Abstract
Close behavioural association between mothers and offspring should enhance survival and growth of the young. Eastern grey kangaroos Macropus giganteus are gregarious and live in fission-fusion societies where adult females do not form strong bonds with other females but associate closely with their juvenile offspring. We aimed to determine whether the strength of these mother-offspring associations correlated with offspring size, survival and reproduction. We observed 129 marked offspring, aged 10 to 21 months, and their mothers in a high-density population at Wilsons Promontory National Park, Australia. We used half-weight indices to quantify mother-offspring associations and determined the proportion of time offspring spent with their mother, but isolated from other kangaroos, while foraging. We found strong cohort effects on size, mass, body condition, survival and reproduction. Mother-offspring sociability indices were not correlated with offspring body condition as 2-year-olds or reproduction as 3-year-olds. Juveniles that spent proportionally more time with their mothers at 18–21 months, however, were 6% larger and 19% heavier as 2-year-olds than those that did not associate closely with their mothers. In addition, juveniles that were often found alone with their mothers were more likely to survive than those that were more often found in larger groups. Stronger mother-offspring associations before weaning likely reflected nutritional maternal care in sons but non-nutritional care in daughters and had a beneficial effect on juvenile growth and survival.
Significance statement
The possible fitness consequences of mother-offspring behavioural associations can affect reproductive decisions by mothers. These fitness consequences affect population dynamics and are relevant to conservation when mothers may be harvested or killed by vehicles, as is the case for many large herbivores. We show that variability in these associations in kangaroos affects correlates of offspring fitness. Juveniles that spent proportionally more time with their mothers between 18 and 21 months of age were larger and heavier as 2-year-olds. In addition, juveniles that spent proportionally more time with their mothers but isolated from other kangaroos experienced improved survival. This study is among very few to examine the relationship between mother-offspring sociability and reproductive success in a non-primate mammal. Improved juvenile growth in sons appears to result from nutritional maternal care through prolonged nursing. Isolation of the mother with her young-at-foot occurs in all large macropod marsupials, and adaptive benefits of this behaviour should therefore occur in other species of macropods.
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References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
Altmann J, Alberts SC (2005) Growth rates in a wild primate population: ecological influences and maternal effects. Behav Ecol Sociobiol 57:490–501
Banks PB, Newsome AE, Dickman CR (2000) Predation by red foxes limits recruitment in populations of eastern grey kangaroos. Austral Ecol 25:283–291
Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36:83–105
Best EC, Dwyer RG, Seddon JM, Goldizen AW (2014) Associations are more strongly correlated with space use than kinship in female eastern grey kangaroos. Anim Behav 89:1–10
Blumstein DT, Daniel JC (2003) Developing predictive models of behaviour: do rock-wallabies receive an antipredator benefit from aggregation? Aust Mammal 25:147–154
Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. P Natl Acad Sci USA 106:13850–13853
Clutton-Brock T (1991) The evolution of parental care. Princeton University Press, Princeton
Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behaviour and ecology of two sexes. Chicago University Press, Chicago
Crawley MJ (2007) The R book. John Wiley & Sons Ltd., Chichester
Cripps JK, Wilson ME, Elgar MA, Coulson G (2011) Experimental manipulation of fertility reveals potential lactation costs in a free-ranging marsupial. Biol Lett 7:859–862
Croft DB (1981) Behaviour of red kangaroos Macropus rufus (Desmarest, 1822) (Macropodidae; Marsupialia) in northwestern New South Wales, Australia. Aust Mammal 4:5–58
Davis NE, Coulson G, Forsyth DM (2008) Diets of native and introduced mammalian herbivores in shrub-encroached grassy woodland, south-eastern Australia. Wildlife Res 35:684–694
Delean S, De'ath G, Marsh H (2009) Climate and maternal effects modify sex ratios in a weakly dimorphic marsupial. Behav Ecol Sociobiol 64:265–277
Fairbanks LA (1996) Individual differences in maternal style: causes and consequences for mothers and offspring. Adv Stud Behav 25:579–611
Festa-Bianchet M, Jorgenson JT, Réale D (2000) Early development, adult mass, and reproductive success in bighorn sheep. Behav Ecol 11:633–639
Frère CH, Krützen M, Mann J, Connor RC, Bejder L, Sherwin WB (2010) Social and genetic interactions drive fitness variation in a free-living dolphin population. P Natl Acad Sci USA 107:19949–19954
Hofer H, East ML (1993) The commuting system of Serengeti spotted hyaenas: how predator copes with migratory prey. III. Attendance and maternal care. Anim Behav 46:575–589
Jaremovic RV, Croft DB (1991a) Social organization of eastern grey kangaroos in southeastern New South Wales. 2. Associations within mixed groups. Mammalia 55:543–554
Jaremovic RV, Croft DB (1991b) Social organization of the eastern gray kangaroo (Macropodidae, Marsupialia) in southeastern New South Wales. 1. Groups and group home ranges. Mammalia 55:169–185
Jarman PJ (1994) Individual behaviour and social organisation of kangaroos. In: Jarman PJ, Rossiter A (eds) Animal societies. Kyoto University Press, Kyoto, pp 70–85
Jarman PJ, Coulson G (1989) Dynamics and adaptiveness of grouping in macropods. In: Grigg G, Jarman P, Hume I (eds) Kangaroos. Wallabies and Rat-kangaroos. Surrey Beatty & Sons Pty. Ltd., Chipping Norton, pp 527–547
King WJ, Goldizen AW (2016) Few sex effects in the ontogeny of mother-offspring relationships in eastern grey kangaroos. Anim Behav 113:59–67
King WJ, Wilson ME, Allen T, Festa-Bianchet M, Coulson G (2011) A capture technique for free-ranging eastern grey kangaroos (Macropus giganteus) habituated to humans. Aust Mammal 33:47–31
King WJ, Forsyth DM, Coulson G, Festa-Bianchet M (2015a) Adoption in eastern grey kangaroos: a consequence of misdirected care? PLoS One 10:e0125182
King WJ, Garant D, Festa-Bianchet M (2015b) Mother-offspring distances reflect sex differences in fine-scale genetic structure of eastern grey kangaroos. Ecol Evol 5:2084–2094
Krockenberger A (2006) Lactation. In: Armati PJ, Dickman CR, Hume ID (eds) Marsupials. Cambridge University Press, Cambridge, pp 108–136
Lee PC, Moss CJ (2011) Calf development and maternal rearing strategies. In: Moss CJ, Croze H, Lee PC (eds) The Amboseli elephants: a long-term perspective on a long-lived mammal. University of Chicago Press, Chicago, pp 224–237
Lee PC, Majluf P, Gordon IJ (1991) Growth, weaning and maternal investment from a comparative perspective. J Zool 225:99–114
Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348
Maestripieri D (2009) Maternal influences on offspring growth, reproduction, and behavior in primates. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. University of Chicago Press, Chicago, pp 256–291
Maestripieri D, Mateo JM (eds) (2009) Maternal effects in mammals. University of Chicago Press, Chicago
Maguire G, Ramp D, Coulson G (2006) Foraging behaviour and dispersion of eastern grey kangaroos (Macropus giganteus) in an ideal free framework. J Zool 268:261–269
Mateo JM (2009) Maternal influences on development, social relationships, and survival behaviors. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. University of Chicago Press, Chicago, pp 133–158
Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos T Roy Soc B 363:1635–1645
Mousseau TA, Fox CW (eds) (1998) Maternal effects as adaptations. Oxford University Press, New York
Nguyen N, Gesquiere L, Alberts SC, Altmann J (2012) Sex differences in the mother-neonate relationship in wild baboons: social, experiential and hormonal correlates. Anim Behav 83:891–903
Ozoga JJ, Verme LJ, Bienz CS (1982) Parturition behavior and territoriality in white-tailed deer: impact on neonatal mortality. J Wildlife Manage 46:1–11
Peig J, Green AJ (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct Ecol 24:1323–1332
Poole WE (1975) Reproduction in the two species of grey kangaroos, Macropus giganteus Shaw and M. fuliginosus (Desmarest). II. Gestation, parturition and pouch life. Aust J Zool 23:333–353
Poole WE (1982) Macropus giganteus. Mamm Species 187:1–8
Poole WE (1983) Breeding in the grey kangaroo, Macropus giganteus, from widespread locations in eastern Australia. Aust Wildlife Res 10:453–466
Poole WE, Catling PC (1974) Reproduction in the two species of grey kangaroos, Macropus giganteus Shaw and M. fuliginosus (Desmarest) I. Sexual maturity and oestrus. Aust J Zool 22:277–302
Poole WE, Carpenter SM, Wood JT (1982) Growth of grey kangaroos and the reliability of age determination from body measurements. I. The eastern grey kangaroo, Macropus giganteus. Aust Wildlife Res 9:9–20
Pratt DM, Anderson VH (1979) Giraffe cow-calf relationships and social development of the calf in the Serengeti. Z Tierpsychol 51:233–251
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna www.R-project.org
Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163
Silk JB (2007) The adaptive value of sociality in mammalian groups. Philos T Roy Soc B 362:539–559
Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234
Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc R Soc Lond B 276:3099–3104
Silk JB, Alberts SC, Altmann J, Cheney DL, Seyfarth RM (2012) Stability of partner choice among female baboons. Anim Behav 83:1511–1518
Southwell CJ (1984) Variability in grouping in the eastern grey kangaroo, Macropus giganteus II. Dynamics of group formation. Aust Wildlife Res 11:437–449
Tyndale-Biscoe H, Renfree M (1987) Reproductive physiology of marsupials. Cambridge University Press, Cambridge
Whitehead H (2008) Analyzing animal societies. University of Chicago Press, Chicago
Acknowledgments
This research was funded by the Natural Sciences and Research Council of Canada and the Holsworth Wildlife Research Endowment. U. Gélin helped monitor the population in 2009 and C. Le Gall-Payne and R. Glass did so in 2012. S. P. Blomberg provided statistical advice. D. T. Blumstein, E. Z. Cameron, D. A. Fisher, M. J. Noad and two anonymous reviewers commented on previous versions of this manuscript.
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This study was funded by the Natural Sciences and Engineering Council of Canada and the Holsworth Wildlife Research Endowment. Captures were undertaken with ethics approval from the University of Melbourne (no. 0810628.1 and no. 0911512.1) and research permits from the Victorian Department of Sustainability and Environment (no. 1004582 and no. 1005558). Following captures, 9 of 241 pouch young were abandoned (4%); however, non-captured females also abandoned young occasionally. There was 1 death in 132 captures of sub-adults (1%; an apparent fox predation during recovery) and 1 death in 369 captures of adult females (0.3%). There were no observed capture-related injuries in the 5 years of study. Observations were conducted with animal ethics approval from the University of Queensland (no. SIB/206/09/(NF)). All applicable international, national and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This article does not contain any studies with human participants by any of the authors.
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King, W.J., Festa-Bianchet, M., Coulson, G. et al. Long-term consequences of mother-offspring associations in eastern grey kangaroos. Behav Ecol Sociobiol 71, 77 (2017). https://doi.org/10.1007/s00265-017-2297-1
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DOI: https://doi.org/10.1007/s00265-017-2297-1