Advertisement

Oecologia

, Volume 181, Issue 3, pp 905–910 | Cite as

Gut passage and secondary metabolites alter the source of post-dispersal predation for bird-dispersed chili seeds

  • Evan C. Fricke
  • David C. Haak
  • Douglas J. Levey
  • Joshua J. Tewksbury
Plant-microbe-animal interactions - original research

Abstract

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.

Keywords

Frugivory Granivory Chemical defense Mutualism Seed fate 

Notes

Acknowledgments

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.

References

  1. 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
  2. Bates D, Maechler M, Bolker B, Walker S (2015) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-8. http://CRAN.R-project.org/package=lme4
  3. 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
  4. Fedriani JM, Delibes M (2013) Pulp feeders alter plant interactions with subsequent animal associates. J Ecol 101:1581–1588CrossRefGoogle Scholar
  5. Fedriani JM, Zywiec M, Delibes M (2012) Thieves or mutualists? Pulp feeders enhance endozoochore local recruitment. Ecology 93:575–587CrossRefPubMedGoogle Scholar
  6. 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
  7. 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
  8. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66CrossRefPubMedGoogle Scholar
  9. Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Evol Syst 13:201–228CrossRefGoogle Scholar
  10. Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Evol Syst 2:465–492CrossRefGoogle Scholar
  11. Lambert JE (2001) Red-tailed guenons (Cercopithecus ascanius) and Strychnos mitis: evidence for plant benefits beyond seed dispersal. Int J Primatol 22:189–201CrossRefGoogle Scholar
  12. Levey DJ, Tewksbury JJ, Cipollini ML, Carlo TA (2006) A field test of the directed deterrence hypothesis in two species of wild chili. Oecologia 150:61–68CrossRefPubMedGoogle Scholar
  13. Levin DA (1976) The chemical defenses of plants to pathogens and herbivores. Annu Rev Ecol Syst 7:121–159CrossRefGoogle Scholar
  14. Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc Biol Sci Ser B 273:2575–2584CrossRefGoogle Scholar
  15. Meyer GA, Witmer MC (1998) Influence of seed processing by frugivorous birds on germination success of three North American shrubs. Am Midl Nat 140:129–139CrossRefGoogle Scholar
  16. Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450CrossRefPubMedGoogle Scholar
  17. Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285CrossRefPubMedGoogle Scholar
  18. Noss CF, Levey DJ (2014) Does gut passage affect post-dispersal seed fate in a wild chili, Capsicum annuum? Southeast Nat 13:475–483CrossRefGoogle Scholar
  19. Orrock JL, Danielson BJ, Burns MJ, Levey DJ (2003) Spatial ecology of predator-prey interactions: corridors and patch shape influence seed predation. Ecology 84:2589–2599CrossRefGoogle Scholar
  20. Rosenthal GA, Berenbaum MR (1992) Herbivores: their interactions with secondary plant metabolites. Ecological and evolutionary processes, vol II, 2nd edn. Academic PressGoogle Scholar
  21. Samuel IA, Levey DJ (2005) Effects of gut passage on seed germination: do experiments answer the questions they ask? Funct Ecol 19:365–368CrossRefGoogle Scholar
  22. Tewksbury JJ, Nabhan C (2001) Seed dispersal: directed deterrence by capsaicin in chillies. Nature 412:403–404CrossRefPubMedGoogle Scholar
  23. 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
  24. 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
  25. 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
  26. 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
  27. 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

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Evan C. Fricke
    • 1
  • David C. Haak
    • 2
  • Douglas J. Levey
    • 3
  • Joshua J. Tewksbury
    • 4
    • 5
    • 6
  1. 1.Department of Ecology, Evolution, and Organismal BiologyIowa State UniversityAmesUSA
  2. 2.Department of Plant Pathology, Physiology, and Weed ScienceVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  3. 3.Division of Environmental BiologyNational Science FoundationArlingtonUSA
  4. 4.Colorado Global Hub, Future EarthBoulderUSA
  5. 5.Sustainability, Energy and Environment ComplexUniversity of ColoradoBoulderUSA
  6. 6.School of Global Environmental StudiesColorado State UniversityFort CollinsUSA

Personalised recommendations