Plant Ecology

, Volume 193, Issue 2, pp 211–222

Seed characteristics and susceptibility to pathogen attack in tree seeds of the Peruvian Amazon

  • Elizabeth G. Pringle
  • Patricia Álvarez-Loayza
  • John Terborgh
Original Article

Abstract

Many studies now suggest that pathogens can cause high levels of mortality in seeds and seedlings. Recruitment from seed to sapling is an important bottleneck for many tree species, and if specialist or generalist pathogens have differential negative effects among species of juvenile trees, then they may have a significant impact on forest community structure. To explore the effects of differential pathogen attack among tropical tree species, we quantified pathogen attack on the seeds of 16 tree species from the southeastern Peruvian Amazon and asked which seed characteristics, including size, hardness, germination time and mode, shade tolerance, and fruit type, were most closely correlated with susceptibility to pathogens. Shade tolerance and seed weight were positively and significantly correlated with susceptibility to pathogen attack by ecological trait regressions (ETRs), and correspondence analysis indicated that there might be increased attack rates in species with brightly colored, pulpy fruits (often dispersed by primates). Only shade tolerance was significantly correlated with pathogen attack when the analyses accounted for phylogenetic relatedness between species. Thus, contrary to standard predictions of size-defense ratios, our results suggest that larger, shade-tolerant seeds tend to be more susceptible to pathogen attack than smaller, light-dependent seeds. Moreover, differential pathogen attack may shape seed community composition, which may affect the successful recruitment of adults.

Keywords

Light dependence Fungi Plant pathogens Recruitment limitation Seed dispersal Seed weight 

References

  1. Augspurger CK (1984) Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65:1705–1712CrossRefGoogle Scholar
  2. Augspurger CK, Kelly CK (1984) Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61:211–217CrossRefGoogle Scholar
  3. Bekker RM, Bakker JP, Grandin U, Kalamees R, Milberg P, Poschlod P, Thompson K, Willems JH (1998) Seed size, shape and vertical distribution in the soil: indicators of seed longevity. Funct Ecol 12:834–842CrossRefGoogle Scholar
  4. Burdon JJ (1987) Diseases and plant population biology. Cambridge University Press, CambridgeGoogle Scholar
  5. Clark JS, Beckage B, Camill P, Cleveland B, HilleRisLambers J, Lighter J, McLachlan J, Mohan J, Wyckoff P (1999) Interpreting recruitment limitation in forests. Am J Bot 86:1–16CrossRefGoogle Scholar
  6. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335CrossRefGoogle Scholar
  7. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899PubMedCrossRefGoogle Scholar
  8. Connell JH (1971) On the role of enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: Den Boer PJ, Gradwell GR (eds) Dynamics of populations. Proceedings of the advanced study institute on dynamics of numbers in populations, Oosterbeek, 1970. Center for Agricultural Publishing and Documentation, Wageningen, The Netherlands, pp 298–310Google Scholar
  9. Crist TO, Friese CF (1993) The impact of fungi on soil seeds: implications for plants and granivores in a semiarid shrub-steppe. Ecology 74:2231–2239CrossRefGoogle Scholar
  10. Dalling JW, Swaine MD, Garwood NC (1997) Soil seed bank community dynamics in seasonally moist lowland tropical forest, Panama. J Trop Ecol 13:659–680Google Scholar
  11. Dalling JW, Swaine MD, Garwood NC (1998) Dispersal patterns and seed bank dynamics of pioneer trees in moist tropical forest. Ecology 79:564–578CrossRefGoogle Scholar
  12. Falster DS, Warton DI, Wright IJ (2003) (S)MATR: standardised major axis tests and routines. http://www.bio.mq.edu.au/ecology/SMATR. Version 1.0Google Scholar
  13. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  14. Foster S, Janson CH (1985) The relationship between seed size and establishment conditions in tropical woody plants. Ecology 66:773–780CrossRefGoogle Scholar
  15. Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32CrossRefGoogle Scholar
  16. Garwood NC (1989) Tropical soil seed banks: a review. In: Leck MA, Parker VT, Simpson RL (eds) Ecology of soil seed banks. Academic Press, Inc., San Diego, pp 149–209Google Scholar
  17. Gautier-Hion A, Duplantier JM, Quris R, Feer F, Sourd C, Decoux JP, Dubost G, Emmons L, Erard C, Hecketsweiler P, Moungazi A, Roussilhon C, Thiollay JM (1985) Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65:324–337CrossRefGoogle Scholar
  18. Gentry AH (1996) A field guide to the families and genera of woody plants in Northwest South America (Colombia, Ecuador, Peru), with supplementary notes on herbaceous taxa. University of Chicago Press, ChicagoGoogle Scholar
  19. Gilbert GS (2002) Evolutionary ecology of plant diseases in natural ecosystems. Annu Rev Phytopathol 40:13–43PubMedCrossRefGoogle Scholar
  20. Green PT, Juniper PA (2004) Seed mass, seedling herbivory and the reserve effect in tropical rainforest seedlings. Funct Ecol 18:539–547CrossRefGoogle Scholar
  21. Hammond DS, Brown VK (1995) Seed size of woody plants in relation to disturbance, dispersal, soil type in wet neotropical forests. Ecology 76:2544–2561CrossRefGoogle Scholar
  22. Henery ML, Westoby M (2001) Seed mass and seed nutrient content as predictors of seed output variation between species. Oikos 92:479–490CrossRefGoogle Scholar
  23. Hood LA, Swaine MD, Mason PA (2004) The influence of spatial patterns of damping-off disease and arbuscular mycorrhizal colonization on tree seedling establishment in Ghanaian tropical forest soil. J Ecol 92:816–823CrossRefGoogle Scholar
  24. Hopkins MS, Graham AW (1987) The viability of seeds of rain-forest species after experimental soil burials under tropical wet lowland forest in northeastern Australia. Australian J Ecol 12:97–108CrossRefGoogle Scholar
  25. Howe HF, Vandekerckhove GA (1981) Removal of wild nutmeg (Virola surinamensis) crops by birds. Ecology 62:1093–1106CrossRefGoogle Scholar
  26. Howe HF, Richter WM (1982) Effects of seed size on seedling size in Virola surinamensis: a within and between tree analysis. Oecologia 53:347–351CrossRefGoogle Scholar
  27. Hubbell SP (1979) Tree dispersion, abundance, and diversity in a tropical dry forest. Science 203:1299–1309PubMedCrossRefGoogle Scholar
  28. Hubbell SP, Foster RB, O’Brien ST, Harms KE, Condit R, Wechsler B, Wright SJ, de Lao SL (1999) Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science 283:554–557PubMedCrossRefGoogle Scholar
  29. Hulme PE (1998) Post-dispersal seed predation and seed bank persistence. Seed Sci Res 8:513–519CrossRefGoogle Scholar
  30. Janzen DH (1969) Seed-eaters versus seed size, number, toxicity and dispersal. Evolution 23:1–27CrossRefGoogle Scholar
  31. Janzen DH (1970) Herbivores and number of tree species in tropical forests. Am Nat 104:501–528CrossRefGoogle Scholar
  32. 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
  33. Leiberman M, Leiberman D (1986) An experimental study of seed ingestion and germination in a plant–animal assemblage in Ghana. J Trop Ecol 2:113–126CrossRefGoogle Scholar
  34. Leigh EG, Davidar P, Dick CW, Puyravaud JP, Terborgh J, ter Steege H, Wright SJ (2004) Why do some tropical forests have so many species of trees? Biotropica 36:447–473Google Scholar
  35. Leps J, Smilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, CambridgeGoogle Scholar
  36. Lonsdale WM (1993) Losses from the seed bank of Mimosa pigra: soil micro-organisms vs. temperature fluctuations. J Appl Ecol 30:654–660CrossRefGoogle Scholar
  37. Mazer SJ (1989) Ecological, taxonomic, and life-history correlates of seed mass among Indiana Dune angiosperms. Ecol Monogr 59:153–175CrossRefGoogle Scholar
  38. Moles AT, Hodson DW, Webb CJ (2000) Seed size and shape and persistence in the soil in the New Zealand flora. Oikos 89:541–545CrossRefGoogle Scholar
  39. Moles AT, Warton DI, Westoby M (2003) Do small-seeded species have higher survival through seed predation than large-seeded species? Ecology 84:3148–3161CrossRefGoogle Scholar
  40. Moles AT, Westoby M (2004) Seedling survival and seed size: a synthesis of the literature. J Ecol 92:372–383CrossRefGoogle Scholar
  41. Moles AT, Ackerly DD, Webb CJ, Tweddle JC, Dickie JB, Pitman AJ, Westoby M (2005) Factors that shape seed mass evolution. Proc Natl Acad Sci USA 102:10540–10544PubMedCrossRefGoogle Scholar
  42. Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281PubMedCrossRefGoogle Scholar
  43. Palmeirim JM, Gorchov DL, Stoleson S (1989) Trophic structure of a neotropical frugivore community: is there competition between birds and bats? Oecologia 79:403–411CrossRefGoogle Scholar
  44. Pearson TRH, Burslem D, Mullins CE, Dalling JW (2002) Germination ecology of neotropical pioneers: interacting effects of environmental conditions and seed size. Ecology 83:2798–2807Google Scholar
  45. Pons TL (1992) Seed responses to light. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CAB International, Wallingford, pp 259–284Google Scholar
  46. Schafer M, Kotanen PM (2004) Impacts of naturally-occurring soil fungi on seeds of meadow plants. Plant Ecol 175:19–35CrossRefGoogle Scholar
  47. Smith CC, Fretwell SD (1974) Optimal balance between size and number of offspring. Am Nat 108:499–506CrossRefGoogle Scholar
  48. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. W. H. Freeman, San FranciscoGoogle Scholar
  49. StatSoft (2006) Electronic statistics textbook. In: http://www.statsoft.com/textbook/stathome.html. StatSoft, Inc. Cited 2 April 2006Google Scholar
  50. Ter Braak CJF, Smilauer P (2002) CANOCO for Windows. Biometrics: Plant Research International, Wageningen. Version 4.5Google Scholar
  51. Terborgh J (1990) An overview of research at Cocha Cashu Biological Station. In: Gentry AH (ed) Four neotropical rainforests. Yale University Press, New Haven, pp 48–59Google Scholar
  52. Terborgh J, Pitman N, Silman M, Schichter H, Nuñez P (2002) Maintenance of tree diversity in tropical forests. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, Wallingford, pp 1–17Google Scholar
  53. Thompson K (1992) The functional ecology of seed banks. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CAB International, Wallingford, pp 231–258Google Scholar
  54. Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183CrossRefGoogle Scholar
  55. Webb CO, Ackerly DD, Kembel S (2004) Phylocom. http://www.phylodiversity.net/phylocom. Version 3.22Google Scholar
  56. Westoby M, Leishman M, Lord J (1996) Comparative ecology of seed size and dispersal. Philos Trans R Soc Lond [Biol] 351:1309–1317CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Elizabeth G. Pringle
    • 1
    • 2
  • Patricia Álvarez-Loayza
    • 1
    • 3
  • John Terborgh
    • 1
  1. 1.Center for Tropical ConservationDuke UniversityDurhamUSA
  2. 2.Department of Biological SciencesStanford UniversityStanfordUSA
  3. 3.Department of Plant Biology and PathologyRutgers UniversityNew BrunswickUSA

Personalised recommendations