Distance-responsive natural enemies strongly influence seedling establishment patterns of multiple species in an Amazonian rain forest

Journal of Ecology

Volumn 98, Issue 5, 2010, Pages 1096-1107

  Swamy, Varun ^a   Terborgh, John W ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Amazonia; Density dependence; Distance dependence; Host specificity; Janzen Connell model; Peru; Seed dispersal; Seedling survival; Tree recruitment; Tropical rain forest

Indexed keywords

CONSPECIFIC; DENSITY DEPENDENCE; HOST SPECIFICITY; MORTALITY; NATURAL ENEMY; RAINFOREST; RECRUITMENT (POPULATION DYNAMICS); SEED DISPERSAL; SEEDLING ESTABLISHMENT; UNDERSTORY;

AMAZONAS [PERU]; PERU;

EID: 77955410162     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/j.1365-2745.2010.01686.x     Document Type: Article

References (70)

1. Alvarez P, White J, Gil N, Svenning J-C, Balslev H, Kristiansen T. Light converts endosymbiotic fungus to pathogen, influencing seedling survival and host tree recruitment. Nature Precedings 2008, http://hdl.handle.net/10101/npre.2008.1908.1, DOI:
2. Antonovics J, Levin DA. The ecological and genetic consequences of density-dependent regulation in plants. Annual Review of Ecology and Systematics 1980, 11:411-452.
3. Augspurger CK. Seed dispersal of the tropical tree Platypodium elegans and the escape of its seedlings from fungal pathogens. Journal of Ecology 1983, 71:759-771.
4. Augspurger CK. Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps and pathogens. Ecology 1984, 65:1705-1712.
5. Augspurger CK, Kelly CK. Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 1984, 61:211-217.
6. Bagchi R, Press MC, Scholes JD. Evolutionary history and distance dependence control survival of dipterocarp seedlings. Ecology Letters 2009, 12:1-9.
7. Bell T, Freckleton RP, Lewis OT. Plant pathogens drive density-dependent seedling mortality in a tropical tree. Ecology Letters 2006, 9:569-574.
8. Brown N, Jennings S, Wheeler P, Nabe-Nielsen J. An improved method for the rapid assessment of forest understorey light environments. Journal of Applied Ecology 2000, 37:1044-1053.
9. Burkey TV. Tropical tree species diversity: a test of the Janzen-Connell model. Oecologia 1994, 97:533-540.
10. Carson WP, Anderson J, Leigh E, Schnitzer SA. Challenges associated with testing and falsifying the Janzen-Connell hypothesis: a review and critique. Tropical Forest Community Ecology 2008, 210-241. Carson WP, Schnitzer SA, eds, pp, Blackwell Publishing, Oxford
11. Cintra R. A test of the Janzen-Connell model with two common tree species in Amazonian forest. Journal of Tropical Ecology 1997, 13:641-658.
12. Cintra R, Horna V. Seed and seedling survival of the palm Astrocaryum murumuru and the legume tree Dipteryx micrantha in gaps in Amazonian forest. Journal of Tropical Ecology 1997, 13:257-277.
13. Clark DA, Clark DB. Spacing dynamics of a tropical rain forest tree: evaluation of the Janzen-Connell model. American Naturalist 1984, 124:769-788.
14. Clark DA, Clark DB. Seedling dynamics of a tropical tree: impacts of herbivory and meristem damage. Ecology 1989, 66:1884-1892.
15. Comita LS, Hubbell SP. Local neighborhood and species' shade tolerance influence survival in a diverse seedling bank. Ecology 2009, 90:328-334.
16. Condit R, Hubbell SP, Foster RB. Recruitment near conspecific adults and the maintenance of tree and shrub diversity in a neotropical forest. The American Naturalist 1992, 140:261-286.
17. Condit R, Hubbell SP, Foster RB. Density dependence in two understorey tree species in a neotropical forest. Ecology 1994, 75:671-680.
18. Condit R, Ashton PS, Baker P, Bunyavejchewin S, Gunatilleke S, Gunatilleke N. Spatial patterns in the distribution of tropical tree species. Science 2000, 288:1414-1418.
19. Connell JH. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Dynamics of Populations 1971, 298-312. Boer PJDGradwell G. eds, pp, Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands
20. Curio E, Reiter J, Tacud B, Urbina H, Fink-Schabacker C. Seedling mortality of six Philippine rain forest tree species: a test of the 'escape hypothesis'. Ecotropica 2003, 9:59-70.
21. HemiView Canopy Analysis Software Version 2.1 1999, University of Kansas Center for Research, Inc., Lawrence, Kansas, KS, USA
22. ArcGIS Version 9.1 2005, Environmental Systems Research Inc., Redland, California, CA, USA
23. Fleming TH, Harrington DP. Nonparametric estimation of the survival distribution in censored data. Communications in Statistics 1984, 13:2469-2486.
24. Fragoso JMV. Tapir-generated seed shadows: scale-dependent patchiness in the Amazon rain forest. Journal of Ecology 1997, 85:519-529.
25. Fragoso JMV, Silvius KM, Correa JA. Long-distance seed dispersal by tapirs increases seed survival and aggregates tropical trees. Ecology 2003, 84:1998-2006.
26. Freckleton RP, Lewis OT. Pathogens, density dependence and the coexistence of tropical trees. Proceedings of the Royal Society of London. Series B, Biological Sciences 2006, 273:2909-2916.
27. Gentry AG. Four Neotropical Rainforests 1990, Yale University Press, New Haven, CT, USA
28. Gilbert GS, Foster RB, Hubbell SP. Density and distance-to-adult effects of a canker disease of trees in a moist tropical forest. Oecologia 1994, 98:100-108.
29. Grubb PJ. The maintenance of species richness in plant communities: the importance of the regeneration niche. Biological Review 1977, 52:107-145.
30. Hammond DS, Brown VK. Disturbance, phenology and life-history characteristics: factors influencing distance/density-dependent attack on tropical seeds and seedlings. Dynamics of Tropical Communities 1998, 51-78. Newbery DM, Prins HHTBrown ND. eds, pp, Blackwell Science, Oxford
31. Harms KE, Powers JS, Montgomery RA. Variation in small sapling density, understory cover, and resource availability in four neotropical forests. Biotropica 2004, 36:40-51.
32. Harms KE, Wright SJ, Calderon O, Hernandez A, Herre EA. Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 2000, 404:493-495.
33. Harrington DP, Fleming TR. A class of rank test procedures for censored survival data. Biometrika 1982, 69:553-566.
34. Hollander M, Wolfe DA. Nonparametric Statistical Methods 1973, 68-75. John Wiley & Sons, New York, pp
35. Howe HF. Survival and growth of juvenile Virola surnamensis in Panama: effects of herbivory and canopy closure. Journal of Tropical Ecology 1990, 6:259-280.
36. Howe HF, Schupp EW, Westley LC. Early consequences of seed dispersal for a neotropical tree (Virola surinamensis). Ecology 1985, 66:781-791.
37. Hubbell SH. Tree dispersion, abundance, and diversity in a tropical dry forest. Science 1979, 203:1299-1309.
38. Hubbell SP, Condit R, Foster RB. Presence and absence of density dependence in a neotropical tree community. Philosophical Transactions of the Royal Society of London B 1990, 330:269-281.
39. Hubbell SP, Foster RB. Biology, chance, and history and the structure of tropical rain forest tree communities. Community Ecology 1986, 314-329. Diamond M, Case T. eds, pp, Harper and Row, New York, NY, USA
40. Hubbell SP, Foster RB, O'Brien ST, Harms KE, Condit R, Wechsler B, Wright SJ, Loo de Lao S. Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science 1999, 283:554-557.
41. Hyatt LA, Rosenberg MS, Howard TG, Bole G, Fang W, Anastasia J, Brown K, Grella R, Hinman K, Kurdziel JP, Gurevitch J. The distance dependence prediction of the Janzen-Connell hypothesis: a meta-analysis. Oikos 2003, 103:590-602.
42. Janzen DH. Herbivores and the number of tree species in tropical forests. American Naturalist 1970, 104:501-528.
43. Janzen DH. Escape in space by Sterculia apetala seeds from the bug Dysdercus fasciatus in a Costa Rican deciduous forest. Ecology 1972, 53:350-361.
44. Lopez L, Terborgh J. Seed predation and seedling herbivory as factors in tree recruitment failure on predator-free forested islands. Journal of Tropical Ecology 2007, 23:129-137.
45. Newcombe RG. Two-sided confidence intervals for the single proportion: comparison of seven methods. Statistics in Medicine 1998a, 17:857-872.
46. Newcombe RG. Interval estimation for the difference between independent proportions: comparison of eleven methods. Statistics in Medicine 1998b, 17:873-890.
47. Packer A, Clay K. Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 2000, 404:278-281.
48. Paine CET, Harms KE, Schnitzer SA, Carson WP. Weak competition among tropical tree seedlings: implications for species coexistence. Biotropica 2008, 40:432-440.
49. Peters HA. Neighbour-regulated mortality: the influence of positive and negative density dependence on tree populations in species-rich tropical forests. Ecology Letters 2003, 6:757-765.
50. Pigot AL, Leather SR. Invertebrate predators drive distance-dependent patterns of seedling mortality in a temperate tree Acer pseudoplatanus. Oikos 2008, 117:521-530.
51. Queenborough SA, Burslem DFRP, Garwood NC, Valencia R. Neighborhood and community interactions determine the spatial pattern of tropical tree seedling survival. Ecology 2007, 88:2248-2258.
52. R: A Language and Environment for Statistical Computing, Reference Index Version 2.6.4 2008, http://www.R-project.org, R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0, Available at:
53. Ruibo L, Shixiao Y, Yongfan W, Christian S, Runguo Z. Distance-dependent effects of soil-derived biota on seedling survival of the tropical tree legume Ormosia semicastrata. Journal of Vegetation Science 2009, 20:527-534.
54. Schupp EW. The Janzen-Connell model for tropical tree diversity: population implications and the importance of spatial scale. American Naturalist 1992, 140:526-530.
55. Silman MR. Regeneration from seed in a neotropical rainforest 1996, PhD thesis, Duke University, USA
56. Steidl RJ, Thomas L. Power analysis and experimental design. Design and Analysis of Ecological Experiments 2001, 14-36. Scheiner S, Gurevitch J. 2nd edn, eds, pp, Oxford University Press, New York, NY, USA
57. Svenning J, Fabbro T, Wright S. Seedling interactions in a tropical forest in Panama. Oecologia 2008, 155:143-150.
58. Terborgh J. Five New World Primates: A Study in Comparative Ecology 1983, Princeton University Press, Princeton, NJ, USA
59. Terborgh J, Foster RB, Núñez VP. Tropical tree communities: a test of the nonequilibrium hypothesis. Ecology 1996, 77:561-567.
60. Terborgh J, Losos E, Riley MP, Riley MB. Predation by vertebrates and invertebrates on the seeds of five canopy tree species of an Amazonian forest. Plant Ecology 1993, 107/108:375-386.
61. Terborgh J, Pitman NCA, Silman M, Schichter H, Núñez PV. Maintenance of tree diversity in tropical forests. Seed Dispersal and Frugivory: Ecology, Evolution and Conservation 2002, 1-17. Levey DJ, Silva WR, Galetti M, eds, pp, CAB International, Wallingford, UK
62. Terborgh J, Nuñez-Iturri G, Pitman NCA, Valverde FHC, Alvarez P, Swamy V, Pringle EG, Paine CET. Tree recruitment in an empty forest. Ecology 2008, 89:1757-1768.
63. Watkinson AR. Plant responses to crowding. Studies on Plant Demography: A Festschrift for John L. Harper 1985, 275-289. White J. ed, pp, Academic Press, London, England
64. Webb CO, Peart DR. Seedling density dependence promotes coexistence of Bornean rain forest trees. Ecology 1999, 80:2006-2017.
65. Wills C, Condit R, Foster RB, Hubbell SP. Strong density- and diversity-related effects help to maintain tree species diversity in a neotropical forest. Proceedings of the National Academy of Sciences, USA 1997, 94:1252-1257.
66. Wright SJ. The dispersion of eggs by a bruchid beetle among Scheelea palm seeds. Ecology 1983, 64:1016-1021.
67. Wright SJ. Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 2002, 130:1-14.
68. Yoda K, Kira T, Ogawa H, Hozumi K. Self-thinning in overcrowded pure stands under cultivated and natural conditions. Journal of Biology of Osaka City University 1963, 14:107-129.
69. Zimmerman JK, Thompson J, Brokaw N. Large tropical forest dynamics plots: testing explanations for the maintenance of species diversity. Tropical Forest Community Ecology 2008, 98-117. Carson WP, Schnitzer SA, eds, pp, Blackwell Publishing, Oxford
70. Zuidema PA, Boot RGA. Demography of the Brazil nut tree (Bertholletia excelsa) in the Bolivian Amazon: impact of seed extraction on recruitment and population dynamics. Journal of Tropical Ecology 2002, 18:1-31.