Skip to main content

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 volume 70, pages 1949–1960 (2016)Cite this article

Abstract

Species with greater expression of fission-fusion dynamics show greater variability in the size, composition, and cohesion of subgroups over time. This may allow their adjustment to local environmental, social, and demographic conditions. We tested which environmental and social factors influenced subgroup size in one such species, the black-and-white ruffed lemur (Varecia variegata) at two sites within a fragmented forest landscape. Using instantaneous focal sampling at 15-min intervals, we collected data on subgroup size and composition, fruit and flower availability, and location. We also collected biweekly data on site-wide fruit and flower availability. We used these data to test the influence of season, food availability, reproduction, and predation risk on adult subgroup size in this species. Ruffed lemur adults consistently formed significantly larger subgroups in times of lower site-wide fruit availability, during the wet season, and when one or more infants were present. There were differences between sites in the relationship between subgroup size and tree size, fruit patch size, and site-wide flower availability. Variables measuring indirect predation risk showed no significant relationship with subgroup size. These results emphasize the strong relationship between fission-fusion dynamics and spatial and temporal variation in food availability, as well as the importance of sociality in a species with communal care of infants. Fission-fusion dynamics may serve as an evolutionary strategy to adapt to the unpredictable and sometimes harsh environmental conditions of Madagascar and may facilitate the persistence of communities of this critically endangered lemur despite widespread anthropogenic habitat modification.

Significance statement

Fission-fusion dynamics (the joining and separating of subgroups within a larger group of animals) may allow species to adjust social benefits to changing environmental conditions. This study examines the underlying ecological and social factors that might influence fission-fusion dynamics in black-and-white ruffed lemurs. Subgroup size in this species was strongly related to food availability, though not always in the direction expected. This suggests that the relationship between food availability and sociality changes when food availability reaches very low levels. Additionally, infant presence was linked to larger adult subgroups, indicating a connection between fission-fusion behavior and the cooperative rearing of offspring seen in this species. Relationships between subgroup size and some environmental variables differed between sites, emphasizing the flexibility of grouping patterns in this species and indicating that local conditions may play a large role in the expression of fission-fusion dynamics.

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

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3

References

  • Abdi H (2010) Holm’s sequential bonferroni procedure. In: Salkind N, Dougherty DM, Frey B (eds) Encyclopedia of research design. Sage Publications Inc., Thousand Oaks, CA, pp. 573–577

    Google Scholar 

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    Article  CAS  PubMed  Google Scholar 

  • Ansmann IC, Parra GJ, Chilvers BL, Lanyon JM (2012) Dolphins restructure social system after reduction of commercial fisheries. Anim Behav 84:575–581

    Article  Google Scholar 

  • Asensio N, Korstjens AH, Aureli F (2009) Fissioning minimizes ranging costs in spider monkeys: a multiple-level approach. Behav Ecol Sociobiol 63:649–659

    Article  Google Scholar 

  • Aureli F, Schaffner CM, Boesch C, et al. (2008) Fission-fusion dynamics new research frameworks. Curr Anthropol 49:627–654

    Article  Google Scholar 

  • Baden AL (2011) Communal infant care in black-and-white ruffed lemurs (Varecia variegata). PhD dissertation, Stony Brook University

  • Baden AL, Wright PC, Louis EE, Bradley BJ (2013) Communal nesting, kinship, and maternal success in a social primate. Behav Ecol Sociobiol 67:1939–1950

    Article  Google Scholar 

  • Baden AL, Webster TH, Kamilar JM (2016) Resource seasonality and reproduction predict fission-fusion dynamics in black-and-white ruffed lemurs (Varecia variegata). Am J Primatol 78:256–279

    Article  PubMed  Google Scholar 

  • Balko EA (1998) A behaviorally plastic response to forest composition and logging disturbance by Varecia variegata variegata in Ranomafana National Park, Madagascar. PhD dissertation, State University of New York College of Environmental Science and Forestry

  • Balko EA, Underwood HB (2005) Effects of forest structure and composition on food availability for Varecia variegata at Ranomafana National Park, Madagascar. Am J Primatol 66:45–70

    Article  PubMed  Google Scholar 

  • Bates LA, Byrne RW (2009) Sex differences in the movement patterns of free-ranging chimpanzees (Pan troglodytes schweinfurthii): foraging and border checking. Behav Ecol Sociobiol 64:247–255

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bercovitch FB, Berry PSM (2010) Ecological determinants of herd size in the Thornicroft’s giraffe of Zambia. Afr J Ecol 48:962–971

    Article  Google Scholar 

  • Body G, Weladji RB, Holand O, Nieminen M (2015) Fission-fusion group dynamics in reindeer reveal an increase of cohesiveness at the beginning of the peak rut. Acta Ethol 18:101–110

    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 Primatol 71:133–141

    Article  CAS  PubMed  Google Scholar 

  • Brouwer L, Richardson DS, Komdeur J (2012) Helpers at the nest improve late-life offspring performance: evidence from a long-term study and a cross-foster experiment. PLoS One 7:e33167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman CA, Chapman LJ, Wangham R, Hunt K, Gebo D, Gardner L (1992) Estimators of fruit abundance of tropical trees. Biotropica 24:527–531

    Article  Google Scholar 

  • Chapman CA, Wrangham RW, Chapman LJ (1995) Ecological constraints on group-size - an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70

    Article  Google Scholar 

  • Clutton-Brock TH, Russell AF, Sharpe LL, Brotherton PNM, McIlrath GM, White S, Cameron EZ (2001) Effects of helpers on juvenile development and survival in meerkats. Science 293:2446–2449

    Article  CAS  PubMed  Google Scholar 

  • Coles RC, Lee PC, Talebi M (2012) Fission-fusion dynamics in southern muriquis (Brachyteles arachnoides) in continuous Brazilian Atlantic Forest. Int J Primatol 33:93–114

    Article  Google Scholar 

  • Davies NB, Krebs JR, West SA (2012) An introduction to behavioural ecology, 4th edn. Wiley, Chichester, UK

    Google Scholar 

  • de Silva S, Ranjeewa ADG, Kryazhimskiy S (2011) The dynamics of social networks among female Asian elephants. BMC Ecol 11:17

    Article  PubMed  PubMed Central  Google Scholar 

  • Ebensperger LA, Rivera DS, Hayes LD (2012) Direct fitness of group living mammals varies with breeding strategy, climate and fitness estimates. J Anim Ecol 81:1013–1023

    Article  PubMed  Google Scholar 

  • Ebensperger LA, Villegas A, Abades S, Hayes LD (2014) Mean ecological conditions modulate the effects of group living and communal rearing on offspring production and survival. Behav Ecol 25:862–870

    Article  Google Scholar 

  • ESRI (2012) ArcGIS Desktop. http://www.esri.com/software/arcgis/arcgis-for-desktop

  • Fennessy J (2004) Ecology of the desert-dwelling giraffe (Giraffa camelopardalis angolensis) in Northwestern Namibia. PhD dissertation, University of Sidney

  • Fishlock V, Lee PC (2013) Forest elephants: fission-fusion and social arenas. Anim Behav 85:357–363

    Article  Google Scholar 

  • Fleischmann D, Kerth G (2014) Roosting behavior and group decision making in 2 syntopic bat species with fission-fusion societies. Behav Ecol 25:1240–1247

    Article  Google Scholar 

  • Fortin D, Fortin ME, Beyer HL, Duchesne T, Courant S, Dancose K (2009) Group-size-mediated habitat selection and group fusion-fission dynamics of bison under predation risk. Ecology 90:2480–2490

    Article  PubMed  Google Scholar 

  • Foster EA, Franks DW, Morrell LJ, Balcomb KC, Parsons KM, van Ginneken A, Croft DP (2012) Social network correlates of food availability in an endangered population of killer whales, Orcinus orca. Anim Behav 83:731–736

    Article  Google Scholar 

  • Ganzhorn JU (1989) Niche separation of 7 lemur species in the eastern rainforest of Madagascar. Oecologia 79:279–286

    Article  Google Scholar 

  • Gerber BD (2010) Madagascar GIS: spatial information to aid research and conservation. http://filebox.vt.edu/users/bgerber/services.htm. Accessed March 5, 2012

  • Google Inc (2009) Google Earth. https://www.google.ca/earth/download/ge/agree.html

  • Harper G, Steininger MK, Tucker CJ, Juhn D, Hawkins F (2007) Fifty years of deforestation and forest fragmentation in Madagascar. Environ Conserv 34:325–333

    Article  Google Scholar 

  • Hart LA, Grieve GRH, Downs CT (2013) Fruiting phenology and implications of fruit availability in the fragmented Ngele Forest Complex, KwaZulu-Natal, South Africa. S Afr J Bot 88:296–305

    Article  Google Scholar 

  • Hashimoto C, Furuichi T, Tashiro Y (2001) What factors affect the size of chimpanzee parties in the Kalinzu Forest, Uganda? Examination of fruit abundance and number of estrous females. Int J Primatol 22:947–959

    Article  Google Scholar 

  • Hashimoto C, Suzuki S, Takenoshita Y, Yamagiwa J, Basabose AK, Furuichi T (2003) How fruit abundance affects the chimpanzee party size: a comparison between four study sites. Primates 44:77–81

    PubMed  Google Scholar 

  • Henzi SP, Lusseau D, Weingrill T, van Schaik CP, Barrett L (2009) Cyclicity in the structure of female baboon social networks. Behav Ecol Sociobiol 63:1015–1021

    Article  Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Hodge SJ (2005) Helpers benefit offspring in both the short and long-term in the cooperatively breeding banded mongoose. Proc R Soc Lond B 272:2479–2484

    Article  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Holmes SM (2012) Habitat use and population genetics of the black-and-white ruffed lemur (Varecia variegata) in a fragmented landscape in southeastern Madagascar, MA thesis, University of Calgary

  • Holmes SM, Baden AL, Brenneman RA, Engberg SE, Louis EE, Johnson SE (2013) Patch size and isolation influence genetic patterns in black-and-white ruffed lemur (Varecia variegata) populations. Conserv Genet 14:615–624

    Article  Google Scholar 

  • Holmes SM, Yaney-Keller AM, Rafidimanana DV, Andrianantenaina HM, Louis EE, Johnson SE (2015) Lemur population surveys in the Kianjavato region. Lemur News 19:9–11

    Google Scholar 

  • Irwin MT, Raharison J, Raubenheimer D, Chapman CA, Rothman JM (2014) Nutritional correlates of the “lean season”: effects of seasonality and frugivory on the nutritional ecology of diademed sifakas. Am J Phys Anthropol 153:78–91

    Article  PubMed  Google Scholar 

  • Itoh N, Nishida T (2007) Chimpanzee grouping patterns and food availability in Mahale Mountains National Park, Tanzania. Primates 48:87–96

    Article  PubMed  Google Scholar 

  • Jaatinen K, Ost M, Lehikoinen A (2011) Adult predation risk drives shifts in parental care strategies: a long-term study. J Anim Ecol 80:49–56

    Article  PubMed  Google Scholar 

  • Johnson SE (2002) Ecology and speciation in brown lemurs: white-collared lemurs (Eulemur albocollaris) and hybrids (Eulemur albocollaris x Eulemur fulvus rufus) in southeastern Madagascar. Dissertation, University of Texas at Austin

  • Karpanty SM (2003) Behavioral and ecological interactions of raptors and lemurs in southeastern Madagascar: a multiple predator approach. PhD dissertation, Stony Brook University

  • Karpanty SM (2006) Direct and indirect impacts of raptor predation on lemurs in southeastern Madagascar. Int J Primatol 27:239–261

    Article  Google Scholar 

  • Kerth G, Perony N, Schweitzer F (2011) Bats are able to maintain long-term social relationships despite the high fission-fusion dynamics of their groups. Proc R Soc Lond B 278:2761–2767

    Article  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical Ecology, vol 20, 2nd edn. Elsevier Science & Technology, Burlington, MA, USA

    Google Scholar 

  • Lehman SM, Rajaonson A, Day S (2006) Edge effects and their influence on lemur density and distribution in southeast Madagascar. Am J Phys Anthropol 129:232–241

    Article  PubMed  Google Scholar 

  • Lehmann J, Boesch C (2004) To fission or to fusion: effects of community size on wild chimpanzee (Pan troglodytes verus) social organisation. Behav Ecol Sociobiol 56:207–216

    Article  Google Scholar 

  • Lehmann J, Korstjens AH, Dunbar RIM (2007) Fission-fusion social systems as a strategy for coping with ecological constraints: a primate case. Evol Ecol 21:613–634

    Article  Google Scholar 

  • Link A, Di Fiore A (2013) Effects of predation risk on the grouping patterns of white-bellied spider monkeys (Ateles belzebuth belzebuth) in western Amazonia. Am J Phys Anthropol 150:579–590

    Article  PubMed  Google Scholar 

  • Lunardi DG, Ferreira RG (2014) Fission-fusion dynamics of Guiana dolphin (Sotalia guianensis) groups at Pipa Bay, Rio Grande do Norte, Brazil. Mar Mamm Sci 30:1401–1416

    Article  Google Scholar 

  • Morland HS (1990) Parental behavior and infant development in ruffed lemurs (Varecia-variegata) in a Northeast Madagascar rain-forest. Am J Primatol 20:253–265

    Article  Google Scholar 

  • Morland HS (1991) Social organization and ecology of black and white ruffed lemurs (Variecia variegata variegata) in lowland rain forest, Nosy Mangabe, Madagascar. PhD dissertation, Yale University

  • Murray CM, Lonsdorf EV, Stanton MA, Wellens KR, Miller JA, Goodall J, Pusey AE (2014) Early social exposure in wild chimpanzees: mothers with sons are more gregarious than mothers with daughters. P Natl Acad Sci USA 111:18189–18194

    Article  CAS  Google Scholar 

  • Newton-Fisher NE, Reynolds V, Plumptre AJ (2000) Food supply and chimpanzee (Pan troglodytes schweinfurthii) party size in the Budongo Forest Reserve, Uganda. Int J Primatol 21:613–628

    Article  Google Scholar 

  • Otali E, Gilchrist JS (2006) Why chimpanzee (Pan troglodytes schweinfurthii) mothers are less gregarious than nonmothers and males: the infant safety hypothesis. Behav Ecol Sociobiol 59:561–570

    Article  Google Scholar 

  • Overdorff DJ, Erhart EM, Mutschler T (2005) Does female dominance facilitate feeding priority in black-and-white ruffed lemurs (Varecia variegata) in southeastern Madagascar? Am J Primatol 66:7–22

    Article  PubMed  Google Scholar 

  • Parra GJ, Corkeron PJ, Arnold P (2011) Grouping and fission-fusion dynamics in Australian snubfin and Indo-Pacific humpback dolphins. Anim Behav 82:1423–1433

    Article  Google Scholar 

  • Parrish JK, Edelstein-Keshet L (1999) Complexity, pattern, and evolutionary trade-offs in animal aggregation. Science 284:99–101

    Article  CAS  PubMed  Google Scholar 

  • Pays O, Benhamou S, Helder R, Gerard JF (2007) The dynamics of group formation in large mammalian herbivores: an analysis in the European roe deer. Anim Behav 74:1429–1441

    Article  Google Scholar 

  • Pearson HC (2009) Influences on dusky dolphin (Lagenorhynchus obscurus) fission-fusion dynamics in Admiralty Bay, New Zealand. Behav Ecol Sociobiol 63:1437–1446

    Article  Google Scholar 

  • Pépin D, Gerard JF (2008) Group dynamics and local population density dependence of group size in the Pyrenean chamois, Rupicapra pyrenaica. Anim Behav 75:361–369

    Article  Google Scholar 

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

  • Raman TRS (1997) Factors influencing seasonal and monthly changes in the group size of chital or axis deer in southern India. J Biosciences 22:203–218

    Article  Google Scholar 

  • Ramos-Fernandez G, Morales JM (2014) Unraveling fission-fusion dynamics: how subgroup properties and dyadic interactions influence individual decisions. Behav Ecol Sociobiol 68:1225–1235

    Article  Google Scholar 

  • Ramos-Fernandez G, Boyer D, Aureli F, Vick LG (2009) Association networks in spider monkeys (Ateles geoffroyi. Behav Ecol Sociobiol 63:999–1013

    Article  Google Scholar 

  • Rasmussen DT (1985) A comparative study of breeding seasonality and litter size in 11 taxa of captive lemurs (Lemur and Varecia. Int J Primatol 6:501–517

    Article  Google Scholar 

  • Ratsimbazafy J (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. PhD dissertation, State University of New York at Stony Brook

  • Ren BP, Li DY, Garber PA, Li M (2012) Fission-fusion behavior in Yunnan snub-nosed monkeys (Rhinopithecus bieti) in Yunnan, China. Int J Primatol 33:1096–1109

    Article  Google Scholar 

  • Ridley AR (2007) Factors affecting offspring survival and development in a cooperative bird: social, maternal and environmental effects. J Anim Ecol 76:750–760

    Article  CAS  PubMed  Google Scholar 

  • Rimbach R, Link A, Montes-Rojas A, Di Fiore A, Heistermann M, Heymann EW (2014) Behavioral and physiological responses to fruit availability of spider monkeys ranging in a small forest fragment. Am J Primatol 76:1049–1061

    Article  PubMed  PubMed Central  Google Scholar 

  • Rubenstein DR (2011) Spatiotemporal environmental variation, risk aversion, and the evolution of cooperative breeding as a bet-hedging strategy. P Natl Acad Sci USA 108:10816–10822

    Article  CAS  Google Scholar 

  • Scantlebury M, Clutton-Brock TH, Speakman JR (2004) Energetics of cooperative breeding in meerkats Suricata suricatta. In: Morris S, Vosloo A (eds) Animals and environments. Elsevier Science, Amsterdam, pp. 367–374

    Google Scholar 

  • Schaffner CM, Rebecchini L, Ramos-Fernandez G, Vick LG, Aureli F (2012) Spider monkeys (Ateles geoffroyi yucatenensis) cope with the negative consequences of hurricanes through changes in diet, activity budget, and fission-fusion dynamics. Int J Primatol 33:922–936

    Article  Google Scholar 

  • Schreier AL, Swedell L (2012) Ecology and sociality in a multilevel society: ecological determinants of spatial cohesion in hamadryas baboons. Am J Phys Anthropol 148:580–588

    Article  PubMed  Google Scholar 

  • Silk JB (2007) The adaptive value of sociality in mammalian groups. Philos T Roy Soc B 362:539–559

    Article  Google Scholar 

  • Smith JE, Kolowski JM, Graham KE, Dawes SE, Holekamp KE (2008) Social and ecological determinants of fission-fusion dynamics in the spotted hyaena. Anim Behav 76:619–636

    Article  Google Scholar 

  • Snaith TV, Chapman CA (2007) Primate group size and interpreting sociolecological models: do folivores really play by different rules? Evol Anthropol 16:94–106

    Article  Google Scholar 

  • Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309

    Article  Google Scholar 

  • Sueur C, King AJ, Conradt L, Kerth G, Lusseau D, Mettke-Hofmann C, Schaffner CM, Williams L, Zinner D, Aureli F (2011) Collective decision-making and fission-fusion dynamics: a conceptual framework. Oikos 120:1608–1617

    Article  Google Scholar 

  • Sundaresan SR, Fischhoff IR, Dushoff J, Rubenstein DI (2007) Network metrics reveal differences in social organization between two fission-fusion species, Grevy’s zebra and onager. Oecologia 151:140–149

    Article  PubMed  Google Scholar 

  • Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21

    Article  Google Scholar 

  • Tilden CD, Oftedal OT (1997) Milk composition reflects pattern of maternal care in prosimian primates. Am J Primatol 41:195–211

    Article  CAS  PubMed  Google Scholar 

  • Tutin CEG (1999) Fragmented living: behavioural ecology of primates in a forest fragment in the Lopé Reserve, Gabon. Primates 41:249–265

    Article  Google Scholar 

  • van Schaik CP (1999) The socioecology of fission-fusion sociality in orangutans. Primates 40:69–86

    Article  PubMed  Google Scholar 

  • Vasey N (2007) The breeding system of wild red ruffed lemurs (Varecia rubra): a preliminary report. Primates 48:41–54

    Article  PubMed  Google Scholar 

  • Wakefield ML (2008) Grouping patterns and competition among female Pan troglodytes schweinfurthii at Ngogo, Kibale National Park, Uganda. Int J Primatol 29:907–929

    Article  Google Scholar 

  • Wey TW, Burger JR, Ebensperger LA, Hayes LD (2013) Reproductive correlates of social network variation in plurally breeding degus (Octodon degus). Anim Behav 85:1407–1414

    Article  PubMed  PubMed Central  Google Scholar 

  • White AM, Cameron EZ (2011) Fitness consequences of maternal rearing strategies in warthogs: influence of group size and composition. J Zool 285:77–84

    Article  Google Scholar 

  • White FJ, Overdorff DJ, Balko EA, Wright PC (1995) Distribution of ruffed lemurs (Varecia-variegata) in Ranomafana National-Park, Madagascar. Folia Primatol 64:124–131

    Article  Google Scholar 

  • White AM, Cameron EZ, Peacock MM (2010) Grouping patterns in warthogs, Phacochoerus africanus: is communal care of young enough to explain sociality? Behaviour 147:1–18

    Article  Google Scholar 

  • Wittemyer G, Douglas-Hamilton I, Getz WM (2005) The socioecology of elephants: analysis of the processes creating multitiered social structures. Anim Behav 69:1357–1371

    Article  Google Scholar 

  • Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yearb Phys Anthropol 42:31–72

    Article  Google Scholar 

  • Wright PC, Razafindratsita VR, Pochron ST, Jernvall J (2005) The key to Madagascar frugivores. In: Dew JL, Boubli JP (eds) Tropical fruits and frugivores: the search for strong interactors. Springer, Dordrecht, pp. 121–138

    Chapter  Google Scholar 

Download references

Acknowledgments

We are grateful to Cressant Razafindravelo, Ferdinah Mbana, Jean Pierre Marolahy, Emilys Edgarçon Rakotoson, Gregor Pachmann, Melanie Vomscheid, Jean Samuelson Randrianarisoa, Jerrad Hayden, Sara Pearce Meijerink, Erin Moody, Jordon Traill, Eric Perlett, and Olivia Hanson for research assistance in Madagascar. We thank the BEAS editors and two anonymous reviewers for their comments on an earlier draft of this paper. We also thank the following organizations for funding: International Primatological Society, Omaha’s Henry Doorly Zoo and Aquarium, the Ahmanson Family Foundation, University at Albany, and the Natural Sciences and Engineering Research Council of Canada.

Author information

Authors and Affiliations

  1. Department of Anthropology, University of Calgary, Calgary, Canada

    Sheila M. Holmes & Steig E. Johnson

  2. Department of Anthropology, University at Albany, Albany, NY, USA

    Adam D. Gordon

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

    Edward E. Louis Jr

Authors
  1. Sheila M. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adam D. Gordon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edward E. Louis Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Steig E. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sheila M. Holmes.

Ethics declarations

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Funding

Funding for this research was provided by the International Primatological Society, Omaha’s Henry Doorly Zoo and Aquarium, the Ahmanson Family Foundation, University at Albany, and the Natural Sciences and Engineering Research Council of Canada.

Informed consent

This study did not involve human participants.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by E. Huchard

Electronic supplementary material

ESM 1

(DOCX 18 kb)

ESM 2

(DOCX 61 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Holmes, S.M., Gordon, A.D., Louis, E.E. et al. 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. Behav Ecol Sociobiol 70, 1949–1960 (2016). https://doi.org/10.1007/s00265-016-2201-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-016-2201-4

Keywords

  • Subgroup size
  • Sociality
  • Communal rearing
  • Ecological conditions
  • Seasonality
  • Madagascar