Skip to main content

Advertisement

SpringerLink
Log in

Ecological correlates and determinants in the geographical variation of deer morphology

  • Population ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Previous studies on patterns in ungulate size variations have emphasized the effect of a particular environmental factor such as Bergmann’s rule and the island rule. However, although multiple environmental factors may influence the body size, these studies focused on a single factor, and various measurements that may be influenced by different environmental factors (at least partly) were used as indices of body size. In this study, we used several skull and limb measurements to examine size variations among island populations of sika deer (Cervus nippon) in southern Japan considering the effects of multiple environmental factors. We found that all measurements differed markedly between populations. We focused on the skull and limb condylobasal length (CBL) and metacarpal length because they had the most important variations among the populations and the largest sample sizes. The common environmental factors influencing CBL and metacarpal length were island area and precipitation. Since these environmental factors reflect the availability of food resources, the causal factor of body size variation may be food resources. Interpopulation variation in metacarpal length was greater than that of CBL, indicating that metacarpal length may be affected by additional factors besides the common factors shared with CBL. Specific environmental factors influencing relative (CBL adjusted) metacarpal length were precipitation and slope. A common direct cause of those environmental factors was discussed in relation to topography. Analyses of phenotypic variation using multiple measurements with multiple environmental factors are useful to gain insight into underlying causes and can lead to identification of a measurement-specific variation with a specific driving force.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ashton KG, Tracy MC, de Queiroz A (2000) Is Bergmann’s rule valid for mammals? Am Nat 156:390–415

    Article  Google Scholar 

  • Blois JL, Feranec RS, Hadly EA (2008) Environmental influences on spatial and temporal patterns of body-size variation in California ground squirrels (Spermophilus beecheyi). J Biogeogr 35:602–613

    Article  Google Scholar 

  • Bonenfant C, Gaillard JM, Coulson T, Festa-Bianchet M, Loison A, Garel M, Loe LE, Blanchard P, Pettorelli N, Owen-Smith N, Du Toit J, Duncan P (2009) Empirical evidence of density-dependence in populations of large herbivores. Adv Ecol Res 41:313–357

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Calsbeek R, Smith TB, Bardeleben C (2007) Intraspecific variation in Anolis sagrei mirrors the adaptive radiation of Greater Antillean anoles. Biol J Linn Soc 90:189–199

    Article  Google Scholar 

  • Capellini I, Gosling LM (2007) Habitat primary production and the evolution of body size within the hartebeest clade. Biol J Linn Soc 92:431–440

    Article  Google Scholar 

  • Case TJ (1978) A general explanation for insular body size trends in terrestrial vertebrates. Ecology 59:1–18

    Article  Google Scholar 

  • Christiansen P (1999) Scaling of the limb long bones to body mass in terrestrial mammals. J Morphol 239:167–190

    Article  PubMed  CAS  Google Scholar 

  • Darwin C (1859) On the origin of species by means of natural selection. Murray, London

    Google Scholar 

  • Endo A, Baba M (2010) Report of sika deer on Nozaki Island in Ojika town. Faculty of Agriculture, Saga University, Saga

    Google Scholar 

  • Endo A, Doi T (1996) Home range of female sika deer Cervus nippon on Nozaki Island, the Goto Archipelago, Japan. Mamm Stud 21:27–35

    Google Scholar 

  • Foster JB (1964) Evolution of mammals on islands. Nature 202:234–235

    Article  Google Scholar 

  • Fox J, Weisberg S (2010) An R Companion to applied regression, 2nd edn. Sage, New York

  • Garel M, Gaillard JM, Chevrier T, Michallet J, Delorme D, van Laere G (2010) Testing reliability of body size measurements using hind foot length in Roe deer. J Wildl Manag 74:1382–1386

    Google Scholar 

  • Geist V (1987) Bergmann’s rule is invalid. Can J Zool 65:1035–1038

    Article  Google Scholar 

  • Grant PR (1986) Ecology and evolution of Darwin’s finches. Princeton University Press, Princeton

    Google Scholar 

  • Grant PR, Grant BR, Smith JN, Abbott IJ, Abbott LK (1976) Darwin’s finches: population variation and natural selection. Proc Natl Acad Sci USA 73:257–261

    Article  PubMed  CAS  Google Scholar 

  • Heaney LR (1978) Island area and body size of insular mammals: evidence from the tri-colored squirrel (Callosciurus prevosti) of Southeast Asia. Evolution 32:29–44

    Article  Google Scholar 

  • Herfindal I, Solberg E, Sæther BE, Høgda KA, Andersen R (2006) Environmental phenology and geographical gradients in moose body mass. Oecologia 150:213–224

    Article  PubMed  Google Scholar 

  • Janis CM (1990) Correlation of cranial and dental variables with body size in ungulates and macropodoids. In: Damuth J, Macfadden BJ (eds) Body size in mammalian paleobiology: estimation and biological implication. Cambridge University Press, Cambridge, pp 255–300

    Google Scholar 

  • Kagoshima Environmental Research and Service (2010) Report to consider measures for accurate management of sika deer population on Yakushima in Kirishima-Yaku National Park. Kagoshima Environmental Research and Service, Kagoshima

    Google Scholar 

  • Kagoshima Prefecture (2007) Specified wildlife management plans for sika deer. Forestry and Fishery Department, Kagoshima prefecture, Kagoshima

  • Klein DR (1964) Range-related differences in growth of deer reflected in skeletal ratios. J Mamm 45:226–235

    Article  Google Scholar 

  • Klein DR, Meldgaard M, Fancy SG (1987) Factors determining leg length in Rangifer tarandus. J Mamm 68:642–655

    Article  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities—a common mistake. Auk 104:116–121

    Google Scholar 

  • Lilje KE, Tardieu C, Fischer MS (2003) Scaling of long bones in ruminants with respect to the scapula. J Zool Syst Evol Res 41:118–126

    Article  Google Scholar 

  • Lister AM (1989) Rapid dwarfing of red deer on Jersey in the last interglacial. Nature 342:539–542

    Article  PubMed  CAS  Google Scholar 

  • Lomolino MV (1985) Body size of mammals on islands—the island rule reexamined. Am Nat 125:310–316

    Article  Google Scholar 

  • Lomolino MV (2005) Body size evolution in insular vertebrates: generality of the island rule. J Biogeogr 32:1683–1699

    Article  Google Scholar 

  • Maxwell SE, Camp CJ, Arvey RD (1981) Measures of strength of association—a comparative-examination. J Appl Psychol 66:525–534

    Article  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • McMahon T (1975) Allometry and biomechanics: limb bones in adult ungulates. Am Nat 109:547–563

    Article  Google Scholar 

  • McMahon TA, Bonner JT (1983) On size and life. Freeman, New York

    Google Scholar 

  • McNab BK (2010) Geographic and temporal correlations of mammalian size reconsidered: a resource rule. Oecologia 164:13–23

    Article  PubMed  Google Scholar 

  • Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. J Biogeogr 30:331–351

    Article  Google Scholar 

  • Meiri S, Dayan T, Simberloff D (2006) The generality of the island rule reexamined. J Biogeogr 33:1571–1577

    Article  Google Scholar 

  • Meiri S, Yom-Tov Y, Geffen E (2007) What determines conformity to Bergmann’s rule? Glob Ecol Biogeogr 16:788–794

    Article  Google Scholar 

  • Meiri S, Cooper N, Purvis A (2008) The island rule: made to be broken? Proc R Soc Lond B 275:141–148

    Article  Google Scholar 

  • Nagasaki Prefecture (2007) Specified wildlife management plans for sika deer (Tsushima). Nagasaki Prefecture, Nagasaki

  • Ochiai K, Asada M (1995) Growth in the body size of sika deer (Cervus nippon) on the Boso Peninsula central Japan. J Nat Hist Mus Inst Chiba 3:223–232

    Google Scholar 

  • Ohdachi SD, Ishibashi Y, Iwasa MA, Saitoh T (2009) The wild mammals of Japan. Shoukadoh, Kyoto

    Google Scholar 

  • Ohtaishi N (1980) Estimation of sex, age, and season of death using mandibles of Cervus nippon excavated from an archaeological site. Archaeol Nat Sci 13:51–74

    Google Scholar 

  • Ohtaishi N (1986) Preliminary memorandum of classification, distribution, and geological variation on sika deer. Mamm Sci 53:13–17

    Google Scholar 

  • Oita Prefecture (2007) Specified wildlife management plans for sika deer. Agriculture, Forestry and Fishery Department, Oita prefecture, Oita

  • Pettorelli N, Vik JO, Mysterud A, Gaillard JM, Tucker CJ, Stenseth NC (2005) Using the satellite-derived NDVI to assess ecological responses to environmental change. Trends Ecol Evol 20:503–510

    Article  PubMed  Google Scholar 

  • Pettorelli N, Gaillard JM, Mysterud A, Duncan P, Stenseth NC, Delorme D, Van Laere G, Töigo C, Klein F (2006) Using a proxy of plant productivity (NDVI) to find key periods for animal performance: the case of roe deer. Oikos 112:565–572

    Article  Google Scholar 

  • Pierce CA, Block RA, Aguinis H (2004) Cautionary note on reporting eta-squared values from multifactor ANOVA designs. Educ Psychol Meas 64:916–924

    Article  Google Scholar 

  • Raia P, Meiri S (2006) The island rule in large mammals: paleontology meets ecology. Evolution 60:1731–1742

    PubMed  Google Scholar 

  • Romano A, Ficetola GF (2010) Ecogeographic variation of body size in the spectacled salamanders (Salamandrina): influence of genetic structure and local factors. J Biogeogr 37:2358–2370

    Article  Google Scholar 

  • Sand H, Cederlund G, Danell K (1995) Geographical and latitudinal variation in growth patterns and adult body size of Swedish moose (Alces alces). Oecologia 102:433–442

    Article  Google Scholar 

  • Scott KM (1985) Allometric trends and locomotor adaptations in the Bovidae. Bull Am Mus Nat Hist 179:197–288

    Google Scholar 

  • Scott KM (1987) Allometry and habitat-related adaptations in the postcranial skeleton of Cervidae. In: Wemmer CM (ed) Biology and management of the Cervidae. Smithdonian Institution Press, Washington, pp 65–80

    Google Scholar 

  • Scott KM (1990) Postcranial dimensions of ungulates as predictors of body mass. In: Damuth J, Macfadden BJ (eds) Body size in mammalian paleobiology: estimation and biological implication. Cambridge University Press, Cambridge, pp 301–336

    Google Scholar 

  • Shiroma T (2002) Why the kerama deer Cervus nippon keramae lives on the Kerama islands: notes on the artificial introduction of sika deer Cervus nippon into Ryukyu in the seventeenth century. Bull Historiogr Inst 27:209–218

    Google Scholar 

  • Sinervo B, Losos JB (1991) Walking the tight rope—arboreal sprint performance among Sceloporus occidentalis lizard populations. Ecology 72:1225–1233

    Article  Google Scholar 

  • Smith PA, Schaefer JA, Patterson BR (2002) Variation at high latitudes: the geography of body size and cranial morphology of the muskox, Ovibos moschatus. J Biogeogr 29:1089–1094

    Article  Google Scholar 

  • Takatsuki S (1992) Foot morphology and distribution of sika deer in relation to snow depth in Japan. Ecol Res 7:19–23

    Article  Google Scholar 

  • Toïgo C, Gaillard JM, Van Laere G, Hewison M, Morellet N (2006) How does environmental variation influence body mass, body size, and body condition? Roe deer as a case study. Ecography 29:301–308

    Article  Google Scholar 

  • von den Driesch A (1976) A guide to the measurement of animal bones from archaeological sites. Harvard University, Peabody Museum of Archaeology and Ethnology, Cambridge

  • Whitehead GK (1993) Encyclopedia of deer. Swann Hill Press, Shrewsbury

    Google Scholar 

  • Whittaker RJ (1998) Island biogeography: ecology, evolution and conservation. Oxford University Press, Oxford

    Google Scholar 

  • Wolverton S, Huston MA, Kennedy JH, Cagle K, Cornelius JD (2009) Conformation to Bergmann’s rule in white-tailed deer can be explained by food availability. Am Midl Nat 162:403–417

    Article  Google Scholar 

  • Yokoyama M (2009) Biology of sika deer in Hyogo: characteristics of reproduction, food habits, growth, and condition. In: McCullough DR, Takatsuki S, Kaji K (eds) Sika deer: biology and management of native and introduced populations. Springer, Tokyo, pp 193–205

    Google Scholar 

  • Yom-Tov Y, Geffen E (2006) Geographic variation in body size: the effects of ambient temperature and precipitation. Oecologia 148:213–218

    Article  PubMed  Google Scholar 

  • Zannèse A, Baïsse A, Gaillard JM, Hewison AJM, Saint-Hilaire K, Toïgo C, Van Laere G, Morellet N (2006) Hind foot length: an indicator for monitoring roe deer populations at a landscape scale. Wildl Soc Bull 34:351–358

    Article  Google Scholar 

Download references

Acknowledgments

We thank members of the hunting clubs at each of our study sites for helping with sample collection. The Primate Research Institute of Kyoto University allowed us to use their facilities at the Yakushima Field Research Station and members of the Institute also helped us in collecting samples. We thank M. Izawa, T. Shiroma, T. Doi, A. Endo, M. Baba, Ryukyu University, and the Kita-Kyushu Museum of Natural History and Human History for providing access to samples; H. Uno, T. Mano, and the Hokkaido Institute of Environmental Sciences for providing a place to prepare osteal specimens; Kanagatake Elementary School and the Sediment Control Division of Kagoshima Prefecture for providing weather data; the Agricultural Administration Division of Nagasaki Prefecture for providing deer density data; T. Akasaka for helping with GIS analysis; T. Kubo and H. Iijima for advice on statistical analyses; E. Dyson for help with the English language editing; O. Kishida for discussion and comments on the manuscript; H. Abe, T. Koizumi, and N. Ohtaishi for their helpful comments; and J-M. Gaillard, C. Bonenfant, and anonymous reviewers for their suggestions to improve the manuscript. This study was supported by a Grant-in-Aid from the Japan Society for the Promotion of Science (JSPS) Fellows (22-2966) and by a grant from the Global COE Program of the Graduate School of Environmental Science, Hokkaido University, to C. Terada.

Author information

Authors and Affiliations

  1. Graduate School of Environmental Science, Hokkaido University, North 9, West 9, Sapporo, 060-0809, Japan

    Chisato Terada & Takashi Saitoh

  2. Research Group of Regional Science, Graduate School of Letters, Hokkaido University, North 10, West 7, Sapporo, 060-0810, Japan

    Shirow Tatsuzawa

  3. Field Science Center, Hokkaido University, North 11, West 10, Sapporo, 060-0811, Japan

    Takashi Saitoh

Authors
  1. Chisato Terada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shirow Tatsuzawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takashi Saitoh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chisato Terada.

Additional information

Communicated by Jean-Michel Gaillard.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 223 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Terada, C., Tatsuzawa, S. & Saitoh, T. Ecological correlates and determinants in the geographical variation of deer morphology. Oecologia 169, 981–994 (2012). https://doi.org/10.1007/s00442-012-2270-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-012-2270-7

Keywords

Search

Navigation