Skip to main content

Advertisement

Log in

Ecological Flexibility as Measured by the Use of Pioneer and Exotic Plants by Two Lemurids: Eulemur collaris and Hapalemur meridionalis

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

Primate responses to habitat alteration vary depending on the species’ dietary guild and forest type. Leaves from secondary vegetation can provide nutritious resources to folivorous primates, whereas frugivores, burdened with a scattered spatial and temporal distribution of fruiting resources, require larger home ranges, potentially limiting their ability to cope with altered landscapes. Within coastal southeastern Madagascar, we sought to determine whether two lemur species occupying contrasting ecological niches respond differently to the changing features of their degraded and fragmented habitat. We conducted behavioral observations between 2011 and 2013 on frugivorous collared brown lemurs (Eulemur collaris) and folivorous southern bamboo lemurs (Hapalemur meridionalis). To estimate the ability of lemurs to use pioneer species, we categorized all plants used for feeding and resting as fast growing, mid-growing, or slow growing. We fitted general linear mixed-effects models, one for each plant growth category with monthly proportional use rates as the dependent variable, and included species (E. collaris and H. meridionalis), activity (feeding and resting), and season (dry and wet) as fixed effects. Our results show that E. collaris used both slow- and mid-growing plant species most often, while H. meridionalis were more likely to use fast-growing plants, which indicated an ability to use secondary/disturbed vegetation. Frugivorous E. collaris appear more limited by climax plants, while folivorous H. meridionalis appear to be slightly more adaptable, a finding that is consistent with that for other primate folivores.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Achard, F., Eva, H. D., Stibig, H. J., Mayaux, P., Gallego, J., et al. (2002). Determination of deforestation rates of the world's humid tropical forests. Science, 297, 999–1002.

    Article  CAS  PubMed  Google Scholar 

  • Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–266.

    Article  CAS  PubMed  Google Scholar 

  • Anderson, J., Rowcliffe, J. M., & Cowlishaw, G. (2007). Does the matrix matter? A forest primate in a complex agricultural landscape. Biological Conservation, 135, 212–222.

    Article  Google Scholar 

  • Arrigo-Nelson, S. J. (2006). The impact of habitat disturbance on the feeding ecology of the Milne-Edwards’ sifaka (Propithecus edwardsi) in Ranomafana National Park, Madagascar. Ph.D. dissertation, Stony Brook University.

  • Asner, G. P., Rudel, T. K., Aide, T. M., Defries, R., & Emerson, R. (2009). A contemporary assessment of change in humid tropical forests. Conservation Biology, 23, 1386–1395.

    Article  PubMed  Google Scholar 

  • Ballhorn, D. J., Rakotoarivelo, F. P., & Kautz, S. (2016). Coevolution of cyanogenic bamboos and bamboo lemurs on Madagascar. PLoS ONE, 11, e0158935.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barthlott, W., Lauer, W., & Placke, A. (1996). Global distribution of species diversity in vascular plants: Towards a world map of phytodiversity. Erdkunde, 50, 317–327.

    Article  Google Scholar 

  • Bates, D., Maechler, M., & Bolker, B. (2012). lme4: Linear mixed-effects models using S4 classes (2011). R package version 0.999375-42.

  • Benitez-Malvido, J. (1998). Impact of forest fragmentation on seedling abundance in a tropical rain forest. Conservation Biology, 12, 380–389.

    Article  Google Scholar 

  • Beyer, H. L. (2012). In Geospatial modelling environment. 0.7.2.0. http://www.spatialecology.com/gme

  • Bicca-Marques, J. C. (2003). How do howler monkeys cope with habitat fragmentation? In L. K. Marsh (Ed.), Primates in fragments: Ecology and conservation (pp. 283–303). New York: Springer Science + Business Media.

    Chapter  Google Scholar 

  • Bicca-Marques, J. C., & Calegaro-Marques, C. (1994). Exotic plant species can serve as staple food sources for wild howler populations. Folia Primatologica, 63, 209–211.

    Article  CAS  Google Scholar 

  • Bollen, A., & Donati, G. (2005). Phenology of the littoral forest of Sainte Luce, southeastern Madagascar. Biotropica, 37, 32–43.

    Article  Google Scholar 

  • Bollen, A., & Donati, G. (2006). Conservation status of the littoral forest of southeastern Madagascar: A review. Oryx, 40, 57–66.

    Article  Google Scholar 

  • Bonilla-Sánchez, Y. M., Serio-Silva, J. C., Pozo-Montuy, G., & Chapman, C. A. (2012). Howlers are able to survive in Eucalyptus plantations where remnant and regenerating vegetation is available. International Journal of Primatology, 33, 233–245.

    Article  Google Scholar 

  • Boyle, S. A., & Smith, A. T. (2010). Can landscape and species characteristics predict primate presence in forest fragments in the Brazilian Amazon? Biological Conservation, 143, 1134–1143.

    Article  Google Scholar 

  • Broadbent, E. N., Asner, G. P., Keller, M., Knapp, D. E., Oliveira, P. J., & Silva, J. N. (2008). Forest fragmentation and edge effects from deforestation and selective logging in the Brazilian Amazon. Biological Conservation, 141, 1745–1757.

    Article  Google Scholar 

  • Brokaw, N., & Busing, R. T. (2000). Niche versus chance and tree diversity in forest gaps. Trends in Ecology & Evolution, 15, 183–188.

    Article  CAS  Google Scholar 

  • Campbell-Smith, G., Campbell-Smith, M., Singleton, I., & Linkie, M. (2011). Apes in space: Saving an imperilled orangutan population in Sumatra. PLoS ONE, 6, e17210.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campera, M., Serra, V., Balestri, M., Barresi, M., Ravaolahy, M., et al. (2014). Effects of habitat quality and seasonality on ranging patterns of collared brown lemur (Eulemur collaris) in littoral forest fragments. International Journal of Primatology, 35, 957–975.

    Article  Google Scholar 

  • Chapman, C. A. (1995). Primate seed dispersal: Co-evolution and conservation implications. Evolutionary Anthropology, 4, 74–82.

    Article  Google Scholar 

  • Chapman, C. A., & Lambert, J. E. (2000). Habitat alteration and the conservation of African primates: Case study of Kibale National Park, Uganda. American Journal of Primatology, 50, 169–185.

    Article  CAS  PubMed  Google Scholar 

  • Chapman, C. A., Balcomb, S. R., Gillespie, T. R., Skorupa, J. P., & Struhsaker, T. T. (2000). Long-term effects of logging on African primate communities: A 28-year comparison from Kibale National Park, Uganda. Conservation Biology, 14, 207–217.

    Article  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Bjorndal, K., & Onderdonk, D. A. (2002). Application of protein to fiber ratios to predict colobine abundance on different spatial scales. International Journal of Primatology, 23, 283–310.

    Article  Google Scholar 

  • Coley, P. D., Bryant, J. P., & Chapin, F. S. (1985). Resource availability and plant antiherbivore defense. Science, 230, 895–899.

    Article  CAS  PubMed  Google Scholar 

  • Colquhoun, I. C. (1997). A predictive socioecological study of the black lemur (Eulemur macaco macaco) in northwestern Madagascar. Ph.D. dissertation, Washington University.

  • Cowlishaw, G., & Dunbar, R. (2000). Primate conservation biology. Chicago: University of Chicago Press.

    Google Scholar 

  • 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, 1013–1029.

    Article  PubMed  Google Scholar 

  • Curtis, D. J. (2004). Diet and nutrition in wild mongoose lemurs (Eulemur mongoz) and their implications for the evolution of female dominance and small group size in lemurs. American Journal of Physical Anthropology, 124, 234–247.

    Article  PubMed  Google Scholar 

  • D’Antonio, C. M., & Vitousek, P. M. (1992). Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annual Review of Ecological Systems, 23, 63–87.

    Article  Google Scholar 

  • Dehgan, A. (2003). The behavior of extinction: Predicting the incidence and local extinction of lemurs in fragmented habitats of southeastern Madagascar. Ph.D. dissertation, University of Chicago.

  • Dirzo, R., & Raven, P. H. (2003). Global state of biodiversity and loss. Annual Review of Environment and Resources, 28, 137–167.

    Article  Google Scholar 

  • Donati, G., Bollen, A., Borgognini-Tarli, S. M., & Ganzhorn, J. U. (2007). Feeding over the 24-h cycle: Dietary flexibility of cathemeral collared lemurs (Eulemur collaris). Behavioral Ecology and Sociobiology, 61, 1237–1251.

    Article  Google Scholar 

  • Donati, G., Kesch, K., Ndremifidy, K., Schmidt, S. L., Ramanamanjato, J. B., et al. (2011). Better few than hungry: Flexible feeding ecology of collared lemurs Eulemur collaris in littoral forest fragments. PLoS ONE, 6, e19807.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dumetz, N. (1999). High plant diversity of lowland rainforest vestiges in eastern Madagascar. Biodiversity and Conservation, 8, 273–315.

    Article  Google Scholar 

  • Eppley, T. M., Verjans, E., & Donati, G. (2011). Coping with low-quality diets: A first account of the feeding ecology of the southern gentle lemur, Hapalemur meridionalis, in the Mandena littoral forest, southeast Madagascar. Primates, 52, 7–13.

    Article  PubMed  Google Scholar 

  • Eppley, T. M., Donati, G., Ramanamanjato, J.-B., Randriatafika, F., Andriamandimbiarisoa, L. N., et al. (2015a). The use of an invasive species habitat by a small folivorous primate: Implications for conservation. PLoS ONE, 10, e0140981.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Eppley, T. M., Hall, K., Donati, G., & Ganzhorn, J. U. (2015b). An unusual case of affiliative association of a female Lemur catta in a Hapalemur meridionalis social group. Behaviour, 152, 1041–1061.

    Article  Google Scholar 

  • Eppley, T. M., Ganzhorn, J. U., & Donati, G. (2015c). Cathemerality in a small, folivorous primate: Proximate control of diet activity in Hapalemur meridionalis. Behavioral Ecology and Sociobiology, 69, 991–1002.

    Article  Google Scholar 

  • Eppley, T. M., Donati, G., & Ganzhorn, J. U. (2016a). Determinants of terrestrial feeding in an arboreal primate: The case of the southern bamboo lemur (Hapalemur meridionalis). American Journal of Physical Anthropology, 161, 328–342.

    Article  PubMed  Google Scholar 

  • Eppley, T. M., Donati, G., & Ganzhorn, J. U. (2016b). Unusual sleeping site selection by southern bamboo lemurs. Primates, 57, 167–173.

    Article  PubMed  Google Scholar 

  • Eppley, T. M., Ganzhorn, J. U., & Donati, G. (2016c). Latrine behaviour as a multimodal communicatory signal station in wild lemurs: The case of Hapalemur meridionalis. Animal Behaviour, 111, 57–67.

    Article  Google Scholar 

  • Estrada, A., & Coates-Estrada, R. (1996). Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas. International Journal of Primatology, 5, 759–783.

    Article  Google Scholar 

  • Federman, S., Dornburg, A., Daly, D. C., Downie, A., Perry, G. H., et al. (2016). Implications of lemuriform extinctions for the Malagasy flora. Proceedings of the National Academy of Sciences of the United States of America, 113, 5041–5046.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galat-Luong, A., & Galat, G. (2005). Conservation and survival adaptations of Temminck’s red colobus (Procolobus badius temmincki), in Senegal. International Journal of Primatology, 26, 585–603.

    Article  Google Scholar 

  • Ganzhorn, J. U. (1992). Leaf chemistry and the biomass of folivorous primates in tropical forests. Oecologia, 91, 540–547.

    Article  PubMed  Google Scholar 

  • Ganzhorn, J. U. (1995). Low-level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology, 76, 2084–2096.

    Article  Google Scholar 

  • Ganzhorn, J. U. (1997). Test of Fox’s assembly rule for functional groups in lemur communities in Madagascar. Journal of Zoology, 241, 533–542.

    Article  Google Scholar 

  • Ganzhorn, J. U., Fietz, J., Rakotovao, E., Schwab, D., & Zinner, D. (1999a). Lemurs and the regeneration of dry deciduous forest in Madagascar. Conservation Biology, 13, 794–804.

    Article  Google Scholar 

  • Ganzhorn, J. U., Wright, P. C., & Ratsimbazafy, J. (1999b). Primate communities: Madagascar. In J. G. Fleagle, C. H. Janson, & K. E. Reed (Eds.), Primate communities (pp. 75–89). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Ganzhorn, J. U., Andrianasolo, T., Andrianjazalahatra, T., Donati, G., Fietz, J., et al. (2007a). Lemurs in evergreen littoral forest fragments. In J. U. Ganzhorn, S. M. Goodman, & M. Vincelette (Eds.), Biodiversity, ecology, and conservation of the littoral ecosystems in Southeastern Madagascar, Tolagnaro (Fort Dauphin) (pp. 223–225). Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Ganzhorn, J. U., Goodman, S. M., & Vincelette, M. (2007b). Biodiversity, ecology and conservation of littoral ecosystems in southeastern Madagascar, Tolagnaro (Fort Dauphin). Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Ganzhorn, J. U., Wilmé, L., & Mercier, J.-L. (2014). Explaining Madagascar’s biodiversity. In I. R. Scales (Ed.), Conservation and environmental management in Madagascar (pp. 17–43). New York: Routledge.

    Google Scholar 

  • Gardner, C. J. (2009). A review of the impacts of anthropogenic habitat change on terrestrial biodiversity in Madagascar: Implications for the design and management of new protected areas. Malayan Nature Journal, 2, 2–29.

    Google Scholar 

  • Gérard, A., Ganzhorn, J. U., Kull, C. A., & Carrière, S. M. (2015). Possible roles of introduced plants for native vertebrate conservation: The case of Madagascar. Restoration Ecology, 23, 768–775.

    Article  Google Scholar 

  • Gibson, L., Lee, T. M., Koh, L. P., Brook, B. W., Gardner, T. A., et al. (2011). Primary forests are irreplaceable for sustaining tropical biodiversity. Nature, 478, 378–381.

    Article  CAS  PubMed  Google Scholar 

  • Grassi, C. (2006). Variability in habitat, diet, and social structure of Hapalemur griseus in Ranomafana National Park, Madagascar. American Journal of Physical Anthropology, 131, 50–63.

    Article  PubMed  Google Scholar 

  • Grimes, K., & Paterson, J. D. (2000). Colobus guereza and exotic plant species in the Entebbe Botanical Gardens. American Journal of Primatology, 51, 59–60.

    Google Scholar 

  • Guo, S., Ji, W., Li, B., & Li, M. (2008). Response of a group of Sichuan snub-nosed monkeys to commercial logging in the Qinling Mountains, China. Conservation Biology, 22, 1055–1064.

    Article  PubMed  Google Scholar 

  • Hannah, L., Dave, R., Lowry, P. P., II, Andelman, S., Andrianarisata, M., et al. (2008). Climate change adaptation for conservation in Madagascar. Biology Letters, 4, 590–594.

    Article  PubMed  PubMed Central  Google Scholar 

  • Harcourt, A. H., & Doherty, D. A. (2005). Species–area relationships of primates in tropical forest fragments: A global analysis. Journal of Applied Ecology, 42, 630–637.

    Article  Google Scholar 

  • Harcourt, A. H., Coppeto, S. A., & Parks, S. A. (2005). The distribution–abundance (density) relationship: Its form and causes in a tropical mammal order, primates. Journal of Biogeography, 32, 565–579.

    Article  Google Scholar 

  • Harper, G. J., Steininger, M. K., Tucker, C. J., Juhn, D., & Hawkins, F. (2007). Fifty years of deforestation and forest fragmentation in Madagascar. Environmental Conservation, 34, 1–9.

    Article  Google Scholar 

  • Hockings, K. J., & McLennan, M. R. (2012). From forest to farm: Systematic review of cultivar feeding by chimpanzees: Management implications for wildlife in anthropogenic landscapes. PLoS ONE, 7, e33391.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingram, J. C., & Dawson, T. P. (2006). Forest cover, condition, and ecology in human-impacted forests, south-eastern Madagascar. Conservation and Society, 4, 194–230.

    Google Scholar 

  • Irwin, M. T., Wright, P. C., Birkinshaw, C., Fisher, B. L., Gardner, C. J., et al. (2010). Patterns of species change in anthropogenically disturbed forests of Madagascar. Biological Conservation, 143, 2351–2362.

    Article  Google Scholar 

  • Isaac, N. J., & Cowlishaw, G. (2004). How species respond to multiple extinction threats. Proceedings of the Royal Society of London B: Biological Sciences, 271, 1135–1141.

    Article  Google Scholar 

  • Isabirye-Basuta, G. M., & Lwanga, J. S. (2008). Primate populations and their interactions with changing habitats. International Journal of Primatology, 29, 35–48.

    Article  Google Scholar 

  • Jernvall, J., & Wright, P. C. (1998). Diversity components of impending primate extinctions. Proceedings of the National Academy of Sciences of the United States of America, 95, 11279–11283.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamilar, J. M., & Paciulli, L. M. (2008). Examining the extinction risk of specialized folivores: A comparative study of colobine monkeys. American Journal of Primatology, 70, 816–827.

    Article  PubMed  Google Scholar 

  • Lake, J. C., & Leishman, M. R. (2004). Invasion success of exotic plants in natural ecosystems: The role of disturbance, plant attributes and freedom from herbivores. Biological Conservation, 117, 215–226.

    Article  Google Scholar 

  • Laurance, W. F., Nascimento, H. E. M., Laurance, S. G., Andrade, A., Fearnside, P. M., et al. (2006). Rain forest fragmentation and the proliferation of successional trees. Ecology, 87, 469–482.

    Article  PubMed  Google Scholar 

  • Laurance, W. F., Nascimento, H. E. M., Laurance, S. G., Andrade, A., Ewers, R. M., et al. (2007). Habitat fragmentation, variable edge effects, and the landscape-divergence hypothesis. PLoS ONE, 2, e1017.

    Article  PubMed  PubMed Central  Google Scholar 

  • Laurance, W. F., Goosem, M., & Laurance, S. G. (2009). Impacts of roads and linear clearings on tropical forests. Trends in Ecology & Evolution, 24, 659–669.

    Article  Google Scholar 

  • Laurance, W. F., Camargo, J. L., Luizão, R. C., Laurance, S. G., Pimm, S. L., et al. (2011). The fate of Amazonian forest fragments: A 32-year investigation. Biological Conservation, 144, 56–67.

    Article  Google Scholar 

  • Lee, P. C. (2003). Innovation as a behavioural response to environmental challenges: A cost and benefit approach. In S. M. Reader (Ed.), Animal innovation (pp. 261–276). Oxford: Oxford University Press.

    Chapter  Google Scholar 

  • Lee, P. C., & Hauser, M. D. (1998). Long-term consequences of changes in territory quality on feeding and reproductive strategies of vervet monkeys. Journal of Animal Ecology, 67, 347–358.

    Article  Google Scholar 

  • Lehman, S. M., Rajaonson, A., & Day, S. (2006). Edge effects and their influence on lemur density and distribution in southeast Madagascar. American Journal of Physical Anthropology, 129, 232–241.

    Article  PubMed  Google Scholar 

  • Marsh, L. K. (2003). Primates in fragments: Ecology and conservation. New York: Kluwer Academic/Plenum Publishers.

    Book  Google Scholar 

  • Marsh, C., Link, A., King-Bailey, G., & Donati, G. (2016). Effects of fragment and vegetation structure on the population abundance of Ateles hybridus, Alouatta seniculus and Cebus albifrons in Magdalena Valley, Colombia. Folia Primatologica, 87, 17–30.

    Article  Google Scholar 

  • Martinez, B. (2008). Occurrence of bamboo lemurs, Hapalemur griseus occidentalis, in an agricultural landscape on the Masoala peninsula. Lemur News, 13, 11–14.

    Google Scholar 

  • McLennan, M. R., & Hockings, K. J. (2014). Wild chimpanzees show group differences in selection of agricultural crops. Scientific Reports, 4, 5956.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nowak, K. (2008). Frequent water drinking by Zanzibar red colobus (Procolobus kirkii) in a mangrove forest refuge. American Journal of Primatology, 70, 1081–1092.

    Article  PubMed  Google Scholar 

  • Nowak, K. (2013). Mangrove and peat swamp forests: Refuge habitats for primates and felids. Folia Primatologica, 83, 361–376.

    Article  Google Scholar 

  • Nowak, K., & Lee, P. C. (2013). “Specialist” primates can be flexible in response to habitat alteration. In L. K. Marsh & C. A. Chapman (Eds.), Primates in fragments: Complexity and resilience (pp. 199–211). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media.

    Google Scholar 

  • Oates, J. F. (1996). Habitat alteration, hunting and the conservation of folivorous primates in African forests. Australian Journal of Ecology, 21, 1–9.

    Article  Google Scholar 

  • Oates, J. F. (2013). Primate conservation: Unmet challenges and the role of the International Primatological Society. International Journal of Primatology, 34, 235–245.

    Article  Google Scholar 

  • Onderdonk, D. A., & Chapman, C. A. (2000). Coping with forest fragmentation: The primates of Kibale National Park, Uganda. International Journal of Primatology, 21, 587–611.

    Article  Google Scholar 

  • Overdorff, D. J. (1993). Similarities, differences, and seasonal patterns in the diets of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park, Madagascar. International Journal of Primatology, 14, 721–753.

    Article  Google Scholar 

  • Plumptre, A. J., & Reynolds, V. (1994). The effect of selective logging on the primate populations in the Budongo Forest Reserve, Uganda. Journal of Applied Ecology, 31, 631–641.

    Article  Google Scholar 

  • Poorter, L. (1999). Growth responses of 15 rain-forest tree species to a light gradient: The relative importance of morphological and physiological traits. Functional Ecology, 13, 396–410.

    Article  Google Scholar 

  • Quinten, M. C., Waltert, M., Syamsuri, F., & Hodges, J. K. (2010). Peat swamp forest supports high primate densities on Siberut Island, Sumatra, Indonesia. Oryx, 44, 147–151.

    Article  Google Scholar 

  • Rabenantoandro, J., Randriatafika, F., & Lowry, P. P. (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 in southeastern Madagascar, Tolagnaro (Fort Dauphin) (pp. 65–77). Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Ramanamanjato, J.-B., Mcintyre, P. B., & Nussbaum, R. A. (2002). Reptile, amphibian, and lemur diversity of the Malahelo Forest, a biogeographical transition zone in southeastern Madagascar. Biodiversity and Conservation, 11, 1791–1807.

    Article  Google Scholar 

  • Razafindratsima, O. H., & Dunham, A. E. (2014). Assessing the impacts of nonrandom seed dispersal by multiple frugivore partners on plant recruitment. Ecology, 96, 24–30.

    Article  Google Scholar 

  • R Development Core Team (2015). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org

  • Riley, E. P. (2007). Flexibility in diet and activity patterns of Macaca tonkeana in response to anthropogenic habitat alteration. International Journal of Primatology, 28, 107–133.

    Article  Google Scholar 

  • Rode, K. D., Chapman, C. A., McDowell, L. R., & Stickler, C. (2006). Nutritional correlates of population density across habitats and logging intensities in redtail monkeys (Cercopithecus ascanius). Biotropica, 38, 625–634.

    Article  Google Scholar 

  • Sala, O. E., Chapin, F. S., III, Armesto, J. J., Berlow, E., Bloomfield, J., et al. (2000). Global biodiversity scenarios for the year 2100. Science, 287, 1770–1774.

    Article  CAS  PubMed  Google Scholar 

  • Sato, H., Santini, L., Patel, E. R., Campera, M., Yamashita, N., et al. (2016). Dietary flexibility and feeding strategies of Eulemur: A comparison with Propithecus. International Journal of Primatology, 37, 109–129.

    Article  Google Scholar 

  • 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. The Journal of Privacy and Confidentiality, 22, 79–87.

    Google Scholar 

  • Simmen, B., Bayart, F., Marez, A., & Hladik, A. (2007). Diet, nutritional ecology, and birth season of Eulemur macaco in an anthropogenic forest in Madagascar. International Journal of Primatology, 28, 1253–1266.

    Article  Google Scholar 

  • Singmann, H. (2014). afex: Analysis of factorial experiments. R package (version 0.9-109).

  • Sussman, R. W. (1977). Feeding behaviour of Lemur catta and Lemur fulvus. In T. H. Clutton-Brock (Ed.), Primate ecology: Studies of feeding and ranging behaviour in lemurs, monkeys, and apes (pp. 1–36). New York: Academic Press.

    Google Scholar 

  • Tan, C. L. (1999). Group composition, home range size, and diet of three sympatric bamboo lemur species (genus Hapalemur) in Ranomafana National Park, Madagascar. International Journal of Primatology, 20, 547–566.

    Article  Google Scholar 

  • Tutin, C. E. G., Ham, R. M., White, L. J. T., & Harrison, M. J. S. (1997a). The primate community of the Lopé Reserve, Gabon: Diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology, 42, 1–24.

    Article  CAS  PubMed  Google Scholar 

  • Tutin, C. E. G., White, L. J. T., & Mackanga-Missandzou, A. (1997b). The use by rain forest mammals of natural forest fragments in an equatorial African savanna. Conservation Biology, 11, 1190–1203.

    Article  Google Scholar 

  • Vincelette, M., Rabenantoandro, J., Randrihasipara, L., Randriatafika, F., & Ganzhorn, J. U. (2007a). Results from ten years of restoration experiments in the southeastern littoral forests of Madagascar. In J. U. Ganzhorn, S. M. Goodman, & M. Vincelette (Eds.), Biodiversity, ecology, and conservation of the littoral ecosystems in southeastern Madagascar, Tolagnaro (Fort Dauphin) (pp. 337–354). Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Vincelette, M., Théberge, M., & Randrihasipara, L. (2007b). Evaluations of forest cover at regional and local levels in the Tolagnaro region since 1950. In J. U. Ganzhorn, S. M. Goodman, & M. Vincelette (Eds.), Biodiversity, ecology, and conservation of the littoral ecosystems in southeastern Madagascar, Tolagnaro (Fort Dauphin) (pp. 49–58). Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Waeber, P. O., Wilmé, L., Ramamonjisoa, B., Garcia, C., Rakotomalala, D., et al. (2015). Dry forests in Madagascar: Neglected and under pressure. International Forestry Review, 17, 127–148.

    Article  Google Scholar 

  • Wasserman, M. D., & Chapman, C. A. (2003). Determinants of colobine monkey abundance: the importance of food energy, protein and fibre content. Journal of Animal Ecology, 72, 650–659.

    Article  Google Scholar 

  • Wieczkowski, J. A. (2003). Aspects of the ecological flexibility of the Tana River mangabey (Cercocebus galeritus) in its fragmented habitat, Tana River, Kenya. Ph.D. dissertation, University of Georgia.

  • Worton, B. J. (1989). Kernel methods for estimating the utilization distribution in home-range studies. Ecology, 70, 164–168.

    Article  Google Scholar 

  • Wright, P. C. (1999). Lemur traits and Madagascar ecology: Coping with an island environment. American Journal of Physical Anthropology, 110, 31–72.

    Article  Google Scholar 

  • Wright, P. C., Johnson, S. E., Irwin, M. T., Jacobs, R., Schlichting, P., et al. (2008). The crisis of the critically endangered greater bamboo lemur (Prolemur simus). Primate Conservation, 23, 5–17.

    Article  Google Scholar 

  • Zárate, D. A., Andresen, E., Estrada, A., & Seri-Silva, J. C. (2014). Black howler monkey (Alouatta pigra) activity, foraging and seed dispersal patterns in shaded cocoa plantations versus rainforest in southern Mexico. American Journal of Primatology, 76, 890–899.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Direction du Système des Aires Protégées, the Ministère de l’Environnement et Forêts of Madagascar, and the Mandena Management Committee (COGEMA) for permission to conduct research. We also thank the QMM Rio Tinto Environmental Team for their assistance and provision of logistical support on site and acknowledge their helpful staff, especially Manon Vincelette, Laza Andriamandimbiarisoa, David Rabehevitra, Christophe Rambolamanana, and Claude Soanary. Thanks to Shauna Mora for assistance with the GIS analysis. T. M. Eppley is grateful to Jacques Rakotondranary and Tolona Andrianasolo for obtaining research permits, and to Robertin Ravelomanantsoa, Katie Hall, and Natalie Breden for assistance in the field. T. M. Eppley also thanks the following organizations for their generous financial and in-kind support: American Society of Primatologists, Conservation International Primate Action Fund, Idea Wild, Mohamed bin Zayed Species Conservation Fund (Project Number: 11253008), Primate Conservation Inc., and the Primate Society of Great Britain/Knowsley Safari Park. M. Campera and M. Balestri thank Aristide Andrianarimisa, Germain, and Crescent for their assistance in the field. M. Campera and M. Balestri were supported by the Rufford Small Grant Foundation, and thank the Madagascar Institute for the Conservation of Tropical Environments (MICET). Many thanks to the guest editors, Matt McLennan, Noemi Spagnoletti, and Kim Hockings for the invitation to contribute to this special issue, and to Joanna Setchell and two anonymous reviewers for helpful comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Timothy M. Eppley.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest and no competing financial interests.

Additional information

Handling Editor: Noemi Spagnoletti

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eppley, T.M., Balestri, M., Campera, M. et al. Ecological Flexibility as Measured by the Use of Pioneer and Exotic Plants by Two Lemurids: Eulemur collaris and Hapalemur meridionalis . Int J Primatol 38, 338–357 (2017). https://doi.org/10.1007/s10764-016-9943-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-016-9943-8

Keywords

Navigation