Variation de la masse et des caractères morphologiques des lémuriens nocturnes dans les forêts primaires et dégradées de Menabe Sud, Belo sur Mer, Madagascar

Authors

Keywords:

lémuriens nocturnes, primates, structure forestière, caractères morphologiques, Madagascar.

Abstract

Forest structure effects primate morphology because it determines the availability and characteristics of resources, such as substrates for locomotion, sleeping trees, and trees food. However, forest degradation may alter environmental condition of habitats and influence lemur behavior and morphology. We evaluated the links between forest degradation, lemur body mass, and lemur morphometric. We surveyed red-tailed sportive lemurs (Lepilemur ruficaudatus) and gray mouse lemurs (Microcebus murinus) in the dry, deciduous forest of southern Menabe, Morondava, Madagascar. The study was conducted in the dry season in 2014 (November–December) and 2015 (July–September). Lemur captures were conducted in five forest sites: two primary forest and three disturbed forest. Sherman and Tomahawk style traps were used to capture mouse lemurs. We conducted three capture sessions in site B in 2014 and three capture sessions for each site in 2015, for a total of 5616 night traps. During each capture session, 80 Sherman traps and 24 Tomahawk traps were installed for three consecutive nights. To capture the red-tailed sportive lemur, we used a gun (Dan Inject Model JM air rifle) with a tranquillizer dart to immobilize the animal. We collected morphometric measurements from 232 mouse lemurs and 31 red-tailed sportive lemurs. Botanic plots (5m x 5m) allowed us to characterize the forest characteristics: tree diameter at breast height (DBH), tree height, tree abundance, tree crown height and diameter. Tree abundance with DBH ≥ 5 cm and trees diversity varied significantly between sites (P < 0.001). Mouse lemur body mass did not vary with seasonality of the capture (P > 0.05). For mouse lemurs, all morphometric from two populations in the pristine forest were similar (P > 0.05). Mouse lemurs in one disturbed habitat had greater body length and body mass than mouse lemurs in the pristine forest (P < 0.05). The difference may be linked with fruit abundance of two trees species (Tamarindus indica and Ziziphus mauritiana) and more insect availability in the disturbed site. In the altered habitat, mouse lemur females had longest body size and heavier than males (P < 0.05). Red-tailed sportive lemur body mass and length did not change between sites (P > 0.05). Our study is consistent with the hypothesis that lemur morphometric and body mass may change with forest degradation in southern forest of Menabe. Additionally, the range of the response varies between species and sex: mouse lemurs had a wider reaction norm to the habitat disturbance than did red-tailed sportive lemurs. Mouse lemurs may have higher ecological flexibility and tolerance for forest changes, specifically the alteration of forest habitats. Understanding how lemur morphology responds to habitat disturbance may be used as a tool to prioritize lemur conservation.

 

Résumé

La perte d’habitat due à l’activité humaine est une menace qui affecte tous les primates à Madagascar. Les lémuriens, primates arboricoles, ont des réponses variées face au changement de leur habitat. La présente recherche vise à déterminer le lien entre la dégradation forestière, la masse et les caractères morphologiques des lémuriens nocturnes de Menabe Sud : Lepilemur ruficaudatus et Microcebus murinus. L’étude a été effectuée dans cinq sites dont deux sites sont des forêts primaires et trois autres sont des forêts perturbées. La capture et la mesure des caractères morphologiques des lémuriens ont été réalisées entre novembre et décembre 2014, puis entre juillet et septembre 2015. Des parcelles botaniques (5m x 5m) ont été utilisées pour décrire les caractéristiques des sites dont l’abondance des arbres, le diamètre à hauteur de poitrine ou la hauteur et le diamètre de la couronne. La masse de M. murinus n’était pas influencée par la saison de capture (P > 0,05), mais elle variait avec le sexe (P < 0,005) et le site (P < 0,001). Tous les caractères morphologiques de M. murinus dans les deux forêts primaires étaient similaires (P > 0,05). Par contre, dans les forêts perturbées, les femelles de M. murinus étaient plus lourdes et avaient des corps plus longs que les mâles (P < 0,05). La masse et la longueur du corps de L. ruficaudatus entre les différents sites étaient similaires (P > 0,05). Comparé à L. ruficaudatus, M. murinus répondrait davantage à la dégradation forestière. Comprendre l’étendue de la réponse morphologique des lémuriens face à la dégradation de leur habitat pourrait être utilisé comme outil pour prioriser leur conservation.

Author Biographies

Jean Elvis Rakotomalala, Mention Zoologie et Biodiversité Animale, Faculté des Sciences, Université d’Antananarivo, BP 906, Antananarivo 101

Mention Zoologie et Biodiversité Animal, Faculté  de Sciences, Université d’Antananarivo, BP 906, Antananarivo 101

Doctorant

Rebecca J. Lewis, Department of Anthropology 2201 Speedway, Stop C3200 University of Texas at Austin, Austin, TX 78712-1723

Department of Anthropology 2201 Speedway, Stop C3200 University of Texas at Austin, Austin, TX 78712-1723 

Full Professor

Edward E. Louis, Department of Conservation Genetics, Omaha’s Henry Doorly Zoo & Aquarium, 3701 S 10th St, Omaha, NE 68107

Department of Conservation Genetics, Omaha’s Henry Doorly Zoo & Aquarium, 3701 S 10th St, Omaha, NE 68107

Director of Conservation Genetics Department

Hajanirina Fanomezantsoa Rakotomanana, Mention Zoologie et Biodiversité Animale, Faculté des Sciences, Université d’Antananarivo, BP 906, Antananarivo 101

Mention Zoologie et Biodiversité Animale,  Faculté des Sciences, Université d’Antananarivo, BP 906, Antananarivo 101, Madagascar.

Professeur Titulaire

 

References

Agostini, G., Rasoazanabary, E. & Godfrey, L. R. 2017.The befuddling nature of mouse lemur hands and feet at Beza Mahafaly, SW Madagascar. American Journal of Primatology 79, 9: e22690. <https://doi.org/10.1002/ajp.22680>

Ah-King, M. & Nylin, S. 2010. Sex in an evolutionary perspective: just another reaction norm. Evolutionary Biology 37, 4: 234–246. <https://doi.org/10.1007%2Fs11692-010-9101-8>

Allen, C. R., Havlicek, T. D., Garmestani, A. S., Peterson, G. D., Stow, C. A., et al. 2006. Patterns in body mass distributions: sifting among alternative hypotheses. Ecology Letters 9, 5: 630–643. <https://doi.org/10.1111/j.1461-0248.2006.00902.x>

Altmann, J., Schoeller, D., Altmann, S. A. Muruthi, P. & Sapolsky, R. M. 1993. Body size and fatness of free-living baboons reflect food availability and activity levels. American Journal of Primatology 30, 2: 149–161. <https://doi.org/10.1002/ajp.1350300207>

Andriatsitohaina, B., Romero‑Mujalli, D., Ramsay, M. S., Kiene, F., Rasoloharijaona, S. et al. 2020. Effects of habitat edges on vegetation structure and the vulnerable golden‑brown mouse lemur (Microcebus ravelobensis) in northwestern Madagascar. BMC Ecology 20: 69. <https://doi.org/10.1186/s12898-020-00337-z>

Axel, A. C. 2018. Burned area mapping of an escaped fire into tropical dry forest in western Madagascar using multi-season landsat OLI data. Remote Sensing 10, 3: 371.

Blanchard, M. L., Furnell, S., Sellers, W. I. & Crompton, R. H. 2015. Locomotor flexibility in Lepilemur explained by habitat and biomechanics. American Journal of Physical Anthropology 156, 1: 58–66. <https://doi.org/10.1002/ajpa.22627>

Burke, R. J. & Lehman, S. M. 2014. Edge effects on morphometrics and body mass in two sympatric species of mouse lemurs in Madagascar. Folia Primatologica 85, 5: 277–291. <https://doi.org/10.1159/000360082>

Chapman, C. A., Struhsaker, T. T., Skorupa, J. P., Snaith, T. V. & Rothman, J. M. 2010. Understanding long-term primate community dynamics: implications of forest change. Ecological Applications 20, 1: 179–191. <https://www.jstor.org/stable/27797797>

Chapman, C. A., Schoof, V. A. M., Bonnell, T. R., Gogarten, J. F. & Calmé, S. 2015. Competing pressures on populations: long-term dynamics of food availability, food quality, disease, stress and animal abundance. Philosophical Transactions of the Royal Society B 370, 1669: 20140112. <https://doi.org/10.1098/rstb.2014.0112>

Dagosto, M. & Yamashita, N. 1998. Effect of habitat structure on positional behavior and support use in three species of lemur. Primates 39: 459–472. <https://doi.org/10.1007/BF02557569>

Dammhahn, M. & Kappeler, P. M. 2008. Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. International Journal of Primatology, 29: 1567–1589. https://doi.org/10.1007/s10764-008-9312-3

Danthu, P., Soloviev, P., Totté, A., Tine, E., Ayessou, N., et al. 2002. Caractères physico-chimiques et organoleptiques comparés de jujubes sauvages et des fruits de la variété Gola introduite au Sénégal. Fruits 57, 3: 173–182. <https://doi.org/10.1051/fruits:2002016>

Ganzhorn, J. U. 2002. Distribution of folivorous lemur in relation to seasonally varying food resources: integrating quantitative and qualitative aspects of food characteristics. Oecologia 131, 3: 427–435. <https://doi.org/10.1007/s00442-002-0891-y>

Ganzhorn, J. U. & Schmid, J. 1998. Different population dynamics of Microcebus murinus in primary and secondary deciduous dry forests of Madagascar. International Journal of Primatology 19: 785–796. <https://doi.org/10.1023/A:1020337211827>

Ganzhorn, J. U., Malcomber, S. Andrianantoanina, O. & Goodman, S. M. 1997. Habitat characteristics and lemur species richness in Madagascar. Biotropica 29, 3: 331–343. <https://www.jstor.org/stable/2389148>

Ganzhorn, J. U., Goodman, S. M., Nash, S. & Thalmann, U. 2006. Lemur biogeography. In Primate Biogeography. S. M. Lehman & J. G. Fleagle (eds.), pp 229–254. Springer, New York. <https://doi.org/10.1007/0-387-31710-4_8>

Goodman, S. M., Raherilalao, M. J., Raselimanana, A., Ralison, J., Soarimalala, V. et Wilmé, L. 2008. Introduction. In Les Forêts Sèches de Madagascar. S.M. Goodman & L. Wilmé (eds.). Malagasy Nature 1: 2–32.

Gordon, A. D., Johnson, S. E. & Louis, E. E. 2016. Environmental correlates of body mass in true lemurs (Eulemur spp.). International Journal of Primatology 37: 89–108. <https://doi.org/10.1007/s10764-015-9874-9>

Hamacek, F. R., Santos, P. R. G., Cardoso, L. M. & Pinheiro-Sant’Ana, H. M. 2013. Nutritional composition of tamarind (Tamarindus indica L.) from the Cerrado of Minas Gerais, Brazil. Fruits 68, 5: 381–395. <https://doi.org/10.1051/fruits/2013083>

Hohenbrink, S., Schaarschmidt, F., Katharina Bünemann, K., Gerberding, S. Zimmermann, E. & Radespiel. U. 2016. Female dominance in two basal primates, Microcebus murinus and Microcebus lehilahytsara: variation and determinants. Animal Behaviour 122: 145–156. <https://doi.org/10.1016/j.anbehav.2016.10.008>

Irwin, M. T. 2008. Diademed sifaka (Propithecus diadema) ranging and habitat use in continuous and fragmented forest: higher density but lower viability in fragments? Biotropica 40, 2: 231–240. <https://doi.org/10.1111/j.1744-7429.2007.00368.x>

Irwin, M. T., Samonds, K. E., Raharison, J.-L., Junge, R. E., Mahefarisoa, K. L., et al. 2019. Morphometric signals of population decline in diademed sifakas occupying degraded rainforest habitat in Madagascar. Scientific Reports 9: 8776. <https://doi.org/10.1038/s41598-019-45426-2>

Kappeler, P. M., Rasoloarison, R. M., Razafimanantsoa, L., Walter, L. & Roos, C. 2005. Morphology, behavior and molecular evolution of giant mouse lemurs (Mirza spp) Gray, 1870, with description of a new species. Primate Report, 71: 3–26.

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. <https://doi.org/10.1007/s10764-006-9055-y>

Levey, D. J. 1990. Habitat-dependent fruiting behavior of an understory tree, Miconia centrodesma, and tropical treefall gaps as keystone habitats for frugivores in Costa Rica. Journal of Tropical Ecology 6, 4: 409–420. <https://doi.org/10.1017/S026646740000479X>

Lewis, R. & Axel, A. C. 2019. Using vegetation phenology and long-term demographic data to assess the impact of Cyclone Fanele on a lemur population in Madagascar. In Primate Research and Conservation in the Anthropocene. A. M. Behie., J. A. Teichroeb & N. Malone (eds.), pp 216–236. Cambridge University Press, Cambridge. <https://doi.org/10.1017/9781316662021.013>

Louis, Jr. E. E., Coles, M. S., Andriantompohavana, R., Sommer, J. A., Engberg, S. E., et al. 2006. Revision of the mouse lemurs (Primates, Microcebus) of eastern Madagascar. International Journal of primatology, 27: 347–389. <https://doi.org/10.1007/s10764-006-9036-1>

Mammides, C., Cords, M. & Peters, M. K. 2009. Effects of habitat disturbance and food supply on population densities of three primate species in the Kakamega forest, Kenya. African Journal of Ecology 47, 1: 87–96. <https://doi.org/10.1111/j.1365-2028.2007.00921.x>

Marshall, J. A. 2010. Effect of habitat quality on primate populations in Kalimantan: Gibbons and leaf monkeys as case studies. In Indonesian Primates. S. Gursky-Doyen & J. Supriatna (eds.), pp. 157–177. Springer, New York.

Moat, J. & Smith, P. 2007. Atlas of the vegetation of Madagascar. Royal Botanic Gardens, Kew.

Manduell, K. L., Harrison, M. E. & Thorpe, S. K. S. 2012. Forest structure and support availability influence orangutan locomotion in Sumatra and Borneo. American Journal of Primatology 74, 12: 1128–1142. <https://doi.org/10.1002/ajp.22072>

Orkin, J. D. & Pontzer, H. 2011. The Narrow Niche Hypothesis: Gray squirrels shed new light on primate origins. American Journal of Physical Anthropology 144, 4: 617–24. <https://doi.org/10.1002/ajpa.21450>

Pavelka, M. S. M. & Behi, A. M. 2005. The effect of hurricane Iris on the food supply of black howlers (Alouatta pigra) in southern Belize. Biotropica 37, 1: 102–108. <https://www.jstor.org/stable/30045512>

Perret, M. & Aujard, F. 2001. Regulation by photoperiod of seasonal changes in body mass and reproductive function in gray mouse lemurs (Microcebus murinus): differential responses by sex. International Journal of Primatology 22: 5–24. <https://doi.org/10.1023/A:1026457813626>

Rakotomalala, J. E., Rakotomanana, H. F., Louis, J. E. E. et Lewis, J. R. 2022. Effets des structures forestières sur l’occurrence et la préférence en microhabitat des lémuriens nocturnes de la forêt sèche de Menabe Sud, Madagascar. Afrique Science 20, 3: 1–12.

Rakotondranary, S. J., Hapke, A. & Ganzhorn, J. U. 2011. Distribution and morphological variation of Microcebus spp. along an environmental gradient in southeastern Madagascar. International Journal of Primatology 32: 1037–1057. <https://doi.org/10.1007/s10764-011-9521-z>

Rakotoniaina, J. H., Kappeler, P. M., Ravoniarimbinina, P., Pechouskova, E., Hämäläinen, A. M., et al. 2016. Does habitat disturbance affect stress, body condition and parasitism in two sympatric lemurs? Conservation Physiology 4, 1: cow034.

Ralison, J. 2008. Les lémuriens des forêts sèches malgaches. In Les Forêts Sèches de Madagascar. S.M. Goodman & L. Wilmé (eds.). Malagasy Nature 1: 135–156.

Rasoazanabary, E. 2006. Male and female activity patterns in Microcebus murinus during the dry season at Kirindy forest, western Madagascar. International Journal of Primatology 27: 437–464. <https://doi.org/10.1007/s10764-006-9017-4>

Rasoloarison, R. M., Goodman, S. M. & Ganzhorn, J. U. 2000. Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. International Journal of Primatology 21: 963–1019. <https://doi.org/10.1023/A:1005511129475>

Rasoloarison, R. M., Weisrock, D. W., Yoder, A. D., Rakotondravony, D. & Kappeler, P. M. 2013. Two new species of mouse lemurs (Cheirogaleidae: Microcebus) from eastern Madagascar. International Journal of Primatology 34: 455–469. <https://doi.org/10.1007/s10764-013-9672-1>

Richard, A. F., Dewar, R. E., Schwartz, M. & Ratsirarson, J. 2000. Mass change, environmental variability and female fertility in wild Propithecus verreauxi. Journal of Human Evolution 39, 4: 381–391.

Schwab, D. & Ganzhorn, J. U. 2004. The distribution and population structure of Microcebus berthae, the smallest known primate and its habitat use in relation to other sympatric cheirogaleids. International Journal of Primatology 25, 2: 307–330. <http://dx.doi.org/10.1023/B:IJOP.0000019154.17401.90>

UICN. 2022. Red List of Threatened Species. <https://www.iucnredlist.org>

Young, J. W. & Chadwell, B. A. 2020. Not all fine-branch locomotion is equal: Grasping morphology determines locomotor performance on narrow supports. Journal of Human Evolution 142: 102767. <https://doi.org/10.1016/j.jhevol.2020.102767>

Zimmermann, E., Cepok, S., Rakotoarison, N., Zietemann, V. & Radespiel, U. 1998. Sympatric mouse lemurs in North-West Madagascar: A new rufous mouse lemur species (Microcebus ravelobensis). Folia Primatologica 69: 106–114. <https://doi.org/10.1159/000021571>

Zinner, D., Wygoda, C., Razafimanantsoa, L., Rasoloarison, R., Andrianandrasana, H. T., et al. 2014. Analysis of deforestation patterns in the central Menabe, Madagascar, between 1973 and 2010. Regional Environmental Change 14, 1: 157–166. <http://dx.doi.org/10.1007/s10113-013-0475-x>

Zvaríková, M., Kiseľák, J., Zvarík, M., Masarovič, R., Prokop, P. & Fedor, P. 2016. Ecological gradients and environnemental impact in the forest dwelling Haplothrips subtilissimus (Thysanoptera: Phlaeothripidae) phenotypic variability. Ecological Indicators 66: 313–320. <https://doi.org/10.1016/j.ecolind.2016.01.038>

Lepilemur ruficaudatus, Kirindy Mité, Site D. Photo Elvis Rakotomalala

Downloads

Published

30-12-2023

Issue

Section

Articles

Most read articles by the same author(s)