Cost of Living Dictates what Whales, Dolphins and Porpoises Eat: The Importance of Prey Quality on Predator Foraging Strategies

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Spitz, Jérôme ^a,b   Trites, Andrew W ^c   Becquet, Vanessa ^a   Brind'Amour, Anik ^d   Cherel, Yves ^e   Galois, Robert ^a   Ridoux, Vincent ^a  

^a UNIVERSITÉ DE LA ROCHELLE   (France)

^b Parc zoologique de La Flèche ^*  (France)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d IFREMER   (France)

^e CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID;

ANIMAL CELL; ARTICLE; BODY SIZE; CELL DENSITY; CONTROLLED STUDY; DIETARY INTAKE; DOLPHIN; ECOLOGY; FOOD QUALITY; FORAGING; MARINE ENVIRONMENT; METABOLIC COST OF LIVING; METABOLIC PARAMETERS; METABOLIC RATE; MITOCHONDRION; MUSCLE FUNCTION; NONHUMAN; NORTH ATLANTIC DEEP WATER; PHYLOGENY; PORPOISE; PREDATOR; PREDICTION; PREY; WHALE;

ANIMALS; BIOLOGICAL EVOLUTION; BODY SIZE; DIET; DOLPHINS; EATING; ENERGY METABOLISM; FEEDING BEHAVIOR; FOOD CHAIN; PHYLOGENY; PORPOISES; PREDATORY BEHAVIOR; SPECIES SPECIFICITY; WHALES;

CETACEA;

EID: 84869793876     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050096     Document Type: Article

References (72)

1. Bozinovic F, Bacigalupe LD, Vasquez RA, Henk Visser G, Veloso C, et al. (2004) Cost of living in free-ranging degus (Octodon degus): seasonal dynamics of energy expenditure. Comp. Bioch. Phys. A 137: 597-604.
2. Hulbert AJ, Else PL, (2000) Mechanisms underlying the cost of living in animals. Ann. Rev. Physiol. 62: 207-235.
3. Sheriff MJ, Speakman JR, Kuchel L, Boutin S, Humphries MM, (2009) The cold shoulder: free-ranging snowshoe hares maintain a low cost of living in cold climates. Can. J. Zool. 87: 956-964.
4. Kleiber M (1975) The fire of life: an introduction to animal energetics. Kreiger. Huntington, NY.
5. Nagy KA, (2005) Field metabolic rate and body size. J. Exp. Biol 208: 1621-1625.
6. Feldhamer GA (2007) Mammalogy: adaptation, diversity, ecology. Johns Hopkins Univ Pr.
7. Grant BR, Grant PR (1989) Natural selection in a population of Darwin's finches. Am. Nat.: 377-393.
8. Perry G, Pianka ER, (1997) Animal foraging: past, present and future. Trends Ecol. Evol. 12: 360-364.
9. Emlen JM, (1966) The role of time and energy in food preference. Am. Nat. 100: 611-617.
10. MacArthur RH, Pianka ER, (1966) On optimal use of a patchy environment. Am. Nat. 100: 603-609.
11. Charnov EL, (1976) Optimal foraging: Attack strategy of a mantid. Am. Nat. 110: 141-151.
12. Sih A, Christensen B, (2001) Optimal diet theory: When does it work, and when and why does it fail? Anim. Behav. 61: 379-390.
13. Österblom H, Olsson O, Blenckner T, Furness RW, (2008) Junk-food in marine ecosystems. Oikos 117: 967-977.
14. Trites AW, Donnelly CP, (2003) The decline of Steller sea lions Eumetopias jubatus in Alaska: A review of the nutritional stress hypothesis. Mam. Rev. 33: 3-28.
15. Berta A, Sumich JL, Kovak K (2008) Marine mammals: Evolutionary biology, 2nd edition. Academic press. San Diego.
16. Spitz J, Mourocq E, Leauté J-P, Quéro J-C, Ridoux V, (2010) Prey selection by the common dolphin: Fulfilling high energy requirements with high quality food. J. Exp. Mar. Biol. Ecol. 390: 73-77.
17. Yodzis P, (2001) Must top predators be culled for the sake of fisheries? Trends Ecol. Evol. 16: 78-84.
18. Jeanniard du Dot T, Rosen DA, Richmond JP, Kitaysky AS, Zinn SA, et al. (2009) Changes in glucocorticoids, IGF-I and thyroid hormones as indicators of nutritional stress and subsequent refeeding in Steller sea lions (Eumetopias jubatus). Comp. Bioch. Phys. A 152: 524-534.
19. Rosen DAS, Trites AW, (2004) Satiation and compensation for short-term changes in food quality and availability in young Steller sea lions (Eumetopias jubatus). Can. J. Zool. 82: 1061-1069.
20. Börjesson P, Berggren P, Ganning B, (2003) Diet of harbor porpoises in the Kattegat and Skagerrak seas: Accounting for individual variation and sample size. Mar. Mammal. Sci. 19: 38-58.
21. Fernández R, Santos MB, Carrillo M, Tejedor M, Pierce GJ, (2009) Stomach contents of cetaceans stranded in the Canary Islands 1996-2006. J. Mar. Biol. Assoc. UK 89: 873-883.
22. González AF, López A, Guerra A, Barreiro A, (1994) Diets of marine mammals stranded on the northwestern Spanish Atlantic coast with special reference to Cephalopoda. Fish. Res. 21: 179-191.
23. Lockyer C, (1986) Body fat condition in Northeast Atlantic fin whales, Balaenoptera physalus, and its relationship with reproduction and food resource. Can. J. Fish. Aquat. Sci. 43: 142-147.
24. López A (2002) Estatus dos pequenos cetáceos da plataforma de Galicia [PhD thesis]. Universidad de Santiago de Compostela.
25. Meynier L, Pusineri C, Spitz J, Santos MB, Pierce GJ, et al. (2008) Intraspecific dietary variation in the short-beaked common dolphin Delphinus delphis in the Bay of Biscay: importance of fat fish. Mar. Ecol. Prog. Ser. 354: 277-287.
26. Olsen E, Holst JC, (2001) A note on common minke whale (Balaenoptera acutorostrata) diets in the Norwegian Sea and the North Sea. J. Cet. Res. Manag. 3: 179-184.
27. Pierce GJ, Santos MB, Reid RJ, Patterson IAP, Ross HM, (2004) Diet of minke whales Balaenoptera acutorostrata in Scottish (UK) waters with notes on strandings of this species in Scotland 1992-2002. J. Mar. Biol. Assoc. UK 84: 1241-1244.
28. Santos MB, Pierce GJ, Boyle PR, Reid RJ, Ross HM, et al. (1999) Stomach contents of sperm whales Physeter macrocephalus stranded in the North Sea 1990-1996. Mar. Ecol. Prog. Ser. 183: 281-294.
29. Santos MB, Pierce GJ, Reid RJ, Patterson IAP, Ross HM, et al. (2001) Stomach contents of bottlenose dolphins (Tursiops truncatus) in Scottish waters. J. Mar. Biol. Assoc. UK 81: 873-878.
30. Santos MB, Pierce GJ, López A, Reid RJ, Ridoux V, et al. (2006) Pygmy sperm whales Kogia breviceps in the Northeast Atlantic: New information on stomach contents and strandings. Mar. Mammal Sci. 22: 600-616.
31. Santos MB, Pierce GJ, Learmonth JA, Reid RJ, Ross HM, et al. (2004) Variability in the diet of harbor porpoises (Phocoena phocoena) in Scottish waters 1992-2003. Mar. Mammal Sci. 20: 1-27.
32. Santos MB, Pierce GJ, López A, Martínez JA, Fernández MT, et al. (2004) Variability in the diet of common dolphins (Delphinus delphis) in Galician waters 1991-2003 and relationship with prey abundance. ICES CM 2004: 09.
33. Santos MB, Pierce GJ, Herman J, López A, Guerra A, et al. (2001) Feeding ecology of Cuvier's beaked whale (Ziphius cavirostris): A review with new information on the diet of this species. J. Mar. Biol. Assoc. UK 81: 687-694.
34. Santos MB, Pierce GJ, García Hartmann M, Smeenk C, Addink MJ, et al. (2002) Additional notes on stomach contents of sperm whales Physeter macrocephalus stranded in the north-east Atlantic. J. Mar. Biol. Assoc. UK 82: 501-507.
35. Santos MB, Pierce GJ, Learmonth JA, Reid RJ, Sacau M, et al. (2008) Strandings of striped dolphin Stenella coeruleoalba in Scottish waters (1992-2003) with notes on the diet of this species. J. Mar. Biol. Assoc. UK 88: 1175-1183.
36. Santos MB, Fernández R, López A, Martínez JA, Pierce GJ, (2007) Variability in the diet of bottlenose dolphin, Tursiops truncatus, in Galician waters, north-western Spain, 1990-2005. J. Mar. Biol. Assoc. UK 87: 231-241.
37. Santos MB, Martin V, Arbelo M, Fernández A, Pierce GJ, (2007) Insights into the diet of beaked whales from the atypical mass stranding in the Canary Islands in September 2002. J. Mar. Biol. Assoc. UK 87: 243-251.
38. Sigurjónsson J, Galan A, Vikingsson GA, (2000) A note on stomach contents of minke whales (Balaenoptera acutorostrata) in Icelandic waters. NAMMCO Sci. Publi. 2: 82-90.
39. Silva MA, (1999) Diet of common dolphins, Delphinus delphis, off the Portuguese continental coast. J. Mar. Biol. Assoc. UK 79: 531-540.
40. Sivertsen SP, Pedersen T, Lindstrøm U, Haug T, (2006) Prey partitioning between cod (Gadus morhua) and minke whale (Balaenoptera acutorostrata) in the Barents Sea. Mar. Biol. Res. 2: 89-99.
41. Spitz J, Cherel Y, Bertin S, Kiszka J, Dewez A, et al. (2011) Prey preferences among the community of deep-diving odontocetes from the Bay of Biscay, Northeast Atlantic. Deep Sea Res. I.
42. Spitz J, Richard E, Meynier L, Pusineri C, Ridoux V, (2006) Dietary plasticity of the oceanic striped dolphin, Stenella coeruleoalba, in the neritic waters of the Bay of Biscay. J. Sea Res. 55: 309-320.
43. Spitz J, Rousseau Y, Ridoux V, (2006) Diet overlap between harbour porpoise and bottlenose dolphin: An argument in favour of interference competition for food? Estuar. Coast. Shelf Sci. 70: 259-270.
44. Vikingsson GA, Olafsdottir D, Sigurjónsson J, (2003) Geographical and seasonal variation in the diet of harbour porpoises (Phocoena phocoena) in Icelandic coastal waters. NAMMCO Sci. Publi. 5: 243-270.
45. Wurtz M, Marrale D, (1993) Food of striped dolphin, Stenella coeruleoalba, in the Ligurian Sea. J. Mar. Biol. Assoc. UK 73: 571-578.
46. Víkingsson GA, (1997) Feeding of fin whales (Balaenoptera physalus) off Iceland-diurnal and seasonal variation and possible rates. J. Northw. Atl. Fish. Sci 22: 77-89.
47. Pierce GJ, Boyle PR, (1991) A review of methods for diet analysis in piscivorous marine mammals. Oceanogr. Mar. Biol. 29: 409-486.
48. Spitz J, Mourocq E, Schoen V, Ridoux V, (2010) Proximate composition and energy content of forage species from the Bay of Biscay: High- or low-quality food? ICES J. Mar. Sci. 67: 909-915.
49. Clarke A, Clarke MR, Holmes LJ, Waters TD, (1985) Calorific values and elemental analysis of eleven species of oceanic squids (Mollusca: Cephalopoda). J. Mar. Biol. Assoc. UK 65: 983-986.
50. Lieber RL (2002) Skeletal muscle structure, function & plasticity: the physiological basis of rehabilitation. Baltimore, MD/Philadelphia, PA: Lippincott Williams & Wilkins.
51. Rich P, (2003) Chemiosmotic coupling: the cost of living. Nature 421: 583-583.
52. Folch J, Lees M, Sloane Stanley GH, (1957) A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: 497-509.
53. Ward JH, (1963) Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58: 236-244.
54. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing Vienna Austria, ISBN 3-900051-07-0.
55. West GB, Brown JH, Enquist BJ, (1997) A general model for the origin of allometric scaling laws in biology. Science 276: 122-126.
56. Muñoz-Garcia A, Williams JB, (2005) Basal metabolic rate in carnivores is associated with diet after controlling for phylogeny. Physiol. Bioch. Zool. 78: 1039-1056.
57. Davis RW, Fuiman LA, Williams TM, Collier SO, Hagey WP, et al. (1999) Hunting behavior of a marine mammal beneath the Antarctic fast ice. Science 283: 993.
58. Williams TM, Estes JA, Doak DF, Springer AM, (2004) Killer appetites: assessing the role of predators in ecological communities. Ecology 85: 3373-3384.
59. Pierce GJ, Santos MB, Cerviño S, (2007) Assessing sources of variation underlying estimates of cetacean diet composition: A simulation study on analysis of harbour porpoise diet in Scottish (UK) waters. J. Mar. Biol. Assoc. UK 87: 213-221.
60. Tollit DU, Steward MJ, Thompson PM, Pierce GJ, Santos MB, et al. (1997) Species and size differences in the digestion of otoliths and beaks: Implications for estimates of pinniped diet composition. Can. J. Fish. Aquat. Sci. 54: 105-119.
61. McNab BK (1986) The influence of food habits on the energetics of eutherian mammals. Ecol. Monogr.: 1-19.
62. Cruz-Neto AP, Bozinovic F, (2004) The relationship between diet quality and basal metabolic rate in endotherms: insights from intraspecific analysis. Physiol. Bioch. Zool. 77: 877-889.
63. Bundle MW, Hoppeler H, Vock R, Tester JM, Weyand PG, (1999) High metabolic rates in running birds. Nature 397: 31-32.
64. Evans M, Green B, Newgrain K, (2003) The field energetics and water fluxes of free-living wombats (Marsupialia: Vombatidae). Oecologia 137: 171-180.
65. Stephens DW, Krebs JR (1986) Foraging theory. Princeton Univ Pr.
66. Hou C, Zuo W, Moses ME, Woodruff WH, Brown JH, et al. (2008) Energy uptake and allocation during ontogeny. Science 322: 736-739.
67. Perrin N, Sibly RM (1993) Dynamic models of energy allocation and investment. Ann. Rev. Ecol. Syst.: 379-410.
68. Gittleman JL, Thompson SD, (1988) Energy allocation in mammalian reproduction. Am. Zool. 28: 863-875.
69. Trillmich F, (1996) Parental investment in pinnipeds. Adv. Stud. Behav. 25: 533-577.
70. Cheung WWL, Lam VWY, Sarmiento JL, Kearney K, Watson R, et al. (2009) Projecting global marine biodiversity impacts under climate change scenarios. Fish Fish. 10: 235-251.
71. Dulvy NK, Rogers SI, Jennings S, Stelzenmüller V, Dye SR, et al. (2008) Climate change and deepening of the North Sea fish assemblage: A biotic indicator of warming seas. J. Appl. Ecol. 45: 1029-1039.
72. Price SA, Bininda-Emonds OR, Gittleman JL, (2005) A complete phylogeny of the whales, dolphins and even-toed hoofed mammals (Cetartiodactyla). Biological reviews 80: 445-473.