case of Vulnerable yelkouan shearwaters in the Mediterranean Sea. Biol. Conserv. 2013, 168:210-221.
66. Pichegru L., Ryan P., van Eeden R., Reid T., Grémillet D., Wanless R. Industrial fishing, no-take zones and endangered penguins. Biol. Conserv. 2012, 156:117-125.
67. Polovina J.J., Abecassis M., Howell E.A., Woodworth P. Increases in the relative abundance of mid-trophic level fishes concurrent with declines in apex predators in the subtropical North Pacific, 1996-2006. Fish. Bull. 2009, 107:523-531.
68. R Development Core Team, 2012. R: A language and environment for statistical computing. ISBN 3-900051-07-0. R Foundation for Statistical Computing. Vienna, Austria, 2013. <>. http://www.R-project.org.
69. Ricklefs R.E. Seabird life histories and the marine environment: some speculations. Colonial Waterbirds 1990, 13:1-6.
70. Rosenbaum H.C., Maxwell S.M., Kershaw F., Mate B. Long-range movement of humpback whales and their overlap with anthropogenic activity in the South Atlantic Ocean. Conserv. Biol. 2014, 28:604-615.
71. Sheppard C., Ateweberhan M., Bowen B., Carr P., Chen C., Clubbe C., Craig M., Ebinghaus R., Eble J., Fitzsimmons N. Reefs and islands of the Chagos Archipelago, Indian Ocean: why it is the world's largest no-take marine protected area. Aquat. Conserv. Mar. Freshwater Ecosyst. 2012, 22:232-261.
72. Shillinger G.L., Palacios D.M., Bailey H., Bograd S.J., Swithenbank A.M., Gaspar P., Wallace B.P., Spotila J.R., Paladino F.V., Piedra R. Persistent leatherback turtle migrations present opportunities for conservation. PLoS Biol. 2008, 6:e171.
73. Silverman B.W. Density Estimation for Statistics and Data Analysis 1986, CRC Press, Boca Raton FL.
74. Sommerfeld J., Kato A., Ropert-Coudert Y., Garthe S., Hindell M.A. The individual counts: within sex differences in foraging strategies are as important as sex-specific differences in masked boobies Sula dactylatra. J. Avian Biol. 2013, 44:531-540.
75. Sommerfeld J., Kato A., Ropert-Coudert Y., Garthe S., Hindell M.A. Foraging parameters influencing the detection and interpretation of area-restricted search behaviour in marine predators: A case study with the masked booby. PloS one 2013, 8:e63742.
76. Spear L.B., Ainley D.G., Walker W. Foraging dynamics of seabirds in the eastern tropical Pacific Ocean. Stud. Avian Biol. 2007, 35:1-99.
77. Thaxter C.B., Lascelles B., Sugar K., Cook A.S., Roos S., Bolton M., Langston R.H., Burton N.H. Seabird foraging ranges as a preliminary tool for identifying candidate marine protected areas. Biol. Conserv. 2012, 156:53-61.
78. U.S. National Geophysical Data Center, 2006. 2-minute Gridded Global Relief Data (ETOPO2). <>. http://www.ngdc.noaa.gov/mgg/fliers/06mgg01.html.
79. Ward P., Myers R.A. Shifts in open-ocean fish communities coinciding with the commencement of commercial fishing. Ecology 2005, 86:835-847.
80. Weimerskirch H. Are seabirds foraging for unpredictable resources?. Deep Sea Res. Part II: Topical Stud. Oceanogr. 2007, 54:211-223.
81. Weimerskirch H., Le Corre M., Jaquemet S., Marsac F. Foraging strategy of a tropical seabird, the red-footed booby, in a dynamic marine environment. Mar. Ecol. Prog. Series 2005, 288:251-261.
82. Weimerskirch H., Le Corre M., Ropert-Coudert Y., Kato A., Marsac F. Sex-specific foraging behaviour in a seabird with reversed sexual dimorphism: the red-footed booby. Oecologia 2006, 146:681-691.
83. Weimerskirch H., Le Corre M., Bost C.A. Foraging strategy of masked boobies from the largest colony in the world: relationship to environmental conditions and fisheries. Mar. Ecol. Prog. Ser. 2008, 362:291-302.
84. Weimerskirch H., Shaffer S.A., Tremblay Y., Costa D.P., Gadenne H., Kato A., Ropert-Coudert Y., Sato K., Aurioles D. Species-and sex-specific differences in foraging behaviour and foraging zones in blue-footed and brown boobies in the Gulf of California. Mar. Ecol. Prog. Series 2009, 391:267-278.
85. Witt M.J., Bonguno E.A., Broderick A.C., Coyne M.S., Formia A., Gibudi A., Mounguengui G.A.M., Moussounda C., Nsafou M., Nougessono S., Parnell R.J., Sounguet G.P., Verhage S., Godley B.J. Tracking leatherback turtles from the world's largest rookery: assessing threats across the South Atlantic. Proc. R. Soc. B-Biol. Sci. 2011, 278:2338-2347.
86. Young H.S., McCauley D.J., Dirzo R., Dunbar R.B., Shaffer S.A. Niche partitioning among and within sympatric tropical seabirds revealed by stable isotope analysis. Mar. Ecol. Prog. Series 2010, 416:285-294.
87. Young H.S., Shaffer S.A., McCauley D.J., Foley D.G., Dirzo R., Block B.A. Resource partitioning by species but not sex in sympatric boobies in the central Pacific Ocean. Mar. Ecol. Prog. Series 2010, 403:291-301.
88. Zavalaga C.B., Halls J.N., Mori G.P., Taylor S.A., Dell'Omo G. At-sea movement patterns and diving behavior of Peruvian boobies Sula variegata in northern Peru. Mar. Ecol. Prog. Series 2010, 404:259-274.