Allometry of milk intake at peak lactation
Tóm tắt
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.
Tài liệu tham khảo
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.
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.
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.
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.
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.
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.
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.
Buss, D.H., Voss, W.R., 1971. Evaluation of four methods for estimating the milk yield of baboons. J. Nutr. 101, 901–909.
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.
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.
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.
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.
Dobenecker, B., Zottmann, B., Kienzle, E., Zentek, J., 1998. Investigations on milk composition and milk yield in queens. J. Nutr. 128, 2618S–2619S.
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.
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.
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.
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.
Felsenstein, J., 1985. Phylogenies and the comparative method. Am. Nat. 125, 1–15.
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.
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.
Garland, T., Dickerman, A.W., Janis, C.M., Jones, J.A., 1993. Phylogenetic analysis of covariance by computer-simulation. Syst. Biol. 42, 265–292.
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.
Gittleman, J.L., Oftedal, O.T., 1987. Comparative growth and lactation energetics in carnivores. Symp. Zool. Soc. London 57, 41–77.
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.
Georges, J.-Y., Guinet, C., 2000. Maternal care in the subantarctic fur seals on Amsterdam Island. Ecology 81, 295–308.
Green, B., 1984. Composition of milk and energetics of growth in marsupials. Symp. Zool. Soc. London 51, 369–387.
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.
Harvey, P.H., Pagel, M.D., 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.
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.
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.
Jordan, G.E., Piel, W.H., 2008. PhyloWidget: web-based visualization for the tree of life. Bioinformatics 24, 1641–1642.
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.
Kleiber, M., 1975. The Fire of Life. Robert E. Krieger Publishing Company, Huntington, New York.
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.
Langer, P., 2008. The phases of maternal investment in eutherian mammals. Zoology 111, 148–162.
Linzell, J.L., 1972. Milk yield, energy loss in milk, and mammary gland weight in different species. Dairy Sci. Abstr. 34, 351–360.
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.
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.
Maltz, E., 1979. Productivity in the desert: Bedouin goat, ibex and desert gazelle. Ph.D. Thesis, Tel Aviv University.
Maltz, E., Shkolnik, A., 1984. Lactational strategies of desert ruminants: the Bedouin goat, ibex and desert gazelle. Symp. Zool. Soc. London 51, 193–213.
Martin, R.D., 1984. Scaling effects and adaptive strategies in mammalian lactation. Symp. Zool. Soc. Lond 51, 87–117.
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.
McNab, B.K., 1980. Food habits, energetics, and the population biology of mammals. Am. Nat. 116, 106–124.
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.
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.
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.
Nagy, K.A., 2001. Food requirements of wild animals: predictive equations for free-living mammals, reptiles, and birds. Nutr. Abstr. Rev. 71, 21R–32R.
Oftedal, O.T., 1981. Milk, protein and energy intakes of suckling mammalian young: a comparative study. Ph.D. Thesis, Cornell University, Ithaca.
Oftedal, O.T., 1984a. Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp. Zool. Soc. London 55, 33–85.
Oftedal, O.T., 1984b. Lactation in the dog: milk composition and intake by puppies. J. Nutr. 114, 803–812.
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.
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.
Paradis, E., Claude, J., Strimmer, K., 2004. APE: analysis of phylogenetics and evolution in R language. Bioinformatics 20, 289–290.
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.
Payne, P.R., Wheeler, E.F., 1968. Comparative nutrition in pregnancy and lactation. Proc. Nutr. Soc. 27, 129–138.
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.
Reese, E.O., Robbins, C.T., 1994. Characteristics of moose lactation and neonatal growth. Can. J. Zool. 72, 953–957.
Riek, A., Gerken, M., 2006. Changes in Llama (Lama glama) milk composition during lactation. J. Dairy Sci. 89, 3484–3493.
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.
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.
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.
SAS Release 9.01., 2001. SAS Inst. Inc., Cary, NC.
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.
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.
StatistiXL Release 1.8., 2007. www.statistiXL.com.
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.
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.
Withers, P.C., Cooper, C.E., Larcombe, A.N., 2006. Environmental correlates of physiological variables in marsupials. Physiol. Biochem. Zool. 79, 437–453.
Withers, P.C., 2008. Independent Contrasts, version 1.14. Distributed by the Author. Department of Zoology, University of Western Australia, Crawley, WA, Australia.