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Spatial Distribution and Exploitation of Trees Gouged by Common Marmosets (Callithrix jacchus)

Abstract

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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References

  1. 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.

    Article  Google Scholar 

  2. Beyer, H.L. (2004). Hawth's analysis tools for ArcGIS. Available at http://www.spatialecology.com/htools.

  3. 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.

    Article  Google Scholar 

  4. Brown, J. L. (1964). The evolution of diversity in avian territorial systems. The Wilson Bulletin, 76(2), 109–208.

    Google Scholar 

  5. 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.

    PubMed  Article  Google Scholar 

  6. Chapman, C. (1990). Ecological constraints on group size in three species of Neotropical primates. Folia Primatologica, 55(1), 1–9.

    Article  CAS  Google Scholar 

  7. 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.

    Article  Google Scholar 

  8. Clark, A. (1978). Sex ratio and local resource competition in a prosimian primate. Science, 201(4351), 163–165.

    PubMed  Article  CAS  Google Scholar 

  9. Clutton-Brock, T. H., & Harvey, P. H. (1977). Primate ecology and social organization. Journal of Zoology, 183(1), 1–39.

    Article  Google Scholar 

  10. 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.

    Google Scholar 

  11. 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.

    PubMed  Article  CAS  Google Scholar 

  12. Cottam, G., & Curtis, J. T. (1956). The use of distance measures in phytosociological sampling. Ecology, 37(3), 451–460.

    Article  Google Scholar 

  13. 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.

    PubMed  Article  CAS  Google Scholar 

  14. 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.

    PubMed  Article  Google Scholar 

  15. Decanini, D., & Macedo, R. (2008). Sociality in Callithrix penicillata: II. Individual strategies during intergroup encounters. International Journal of Primatology, 29(3), 627–639.

    Article  Google Scholar 

  16. 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.

    Article  Google Scholar 

  17. 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.

    Google Scholar 

  18. Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science, 197(4300), 215–223.

    PubMed  Article  CAS  Google Scholar 

  19. ESRI. (2011). ArcGIS Desktop: Release 10. Redlands: Environmental Systems Research Institute.

    Google Scholar 

  20. 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.

    Google Scholar 

  21. 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.

    PubMed  Article  CAS  Google Scholar 

  22. 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.

    Article  CAS  Google Scholar 

  23. Fragaszy, D. M., & Perry, S. (2003). The biology of traditions: Models and evidence. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  24. 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.

    PubMed  Article  CAS  Google Scholar 

  25. 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.

    Chapter  Google Scholar 

  26. 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.

    PubMed  Article  Google Scholar 

  27. Grant, J. W. A. (1993). Whether or not to defend? The influence of resource distribution. Marine Behaviour and Physiology, 23(1–4), 137–153.

    Article  Google Scholar 

  28. 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.

    PubMed  Article  CAS  Google Scholar 

  29. Harrison, M. L., & Tardif, S. D. (1994). Social implications of gummivory in marmosets. American Journal of Physical Anthropology, 95(4), 399–408.

    PubMed  Article  CAS  Google Scholar 

  30. Hubbell, S. P. (1979). Tree dispersion, abundance, and diversity in a tropical dry forest. Science, 203(4387), 1299–1309.

    PubMed  Article  CAS  Google Scholar 

  31. 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.

    Article  Google Scholar 

  32. 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.

    Article  Google Scholar 

  33. 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.

    Article  Google Scholar 

  34. 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.

    Article  Google Scholar 

  35. Jackson, C. (2011). The positional behavior of pygmy marmosets (Cebuella pygmaea) in northwestern Bolivia. Primates, 52(2), 171–178.

    PubMed  Article  Google Scholar 

  36. 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.

    Article  Google Scholar 

  37. Kinzey, W. G. (1997). New world primates: Ecology, evolution, and behavior. New York: Aldine de Gruyter.

    Google Scholar 

  38. 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.

    Google Scholar 

  39. 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.

    Article  Google Scholar 

  40. Lazaro-Perea, C. (2001). Intergroup interactions in wild common marmosets, Callithrix jacchus: territorial defence and assessment of neighbours. Animal Behaviour, 62, 11–21.

    Article  Google Scholar 

  41. 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.

    Article  Google Scholar 

  42. Leite, E. J. (2001). Spatial distribution patterns of riverine forest taxa in Brasília, Brazil. Forest Ecology and Management, 140(2–3), 257–264.

    Article  Google Scholar 

  43. Maier, W. C., Alonso, C., & Langguth, A. (1982). Field observations on Callithrix jacchus jacchus L. Zeitschrift fur Saugetierkunde, 47, 334–346.

    Google Scholar 

  44. 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.

    Article  CAS  Google Scholar 

  45. 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.

  46. 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.

    Article  Google Scholar 

  47. 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.

    Article  CAS  Google Scholar 

  48. 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.

  49. Nash, L. T. (1986). Dietary, behavioral, and morphological aspects of gummivory in primates. American Journal of Physical Anthropology, 29(S7), 113–137.

    Article  Google Scholar 

  50. 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.

    Google Scholar 

  51. 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.

    Google Scholar 

  52. 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.

    Chapter  Google Scholar 

  53. 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.

    Article  Google Scholar 

  54. Rasmussen, D. (1980). Clumping and consistency in primates' patterns of range use: Definitions, sampling, assessment and applications. Folia Primatologica, 34(1–2), 111–139.

    Article  CAS  Google Scholar 

  55. 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.

    PubMed  Article  CAS  Google Scholar 

  56. Ripley, B. D. (1977). Modelling spatial patterns. Journal of the Royal Statistical Society B (Methodological), 39(2), 172–212.

    Google Scholar 

  57. 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.

    Google Scholar 

  58. 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.

    Article  Google Scholar 

  59. Rylands, A. B. (1987). Primate communities in Amazonian forests: Their habitats and food resources. Cellular and Molecular Life Sciences, 43(3), 265–279.

    Article  Google Scholar 

  60. 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.

    Google Scholar 

  61. 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.

    Article  Google Scholar 

  62. 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.

    Article  Google Scholar 

  63. Seidler, T. G., & Plotkin, J. B. (2006). Seed dispersal and spatial pattern in tropical trees. PLoS Biology, 4(11), 2132–2137.

    Article  CAS  Google Scholar 

  64. 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.

    Article  Google Scholar 

  65. 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.

    Google Scholar 

  66. 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.

    Article  Google Scholar 

  67. 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.

    Chapter  Google Scholar 

  68. 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.

    Article  Google Scholar 

  69. 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.

    Article  Google Scholar 

  70. 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.

    Article  Google Scholar 

  71. 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.

    Google Scholar 

  72. Strier, K. B. (1989). Effects of patch size on feeding associations in muriquis (Brachyteles arachnoides). Folia Primatologica, 52(1–2), 70–77.

    Article  CAS  Google Scholar 

  73. 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.

    Google Scholar 

  74. 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.

    Google Scholar 

  75. 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.

    PubMed  Article  CAS  Google Scholar 

  76. 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.

    Article  Google Scholar 

  77. 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.

    Article  Google Scholar 

  78. Tuomisto, H., Ruokolainen, K., & Yli-Halla, M. (2003). Dispersal, environment, and floristic variation of western Amazonian forests. Science, 299(5604), 241–244.

    PubMed  Article  CAS  Google Scholar 

  79. van Schaik, C. P. (1983). Why are diurnal primates living in groups? Behaviour, 87(1–2), 120–144.

    Article  Google Scholar 

  80. 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.

    Google Scholar 

  81. 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.

    Article  Google Scholar 

  82. 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.

    PubMed  Article  Google Scholar 

  83. 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.

    Article  CAS  Google Scholar 

  84. 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.

    Chapter  Google Scholar 

  85. Waser, P. M. (1981). Sociality or territorial defense? The influence of resource renewal. Behavioral Ecology and Sociobiology, 8(3), 231–237.

    Article  Google Scholar 

  86. Waser, P. M., & Waser, M. S. (1985). Ichneumia alhicauda and the evolution of viverrid gregariousness. Zeitschrift für Tierpsychologie, 68(2), 137–151.

    Article  Google Scholar 

  87. 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.

    Article  Google Scholar 

  88. Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262–299.

    Article  Google Scholar 

  89. 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.

    Chapter  Google Scholar 

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Acknowledgments

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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Correspondence to Cynthia L. Thompson.

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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

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Keywords

  • Callitrichids
  • Exudativory
  • GIS
  • Intergroup competition
  • Renewable resources
  • Resource distribution