Flexible foraging behaviour of a sexually dimorphic seabird: Large males do not always dive deep

Marine Ecology Progress Series

Volumn 428, Issue , 2011, Pages 271-287

  Quillfeldt, Petra ^a   Schroff, Simone ^a   Van Noordwijk, Hendrika J ^a   Michalik, Andreas ^a   Ludynia, Katrin ^b   Masello, Juan F ^a  

^a MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Behavioural plasticity; Diving behaviour; Optimal foraging; Phalacrocorax atriceps; Sexual size dimorphism; Stable isotope analysis; Stable isotope mixing model

Indexed keywords

ADAPTATION; DIVING BEHAVIOR; EVOLUTIONARY BIOLOGY; FORAGING BEHAVIOR; INTERSEXUAL INTERACTION; MALE BEHAVIOR; PHENOTYPIC PLASTICITY; SEABIRD; SEXUAL DIMORPHISM; STABLE ISOTOPE;

FALKLAND ISLANDS (MALVINAS); NEW ISLAND;

PHALACROCORAX ATRICEPS;

EID: 79955649645     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps09058     Document Type: Article

References (97)

1. Arnould JPY, Kirkwood R (2007) Habitat selection by female Australian fur seals (Arctocephalus pusillus doriferus). Aquatic Conserv: Mar Freshw Ecosyst 17:S53-S67 (Pubitemid 351363017)
2. Beck CA, Bowen WD, McMillan JI, Iverson SJ (2003) Sex differences in the diving behaviour of a size-dimorphic capital breeder: the grey seal. Anim Behav 66:777-789 (Pubitemid 37284126)
3. Becker BH, Beissinger SR (2003) Scale-dependent habitat selection by a nearshore seabird, the marbled murrelet, in a highly dynamic upwelling system. Mar Ecol Prog Ser 256:243-255 (Pubitemid 36964847)
4. Bernstein NP, Maxson SJ (1984) Sexually distinct daily activity patterns of blue-eyed shags in Antarctica. Condor 86: 151-156
5. Beyer HL (2004) Hawth's analysis tools for ArcGIS. http://www. spatialecology.com/htools
6. Boyd IL, Wanless S, Camphuysen CJ (eds) (2006) Top predators in marine ecosystems: their role in monitoring and management. Cambridge University Press, Cambridge
7. Casaux R, Barrera-Oro ER (2006) Shags in Antarctica: their feeding behaviour and ecological role in the marine food web. Antarct Sci 18:3-14
8. Casaux R, Favero M, Silva P, Baroni A (2001) Sex differences in diving depths and diet of Antarctic shags at the South Shetland Islands. J Field Ornithol 72:22-29
9. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (δ15N and δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443-453
10. Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behaviour and ecology of two sexes. The University of Chicago Press, Chicago
11. Cook TR, Cherel Y, Tremblay Y (2005) Foraging tactics of chick-rearing Crozet shags: individuals display repetitive activity and diving patterns over time.Polar Biol 29: 562-569
12. Cook TR, Cherel Y, Bost CA, Tremblay Y (2007) Chickrearing Crozet shags (Phalacrocorax melanogenis) display sex-specific foraging behaviour. Antarct Sci 19:55-63 (Pubitemid 46662192)
13. Cook TR, Lescroel A, Tremblay Y, Bost CA (2008) To breathe or not to breathe? Optimal breathing, aerobic dive limit and oxygen stores in deep-diving blue-eyed shags. Anim Behav 76:565-576
14. Croll DA, Gaston AJ, Burger AE, Konnoff D (1992) Foraging behavior and physiological adaptation for diving in thickbilled murres. Ecology 73:344-356
15. de Solla SR, Bonduriansky R, Brooks RJ (1999) Eliminating autocorrelation reduces biological relevance of home range estimates. J Anim Ecol 68:221-234 (Pubitemid 29139155)
16. Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967-971 (Pubitemid 41416642)
17. Enstipp MR, Gremillet D, Jones DR (2006) The effects of depth,temperature and food ingestion on the foraging ener - getics of a diving endotherm, the double-crested cormorant (Phalacrocorax auritus). J Experim Biol 209: 845-859
18. Favero M, Casaux R, Silva P, Barrera-Oro E, Coria N (1998) The diet of the Antarctic shag during summer at Nelson Island, Antarctica. Condor 100:112-118 (Pubitemid 28129429)
19. Ferrari S, Alegre B, Gandini P (2004) The diet of imperial cormorant (Phalacrocorax atriceps) in southern Santa Cruz (Patagonia, Argentina). Ornitol Neotrop 15:103-110
20. Forcada J, Trathan PN, Reid K, Murphy EJ, Croxall JP (2006) Contrasting population changes in sympatric penguin species in association with climate warming. Glob Change Biol 12:411-423
21. Frere E, Quintana F, Gandini P, Wilson RP (2008) Foraging behaviour and habitat partitioning of two sympatric cormorants in Patagonia, Argentina. Ibis 150:558-564
22. Fretwell SD, Lucas HL Jr (1969) On territorial behaviour and other factors influencing habitat distribution in birds. Acta Biotheor 19:16-36
23. González-Solís J, Croxall JP, Wood AG (2000) Sexual dimorphism and sexual segregation in foraging strategies of northern giant petrels, Macronectes halli, during incubation. Oikos 90:390-398
24. Green K, Williams R (1997) Biology of the Heard Island Shag Phalacrocorax nivalis: 3. Foraging, diet and diving behaviour. Emu 97:76-83
25. Grémillet D, Wanless S, Carss DN, Linton D, Harris MP, Speakman JR, Le Maho Y (2001) Foraging energetics of arctic cormorants and the evolution of diving birds. Ecol Lett 4:180-184 (Pubitemid 32516070)
26. Haccou P, Meelis E (1994) Statistical analysis of behavioural data: an approach based on time-structured models. Oxford University Press, Oxford
27. Heithaus MR, Wirsing AJ, Burkholder D, Thomson J, Dill LM (2009) Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics. J Anim Ecol 78:556-562
28. Hinke JT, Salwicka K, Trivelpiece SG, Watters GM, Trivelpiece WZ (2007) Divergent responses of Pygoscelis penguins reveal a common environmental driver. Oecologia 153:845-855 (Pubitemid 47389316)
29. Hobson KA, Clark RG (1993) Turnover of 13C in cellular and plasma reactions of blood: implications for nondestructive sampling in avian dietary studies. Auk 110:638-641
30. Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150:447-461
31. Ishikawa K, Watanuki Y (2002) Sex and individual differences in foraging behavior of Japanese cormorants in years of different prey availability. J Ethol 20:49-54 (Pubitemid 34766758)
32. Jenkins JM (1979) Foraging behavior of male and female Nuttall woodpeckers. Auk 96:418-420
33. Kato A, Nishiumi I, Naito Y (1996) Sexual differences in the diet of king cormorants at Macquarie Island. Polar Biol 16:75-77
34. Kato A, Watanuki Y, Shaughnessy P, Maho YL, Naito Y (1999) Intersexual differences in the diving behaviour of foraging subantarctic cormorant (Phalacrocorax albiventer) and Japanese cormorant (P. filamentosus). C R Acad Sci Paris. Sci Vie 322:557-562
35. Kato A, Watanuki Y, Nishiumi I, Kuroki M, Naito Y (2000) Variation in foraging and parental behavior of king cormorants.Auk 117:718-730 (Pubitemid 30491594)
36. Kato A, Watanuki Y, Naito Y (2001) Foraging and breeding performance of Japanese cormorants in relation to prey type. Ecol Res 16:745-758 (Pubitemid 33723027)
37. Kooyman GL, Kooyman TG (1995) Diving behaviour of Emperor penguins nurturing chicks at Coulman Island, Antarctica. Condor 97:536-549
38. Kooyman GL, Ponganis PJ (1990) Behavior and physiology of diving in emperor and king penguins. In: Davis LS, Darby J (eds) Penguin Biology. Academic Press, New York, p 229-242
39. Kooyman GL, Wahrenbrock EA, Castellini MA, Davis RW, Sinnett EE (1980) Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior. J Comp Physiol B 138:335-346
40. Kooyman GL, Castellini MA, Davis RW, Maure RA (1983) Aerobic diving limits of immature Weddell seals. J Comp Physiol 151:171-174
41. Le Boeuf BJ, Crocker DE, Costa DP, Blackwell SB, Webb PM, Houser DS (2000) Foraging ecology of northern elephant seals. Ecol Monogr 70:353-382
42. Lewis S, Benvenuti S, Dall'Antonia L, Griffith R and others (2002) Sex-specific foraging behaviour in a monomorphic seabird. Proc Biol Sci 269:1687-1693 (Pubitemid 34925524)
43. MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603-609
44. Malacalaza VE, Hall MA (1988) Sexing adult king cormorants (Phalacrocorax albiventer) by discriminant analysis. Colon Waterbirds 11:32-37
45. Malacalaza VE, Poretti TI, Bertellotti NM (1994) La dieta de Phalacrocorax albiventer en Punta León (Chubut, Ar gen -tina) durante la temporada reproductiva. Ornitol Neotrop 5:91-97
46. Masello JF, Mundry R, Poisbleau M, Demongin L, Voigt C, Wikelski M, Quillfeldt P (2010) Diving seabirds share foraging space and time within and among species. Eco - sphere 1:19
47. Mattern T, Ellenberg U, Houston DM, Davis LS (2007) Consistent foraging routes and benthic foraging behaviour in yellow-eyed penguins. Mar Ecol Prog Ser 343:295-306 (Pubitemid 47359806)
48. Michalik A, van Noordwijk H, Brickle P, Eggers T, Quillfeldt P (2010) The diet of the imperial shag Phalacrocorax atriceps at a colony on New Island, Falkland/Malvinas Islands combining different sampling techniques. Polar Biol 33: 1537-1546
49. Miller AK, Trivelpiece WZ (2008) Chinstrap penguins alter foraging and diving behavior in response to the size of their principle prey, Antarctic krill. Mar Biol 154:201-208
50. Miller AK, Karnovsky NJ, Trivelpiece WZ (2009) Flexible foraging strategies of gentoo penguins Pygoscelis papua over five years in the South Shetland Islands, Antarctica. Mar Biol 156:2527-2537
51. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135-1140
52. Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11:470-480 (Pubitemid 351499224)
53. Owens NJP (1987) Natural variations in 15N in the marine environment. Adv Mar Biol 24:389-451
54. Parnell A, Inger R, Bearhop S, Jackson AL (2008) Stable isotope analysis in R (SIAR). http://cran.r-project.org/web/packages/siar/index.html
55. Persson L (1985) Asymmetrical competition: Are larger animals competitively superior? Am Nat 126:261-266
56. Ponganis PJ, Kooyman GL, Starke LN, Kooyman CA, Kooyman TG (1997) Post-dive blood lactate concentrations in emperor penguins, Aptenodytes forsteri. J Exp Biol 200: 1623-1626 (Pubitemid 27268927)
57. Punta G, Yorio P, Herrera G (2003) Temporal patterns in the diet and food partitioning in imperial cormorants (Phalacrocoraxatriceps) and rock shags (P. magellanicus) breeding at Bahía Bustamante, Argentina. Wilson Bull 115:307-315 (Pubitemid 38536992)
58. Quillfeldt P, McGill RAR, Furness RW (2005) Diet and foraging areas of Southern Ocean seabirds and their prey inferred from stable isotopes: review and case study of Wilson's storm-petrel. Mar Ecol Prog Ser 295:295-304 (Pubitemid 41026831)
59. Quillfeldt P, Strange IJ, Masello JF (2007a) Sea surface temperatures and behavioural buffering capacity in thinbilled prions Pachyptila belcheri: breeding success, provisioning and chick begging. J Avian Biol 38:298-308 (Pubitemid 46699587)
60. Quillfeldt P, Poisbleau M, Chastel O, Masello JF (2007b) Corticosterone in thin-billed prion Pachyptila belcheri chicks: diel rhythm, timing of fledging and nutritional stress. Naturwissenschaften 94:919-925 (Pubitemid 47524758)
61. Quillfeldt P, McGill R, Strange IJ, Masello JF, Weiss F, Brickle P, Furness RW (2008) Stable isotope analysis reveals sexual and environmental variability and individual consistency in foraging of thin-billed prions. Mar Ecol Prog Ser 373:137-148
62. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
63. Quintana F (2008) Foraging behaviour and feeding locations of rock shags (Phalacrocorax magellanicus) from a colony in Patagonia, Argentina. Ibis 143:547-553
64. Quintana F, Wilson RP, Yorio P (2007) Dive depth and plumage air in wettable birds: the extraordinary case of the imperial cormorant. Mar Ecol Prog Ser 334:299-310 (Pubitemid 46657929)
65. Quintana F, Wilson RP, Dell'Archipetre P, Shepard E, Gómez Laigh A (2011) Women from Venus, men from Mars: intersex foraging differences in the imperial cormorant Phalacrocorax atriceps, a colonial seabird. Oikos 120:350-358
66. R Development Core Team 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
67. Ropert-Coudert Y, Wilson RP, Daunt F, Kato A (2004) A finescal etime budget of Cape gannets provides insight into the foraging strategies of coastal seabirds. Anim Behav 67:985-992 (Pubitemid 38617326)
68. Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2:369-404
69. Schreer JF, Kovacs KM (1997) Allometry of diving capacity in air-breathing vertebrates. Can J Zool 75:339-358
70. Schreiber EA, Burger J (2001) Biology of marine birds. CRC Press, Boca Raton
71. Shaffer SA, Weimerskirch H, Costa DP (2001) Functional significance of sexual dimorphism in wandering albatrosses, Diomedea exulans. Funct Ecol 15:203-210 (Pubitemid 32329108)
72. Shepard ELC, Wilson PR, Quintana F, Gómez Laich A, Forman DW (2009) Pushed for time or saving on fuel: finescale energy budgets shed light on currencies in a diving bird. Proc Biol Sci 276:3149-3155
73. Shepard ELC, Wilson PR, Gómez Laich A, Quintana F (2010) Buoyed up and slowed down: speed limits for diving birds in shallow water. Aquat Biol 8:259-267
74. Siegel-Causey D (1988) Phylogeny of the Phalacrocoracidae. Condor 90:885-905
75. Suryan RM, Sato F, Balogh GR, Hyrenbach KD, Sievert PR, Ozaki K (2006) Foraging destinations and marine habitat use of short-tailed albatrosses: a multi-scale approach using first-passage time analysis. Deep-Sea Res II 53: 370-386 (Pubitemid 43817532)
76. SvageljW, Quintana F (2007) Sexual size dimorphism and sex determination by morphometric measurements in breeding imperial shags (Phalacrocorax atriceps). Waterbirds 30:97-102 (Pubitemid 46882170)
77. Takahashi A, Sato K, Naito Y, Dunn MJ, Trathan PN, Croxall JP (2004) Penguin-mounted cameras glimpse underwater group behaviour. Proc Biol Sci 271(Suppl):S281-S282 (Pubitemid 38998725)
78. Thaxter CB, Daunt F, Hamer KC, Watanuki Y and others (2009) Sex-specific food provisioning in a monomorphic seabird, the common guillemot Uria aalge: Nest defence, foraging efficiency or parental effort? J Avian Biol 40: 75-84
79. Thompson KR (1989) An assessment of the potential for competition between seabirds and fisheries in the Falkland Islands. Falkland Islands Foundation, Brighton, UK
80. Thompson KR (1994) Predation on Gonatus antarcticus by Falkland Islands seabirds. Antarct Sci 6:269-274
81. Tremblay Y, Cherel Y (2000) Benthic and pelagic dives: a new foraging behaviour in rockhopper penguins. Mar Ecol Prog Ser 204:257-267
82. Tremblay Y, Cook TR, Cherel Y (2005) Time budget and diving behaviour of chick-rearing Crozet shags. Can J Zool 83:971-982 (Pubitemid 41587267)
83. Trivelpiece WZ, Trivelpiece SG, Volkman NJ (1987) Ecological segregation of Adelie, gentoo and chinstrap penguins at King George Island, Antarctica. Ecology 68:351-361
84. Van Tets GF (1976) Australasia and the origin of shags and cormorants, Phalacrocoracidae. In: Frith HV, Calaby JH (eds) Proc 16th Ann Ornith Congr, Canberra, p 121-124
85. Walton P, Ruxton GD, Monaghan P (1998) Avian diving, respiratory physiology and the marginal value theorem. Anim Behav 56:165-174 (Pubitemid 28348971)
86. Wanless S, Harris MP, Morris JA (1992) Diving behaviour and diet of the blue-eyed shag at South Georgia. Polar Biol 12:713-719 (Pubitemid 24406814)
87. Wanless S, Harris MP, Morris JA (1995) Factors affecting daily activity budgets of South Georgian shags during chick rearing at Bird Island, South Georgia. Condor 97:550-558
88. Watanuki Y, Kato A, Naito Y (1996) Diving performance of male and female Japanese cormorants. Can J Zool 74: 1098-1109
89. Weimerskirch H, Cherel Y, Cuenot-Chaillet F, Ridoux V (1997) Alternative foraging strategies and resource allocation by male and female wandering albatrosses. Ecology 78:2051-2063
90. Willmer P, Stone G, Johnston IA (2005) Environmental physiology of animals, 2nd edn. Blackwell Publishing, Malden, Massachusetts
91. Wilson RP (1995) Foraging ecology. In: Williams TD (ed) The penguins. Oxford University Press, Oxford, p 81-106
92. Wilson RP, Quintana F (2004) Surface pauses in relation to dive duration in imperial cormorants: How much time for a breather? J Exp Biol 207:1789-1796 (Pubitemid 38826053)
93. Wilson RP, Wilson MP (1988) Dead reckoning: a new technique for determining penguin movements at sea. Meeres forschung 32:155-158
94. Wilson RP, Wilson MPT, Link R, Mempel H, Adams NJ (1991) Determination of movements of African penguins Sphe - niscus demersus using a compass system: Dead reckoning may be an alternative to telemetry. J.Exp.Biol 157:557-564
95. Woo K, Kober K, Gaston AJ (1999) Difference in timing of incubation shifts between male and female thick-billed murres are associated with variation in maximum diving depth. Pacific Seabirds 26:55
96. Wood AG, Naef-Daenzer B, Prince PA, Croxall JP (2000) Quantifying habitat use in satellite-tracked pelagic seabirds: application of kernel estimation to albatross locations. J Avian Biol 31:278-286
97. Yorio P, Copello S, Kuba L, Gosztonyi A, Quintana F (2010) Diet of imperial cormorants Phalacrocorax atricep breeding at central Patagonia, Argentina. Waterbirds 33:70-78