Abstract
Foraging theory proposes that the nutritional driver of food choice and foraging in carnivores is energy gain. In contrast, recent laboratory experiments have shown that several species of carnivore select prey that provides a diet with a specific balance of macronutrients, rather than the highest energy content. It remains, however, to be determined how nutritionally variable the foods of predators in the wild are, and whether they feed selectively from available prey to balance their diet. Here, we used a geometric method named the right-angled mixture triangle (RMT) for examining nutritional variability in the prey and selected diets of a group of wild carnivores and marine top predators, the gannets (Morus spp.). A prey-level diet analysis was performed on Australasian gannets (M. serrator) from two New Zealand locations, and the macronutrient composition of their chosen prey species was measured. We use RMT to extend the comparison in the compositions of foods and diets from Australasian gannets from Australia as well as Northern gannets (M. bassanus) and Cape gannets (M. capensis). We found nutritional variability at multiple scales: intra- and interspecific variability in the pelagic fish and squid prey themselves; and intra- and interspecific variability in the diets consumed by geographically disparate populations of gannets. This nutritional variability potentially presents these predatory seabirds with both opportunity to select an optimal diet, and constraint if prevented from securing an optimal diet.
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References
Adams N, Abrams R, Siegrfried W, Nagy K, Kaplan I (1991) Energy expenditure and food consumption by breeding Cape gannets Morus capensis. Mar Ecol Prog Ser 70:1–9
Annett CA, Pierotti R (1999) Long-term reproductive output in western gulls: consequences of alternate tactics in diet choice. Ecology 80:288–297
AOAC (2005) Official methods of analysis of AOAC International, 18th edn. AOAC International, Arlington
Bunce A (2001) Prey consumption of Australasian gannets (Morus serrator) breeding in Port Phillip Bay, southeast Australia, and potential overlap with commercial fisheries. ICES J Mar Sci 58:904–915
Chambers PG, Simpson SJ, Raubenheimer D (1995) Behavioural mechanisms of nutrient balancing in Locusta migratoria nymphs. Anim Behav 50:1513–1523
Cherel Y, Hobson KA, Weimerskirch H (2000) Using stable-isotope analysis of feathers to distinguish moulting and breeding origins of seabirds. Oecologia 122:155–162
Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005) Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888
Davies DH (1956) The South African pilchard (Sardinops ocellata) and maasbanker (Trachurus trachurus) bird predators, 1954–1955. South African Department of Commerce and Industry, Division of Fisheries Investigational Report 23
Duffy DC, Jackson S (1986) Diet studies of seabirds: a review of methods. Colon Waterbird 9:1–17
Ellis HI (1984) Energetics of free-ranging seabirds. In: Whittow GC, Rahn H (eds) Seabird energetics. Springer, New York, pp 203–234
Evans P, Halliwell B (2001) Micronutrients: oxidant/antioxidant status. Br J Nutr 85:S67–S74
Fryxell JM, Lundberg P (1997) Individual behavior and community dynamics. Chapman and Hall, New York
Furness RW (1978) Energy requirements of seabird communities: a bioenergetics model. J Anim Ecol 47:39–53
Galef BG (1996) Food selection: problems in understanding how we choose foods to eat. Neurosci Biobehav Rev 20:67–73
Garthe S, Montevecchi WA, Davoren GK (2011) Inter-annual changes in prey fields trigger different foraging tactics in a large marine predator. Limnol Oceanogr 56:802–812
Grémillet D, Pichegru L, Kuntz G, Woakes AG, Wilkinson S, Crawford RJM, Ryan PG (2008) A junk-food hypothesis for gannets feeding on fishery waste. Proc R Soc Lond Biol 275:1149–1156
Hamer KC, Phillips RA, Wanless S, Harris MP, Wood AG (2000) Foraging ranges, diets and feeding locations of gannets (Morus bassanus) in the North Sea: evidence from satellite telemetry. Mar Ecol Prog Ser 200:257–264
Hamer KC, Humphreys EM, Wanless S, Garthe S, Hennicke J, Peters G, Phillips RA, Harris MP (2007) Annual variation in diets, feeding locations and foraging behaviour of gannets in the North Sea: flexibility, consistency and constraint. Mar Ecol Prog Ser 338:295–305
Hawkins JM (1988) The Farewell Spit gannetry—a new sea level colony. Notornis 35:249–260
Hegseth MN, Camus L, Helgason LB, Bocchetti R, Gabrielsen GW, Regoli F (2011) Hepatic antioxidant responses related to levels of PCBs and metals in chicks of three Arctic seabird species. Comp Biochem Physiol C Toxicol Pharmacol 154:28–35
Jarvis MJF (1970) Interactions between man and the South African Gannet Sula capensis. Ostrich 40(Suppl. 8):497–513
Lea MA, Cherel Y, Guinet C, Nichols PD (2002) Antarctic fur seals foraging in the polar frontal zone: inter-annual shifts in diet as shown from fecal and fatty acid analyses. Mar Ecol Prog Ser 245:281–297
Lenky C, Eisert R, Oftedal OT, Metcalf V (2012) Proximate composition and energy density of nototheniid and myctophid fish in McMurdo Sound and the Ross Sea, Antarctica. Polar Biol 35:717–724
Lucas A, Morales J, Velando A (2014) Differential effects of specific carotenoids on oxidative damage and immune response of gull chicks. J Exp Biol 217:1253–1262
Machovsky-Capuska GE, Vaughn RL, Würsig B, Katzir G, Raubenheimer D (2011a) Dive strategies and foraging effort in the Australasian gannet Morus serrator revealed by underwater videography. Mar Ecol Prog Ser 442:255–261
Machovsky-Capuska GE, Dwyer SL, Alley MR, Stockin KA, Raubenheimer D (2011b) Evidence for fatal collisions and kleptoparasitism while plunge diving in gannets. Ibis 153:631–635
Machovsky-Capuska GE, Howland HC, Vaughn RL, Würsig B, Raubenheimer D, Hauber ME, Katzir G (2012) Visual accommodation and active pursuit of prey underwater in a plunge diving bird: the Australasian gannet. Proc R Soc B 279:4118–4125
Machovsky-Capuska GE, Hauber ME, Libby E, Amiot C, Raubenheimer D (2013) The contribution of private and public information in foraging by Australasian gannets. Anim Cogn 17:849–858
Machovsky-Capuska GE, Hauber ME, Dassis M, Libby E, Wikelski MC, Schuckard R, Melville D, Cook W, Houston M, Raubenheimer D (2014) Foraging behaviour and habitat use of chick-rearing Australasian Gannets in New Zealand. J Ornithol 155:379–387
Manighetti B, Carter L (1999) Across-shelf sediment dispersal, Hauraki Gulf, New Zealand. Mar Geol 160:271–300
Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005) Nutrient-specific foraging in invertebrate predators. Science 307:111–113
Mayntz D, Nielsen VH, Sørensen A, Toft S, Raubenheimer D, Hejlesen C, Simpson SJ (2009) Balancing of protein and lipid intake by a mammalian carnivore, the mink Mustela vison. Anim Behav 77:349–355
Meynier L, Stockin KA, Bando MKH, Duignan PJ (2008) Stomach contents of common dolphin (Delphinus sp.) from New Zealand waters. NZ J Mar Freshw 42:257–268
Montevecchi WA, Ricklefs RE, Kirkham IR, Gabaldon D (1984) Growth energetics of nestling northern gannets (Sula bassanus). Auk 101:334–341
Nelson JB (2005) Pelicans, cormorants and their relatives. Oxford University Press, Oxford
Nie Y, Zhang Z, Raubenheimer D, Elser JJ, Wei W, Wei F (2014) Obligate herbivory in an ancestrally carnivorous lineage: the giant panda and bamboo from the perspective of nutritional geometry. Funct Ecol. doi:10.1111/1365-2435.12302
Paddack MJ, Cowen RK, Sponaugle S (2006) Grazing pressure of herbivorous coral reef fishes on low coral-cover reefs. Coral Reefs 25:461–472
Paulin C, Stewart A, Roberts C, McMillan P (1989) New Zealand Fish: a complete guide. In: National museum of New Zealand miscellaneous series no. 19
Petry MV, Fonseca VSD, Scherer AL (2007) Analysis of stomach contents from the black-browed albatross, Thalassarche melanophris, on the coast of Rio grande do sul, southern Brazil. Polar Biol 30:321–325
Pichegru L, Ryan P, van der Lingen C, Coetzee J, Ropert-Coudert Y, Grémillet D (2007) Foraging behaviour and energetics of Cape gannets Morus capensis feeding on live prey and fishery discards in the Benguela upwelling system. Mar Ecol Prog Ser 350:127–136
Polis GA, Holt RD (1992) Intraguild predation—the dynamics of complex trophic interactions. Trends Ecol Evol 7:151–154
Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330
Raubenheimer D (2011) Toward a quantitative nutritional ecology: the right-angled mixture triangle. Ecol Monogr 81:407–427
Raubenheimer D, Jones SA (1996) Nutritional imbalance in an extreme generalist omnivore: tolerance and recovery through complementary food selection. Anim Behav 71:1253–1262
Raubenheimer D, Simpson SJ (2006) The challenge of supplementary feeding: can geometric analysis help save the kakapo? Notornis 53:100–111
Raubenheimer D, Mayntz D, Simpson SJ, Toft S (2007) Nutrient-specific compensation following diapause in a predator: implications for intraguild predation. Ecology 88:2598–2608
Raubenheimer D, Machovsky-Capuska GE, Gosby AK, Simpson S (2014) The nutritional ecology of obesity: from humans to companion animals. Br J Nutr. doi:10.1017/S0007114514002323
Richoux NB, Jaquemet S, Bonnevie BT, Cherel Y, McQuaid CD (2010) Trophic ecology of grey-headed albatrosses from Marion Island, Southern Ocean: insights from stomach contents and diet tracers. Mar Biol 157:1755–1766
Robertson D (1992) Diet of the Australasian gannet Morus serrator (G.R. Gray) around New Zealand. N Z J Ecol 16:77–81
Ropert-Coudert Y, Grémillet D, Kato A, Ryan P, Naito Y, Le Maho Y (2004) A fine-scale time budget of Cape gannets provides insights into the foraging strategies of coastal seabirds. Anim Behav 67:985–992
Rothman JM, Raubenheimer D, Chapman CA (2011) Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein. Biol Lett 7:847–849
Rubio V, Sanchez F, Zamora S, Madrid J (2008) Endogenous modification of macronutrient selection pattern in sea bass (Dicentrarchus labrax). Physiol Behav 95:32–35
Rubio VC, Navarro DB, Madrid JA, Sanchez-Vazquez FJ (2009) Macronutrient self-selection in Solea senegalensis fed macronutrient diets and challenged with dietary protein dilutions. Aquaculture 291:95–100
Schuckard R, Melville DS, Cook W, Machovsky-Capuska GE (2012) Diet of the Australasian gannet (Morus serrator) at Farewell Spit, New Zealand. Notornis 59:66–70
Simpson SJ, Raubenheimer D (2012) The nature of nutrition: an integrative framework from animal adaptation to human obesity. Princeton University Press, Princeton
Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton
Votier SC, Bearhop S, MacCormick A, Ratcliffe N, Furness RW (2003) Assessing the diet of great skuas, Catharacta skua, using five different techniques. Polar Biol 26:20–26
Votier SC, Bearhop S, Witt MJ, Inger R, Thompson D, Newton J (2010) Individual responses of seabirds to commercial fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems. J Appl Ecol 47:487–497
Wanless S, Harris MP, Redman P, Speakman JR (2005) Low energy values of fish as a probable cause of a major seabird breeding failure in the North Sea. Mar Ecol Prog Ser 294:1–8
Westoby M (1974) An analysis of diet selection by large generalist herbivores. Am Nat 108:290–304
Westoby M (1978) What are biological bases of varied diets? Am Nat 112:627–631
Wilder SM, Eubanks MD (2010) Might nitrogen limitation promote omnivory among carnivorous arthropods? Comment. Ecology 91:3114–3117
Wingham EJ (1985) Food and feeding range of the Australasian gannet Morus serrator (gray). Emu 85:231–239
Wingham E (1989) Energy requirements of Australasian gannets Morus serrator (Gray) at a breeding colony. Emu 89:65–70
Work TM (2000) Avian necropsy manual for biologists in remote refuges. US Geological Survey, National Wildlife Health Centre, Hawaii Field Station, Honolulu
Acknowledgments
We thank Sarah Dwyer, Rob Schuckard, Willie Cook, David Melville, Danny Boulton, Karen and Sabrina Machovsky and Sonja Clements for their assistance with sample collection. We also thank the anonymous reviewers for helpful comments on early versions of the manuscript. Aspects of this work were funded by Massey University Research Fund (MURF) and Faculty of Veterinary Science (The University of Sydney). Samples were collected under Department of Conservation permits NM-32772-FAU and AK-26359-FAU.
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Communicated by Y. Cherel.
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Tait, A.H., Raubenheimer, D., Stockin, K.A. et al. Nutritional geometry and macronutrient variation in the diets of gannets: the challenges in marine field studies. Mar Biol 161, 2791–2801 (2014). https://doi.org/10.1007/s00227-014-2544-1
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DOI: https://doi.org/10.1007/s00227-014-2544-1