Influence of the number of calves and lactating adult females in a herd on the adrenocortical activity of free-ranging Asian elephants
Sanjeeta Sharma Pokharel
A C , Polani B. Seshagiri B and Raman Sukumar A
+ Author Affiliations
- Author Affiliations
A Centre for Ecological Sciences, Indian Institute of Science, Bengaluru 560012, India.
B Department of Molecular Reproduction and Developmental Genetics, Indian Institute of Science, Bengaluru 560012, India.
C Corresponding author. Email: sanjeetap@iisc.ac.in
Wildlife Research 46(8) 679-689 https://doi.org/10.1071/WR18163
Submitted: 17 October 2018 Accepted: 1 August 2019 Published: 4 December 2019
Abstract
Context: Physiological stress has the potential to influence animal population persistence. The endangered Asian elephant (Elephas maximus) is involved in intense conflict with humans in many parts of its range, which likely leads to stress for individuals and groups, with consequences for population survival. Thus, it is important to understand how the elephants’ stress levels are influenced by socio-ecological factors when not directly exposed to human-induced threats, and to use this understanding to improve conservation and management strategies.
Aims: The present study was designed to provide baseline information on the link between socio-ecological factors and stress levels of undisturbed populations of elephants. The main aim was to determine the influence of a number of factors – herd size, season, number of calves and adult females present in a herd and their lactational status and body condition – on the adrenocortical activity of free-ranging adult female Asian elephants living in protected forests (without any direct exposure to human-induced threats), by measuring their faecal glucocorticoid metabolite (fGCM) levels.
Methods: A total of 145 fresh faecal samples were collected from 123 identified adult female elephants inhabiting Bandipur and Nagarahole National Parks of southern India, between the years 2013 and 2015. fGCM levels were measured by employing a group-specific standardised 11-oxoetiocholanolone enzyme immunoassay (EIA). A generalised linear mixed-effects model (GLMM) was used to assess the influence of socio-ecological factors on fGCM levels of adult female elephants.
Key results: When fGCM levels were analysed with a GLMM, the following patterns were observed: fGCM levels were negatively correlated with the number of adult females (herd size) and positively correlated with the number of calves in a herd and active lactational status of an adult female. fGCM levels of adult female elephants were higher during the dry season (February to May) than wet season (August to December) and negatively correlated with body condition scores.
Conclusions: Adrenocortical activity of female elephants is significantly influenced by the number of calves and adult females present in the herd, seasonality and lactational status.
Implications: It is important to consider the influence of multiple ecological and social correlates when assessing and interpreting the adrenocortical activity of Asian elephants. Our findings highlight the importance of maintaining the social structure of elephants in the wild to avoid detrimental effects on their physiological health. Insights from such assessments could be used to evaluate the stress in elephants that are involved in direct conflicts with humans to take appropriate management decisions for mitigating conflicts.
Additional keywords: Elephas maximus, faecal glucocorticoid metabolite (fGCM), lactation, seasonality, stress.
References
Abbondanza, F. N., Power, M. L., Dickson, M. A., Brown, J., and Oftedal, O. T. (2013). Variation in the composition of milk of Asian elephants (Elephas maximus) throughout lactation. Zoo Biology 32, 291–298.| Variation in the composition of milk of Asian elephants (Elephas maximus) throughout lactation.Crossref | GoogleScholarGoogle Scholar | 22588804PubMed |
Alexander, R. D. (1974). The evolution of social behavior. Annual Review of Ecology and Systematics 5, 325–383.
| The evolution of social behavior.Crossref | GoogleScholarGoogle Scholar |
Altemus, M. A., Deuster, P. A., Galliven, E., Carter, C. S., and Gold, P. W. (1995). Suppression of hypothalmic–pituitary–adrenal axis responses to stress in lactating women. Clinics in Endocrinology and Metabolism 80, 2954–2959.
| Suppression of hypothalmic–pituitary–adrenal axis responses to stress in lactating women.Crossref | GoogleScholarGoogle Scholar |
Bates, D., Maechler, M., Bolker, B., and Walker, S. (2014). lme4: Linear mixed-effects models using Eigen and S4. R package version 1, 1–23.
Bist, S. S. (2002). An overview of elephant conservation in India. Indian Forester 128, 121–136.
Bonier, F., Martin, P. R., Moore, I. T., and Wingfield, J. C. (2009). Do baseline glucocorticoids predict fitness? Trends in Ecology & Evolution 24, 634–642.
| Do baseline glucocorticoids predict fitness?Crossref | GoogleScholarGoogle Scholar |
Borries, C., Larney, E., Lu, A., Ossi, K., and Koenig, A. (2008). Costs of group size: lower developmental and reproductive rates in larger groups of leaf monkeys. Behavioral Ecology 19, 1186–1191.
| Costs of group size: lower developmental and reproductive rates in larger groups of leaf monkeys.Crossref | GoogleScholarGoogle Scholar |
Boswell, T., Woods, S. C., and Kenagy, G. J. (1994). Seasonal changes in body mass, insulin, and glucocorticoids of free-living golden-mantled ground squirrels. General and Comparative Endocrinology 96, 339–346.
| Seasonal changes in body mass, insulin, and glucocorticoids of free-living golden-mantled ground squirrels.Crossref | GoogleScholarGoogle Scholar | 7883140PubMed |
Bradbury, J. W., and Vehrencamp, S. L. (1976). Social organization and foraging in emballonurid bats. Behavioral Ecology and Sociobiology 1, 337–381.
| Social organization and foraging in emballonurid bats.Crossref | GoogleScholarGoogle Scholar |
Brown, J. L. (2014). Comparative reproductive biology of elephants. In ‘Reproductive Sciences in Animal Conservation.’ (Eds W. V. Holt, J. L. Brown, and P. Comizzoli.) pp. 135–169. (Springer: New York.)
Brunton, P. J., Russell, J. A., and Douglas, A. J. (2008). Adaptive responses of the maternal hypothalamic–pituitary–adrenal axis during pregnancy and lactation. Neuroendocrinology 20, 764–776.
| Adaptive responses of the maternal hypothalamic–pituitary–adrenal axis during pregnancy and lactation.Crossref | GoogleScholarGoogle Scholar |
Burnham, K. P., and Anderson, D. R. (2002). ‘Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach.’ 2nd edn. (Springer-Verlag: New York.)
Campos-Arceiz, A., and Blake, S. (2011). Megagardeners of the forest – the role of elephants in seed dispersal. Acta Oecologica 37, 542–553.
| Megagardeners of the forest – the role of elephants in seed dispersal.Crossref | GoogleScholarGoogle Scholar |
Chapman, C. A. (2000). Determinants of group size in primates: the importance of travel costs. In ‘On the Move: How and Why Animals Travel in Groups’. (Eds S. Boinski, and P. A. Garber.) pp. 24–42. (University of Chicago Press: Chicago, IL.)
Chen, D. C., Nommsen-Rivers, L., Dewey, K. G., and Lönnerdal, B. (1998). Stress during labor and delivery and early lactation performance. The American Journal of Clinical Nutrition 68, 335–344.
| Stress during labor and delivery and early lactation performance.Crossref | GoogleScholarGoogle Scholar | 9701191PubMed |
Choudhury, A., Lahiri Choudhury, D.K., Desai, A., Duckworth, J.W., Easa, P.S., Johnsingh, A.J.T., Fernando, P., Hedges, S., Gunawardena, M., Kurt, F., Karanth, U., Lister, A., Menon, V., Riddle, H., Rübel, A. and Wikramanayake, E. (IUCN SSC Asian Elephant Specialist Group) (2008). Elephas maximus. The IUCN Red List of Threatened Species. IUCN, Gland, Switzerland
Clark, C. W., and Mangel, M. (1986). The evolutionary advantages of group foraging. Theoretical Population Biology 30, 45–75.
| The evolutionary advantages of group foraging.Crossref | GoogleScholarGoogle Scholar |
Cockrem, J. F. (2013). Individual variation in glucocorticoid stress responses in animals. General and Comparative Endocrinology 181, 45–58.
| Individual variation in glucocorticoid stress responses in animals.Crossref | GoogleScholarGoogle Scholar | 23298571PubMed |
Creel, S., Dantzer, B., Goymann, W., and Rubenstein, D. R. (2013). The ecology of stress: effects of the social environment. Functional Ecology 27, 66–80.
| The ecology of stress: effects of the social environment.Crossref | GoogleScholarGoogle Scholar |
Dantzer, B., Fletcher, Q. E., Boonstra, R., and Sheriff, M. J. (2014). Measures of physiological stress: a transparent or opaque window into the status, management and conservation of species? Conservation Physiology 2, cou023.
| Measures of physiological stress: a transparent or opaque window into the status, management and conservation of species?Crossref | GoogleScholarGoogle Scholar | 27293644PubMed |
de Silva, S., and Wittemyer, G. (2012). A comparison of social organization in Asian elephants and African savannah elephants. International Journal of Primatology 33, 1125–1141.
| A comparison of social organization in Asian elephants and African savannah elephants.Crossref | GoogleScholarGoogle Scholar |
de Silva, S., Ranjeewa, A. D., and Kryazhimskiy, S. (2011a). The dynamics of social networks among female Asian elephants. BMC Ecology 11, 17.
| The dynamics of social networks among female Asian elephants.Crossref | GoogleScholarGoogle Scholar | 21794147PubMed |
de Silva, S., Ranjeewa, A. D., and Weerakoon, D. (2011b). Demography of Asian elephants (Elephas maximus) at Uda Walawe National Park, Sri Lanka based on identified individuals. Biological Conservation 144, 1742–1752.
| Demography of Asian elephants (Elephas maximus) at Uda Walawe National Park, Sri Lanka based on identified individuals.Crossref | GoogleScholarGoogle Scholar |
Dewey, K. G. (2001). Maternal and fetal stress are associated with impaired lactogenesis in humans. Nutrition 131, 3012S–3015S.
ETF-MoEF (2010). Gajah: Securing the future for elephants in India. The report of the Elephant Task Force, Ministry of Environment and Forests (MoEF), Government of India, New Delhi.
Fernando, P., and Lande, R. (2000). Molecular genetic and behavioral analysis of social organization in the Asian elephant (Elephas maximus). Behavioral Ecology and Sociobiology 48, 84–91.
| Molecular genetic and behavioral analysis of social organization in the Asian elephant (Elephas maximus).Crossref | GoogleScholarGoogle Scholar |
Fernando, P., Wikramanayake, E. D., Janaka, H. K., Jayasinghe, L. K. A., Gunawardena, M., Kotagama, S. W., Weerakoon, D., and Pastorini, J. (2008). Ranging behavior of the Asian elephant in Sri Lanka. Mammalian Biology-Zeitschrift für Säugetierkunde 73, 2–13.
| Ranging behavior of the Asian elephant in Sri Lanka.Crossref | GoogleScholarGoogle Scholar |
Foley, C. A. H., Papageorge, S., and Wasser, S. K. (2001). Noninvasive stress and reproductive measures of social and ecological pressures in free‐ranging African elephants. Conservation Biology 15, 1134–1142.
| Noninvasive stress and reproductive measures of social and ecological pressures in free‐ranging African elephants.Crossref | GoogleScholarGoogle Scholar |
Fox, J., and Monette, G. (1992). Generalized collinearity diagnostics. JASA 87, 178–183.
| Generalized collinearity diagnostics.Crossref | GoogleScholarGoogle Scholar |
Fox, J., Weisberg, S., Price, B.,Adler, D., Bates, D., Baud-Bovy, G., Bolker, B., Ellison, S., Firth, D., Friendly, M., Gorjanc, G., Graves, S., Heiberger, R., Laboissiere, R., Maechler, M., Monette, G., Murdoch, D., Nilsson, H., Ogle, D., Ripley, B., Venables, W., Walker, S., Winsemius, D., and Zeileis, A. (2012). Package ‘car’. R Foundation for Statistical Computing, Vienna. Available at https://cran.r-project.org/web/packages/car/index.html [verified October 2019].
Gadgil, M., and Nair, P. V. (1984). Observations on the social behaviour of free ranging groups of tame Asiatic elephant (Elephas maximus Linn). Proceedings: Animal Science 93, 225–233.
Ganswindt, A., Palme, R., Heistermann, M., Borragan, S., and Hodges, J. K. (2003). Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. General and Comparative Endocrinology 134, 156–166.
| Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth.Crossref | GoogleScholarGoogle Scholar | 14511986PubMed |
Gittleman, J. L., and Thompson, S. D. (1988). Energy allocation in mammalian reproduction. American Zoologist 28, 863–875.
| Energy allocation in mammalian reproduction.Crossref | GoogleScholarGoogle Scholar |
Gobush, K. S., Mutayoba, B. M., and Wasser, S. K. (2008). Long‐term impacts of poaching on relatedness, stress physiology, and reproductive output of adult female African elephants. Conservation Biology 22, 1590–1599.
| Long‐term impacts of poaching on relatedness, stress physiology, and reproductive output of adult female African elephants.Crossref | GoogleScholarGoogle Scholar | 18759771PubMed |
Government of India (2017). Synchronized Elephant Population Estimation 2017. Statistics from the Project Elephant Division, Ministry of Environment and Forests (MoEF), Government of India.
Goymann, W. (2012). On the use of non‐invasive hormone research in uncontrolled, natural environments: the problem with sex, diet, metabolic rate and the individual. Methods in Ecology and Evolution 3, 757–765.
| On the use of non‐invasive hormone research in uncontrolled, natural environments: the problem with sex, diet, metabolic rate and the individual.Crossref | GoogleScholarGoogle Scholar |
Goymann, W., East, M. L., Wachter, B., Höner, O. P., Möstl, E., Van’t Holf, T. J., and Hofer, H. (2001). Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas. Proceedings of the Royal Society of London. Series B, Biological Sciences 268, 2453–2459.
| Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas.Crossref | GoogleScholarGoogle Scholar |
Hamilton, W. D. (1964). The genetical evolution of social behaviour. II. Theoretical Biology 7, 17–52.
| The genetical evolution of social behaviour. II.Crossref | GoogleScholarGoogle Scholar |
Hanwell, A., and Peaker, M. (1977). Physiological effects of lactation on the mother. Symposia of the Zoological Society of London 41, 297–312.
Heinrichs, M., Meinlschmidt, G., Neumann, I., Wagner, S., Kirschbaum, C., Ehlert, U., and Hellhammer, D. H. (2001). Effects of suckling on hypothalamic–pituitary–adrenal axis responses to psychosocial stress in postpartum lactating women. Clinics in Endocrinology and Metabolism 86, 4798–4804.
| Effects of suckling on hypothalamic–pituitary–adrenal axis responses to psychosocial stress in postpartum lactating women.Crossref | GoogleScholarGoogle Scholar |
Heinrichs, M., Neumann, I., and Ehlert, U. (2002). Lactation and stress: protective effects of breast-feeding in humans. Stress 5, 195–203.
| Lactation and stress: protective effects of breast-feeding in humans.Crossref | GoogleScholarGoogle Scholar | 12186682PubMed |
Hintz, W. D., and Lonzarich, D. G. (2018). Maximizing foraging success: the roles of group size, predation risk, competition, and ontogeny. Ecosphere 9, e02456.
| Maximizing foraging success: the roles of group size, predation risk, competition, and ontogeny.Crossref | GoogleScholarGoogle Scholar |
Jaeggi, A. V., Trumble, B. C., and Brown, M. (2018). Group-level competition influences urinary steroid hormones among wild red-tailed monkeys, indicating energetic costs. American Journal of Primatology 80, e22757.
| Group-level competition influences urinary steroid hormones among wild red-tailed monkeys, indicating energetic costs.Crossref | GoogleScholarGoogle Scholar |
Joubert, D., and Joubert, B. (1994). Lions of darkness. National Geographic 186, 35–53.
Karanth, K. U., and Sunquist, M. E. (1992). Population structure, density and biomass of large herbivores in the tropical forests of Nagarahole, India. Tropical Ecology 8, 21–35.
| Population structure, density and biomass of large herbivores in the tropical forests of Nagarahole, India.Crossref | GoogleScholarGoogle Scholar |
Kenagy, G. J., and Place, N. J. (2000). Seasonal changes in plasma glucocorticosteroids of free-living female yellow-pine chipmunks: effects of reproduction and capture and handling. General and Comparative Endocrinology 117, 189–199.
| Seasonal changes in plasma glucocorticosteroids of free-living female yellow-pine chipmunks: effects of reproduction and capture and handling.Crossref | GoogleScholarGoogle Scholar | 10642441PubMed |
Kenagy, G.J., Masman, D., Sharbaugh, S.M., and Nagy, K.A. (1990). Energy expenditure during lactation in relation to litter size in free-living golden-mantled ground squirrels. Animal Ecology , 73–88.
| Energy expenditure during lactation in relation to litter size in free-living golden-mantled ground squirrels.Crossref | GoogleScholarGoogle Scholar |
Kerth, G., Ebert, C., and Schmidtke, C. (2006). Group decision making in fission–fusion societies: evidence from two-field experiments in Bechstein’s bats. Proceedings of the Royal Society of London. Series B, Biological Sciences 273, 2785–2790.
| Group decision making in fission–fusion societies: evidence from two-field experiments in Bechstein’s bats.Crossref | GoogleScholarGoogle Scholar |
KETF (2012). Report of the Karnataka Elephant Task Force. Submitted to Honourable High Court of Karnataka. Government of India, Karnataka, India.
Koolhaas, J. M., Korte, S. M., De Boer, S. F., Van Der Vegt, B. J., Van Reenen, C. G., Hopster, H., De Jong, I. C., Ruis, M. A. W., and Blokhuis, H. J. (1999). Coping styles in animals: current status in behavior and stress-physiology. Neuroscience and Biobehavioral Reviews 23, 925–935.
| Coping styles in animals: current status in behavior and stress-physiology.Crossref | GoogleScholarGoogle Scholar | 10580307PubMed |
Krause, J., and Ruxton, G. D. (2002). ‘Living in Groups.’ (Oxford University Press: Oxford, UK.)
Lee, P. C. (1987). Allomothering among African elephants. Animal Behaviour 35, 278–291.
| Allomothering among African elephants.Crossref | GoogleScholarGoogle Scholar |
Lee, P. C., Majluf, P., and Gordon, I. J. (1991). Growth, weaning and maternal investment from a comparative perspective. Zoology (Jena, Germany) 225, 99–114.
Loveridge, A. J., Hunt, J. E., Murindagomo, F., and Macdonald, D. W. (2006). Influence of drought on predation of elephant (Loxodonta africana) calves by lions (Panthera leo) in an African wooded savannah. Zoology (Jena, Germany) 270, 523–530.
Lüdecke, D. (2016). sjPlot: data visualization for statistics in social science. R package version, 2(1). Available at https://rdrr.io/cran/sjPlot/ [verified October 2019].
Lueders, I., Niemuller, C., Rich, P., Gray, C., Hermes, R., Goeritz, F., and Hildebrandt, T. B. (2012). Gestating for 22 months: luteal development and pregnancy maintenance in elephants. Proceedings of the Royal Society of London B: Biological Sciences 279, 3687–3696.
| Gestating for 22 months: luteal development and pregnancy maintenance in elephants.Crossref | GoogleScholarGoogle Scholar |
Maestripieri, D., Badiani, A., and Puglisi-Allegra, S. (1991). Prepartal chronic stress increases anxiety and decreases aggression in lactating female mice. Behavioral Neuroscience 105, 663–668.
| Prepartal chronic stress increases anxiety and decreases aggression in lactating female mice.Crossref | GoogleScholarGoogle Scholar | 1815617PubMed |
Maestripieri, D., Hoffman, C. L., Fulks, R., and Gerald, M. S. (2008). Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques. Hormones and Behavior 53, 170–176.
| Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques.Crossref | GoogleScholarGoogle Scholar | 17963759PubMed |
Majolo, B., de Bortoli Vizioli, A., and Schino, G. (2008). Costs and benefits of group living in primates: group size effects on behaviour and demography. Animal Behaviour 76, 1235–1247.
| Costs and benefits of group living in primates: group size effects on behaviour and demography.Crossref | GoogleScholarGoogle Scholar |
Markham, A. C., Gesquiere, L. R., Alberts, S. C., and Altmann, J. (2015). Optimal group size in a highly social mammal. Proceedings of the National Academy of Sciences of the United States of America 112, 14882–14887.
| Optimal group size in a highly social mammal.Crossref | GoogleScholarGoogle Scholar | 26504236PubMed |
McComb, K., Moss, C., Durant, S. M., Baker, L., and Sayialel, S. (2001). Matriarchs as repositories of social knowledge in African elephants. Science 292, 491–494.
| Matriarchs as repositories of social knowledge in African elephants.Crossref | GoogleScholarGoogle Scholar | 11313492PubMed |
McComb, K., Shannon, G., Durant, S. M., Sayialel, K., Slotow, R., Poole, J., and Moss, C. (2011). Leadership in elephants: the adaptive value of age. Proceedings of the Royal Society of London B: Biological Sciences 278, 3270–3276.
| Leadership in elephants: the adaptive value of age.Crossref | GoogleScholarGoogle Scholar |
Michelena, P., Pillot, M. H., Henrion, C., Toulet, S., Boissy, A., and Bon, R. (2012). Group size elicits specific physiological response in herbivores. Biology Letters 8, 537–539.
| Group size elicits specific physiological response in herbivores.Crossref | GoogleScholarGoogle Scholar | 22496078PubMed |
Moberg, G.P. (2000). Biological response to stress: implications for animal welfare. In ‘The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare’. (Eds G. Moberg, and J. Mench.) pp. 1–21. (CAB International: Wallingford, UK.)
Möstl, E., and Palme, R. (2002). Hormones as indicators of stress. Domestic Animal Endocrinology 23, 67–74.
| Hormones as indicators of stress.Crossref | GoogleScholarGoogle Scholar | 12142227PubMed |
Nandini, S., Keerthipriya, P., and Vidya, T. N. C. (2017). Seasonal variation in female Asian elephant social structure in Nagarahole-Bandipur, southern India. Animal Behaviour 134, 135–145.
| Seasonal variation in female Asian elephant social structure in Nagarahole-Bandipur, southern India.Crossref | GoogleScholarGoogle Scholar |
Neumann, I. D. (2001). Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats. Progress in Brain Research 133, 143–152.
| Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats.Crossref | GoogleScholarGoogle Scholar | 11589127PubMed |
Neville, M. C., Morton, J., and Umemura, S. (2001). Lactogenesis: the transition from pregnancy to lactation. Pediatric Clinics of North America 48, 35–52.
| Lactogenesis: the transition from pregnancy to lactation.Crossref | GoogleScholarGoogle Scholar | 11236732PubMed |
Oftedal, O. T. (2000). Use of maternal reserves as a lactation strategy in large mammals. The Proceedings of the Nutrition Society 59, 99–106.
| Use of maternal reserves as a lactation strategy in large mammals.Crossref | GoogleScholarGoogle Scholar | 10828179PubMed |
Owen-Smith, R. N. (1988). ‘Megaherbivores: the Influence of Very Large Body Size on Ecology.’ (Cambridge University Press: Cambridge, UK.)
PED-MoEF (2017). Statistics from the Project Elephant Division, Ministry of Environment and Forests (MoEF), Government of India.
Pokharel, S. S., Seshagiri, P. B., and Sukumar, R. (2017). Assessment of season-dependent body condition scores in relation to faecal glucocorticoid metabolites in free-ranging Asian elephants. Conservation Physiology 5, cox039.
| Assessment of season-dependent body condition scores in relation to faecal glucocorticoid metabolites in free-ranging Asian elephants.Crossref | GoogleScholarGoogle Scholar | 28721215PubMed |
Pokharel, S. S., Singh, B., Seshagiri, P. B., and Sukumar, R. (2019). Lower levels of glucocorticoids in crop-raiders: diet quality as a potential ‘pacifier’against stress in free-ranging Asian elephants in a human-production habitat. Animal Conservation 22, 177–188.
| Lower levels of glucocorticoids in crop-raiders: diet quality as a potential ‘pacifier’against stress in free-ranging Asian elephants in a human-production habitat.Crossref | GoogleScholarGoogle Scholar |
Pride, R. E. (2005). Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta). Behavioral Ecology 16, 550–560.
| Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta).Crossref | GoogleScholarGoogle Scholar |
Pulliam, R. H., and Caraco, T. (1984). Living in groups: is there an optimal group size? In ‘Behavioural Ecology,’ 2nd edn. (Eds C. J. Krebs and N. B. Davies.) pp. 122–147. (Blackwell Scientific Publications: Oxford, UK.)
R Core Team (2015). R: A Language and Environment for Statistical Computing. Version 3.1.3. (R Foundation for Statistical Computing: Vienna.) Available at http://www.R-project.org/ [verified 9 March 2015].
Reilly, J. (2002). Growth in the Sumatran elephant (Elephas maximus sumatranus) and age estimation based on dung diameter. Zoology (Jena, Germany) 258, 205–213.
Santema, P., Teitel, Z., Manser, M., Bennett, N., and Clutton-Brock, T. (2013). Effects of cortisol administration on cooperative behavior in meerkat helpers. Behavioral Ecology 24, 1122–1127.
| Effects of cortisol administration on cooperative behavior in meerkat helpers.Crossref | GoogleScholarGoogle Scholar |
Sapolsky, R. M., Romero, L. M., and Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21, 55–89.
| 10696570PubMed |
Schaller, G. B. (1972). ‘The Serengeti Lion. A Study of Predator–prey Relations.’ (Chicago University Press: Chicago, IL.)
Scott, K., Heistermann, M., Cant, M. A., and Vitikainen, E. I. (2017). Group size and visitor numbers predict faecal glucocorticoid concentrations in zoo meerkats. Royal Society Open Science 4, 161017.
| Group size and visitor numbers predict faecal glucocorticoid concentrations in zoo meerkats.Crossref | GoogleScholarGoogle Scholar | 28484620PubMed |
Sheriff, M. J., Krebs, C. J., and Boonstra, R. (2011). From process to pattern: how fluctuating predation risk impacts the stress axis of snowshoe hares during the 10-year cycle. Oecologia 166, 593–605.
| From process to pattern: how fluctuating predation risk impacts the stress axis of snowshoe hares during the 10-year cycle.Crossref | GoogleScholarGoogle Scholar | 21246218PubMed |
Snaith, T. V., Chapman, C. A., Rothman, J. M., and Wasserman, M. D. (2008). Bigger groups have fewer parasites and similar cortisol levels: a multi-group analysis in red colobus monkeys. American Journal of Primatology 70, 1072–1080.
| Bigger groups have fewer parasites and similar cortisol levels: a multi-group analysis in red colobus monkeys.Crossref | GoogleScholarGoogle Scholar | 18666135PubMed |
Sterck, E. H., Watts, D. P., and van Schaik, C. P. (1997). The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology 41, 291–309.
Sukumar, R. (1985). Ecology of the Asian elephant (Elephas maximus) and its interaction with man in south India. Ph.D. Thesis, Indian Institute of Science, Karnataka, India.
Sukumar, R. (1989). ‘The Asian Elephant: Ecology and Management.’ (Cambridge University Press: Cambridge, UK.)
Sukumar, R. (2003). ‘The Living Elephants: Evolutionary Ecology, Behaviour, and Conservation.’ (Oxford University Press: Oxford, UK.)
Sukumar, R. (2006). A brief review of the status, distribution and biology of wild Asian elephants. International Zoo Yearbook 40, 1–8.
| A brief review of the status, distribution and biology of wild Asian elephants.Crossref | GoogleScholarGoogle Scholar |
Sukumar, R., Varma, S., Tiwari, S. K., and Menon, V. (2016). Sustainable landscapes and corridors to conserve Asian elephants in India. In ‘Tropical Conservation: Perspectives on Local and Global Priorities’. (Eds A. A. Aguirre and R. Sukumar.) pp. 29–39. (Oxford University Press: Oxford, UK.)
Takahata, Y., Suzuki, S., Okayasu, N., Sugiura, H., Takahashi, H., Yamagiwa, J., Izawa, K., Agetsuma, N., Hill, D., Saito, C., and Sato, S. (1998). Does troop size of wild Japanese macaques influence birth rate and infant mortality in the absence of predators? Primates 39, 245–251.
| Does troop size of wild Japanese macaques influence birth rate and infant mortality in the absence of predators?Crossref | GoogleScholarGoogle Scholar |
van Noordwijk, M. A., and van Schaik, C. P. (1999). The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40, 105–130.
| The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis.Crossref | GoogleScholarGoogle Scholar | 23179535PubMed |
Vidya, T. N. C., and Sukumar, R. (2005). Social organization of the Asian elephant (Elephas maximus) in southern India inferred from microsatellite DNA. Ethology 23, 205–210.
| Social organization of the Asian elephant (Elephas maximus) in southern India inferred from microsatellite DNA.Crossref | GoogleScholarGoogle Scholar |
Vidya, T. N. C., Prasad, D., and Ghosh, A. (2014). Individual identification in Asian elephants. Gajah 40, 3–17.
Viljoen, J. J., Ganswindt, A., Palme, R., Reynecke, H. C., Du Toit, J. T., and Langbauer, W. R. (2008). Measurement of concentrations of faecal glucocorticoid metabolites in free-ranging African elephants within the Kruger National Park. Koedoe 50, 18–21.
| Measurement of concentrations of faecal glucocorticoid metabolites in free-ranging African elephants within the Kruger National Park.Crossref | GoogleScholarGoogle Scholar |
Wingfield, J. C., and Romero, L. M. (2001). Adrenocortical responses to stress and their modulation in free-living vertebrates. In ‘Handbook of Physiology’. (Eds B. S. McEwen, and H. M. Goodman.) pp. 211–236. (Oxford University Press: New York.)
Wingfield, J. C., Maney, D. L., Breuner, C. W., Jacobs, J. D., Lynn, S., Ramenofsky, M., and Richardson, R. D. (1998). Ecological bases of hormone – behavior interactions: the ‘emergency life history stage’. American Zoologist 38, 191–206.
| Ecological bases of hormone – behavior interactions: the ‘emergency life history stage’.Crossref | GoogleScholarGoogle Scholar |
Wrangham, R. W. (1980). An ecological model of females-bonded primate groups. Behaviour 75, 262–300.
| An ecological model of females-bonded primate groups.Crossref | GoogleScholarGoogle Scholar |
