Abstract
Evolved patterns of resource expenditure for reproduction have resulted in a life history continuum across species. A strictly capital-breeding strategy relies extensively on stored energy for reproduction, whereas income breeding uses energy acquired throughout the reproductive period. However, facultative income breeding has been shown in some classically capital-breeding animals, and was originally thought to provide a nutritional refuge for smaller females incapable of securing sufficient reserves during pre-partum foraging. We examined milk composition and milk output for the Weddell seal to determine to what degree lactation was aided by food intake, and what factors contributed to its manifestation. Milk composition was independent of maternal post-partum mass and condition, but did change over lactation. Changes were most likely in response to energetic and nutritional demands of the pup at different stages of development. During early lactation, females fasted and devoted 54.9% of total energy loss to milk production. Later in lactation 30.5% more energy was devoted to milk production and evidence suggested that larger females fed more during lactation than smaller females. It appears that Weddell seals may exhibit a flexible strategy to adjust reproductive investment to local resource levels by taking advantage of periods when prey are occasionally abundant, although it is restricted to larger females possessing the physiological capacity to dive for longer and exploit different resources during lactation. This supports the assumption that although body mass and phylogenetic history explain most of the variation in lactation patterns (20–69%), the remaining variation has likely resulted from physiological adaptations to local environmental conditions. Our study confirms that Weddell seals use a mixed capital–income breeding strategy, and that considerable intraspecific variation exists. Questions remain as to the amount of energy gain derived from the income strategy, and the consequences for pup condition and survival.
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References
Arnould JPY, Boyd IL (1995) Inter- and intra-annual variation in milk composition in Antarctic fur seals (Arctocephalus gazella). Physiol Zool 68:1164–1180
Blaxter K (1989) Energy metabolism in animals and man. Cambridge University Press, Cambridge
Bligh EG, Dyer WJ (1959) A rapid method of lipid extraction and purification. Can J Biochem Physiol 37:911–917
Bonnet X, Bradshaw D, Shine R (1998) Capital versus income breeding: an ectothermic perspective. Oikos 83:333–342
Bowen WD, Iverson SJ, Boness DJ, Oftedal OT (2001) Foraging effort, food intake and lactation performance depend on maternal mass in a small phocid seal. Funct Ecol 15:325–334
Boyd IL (1998) Time and energy constraints in pinniped lactation. Am Nat 152:717–728
Boyd IL (2000) State-dependent fertility in pinnipeds: contrasting capital and income breeders. Funct Ecol 14:623–630
Burnham KP, Anderson DR (2002) Model selection and multimodal inference: a practical information-theoretic approach. Springer, New York
Casas J, Pincebourde S, Mandon N, Vannier F, Poujol R, Giron D (2005) Lifetime nutrient dynamics reveal simultaneous capital and income breeding in a parasitoid. Ecology 86:545–554
Clayton JR, Dortch Q, Thoresen SS, Ahmed SI (1988) Evaluation of methods for the separation and analysis of proteins and free amino acids in phytoplankton samples. J Plankton Res 10:341–358
Costa DP, LeBoeuf BJ, Huntley AC, Ortiz CL (1986) The energetics of lactation in the northern elephant seal, Mirounga angustirostris. J Zool (Lond) 209:21–33
de Little SC, Bradshaw CJA, McMahon CR, Hindell MA (2007) Complex interplay between intrinsic and extrinsic drivers of long-term survival trends in southern elephant seals. BMC Ecol 7:3
Eisert R, Oftedal OT, Lever M, Ramdohr S, Breier BH, Barrell GK (2005) Detection of food intake in a marine mammal using marine osmolytes and their analogues as dietary biomarkers. Mar Ecol Prog Ser 300:213–228
Ferguson SH (2006) The influence of environment, mating habitat, and predation on evolution of pinniped lactation strategies. J Mamm Evol 13:63–82
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
Gauthier G, Bêty J, Hobson KA (2003) Are greater snow geese capital breeders? New evidence from a stable isotope model. Ecology 84:3250–3264
Hadley GL, Rotella JJ, Garrott RA, Nichols JD (2006) Variation in probability of first reproduction of Weddell seals. J Anim Ecol 75:1058–1070
Hall AJ, McConnell BJ, Barker RJ (2001) Factors affecting first-year survival in grey seals and their implications for life history strategy. J Anim Ecol 70:138–149
Harshman LG, Zera AJ (2006) The cost of reproduction: the devil in the details. Trends Ecol Evol 22:80–86
Hindell MA, Slip DJ (1997) The importance of being fat: maternal expenditure in the southern elephant seal Mirounga leonina. In: Hindell MA, Kemper C (eds) Marine mammal research in the southern hemisphere volume 1: status, ecology and medicine, vol 1. Surrey Beatty & Sons, Chipping Norton, Australia, pp 72–77
Hindell MA, Bryden MM, Burton HR (1994) Early growth and milk-composition in southern elephant seals (Mirounga leonina). Aust J Zool 42:723–732
Hindell MA, Harcourt R, Waas JR, Thompson D (2002) Fine-scale three-dimensional spatial use by diving, lactating female Weddell seals Leptonychotes weddellii. Mar Ecol Prog Ser 242:275–284
Iverson SJ, Bowen WD, Boness DJ, Oftedal OT (1993) The effect of maternal size and milk output on pup growth in grey seals (Halichoerus grypus). Physiol Zool 66:61–88
Iverson SJ, Hamosh M, Bowen WD (1995a) Lipoprotein lipase activity and its relationship to high milk fat transfer during lactation in grey seals. J Comp Physiol B 165:384–395
Iverson SJ, Oftedal OT, Bowen WD, Boness DJ, Sampugna J (1995b) Prenatal and postnatal transfer of fatty acids from mother to pup in the hooded seal. J Comp Physiol B 165:1–12
Iverson SJ, Lang SLC, Cooper MH (2001) Comparison of the Bligh and Dyer and Folch methods for total lipid determination in a broad range of marine tissue. Lipids 36:1283–1287
Jenness R (1986) Symposium: species variation in mammary gland function. J Dairy Sci 69:869–885
Jönsson KI (1997) Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78:57–66
Kooyman GL (1989) Diverse divers. Springer, Berlin
Lang SLC, Iverson SJ, Bowen WD (2005) Individual variation in milk composition over lactation in harbour seals (Phoca vitulina) and the potential consequences of intermittent attendance. Can J Zool 83:1525–1531
Le Boeuf BJ (1994) Variation in the diving pattern of northern elephant seals with age, mass, sex, and reproductive condition. In: Le Boeuf BJ, Law RJ (eds) Elephant seals: population ecology, behaviour, and physiology. University of California Press, Berkeley, CA, pp 237–252
Lydersen C, Kovacs KM (1996) Energetics of lactation in harp seals (Phoca groenlandica) from the Gulf of St. Lawrence, Canada. J Comp Physiol B 166:295–304
Lydersen C, Kovacs KM (1999) Behaviour and energetics of ice-breeding, North Atlantic phocid seals during the lactation period. Mar Ecol Prog Ser 187:265–281
McMahon CR, Burton HR, Bester MN (2000) Weaning mass and the future survival of juvenile southern elephant seals, Mirounga leonina, at Macquarie Island. Antarct Sci 12:149–153
Meijer T, Drent RH (1999) Re-examination of the capital and income dichotomy in breeding birds. Ibis 141:399–414
Mellish J-AE, Iverson SJ, Bowen WD (1999) Variation in milk production and lactation performance in grey seals and consequences for pup growth and weaning characteristics. Physiol Biochem Zool 72:677–690
Nagy KA, Costa DP (1980) Water flux in animals: analysis of potential errors in the tritiated water method. Am J Zool 238:R454–R465
Oftedal OT, Iverson SJ (1987) Hydrogen isotope methodology for measurement of milk intake and energetics of growth in suckling young. In: Huntley AC, Costa DP, Worthy GAJ, Castellini MA (eds) Approaches to marine mammal energetics. Allen Press, Lawrence, KS, pp 67–96
Pond CM (1977) Significance of lactation in evolution of mammals. Evolution 31:177–199
Reilly JR, Fedak MA (1990) Measurement of the body composition of living gray seals by hydrogen isotope dilution. J Appl Physiol 69:885–891
Scrimgeour CM, Rollo MM, Mudambo MKT, Handley LL, Prosser SJ (1993) A simplified method for deuterium/hydrogen isotope ratio measurements on water samples of biological origin. Biol Mass Spectrom 22:383–387
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Stirling I (1969) Ecology of the Weddell seal in McMurdo Sound, Antarctica. Ecology 50:574–585
Tedman RA (1980) Lactation in the Weddell seal, Leptonychotes weddellii (Lesson). Department of Anatomy, University of Queensland, Brisbane, Australia, p 305
Tedman RA, Green B (1987) Water and sodium fluxes and lactational energetics in suckling pups of Weddell seals (Leptonychotes weddellii). J Zool (Lond) 212:29–42
Trillmich F (1996) Parental investment in pinnipeds. Adv Study Behav 25:533–577
Trillmich F, Weissing FJ (2006) Lactation patterns of pinnipeds are not explained by optimization of maternal energy delivery rates. Behav Ecol Sociobiol 60:137–149
Wheatley KE, Bradshaw CJA, Davis LS, Harcourt RG, Hindell MA (2006a) Influence of maternal mass and condition on energy transfer in Weddell seals. J Anim Ecol 75:724–733
Wheatley KE, Bradshaw CJA, Harcourt RG, Davis LS, Hindell MA (2006b) Chemical immobilization of adult female Weddell seals with tiletamine and zolazepam: effects of age, condition and stage of lactation. BMC Vet Res 2:8
Acknowledgments
We thank P. Brewin, M. Brock, W. Cook, L. Davis, D. Geddes, A. Hall, P. Isherwood, C. Littnan, B. Mooney, P. Nichols and volunteers from Scott Base for assistance in the field and laboratory. This study was supported by funds from an Australian Research Council Discovery Project grant (DP0342714), the University of Tasmania Institutional Research Grants Scheme and Sea World Research & Rescue Foundation, Inc. We thank Antarctica New Zealand for providing logistical support and the Australian Antarctic Division for providing some field clothing. S.T. Pochron and two anonymous reviewers provided constructive comments on the manuscript. Data were collected under permits from the University of Tasmania Animal Ethics Committee (A6790 and A6711), and the Department of Conservation of New Zealand (Per/22/2002/149 and Per/17/2003/188). This study was conducted in accordance with the current laws of Australia and New Zealand.
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Communicated by Jörg Ganzhorn.
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Wheatley, K.E., Bradshaw, C.J.A., Harcourt, R.G. et al. Feast or famine: evidence for mixed capital–income breeding strategies in Weddell seals. Oecologia 155, 11–20 (2008). https://doi.org/10.1007/s00442-007-0888-7
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DOI: https://doi.org/10.1007/s00442-007-0888-7