Advertisement

Mammalian Biology

, Volume 76, Issue 1, pp 3–11 | Cite as

Allometry of milk intake at peak lactation

  • Alexander RiekEmail author
Original Investigation

Abstract

Much attention has been given to the scaling of milk output and lactational strategies across species. However developed allometric equations for milk output in adult animals cannot be used for suckling young. Therefore, the purpose of the present study was to investigate milk intake and intake of milk nutrients in suckling mammalian young at peak lactation using phylogenetic independent contrasts in order to derive allometric relationships corrected for phylogeny. Milk intake and intake of milk nutrients (solid, fat, protein and sugar) at peak lactation for 40 mammalian species were evaluated for the present analysis to derive allometric relationships for suckling young. K*-values were calculated in order to detect phylogenetic signals across traits. Phylogenetic signals were high and significant for all traits examined, thus phylogenetically independent contrasts were calculated for log10 transformed milk intake and intake of milk nutrients, body mass and average daily gain to eliminate the potential lack of independence between species, because of their shared evolutionary history. The phylogeny for the species used in the present study was derived from a recently published mammalian Supertree with branch lengths derived from dated estimates of divergence times. Thirty allometric equations were calculated using phylogenetically independent contrasts. A strong (P < 0.001) positive relationship exists between neonate body mass and the response variables (milk intake, intake of milk nutrients), whether calculated for all mammals or separately for artiodactyls and carnivores, with the exception of sugar intake in carnivores. However, large deviations for some species and few outliers were found. The present equations could be used to predict values for species similar to those included in the present study that have not been studied, providing that the body mass falls inside the range of masses used to derive the equations. However, predicting values for missing species should be done with caution as they are not included in the phylogenetic tree that was used to derive the phylogenetically corrected equations.

Keywords

Allometry Lactation Milk intake Milk nutrients Phylogeny 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arnould, J.P.Y., Hindell, M.A., 1999. The composition of Australian fur seal (Arctocephalus pusillus doriferus) milk throughout lactation. Physiol. Biochem. Zool. 72, 605–612.PubMedCrossRefPubMedCentralGoogle Scholar
  2. Arnould, J.P.Y., Hindell, M.A., 2002. Milk consumption, body composition and pre-weaning growth rates of Australian fur seal (Arctocephalus pusillus doriferus) pups. J. Zool. 256, 351–359.CrossRefGoogle Scholar
  3. Arnould, J.P.Y., Boyd, I.L., Socha, D.G., 1996. Milk consumption and growth efficiency in Antarctic fur seal (Arctocephalus gazella) pups. Can. J. Zool. 74, 254–266.CrossRefGoogle Scholar
  4. Baker, B.E., Cook, H.W., Teal, J.J., 1970. Muskox (Ovibos moschatus) milk. I. Gross composition, fatty acid, and mineral constitution. Can. J. Zool. 48, 1345–1347.PubMedCrossRefPubMedCentralGoogle Scholar
  5. Bininda-Emonds, O.R.P., Cardillo, M., Jones, K.E., MacPhee, R.D.E., Beck, R.M.D., Grenyer, R., Price, S.A., et al., 2007. The delayed rise of present-day mammals. Nature 446, 507–512.PubMedPubMedCentralGoogle Scholar
  6. Blomberg, S.P., Garland, T., Ives, A.R., 2003. Testing for phylogenetic signal in comparative data: behavioural traits are more labile. Evolution 57, 717–745.PubMedPubMedCentralGoogle Scholar
  7. Bowen, W.D., Oftedal, O.T., Boness, D.J., 1992. Mass and energy-transfer during lactation in a small Phocid, the harbor seal (Phoca vitulina). Physiol. Zool. 65, 844–866.CrossRefGoogle Scholar
  8. Buss, D.H., Voss, W.R., 1971. Evaluation of four methods for estimating the milk yield of baboons. J. Nutr. 101, 901–909.PubMedPubMedCentralGoogle Scholar
  9. Carl, G.R., Robbins, C.T., 1988. The energetic cost of predator avoidance in neonatal ungulates: hiding versus following. Can. J. Zool. 66, 239–246.CrossRefGoogle Scholar
  10. Coward, W.A., Sawyer, M.B., Whitehead, R.G., Prentice, A.M., Evans, J., 1979. New method for measuring milk intakes in breast-fed babies. Lancet 2, 13–14.PubMedCrossRefPubMedCentralGoogle Scholar
  11. Cowie, A.T., 1969. Variations in the yield and composition of the milk during lactation in the rabbit and the galactopoietic effect of prolactin. J. Endocrinol. 44, 437–450.PubMedCrossRefPubMedCentralGoogle Scholar
  12. Degen, A.A., Elias, E., Kam, M., 1987. A preliminary report on the energy intake and growth rate of early weaned camel (Camelus dromedarius) calves. Anim. Prod. 45, 301–306.Google Scholar
  13. Dobenecker, B., Zottmann, B., Kienzle, E., Zentek, J., 1998. Investigations on milk composition and milk yield in queens. J. Nutr. 128, 2618S–2619S.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Donohue, M.J., Costa, D.P., Goebel, E., Antonelis, G.A., Baker, J.D., 2002. Milk intake and energy expenditure of free-ranging northern fur seal, Callorhinus ursinus, pups. Physiol. Biochem. Zool. 75, 3–18.PubMedCrossRefPubMedCentralGoogle Scholar
  15. Dove, H., Axelsen, A., 1979. Estimation of milk consumption in beef calves using a tritiated water dilution technique. Aust. J. Exp. Agric. 19, 666–672.CrossRefGoogle Scholar
  16. Dove, H., Cork, S.J., 1989. Lactation in the tammar wallaby (Macropus eugenii). I. Milk consumption and the algebraic description of the lactation curve. J. Zool. 219, 385–397.CrossRefGoogle Scholar
  17. Farley, S.D., Robbins, C.T., 1995. Lactation, hibernation, and mass dynamics of American black bears and grizzly bears. Can. J. Zool. 73, 2216–2222.CrossRefGoogle Scholar
  18. Felsenstein, J., 1985. Phylogenies and the comparative method. Am. Nat. 125, 1–15.CrossRefGoogle Scholar
  19. Fortun-Lamothe, L., Gidenne, T., 2000. The effects of size of suckled litter on intake behaviour, performance and health status of young and reproducing rabbits. Ann. Zootech. 49, 517–529.CrossRefGoogle Scholar
  20. Garland, T., Harvey, P.H., Ives, A.R., 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41, 18–32.CrossRefGoogle Scholar
  21. Garland, T., Dickerman, A.W., Janis, C.M., Jones, J.A., 1993. Phylogenetic analysis of covariance by computer-simulation. Syst. Biol. 42, 265–292.CrossRefGoogle Scholar
  22. Garland, T., Ives, A.R., 2000. Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am. Nat. 155, 346–364.PubMedCrossRefPubMedCentralGoogle Scholar
  23. Gittleman, J.L., Oftedal, O.T., 1987. Comparative growth and lactation energetics in carnivores. Symp. Zool. Soc. London 57, 41–77.Google Scholar
  24. Gjostein, H., Holand, O., Weladji, R.B., 2004. Milk production and composition in reindeer (Rangifer tarandus): effect of lactational stage. Comp. Biochem. Physiol. A 137, 649–656.CrossRefGoogle Scholar
  25. Georges, J.-Y., Guinet, C., 2000. Maternal care in the subantarctic fur seals on Amsterdam Island. Ecology 81, 295–308.CrossRefGoogle Scholar
  26. Green, B., 1984. Composition of milk and energetics of growth in marsupials. Symp. Zool. Soc. London 51, 369–387.Google Scholar
  27. Hackländer, K., Tataruch, F., Ruf, T., 2002. The effect of dietary fat content on lactation energetics in the European hare (Lepus europaeus). Physiol. Biochem. Zool. 75, 19–28.CrossRefGoogle Scholar
  28. Harvey, P.H., Pagel, M.D., 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.Google Scholar
  29. Hendriks, W.H., Wamberg, S., 2000. Milk intake of suckling kittens remains relatively constant from one to four weeks of age. J. Nutr. 130, 77–82.PubMedCrossRefPubMedCentralGoogle Scholar
  30. Iverson, S.J., Bowen, W.D., Boness, D.J., Oftedal, O.T., 1993. The effect of maternal size and milk energy output on pup growth in grey seals (Halichoerus grypus). Physiol. Zool. 66, 61–88.CrossRefGoogle Scholar
  31. Jordan, G.E., Piel, W.H., 2008. PhyloWidget: web-based visualization for the tree of life. Bioinformatics 24, 1641–1642.PubMedCrossRefPubMedCentralGoogle Scholar
  32. Kametaka, M., Inaba, J., Ichikawa, R., 1974. Estimation of daily milk intake of suckling rat using turnover rate of potassium. J. Nutr. Sci. Vitaminol. 20, 421–429.PubMedCrossRefPubMedCentralGoogle Scholar
  33. Kleiber, M., 1975. The Fire of Life. Robert E. Krieger Publishing Company, Huntington, New York.Google Scholar
  34. Knight, C.H., Maltz, E., Docherty, A.H., 1986. Milk yield and composition in mice: effects of litter size and lactation number. Comp. Biochem. Physiol. A 84, 127–133.PubMedCrossRefPubMedCentralGoogle Scholar
  35. Langer, P., 2008. The phases of maternal investment in eutherian mammals. Zoology 111, 148–162.PubMedCrossRefPubMedCentralGoogle Scholar
  36. Linzell, J.L., 1972. Milk yield, energy loss in milk, and mammary gland weight in different species. Dairy Sci. Abstr. 34, 351–360.Google Scholar
  37. Lydersen, C., Kovacs, K.M., Hammill, M.O., 1997. Energetics during nursing and early postweaning fasting in hooded seal (Cystophora cristata) pups from the Gulf of St Lawrence, Canada. J. Comp. Physiol. B 167, 81–88.PubMedCrossRefPubMedCentralGoogle Scholar
  38. Lydersen, C., Kovacs, K.M., Hammill, M.O., Gjertz, I., 1996. Energy intake and utilisation by nursing bearded seal (Erignathus barbatus) pups from Svalbard, Norway. J. Comp. Physiol. B 166, 405–411.PubMedCrossRefPubMedCentralGoogle Scholar
  39. Maltz, E., 1979. Productivity in the desert: Bedouin goat, ibex and desert gazelle. Ph.D. Thesis, Tel Aviv University.Google Scholar
  40. Maltz, E., Shkolnik, A., 1984. Lactational strategies of desert ruminants: the Bedouin goat, ibex and desert gazelle. Symp. Zool. Soc. London 51, 193–213.Google Scholar
  41. Martin, R.D., 1984. Scaling effects and adaptive strategies in mammalian lactation. Symp. Zool. Soc. Lond 51, 87–117.Google Scholar
  42. McEwan, E.H., Whitehead, P.E., 1971. Measurement of the milk intake of reindeer and caribou calves using tritiated water. Can. J. Zool. 49, 443–447.PubMedCrossRefPubMedCentralGoogle Scholar
  43. McNab, B.K., 1980. Food habits, energetics, and the population biology of mammals. Am. Nat. 116, 106–124.CrossRefGoogle Scholar
  44. Merchant, J.C., Libke, J.A., Smith, M.J., 1994. Lactation and energetics of growth in the brush-tailed bettong, Bettongia penicillata (Marsupialia: Potoroidae) in captivity. Aust. J. Zool. 42, 267–277.CrossRefGoogle Scholar
  45. Munks, S.A., Green, B., 1997. Milk consumption and growth in a marsupial arboreal folivore, the common ringtail possum, Pseudocheirus peregrinus. Physiol. Zool. 70, 691–700.PubMedCrossRefPubMedCentralGoogle Scholar
  46. Munks, S.A., Green, B., Newgrain, K., Messer, M., 1991. Milk-composition in the common ringtail possum, Pseudocheirus peregrinus (Petauridae, Marsupialia). Aust. J. Zool. 39, 403–416.CrossRefGoogle Scholar
  47. Nagy, K.A., 2001. Food requirements of wild animals: predictive equations for free-living mammals, reptiles, and birds. Nutr. Abstr. Rev. 71, 21R–32R.Google Scholar
  48. Oftedal, O.T., 1981. Milk, protein and energy intakes of suckling mammalian young: a comparative study. Ph.D. Thesis, Cornell University, Ithaca.Google Scholar
  49. Oftedal, O.T., 1984a. Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp. Zool. Soc. London 55, 33–85.Google Scholar
  50. Oftedal, O.T., 1984b. Lactation in the dog: milk composition and intake by puppies. J. Nutr. 114, 803–812.PubMedCrossRefPubMedCentralGoogle Scholar
  51. Oftedal, O.T., Bowen, W.D., Boness, D.J., 1996. Lactation performance and nutrient deposition in pups of the Harp seal, Phoca groenlandica, on ice floes off southeast Labrador. Physiol. Zool. 69, 635–657.CrossRefGoogle Scholar
  52. Oftedal, O.T., Hintz, H.F., Schryver, H.F., 1983. Lactation in the horse: milk composition and intake by foals. J. Nutr. 113, 2096–2106.PubMedCrossRefPubMedCentralGoogle Scholar
  53. Paradis, E., Claude, J., Strimmer, K., 2004. APE: analysis of phylogenetics and evolution in R language. Bioinformatics 20, 289–290.PubMedCrossRefPubMedCentralGoogle Scholar
  54. Parker, K.L., White, R.G., Gillingham, M.P., Holleman, D.F., 1990. Comparison of energy metabolism in relation to daily activity and milk consumption by caribou and muskox neonates. Can. J. Zool. 68, 106–114.CrossRefGoogle Scholar
  55. Payne, P.R., Wheeler, E.F., 1968. Comparative nutrition in pregnancy and lactation. Proc. Nutr. Soc. 27, 129–138.PubMedCrossRefPubMedCentralGoogle Scholar
  56. Pluske, J.R., Williams, I.H., Zak, L.J., Clowes, E.J., Cegielski, A.C., Aherne, F.X., 1998. Feeding lactating primiparous sows to establish three divergent metabolic states: III. Milk production and pig growth. J. Anim. Sci. 76, 1165–1171.PubMedCrossRefPubMedCentralGoogle Scholar
  57. Reese, E.O., Robbins, C.T., 1994. Characteristics of moose lactation and neonatal growth. Can. J. Zool. 72, 953–957.CrossRefGoogle Scholar
  58. Riek, A., Gerken, M., 2006. Changes in Llama (Lama glama) milk composition during lactation. J. Dairy Sci. 89, 3484–3493.PubMedCrossRefPubMedCentralGoogle Scholar
  59. Riek, A., Gerken, M., Moors, E., 2007. Measurement of milk intake in suckling llamas (Lama glama) using deuterium oxide dilution. J. Dairy Sci. 90, 867–875.PubMedCrossRefPubMedCentralGoogle Scholar
  60. Riek, A., 2008. Relationship between milk energy intake and growth rate in suckling mammalian young at peak lactation: an updated meta-analysis. J. Zool. 274, 160–170.CrossRefGoogle Scholar
  61. Robbins, C.T., Podbielanciknorman, R.S., Wilson, D.L., Mould, E.D., 1981. Growth and nutrient consumption of elk calves compared to other ungulate species. J. Wildlife Manage. 45, 172–186.CrossRefGoogle Scholar
  62. SAS Release 9.01., 2001. SAS Inst. Inc., Cary, NC.Google Scholar
  63. Sawaya, W.N., Khalil, J.K., Alshalhat, A., Almohammad, H., 1984. Chemical composition and nutritional quality of camel milk. J. Food Sci. 49, 744–747.CrossRefGoogle Scholar
  64. Scantlebury, M., Russell, A.F., McIlrat, G.M., Speakman, J.R., Clutton-Brock, T.H., 2002. The energetics of lactation in cooperatively breeding meerkats Suricata suricatta. Proc. R. Soc. London B 269, 2147–2153.CrossRefGoogle Scholar
  65. StatistiXL Release 1.8., 2007. www.statistiXL.com.
  66. Stern, A.A., Kunz, T.H., Studier, E.H., Oftedal, O.T., 1997. Milk composition and lactational output in the greater spear-nosed bat, Phyllostomus hastatus. J. Comp. Physiol. B 167, 389–398.PubMedCrossRefPubMedCentralGoogle Scholar
  67. Taylor, B.A., Varga, G.A., Whitsel, T.J., Hershberger, T.V., 1990. Composition of blue duiker (Cephalophus monticola) milk and milk intake by the calf. Small Rum. Res. 3, 551–560.CrossRefGoogle Scholar
  68. Withers, P.C., Cooper, C.E., Larcombe, A.N., 2006. Environmental correlates of physiological variables in marsupials. Physiol. Biochem. Zool. 79, 437–453.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Withers, P.C., 2008. Independent Contrasts, version 1.14. Distributed by the Author. Department of Zoology, University of Western Australia, Crawley, WA, Australia.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2010

Authors and Affiliations

  1. 1.Centre for Behavioural and Physiological Ecology, ZoologyUniversity of New EnglandArmidaleAustralia
  2. 2.Department of Animal SciencesUniversity of GöttingenGöttingenGermany

Personalised recommendations