, Volume 155, Issue 2, pp 277–286 | Cite as

Does attraction to frugivores or defense against pathogens shape fruit pulp composition?

  • Eliana CazettaEmail author
  • H. Martin Schaefer
  • Mauro Galetti
Plant-Animal Interactions - Original Paper


Fruit traits evolve in response to an evolutionary triad between plants, seed dispersers, and antagonists that consume fruits but do not disperse seeds. The defense trade-off hypothesis predicts that the composition of nutrients and of secondary compounds in fruit pulp is shaped by a trade-off between defense against antagonists and attraction to seed dispersers. The removal rate model of this hypothesis predicts a negative relationship between nutrients and secondary compounds, whereas the toxin-titration model predicts a positive relationship. To test these alternative models, we evaluated whether the contents of nutrients and secondary compounds can be used to predict fruit removal by mutualists and pathogens in 14 bird-dispersed plants on a subtropical island in São Paulo state, southeastern Brazil. We selected eight to ten individuals of each species and prevented fruit removal by covering four branches with a net and left fruits on four other branches available to both, vertebrate fruit consumers and pathogens. The persistence of ripe fruits was drastically different among species for bagged and open fruits, and all fruit species persisted longer when protected against seed dispersers. We found that those fruits that are quickly removed by vertebrates are nutrient-rich, but although the attack rate of pathogens is also high, these fruits have low contents of quantitative defenses such as tannins and phenols. Thus, we suggest that the fruit removal rate by seed dispersers is the primary factor selecting the levels of fruit defense. Likewise, nutrient-poor fruits have low removal of seed dispersers and low probability of attack by pathogens. These species retain ripe fruits in an intact condition for a prolonged period because they are highly defended by secondary compounds, which reduce overall attractiveness. However, this strategy might be advantageous for plants that depend on rare or unreliable dispersers.


Fruit pathogens Fruit removal Secondary compounds Plant–animal interactions 



We would like to thank Dr. Douglas Levey for help in statistical analysis and Dr. Josi Roberto Trigo for help in chemical analysis. This project received financial support from FAPESP (Proc. 05/52726-9). E. Cazetta thanks FAPESP (Proc. 03/08447-2) and M. Galetti receives a fellowship from CNPq. E. Cazetta and H. M. Schaefer received a DAAD fellowship for field work and was supported by DFG grant (Scha 1008/4-1) during this project. All experiments comply with the current Brazilian laws.

Supplementary material

442_2007_917_MOESM1_ESM.doc (114 kb)
Appendix) Morphological and nutritional fruit traits of the 14 plant species evaluated on Ilha do Cardoso. (DOC 114 kb)


  1. Ab’Saber AN (1955) Contribuição à geomorfologia do litoral paulista. Rev Bras Geogr 17:1–48Google Scholar
  2. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedGoogle Scholar
  3. Clark L, Shah PS, Mason JR (1991) Chemical repellency in birds; relationship between chemical structure and avoidance response. J Exp Zool 260:310–322PubMedCrossRefGoogle Scholar
  4. Cipollini ML, Levey DJ (1997a) Why are some fruit toxic? Glycoalkaloids in Solanum and fruit choice by vertebrates. Ecology 78:782–798Google Scholar
  5. Cipollini ML, Levey DJ (1997b) Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypothesis and implications for seed dispersal. Am Nat 150:346–372CrossRefPubMedGoogle Scholar
  6. Cipollini ML, Levey DJ (1997c) Antifungal activity of Solanum fruit glycoalkaloids: implications for frugivory and seed dispersal. Ecology 78:799–809Google Scholar
  7. Cipollini ML, Stiles EW (1992a) Relative risks of microbial rot for fleshy fruits: significance with respect to dispersal and selection for secondary defense. Adv Ecol Res 23:35–91Google Scholar
  8. Cipollini ML, Stiles EW (1992b) Antifungal activity of ripe ericaceous fruits: phenolic–acid interactions and palatability for dispersers. Biochem Syst Ecol 20:501–514CrossRefGoogle Scholar
  9. Cipollini ML, Stiles EW (1992c) Relative risks of fungal rot for temperate ericaceous fruits: effects of seasonal variation on selection for chemical defense. Can J Bot 70:1868–1877Google Scholar
  10. Cipollini ML, Stiles EW (1993) Fruit rot, antifungal defense, and palatability of fleshy fruits for frugivorous birds. Ecology 74:751–762CrossRefGoogle Scholar
  11. Couto OS, Cordeiro RMS (2005) Manual do reconhecimento das espécies vegetais da restinga do Estado de São Paulo, 1st edn. Secretaria do Meio Ambiente, Departamento Estadual de Proteção dos Recursos Naturais – DEPRN, São Paulo, BrasilGoogle Scholar
  12. Davidson PM, Juneja VK (1990) Antimicrobial agents. In: Branen AL, Davidson PM, Salminen S (eds) Food additives. Marcel Dekker, New York, pp 83–137Google Scholar
  13. Denslow JS (1987) Fruit removal rates from aggregation and isolated bushes of the red elderberry, Sambacus pubens. Can J Bot 65:1229–1235CrossRefGoogle Scholar
  14. Fineblum WL, Rausher MD (1997) Do floral pigmentation genes also influence resistance to enemies? The W locus in Ipomea purpurea. Ecology 78:1646–1654Google Scholar
  15. Foley WJ, McLean S, Cork SJ (1995) Consequences of biotransformation of plant secondary metabolites on acid-base metabolism in mammals-a final common pathway. J Chem Ecol 21:721–743CrossRefGoogle Scholar
  16. Francisco MR, Galetti M (2001) Frugivoria e dispersão de sementes de Rapanea lanciolata (Myrsinaceae) por aves numa área de cerrado do Estado de São Paulo, sudeste do Brasil. Ararajuba 9:13–19Google Scholar
  17. Francisco MR, Galetti M (2002) Aves como potenciais dispersoras de sementes de Ocotea pulchella Mart. (Lauraceae) numa área de vegetação de cerrado do sudeste brasileiro. Rev Bras Bot 25:11–17CrossRefGoogle Scholar
  18. Guglielmo CG, Karasov WH, Jakubas WJ (1996) Nutritional costs of a plant secondary metabolite explain selective foraging by Ruffed Grouse. Ecology 77:1103–1115CrossRefGoogle Scholar
  19. Harborne JB (1979) Flavonoid pigments. In: Rosenthal GA, Janzen DH (eds) Herbivores—their interaction with secondary plant metabolites. Academic, New York, pp 619–656Google Scholar
  20. Harborne JB (1980) Plant phenolics. In: Pirson A, Zimmermann M (eds) Encyclopedia of plant physiology. Secondary Plant Products, vol 8. Springer, BerlinGoogle Scholar
  21. Herrera CM (1982) Defense of ripe fruits from pests: its significance in relation to plant–disperser interactions. Am Nat 120:218–241CrossRefGoogle Scholar
  22. Irwin RE, Strauss SY, Storz S, Emerson A, Guibert G (2003) The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84:1733–1743CrossRefGoogle Scholar
  23. Janzen DH (1974) Tropical blackwater rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6:69–103CrossRefGoogle Scholar
  24. Janzen DH (1977) Why fruits rot, seeds mold, and meat spoils. Am Nat 111:691–713CrossRefGoogle Scholar
  25. Jeffery JH, Bassett J, Mendaham J, Denney RC (1989) Vogel’s test book of quantitative chemical analices, 5th edn. Longman Group, Londres, UKGoogle Scholar
  26. Jones E, Wheelwright NT (1987) Seasonal changes in the fruits of Viburnun opulus, a fleshy-fruited temperate-zone shrub. Can J Bot 65:2291–2296Google Scholar
  27. Jordano P (1995) Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant–animal interactions. Am Nat 145:163–191CrossRefGoogle Scholar
  28. Karlson P (1972) Biochemie, 8th edn. Thieme, StuttgartGoogle Scholar
  29. Laks PE (1989) An overview of condensed tannins structure. In: Hemingway RW, Karchesy JJ (eds) Chemistry and the significance of condensed tannins. Plenum, New York, pp 131–138Google Scholar
  30. Levey DJ (1987) Sugar-tasting ability and fruit selection in tropical fruit-eating birds. Auk 104:173–179Google Scholar
  31. Levey DJ, Cipollini ML (1997) A glycoalkaloid in ripe fruit deters consumption by cedar waxwings, Auk 115:359–367Google Scholar
  32. Levey DJ, Tewksbury JJ, Cipollini ML, Carlo TA (2006) A field of the directed deterrent hypothesis in two species of wild chili. Oecologia 150:61–68PubMedCrossRefGoogle Scholar
  33. Manasse RS, Howe HF (1983) Competition or dispersal agents among tropical trees: influences of neighbors. Oecologia 59:185–190CrossRefGoogle Scholar
  34. Manhães MA (2003) Variação da dieta e do comportamento alimentar de traupíneos (Passeriformes: Emberezidae) em Ibitipoca, Minas Gerais, Brasil. Ararajuba 11:45–55Google Scholar
  35. Martínez del Rio C, Restrepo C (1993) Ecological and behavioral consequences of digestion in frugivorous animals. Vegetatio 107/108:205–216Google Scholar
  36. McCarty JP, Levey DJ, Greenberg CH, Sargent S (2002) Spatial and temporal variation in fruit use by wildlife in a forested landscape. Forest Ecol Manag 164:277–291CrossRefGoogle Scholar
  37. Murphy ME (1994) Dietary complementation by wild birds: consideration for field studies. J Biosci 19:355–368CrossRefGoogle Scholar
  38. Noffs MS, Baptista-Noffs LJ (1982) Mapa da vegetação do Parque Estadual da Ilha do Cardoso—As principais formações. Silvicultura em São Paulo 16:620–628Google Scholar
  39. Oliveira-Filho AT, Fontes MAL (2000) Patterns of floristic differentiation among Atlantic forests in south-eastern Brazil and the influence of climate. Biotropica 32:793–810Google Scholar
  40. Panizzi L, Caponi C, Catalano S, Cioni PL, Morelli I (2002) In vitro antimicrobial activity of extracts and isolated constituents of Rubus ulmifolius. J Ethnopharmacol 79:165–168PubMedCrossRefGoogle Scholar
  41. Pizo MA, Silva WR, Galetti M, Laps R (2002) Frugivory in cotingas of the Atlantic Forest of southeast Brazil. Ararajuba 10:177–185Google Scholar
  42. Pizo MA (2004) Frugivory and habitat use by fruit-eating birds in a fragmented landscape of southeast Brazil. Ornitol Neotrop 15:117–126Google Scholar
  43. Pooter H, Villar R (1997) The fate acquire carbon in plants: chemical composition and constructions costs. In: Barraz FA, Grace J (eds) Plant resource and allocation. Academic, Hague, pp 39–72Google Scholar
  44. Price ML, Butler LG (1977) Rapid visual estimation and spectrophometric determination of tannin content of sorghum grain. J Agr Food Chem 25:1268–1273CrossRefGoogle Scholar
  45. Provenza FD, Burritt EA, Clausen TP, Bryant JP, Reichardt PB, Distel RA (1990) Conditioned flavor aversion: a mechanism for goats to avoid condensed tannins in blackbrush. Am Nat 136:801–826CrossRefGoogle Scholar
  46. Saracco JF, Collazo JA, Groom MJ (2004) How do frugivores track resources? Insights from spatial analyses of bird foraging in a tropical forest. Oecologia 139:235–245PubMedCrossRefGoogle Scholar
  47. Saracco JF, Collazo JA, Groom MJ, Carlo TA (2005) Crop size and fruit neighborhood effects on bird visitation to fruiting Schefflera morototoni trees in Puerto Rico. Biotropica 37:81–87CrossRefGoogle Scholar
  48. Sargent S (1990) Neighborhood effects on fruit removal by birds: a field experiment with Viburnum dentatum (Caprifoliaceae). Ecology 71:1289–1298CrossRefGoogle Scholar
  49. Scalbert A (1991) Antimicrobial properties of tannins. Phytochemistry 30:3875–3883CrossRefGoogle Scholar
  50. Schaefer HM, Schmidt V, Winkler H (2003) Testing the defence trade-off hypothesis: how contents of nutrients and secondary compounds affect fruit removal. Oikos 102:318–328CrossRefGoogle Scholar
  51. Schrerer A, Maraschin-Silva F, Baptista LRM (2007) Patterns of mutualistic interactions between trees and frugivorous birds in a restinga community at Itapuã State Park, Rio Grande do Sul, Brazil. Acta Botanica Brasilica 21:203–212Google Scholar
  52. Sugiyama M (1998) Estudo de florestas da restinga da Ilha do Cardoso, Cananéia, São Paulo, Brasil. Bol Inst Bot 11:119–159Google Scholar
  53. Tang AMC, Corlett RT, Hyde KD (2005) The persistence of ripe fleshy fruits in the presence and absence of frugivores. Oecologia 142:232–237PubMedCrossRefGoogle Scholar
  54. Tewksbury JJ (2002) Fruits, frugivores and the evolutionary arms race. New Phytol 156:137–139CrossRefGoogle Scholar
  55. Tsahar E, Friedman J, Izhaki I (2002) Impact on fruit removal and seed predation of a secondary metabolite, emodin, in Rhamnus alaternus fruit pulp. Oikos 99:290–299CrossRefGoogle Scholar
  56. Thompson JN, Willson MF (1978) Disturbance and the dispersal of fleshy fruits. Science 200:1161–1163PubMedCrossRefGoogle Scholar
  57. Van Buren J (1970) Fruit phenolics. In: Hulme AD (eds) The biochemistry of fruits and their products. Academic, London, pp 269–304Google Scholar
  58. Wahaj SA, Levey DJ, Sanders AK, Cipollini ML (1998) Control of gut retention time by secondary metabolites in ripe Solanum fruits. Ecology 79:2309–2319Google Scholar
  59. Willson MF, Whelan CJ (1993) Variation of dispersal phenology in a bird- dispersed shrub, Cornus drummondii. Ecol Monogr 63:151–172CrossRefGoogle Scholar
  60. Whitney KD, Stanton ML (2004) Insect seed predators as novel agents of selection on fruit color. Ecology 85:2153–2160CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Eliana Cazetta
    • 1
    Email author
  • H. Martin Schaefer
    • 2
  • Mauro Galetti
    • 1
  1. 1.Plant Phenology and Seed Dispersal Research Group. Departamento de EcologiaUniversidade Estadual Paulista - UNESPRio ClaroBrazil
  2. 2.Faculty of BiologyUniversity of Freiburg, Evolutionary Biology and Animal EcologyFreiburgGermany

Personalised recommendations