Plants can influence the source and severity of seed predation through various mechanisms; the use of secondary metabolites for chemical defense, for example, is well documented. Gut passage by frugivores can also reduce mortality of animal-dispersed seeds, although this mechanism has gained far less attention than secondary metabolites. Apart from influencing the severity of seed predation, gut passage may also influence the source of seed predation. In Bolivia, we compared impacts of these two mechanisms, gut passage and secondary metabolites, on the source of seed predation in Capsicum chacoense, a wild chili species that is polymorphic for pungency (individual plants either produce fruits and seeds containing or lacking capsaicinoids). Using physical exclosures, we isolated seed removal by insects, mammals, and birds; seeds in the trials were from either pungent or non-pungent fruits and were either passed or not passed by seed-dispersing birds. Pungency had little influence on total short-term seed removal by animals, although prior work on this species indicates that capsaicin reduces mortality caused by fungi at longer time scales. Gut passage strongly reduced removal by insects, altering the relative impact of the three predator types. The weak impact of pungency on short-term predation contrasts with previous studies, highlighting the context dependence of secondary metabolites. The strong impact of gut passage demonstrates that this mechanism alone can influence which seed predators consume seeds, and that impacts of gut passage can be larger than those of secondary metabolites, which are more commonly acknowledged as a defense mechanism.
Frugivory Granivory Chemical defense Mutualism Seed fate
This is a preview of subscription content, log in to check access.
We thank Uco Sapag Ruta, Don Odon, and many others for field assistance. This research was supported by National Science Foundation grant DEB 0129168 (to D. L. and J. T.), National Geographic Society grants (to J. T. and D. L.), and a National Science Foundation Graduate Research Fellowship (to E. F.). Logistical support in Bolivia was provided by Fundación Amigos de la Naturaleza and the Wildlife Conservation Society.
Author contribution statement
D. L., J. T., and D. H. designed the experiments. J. T. and D. H. conducted the field experiments. E. F. performed the statistical analyses and wrote the first draft of the manuscript. All authors revised the manuscript.
Bagchi R, Gallery RE, Gripenberg S, Gurr SJ, Narayan L, Addis CE, Freckleton RP, Lewis OT (2014) Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506:85–88CrossRefPubMedGoogle Scholar
Crawley MJ (1992) Seed predators and plant population dynamics. In: Fenner M (ed) Seeds, the ecology of regeneration in plant communities. CAB International, Wallingford, pp 157–191Google Scholar
Fedriani JM, Delibes M (2013) Pulp feeders alter plant interactions with subsequent animal associates. J Ecol 101:1581–1588CrossRefGoogle Scholar
Fedriani JM, Zywiec M, Delibes M (2012) Thieves or mutualists? Pulp feeders enhance endozoochore local recruitment. Ecology 93:575–587CrossRefPubMedGoogle Scholar
Fricke EC, Simon MJ, Reagan KM, Levey DJ, Riffell JA, Carlo TA, Tewksbury JJ (2013) When condition trumps location: seed consumption by fruit-eating birds removes pathogens and predator attractants. Ecol Lett 16:1031–1036CrossRefPubMedPubMedCentralGoogle Scholar
Fricke EC, Tewksbury JJ, Rogers HS (2014) Multiple natural enemies cause distance-dependent mortality at the seed-to-seedling transition. Ecol Lett 17:593–598CrossRefPubMedGoogle Scholar
Tewksbury JJ, Manchego C, Haak DC, Levey DJ (2006) Where did the chili get its spice? Biogeography of capsaicinoid production in ancestral wild chili species. J Chem Ecol 32(547):564Google Scholar
Tewksbury JJ, Levey DJ, Huizinga M, Haak DC (2008a) Costs and benefits of capsaicin-mediated control of gut retention in dispersers of wild chilies. Ecology 89:107–117CrossRefPubMedGoogle Scholar
Tewksbury JJ, Reagan KM, Machnicki NJ, Carlo TA, Haak DC, Peñaloza ALC, Levey DJ (2008b) Evolutionary ecology of pungency in wild chilies. Proc Natl Acad Sci USA 105:11808–11811CrossRefPubMedPubMedCentralGoogle Scholar
Traveset A, Robertson A, Rodríguez-Pérez J (2007) A review on the role of endozoochory on seed germination. In: Dennis AJ, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CABI, Wallingford, UK, pp 78–103CrossRefGoogle Scholar
Vander Wall SB (2003) Effect of seed size of wind-dispersed pines (Pinus) on secondary seed dispersal and the caching behavior of rodents. Oikos 100:23–24CrossRefGoogle Scholar