International Journal of Primatology

, Volume 39, Issue 3, pp 397–414 | Cite as

Primates and Dung Beetles: Two Dispersers Are Better than One in Secondary Forest

  • Laurence CulotEmail author
  • Marie-Claude Huynen
  • Eckhard W. Heymann


Primary seed dispersal by primates (phase I) followed by secondary seed dispersal by dung beetles (phase II) is a common diplochorous system in tropical forests. In such systems, phase I affects the occurrence/outcome of phase II, triggering cascading effects along the chain of plant recruitment with direct consequences on seed dispersal effectiveness. However, we know very little regarding whether seed dispersal effectiveness is increased or decreased by phase II and whether this effect is consistent among habitats. Using a primate–dung beetle diplochorous system, we determined 1) the characteristics of phase I that may affect phase II; 2) the pathways relating biotic/abiotic factors to seed/seedling survival; and 3) if the direction and/or magnitude of phase II effects on seed dispersal effectiveness depend on phase I characteristics. We marked and characterized the dispersal characteristics of 981 seeds dispersed by two tamarin species (Saguinus mystax, Leontocebus nigrifrons) and checked the fate of 503 of them for ≥1 year. Seeds dispersed by L. nigrifrons and seeds surrounded by larger amounts of dung were more likely to be buried by dung beetles. Burial increased seed survival in secondary forest while low seed density increased germination in both habitats. Seed burial increased seed dispersal effectiveness more strongly in secondary (+52.2%) vs. in primary forest (+5.0%), in L. nigrifrons (+12.9%) vs. in S. mystax (+7.9%) feces, and in larger fecal portions (+22.1%) vs. in small–medium ones (+7.3–7.4%). In conclusion, two seed dispersers are more effective than one only in secondary forest, and the magnitude of increase of seed dispersal effectiveness with phase II depends on how the seeds are primarily dispersed.


Context dependence Primary and secondary dispersal Seed burial Seed survival Seedling recruitment 



We are grateful to our field assistant, Jeisen Shahuano Tello, for his help on the field, and to Ricardo Zárate and Carlos Amasifuen for the identification of plant species and forest characterization. We thank Ellen Andresen and three anonymous reviewers for their useful comments on a previous version of the article, as well as the editor-in-chief, Dr. Joanna M. Setchell, and the guest editor, Dr. Onja H. Razafindratsima. This study was made possible thanks to a grant from FRIA (Fonds pour la formation à la recherche dans l’industrie et dans l’agriculture) and FNRS (Fonds National de la Recherche Scientifique), Belgium, to L. Culot. L. Culot was financed by a FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) grant during the writing of this article (2014/14739-0). We thank Drs. Yamato Tsuji, Hiroki Sato, and Onja H. Razafindratsima for inviting us to contribute to this special issue.

Supplementary material

10764_2018_41_MOESM1_ESM.docx (88 kb)
ESM 1 (DOCX 88 kb)


  1. Akaike, H. (1973). Information theory as an extension of the maximum likelihood principle. In B. N. Petrov & F. Csaki (Eds.), Second international symposium on information theory (pp. 267–281). Budapest: Akademiai Kiado.Google Scholar
  2. Andresen, E. (2001). Effects of dung presence, dung amount and secondary dispersal by dung beetles on the fate of Micropholis guyanensis (Sapotaceae) seeds in Central Amazonia. Journal of Tropical Ecology, 17(1), 61–78.CrossRefGoogle Scholar
  3. Andresen, E., & Feer, F. (2005). The role of dung beetles as secondary seed dispersers and their effect on plant regeneration in tropical rainforests (432, Trans.). In P.-M. Forget, J. E. Lambert, P. E. Hulme, & S. B. Vander Wall (Eds.), Seed fate: Predation, dispersal and seedling establishment (pp. 331–349). Wallingford: CAB International.CrossRefGoogle Scholar
  4. Andresen, E., & Levey, D. J. (2004). Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia, 139, 45–54.CrossRefPubMedGoogle Scholar
  5. Balcomb, S. R., & Chapman, C. A. (2003). Bridging the gap: Influence of seed deposition on seedling recruitment in a primate–tree interaction. Ecological Monographs, 73(4), 625–642.CrossRefGoogle Scholar
  6. Beaune, D., Bollache, L., Bretagnolle, F., & Fruth, B. (2012). Dung beetles are critical in preventing post-dispersal seed removal by rodents in Congo rain forest. Journal of Tropical Ecology, 28(5), 507–510.CrossRefGoogle Scholar
  7. Beckman, N. G., & Rogers, H. S. (2013). Consequences of seed dispersal for plant recruitment in tropical forests: Interactions within the seedscape. Biotropica, 45(6), 666–681.CrossRefGoogle Scholar
  8. Chambers, J. C., & MacMahon, J. A. (1994). A day in the life of a seed: Movements and fates of seeds and their implications for natural and managed systems. Annual Review of Ecology and Systematics, 25, 263–292.CrossRefGoogle Scholar
  9. Chapman, C. A. (1995). Primate seed dispersal: Coevolution and conservation implications. Evolutionary Anthropology, 4(3), 74–82.CrossRefGoogle Scholar
  10. Chapman, C. A., & Russo, S. E. (2006). Primate seed dispersal: Linking behavioral ecology with forest community structure. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & K. Bearder (Eds.), Primates in perspective (pp. 510–525). Oxford: Oxford University Press.Google Scholar
  11. Culot, L., Bello, C., Batista, J. L. F., do Couto, H. T. Z., & Galetti, M. (2017). Synergistic effects of seed disperser and predator loss on recruitment success and long-term consequences for carbon stocks in tropical rainforests. Scientific Reports, 7(1), 7662.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Culot, L., Huynen, M.-C., Gérard, P., & Heymann, E. W. (2009). Short-term post-dispersal fate of seeds defecated by two small primate species (Saguinus mystax and Saguinus fuscicollis) in the Amazonian forest of Peru. Journal of Tropical Ecology, 25(3), 229–238.CrossRefGoogle Scholar
  13. Culot, L., Huynen, M.-C., & Heymann, E. W. (2015). Partitioning the relative contribution of one-phase and two-phase seed dispersal when evaluating seed dispersal effectiveness. Methods in Ecology and Evolution, 6(2), 178–186.CrossRefGoogle Scholar
  14. Culot, L., Mann, D. J., Muñoz Lazo, F. J. J., Huynen, M.-C., & Heymann, E. W. (2011). Tamarins and dung beetles: An efficient diplochorous dispersal system for forest regeneration. Biotropica, 43(1), 84–92.CrossRefGoogle Scholar
  15. Culot, L., Muñoz Lazo, F. J. J., Huynen, M.-C., Poncin, P., & Heymann, E. W. (2010). Seasonal variation in seed dispersal by tamarins alters seed rain in a secondary rainforest. International Journal of Primatology, 31(4), 553–569.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Development Core Team, R. (2014). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing Scholar
  17. Dowsett-Lemaire, F. (1988). Fruit choice and seed dissemination by birds and mammals in the evergreen forests of upland Malawi. Terre et Vie, 43, 251–285.Google Scholar
  18. Encarnación, F. (1985). Introducción a la flora y vegetación de la Amazonía peruana: Estado actual de los estudios, medio natural y ensayo de una clave de determinación de las formaciones vegetales en la llanura amazónica. Candollea, 40, 237–252.Google Scholar
  19. Errouissi, F., Haloti, S., Jay-Robert, P., Janati-Idrissi, A., & Lumaret, J. (2004). Effects of the attractiveness for dung beetles of dung pat origin and size along a climatic gradient. Environmental Entomology, 33(1), 45–53.CrossRefGoogle Scholar
  20. Foster, S. A., & Janson, C. H. (1985). The relationship between seed size and establishment conditions in tropical woody plants. Ecology, 66(3), 773–780.CrossRefGoogle Scholar
  21. Fuzessy, L. F., Cornelissen, T. G., Janson, C., & Silveira, F. A. O. (2016). How do primates affect seed germination? A meta-analysis of gut passage effects on neotropical plants. Oikos, 125(8), 1069–1080.CrossRefGoogle Scholar
  22. Gallegos, S. C., Hensen, I., & Schleuning, M. (2014). Secondary dispersal by ants promotes forest regeneration after deforestation. Journal of Ecology, 102(3), 659–666.CrossRefGoogle Scholar
  23. Gautier-Hion, A., Duplantier, J. M., Quris, R., Feer, F., Sourd, C., et al (1985). Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia, 65(3), 324–337.CrossRefPubMedGoogle Scholar
  24. Gross-Camp, N., & Kaplin, B. A. (2011). Differential seed handling by two African primates affects seed fate and establishment of large-seeded trees. Acta Oecologica, 37(6), 578–586.CrossRefGoogle Scholar
  25. Hanski, I., & Cambefort, Y. (1991). Dung beetle ecology. Princeton: Princeton University Press.CrossRefGoogle Scholar
  26. Heiberger, R. M. (2017). HH: Statistical analysis and data display: Heiberger and Holland. R package version, 3, 1–34 Scholar
  27. Heymann, E. W. (1990). Interspecific relations in a mixed-species troop of moustached tamarins, Saguinus mystax, and saddle-back tamarins, Saguinus fuscicollis (Platyrrhini:Callitrichidae), at the Rio Blanco, Peruvian Amazonia. American Journal of Primatology, 21(2), 115–127.CrossRefGoogle Scholar
  28. Heymann, E. W. (1995). Sleeping habits of tamarins, Saguinus mystax and Saguinus fuscicollis (Mammalia; Primates; Callitrichidae), in north-eastern Peru. Journal of Zoology, 237(2), 211–226.CrossRefGoogle Scholar
  29. Heymann, E. W., & Buchanan-Smith, H. M. (2000). The behavioural ecology of mixed-species troops of callitrichine primates. Biological Reviews, 75(2), 169–190.CrossRefPubMedGoogle Scholar
  30. Heymann, E. W., Knogge, C., & Tirado Herrera, E. R. (2000). Vertebrate predation by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis. American Journal of Primatology, 51(2), 153–158.CrossRefPubMedGoogle Scholar
  31. Heymann, E. W., Wörner, L. L. B., Ziegenhagen, B., & Bialozyt, R. (2014). Research trails affect the abundance of an epiphytic tropical bromeliad. Biotropica, 46, 166–169.CrossRefGoogle Scholar
  32. Hothorn, T., Hornik, K., van de Wiel, M. A., & Zeileis, A. (2008). Implementing a class of permutation tests: The coin package. Journal of Statistical Software, 28(8), 1–23.Google Scholar
  33. Johnson, J. B., & Omland, K. S. (2004). Model selection in ecology and evolution. Trends in Ecology & Evolution, 19(2), 101–108.CrossRefGoogle Scholar
  34. Kitajima, K., & Fenner, M. (2000). Ecology of seedling regeneration. In M. Fenner (Ed.), Seeds: The ecology of regeneration in plant communities (pp. 331–359). Wallingford: CAB International.CrossRefGoogle Scholar
  35. Knogge, C., & Heymann, E. W. (2003). Seed dispersal by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis: Diversity and characteristics of plant species. Folia Primatologica, 74(1), 33–47.CrossRefGoogle Scholar
  36. Kupsch, D., Waltert, M., & Heymann, E. (2014). Forest type affects prey foraging of saddleback tamarins, Saguinus nigrifrons. Primates, 55(3), 403–413.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lawson, C. R., Mann, D. J., & Lewis, O. T. (2012). Dung beetles reduce clustering of tropical tree seedlings. Biotropica, 44(3), 271–275.CrossRefGoogle Scholar
  38. Leishman, M., Wright, I., Moles, A., & Westoby, M. (2000). The evolutionary ecology of seed size. In M. Fenner (Ed.), Seeds: The ecology of regeneration in plant communities (pp. 31–57). Wallingford: CAB International.CrossRefGoogle Scholar
  39. Levey, D. J. (1987). Seed size and fruit-handling techniques of avian frugivores. The American Naturalist, 129(4), 471–485.CrossRefGoogle Scholar
  40. Lugon, A. P., Boutefeu, M., Bovy, E., Vaz-de-Mello, F. Z., Huynen, M.-C., Galetti, M., et al. (2017). Persistence of the effect of frugivore identity on post-dispersal seed fate: consequences for the assessment of functional redundancy. Biotropica, 49(3), 293–302.Google Scholar
  41. McConkey, K. R., & Brockelman, W. Y. (2011). Nonredundancy in the dispersal network of a generalist tropical forest tree. Ecology, 92(7), 1492–1502.CrossRefPubMedGoogle Scholar
  42. McNair, J. N., Sunkara, A., & Frobish, D. (2012). How to analyse seed germination data using statistical time-to-event analysis: Non-parametric and semi-parametric methods. Seed Science Research, 22(2), 77–95.CrossRefGoogle Scholar
  43. Nathan, R., & Muller-Landau, H. (2000). Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology & Evolution, 15(7), 278–285.CrossRefGoogle Scholar
  44. Nickle, D. A., & Heymann, E. W. (1996). Predation on Orthoptera and other orders of insects by tamarin monkeys, Saguinus mystax mystax and Saguinus fuscicollis nigrifrons (Primates: Callitrichidae), in north-eastern Peru. Journal of Zoology, 239(4), 799–819.CrossRefGoogle Scholar
  45. Peres, C. A. (1993). Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and moustached (S. mystax) tamarins in an Amazonian terra firme forest. Journal of Zoology, 230(4), 567–592.CrossRefGoogle Scholar
  46. Pons, T. L. (2000). Seed responses to light. In M. Fenner (Ed.), Seeds: The ecology of regeneration in plant communities (pp. 237–260). Wallingford: CAB International.CrossRefGoogle Scholar
  47. Razafindratsima, O. H., & Dunham, A. E. (2014). Assessing the impacts of nonrandom seed dispersal by multiple frugivore partners on plant recruitment. Ecology, 96(1), 24–30.CrossRefGoogle Scholar
  48. Santos-Heredia, C., Andresen, E., & Zárate, D. A. (2010). Secondary seed dispersal by dung beetles in a Colombian rain forest: Effects of dung type and defecation pattern on seed fate. Journal of Tropical Ecology, 26, 355–364.CrossRefGoogle Scholar
  49. Schupp, E. W. (1993). Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio, 107(108), 15–29.Google Scholar
  50. Schupp, E. W., Jordano, P., & Gómez, J. M. (2010). Seed dispersal effectiveness revisited: A conceptual review. New Phytologist, 188(2), 333–353.CrossRefPubMedGoogle Scholar
  51. Shepherd, V. E., & Chapman, C. A. (1998). Dung beetles as secondary seed dispersers: Impact on seed predation and germination. Journal of Tropical Ecology, 14, 199–215.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. Soini, P., & Coppula, M. (1981). Ecología y dinámica poblacional de pichico Saguinus fuscicollis (Primates, Callitrichidae). Informe de Pacaya, 4, 1–43.Google Scholar
  54. Soini, P., & Soini, M. (1982). Distribución geográfica y ecología poblacional de Saguinus mystax (Primates, Callitrichidae). Informe de Pacaya, 6, 1–56.Google Scholar
  55. Stevenson, P. R. (2011). Pulp–seed attachment is a dominant variable explaining legitimate seed dispersal: A case study on woolly monkeys. Oecologia, 166, 693–701.CrossRefPubMedGoogle Scholar
  56. Stiles, E. (2000). Animals as seed dispersers. In M. Fenner (Ed.), Seeds: The ecology of regeneration in plant communities (pp. 111–124). Wallingford, UK: CAB International.CrossRefGoogle Scholar
  57. Therneau, T. (2014). A Package for Survival Analysis in S. R package version, 2, 37–37 Scholar
  58. Traveset, A., Bermejo, T., & Willson, M. (2001). Effect of manure composition on seedling emergence and growth of two common shrub species of Southeast Alaska. Plant Ecology, 155, 29–34.CrossRefGoogle Scholar
  59. Traveset, A., Robertson, A. W., & Rodríguez-Pérez, J. (2007). A review on the role of endozoochory in seed germination. In A. J. Dennis, E. W. Schupp, R. J. Green, & D. A. Westcott (Eds.), Seed dispersal: Theory and its application in a changing world (pp. 78–103). Wallingford: CAB International.CrossRefGoogle Scholar
  60. Vander Wall, S. B., & Longland, W. S. (2004). Diplochory: Are two seed dispersers better than one? Trends in Ecology & Evolution, 19(3), 155–161.CrossRefGoogle Scholar
  61. Vulinec, K. (2000). Dung beetles (Coleoptera: Scarabaeidae), monkeys, and conservation in Amazonia. Florida Entomologist, 83(3), 229–241.CrossRefGoogle Scholar
  62. Wang, B. C., & Smith, T. B. (2002). Closing the seed dispersal loop. Trends in Ecology & Evolution, 17(8), 379–385.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratório de Primatologia, Departamento de Zoologia, Instituto de BiociênciasUniversidade Estadual Paulista (UNESP)Rio ClaroBrazil
  2. 2.Behavioral Biology Unit, Primatology Research GroupUniversity of LiègeLiègeBelgium
  3. 3.Abteilung Verhaltensökologie & Soziobiologie, Deutsches Primatenzentrum (DPZ)GöttingenGermany

Personalised recommendations