Resource distribution shapes many aspects of primate behavioral ecology. Though the spatial patterning of fruits, leaves, and insects has been explored among primate foods, comparatively less is known about exudate distributions. Tree exudates are a renewable resource, provide long-term evidence of exploitation, and may be selectively exploited to manipulate spatial distribution. We assessed the spatial patterning of trees gouged by common marmosets (Callithrix jacchus) to determine if they exhibit a uniform, random, or clumped distribution. We also asked whether marmosets selectively gouge trees in home range centers, which may afford them exclusive access to exudates. We explored whether spatial or physical characteristics of trees predict how intensely gouged trees were exploited. The mean nearest neighbor distance of gouged trees was significantly closer than expected for a random distribution and Ripley’s K-function showed that gouged trees were clumped across all spatial scales in our study area. Clumping may enable marmosets to reduce day and home ranges and facilitate repeated gouging of trees. Gouged trees were not closer to marmosets’ home range centers than peripheries, nor were centrally located trees more intensely gouged. Increased gouging intensity was associated with larger tree circumferences, although this effect was primarily driven by interspecific differences in circumference. Although marmosets may benefit from exploiting clumped exudates, they do not concentrate gouging in areas where they are more likely to gain exclusive access. Species-specific tree characteristics such as exudate quality and/or bark properties may play a larger role in determining gouging patterns than intergroup feeding competition.
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Bacon, P. J., Ball, F., & Blackwell, P. (1991). A model for territory and group formation in a heterogeneous habitat. Journal of Theoretical Biology, 148(4), 445–468.
Beyer, H.L. (2004). Hawth's analysis tools for ArcGIS. Available at http://www.spatialecology.com/htools.
Boinski, S., Kauffman, L., Ehmke, E., Schet, S., & Vreedzaam, A. (2005). Dispersal patterns among three species of squirrel monkeys (Saimiri oerstedii, S. boliviensis and S. sciureus): I. Divergent costs and benefits. Behaviour, 142(5), 525–632.
Brown, J. L. (1964). The evolution of diversity in avian territorial systems. The Wilson Bulletin, 76(2), 109–208.
Chancellor, R. L., & Isbell, L. A. (2009). Food site residence time and female competitive relationships in wild gray-cheeked mangabeys (Lophocebus albigena). Behavioral Ecology and Sociobiology, 63(10), 1447–1458.
Chapman, C. (1990). Ecological constraints on group size in three species of Neotropical primates. Folia Primatologica, 55(1), 1–9.
Chapman, C. A., Chapman, L. J., & Wrangham, R. W. (1995). Ecological constraints on group size: An analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36(1), 59–70.
Clark, A. (1978). Sex ratio and local resource competition in a prosimian primate. Science, 201(4351), 163–165.
Clutton-Brock, T. H., & Harvey, P. H. (1977). Primate ecology and social organization. Journal of Zoology, 183(1), 1–39.
Coimbra-Filho, A. F., & Mittermeier, R. A. (1977). Tree-gouging, exudate-eating and the “short-tusked” condition in Callithrix and Cebuella. In D. G. Kleiman (Ed.), The biology and conservation of the callitrichidae (pp. 105–115). Washington, DC: Smithsonian Institution Press.
Condit, R., Ashton, P. S., Baker, P., Bunyavejchewin, S., Gunatilleke, S., Gunatilleke, N., Hubbell, S. P., Foster, R. B., Itoh, A., LaFrankie, J. V., Lee, H. S., Losos, E., Manokaran, N., Sukumar, R., & Yamakura, T. (2000). Spatial patterns in the distribution of tropical tree species. Science, 288(5470), 1414–1418.
Cottam, G., & Curtis, J. T. (1956). The use of distance measures in phytosociological sampling. Ecology, 37(3), 451–460.
Crofoot, M. C., Gilby, I. C., Wikelski, M. C., & Kays, R. W. (2008). Interaction location outweighs the competitive advantage of numerical superiority in Cebus capucinus intergroup contests. Proceedings of the National Academy of Sciences of the USA, 105(2), 577–581.
de Oliveira, R., Lins Neto, E., Araújo, E., & Albuquerque, U. (2007). Conservation priorities and population structure of woody medicinal plants in an area of Caatinga vegetation (Pernambuco State, NE Brazil). Environmental Monitoring and Assessment, 132(1), 189–206.
Decanini, D., & Macedo, R. (2008). Sociality in Callithrix penicillata: II. Individual strategies during intergroup encounters. International Journal of Primatology, 29(3), 627–639.
Delvaux, C., Sinsin, B., & Van Damme, P. (2010). Impact of season, stem diameter and intensity of debarking on survival and bark re-growth pattern of medicinal tree species, Benin, West Africa. Biological Conservation, 143(11), 2664–2671.
Digby, L. J., Ferrari, S. F., & Saltzman, W. (2011). Callitrichines: The role of competition in cooperatively breeding species. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, S. K. Bearder, & R. M. Stumpf (Eds.), Primates in perspective (pp. 91–107). New York: Oxford University Press.
Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science, 197(4300), 215–223.
ESRI. (2011). ArcGIS Desktop: Release 10. Redlands: Environmental Systems Research Institute.
Fashing, P. J. (2007). African colobine monkeys: Patterns of between-group interaction. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 201–224). New York: Oxford University Press.
Faulkes, C. G., Arruda, M. F., & Monteiro Da Cruz, M. A. O. (2003). Matrilineal genetic structure within and among populations of the cooperatively breeding common marmoset, Callithrix jacchus. Molecular Ecology, 12(4), 1101–1108.
Ferrari, S., & Lopes Ferrari, M. (1989). A re-evaluation of the social organisation of the callitrichidae, with reference to the ecological differences between genera. Folia Primatologica, 52(3–4), 132–147.
Fragaszy, D. M., & Perry, S. (2003). The biology of traditions: Models and evidence. Cambridge: Cambridge University Press.
Garber, P. A. (1992). Vertical clinging, small body size, and the evolution of feeding adaptations in the callitrichinae. American Journal of Physical Anthropology, 88(4), 469–482.
Garber, P. A., & Porter, L. M. (2010). The ecology of exudate production and exudate feeding in Saguinus and Callimico. In A. M. Burrows & L. T. Nash (Eds.), The evolution of exudativory in primates (pp. 89–108). New York: Springer.
Go, M. (2010). Seasonal changes in food resource distribution and feeding sites selected by Japanese macaques on Koshima Islet, Japan. Primates, 51(2), 149–158.
Grant, J. W. A. (1993). Whether or not to defend? The influence of resource distribution. Marine Behaviour and Physiology, 23(1–4), 137–153.
Hamrick, M. W. (1998). Functional and adaptive significance of primate pads and claws: evidence from New World anthropoids. American Journal of Physical Anthropology, 106(2), 113–127.
Harrison, M. L., & Tardif, S. D. (1994). Social implications of gummivory in marmosets. American Journal of Physical Anthropology, 95(4), 399–408.
Hubbell, S. P. (1979). Tree dispersion, abundance, and diversity in a tropical dry forest. Science, 203(4387), 1299–1309.
Hubrecht, R. (1984). Field observations on group size and composition of the common marmoset (Callithrix jacchus jacchus), at Tapacura, Brazil. Primates, 25(1), 13–21.
Hubrecht, R. (1985). Home-range size and use and territorial behavior in the common marmoset, Callithrix jacchus jacchus, at the Tapacura Field Station, Recife, Brazil. International Journal of Primatology, 6(5), 533–550.
Isbell, L. A., Pruetz, J. D., & Young, T. P. (1998). Movements of vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density, and distribution. Behavioral Ecology and Sociobiology, 42(2), 123–133.
Izumiyama, S., Mochizuki, T., & Shiraishi, T. (2003). Troop size, home range area and seasonal range use of the Japanese macaque in the northern Japan Alps. Ecological Research, 18(5), 465–474.
Jackson, C. (2011). The positional behavior of pygmy marmosets (Cebuella pygmaea) in northwestern Bolivia. Primates, 52(2), 171–178.
Johnson, D. D. P., Kays, R., Blackwell, P. G., & Macdonald, D. W. (2002). Does the resource dispersion hypothesis explain group living? Trends in Ecology & Evolution, 17(12), 563–570.
Kinzey, W. G. (1997). New world primates: Ecology, evolution, and behavior. New York: Aldine de Gruyter.
Kumar, R. S., Mishra, C., & Sinha, A. (2007). Foraging ecology and time-activity budget of the Arunachal macaque Macaca munzala – a preliminary study. Current Science, 93(4), 532–539.
Lacher, T. E., Bouchardet da Fonseca, G. A., Alves, C., & Magalhaes-Castro, B. (1984). Parasitism of trees by marmosets in a central Brazilian gallery forest. Biotropica, 16(3), 202–209.
Lazaro-Perea, C. (2001). Intergroup interactions in wild common marmosets, Callithrix jacchus: territorial defence and assessment of neighbours. Animal Behaviour, 62, 11–21.
Leighton, M., & Leighton, D. R. (1982). The relationship of size of feeding aggregate to size of food patch: Howler monkeys (Alouatta palliata) feeding in trichilia cipo fruit trees on Barro Colorado Island. Biotropica, 14, 81–90.
Leite, E. J. (2001). Spatial distribution patterns of riverine forest taxa in Brasília, Brazil. Forest Ecology and Management, 140(2–3), 257–264.
Maier, W. C., Alonso, C., & Langguth, A. (1982). Field observations on Callithrix jacchus jacchus L. Zeitschrift fur Saugetierkunde, 47, 334–346.
Malhado, A. C., & Petrere, M. (2004). Behaviour of dispersion indices in pattern detection of a population of angico, Anadenanthera peregrina (Leguminosae). Brazilian Journal of Biology, 64(2), 243–249.
Melo, L.C.O. (2001). Seleção de recursos alimentares por Callithrix jacchus – sagui-do-nordeste: Um foco sobre a teoria de otimização. Master’s thesis, Brazil: Universidade Federal de Pernambuco.
Mendes Pontes, A., & Monteiro da Cruz, M. (1995). Home range, intergroup transfers, and reproductive status of common marmosets Callithrix jacchus in a forest fragment in north-eastern Brazil. Primates, 36(3), 335–347.
Milton, K. (1979). Factors influencing leaf choice by howler monkeys – test of some hypotheses of food selection by generalist herbivores. American Naturalist, 114(3), 362–378.
Monteiro da Cruz, M.A. (1998). Dinâmica Reprodutiva em uma População de Sagui-do-Nordeste (Callithrix jacchus) na Estação Ecológica do Tapacurá, Pernambuco. Ph.D. thesis, Brazil: Universidade de São Paulo.
Nash, L. T. (1986). Dietary, behavioral, and morphological aspects of gummivory in primates. American Journal of Physical Anthropology, 29(S7), 113–137.
Oates, J. F. (1987). Food distribution and foraging behavior. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 197–209). Chicago: University of Chicago Press.
Oates, J. F. (1994). The natural history of African colobines. In A. G. Davies & J. F. Oates (Eds.), Colobine monkeys: Their ecology, behaviour, and evolution (pp. 75–128). Cambridge: Cambridge University Press.
Power, M. L. (1996). The other side of callitrichine gummivory: Digestibility and nutritional value. In M. A. Norconk, A. L. Rosenberger, & P. A. Garber (Eds.), Adaptive radiations of Neotropical primates (pp. 97–110). New York: Plenum Press.
Pruetz, J. D., & Isbell, L. A. (2000). Correlations of food distribution and patch size with agonistic interactions in female vervets (Chlorocebus aethiops) and patas monkeys (Erythrocebus patas) living in simple habitats. Behavioral Ecology and Sociobiology, 49(1), 38–47.
Rasmussen, D. (1980). Clumping and consistency in primates' patterns of range use: Definitions, sampling, assessment and applications. Folia Primatologica, 34(1–2), 111–139.
Reeve, H. K., & Hölldobler, B. (2007). The emergence of a superorganism through intergroup competition. Proceedings of the National Academy of Sciences of the USA, 104(23), 9736–9740.
Ripley, B. D. (1977). Modelling spatial patterns. Journal of the Royal Statistical Society B (Methodological), 39(2), 172–212.
Rylands, A. B. (1984). Exudate-eating and tree-gouging by marmosets (Callitrichidae, Primates). In A. C. Chadwick & S. L. Sutton (Eds.), Tropical rain forest: The Leeds Symposium (pp. 155–168). Leeds: Leeds Philosophical and Literary Society.
Rylands, A. B. (1986). Ranging behaviour and habitat preference of a wild marmoset group, Callithrix humeralifer (Callitrichidae, Primates). Journal of Zoology, 210(4), 489–514.
Rylands, A. B. (1987). Primate communities in Amazonian forests: Their habitats and food resources. Cellular and Molecular Life Sciences, 43(3), 265–279.
Rylands, A. B., & de Faria, D. S. (1993). Habitats, feeding ecology, and home range size in the genus Callithrix. In A. B. Rylands (Ed.), Marmosets and tamarins: Systematics, behaviour, and ecology (pp. 262–272). Oxford: Oxford University Press.
Scanlon, C., Chalmers, N., & Monteiro da Cruz, M. (1988). Changes in the size, composition, and reproductive condition of wild marmoset groups (Callithrix jacchus jacchus) in northeast Brazil. Primates, 29(3), 295–305.
Scanlon, C., Chalmers, N., & Monteiro da Cruz, M. (1989). Home range use and the exploitation of gum in the marmoset Callithrix jacchus jacchus. International Journal of Primatology, 10(2), 123–136.
Seidler, T. G., & Plotkin, J. B. (2006). Seed dispersal and spatial pattern in tropical trees. PLoS Biology, 4(11), 2132–2137.
Shopland, J. M. (1987). Food quality, spatial deployment, and the intensity of feeding interference in yellow baboons (Papio cynocephalus). Behavioral Ecology and Sociobiology, 21(3), 149–156.
Slobodchikoff, C. N. (1984). Resources and the evolution of social behavior. In P. W. Price, C. N. Slobodchikoff, & S. W. Guad (Eds.), A new ecology: Novel approaches to integrative systems (pp. 227–251). New York: John Wiley & Sons.
Smith, A. C. (2000). Composition and proposed nutritional importance of exudates eaten by saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins. International Journal of Primatology, 21(1), 69–83.
Smith, A. C. (2010). Exudativory in primates: Interspecific patterns. In A. M. Burrows & L. T. Nash (Eds.), The evolution of exudativory in primates (pp. 45–87). New York: Springer.
Snaith, T. V., & Chapman, C. A. (2005). Towards an ecological solution to the folivore paradox: patch depletion as an indicator of within-group scramble competition in red colobus monkeys (Piliocolobus tephrosceles). Behavioral Ecology and Sociobiology, 59(2), 185–190.
Snaith, T. V., & Chapman, C. A. (2007). Primate group size and interpreting socioecological models: do folivores really play by different rules? Evolutionary Anthropology: Issues, News, and Reviews, 16(3), 94–106.
Sterck, E. H. M., Watts, D. P., & van Schaik, C. P. (1997). The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology, 41, 291–309.
Stevenson, M. F., & Rylands, A. B. (1988). The marmosets, genus Callithrix. In R. A. Mittermeier, A. B. Rylands, & A. F. Coimbra-Filho (Eds.), Ecology and behavior of Neotropical primates ((pp, Vol. II, pp. 131–177). Washington, DC: World Wildlife Fund.
Strier, K. B. (1989). Effects of patch size on feeding associations in muriquis (Brachyteles arachnoides). Folia Primatologica, 52(1–2), 70–77.
Sussman, R. W., & Garber, P. A. (2007). Cooperation and competition in primate social interactions. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 636–651). New York: Oxford University Press.
Sussman, R. W., & Garber, P. A. (2011). Cooperation, collective action, and competition in primate social interactions. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, S. K. Bearder, & R. M. Stumpf (Eds.), Primates in perspective (pp. 587–598). New York: Oxford University Press.
Teaford, M. F., Lucas, P. W., Ungar, P. S., & Glander, K. E. (2006). Mechanical defenses in leaves eaten by Costa Rican howling monkeys (Alouatta palliata). American Journal of Physical Anthropology, 129(1), 99–104.
Travis, S. E., & Slobodchikoff, C. N. (1993). Effects of food resource distribution on the social system of Gunnison's prairie dog (Cynomys gunnisoni). Canadian Journal of Zoology, 71(6), 1186–1192.
Tsuji, Y., & Takatsuki, S. (2004). Food habits and home range use of Japanese macaques on an island inhabited by deer. Ecological Research, 19(4), 381–388.
Tuomisto, H., Ruokolainen, K., & Yli-Halla, M. (2003). Dispersal, environment, and floristic variation of western Amazonian forests. Science, 299(5604), 241–244.
van Schaik, C. P. (1983). Why are diurnal primates living in groups? Behaviour, 87(1–2), 120–144.
van Schaik, C. P. (1989). The ecology of social relationships amongst female primates. In V. Standen & R. A. Foley (Eds.), Comparative socioecology: The behavioural ecology of humans and other mammals (pp. 195–218). Oxford: Blackwell.
Vasiliauskas, R. (1998). Patterns of wounding and decay in stems of Quercus robur due to bark peeling. Scandinavian Journal of Forest Research, 13(1–4), 437–441.
Vasudev, D., Kumar, A., & Sinha, A. (2008). Resource distribution and group size in the common langur Semnopithecus entellus in southern India. American Journal of Primatology, 70(7), 680–689.
Vilela, S. L., & de Faria, D. S. (2004). Seasonality of the activity pattern of Callithrix penicillata (Primates, Callitrichidae) in the cerrado (scrub savanna vegetation). Brazilian Journal of Biology, 64(2), 363–370.
Vinyard, C. J., Wall, C. E., Williams, S. H., Mork, A. L., Armfield, B. A., Melo, L. C. O., Valença-Montenegro, M. M., Valle, Y. B. M., Oliveira, M. A. B., Lucas, P. W., Schmitt, D., Taylor, A. B., & Hylander, W. L. (2009). The evolutionary morphology of tree gouging in marmosets. In S. M. Ford, L. M. Porter, & L. C. Davis (Eds.), The smallest anthropoids (pp. 395–409). New York: Springer.
Waser, P. M. (1981). Sociality or territorial defense? The influence of resource renewal. Behavioral Ecology and Sociobiology, 8(3), 231–237.
Waser, P. M., & Waser, M. S. (1985). Ichneumia alhicauda and the evolution of viverrid gregariousness. Zeitschrift für Tierpsychologie, 68(2), 137–151.
Welch, D., Scott, D., & Staines, B. W. (1997). Bark stripping damage by red deer in a sitka spruce forest in western Scotland III. Trends in wound condition. Forestry, 70(2), 113–120.
Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262–299.
Youlatos, D. (2009). Locomotion, postures, and habitat use by pygmy marmosets (Cebuella pygmaea). In S. M. Ford, L. M. Porter, & L. C. Davis (Eds.), The smallest anthropoids (pp. 279–297). New York: Springer.
We thank P. Lucas for advice and assistance in collecting these data as well as two anonymous reviewers, the associate editor, and editor-in-chief for their helpful comments. Funding was provided by the National Science Foundation (BCS-0094666), The National Geographic Society, and The Leakey Foundation.
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Thompson, C.L., Robl, N.J., de Oliveira Melo, L.C. et al. Spatial Distribution and Exploitation of Trees Gouged by Common Marmosets (Callithrix jacchus). Int J Primatol 34, 65–85 (2013). https://doi.org/10.1007/s10764-012-9647-7
- Intergroup competition
- Renewable resources
- Resource distribution