Abstract
Habitat structure and population density have long been considered key factors in determining intraspecific variation in the group size of social ungulates. However, the effect of interaction between habitat structure and population density on group size is poorly understood, and whether the underlying causes of these relationships are biological adaptation, emergent properties, or both is still debated. Therefore, over 10 years, we examined group size of the sika deer (Cervus nippon) at different population densities and habitat types (open habitats vs closed forests). We found that deer group size was larger in open habitats than closed forests and increased with population density, and population density and habitat type had a synergistic effect on group size. There was greater density effect in open habitats, while the density effect was very weak in closed forests. Our findings in open habitat support emergent properties, because both population density and visibility enhanced the frequency of group fusion. Alternatively, our findings in closed forests support biological adaptation; the scarce food supply in closed forests may increase the cost of conspecific feeding competition, which consequently limits group size even under high densities. We suggest that both emergent properties and biological adaptation determine group size variability of sika deer, and emergent properties may be the mechanism that contributes to group size increase, whereas biological adaptation may be the mechanism that contributes to group size restriction.
Similar content being viewed by others
References
Agetsuma N, Sugiura H, Hill DA, Agetsuma-Yanagihara Y, Tanaka T (2003) Population density and group composition of Japanese sika deer (Cervus nippon yakushimae) in an evergreen broad-leaved forest in Yakushima, southern Japan. Ecol Res 18:475–483. https://doi.org/10.1046/j.1440-1703.2003.00571.x
Barja I, Rosellini S (2008) Does habitat type modify group size in roe deer and red deer under predation risk by Iberian wolves? Can J Zool 86:170–176. https://doi.org/10.1139/Z07-129
Barrette C (1991) The size of axis deer fluid groups in Wilpattu National Park, Sri Lanka. Mammalia 55:207–220. https://doi.org/10.1515/mamm.1991.55.2.207
Barton K (2019) MuMIn: multi-model inference. R package version 1.43.6. https://CRAN.R-project.org/package=MuMIn
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Bekenov A, Grachev IA, Milner-Gulland E (1998) The ecology and management of the saiga antelope in Kazakhstan. Mamm Rev 28:1–52. https://doi.org/10.1046/j.1365-2907.1998.281024.x
Berger J (1978) Group size, foraging, and antipredator ploys: an analysis of bighorn sheep decisions. Behav Ecol Sociobiol 4:91–99. https://doi.org/10.1007/BF00302563
Blank DA, Ruckstuhl K, Yang W (2012) Influence of population density on group sizes in goitered gazelle (Gazella subgutturosa Guld., 1780). Eur J Wildl Res 58:981–989. https://doi.org/10.1007/s10344-012-0641-3
Borkowski J (2000) Influence of the density of a sika deer population on activity, habitat use, and group size. Can J Zool 78:1369–1374. https://doi.org/10.1139/z00-071
Borkowski J, Furubayashi K (1998) Seasonal changes in number and habitat use of foraging sika deer at the high altitude of Tanzawa Mountains, Japan. J. Zool 245:95–106. https://doi.org/10.1111/j.1469-7998.1998.tb00068.x
Brashares JS, Garland T, Arcese P (2000) Phylogenetic analysis of coadaptation in behavior, diet, and body size in the African antelope. Behav Ecol 11:452–463. https://doi.org/10.1093/beheco/11.4.452
Buckland ST, Anderson DR, Burnham KP, Laake JL (1993) Distance sampling: estimating abundance of biological populations. Chapman and Hall, London
Burnham KP, Anderson D (2002) Model selection and multimodel inference. Springer-Verlag, New York
Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago
Caughley G (1964) Social organization and daily activity of the red kangaroo and the grey kangaroo. J Mamm 45:429–436. https://doi.org/10.2307/1377416
Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. University of Chicago press, Chicago
Creel S, Winnie JA Jr (2005) Responses of elk herd size to fine-scale spatial and temporal variation in the risk of predation by wolves. Anim Behav 69:1181–1189. https://doi.org/10.1016/j.anbehav.2004.07.022
Endo K (2015) Canis lupus (Linnaeus, 1758). In: Ohdachi DS, Ishibashi Y, Saitoh T, Fukui D, Saitoh T (eds) The wild mammals of Japan, 2nd edn. Shoukadoh Book Sellers and the Mammalogical Society of Japan, Kyoto, pp 226–2227
Estes RD (1974) Social organization of the African Bovidae. In: Geist V, Walther F (eds) IUCN publication new series no. 24: the behaviour of ungulates and its relation to management. IUCN, Morges, pp 166–205
Estes RD (1991) The behavior guide to African mammals. University of California Press, Berkeley
Fichter E (1987) Pronghorn groups: on social organization. Tebiwa 23:1–22
Fortin D, Fortin M, Beyer HL, Duchesne T, Courant S, Dancose K (2009) Group-size-mediated habitat selection and group fusion–fission dynamics of bison under predation risk. Ecology 90:2480–2490. https://doi.org/10.1890/08-0345.1
Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Thousand Oaks, Sage. Available online at http://socserv.socsci.mcmaster.ca/jfox/Books/Companion
Geist V (1974) On the relationship of social evolution and ecology in ungulates. Am Zool 14:205–220. https://doi.org/10.1093/icb/14.1.205
Geist V (1977) A comparison of social adaptions in relation to ecology in gallinaceous birds and ungulate societies. Ann Rev Ecol Syst 1977(8):193–207. https://doi.org/10.1146/annurev.es.08.110177.001205
Gerard J, Richard-Hansen C, Maublanc M, Biedau E (1993) Probable exaptations within the “distributed” herd. Revue d’écologie (Terre Vie) 48:239–248
Gerard J, Le Pendu Y, Maublanc M, Vincent J, Poulle M, Cibien C (1995) Large group formation in European roe deer: an adaptive feature? Revue d’écologie (Terre Vie) 50:391–401
Gerard J, Bideau E, Maublanc M, Loisel P, Marchal C (2002) Herd size in large herbivores: encoded in the individual or emergent? Biol Bull 202:275–282. https://doi.org/10.2307/1543479
Hirth DH (1977) Social behavior of white-tailed deer in relation to habitat. Wildlife Monogr 53:1–55
Isvaran K (2007) Intraspecific variation in group size in the blackbuck antelope: the roles of habitat structure and forage at different spatial scales. Oecologia 154:435–444. https://doi.org/10.1007/s00442-007-0840-x
Jarman PJ (1974) The social organisation of antelope in relation to their ecology. Behaviour 48:215–267. https://doi.org/10.1163/156853974X00345
Kohira M, Katsumata E (2017) Demographic trends of sika deer on the northern slope of Mt. Fuji. Mount Fuji Res 11:45–52. https://doi.org/10.24769/00000043(in Japanese)
Krause J, Ruxton GD, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford
Lawes M, Nanni R (1993) The density, habitat use and social organisation of Dorcas gazelles (Gazella dorcas) in Makhtesh Ramon, Negev desert, Israel. J. Arid Environ 24:177–196. https://doi.org/10.1006/jare.1993.1016
Le Pendu Y, Briedermann L, Gerard J, Maublanc M (1995) Inter-individual associations and social structure of a mouflon population (Ovis orientalis musimon). Behav Process 34:67–80. https://doi.org/10.1016/0376-6357(94)00055-L
Leuthold W (1977) African ungulates—a comparative review of their ethology and behavioral ecology. Springer, Belin
Lott DF (1991) Intraspecific variation in the social systems of wild vertebrates. Cambridge University Press, Cambridge
Lott DF, Minta SC (1983) Random individual association and social group instability in American bison (Bison bison). Zeitschrift für Tierpsychologie 61:153–172. https://doi.org/10.1111/j.1439-0310.1983.tb01335.x
Lovari S, Cosentino R (1986) Seasonal habitat selection and group size of the Abruzzo chamois (Rupicapra pyrenaica ornata). Ital J Zool 53:73–78. https://doi.org/10.1080/11250008609355486
Marino A (2010) Costs and benefits of sociality differ between female guanacos living in contrasting ecological conditions. Ethology 116:999–1010. https://doi.org/10.1111/j.1439-0310.2010.01812.x
Marino A, Baldi R (2014) Ecological correlates of group-size variation in a resource-defense ungulate, the sedentary guanaco. PLoS One 9:e89060. https://doi.org/10.1371/journal.pone.0089060
Maruyama N (1981) A study of the seasonal movements and aggregation patterns of sika deer. Bull Fac Agric Tokyo Univ Agric Technol 23:1–85 (in Japanese)
Maruyama N, Sugimori F, Totake Y, Miura S (1975) The snorting voice of the sika deer in relation to its spacing distribution. J Mammal Soc Japan 6:155–162. https://doi.org/10.11238/jmammsocjapan1952.6.155
McCullough DR (1982) Evaluation of night spotlighting as a deer study technique. J Wildl Manage 43:963–973. https://doi.org/10.2307/3808229
Mechkour F, Gautier P, Guilhem C, Boisard J (1997) Preliminary results on the social organisation of enclosed spring-bok (Antidorcas marsupialis). Zeitschrift fur Saugetierkunde 62:150–154
Miura S (1974) On the seasonal movements of sika deer population in Mt. Hinokiboramaru. J Mammal Soc Japan 6:51–66. https://doi.org/10.11238/jmammsocjapan1952.6.51
Murray MG (1981) Structure of association in impala, Aepyceros melampus. Behav Ecol Sociobiol 9:23–33. https://doi.org/10.1007/BF00299849
Ohwaki A, Koyanagi TF, Maeda S (2018) Evaluating forest clear-cuts as alternative grassland habitats for plants and butterflies. For Ecol Manage 430:337–345. https://doi.org/10.1016/j.foreco.2018.08.032
Pays O, Benhamou S, Helder R, Gerard J (2007) The dynamics of group formation in large mammalian herbivores: an analysis in the European roe deer. Anim Behav 74:1429–1441. https://doi.org/10.1016/j.anbehav.2007.02.012
Peek JM, LeResche RE, Stevens DR (1974) Dynamics of moose aggregations in Alaska, Minnesota, and Montana. J Mammal 55:126–137. https://doi.org/10.2307/1379262
Pépin D, Gerard J (2008) Group dynamics and local population density dependence of group size in the Pyrenean chamois, Rupicapra pyrenaica. Anim Behav 75:361–369. https://doi.org/10.1016/j.anbehav.2006.09.030
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: https://www.R-project.org/. Accessed 20 Feb 2020
Southwell C (1984) Variability in grouping in the eastern grey kangaroo, Macropus giganteus I. Group density and group size. Wildl Res 11:423–435. https://doi.org/10.1071/WR9840423
Takada H, Minami M (2019) Do differences in ecological conditions influence grouping behaviour in a solitary ungulate, the Japanese serow? Behaviour 156:245–264. https://doi.org/10.1163/1568539X-00003540
Takatsuki S (1982) A note on the herd size of sika deer on Kashima Island. J Mammal Soc Japan 9:54–56. https://doi.org/10.11238/jmammsocjapan1952.9.54
Takatsuki S (1983) Group size of sika deer in relation to habitat type on Kinkazan Island. Japan J Ecol 33:419–425. https://doi.org/10.18960/seitai.33.4_419
Takatsuki S (1989) Edge effects created by clear-cutting on habitat use by sika deer on Mt. Goyo, northern Honshu, Japan. Ecol Res 4:287–295. https://doi.org/10.1007/BF02348449
Thaker M, Vanak AT, Owen CR, Ogden MB, Slotow R (2010) Group dynamics of zebra and wildebeest in a woodland savanna: effects of predation risk and habitat density. PLoS One. https://doi.org/10.1371/journal.pone.0012758
Vander Wal E, Van Beest FM, Brook RK (2013) Density-dependent effects on group size are sex-specific in a gregarious ungulate. PLoS One 8:e53777. https://doi.org/10.1371/journal.pone.0053777
Walther FR (1972) Social grouping in Grant’s gazelle (Gazella granti Brooke 1827) in the Serengeti National Park. Ethology 31:348–403. https://doi.org/10.1111/j.1439-0310.1972.tb01775.x
Wirtz P, Lörscher J (1983) Group sizes of antelopes in an East African national park. Behaviour 84:135–156. https://doi.org/10.1163/156853983X00327
Wronski T, Apio A, Plath M, Averbeck C (2009) Do ecotypes of bushbuck differ in grouping patterns? Acta Ethol 12:71–78. https://doi.org/10.1007/s10211-009-0058-5
Yamazaki K (2015) Ursus thibetanus (G. Cuvier, 1823). In: Ohdachi DS, Ishibashi Y, Saitoh T, Fukui D, Saitoh T (eds) The wild mammals of Japan, 2nd edn. Shoukadoh Book Sellers and the Mammalogical Society of Japan, Kyoto, pp 243–245
Yoshida Y, Hayashi S, Nakamura D, Kitahara M (2013) Population dynamics of sika deer (Cervus nippon) on the north slope of Mount Fuji. Mount Fuji Res 7:15–17 (in Japanese)
Acknowledgements
Takuma Suzuki (Animal Life Solutions Co. Ltd.), Keita Nakamura (Idea Co. Ltd.), Konoka Aiba (Japan Wildlife Research Center), Mitsuko Hiruma (Tokyo University of Agriculture and Technology), and Miki Toda (Hayakawa City, Yamanashi Prefecture) helped with fieldwork. Taisuke Yasuda (Mount Fuji Research Institute Yamanashi Prefecture Government) provided advice on the statistical analysis, and Eri Katsumata (Mount Fuji Research Institute Yamanashi Prefecture Government) helped organize the data. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. We thank Mallory Eckstut, PhD, from Edanz Group (https://en-author-services.edanzgroup.com/) for editing a draft of this manuscript.
Funding
Not applicable.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Not applicable.
Ethics approval
All investigation was performed in accordance with the Ethics Committee for Animal Experiments, Mount Fuji Research Institute, Yamanashi Prefecture Government (ECAE-01-2013-2019).
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Availability of data and material
Not applicable.
Code availability
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling editor: Luca Corlatti.
Appendix
Appendix
See Table 3.
Rights and permissions
About this article
Cite this article
Takada, H., Washida, A. Ecological drivers of group size variation in sika deer: habitat structure, population density, or both?. Mamm Biol 100, 445–452 (2020). https://doi.org/10.1007/s42991-020-00041-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42991-020-00041-x