Individual traits influence vigilance in wild female eastern grey kangaroos
A. M. Edwards A B C , E. C. Best A , S. P. Blomberg A and A. W. Goldizen A
+ Author Affiliations
- Author Affiliations
A The University of Queensland, School of Biological Sciences, Brisbane, Qld 4072, Australia.
B Present address: The University of Tasmania, School of Zoology, Sandy Bay, Tas. 7005, Australia.
C Corresponding author. Email: amy.edwards@uqconnect.edu.au
Australian Journal of Zoology 61(4) 332-341 https://doi.org/10.1071/ZO13025
Submitted: 19 March 2013 Accepted: 8 September 2013 Published: 26 September 2013
Abstract
Vigilance is an essential component of antipredator behaviour and is also used to monitor conspecifics, but is traded off against feeding in herbivores. This trade-off can be influenced by variation in many environmental, social and individual traits. Our aim was to test the relationship between individual-level traits, including boldness, body condition and reproductive state, and vigilance, while controlling for environmental and social variables. Using multiple 5-min video samples of 30 foraging, individually recognisable, female eastern grey kangaroos (Macropus giganteus) at Sundown National Park in Queensland, we investigated individual-level variation in the duration, intensity and target of vigilance behaviour during foraging. On separate occasions, we used flight-initiation distance tests to measure boldness in our kangaroos. Females with longer flight-initiation distances (shyer females) spent more time vigilant, providing preliminary support for studies of animal personality that have suggested that boldness may covary with vigilance. Body condition did not affect the total time spent vigilant, but females in poorer body condition spent more of their vigilance time in low-intensity vigilance. Vigilance patterns were not related to reproductive state, but varied among months and differed between mornings and afternoons, and females spent more time in high-intensity vigilance when further from cover. Even after accounting for all our variables we found that 7% of the variation in total time vigilant and 14% of the variation in vigilance intensity was explained by individual identity. This highlights the importance of individual-level variation in vigilance behaviour.
Additional keywords: antipredator behaviour, boldness, group-size effect, personality.
References
Baayen, R. H. (2011). LanguageR: Data sets and functions with ‘Analyzing Linguistic Data: A Practical Introduction to Statistics’. R package version 1.2. Available at: http://CRAN.R-project.org/package=languageRBaayen, R., Davidson, D., and Bates, D. (2008). Mixed-effects modeling with crossed random effects for subjects and items. Journal of Memory and Language 59, 390–412.
| Mixed-effects modeling with crossed random effects for subjects and items.Crossref | GoogleScholarGoogle Scholar |
Bachman, G. C. (1993). The effect of body condition on the trade-off between vigilance and foraging in Belding’s ground squirrels. Animal Behaviour 46, 233–244.
| The effect of body condition on the trade-off between vigilance and foraging in Belding’s ground squirrels.Crossref | GoogleScholarGoogle Scholar |
Banks, P. B. (2001). Predation-sensitive grouping and habitat use by eastern grey kangaroos: a field experiment. Animal Behaviour 61, 1013–1021.
| Predation-sensitive grouping and habitat use by eastern grey kangaroos: a field experiment.Crossref | GoogleScholarGoogle Scholar |
Bates, D., Maechler, M., and Bolker, B. (2011). lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42. Available at: http://CRAN.R-project.org/package=lme4
Bell, A. M. (2007). Future directions in behavioural syndromes research. Proceedings of the Royal Society of London. Series B, Biological Sciences 274, 755–761.
| Future directions in behavioural syndromes research.Crossref | GoogleScholarGoogle Scholar |
Bergvall, U. A., Schäpers, A., Kjellander, P., and Weiss, A. (2011). Personality and foraging decisions in fallow deer (Dama dama). Animal Behaviour 81, 101–112.
| Personality and foraging decisions in fallow deer (Dama dama).Crossref | GoogleScholarGoogle Scholar |
Best, E. C. (2013). Network analysis of the social structure of female eastern grey kangaroos (Macropus giganteus). Ph.D. Thesis. Univeristy of Queensland, Brisbane.
Blumstein, D. T., Runyan, A., Seymour, M., Nicodemus, A., Ozgul, A., Ransler, F., Im, S., Stark, T., Zugmeyer, C., and Daniel, J. C. (2004). Locomotor ability and wariness in yellow-bellied marmots. Journal of Ethology 110, 615–634.
| Locomotor ability and wariness in yellow-bellied marmots.Crossref | GoogleScholarGoogle Scholar |
Brook, L. A., Johnson, C. N., and Ritchie, E. G. (2012). Effects of predator control on behaviour of an apex predator and indirect consequences for mesopredator suppression. Journal of Applied Ecology 49, 1278–1286.
| Effects of predator control on behaviour of an apex predator and indirect consequences for mesopredator suppression.Crossref | GoogleScholarGoogle Scholar |
Brown, J. S. (1999). Vigilance, patch use and habitat selection: foraging under predation risk. Evolutionary Ecology Research 1, 49–71.
Burger, J., and Gochfeld, M. (1994). Vigilance in African mammals – differences among mothers, other females, and males. Behaviour 131, 153–169.
| Vigilance in African mammals – differences among mothers, other females, and males.Crossref | GoogleScholarGoogle Scholar |
Cameron, E. Z., and du Toit, J. T. (2005). Social influences on vigilance behaviour in giraffes, Giraffa camelopardalis. Animal Behaviour 69, 1337–1344.
| Social influences on vigilance behaviour in giraffes, Giraffa camelopardalis.Crossref | GoogleScholarGoogle Scholar |
Carter, K., and Goldizen, A. W. (2003). Habitat choice and vigilance behaviour of brush-tailed rock-wallabies (Petrogale penicillata) within their nocturnal foraging ranges. Wildlife Research 30, 355–364.
| Habitat choice and vigilance behaviour of brush-tailed rock-wallabies (Petrogale penicillata) within their nocturnal foraging ranges.Crossref | GoogleScholarGoogle Scholar |
Carter, A. J., Macdonald, S. L., Thomson, V. A., and Goldizen, A. W. (2009a). Structured association patterns and their energetic benefits in female eastern grey kangaroos, Macropus giganteus. Animal Behaviour 77, 839–846.
| Structured association patterns and their energetic benefits in female eastern grey kangaroos, Macropus giganteus.Crossref | GoogleScholarGoogle Scholar |
Carter, A. J., Pays, O., and Goldizen, A. W. (2009b). Individual variation in the relationship between vigilance and group size in eastern grey kangaroos. Behavioral Ecology and Sociobiology 64, 237–245.
| Individual variation in the relationship between vigilance and group size in eastern grey kangaroos.Crossref | GoogleScholarGoogle Scholar |
Carter, A. J., Goldizen, A. W., and Tromp, S. A. (2010). Agamas exhibit behavioural syndromes: bolder males bask and feed more but may suffer higher predation. Behavioral Ecology 21, 655–661.
| Agamas exhibit behavioural syndromes: bolder males bask and feed more but may suffer higher predation.Crossref | GoogleScholarGoogle Scholar |
Childress, M. J., and Lung, M. A. (2003). Predation risk, gender and the group size effect: does elk vigilance depend upon the behaviour of conspecifics? Animal Behaviour 66, 389–398.
| Predation risk, gender and the group size effect: does elk vigilance depend upon the behaviour of conspecifics?Crossref | GoogleScholarGoogle Scholar |
Clarke, J. L., Jones, M. E., and Jarman, P. J. (1995). Diurnal and nocturnal grouping and foraging behaviours of free-ranging eastern grey kangaroos. Australian Journal of Zoology 43, 519–529.
| Diurnal and nocturnal grouping and foraging behaviours of free-ranging eastern grey kangaroos.Crossref | GoogleScholarGoogle Scholar |
Colagross, A. M. L., and Cockburn, A. (1993). Vigilance and grouping in the eastern gray kangaroo, Macropus giganteus. Australian Journal of Zoology 41, 325–334.
| Vigilance and grouping in the eastern gray kangaroo, Macropus giganteus.Crossref | GoogleScholarGoogle Scholar |
Cork, S. J. (1991). Meeting the energy requirements for lactation in a macropodid marsupial: current nutrition versus stored body reserves. Journal of Zoology 225, 567–576.
| Meeting the energy requirements for lactation in a macropodid marsupial: current nutrition versus stored body reserves.Crossref | GoogleScholarGoogle Scholar |
Dannock, R. J., Blomberg, S. P., and Goldizen, A. W. (2013). Individual variation in vigilance in female eastern grey kangaroos. Australian Journal of Zoology 61, 312–319.
| Individual variation in vigilance in female eastern grey kangaroos.Crossref | GoogleScholarGoogle Scholar |
Dewitt, T. J., Sih, A., and Hucko, J. A. (1999). Trait compensation and cospecialization in a freshwater snail: size, shape and antipredator behaviour. Animal Behaviour 58, 397–407.
| Trait compensation and cospecialization in a freshwater snail: size, shape and antipredator behaviour.Crossref | GoogleScholarGoogle Scholar | 10458891PubMed |
Dingemanse, N. J., Dochtermann, N. A., and Nakagawa, S. (2012). Defining behavioural syndromes and the role of ‘syndrome deviation’ in explaining their evolution. Behavioral Ecology and Sociobiology 66, 1543–1548.
| Defining behavioural syndromes and the role of ‘syndrome deviation’ in explaining their evolution.Crossref | GoogleScholarGoogle Scholar |
Dyer, J. R. G., Croft, D. P., Morrell, L. J., and Krause, J. (2009). Shoal composition determines foraging success in the guppy. Behavioral Ecology 20, 165–171.
| Shoal composition determines foraging success in the guppy.Crossref | GoogleScholarGoogle Scholar |
Elgar, M. A. (1989). Predator vigilance and group-size in mammals and birds – a critical review of the empirical evidence. Biological Reviews of the Cambridge Philosophical Society 64, 13–33.
| Predator vigilance and group-size in mammals and birds – a critical review of the empirical evidence.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M3kslKltQ%3D%3D&md5=7d050bbf2e2eaad4504c0b562cd90cffCAS | 2655726PubMed |
Fairbanks, B., and Dobson, F. S. (2007). Mechanisms of the group-size effect on vigilance in Columbian ground squirrels: dilution versus detection. Animal Behaviour 73, 115–123.
| Mechanisms of the group-size effect on vigilance in Columbian ground squirrels: dilution versus detection.Crossref | GoogleScholarGoogle Scholar |
Favreau, F. R., Goldizen, A. W., and Pays, O. (2010). Interactions among social monitoring, anti-predator vigilance and group size in eastern grey kangaroos. Proceedings of the Royal Society of London. Series B, Biological Sciences 277, 2089–2095.
| Interactions among social monitoring, anti-predator vigilance and group size in eastern grey kangaroos.Crossref | GoogleScholarGoogle Scholar |
Garamszegi, L. Z., and Herczeg, G. (2012). Behavioural syndromes, syndrome deviation and the within- and between-individual components of phenotypic correlations: when reality does not meet statistics. Behavioral Ecology and Sociobiology 66, 1651–1658.
| Behavioural syndromes, syndrome deviation and the within- and between-individual components of phenotypic correlations: when reality does not meet statistics.Crossref | GoogleScholarGoogle Scholar |
Gaynor, K. M., and Cords, M. (2012). Antipredator and social monitoring functions of vigilance behaviour in blue monkeys. Animal Behaviour 84, 531–537.
| Antipredator and social monitoring functions of vigilance behaviour in blue monkeys.Crossref | GoogleScholarGoogle Scholar |
Harden, R. H. (1985). The ecology of the dingo in north-eastern New South Wales. 1. Movements and home range. Australian Wildlife Research 12, 25–37.
| The ecology of the dingo in north-eastern New South Wales. 1. Movements and home range.Crossref | GoogleScholarGoogle Scholar |
Heathcote, C. F. (1987). Grouping of eastern grey kangaroos in open habitat. Australian Wildlife Research 14, 343–348.
| Grouping of eastern grey kangaroos in open habitat.Crossref | GoogleScholarGoogle Scholar |
Heptner, V., and Naumov, N. (1998). Sirenia and Carnivora (seacows, bears and wolves). In ‘Mammals of the Soviet Union. Vol. II, Part 1a’. (Science Publishers, Inc.: USA.)
Hoogland, J. L., Hale, S. L., Kirk, A. D., and Sui, Y. D. (2013). Individual variation in vigilance among white-tailed prairie dogs (Cynomys leucurus). The Southwestern Naturalist , .
Houston, A. I., McNamara, J. M., and Hutchinson, J. M. C. (1993). General results concerning the trade-off between gaining energy and avoiding predation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 341, 375–397.
| General results concerning the trade-off between gaining energy and avoiding predation.Crossref | GoogleScholarGoogle Scholar |
Hunter, L. T. B., and Skinner, J. D. (1998). Vigilance behaviour in African ungulates: the role of predation pressure. Behaviour 135, 195–211.
| Vigilance behaviour in African ungulates: the role of predation pressure.Crossref | GoogleScholarGoogle Scholar |
Jarman, P. J. (1987). Group-size and activity in eastern grey kangaroos. Animal Behaviour 35, 1044–1050.
| Group-size and activity in eastern grey kangaroos.Crossref | GoogleScholarGoogle Scholar |
Jarman, P. J. (1994). Individual behaviour and social organisation of kangaroos. In ‘Animal Societies: Individuals, Interactions and Organisation’. (Eds P. J. Jarman, and A. Rossiter.) pp. 69–85. (Kyoto University Press: Kyoto.)
Jarman, P. J., Jones, M. E., Johnson, C. N., Southwell, C. J., Stuartdick, R. I., Higginbottom, K. B., and Clarke, J. L. (1989). Macropod studies at Wallaby Creek. 8. Individual recognition of kangaroos and wallabies. Australian Wildlife Research 16, 179–185.
| Macropod studies at Wallaby Creek. 8. Individual recognition of kangaroos and wallabies.Crossref | GoogleScholarGoogle Scholar |
Kurvers, R. H. J. M., Prins, H. H. T., van Wieren, S. E., van Oers, K., Nolet, B. A., and Ydenberg, R. C. (2010). The effect of personality on social foraging: shy barnacle geese scrounge more. Proceedings of the Royal Society of London. Series B, Biological Sciences 277, 601–608.
| The effect of personality on social foraging: shy barnacle geese scrounge more.Crossref | GoogleScholarGoogle Scholar |
Lea, A. J., and Blumstein, D. T. (2011). Age and sex influence marmot antipredator behaviour during periods of heightened risk. Behavioral Ecology and Sociobiology 65, 1525–1533.
| Age and sex influence marmot antipredator behaviour during periods of heightened risk.Crossref | GoogleScholarGoogle Scholar | 21874082PubMed |
Lima, S. L. (1995). Back to the basics of antipredatory vigilance – the group-size effect. Animal Behaviour 49, 11–20.
| Back to the basics of antipredatory vigilance – the group-size effect.Crossref | GoogleScholarGoogle Scholar |
Lung, M. A., and Childress, M. J. (2007). The influence of conspecifics and predation risk on the vigilance of elk (Cervus elaphus) in Yellowstone National Park. Behavioral Ecology 18, 12–20.
| The influence of conspecifics and predation risk on the vigilance of elk (Cervus elaphus) in Yellowstone National Park.Crossref | GoogleScholarGoogle Scholar |
Monclús, R., and Rödel, H. G. (2009). Influence of different individual traits on vigilance behaviour in European rabbits. Journal of Ethology 115, 758–766.
| Influence of different individual traits on vigilance behaviour in European rabbits.Crossref | GoogleScholarGoogle Scholar |
Pangle, W. M., and Holekamp, K. E. (2010). Functions of vigilance behaviour in a social carnivore, the spotted hyaena, Crocuta crocuta. Animal Behaviour 80, 257–267.
| Functions of vigilance behaviour in a social carnivore, the spotted hyaena, Crocuta crocuta.Crossref | GoogleScholarGoogle Scholar |
Patrick, S. C., Chapman, J. R., Dugdale, H. L., Quinn, J. L., and Sheldon, B. C. (2012). Promiscuity, paternity and personality in the great tit. Proceedings of the Royal Society of London. Series B, Biological Sciences 279, 1724–1730.
| Promiscuity, paternity and personality in the great tit.Crossref | GoogleScholarGoogle Scholar |
Pays, O., and Jarman, P. J. (2008). Does sex affect both individual and collective vigilance in social mammalian herbivores: the case of the eastern grey kangaroo? Behavioral Ecology and Sociobiology 62, 757–767.
| Does sex affect both individual and collective vigilance in social mammalian herbivores: the case of the eastern grey kangaroo?Crossref | GoogleScholarGoogle Scholar |
Pays, O., Goulard, M., Blomberg, S. P., Goldizen, A. W., Sirot, E., and Jarman, P. J. (2009). The effect of social facilitation on vigilance in the eastern gray kangaroo, Macropus giganteus. Behavioral Ecology 20, 469–477.
| The effect of social facilitation on vigilance in the eastern gray kangaroo, Macropus giganteus.Crossref | GoogleScholarGoogle Scholar |
Pinheiro, J. C., and Bates, D. M. (2000). ‘Mixed-effects Models in S and S-PLUS.’ (Springer.)
Preisser, E. L., Bolnick, D. I., and Benard, M. F. (2005). Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86, 501–509.
| Scared to death? The effects of intimidation and consumption in predator–prey interactions.Crossref | GoogleScholarGoogle Scholar |
Pulliam, H. R. (1973). Advantages in flocking. Journal of Theoretical Biology 38, 419–422.
| Advantages in flocking.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3s7jt1OjsA%3D%3D&md5=0a66b0e02b2b06c8de2db98118ce1da3CAS | 4734745PubMed |
R Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org
Réale, D., Reader, S. M., Sol, D., McDougall, P. T., and Dingemanse, N. J. (2007). Integrating animal temperament within ecology and evolution. Biological Reviews of the Cambridge Philosophical Society 82, 291–318.
| Integrating animal temperament within ecology and evolution.Crossref | GoogleScholarGoogle Scholar | 17437562PubMed |
Rieucau, G., and Martin, J. G. A. (2008). Many eyes or many ewes: vigilance tactics in female bighorn sheep Ovis canadensis vary according to reproductive status. Oikos 117, 501–506.
| Many eyes or many ewes: vigilance tactics in female bighorn sheep Ovis canadensis vary according to reproductive status.Crossref | GoogleScholarGoogle Scholar |
Rieucau, G., Morand-Ferron, J., and Giraldeau, L.-A. (2010). Group size effect in nutmeg mannikin: between-individuals behavioural differences but same plasticity. Behavioral Ecology 21, 684–689.
| Group size effect in nutmeg mannikin: between-individuals behavioural differences but same plasticity.Crossref | GoogleScholarGoogle Scholar |
Roberts, G. (1996). Why individual vigilance declines as group size increases. Animal Behaviour 51, 1077–1086.
| Why individual vigilance declines as group size increases.Crossref | GoogleScholarGoogle Scholar |
Shorrocks, B., and Cockayne, A. (2005). Vigilance and group size in impala (Aepyceros melampus Lichtenstein): a study in Nairobi National Park, Kenya. African Journal of Ecology 43, 91–96.
| Vigilance and group size in impala (Aepyceros melampus Lichtenstein): a study in Nairobi National Park, Kenya.Crossref | GoogleScholarGoogle Scholar |
Sih, A., Bell, A., and Johnson, J. C. (2004). Behavioural syndromes: an ecological and evolutionary overview. Trends in Ecology & Evolution 19, 372–378.
| Behavioural syndromes: an ecological and evolutionary overview.Crossref | GoogleScholarGoogle Scholar |
Smith, A. C., Kelez, S., and Buchanan-Smith, H. M. (2004). Factors affecting vigilance within wild mixed-species troops of saddleback (Saguinus fuscicollis) and moustached tamarins (S. mystax). Behavioral Ecology and Sociobiology 56, 18–25.
| Factors affecting vigilance within wild mixed-species troops of saddleback (Saguinus fuscicollis) and moustached tamarins (S. mystax).Crossref | GoogleScholarGoogle Scholar |
Southwell, C. J. (1984a). Variability in grouping in the eastern grey kangaroo, Macropus giganteus. 1. Group density and group-size. Australian Wildlife Research 11, 423–435.
| Variability in grouping in the eastern grey kangaroo, Macropus giganteus. 1. Group density and group-size.Crossref | GoogleScholarGoogle Scholar |
Southwell, C. J. (1984b). Variability in grouping in the eastern grey kangaroo, Macropus giganteus. 2. Dynamics of group formation. Australian Wildlife Research 11, 437–449.
| Variability in grouping in the eastern grey kangaroo, Macropus giganteus. 2. Dynamics of group formation.Crossref | GoogleScholarGoogle Scholar |
Stankowich, T., and Blumstein, D. T. (2005). Fear in animals: a meta-analysis and review of risk assessment. Proceedings of the Royal Society of London. Series B, Biological Sciences 272, 2627–2634.
| Fear in animals: a meta-analysis and review of risk assessment.Crossref | GoogleScholarGoogle Scholar |
Steenbeek, R., Piek, R. C., van Buul, M., and van Hooff, J. (1999). Vigilance in wild Thomas’s langurs (Presbytis thomasi): the importance of infanticide risk. Behavioral Ecology and Sociobiology 45, 137–150.
| Vigilance in wild Thomas’s langurs (Presbytis thomasi): the importance of infanticide risk.Crossref | GoogleScholarGoogle Scholar |
Treves, A., Drescher, A., and Snowdon, C. T. (2003). Maternal watchfulness in black howler monkeys (Alouatta pigra). Journal of Ethology 109, 135–146.
| Maternal watchfulness in black howler monkeys (Alouatta pigra).Crossref | GoogleScholarGoogle Scholar |
Unck, C. E., Waterman, J. M., Verburgt, L., and Bateman, P. W. (2009). Quantity versus quality: how does level of predation threat affect Cape ground squirrel vigilance? Animal Behaviour 78, 625–632.
| Quantity versus quality: how does level of predation threat affect Cape ground squirrel vigilance?Crossref | GoogleScholarGoogle Scholar |
Valeix, M., Fritz, H., Loveridge, A. J., Davidson, Z., Hunt, J. E., Murindagomo, F., and Macdonald, D. W. (2009). Does the risk of encountering lions influence African herbivore behaviour at waterholes? Behavioral Ecology and Sociobiology 63, 1483–1494.
| Does the risk of encountering lions influence African herbivore behaviour at waterholes?Crossref | GoogleScholarGoogle Scholar |
Wilson, A. D. M., and Godin, J.-G. J. (2010). Boldness and intermittent locomotion in the bluegill sunfish, Lepomis macrochirus. Behavioral Ecology 21, 57–62.
| Boldness and intermittent locomotion in the bluegill sunfish, Lepomis macrochirus.Crossref | GoogleScholarGoogle Scholar |
Wilson, A. J., de Boer, M., Arnott, G., and Grimmer, A. (2011). Integrating personality research and animal contest theory: aggressiveness in the green swordtail Xiphophorus helleri. PLoS ONE 6, e28024.
| Integrating personality research and animal contest theory: aggressiveness in the green swordtail Xiphophorus helleri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Cnu7fE&md5=178901585d4a729cd95362813734ed4fCAS | 22140502PubMed |
Wolf, M., van Doorn, G. S., Leimar, O., and Weissing, F. J. (2007). Life-history trade-offs favour the evolution of animal personalities. Nature 447, 581–584.
| Life-history trade-offs favour the evolution of animal personalities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvVyktLc%3D&md5=e7e84b8895e28c91269e99ff792fc549CAS | 17538618PubMed |
Wright, J., Maklakov, A. A., and Khazin, V. (2001). State-dependent sentinels: an experimental study in the Arabian babbler. Proceedings of the Royal Society of London. Series B, Biological Sciences 268, 821–826.
| State-dependent sentinels: an experimental study in the Arabian babbler.Crossref | GoogleScholarGoogle Scholar |
Yeo, I. K., and Johnson, R. A. (2000). A new family of power transformations to improve normality or symmetry. Biometrika 87, 954–959.
| A new family of power transformations to improve normality or symmetry.Crossref | GoogleScholarGoogle Scholar |
