Abstract
Degraded forest habitats typically show low fruit availability and scattered fruit tree distribution. This has been shown to force frugivorous primates either to move further in search of food, resulting in large home ranges, or to use energy saving strategies. Malagasy lemurs are known to face pronounced seasonality and resource unpredictability, which is amplified by the overall reduction in food availability due to the human-driven habitat disturbance on the island. To explore lemur flexibility to habitat disturbance, we examined the ranging behavior of collared brown lemurs (Eulemur collaris) in two differently degraded fragments of littoral forest of southeastern Madagascar. We collected data from February 2011 to January 2012 on two groups living in a degraded area and two groups living in a less disturbed forest. We calculated annual ranges, monthly ranges, and daily distance traveled. We then ran repeated measures ANOVAs using seasonality as dichotomous, intrasubject factor and site/group as intersubject nested factors. In the degraded forest, the lemurs had larger monthly ranges, and their annual ranges were either fragmented or characterized by multiple core areas. They were able to use a habitat mosaic that also included nonforested areas and swamps. In addition, they shortened their daily path length, possibly to preserve energy, and used different areas of their annual home ranges seasonally. Although a number of possible confounding factors may have been responsible for the observed differences between sites, our findings highlight the ranging flexibility of collared brown lemurs in littoral forest fragments.
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References
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3), 227–267.
Barton, R. A., Whiten, A., Strum, S. C., Byrne, R. W., & Simpson, A. J. (1992). Habitat use and resource availability in baboons. Animal Behaviour, 43, 831–844.
Bayart, F., & Simmen, B. (2005). Demography, range use, and behavior in black lemurs (Eulemur macaco macaco) at Ampasikely, northwest Madagascar. American Journal of Primatology, 67(3), 299–312.
Bollen, A., & Donati, G. (2005). Phenology of the littoral forest of Sainte Luce, Southeastern Madagascar. Biotropica, 37(1), 32–43.
Bollen, A., & Donati, G. (2006). Conservation status of the littoral forest of south-eastern Madagascar: A review. Oryx, 40(1), 57–66.
Boyle, S. A., Lourenço, W. A., da Silva, L. R., & Smith, A. T. (2009). Travel and spatial patterns change when Chiropotes satanas chiropotes inhabit forest fragments. International Journal of Primatology, 30(4), 515–531.
Burt, W. H. (1943). Territoriality and home range concepts as applied to mammals. Journal of Mammalogy, 24(3), 346–352.
Butynski, T. M. (1990). Comparative ecology of blue monkeys (Cercopithecus mitis) in high-density and low-density subpopulations. Ecological Monographs, 60(1), 1–26.
Chapman, C. (1988). Patterns of foraging and range use by three species of Neotropical primates. Primates, 29(2), 177–194.
Clutton-Brock, T. H. (1975). Ranging behaviour of red colobus (Colobus badius tephrosceles) in the Gombe National Park. Animal behaviour, 23(August), 706–722.
Clutton-Brock, T. H. (1977). Some aspects of intraspecific variation in feeding and ranging behaviour in primates. In T. H. Clutton-Brock (Ed.), Primate ecology (pp. 539–556). London: Academic Press.
Clutton-Brock, T. H., & Harvey, P. H. (1979). Home range size, population density and phylogeny in primates. In I. S. Berstein & E. O. Smith (Eds.), Primate ecology and human origins: Ecological influences on social organization (pp. 201–214). New York: Garland.
Colquhoun, I. C. (1993). The socioecology of Eulemur macaco: A preliminary report. In P. M. Kappeler & J. U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 11–25). New York: Plenum Press.
Cristóbal-Azkarate, J., & Arroyo-Rodríguez, V. (2007). Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: Effects of habitat fragmentation and implications for conservation. American Journal of Primatology, 69(9), 1013–1029.
Curtis, D. J., & Zaramody, A. (1998). Group size, home range, and seasonal variation in the ecology of Eulemur mongoz. International Journal of Primatology, 19(5), 811–835.
Dewar, R. E., & Richard, A. F. (2007). Evolution in the hypervariable environment of Madagascar. Proceedings of the National Academy of Sciences of the USA, 104(34), 13723–13727.
Donati, G. (2002). The activity cycle and its ecological correlates in the collared brown lemur, Eulemur fulvus collaris (Lemuridae), in the Littoral Forest of Ste. Luce (Fort Dauphin, Madagascar). Ph.D. dissertation, University of Pisa.
Donati, G., Bollen, A., Borgognini-Tarli, S. M., & Ganzhorn, J. U. (2007a). Feeding over the 24-hour cycle: Dietary flexibility of cathemeral collared lemurs (Eulemur collaris). Behavioral Ecology and Sociobiology, 61(8), 1237–1251.
Donati, G., Kesch, K., Ndremifidy, K., Schmidt, S. L., Ramanamanjato, J. B., Borgognini-Tarli, S. M., & Ganzhorn, J. U. (2011a). Better few than hungry: Flexible feeding ecology of collared lemurs Eulemur collaris in littoral forest fragments. PLoS ONE, 6(5), e19807. doi:10.1371/journal.pone.0019807.
Donati, G., Ramanamanjato, J. B., Ravoahangy, A. M., & Vincelette, M. (2007b). Translocation as a conservation measure for a threatened species: The case of Eulemur collaris in the Mandena littoral forest, south-eastern Madagascar. In J. U. Ganzhorn, S. M. Goodman, & M. Vincelette (Eds.), Biodiversity, ecology and conservation of the littoral ecosystems of south-eastern Madagascar (pp. 237–245). Washington, DC: Smithsonian Institution Press.
Donati, G., Ricci, E., Baldi, N., Morelli, V., & Borgognini-Tarli, S. M. (2011b). Behavioral thermoregulation in a gregarious lemur, Eulemur collaris: Effects of climatic and dietary-related factors. American Journal of Physical Anthropology, 144(3), 355–364.
Du Puy, D. J., & Most, J. (1996). A refined classification of the primary vegetation of Madagascar based on the underlying geology: Using GIS to map its distribution and to assess its conservation status. In W. R. Lourence (Ed.), Biogeography of Madagascar (pp. 205–218). Paris: Orstom.
Fleury, M. C., & Gauthier-Hion, C. (1999). Seminomadic ranging in a population of black colobus (Colobus satanas) in Gabon and its ecological correlates. International Journal of Primatology, 20(4), 491–509.
Ganzhorn, J. U., Andrianasolo, T., Andrianjazalahatra, T., Donati, G., & Fietz, J. (2007). Lemurs in evergreen littoral forest fragments. In J. U. Ganzhorn, S. M. Goodman, & M. Vincelette (Eds.), Biodiversity, ecology and conservation of the littoral ecosystems of South-Eastern Madagascar (pp. 223–236). Washington, DC: Smithsonian Institution Press.
Goodall, A. J. (1977). Feeding and ranging behavior of a mountain gorilla group (Gorilla gorilla beringei) in the Tshibinda-Kahuzi region (Zaire). In T. H. Clutton-Brock (Ed.), Primate ecology (pp. 450–479). London: Academic Press.
Green, G. M., & Sussman, R. W. (1990). Deforestation history of the eastern rain forests of Madagascar from satellite images. Science, 248(4952), 212–215.
Harestad, A. S., & Bunnel, F. L. (1979). Home range and body weight: A reevaluation. Ecology, 60(2), 389–402.
Haskell, J. P., Ritchie, M. E., & Olff, H. (2002). Fractal geometry predicts varying body size scaling relationships for mammal and bird home ranges. Nature, 418(6897), 527–530.
Hixon, M. A. (1982). Energy maximizers and time minimizers: Theory and reality. The American Naturalist, 119(4), 596–599.
Horne, J. S., & Garton, E. O. (2006). Likelihood cross-validation versus least squares cross-validation for choosing the smoothing parameter in kernel home-range analysis. The Journal of Wildlife Management, 70(3), 641–648.
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.
Jaffe, K. E., & Isabell, L. A. (2010). Changes in ranging and agonistic behavior of vervet monkeys (Cercopithecus aethiops) after predator-induced group fusion. American Journal of Primatology, 72(7), 634–644.
Janson, C. H. (1988). Food competition in brown capuchin monkey (Cebus apella) – quantitative effects of group-size and tree productivity. Behaviour, 105(1–2), 53–73.
Johnson, S. E. (2002). Ecology and speciation in brown lemurs: White-collared lemurs (Eulemur albocollaris) and hybrids (Eulemur albocollaris × Eulemur fulvus rufus) in Southeastern Madagascar. Ph.D. dissertation, University of Texas, Austin.
Jolly, A. (1984). The puzzle of female feeding priority. In M. Small (Ed.), Female primates: Studies by women primatologists (pp. 197–215). New York: Alan R. Liss.
Kaplin, B. (2001). Ranging behavior of two species of guenons (Cercopithecus lhoesti and C. mitis doggetti) in the Nyungwe Forest Reserve, Rwanda. International Journal of Primatology, 22(4), 521–548.
Kelley, E. A. (2013). The ranging behavior of Lemur catta in the region of Cap Sainte-Marie, Madagascar. American Journal of Physical Anthropology, 150(1), 122–132.
Li, Y., Jiang, Z., Li, C., & Grueter, C. C. (2010). Effects of seasonal folivory and frugivory on ranging patterns in Rhinopithecus roxellana. International Journal of Primatology, 31(4), 609–626.
Lurz, P. W., Garson, P. J., & Wauters, L. A. (2000). Effects of temporal and spatial variations in food supply on the space and habitat use of red squirrels (Sciurus vulgaris L.). Journal of Zoology, 251(2), 167–178.
Martinez, B. (2008). Occurrence of bamboo lemurs, Hapalemur griseus occidentalis, in an agricultural landscape on the Masoala peninsula. Lemur News, 13, 11–14.
McCann, C., Williams-Guillen, K., Koontz, F., Espinoza, A. A. R., Martinez Sanches, J. C., & Koontz, C. (2003). Shade coffee plantations as wildlife refuge for mantled howler monkeys (Alouatta palliata) in Nicaragua. In L. K. Marsh (Ed.), Primates in fragments: Ecology and conservation (pp. 321–341). New York: Kluwer Academic/Plenum.
Mitani, J. C., & Rodman, P. S. (1979). Territoriality: The relation of ranging pattern and home range size to defendability, with an analysis of territoriality among primate species. Behavioral Ecology and Sociobiology, 5(3), 241–251.
Mitchell, M. S., & Powell, R. A. (2004). A mechanistic home range model for optimal use of spatially distributed resources. Ecological Modelling, 177(1–2), 209–232.
Mitchell, M. S., & Powell, R. A. (2012). Foraging optimally for home ranges. Journal of Mammalogy, 93(4), 917–928.
Morland, H. S. (1993). Seasonal behavioral variation and its relationship to thermoregulation in ruffed lemurs (Varecia variegata variegata). In P. M. Kappeler & J. U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 193–203). New York: Plenum Press.
Nilsen, E. B., Pedersen, S., & Linnell, J. D. C. (2008). Can minimum convex polygon home ranges be used to draw biologically meaningful conclusions? Ecological Research, 23(3), 635–639
Oates, J. F. (1987). Food distribution and foraging behavior. In B. B. Smuts, R. W. Wrangham, D. L. Cheney, T. T. Struhsaker, & R. M. Seyfarth (Eds.), Primate societies (pp. 197–209). Chicago: University of Chicago Press.
Ostro, L. E. T., Silver, S. C., Koontz, F. W., Young, T. P., & Horwich, R. H. (1999). Ranging behavior of translocated and established groups of black howler monkeys Alouatta pigra in Belize, Central America. Biological Conservation, 87(2), 181–190.
Overdorff, D. J. (1993). Ecological and reproductive correlates to range use in redbellied lemurs (Eulemur rubriventer) and rufous lemurs (Eulemur fulvus rufus). In P. M. Kappeler & J. U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 167–177). New York: Plenum Press.
Overdorff, D. J., Merenlender, A. M., Talata, P., Telo, A., & Forward, Z. (1999). Life history of Eulemur fulvus rufus from 1988–1998 in Southeastern Madagascar. American Journal of Physical Anthropology, 108(3), 295–310.
Pasch, B., & Koprowski, J. L. (2011). Impacts of fire suppression on space use by Mexican fox squirrels. Journal of Mammalogy, 92(1), 227–234.
Pereira, M. E., Strohecker, R. A., Cavigelli, S. A., Hughes, C. L., & Pearson, D. D. (1999). Metabolic strategy and social behavior in Lemuridae. In B. Rakotosamimanana, H. Rasamimanana, J. U. Ganzhorn, & S. M. Goodman (Eds.), New directions in lemur studies (pp. 93–118). New York: Kluwer Academic/Plenum Press.
Pielou, E. C. (1969). An introduction to mathematical ecology. New York: John Wiley & Sons.
Powell, R. A. (2000). Animal home ranges and territories and home range estimators. In L. Boitani & T. K. Fuller (Eds.), Research techniques in animal ecology: Controversies and consequences (pp. 65–110). New York: Columbia University Press.
Rabenantoandro, J., Randriatafika, F., & Lowry, P. P., II. (2007). Floristic and structural characteristics of remnant littoral forest sites in the Tolagnaro area. In J. U. Ganzhorn, S. M. Goodman, & M. Vincelette (Eds.), Biodiversity, ecology and conservation of the littoral ecosystems of South-Eastern Madagascar (pp. 65–77). Washington, DC: Smithsonian Institution Press.
Rasmussen, M. A. (1999). Ecological influences on activity cycle in two cathemeral primates, Eulemur mongoz (mongoose lemur) and Eulemur fulvus fulvus (common brown lemur). Ph.D. dissertation, Duke University.
Richard, A. (1978). Behavioural variation: Case study of a Malagasy lemur. Lewisburg: Bucknell University Press.
Richard, E., Said, S., Hamann, J. L., & Gaillard, J. M. (2011). Toward an identification of resources influencing habitat use in a multi-specific context. PLoS ONE, 6(12), e29048. doi:10.1371/journal.pone.0029048.
Richard-Hansen, C., Vie, J. C., & de Thoisy, B. (2000). Translocation of red howler monkeys (Alouatta seniculus) in French Guiana. Biological Conservation, 93(2), 247–253.
Rodríguez-Toledo, E. M., Mandujano, S., & Garcia-Orduña, F. (2003). Relationships between forest fragments and howler monkeys (Alouatta palliata mexicana) in southern Veracruz, Mexico. In L. K. Marsh (Ed.), Primates in fragments: Ecology and conservation (pp. 79–97). New York: Kluwer Academic/Plenum Press.
Sato, H. (2012). Diurnal resting in brown lemurs in a dry deciduous forest, northwestern Madagascar: Implications for seasonal thermoregulation. Primates, 53(3), 255–263.
Sato, H. (2013). Habitat shifting by the common brown lemur (Eulemur fulvus fulvus): A response to food scarcity. Primates, 54(3), 229–235.
Schoener, T. W. (1971). Theory of feeding strategies. Annual Review of Ecology and Systematics, 2, 369–404.
Scholz, F., & Kappeler, P. M. (2004). Effects of seasonal water scarcity on the ranging behavior of Eulemur fulvus rufus. International Journal of Primatology, 25(3), 599–613.
Schwitzer, C., Glatt, L., Nekaris, K. A. I., & Ganzhorn, J. U. (2011). Response of animals to habitat alteration: An overview focusing on primates. Endangered Species Research, 14, 31–38.
Schwitzer, C., Mittermeier, R. A., Johnson, S. E., Donati, G., Irwin, M., Peacock, H., Ratsimbazafy, J., Razafindramanana, J., Louis, E. E., Jr., Chikhi, L., Colquhoun, I. C., Tinsman, J., Dolch, R., LaFleur, M., Nash, S., Patel, E., Randrianambinina, B., Rasolofoharivelo, T., & Wright, P. C. (2014). Averting lemur extinctions amid Madagascar’s political crisis. Science, 343(6173), 842–843.
Schwitzer, N., Randriatahina, G. H., Kaumanns, W., Hoffmeister, D., & Schwitzer, C. (2007). Habitat utilization of blue-eyed black lemurs, Eulemur macaco flavifrons (Gray, 1867), in primary and altered forest fragments. Primate Conservation, 22, 79–87.
Seaman, D. E., Millspaugh, J. J., Kernohan, B. J., Brundige, G. C., Raedeke, K. J., & Gitzen, R. A. (1999). Effects of sample size on kernel home range estimates. Journal of Wildlife Management, 63(2), 739–747.
Seaman, D. E., & Powell, R. A. (1996). An evaluation of the accuracy of kernel density estimators for home range analysis. Ecology, 77(7), 2075–2085.
Steenbeek, R. (1999). Tenure related changes in wild Thomas's langurs I: Between-group interactions. Behaviour, 136(5), 595–625.
Stevenson, P. R. (2006). Activity and ranging patterns of Colombian woolly monkeys in north-western Amazonia. Primates, 47(3), 239–247.
Sussman, R. W. (1974). Ecological distinctions in sympatric species of lemur. In R. D. Martin, G. A. Doyle, & A. C. Walker (Eds.), Prosimian biology (pp. 75–108). London: Duckworth.
Vander Wal, E., & Rodgers, A. R. (2012). An individual-based quantitative approach for delineating core areas of animal space use. Ecological Modeling, 224(1), 48–53.
Vasey, N. (1997). How many red ruffed lemurs are left? International Journal of Primatology, 18(2), 207–216.
Volampeno, M. S. N., Masters, J. C., & Downs, C. T. (2011). Home range size in the blue-eyed black lemur (Eulemur flavifrons): A comparison between dry and wet seasons. Mammalian Biology, 76(2), 157–164.
Wallace, R. B. (2006). Seasonal variations in black-faced black spider monkey (Ateles chamek) habitat use and ranging behavior in a southern Amazonian tropical forest. American Journal of Primatology, 68(4), 313–332.
Wieczkowski, J. (2005). Examination of increased annual range of a Tana mangabey (Cercocebus galeritus) group. American Journal of Physical Anthropology, 128(2), 381–388.
Wong, S. N. P., & Sicotte, P. (2007). Activity budget and ranging patterns of Colobus vellerosus in forest fragments in central Ghana. Folia Primatologica, 78(4), 245–254.
Worton, B. J. (1995). Using Monte Carlo simulation to evaluate kernel-based home range estimators. Journal of Wildlife Management, 59(4), 794–800.
Wright, P. C. (1999). Lemur traits and Madagascar ecology: Coping with an island environment. Yearbook of Physical Anthropology, 42, 31–72.
Wright, P. C., Razafindratsita, V. R., Pochron, S. T., & Jernvall, J. (2005). The key to Madagascar frugivores. In J. L. Dew & J. P. Boubli (Eds.), Tropical fruits and frugivores (pp. 121–138). Dordrecht: Springer.
Yamagiwa, J., & Mwanza, N. (1994). Day-journey length and daily diet of solitary male gorillas in lowland and highland habitats. International Journal of Primatology, 15(2), 207–224.
Acknowledgments
This work was conducted under the collaboration agreement with the Department of Animal Biology and Anthropology of the University of Antananarivo and QIT Madagascar Minerals (QMM). This research was supported by the Rufford Small Grant Foundation. We thank the Madagascar Institute for the Conservation of Tropical Environments (MICET), the Association of Managers of Forests of Ambatoatsinana (FIMPIA), the Mandena Management Committee (COGEMA), and the Ministère des Eaux et Forets for their collaboration and permission to work in Madagascar. We thank Aristide Andrianarimisa for his help during this research. We are also grateful to Silvana Borgognini for her support in the early stages of this research and to Lauren Lansdowne and Rachel Sawyer for the language revision of this manuscript. We acknowledge the QMM biodiversity staff, especially Jean-Baptiste Ramanamanjato, Manon Vincelette, Johny Rabenantoandro, Christophe Rambolamanana, Laza Andriamandimbiarisoa, David Rabehevitra, Sylvio Angelico, Claude Soanary, and the field assistants (Kadofa, Josette, Faris, Philemon, Germain, Crescent) at Mandena and Ste. Luce. Joanna Setchell and two anonymous reviewers provided key suggestions and feedbacks that greatly improved this manuscript.
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Campera, M., Serra, V., Balestri, M. et al. Effects of Habitat Quality and Seasonality on Ranging Patterns of Collared Brown Lemur (Eulemur collaris) in Littoral Forest Fragments. Int J Primatol 35, 957–975 (2014). https://doi.org/10.1007/s10764-014-9780-6
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DOI: https://doi.org/10.1007/s10764-014-9780-6