Abstract
Like other members of their subfamily (e.g., spider monkeys and muriquis), woolly monkeys have long been suspected to have flexible association patterns. Yet, the dispersed nature of woolly monkey groups as they perform their daily activities has made it difficult for previous studies to quantitatively describe how spatial cohesion and ranging dynamics, both within and between groups, may vary over time and in relation to temporal fluctuations in resources, such as fruit and mating opportunities. Using a combination of location and subgroup composition records collected by multiple observers on animals belonging to four neighboring social groups, we found that lowland woolly monkeys (Lagothrix lagotricha poeppigii) at the Tiputini Biodiversity StationĀ in Amazonian Ecudaor demonstrate relatively high degrees of fission-fusion dynamics, with groups dividing frequently into subgroups and showing temporally variable cohesion among group members. Associations were not limited to members of a single social group, and tolerant associations between members of some neighboring social groups occurred with relatively high frequency. As observed in other woolly monkey populations, home range overlap between neighboring groups was extensive, with particular pairs of groups showing higher degrees of overlap than others. Although woolly monkeys are considered non-territorial, the four focal social groups retained some exclusivity of their core areas as evidenced by minimal core area overlap during most months of sampling for most pairs of groups. Surprisingly, habitat-wide estimates of fruit availability had little to no influence on the observed variation in group cohesion and ranging patterns among the four groups, while indices of mating opportunities did, suggesting that grouping and ranging dynamics in woolly monkeys may not primarily be the result of competition over food, but rather of competition over mates.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227ā266
Anderson DP, Nordheim EV, Boesch C, Moermond TC (2002) Factors influencing fission-fusion grouping in chimpanzees. In: Boesch C, Hohmann G, Marchant L (eds) Behavioral diversity in chimpanzees and bonobos. Cambridge University Press, Cambridge, UK, pp 90ā101
Asensio N, Korstjens AH, Aureli F (2009) Fissioning minimizes ranging costs in spider monkeys: a multiple-level approach. Behav Ecol Sociobiol 63:649ā659
Aureli F, Schaffner CM, Boesch C et al (2008) Fission-fusion dynamics: new research frameworks. Curr Anthropol 49:627ā654
Barton K (2016) MuMIn: multi-model inference. R package version 1.15.6. http://CRAN.R-project.org/package=MuMIn
Bates D, MƤchler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1ā48. https://doi.org/10.18637/jss.v067.i01
Bermejo M (2004) Home-range use and intergroup encounters in western gorillas (Gorilla g. gorilla) at Lossi forest, North Congo. Am J Primatol 64:223ā232. https://doi.org/10.1002/ajp.20073
Bezanson M, Garber PA, Murphy JT, Premo LS (2008) Patterns of subgrouping and spatial affiliation in a community of mantled howling monkeys (Alouatta palliata). Am J Primatol 70:282ā293. https://doi.org/10.1002/ajp.20486
Blake JG, Guerra J, Mosquera D et al (2010) Use of mineral licks by white-bellied spider monkeys (Ateles belzebuth) and red howler monkeys (Alouatta seniculus) in Eastern Ecuador. Int J Primatol 31:471ā483. https://doi.org/10.1007/s10764-010-9407-5
Blake JG, Mosquera D, Loiselle BA et al (2012) Temporal activity patterns of terrestrial mammals in lowland rainforest of eastern Ecuador. Ecotropica 18:137ā146
Boesch C (1996) Social grouping in Tai chimpanzees. In: McGrew W, Marchant L, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, UK, pp 101ā113
Boesch C, Boesch-Achermann H (2000) The chimpanzees of the TaĆÆ forest: behavioural ecology and evolution. Oxford University Press, New York
Bradley BJ, Doran-Sheehy DM, Lukas D et al (2004) Dispersed male networks in Western gorillas. Curr Biol 14:510ā513. https://doi.org/10.1016/j.cub.2004.02.062
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer Science & Business Media, New York
Burt WH (1949) Territoriality. J Mammal 30:25ā27. https://doi.org/10.2307/1375192
Caillaud D, Ndagijimana F, Giarrusso AJ et al (2014) Mountain gorilla ranging patterns: influence of group size and group dynamics. Am J Primatol 76:730ā746. https://doi.org/10.1002/ajp.22265
Calenge C (2006) The package āadehabitatā for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516ā519. https://doi.org/10.1016/j.ecolmodel.2006.03.017
Chapman CA (1990) Association patterns of spider monkeys: the influence of ecology and sex on social organization. Behav Ecol Sociobiol 26:409ā414
Chapman CA, Chapman LJ (2000) Determinants of group size in social primates: the importance of travel costs. In: Boinski S, Garber PA (eds) On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 24ā42
Chapman CA, Chapman LJ, Wrangham R et al (1992) Estimators of fruit abundance of tropical trees. Biotropica 24:527ā531
Chapman CA, Chapman LJ, Wrangham RW (1995) Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59ā70
Crofoot MC, Gilby IC, Wikelski MC, Kays RW (2008) Interaction location outweighs the competitive advantage of numerical superiority in Cebus capucinus intergroup contests. Proc Natl Acad Sci 105:577ā581. https://doi.org/10.1073/pnas.0707749105
Defler TR (1996) Aspects of the ranging pattern in a group of wild woolly monkeys (Lagothrix lagothricha). Am J Primatol 38:289ā302
Defler TR, Defler SB (1996) Diet of a group of Lagothrix lagothricha lagothricha in southeastern Colombia. Int J Primatol 17:161ā190
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Dew JL (2005) Foraging, food choice, and food processing by sympatric ripe-fruit specialists: Lagothrix lagotricha poeppigii and Ateles belzebuth belzebuth. Int J Primatol 26:1107ā1135. https://doi.org/10.1007/s10764-005-6461-5
Di Fiore A (1997) Ecology and behavior of lowland woolly monkeys (Lagothrix lagotricha poeppigii, Atelinae) in eastern Ecuador. University of California, Davis
Di Fiore A (2003) Ranging behavior and foraging ecology of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in YasunĆ National Park, Ecuador. Am J Primatol 59:47ā66. https://doi.org/10.1002/ajp.10065
Di Fiore A (2004) Diet and feeding ecology of woolly monkeys in a western Amazonian rain forest. Int J Primatol 25:767ā801
Di Fiore A, Rodman PS (2001) Time allocation patterns of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in a neotropical terra firma forest. Int J Primatol 22:449ā480
Di Fiore A, Strier KB (2004) Flexibility in social organization in atelin primates. In: XXth Congress of the International Primatological Society. Folia Primatologica, Turin, Italy, p 140
Di Fiore A, Link A, Schmitt CA, Spehar SN (2009) Dispersal patterns in sympatric woolly and spider monkeys: integrating molecular and observational data. Behaviour 146:437ā470
Di Fiore A, Link A, Campbell C (2011) The atelines: behavioral an socioecological diversity in a New World monkey radiation. In: Primates in perspective. Oxford University Press, New York, pp 155ā188
Dias LG, Strier KB (2003) Effects of group size on ranging patterns in Brachyteles arachnoides hypoxanthus. Int J Primatol 24:209ā221. https://doi.org/10.1023/A:1023054513354
Ellis K, Pain E, Schmitt CA, Di Fiore A (2014) Ranging and association patterns of woolly monkeys (Lagothrix poeppigii) in lowland Ecuador. Am J Phys Anthropol 153:119
Ellis K, Abondano L, Montes-Rojas A et al (in review) Reproductive seasonality in two sympatric primates (Ateles belzebuth and Lagothrix lagotricha poeppigii) from Amazonian Ecuador. Am J Primatol
Fashing PJ (2001) Male and female strategies during intergroup encounters in guerezas Colobus guereza: evidence for resource defense mediated through males and a comparison with other primates. Behav Ecol Sociobiol 50:219ā230. https://doi.org/10.1007/s002650100358
Fieberg J, Kochanny CO (2005) Quantifying home-range overlap: the importance of the utilization distribution. J Wildl Manag 69:1346ā1359. https://doi.org/10.2193/0022-541X(2005)69[1346:QHOTIO]2.0.CO;2
Ganas J, Robbins MM (2005) Ranging behavior of the mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda: a test of the ecological constraints model. Behav Ecol Sociobiol 58:277ā288. https://doi.org/10.1007/s00265-005-0920-z
Goodall J (1986) The chimpanzees of Gombe. Belknap Press, Cambridge
Grueter CC, Chapais B, Zinner D (2012) Evolution of multilevel social systems in nonhuman primates and humans. Int J Primatol 33:1002ā1037. https://doi.org/10.1007/s10764-012-9618-z
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 22:947ā959
Hurlbert SH (1978) The measurement of niche overlap and some relatives. Ecology 59:67ā77. https://doi.org/10.2307/1936632
Isbell LA, Pruetz JD, Young TP (1998) Movements of vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density, and distribution. Behav Ecol Sociobiol 42:123ā133. https://doi.org/10.1007/s002650050420
Janson CH, Goldsmith ML (1995) Predicting group size in primates: foraging costs and predation risks. Behav Ecol 6:326ā336
Kavanagh M, Dresdale L (1975) Observations on the woolly monkey (Lagothrix lagothricha) in northern Colombia. Primates 16:285ā294. https://doi.org/10.1007/BF02381556
Kays R, Crofoot MC, Jetz W, Wikelski M (2015) Terrestrial animal tracking as an eye on life and planet. Science 348:aaa2478. https://doi.org/10.1126/science.aaa2478
Kenward RE, Hodder KH (1996) Ranges V. An analysis system for biological location data. Institute of Terrestrial Ecology, Dorset
Kie JG (2013) A rule-based ad hoc method for selecting a bandwidth in kernel home-range analyses. Anim Biotelemetry 1:13. https://doi.org/10.1186/2050-3385-1-13
Kie JG, Matthiopoulos J, Fieberg J etĀ al (2010) The home-range concept: are traditional estimators still relevant with modern telemetry technology? Philos Trans R Soc Lond B Biol Sci 365:2221ā2231. https://doi.org/10.1098/rstb.2010.0093
Klein LL, Klein DJ (1977) Feeding behaviour of the Colombian spider monkey, Ateles belzebuth. In: Clutton-Brock TH (ed) Primate ecology: studies in feeding and ranging behavior in lemurs, monkeys, and apes. Academic, London, pp 153ā181
Koch F, Signer J, Kappeler PM, Fichtel C (2016) The role of the residence-effect on the outcome of intergroup encounters in Verreauxās sifakas. Sci Rep 6:28457. https://doi.org/10.1038/srep28457
Kummer H (1968) Social organization of hamadryas baboons. Chicago University Press, Chicago
Kummer H (1971) Primate societies: group techniques of ecological adaptation. Aldine, Chicago
Kuznetsova A, Brockhoff PB, Christensen RHB (2014) lmerTest: tests for random and fixed effects for linear mixed effect models. R. Package version 2.0-20. http://cran.r-project.org/web/packages/lmerTest/index.html
Langrock R, Hopcraft JGC, Blackwell PG et al (2014)Ā Modelling group dynamic animal movement. Methods Ecol Evol 5:190ā199. https://doi.org/10.1111/2041-210X.12155
Laver PN, Kelly MJ (2008) A critical review of home range studies. J Wildl Manag 72:290ā298. https://doi.org/10.2193/2005-589
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 56:207ā216. https://doi.org/10.1007/s00265-004-0781-x
Link A (2011) Social and ecological determinants of āfission-fusionā sociality and grouping strategies in the white bellied spider monkey (Ateles belzebuth belzebuth) in a lowland rainforest in Western Amazonia. New York University, New York
Link A, Galvis N, Fleming E, Di Fiore A (2011) Patterns of mineral lick visitation by spider monkeys and howler monkeys in Amazonia: are licks perceived as risky areas? Am J Primatol 73:386ā396. https://doi.org/10.1002/ajp.20910
Majolo B, Ventura R, Koyama NF (2005) Sex, rank and age differences in the Japanese macaque (Macaca fuscata yakui) participation in inter-group encounters. Ethology 111:455ā468. https://doi.org/10.1111/j.1439-0310.2005.01087.x
Markham AC, Guttal V, Alberts SC, Altmann J (2013) When good neighbors donāt need fences: temporal landscape partitioning among baboon social groups. Behav Ecol Sociobiol 67:875ā884. https://doi.org/10.1007/s00265-013-1510-0
Matsumoto-Oda A, Hosaka K, Huffman MA, Kawanaka K (1998) Factors affecting party size in chimpanzees of the Mahale Mountains. Int J Primatol 19:999ā1011. https://doi.org/10.1023/A:1020322203166
Mitani JC, Watts DP, Lwanga JS (2002) In: Boesch C, Hohmann G, Marchant L (eds) Ecological and social correlates of chimpanzee party size and composition. Cambrige University Press, Cambridge, UK, pp 102ā111
Nakamura M, Corp N, Fujimoto M et al (2013) Ranging behavior of Mahale chimpanzees: a 16 year study. Primates 54:171ā182. https://doi.org/10.1007/s10329-012-0337-z
Nathan R, Getz WM, Revilla E et al (2008) A movement ecology paradigm for unifying organismal movement research. PNAS pnas.0800375105. https://doi.org/10.1073/pnas.0800375105
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 21:613ā628. https://doi.org/10.1023/A:1005561203763
Nishimura A (1990) A sociological and behavioral study of woolly monkeys, Lagothrix lagotricha, in the upper Amazon. Sci Eng Rev Doshisha Univ 31:87ā121
Nishimura A (1994) Social interaction patterns of woolly monkeys (Lagothrix lagotricha): a comparison among the atelines. Sci Eng Rev Doshisha Univ 35:91ā110
Nishimura A (2003) Reproductive parameters of wild female Lagothrix lagotricha. Int J Primatol 24:707ā722
Peres CA (1994) Diet and feeding ecology of gray woolly monkeys (Lagothrix lagotricha cana) in central Amazonia: comparisons with other atelines. Int J Primatol 15:333ā372
Peres CA (1996) Use of space, spatial group structure, and foraging group size of gray woolly monkeys (Lagothrix lagotricha cana) at Urucu, Brazil. In: Adaptive radiations of neotropical primates. Springer, New York, pp 467ā488
Ramos-FernĆ”ndez G (2005) Vocal communication in a fission-fusion society: do spider monkeys stay in touch with close associates? Int J Primatol 26:1077ā1092. https://doi.org/10.1007/s10764-005-6459-z
Schmitt CA, Di Fiore A (2014) Life history, behavior, and development of wild immature lowland woolly monkeys (Lagothrix poeppigii) in Amazonian Ecuador. In: The woolly monkey. Springer, New York, pp 113ā146
Seiler N, Boesch C, Mundry R et al (2017) Space partitioning in wild, non-territorial mountain gorillas: the impact of food and neighbours. R Soc Open Sci 4:170720. https://doi.org/10.1098/rsos.170720
Shanee S (2014) Ranging behaviour, daily path lengths, diet and habitat use of yellow-tailed woolly monkeys (Lagothrix flavicauda) at La Esperanza, Peru. In: Defler TR (ed) The woolly monkey: behavior, ecology, systematics, and captive research. Springer, New York, pp 167ā185
Shimooka Y (2003) Seasonal variation in association patterns of wild spider monkeys (Ateles belzebuth belzebuth) at La Macarena, Colombia. Primates 44:83ā90. https://doi.org/10.1007/s10329-002-0028-2
Snodderly, D.M., Ellis, K.M., Lieberman, S.R., Link., A., Fernandez-Duque, E., and Di Fiore, A. [in review]. Initiation of feeding by four sympatric Neotropical primates (Ateles belzebuth, Lagothrix lagotricha poeppigii, Plecturocebus (Callicebus) discolor, and Pithecia aequatorialis) in Amazonian Ecuador: Relationships to photic and ecological factors. PLoS ONE
Stevenson PR (1992) Diet of woolly monkeys (Lagothrix lagotricha) at La Macarena, Colombia. Field Stud New World Monkeys Macarena Colomb 6:3ā14
Stevenson PR (2004) Phenological patterns of woody vegetation at Tinigua Park, Colombia: methodological comparisons with emphasis on fruit production/Patrones fenolĆ³gicos de vegetaciĆ³n leƱosa en el Parque Tinigua, Colombia: comparaciones metodolĆ³gicas con Ć©nfasis en la producciĆ³n de frutos. Caldasia 26:125ā150
Stevenson PR (2006) Activity and ranging patterns of Colombian woolly monkeys in North-Western Amazonia. Primates 47:239ā247
Stevenson PR, Quinones MJ, Ahumada JA (1994) Ecological strategies of woolly monkeys (Lagothrix lagotricha) at Tinigua National Park, Colombia. Am J Primatol 32:123ā140
Symington MM (1987) Sex ratio and maternal rank in wild spider monkeys: when daughters disperse. Behav Ecol Sociobiol 20:421ā425
Symington MM (1990) Fission-fusion social organization in Ateles and Pan. Int J Primatol 11:47ā61. https://doi.org/10.1007/BF02193695
Watts DP (1998) Long-term habitat use by mountain gorillas (Gorilla gorilla beringei). 1. Consistency, variation, and home range size and stability. Int J Primatol 19:651ā680. https://doi.org/10.1023/A:1020324909101
Westley PAH, Berdahl AM, Torney CJ, Biro D (2018) Collective movement in ecology: from emerging technologies to conservation and management. Philos Trans R Soc B 373:20170004. https://doi.org/10.1098/rstb.2017.0004
Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. University of Chicago Press, Chicago
Wrangham RW (1977) Feeding behavior of chimpanzees in Gombe National Park, Tanzania. In: Clutton-Brock TH (ed) Primate ecology. Academic, London
Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262ā300
Wrangham RW (1986) Ecology and social relationships in two species of chimpanzee. In: Rubenstein DI, Wrangham RW (eds) Ecology and social evolution: birds and mammals. Princeton University Press, Princeton, pp 352ā378
Wrangham RW (2000) Why are male chimpanzees more gregarious than mothers? A scramble competition hypothesis. In: Kappeler PM (ed) Studies of feeding and ranging behavior in lemurs, monkeys, and apes. Cambridge University Press, Cambridge, UK, pp 248ā258
ZĆ”rate DA, Stevenson PR (2014) Behavioral ecology and interindividual distance of woolly monkeys (Lagothrix lagothricha) in a rainforest fragment in Colombia. In: The woolly monkey. Springer, New York, pp 227ā245
Zhao Q-K (1997) Intergroup interactions in Tibetan macaques at Mt. Emei, China. Am J Phys Anthropol 104:459ā470. https://doi.org/10.1002/(SICI)1096-8644(199712)104:4<459::AID-AJPA3>3.0.CO;2-N
Acknowledgments
We would like to thank the Ecuadorian government and the Ministerio de Ambiente for permission to work in the YasunĆ region and the wonderful directors and staff of the Universidad San Francisco de Quito and Tiputini Biodiversity Station for facilitating our primatological research at the site. Special thanks are due to David and Consuelo Romo, Kelly Swing, Diego Mosquera, Gaby Vinueza, Tomi Sugahara, Majo RendĆ³n, and all of the stationās ātigresā who have provided immeasurable logistical support and friendship to our research team in the field. We are grateful for the hard work and dedication of many of our fellow Proyecto Primates team members (Laura Abondano, Rebekah Ellis, Miguel GarcĆa, Nausica de Gibert, Janel Mayo, Pearson McGovern, Lucy Millington, Evelyn Pain, SebastiĆ”n RamĆrez, Robyn Reeder, Kelly Sampeck) who spent extended periods in the field collecting the behavioral and phenological data on which the study relies. We further thank our colleagues Becca Lewis, Mariah Hopkins, AndrĆ©s Link, and DennĆ© Reed who assisted with the design of this study and Maryjka Blaszczyk and Amanda Perofsky who provided helpful editorial comments in the early stages of writing. This research was funded by NSF BCS-1062540, NSF BCS-1540403, NSF BCS-1638822; the Wenner-Gren, L.S.B. Leakey, and Nacey Maggioncalda Foundations; the National Geographic Society; the Explorers Club; Idea Wild; New York University; and the University of Texas at Austin.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Appendix
Appendix
Rights and permissions
Copyright information
Ā© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Ellis, K., Di Fiore, A. (2019). Variation in Space Use and Social Cohesion Within and Between Four Groups of Woolly Monkeys (Lagothrix lagotricha poeppigii) in Relation to Fruit Availability and Mating Opportunities at the Tiputini Biodiversity Station, Ecuador. In: Reyna-Hurtado, R., Chapman, C. (eds) Movement Ecology of Neotropical Forest Mammals. Springer, Cham. https://doi.org/10.1007/978-3-030-03463-4_10
Download citation
DOI: https://doi.org/10.1007/978-3-030-03463-4_10
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-03462-7
Online ISBN: 978-3-030-03463-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)