Skip to main content

Environmental Correlates of Body Mass in True Lemurs (Eulemur spp.)

International Journal of Primatology volume 37, pages 89–108 (2016)Cite this article

Abstract

An organism’s body size is intrinsically related to its metabolic requirements, life history profile, and ecological niche. Previous work in primates generally, and lemurs specifically, has shown that body size often correlates with ecological parameters related to temperature and energy availability in the environment, although other studies indicate the absence of any such patterns in lemurs. Here we test hypotheses that predict that body mass in Eulemur should covary with 1) overall food availability or resource seasonality and/or 2) temperature, i.e., Bergmann’s rule. We use data from 722 wild true lemurs to identify population-specific body mass for 27 populations representing 11 of the 12 described Eulemur species, and derive climatic data for each population from the WorldClim database. We use phylogenetic generalized least squares models to evaluate these hypotheses and find that body mass significantly negatively correlates with annual mean temperature and positively correlates with standard deviation of temperature, but does not significantly correlate with annual rainfall or number of dry months. These results indicate that body mass distribution across populations in Eulemur is consistent with Bergmann’s rule, but does not track resource seasonality as seen in other lemurs, e.g., Propithecus. We suggest that the fact that body mass in various lemur radiations correlates with different environmental variables may result in these patterns being obscured when such taxa are combined in a single analysis. This may help explain why some previous work has found little evidence of ecogeographical correlates with body mass across all Lemuriformes.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2

References

  • Albrecht, G. H., Jenkins, P. D., & Godfrey, L. R. (1990). Ecogeographic size variation among the living and subfossil prosimians of Madagascar. American Journal of Primatology, 22, 1–50.

    Article  Google Scholar 

  • Altmann, J., & Alberts, S. (1987). Body mass and growth rate in a wild primate population. Oecologia, 72, 15–20.

    Article  Google Scholar 

  • Altmann, J., & Alberts, S. C. (2005). Growth rates in a wild primate population: ecological influences and maternal effects. Behavioral Ecology and Sociobiology, 57, 490–501.

    Article  Google Scholar 

  • Ashton, K. G., Tracy, M. C., & de Queiroz, A. (2000). Is Bergmann’s rule valid for mammals? The American Naturalist, 156, 390–415.

    Article  Google Scholar 

  • Bergmann, C. (1847). Uber die verhaltnisse der warmeokonomie der thiere zu ihrer grosse. Göttinger Studien, 595–708.

  • Blackburn, T. M., & Hawkins, B. A. (2004). Bergmann's rule and the mammal fauna of northern North America. Ecography, 27, 715–724.

    Article  Google Scholar 

  • Blackburn, T. M., Gaston, K. J., & Loder, N. (1999). Geographic gradients in body size: a clarification of Bergmann’s rule. Diversity and Distributions, 5, 165–174.

    Article  Google Scholar 

  • Blanco, M., & Godfrey, L. (2014). Hibernation patterns of dwarf lemurs in the high altitude forest of eastern Madagascar. In N. B. Grow, S. Gursky-Doyen, & A. Krzton (Eds.), High altitude primates (pp. 23–42). New York: Springer Science+Business Media.

    Chapter  Google Scholar 

  • Brenneman, R. A., Johnson, S. E., Bailey, C. A., Ingraldi, C., Delmore, K. E., Wyman, T. M., Andriamaharoa, H. E., Ralainasolo, F. B., Ratsimbazafy, J. H., & Louis, E. E. (2012). Population genetics and abundance of the endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: assessing risks for fragmented and continuous populations. Oryx, 46, 298–307.

    Article  Google Scholar 

  • Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference (2nd ed.). New York: Springer Science+Business Media.

    Google Scholar 

  • Delmore, K. E., Louis, E. E., & Johnson, S. E. (2011). Morphological characterization of a brown lemur hybrid zone (Eulemur rufifrons × E. cinereiceps). American Journal of Physical Anthropology, 145, 55–66.

    Article  PubMed  Google Scholar 

  • Delmore, K. E., Brenneman, R. A., Lei, R., Bailey, C. A., Brelsford, A., Louis, E. E., & Johnson, S. E. (2013). Clinal variation in a brown lemur (Eulemur spp.) hybrid zone: combining morphological, genetic and climatic data to examine stability. Journal of Evolutionary Biology, 26, 1677–1690.

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein, J. (1985). Phylogenies and the comparative method. The American Naturalist, 125, 1–15.

    Article  Google Scholar 

  • Fernandez-Duque, E. (2011). Rensch's rule, Bergmann's effect and adult sexual dimorphism in wild monogamous owl monkeys (Aotus azarai) of Argentina. American Journal of Physical Anthropology, 146, 38–48.

    Article  PubMed  Google Scholar 

  • Gerson, J. S. (1999). Size in Eulemur fulvus rufus from western Madagascar: sexual dimorphism and ecogeographic variation. American Journal of Physical Anthropology (Supplement), 28, 134.

    Google Scholar 

  • Gerson, J. S. (2000). Social relationships in wild red-fronted brown lemurs (Eulemur fulvus rufus). Ph.D. dissertation, Duke University.

  • Godfrey, L. R., Sutherland, M. R., Petto, A. J., & Boy, D. S. (1990). Size, space, and adaptation in some subfossil lemurs from Madagascar. American Journal of Physical Anthropology, 81, 45–66.

    Article  CAS  PubMed  Google Scholar 

  • Gordon, A. D. (2006). Scaling of size and dimorphism in primates II: macroevolution. International Journal of Primatology, 27, 63–105.

    Article  Google Scholar 

  • Gordon, A. D., Johnson, S. E., & Louis, E. E., Jr. (2013). Females are the ecological sex: sex-specific body mass ecogeography in wild sifaka populations (Propithecus spp.). American Journal of Physical Anthropology, 151, 77–87.

    Article  PubMed  Google Scholar 

  • Harcourt, A. H., & Schreier, B. M. (2009). Diversity, body mass, and latitudinal gradients in primates. International Journal of Primatology, 30, 283–300.

    Article  Google Scholar 

  • Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978.

    Article  Google Scholar 

  • Ito, T., Nishimura, T., & Takai, M. (2014). Ecogeographical and phylogenetic effects on craniofacial variation in macaques. American Journal of Physical Anthropology, 154, 27–41.

    Article  PubMed  Google Scholar 

  • IUCN (2014). IUCN Red List of Threatened Species. Version 2014.3.

  • Johnson, S. E., Gordon, A. D., Stumpf, R. M., Overdorff, D. J., & Wright, P. (2005). Morphological variation in populations of Eulemur albocollaris and E. fulvus rufus. International Journal of Primatology, 26, 1399–1416.

    Article  Google Scholar 

  • Johnson, S. E., Lei, R., Martin, S. K., Irwin, M. T., & Louis, E. E. (2008). Does Eulemur cinereiceps exist? Preliminary evidence from genetics and ground surveys in southeastern Madagascar. American Journal of Primatology, 70, 372–385.

    Article  CAS  PubMed  Google Scholar 

  • Kamilar, J. M., & Muldoon, K. M. (2010). The climatic niche diversity of Malagasy primates: a phylogenetic approach. PLoS ONE, 5, e11073.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kamilar, J. M., Muldoon, K. M., Lehman, S. M., & Herrera, J. P. (2012). Testing Bergmann's rule and the resource seasonality hypothesis in Malagasy primates using GIS-based climate data. American Journal of Physical Anthropology, 147, 401–408.

    Article  PubMed  Google Scholar 

  • Kappeler, P. M. (1990). The evolution of sexual size dimorphism in prosimian primates. American Journal of Primatology, 21, 201–214.

    Article  Google Scholar 

  • Kappeler, P. M. (1991). Patterns of sexual dimorphism in body weight among prosimian primates. Folia Primatologica, 57, 132–146.

    Article  CAS  Google Scholar 

  • Lahann, P., Schmid, J., & Ganzhorn, J. U. (2006). Geographic variation in populations of Microcebus murinus in Madagascar: resource seasonality or Bergmann's rule? International Journal of Primatology, 27, 983–999.

    Article  Google Scholar 

  • Lehman, S. M. (2007). Ecological and phylogenetic correlates to body size in the Indriidae. International Journal of Primatology, 28, 183–210.

    Article  Google Scholar 

  • Lehman, S. M., Mayor, M., & Wright, P. C. (2005). Ecogeographic size variations in sifakas: a test of the resource seasonality and resource quality hypotheses. American Journal of Physical Anthropology, 126, 318–328.

    Article  PubMed  Google Scholar 

  • Leigh, S. R., & Shea, B. T. (1996). Ontogeny of body size variation in African apes. American Journal of Physical Anthropology, 99, 43–65.

    Article  CAS  PubMed  Google Scholar 

  • Leigh, S. R., & Terranova, C. J. (1998). Comparative perspectives on bimaturism, ontogeny, and dimorphism in lemurid primates. International Journal of Primatology, 19, 723–749.

    Article  Google Scholar 

  • Lindstedt, S. L., & Boyce, M. S. (1985). Seasonality, fasting endurance, and body size in mammals. The American Naturalist, 125, 873–878.

    Article  Google Scholar 

  • Markolf, M., & Kappeler, P. M. (2013). Phylogeographic analysis of the true lemurs (genus Eulemur) underlines the role of river catchments for the evolution of micro-endemism in Madagascar. Frontiers in Zoology, 10, 70.

    Article  PubMed  PubMed Central  Google Scholar 

  • Martins, E. P., & Hansen, T. F. (1997). Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. The American Naturalist, 149, 646–667. Erratum 153:448.

    Article  Google Scholar 

  • Mayr, E. (1956). Geographical character gradients and climatic adaptation. Evolution, 10, 105–108.

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Meiri, S., Yom-Yov, Y., & Geffen, E. (2007). What determines conformity to Bergmann’s rule? Global Ecology and Biogeography, 16, 788–794.

    Article  Google Scholar 

  • Mittermeier, R. A., Ganzhorn, J. U., Konstant, W. R., Glander, K., Tattersall, I., Groves, C. P., Rylands, A. B., Hapke, A., Ratsimbazafy, J., Mayor, M. I., Louis, E. E., Jr., Rumpler, Y., Schwitzer, C., & Rasoloarison, R. M. (2008). Lemur diversity in Madagascar. International Journal of Primatology, 29, 1607–1656.

    Article  Google Scholar 

  • Muldoon, K. M., & Simons, E. L. (2007). Ecogeographic size variation in small-bodied subfossil primates from Ankilitelo, southwestern Madagascar. American Journal of Physical Anthropology, 134, 152–161.

    Article  PubMed  Google Scholar 

  • Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N., & Pearse, W. (2012). Caper: Comparative analyses of phylogenetics and evolution in R. R package version 0.5.

  • Overdorff, D. J., & Johnson, S. E. (2004). Eulemur, true lemur. In S. M. Goodman & J. Benstead (Eds.), The natural history of Madagascar (pp. 1320–1324). Chicago: University of Chicago Press.

    Google Scholar 

  • Pagel, M. (1997). Inferring evolutionary processes from phylogenies. Zoologica Scripta, 26, 331–348.

    Article  Google Scholar 

  • Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401, 877–884.

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team. (2014). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Ravosa, M. J. (1998). Cranial allometry and geographic variation in slow lorises (Nycticebus). American Journal of Primatology, 45, 225–243.

    Article  CAS  PubMed  Google Scholar 

  • Ravosa, M. J., Meyers, D. M., & Glander, K. E. (1993). Relative growth of the limbs and trunk in sifakas: heterochronic, ecological, and functional considerations. American Journal of Physical Anthropology, 92, 499–520.

    Article  CAS  PubMed  Google Scholar 

  • Scholander, P. F. (1955). Evolution of climatic adaptation in homeotherms. Evolution, 9, 15–26.

    Article  Google Scholar 

  • Smith, R. J., & Cheverud, J. M. (2002). Scaling of sexual dimorphism in body mass: a phylogenetic analysis of Rensch's rule in primates. International Journal of Primatology, 23, 1095–1135.

    Article  Google Scholar 

  • Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of Human Evolution, 32, 523–559.

    Article  CAS  PubMed  Google Scholar 

  • Steudel, K., Porter, W. P., & Sher, D. (1994). The biophysics of Bergmann's rule: a comparison of the effects of pelage and body size variation on metabolic rate. Canadian Journal of Zoology, 72, 70–77.

    Article  Google Scholar 

  • Symonds, M. E., & Moussalli, A. (2011). A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behavioral Ecology and Sociobiology, 65, 13–21.

    Article  Google Scholar 

  • Terborgh, J., & van Schaik, C. P. (1987). Convergence vs. non-convergence in primate communities. In J. H. R. Gee & P. S. Giller (Eds.), Organization of communities, past and present (pp. 205–226). Oxford: Blackwell.

    Google Scholar 

  • Tokiniaina, H., Bailey, C., Shore, G., Delmore, K., Johnson, S., Louis, E., & Brenneman, R. (2009). Characterization of 18 microsatellite marker loci in the white-collared lemur (Eulemur cinereiceps). Conservation Genetics, 10, 1459–1462.

    Article  CAS  Google Scholar 

  • Zehr, S. M., Roach, R. G., Haring, D., Taylor, J., Cameron, F. H., & Yoder, A. D. (2014). Life history profiles for 27 strepsirrhine primate taxa generated using captive data from the Duke Lemur Center. Scientific Data, 1, 140019.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We are grateful to Giuseppe Donati for inviting us to contribute to this issue, and we thank him, Joanna Setchell, and three anonymous reviewers for their valuable comments on earlier versions of this manuscript. We also thank the government of Madagascar for permission to conduct the original research that was used for this analysis. We thank Omaha’s Henry Doorly Zoo and Aquarium Center for Conservation and Research, the Madagascar Biodiversity Partnership, and Madagascar Institut pour la Conservation des Écosystèmes Tropicaux (MICET) for assistance in original data collection, along with many individuals involved in original research (including Kira Delmore, Sheila Holmes, Christina Ingraldi, Annemarie Rued, and Hobinjatovo Tokiniaina). Grant sponsors for original research included the National Geographic Society (6613.99); Margot Marsh Biodiversity Fund; Conservation International; Primate Conservation, Inc.; the Natural Science and Engineering Research Council of Canada; the University of Calgary; the American Society of Primatologists; and the Ahmanson Family Foundation. A. D. Gordon also thanks the participants of the 2014 AnthroTree Workshop (supported by the National Science Foundation and the National Evolutionary Synthesis Center, NSF grants BCS-0923791 and EF-0905606) for discussions on phylogenetic comparative methods.

Author information

Authors and Affiliations

  1. Department of Anthropology, University at Albany – SUNY, Albany, NY, 12222, USA

    Adam D. Gordon

  2. Department of Anthropology and Archaeology, University of Calgary, Calgary, Alberta, Canada, T2N 1N4

    Steig E. Johnson

  3. Center for Conservation and Research, Omaha’s Henry Doorly Zoo and Aquarium, Omaha, NE, 68107, USA

    Edward E. Louis Jr.

Authors
  1. Adam D. Gordon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Steig E. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edward E. Louis Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adam D. Gordon.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

Supporting information regarding the maximum likelihood-based selection of consensus branch lengths for the phylogeny used in this analysis (ESM Fig. S1) and the resulting phylogram (ESM Fig. S2) are available online. (PDF 1.19 mb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gordon, A.D., Johnson, S.E. & Louis, E.E. Environmental Correlates of Body Mass in True Lemurs (Eulemur spp.). Int J Primatol 37, 89–108 (2016). https://doi.org/10.1007/s10764-015-9874-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-015-9874-9

Keywords

  • Bergmann’s rule
  • Heat conservation hypothesis
  • Madagascar
  • Phylogenetic methods