Skip to main content
SpringerLink
Log in

Flextime: Black-and-White Ruffed Lemurs (Varecia variegata) use Opposing Strategies to Counter Resource Scarcity in Fragmented Habitats

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

Abstract

Forest fragmentation may lead to substantial declines in food availability for primary consumers, especially presenting a challenge for frugivores, such as the Critically Endangered black-and-white ruffed lemur (Varecia variegata). We investigated how forest fragmentation impacts the diet and activity budgets of V. variegata across three forest fragments—71 ha, 232 ha, and 597 ha—in Kianjavato, Madagascar. We collected phenological and lemur behavioural data over 17 months. We found that in both small fragments (< 500 ha), there was lower tree basal area, tree species diversity, and availability of fruit from large tree species compared to the largest fragment. Despite overall lower fruit availability, we found that individuals in the smallest forest maintained a high degree of frugivory year-round but had high measures of dietary diversity. In contrast, individuals in the other small-fragment consumed large proportions of flowers seasonally and showed low dietary diversity. These individuals consumed nectar from the traveller’s tree (Ravenala sp.) for more than 40% of the annual diet—much higher than the 3–5% reported for continuous forest populations. In both smaller fragments, individuals rested less and fed more than in the largest forest (i.e., energy-maximizing strategies). These results suggest that highly frugivorous lemurs have the flexibility to employ starkly contrasting strategies in response to reduced food availability and habitat quality, even within the same network of forests.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Altmann, J. (1974). Observational study of behaviour: Sampling methods. Behaviour, 49(3/4), 227–267.

    Article  CAS  PubMed  Google Scholar 

  • Ancrenaz, M., Oram, F., Nardiyono, N., Silmi, M., Jopony, M. E. M., Voigt, M., … Meijaard, E. (2021). Importance of small forest fragments in agricultural landscapes for maintaining orangutan metapopulations. Frontiers in Forests and Global Change, 4, 560944. https://doi.org/10.3389/ffgc.2021.560944

  • 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. New York, State University of New York at Stony Brook.

  • Arroyo-Rodríguez, V., & Dias, P. A. D. (2010). Effects of habitat fragmentation and disturbance on howler monkeys: A review. American Journal of Primatology, 72(1), 1–16. https://doi.org/10.1002/ajp.20753

    Article  PubMed  Google Scholar 

  • Asensio, N., Cristobal-Azkarate, J., Dias, P. A. D., Vea, J. J., & Rodríguez-Luna, E. (2007). Foraging habits of Alouatta palliata mexicana in three forest fragments. Folia Primatologica, 78(3), 141–153. https://doi.org/10.1159/000099136

    Article  Google Scholar 

  • Aureli, F., Schaffner, C. M., Boesch, C., Bearder, S. K., Call, J., Chapman, C. A., ... & van Schaik, C. P. (2008). Fission-fusion dynamics new research frameworks. Current Anthropology, 49(4), 627–654. https://doi.org/10.1086/586708

  • Baden, A. L., Webster, T. H., & Kamilar, J. M. (2016). Resource seasonality and reproduction predict fission–fusion dynamics in black-and-white ruffed lemurs (Varecia variegata). American Journal of Primatology, 78, 256–279. https://doi.org/10.1002/ajp.22507

    Article  PubMed  Google Scholar 

  • Balko, E. A. (1993). A Behaviorally Plastic Response to Forest Composition and Logging Disturbance by Varecia variegata variegata in Ranomafana National Park, Madagascar. Ph.D. dissertation. New York, State University of New York College of Environmental Science and Forestry.

  • Balko, E. A., & Underwood, H. B. (2005). Effects of forest structure and composition on food availability for Varecia variegata at Ranomafana National Park, Madagascar. American Journal of Primatology, 66(1), 45–70. https://doi.org/10.1002/ajp.20127

    Article  PubMed  Google Scholar 

  • Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1–48. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  • Beeby, N., & Baden, A. L. (2021). Seasonal variability in the diet and feeding ecology of black-and-white ruffed lemurs (Varecia variegata) in Ranomafana National Park, southeastern Madagascar. American Journal of Physical Anthropology, 174(4), 763–775. https://doi.org/10.1002/ajpa.24230

    Article  PubMed  Google Scholar 

  • Bolt, L. M., Schreier, A. L., Voss, K. A., Sheehan, E. A., Barrickman, N. L., Pryor, N. P., & Barton, M. C. (2018). The influence of anthropogenic edge effects on primate populations and their habitat in a fragmented rainforest in Costa Rica. Primates, 59(3), 301–311. https://doi.org/10.1007/s10329-018-0652-0

    Article  PubMed  Google Scholar 

  • Boyle, S. A., & Smith, A. T. (2010a). Behavioral modifications in northern bearded saki monkeys (Chiropotes satanas chiropotes) in forest fragments of central Amazonia. Primates, 51(1), 43–51. https://doi.org/10.1007/s10329-009-0169-7

    Article  PubMed  Google Scholar 

  • Boyle, S. A., & Smith, A. T. (2010b). Can landscape and species characteristics predict primate presence in forest fragments in the Brazilian Amazon? Biological Conservation, 143(5), 1134–1143. https://doi.org/10.1016/j.biocon.2010.02.008

    Article  Google Scholar 

  • Boyle, S. A., Zartman, C. E., Spironello, W. R., & Smith, A. T. (2012). Implications of habitat fragmentation on the diet of bearded saki monkeys in central Amazonian forest. Journal of Mammalogy, 93(4), 959–976. https://doi.org/10.1644/11-mamm-a-286.1

    Article  Google Scholar 

  • Bracebridge, C. E., Davenport, T. R., & Marsden, S. J. (2018). The impact of forest disturbance on the seasonal foraging ecology of a critically endangered African primate. Biotropica, 44(4), 560–568.

    Article  Google Scholar 

  • Britt, A. (2000). Diet and feeding behaviour of the black-and-white ruffed lemur (Varecia variegata variegata) in the Betampona Reserve, Eastern Madagascar. Folia Primatologica, 71(3), 133–141. https://doi.org/10.1159/000021741

    Article  CAS  Google Scholar 

  • Brooks, M. E., Kristensen, K., van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A. … Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal, 9(2), 378–400. https://journal.r-project.org/archive/2017/RJ-2017-066/index.html

  • Calley, M., Braithwaite, R. W., & Ladd, P. G. (1993). Reproductive biology of Ravenala madagascariensis Gmel. as an alien species. Biotropica, 25(1), 61. https://doi.org/10.2307/2388979

  • Campera, M., Serra, V., Balestri, M., Barresi, M., Ravaolahy, M., Randriatafika, F., & Donati, G. (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. https://doi.org/10.1007/s10764-014-9780-6

    Article  Google Scholar 

  • Chapman, C. (1988). Patch use and patch depletion by the spider and howling monkeys of Santa Rosa National Park, Costa Rica. Behaviour, 105(1/2), 99–116.

    Article  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Wrangham, R., Hunt, K., Gebo, D., & Gardner, L. (1992). Estimators of fruit abundance of tropical trees. Biotropica, 24(4), 527–531.

    Article  Google Scholar 

  • Chapman, C. A., Rothman, J. M., & Lambert, J. E. (2012). Food as a selective force in primates. In J. Call, P. M. Kappeler, J. B. Silk, J. C. Mitani, & R. A. Palombit (Eds.), The Evolution of Primate Societies (pp. 149–168). The University of Chicago Press.

    Google Scholar 

  • Chaves, Ó. M., Stoner, K. E., & Arroyo-rodríguez, V. (2012). Differences in diet between spider monkey groups living in forest fragments and continuous forest in Mexico. Biotropica, 44(1), 105–113.

    Article  Google Scholar 

  • Chen, K.S., Li, J.Q., Rasoarahona, J., Folega F., & Manjaribe, C. (2016). Diet and effects of Sanford's brown lemur (Eulemur sanfordi, Archbold 1932) gut-passage on the germination of plant species in Amber forest, Madagascar. Zoological Studies, 55, e21. https://doi.org/10.6620/ZS.2016.55-21

  • Dehgan, A. (2003). The Behaviour of Extinction: Predicting the Incidence and Local Extinction of Lemurs in Fragmented Habitats of Southeastern Madagascar. Ph.D. dissertation. Chicago: University of Chicago.

  • Donati, G., Kesch, K., Ndremifidy, K., Schmidt, S. L., Ramanamanjato, J. B., Borgognini-Tarli, S. M., & Ganzhorn, J. U. (2011). Better few than hungry: Flexible feeding ecology of collared lemurs Eulemur collaris in littoral forest fragments. PLoS ONE, 6(5), 1–10. https://doi.org/10.1371/journal.pone.0019807

    Article  CAS  Google Scholar 

  • Dunham, N. T. (2017). Feeding ecology and dietary flexibility of Colobus angolensis palliatus in relation to habitat disturbance. International Journal of Primatology, 38(3), 553–571. https://doi.org/10.1007/s10764-017-9965-x

    Article  Google Scholar 

  • Dunn, J. C., Cristóbal-Azkarate, J., & Veà, J. J. (2009). Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa. American Journal of Primatology, 71(8), 654–662. https://doi.org/10.1002/ajp.20700

    Article  PubMed  Google Scholar 

  • Dunn, J. C., Cristóbal-Azkarate, J., & Veà, J. J. (2010). Seasonal variations in the diet and feeding effort of two groups of howlers in different sized forest fragments. International Journal of Primatology, 31(5), 887–903. https://doi.org/10.1007/s10764-010-9436-0

    Article  Google Scholar 

  • Edwards, M. S., & Ullrey, D. E. (1999). Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. II. Hindgut- and foregut-fermenting folivores. Zoo Biology, 18(6), 537–549. https://doi.org/10.1002/(SICI)1098-2361(1999)18:6%3C537::AID-ZOO8%3E3.0.CO;2-F

  • Esri Inc. (2022). ArcGIS Pro (Version 3.0.3). Esri Inc.  https://www.esri.com/en-us/arcgis/products/arcgis-pro/overview. Accessed May 2022.

  • Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., Fiore, A. … Li, B. (2017). Impending extinction crisis of the world’s primates: Why primates matter. Science Advances, 3(1), 1–16. https://doi.org/10.1126/sciadv.1600946

  • FAO. (2020). Global forest resources assessment 2020 – Key findings. Rome, Italy. https://doi.org/10.4060/ca8753en

  • Ferrari, S. F., & Strier, K. B. (1992). Exploitation of Mabea fistulifera nectar by marmosets (Callithrix flaviceps) and muriquis (Brachyteles arachnoides) in South-East Brazil. Journal of Tropical Ecology, 8(3), 225–239.

    Article  Google Scholar 

  • Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: New 1km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12), 4302–4315.

    Article  Google Scholar 

  • Fox, J., & Weisberg, S. (2019). An R Companion to applied regression, Third Edition. Sage Publications.

  • Freeland, W. J., & Janzen, D. H. (1974). Strategies in herbivory by mammals: The role of plant secondary compounds. The American Naturalist, 108(961), 269–289. https://doi.org/10.1086/282907

    Article  CAS  Google Scholar 

  • Gabriel, D. N. (2013). Habitat use and activity patterns as an indication of fragment quality in a strepsirrhine primate. International Journal of Primatology, 34(2), 388–406. https://doi.org/10.1007/s10764-013-9668-x

    Article  Google Scholar 

  • Garber, P. A. (1988). Foraging decisions during nectar feeding by tamarin monkeys (Saguinus mystax and Saguinus fuscicollis, Callitrichidae, Primates) in Amazonian Peru. Biotropica, 20(2), 100–106. https://doi.org/10.2307/2388181

    Article  Google Scholar 

  • Gould, L., & Gabriel, D. N. (2015). Wet and dry season diets of the Endangered Lemur catta (ring-tailed lemur) in two mountainous rocky outcrop forest fragments in south-central Madagascar. African Journal of Ecology, 53(3), 320–330. https://doi.org/10.1111/aje.12186

    Article  Google Scholar 

  • Haddad, N. M., Brudvig, L. A., Clobert, J., Davies, K. F., Gonzalez, A., Holt, R. D., ... & Townshend, J. R. (2015). Habitat fragmentation and its lasting impact on Earth’s ecosystems. Science Advances, 1(2), 1–9. https://doi.org/10.1126/sciadv.1500052

  • Harris, I., Osborn, T. J., Jones, P. D., & Lister, D. H. (2020). Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Scientific Data, 7, 109.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hartig, F., & Lohse, L. (2022). DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.5. https://cran.r-project.org/web/packages/DHARMa/vignettes/DHARMa.html

  • Heymann, E. W. (2011). Florivory, nectarivory, and pollination – A review of primate-flower interactions. Ecotropica, 17, 41–52.

    Google Scholar 

  • Hogan, J. D., Melin, A. D., Mosdossy, K. N., & Fedigan, L. M. (2016). Seasonal importance of flowers to Costa Rican capuchins (Cebus capucinus imitator): Implications for plant and primate. American Journal of Physical Anthropology, 161(4), 591–602. https://doi.org/10.1002/ajpa.23059

    Article  PubMed  Google Scholar 

  • Holmes, S. M. (2012). Habitat Use and population Genetics of the Black-and-White Ruffed Lemur (Varecia variegata) in a Fragmented Landscape in southeastern Madagascar. M.A. thesis. Calgary: University of Calgary.

  • Holmes, S. M., Gordon, A. D., Louis, E. E., & Johnson, S. E. (2016). Fission-fusion dynamics in black-and-white ruffed lemurs may facilitate both feeding strategies and communal care of infants in a spatially and temporally variable environment. Behavioral Ecology and Sociobiology, 70(11), 1949–1960. https://doi.org/10.1007/s00265-016-2201-4

    Article  Google Scholar 

  • Holmes, S. M. (2017). Sharing Space: Habitat Use and Spatial Relationships of Frugivorous Lemurs in Fragmented Forests. Ph.D. dissertation. Calgary: University of Calgary.

  • Huang, Z. P., Scott, M. B., Li, Y. P., Ren, G. P., Xiang, Z. F., Cui, L. W., & Xiao, W. (2017). Black-and-white snub-nosed monkey (Rhinopithecus bieti) feeding behavior in a degraded forest fragment: Clues to a stressed population. Primates, 58(4), 517–524. https://doi.org/10.1007/s10329-017-0618-7

    Article  PubMed  Google Scholar 

  • Irwin, M. T. (2008). Feeding ecology of Propithecus diadema in forest fragments and continuous forest. International Journal of Primatology, 29(1), 95–115. https://doi.org/10.1007/s10764-007-9222-9

    Article  Google Scholar 

  • Irwin, M. T., Wright, P. C., Birkinshaw, C., Fisher, B. L., Gardner, C. J., Glos, J., … Ganzhorn, J. U. (2010). Patterns of species change in anthropogenically disturbed forests of Madagascar. Biological Conservation, 143(10), 2351–2362. https://doi.org/10.1016/j.biocon.2010.01.023

  • Irwin, M. T., Raharison, J. L., Raubenheimer, D. R., Chapman, C. A., & Rothman, J. M. (2015). The nutritional geometry of resource scarcity: Effects of lean seasons and habitat disturbance on nutrient intakes and balancing in wild sifakas. PLoS ONE, 10(6). https://doi.org/10.1371/journal.pone.0128046

  • Irwin, M. T., Samonds, K. E., Raharison, J.-L., Junge, R. E., Mahefarisoa, K. L., Rasambainarivo, F., … Glander, K. E. (2019). Morphometric signals of population decline in diademed sifakas occupying degraded rainforest habitat in Madagascar. Scientific Reports, 9(1), 8776. https://doi.org/10.1038/s41598-019-45426-2

  • Johns, A. D. (1986). Effects of selective logging on the behavioral ecology of West Malaysian primates. Ecology, 67(3), 684–694. https://doi.org/10.2307/1937692

    Article  Google Scholar 

  • Kress, W. J. (1993). Coevolution of plants and animals: Pollination of flowers by primates in Madagascar. Current Science, 65(3), 253–257.

    Google Scholar 

  • Kress, W. J., Schatz, G. E., Andrianifahanana, M., & Morland, H. S. (1994). Pollination of Ravenala madagascariensis (Strelitziaceae) by lemurs in Madagascar: Evidence for an archaic coevolutionary system? American Journal of Botany, 81(5), 542–551.

    Article  Google Scholar 

  • Lambert, J. E., & Rothman, J. M. (2015). Fallback foods, optimal diets, and nutritional targets: Primate responses to varying food availability and quality. Annual Review of Anthropology, 44(1), 493–512. https://doi.org/10.1146/annurev-anthro-102313-025928

    Article  Google Scholar 

  • Laurance, W. F., Ferreira, L. V., Merona, J. M. R., & Laurance, S. G. (1998). Rain forest fragmentation and the dynamics of Amazonian tree communities. Ecology, 79(6), 2032–2040. https://doi.org/10.1890/0012-9658(1998)079[2032:RFFATD]2.0.CO;2

    Article  Google Scholar 

  • Laurance, W. F., Delamonica, P., Laurance, S. G., Vasconcelos, H. L., & Lovejoy, T. E. (2000). Rainforest fragmentation kills big trees. Nature, 404(6780), 836. https://doi.org/10.1038/35009032

    Article  CAS  PubMed  Google Scholar 

  • Laurance, W. F., Nascimento, H. E. M., Laurance, S. G., Andrade, A. C., Fearnside, P. M., Ribeiro, J. E. L., & Capretz, R. L. (2006). Rain forest fragmentation and the proliferation of successional trees. Ecology, 87(2), 469–482. https://doi.org/10.1890/05-0064

    Article  PubMed  Google Scholar 

  • Laurance, W. F., Sayer, J., & Cassman, K. G. (2014). Agricultural expansion and its impacts on tropical nature. Trends in Ecology & Evolution, 29(2), 107–116. https://doi.org/10.1016/j.tree.2013.12.001

    Article  Google Scholar 

  • Lenth, R. V., Buerkner, P., Herve, M., Love, J., Miguez, F., Riebl, H., & Singmann, H. (2022). Emmeans: Estimated marginal means, aka least-squares means. R package version 1.7.3. https://cran.r-project.org/web/packages/emmeans/index.html

  • Lenz, B. B., Jack, K. M., & Spironello, W. R. (2014). Edge effects in the primate community of the biological dynamics of forest fragments project, Amazonas, Brazil. American Journal of Physical Anthropology, 155(3), 436–446. https://doi.org/10.1002/ajpa.22590

    Article  PubMed  Google Scholar 

  • Louis, E. E., Coles, M. S., Andriantompohavana, R., Sommer, J. A., Engberg, S. E., Zaonarivelo, J. R., … Brenneman, R. A. (2006). Revision of the mouse lemurs (Microcebus) of Eastern Madagascar. International Journal of Primatology, 27(2), 347–389. https://doi.org/10.1007/s10764-006-9036-1

  • Martínez-Mota, R., Valdespino, C., Sánchez-Ramos, M. A., & Serio-Silva, J. C. (2007). Effects of forest fragmentation on the physiological stress response of black howler monkeys. Animal Conservation, 10(3), 374–379. https://doi.org/10.1111/j.1469-1795.2007.00122.x

    Article  Google Scholar 

  • Marshall, A. J., & Wrangham, R. W. (2007). Evolutionary consequences of fallback foods. International Journal of Primatology, 28(6), 1219–1235. https://doi.org/10.1007/s10764-007-9218-5

    Article  Google Scholar 

  • Manjaribe, C., Frasier, C. L., Rakouth, B., & Louis, E. E. (2013). Ecological restoration and reforestation of fragmented forests in Kianjavato, Madagascar. International Journal of Ecology, 2013, 1–12. https://doi.org/10.1155/2013/726275

    Article  Google Scholar 

  • McLennan, M. R., Spagnoletti, N., & Hockings, K. J. (2017). The implications of primate behavioral flexibility for sustainable human–primate coexistence in anthropogenic habitats. International Journal of Primatology, 38(2), 105–121. https://doi.org/10.1007/s10764-017-9962-0

    Article  Google Scholar 

  • Mekonnen, A., Fashing, P. J., Bekele, A., Hernandez-Aguilar, R. A., Rueness, E. K., Nguyen, N., & Stenseth, N. C. (2017). Impacts of habitat loss and fragmentation on the activity budget, ranging ecology and habitat use of Bale monkeys (Chlorocebus djamdjamensis) in the southern Ethiopian Highlands. American Journal of Primatology, 79(7), 1–13. https://doi.org/10.1002/ajp.22644

    Article  Google Scholar 

  • Mekonnen, A., Fashing, P. J., Bekele, A., Hernandez-Aguilar, R. A., Rueness, E. K., & Stenseth, N. C. (2018). Dietary flexibility of Bale monkeys (Chlorocebus djamdjamensis) in southern Ethiopia: Effects of habitat degradation and life in fragments. BMC Ecology, 18(1), 4. https://doi.org/10.1186/s12898-018-0161-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Milich, K. M., Stumpf, R. M., Chambers, J. M., & Chapman, C. A. (2014). Female red colobus monkeys maintain their densities through flexible feeding strategies in logged forests in Kibale National Park, Uganda: Ideal distribution in primates. American Journal of Physical Anthropology, 154(1), 52–60. https://doi.org/10.1002/ajpa.22471

    Article  PubMed  Google Scholar 

  • Milton, K. (1993). Diet and primate evolution. Scientific American, 269(2), 86–93.

    Article  CAS  PubMed  Google Scholar 

  • Morland, H. S. (1991). Social Organization and Ecology of Black and White Ruffed Lemurs (Varecia variegata variegata) in Lowland Rain Forest, Nosy Mangabe, Madagascar. Ph.D. dissertation. Connecticut: Yale University.

  • Murcia, C. (1995). Edge effects in fragmented forests: Implications for conservation. Trends in Ecology & Evolution, 10(2), 58–62. https://doi.org/10.1016/S0169-5347(00)88977-6

    Article  CAS  Google Scholar 

  • Ortiz-Burgos, S. (2015). Shannon-Weaver diversity index. In M. J. Kennish (Ed.), Encyclopedia of Estuaries (pp. 572–573). Springer Publishing.

    Google Scholar 

  • Petersen, M.A. (2022). Behavioural Responses to Habitat Fragmentation in the Frugivorous Black-and-White Ruffed Lemur (Varecia variegata): Implications for the Conservation of a Critically Endangered Species. MA Thesis. Calgary: University of Calgary.

  • Ratsimbazafy, J. H. (2002). On the Brink of Extinction and the Process of Recovery: Responses of Black -and -White Ruffed Lemurs (Varecia variegata variegata) to Disturbance in Manombo Forest, Madagascar. Ph.D. dissertation. New York, State University of New York at Stony Brook.

  • Ratsimbazafy, J. (2006). Diet composition, foraging, and feeding behaviour in relation to habitat disturbance: Implications for the adaptability of ruffed lemurs (Varecia v. editorium) in Manombo Forest, Madagascar. In L. Gould & M. L. Sauther (Eds.) Lemurs: Ecology and Adaptation (pp. 403–422). Springer US.

  • Riba-Hernández, P., & Stoner, K. E. (2005). Massive destruction of Symphonia globulifera (Clusiaceae) flowers by Central American spider monkeys (Ateles geoffroyi). Biotropica, 37(2), 274–278. https://doi.org/10.1111/j.1744-7429.2005.00037.x

    Article  Google Scholar 

  • Riley, E. P. (2007). Flexibility in diet and activity patterns of Macaca tonkeana in response to anthropogenic habitat alteration. International Journal of Primatology, 28(1), 107–133. https://doi.org/10.1007/s10764-006-9104-6

    Article  Google Scholar 

  • R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r-project.org/. Accessed May 2021.

  • RStudio Team. (2020). RStudio: Integrated development for R. RStudio, PBC. https://www.rstudio.com/. Accessed May 2021.

  • Salinas, H., & Ramirez-Delgado, D. (2021). ecolTest: Community ecology tests. R package version 0.0.1. https://cran.r-project.org/web/packages/ecolTest/index.html

  • Sawyer, R. M., Fenosoa, Z. S. E., Andrianarimisa, A., & Donati, G. (2017). The effect of habitat disturbance on the abundance of nocturnal lemur species on the Masoala Peninsula, northeastern Madagascar. Primates, 58(1), 187–197. https://doi.org/10.1007/s10329-016-0552-0

    Article  PubMed  Google Scholar 

  • Schoener, T. W. (1971). Theory of feeding strategies. Annual Review of Ecology & Systematics, 2, 369–404. https://doi.org/10.1146/annurev.es.02.110171.002101

    Article  Google Scholar 

  • Tabarelli, M., Aguiar, A. V., Girão, L. C., Peres, C. A., & Lopes, A. V. (2010). Effects of pioneer tree species hyperabundance on forest fragments in Northeastern Brazil. Conservation Biology, 24(6), 1654–1663. https://doi.org/10.1111/j.1523-1739.2010.01529.x

    Article  PubMed  Google Scholar 

  • The IUCN Red List of Threatened Species. (2021). from IUCN. Red List of Threatened Species website: https://www.iucnredlist.org/en. Accessed 28 Apr 2021.

  • Tutin, C. G. (1999). Fragmented living: Behavioural ecology of primates in a forest fragment in the Lope Reserve, Gabon. Primates, 40(1), 249–265.

    Article  CAS  PubMed  Google Scholar 

  • Westoby, M. (1978). What are the biological bases of varied diets? The American Naturalist, 112(985), 627–631. https://doi.org/10.1086/283303

    Article  Google Scholar 

  • White, F. J., Overdorff, D. J., Balko, E. A., & Wright, P. C. (1995). Distribution of ruffed lemurs (Varecia variegata) in Ranomafana National Park, Madagascar. Folia Primatologica, 64(3), 124–131. https://doi.org/10.1159/000156842

    Article  Google Scholar 

  • Wong, S. N. P., Saj, T. L., & Sicotte, P. (2006). Comparison of habitat quality and diet of Colobus vellerosus in forest fragments in Ghana. Primates, 47(4), 365–373. https://doi.org/10.1007/s10329-006-0186-8

    Article  PubMed  Google Scholar 

  • van Schaik, C. P. (2013). The costs and benefits of flexibility as an expression of behavioural plasticity: A primate perspective. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1618), 20120339. https://doi.org/10.1098/rstb.2012.0339

    Article  Google Scholar 

  • van Schaik, C. P., & Brockman, D. K. (2005). Seasonality in primate ecology, reproduction, and life history: An overview. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in Primates (pp. 3–20). Cambridge University Press. https://doi.org/10.1017/CBO9780511542343.002

  • Vasey, N. (2002). Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: II. Intraspecific patterns. American Journal of Physical Anthropology, 118, 169–183. https://doi.org/10.1002/ajpa.10054

    Article  PubMed  Google Scholar 

  • Vasey, N. (2005). Activity budgets and activity rhythms in red ruffed lemurs (Varecia rubra) on the Masoala Peninsula, Madagascar: Seasonality and reproductive energetics. American Journal of Primatology, 66, 23–44. https://doi.org/10.1002/ajp.20126

    Article  PubMed  Google Scholar 

  • Vieilledent, G., Grinand, C., Rakotomalala, F. A., Ranaivosoa, R., Rakotoarijaona, J.-R., Allnutt, T. F., & Achard, F. (2018). Combining global tree cover loss data with historical national forest cover maps to look at six decades of deforestation and forest fragmentation in Madagascar. Biological Conservation, 222, 189–197. https://doi.org/10.1016/j.biocon.2018.04.008

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the Natural Sciences and Engineering Research Council of Canada, the Calgary Zoological Society, and Sigma Xi. We thank Madagascar National Parks and the Kianjavato Commune for permission to conduct this research. We would also like to thank the guides with the Madagascar Biodiversity Partnership, Mbana Ferdinand, Razafiarisona Jean Clement, Zakamanana Michel Patric, Tsarandro Nomenjanahary Rafidison Benjamin, Rakotoson Emilys Edgarson, Marolahy Jean Piere, Rabearivelo Etienne, Ramanamihaja Prosper, and Rasolomampionona for collecting the data used in this study, and especially Razafindravelo Padou Cressant for coordinating the data collection and reporting. Furthermore, we would like to thank Nicola Guthrie for providing maps of the Kianjavato region and Jay Reid for assistance in processing weather data. Finally, we are grateful for the editors and two anonymous reviewers for their comments and suggestions to improve the manuscript.

Author information

Authors and Affiliations

  1. Department of Anthropology and Archaeology, University of Calgary, 2500 University Drive NW, Calgary, AB, T2N 1N4, Canada

    Melody A. Petersen & Steig E. Johnson

  2. Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural Sciences, Umeå, Sweden

    Sheila M. Holmes

  3. Department of Biochemistry, Molecular Biology, Entomology, and Plant Pathology, Mississippi State University, Starkville, MS, USA

    Li-Dunn Chen

  4. Faculty of Sciences, Technologies, and the Environment, University of Mahajanga, Mahajanga, Madagascar

    Patricia V. Ravoniarinalisoa

  5. IUCN Species Survival Commission Conservation Translocation Specialist Group, Calgary, AB, Canada

    Axel Moehrenschlager

  6. Department of Conservation Genetics, Omaha’s Henry Doorly Zoo and Aquarium, Omaha, NE, USA

    Edward E. Louis Jr.

Authors
  1. Melody A. Petersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sheila M. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Li-Dunn Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patricia V. Ravoniarinalisoa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Axel Moehrenschlager
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Edward E. Louis Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Steig E. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.M.H, E. E. L, and S.E.J designed the data collection protocol, and L.C and P.V.R contributed to data collection. M.A.P conceived the study, conducted the analyses and wrote the first draft of the manuscript. All authors contributed to subsequent drafts of the manuscript.

Corresponding author

Correspondence to Steig E. Johnson.

Ethics declarations

Inclusion and Diversity

The author list includes contributors from the location where the research was conducted, who participated in the data collection.

Additional information

Handling Editor: Joanna (Jo) M. Setchell

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Petersen, M.A., Holmes, S.M., Chen, LD. et al. Flextime: Black-and-White Ruffed Lemurs (Varecia variegata) use Opposing Strategies to Counter Resource Scarcity in Fragmented Habitats. Int J Primatol 44, 1200–1225 (2023). https://doi.org/10.1007/s10764-023-00397-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-023-00397-0

Keywords

Search

Navigation