, Volume 172, Issue 3, pp 857–867

Consumer preference for seeds and seedlings of rare species impacts tree diversity at multiple scales

  • Hillary S. Young
  • Douglas J. McCauley
  • Roger Guevara
  • Rodolfo Dirzo
Plant-animal interactions - Original research


Positive density-dependent seed and seedling predation, where herbivores selectively eat seeds or seedlings of common species, is thought to play a major role in creating and maintaining plant community diversity. However, many herbivores and seed predators are known to exhibit preferences for rare foods, which could lead to negative density-dependent predation. In this study, we first demonstrate the occurrence of increased predation of locally rare tree species by a widespread group of insular seed and seedling predators, land crabs. We then build computer simulations based on these empirical data to examine the effects of such predation on diversity patterns. Simulations show that herbivore preferences for locally rare species are likely to drive scale-dependent effects on plant community diversity: at small scales these foraging patterns decrease plant community diversity via the selective consumption of rare plant species, while at the landscape level they should increase diversity, at least for short periods, by promoting clustered local dominance of a variety of species. Finally, we compared observed patterns of plant diversity at the site to those obtained via computer simulations, and found that diversity patterns generated under simulations were highly consistent with observed diversity patterns. We posit that preference for rare species by herbivores may be prevalent in low- or moderate-diversity systems, and that these effects may help explain diversity patterns across different spatial scales in such ecosystems.


Plant–herbivore interactions Plant diversity Density dependence Seed predation Seedling predation 

Supplementary material

442_2012_2542_MOESM1_ESM.docx (1.3 mb)
Supplementary material 1 (DOCX 1320 kb)


  1. Adler PB, Ellner SP, Levine JM (2010) Coexistence of perennial plants: an embarrassment of niches. Ecol Lett 13:1019–1029PubMedGoogle Scholar
  2. Allen JA, Anderson KP (1984) Selection by passerine birds is anti-apostatic at high prey densities. Biol J Linn Soc 23:237–246CrossRefGoogle Scholar
  3. Allen JA, Weale ME (2004) Anti-apostatic selection by wild birds on quasi-natural morphs of the land snail Cepaea hortensis: a generalized mixed models approach. Oecologia 108:335–343Google Scholar
  4. Bagchi R, Swinfield T, Gallery RE, Lewis OT, Gripenberg S, Narayan L, Freckleton RP (2010) Testing the Janzen–Connell mechanism: pathogens cause overcompensating density dependence in a tropical tree. Ecology 13:1262–1269Google Scholar
  5. Burger AE (2005) Dispersal and germination of seeds of Pisonia grandis, an Indo-Pacific tropical tree associated with insular seabird colonies. J Trop Ecol 21:263–271CrossRefGoogle Scholar
  6. Carson WP, Anderson JT, Leigh EG, Schnitzer SA (2008) Challenges associated with testing and falsifying the Janzen–Connell hypothesis: a review and critique. In: Carson WP, Schnitzer SA (eds) Tropical forest ecology. Wiley–Blackwell, Oxford, pp 210–241Google Scholar
  7. Chen L, Mi XC, Comita LS, Zhang LW, Ren HB, Ma KP (2010) Community-level consequences of density dependence and habitat association in a subtropical broad-leaved forest. Ecol Lett 13:695–704PubMedCrossRefGoogle Scholar
  8. Clark DA, Clark DB (1984) Spacing dynamics of a tropical rainforest tree: evaluation of the Janzen–Connell model. Am Nat 124:769–788CrossRefGoogle Scholar
  9. Clarke PJ, Kerrigan RA (2002) The effects of seed predators on the recruitment of mangroves. J Ecol 90:728–736CrossRefGoogle Scholar
  10. Comita LS, Muller-Landau HC, Aguilar S, Hubbell SP (2010) Asymmetric density dependence shapes species abundances in a tropical tree community. Science 5989:330–332CrossRefGoogle Scholar
  11. Condit R, Pitman N, Leigh EG, Chave J, Terborgh J, Foster RB, Núňez P, Aguilar S, Valencia R, Villa G, Muller-Landau HC, Losos E, Hubbell SP (2002) Beta-diversity in tropical forest trees. Science 295:666–669PubMedCrossRefGoogle Scholar
  12. Connell J (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: Boer PD, Gradwell G (eds) Dynamics of populations. Center for Agriculture Publishing and Documentation, Wageningen, pp 283–313Google Scholar
  13. Cottam DA (1985) Frequency-dependent grazing by slugs and grasshoppers. J Ecol 73:925–933CrossRefGoogle Scholar
  14. Gentry AH (1982) Patterns of neotropical plant species diversity. Evol Biol 15:1–84CrossRefGoogle Scholar
  15. Green PT, O’Dowd DJ, Lake PS (1997) Control of seedling recruitment by land crabs in rain forest on a remote oceanic island. Ecology 78:2474–2486CrossRefGoogle Scholar
  16. Harms KE, Wright SJ, Calderón O, Hernández A, Herre EA (2000) Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404:493–495PubMedCrossRefGoogle Scholar
  17. Hassell MB (1984) Parasitism in patchy environments: inverse density dependence can be stabilizing. Math Med Biol 1:123–133CrossRefGoogle Scholar
  18. Hubbell SP, Ahumada JA, Condit R, Foster RB (2001) Local neighborhood effects on long-term survival of individual trees in a neotropical forest. Ecol Res 16:859–875CrossRefGoogle Scholar
  19. Ives AR, Carpenter SR (2007) Stability and diversity of ecosystems. Science 317:58–62PubMedCrossRefGoogle Scholar
  20. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528CrossRefGoogle Scholar
  21. Kreft H, Jetz W (2007) Global patterns and determinants of vascular plant diversity. Proc Natl Acad Sci USA 104:5925–5930PubMedCrossRefGoogle Scholar
  22. Lindquist ES, Carroll CR (2004) Differential seed and seedling predation by crabs: impacts on tropical coastal forest composition. Oecologia 141:661–671PubMedCrossRefGoogle Scholar
  23. Lindquist ES, Krauss KW, Green PT, O’Dowd DJ, Sherman PM, Smith TJ (2009) Land crabs as key drivers in tropical coastal forest recruitment. Biol Rev 84:203–223PubMedCrossRefGoogle Scholar
  24. Molino JF, Sabatier D (2001) Tree diversity in tropical rain forests: a validation of the intermediate disturbance hypothesis. Science 294:1702–1704PubMedCrossRefGoogle Scholar
  25. Molofsky J, Durrett R, Dushoff J, Griffeath D (1999) Local frequency dependence and global coexistence. Theor Popul Biol 55:270–282PubMedCrossRefGoogle Scholar
  26. O’Dowd DJ, Lake PS (1991) Red crabs in rain forest, Christmas Island: removal and fate of fruits and seeds. J Trop Ecol 7:113–122CrossRefGoogle Scholar
  27. Phillips O, Miller JS (2002) Global patterns of plant biodiversity. In: Alwyn H (ed) Gentry forest transect dataset. Missouri Botanical Garden Press, St. LouisGoogle Scholar
  28. Ricklefs RE, Schluter D (1993) Species diversity in ecological communities: historical and geographical perspectives. University of Chicago Press, ChicagoGoogle Scholar
  29. Schupp EW (1992) The Janzen–Connell model for tropical tree diversity: population implications and the importance of spatial scale. Am Nat 140:526–530PubMedCrossRefGoogle Scholar
  30. Sherman PM (2002) Effects of land crabs on seedling densities and distributions in a mainland neotropical rain forest. J Trop Ecol 18:67–89CrossRefGoogle Scholar
  31. Smith TJ (1987) Seed predation in relation to tree dominance and distribution in mangrove forests. Ecology 68:266–273CrossRefGoogle Scholar
  32. Smith BH, deRivera CE, Bridgman CL, Woida JJ (1989) Frequency-dependent seed dispersal by ants of two deciduous forest herbs. Ecology 70:1645–1648Google Scholar
  33. Swamy V, Terborgh JW (2010) Distance-responsive natural enemies strongly influence seedling establishment patterns of multiple species in an Amazonian rain forest. J Ecol 98:1096–1107CrossRefGoogle Scholar
  34. Terborgh J (2012) Enemies maintain hyperdiverse tropical forests. Am Nat 179:303–314PubMedCrossRefGoogle Scholar
  35. Thacker RW (1996) Food choices of land hermit crabs (Coenobita compressus H Milne Edwards) depend on past experience. J Exp Mar Biol Ecol 199:179–191CrossRefGoogle Scholar
  36. Visser MD, Muller-Landau HC, Wright SJ, Rutten G, Jansen PA (2011) Tri-trophic interactions affect density dependence of seed fate in a tropical forest palm. Eco Lett 14:1093–1100CrossRefGoogle Scholar
  37. Volkov I, Banavar J, He F, Hubbell SP, Maritan A (2005) Density dependence explains tree species abundance and diversity in tropical forests. Nature 438:658–661PubMedCrossRefGoogle Scholar
  38. Wester L (1985) Checklist of the vascular plants of the northern Line Islands. Atoll Res Bull 287:1–38CrossRefGoogle Scholar
  39. Wills C, Harms KE, Condit R, King D, Thompson J, He F, Muller-Landau HC, Ashton P, Losos E, Comita L, Hubbell S, Lafrankie J, Bunyavejchewin S, Dattaraja HS, Davies S, Esufali S, Foster R, Gunatilleke N, Gunatilleke S, Hall P, Itoh A, John R, Kiratiprayoon S, de Lao SL, Massa M, Nath C, Noor MN, Kassim AR, Sukumar R, Suresh HS, Sun IF, Tan S, Yamakura T, Zimmerman J (2006) Nonrandom processes maintain diversity in tropical forests. Science 311:527–531Google Scholar
  40. Wright SJ (2002) Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130:1–14Google Scholar
  41. Young HS, McCauley DJ, Dunbar RB, Dirzo R (2010a) Plants cause ecosystem nutrient depletion via the interruption of bird-derived spatial subsidies. Proc Natl Acad Sci USA 107:2072–2077PubMedCrossRefGoogle Scholar
  42. Young HS, Raab TK, McCauley DJ, Briggs AA, Dirzo R (2010b) The coconut palm, Cocos nucifera, impacts forest composition and soil characteristics at Palmyra Atoll, Central Pacific. J Veg Sci 21:1058–1068CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Hillary S. Young
    • 1
    • 2
    • 3
  • Douglas J. McCauley
    • 4
  • Roger Guevara
    • 5
  • Rodolfo Dirzo
    • 1
  1. 1.Department of BiologyStanford UniversityStanfordUSA
  2. 2.Division of Vertebrate ZoologySmithsonian InstitutionWashingtonUSA
  3. 3.Center for the EnvironmentHarvard UniversityCambridgeUSA
  4. 4.Hopkins Marine StationStanford UniversityPacific GroveUSA
  5. 5.Red de Biología EvolutivaInstituto de Ecología ACVeracruzMexico

Personalised recommendations