Primates and Dung Beetles: Two Dispersers Are Better than One in Secondary Forest
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.
KeywordsContext 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Schupp, E. W. (1993). Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio, 107(108), 15–29.Google Scholar
- Soini, P., & Coppula, M. (1981). Ecología y dinámica poblacional de pichico Saguinus fuscicollis (Primates, Callitrichidae). Informe de Pacaya, 4, 1–43.Google Scholar
- Soini, P., & Soini, M. (1982). Distribución geográfica y ecología poblacional de Saguinus mystax (Primates, Callitrichidae). Informe de Pacaya, 6, 1–56.Google Scholar
- 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