Plant Ecology

, Volume 215, Issue 2, pp 209–220 | Cite as

Leaf synchrony and insect herbivory among tropical tree habitat specialists

  • Greg P. A. Lamarre
  • Irene Mendoza
  • Paul V. A. Fine
  • Christopher Baraloto


Growth defense tradeoff theory predicts that plants in low-resource habitats invest more energy in defense mechanisms against natural enemies than growth, whereas plants in high-resource habitats can afford higher leaf loss rates. A less-studied defense against herbivores involves the synchrony of leaf production, which can be an effective defense strategy if leaf biomass production exceeds the capacity of consumption by insects. The aim of this study was to determine whether leaf synchrony varied across habitats with different available resources and whether insects were able to track young leaf production among tree habitat specialists in a tropical forest of French Guiana. We predicted that high-resource habitats would exhibit more synchrony in leaf production due to the low cost and investment to replace leaf tissue. We also expected closer patterns of leaf synchrony and herbivory within related species, assuming that they shared herbivores. We simultaneously monitored leaf production and herbivory rates of five pairs of tree species, each composed of a specialist of terra firme or white-sand forests within the same lineage. Our prediction was not supported by the strong interaction of habitat and lineage for leaf synchrony within individuals of the same species; although habitat specialists differed in leaf synchrony within four of five lineages, the direction of the effect was variable. All species showed short time lags for the correlation between leaf production and herbivory, suggesting that insects are tightly tracking leaf production, especially for the most synchronous species. Leaf synchrony may provide an important escape defense against herbivores, and its expression appears to be constrained by both evolutionary history and environmental factors.


Phenology Escape Herbivorous insects Resource availability Time lag French Guiana 



We thank Eléonore Bernardo, Jocelyn Cazal, Jean-Yves Goret, and Antonin Leclercq for help in field work. This manuscript has been improved by the help of Q. Molto, P.-C. Zalamea, and C.E.T. Paine. Research was supported by a collaborative NSF Grant (DEB-0743103/0743800) to C. Baraloto and P.V.A. Fine, the Fond Social Européen (FSE) to G.P.A. Lamarre, and an INRA Package Grant to C. Baraloto. I. Mendoza benefited of a Brazilian CNPq Grant (150483/2012-0) during the writing of this paper. This work has benefited from an “Investissement d’Avenir” grant managed by Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01). This article is an output of the interaction held during the ATBC meeting in Bonito (June 2012).


  1. Agrawal AA, Fishbein M, Halitschke R, Hastings AP, Rabosky DL, Rasmann S (2009) Evidence for adaptive radiation from a phylogenetic study of plant defenses. Proc Natl Acad Sci USA 106:18067–18072PubMedCrossRefGoogle Scholar
  2. Aide TM (1988) Herbivory as a selective agent on the timing of leaf production in a tropical understory community. Nature 336:574–575CrossRefGoogle Scholar
  3. Aide TM (1991) Synchronous leaf production and herbivory in juveniles of Gustavia superba. Oecologia 88:511–514Google Scholar
  4. Aide TM (1992) Dry season leaf production: an escape from herbivory. Biotropica 24:532–537CrossRefGoogle Scholar
  5. Aide TM (1993) Patterns of leaf development and herbivory in a tropical understory community. Ecology 74:455–466CrossRefGoogle Scholar
  6. Augspurger CK (1983) Phenology, flowering synchrony, and fruit-set of six neotropical shrubs. Biotropica 15:257–267CrossRefGoogle Scholar
  7. Baraloto C, Rabaud S, Molto Q, Blanc L, Fortunel C, Herault B, Davila N, Mesones I, Rios M, Valderrama E, Fine PVA (2011) Disentangling stand and environmental correlates of aboveground biomass in Amazonian forests. Glob Change Biol 17:2677–2688CrossRefGoogle Scholar
  8. Baraloto C, Molto Q, Rabaud S, Hérault B, Valencia R, Blanc L, Fine PVA, Thompson J (2013) Rapid simultaneous estimation of aboveground biomass and tree diversity across Neotropical forests: a comparison of field inventory methods. Biotropica 45:288–298Google Scholar
  9. Becerra JX (1997) Insects on plants: macroevolutionary chemical trends in host use. Science 276:253–256PubMedCrossRefGoogle Scholar
  10. Bixenmann RJ, Coley PD, Kursar TA (2013) Developmental changes in direct and indirect defenses in the young leaves of the Neotropical tree genus Inga (Fabaceae). Biotropica 45:175–184CrossRefGoogle Scholar
  11. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135PubMedCrossRefGoogle Scholar
  12. Bonal D, Bosc A, Ponton S, Goret J-Y, Burban B, Gross P, Bonnefond J-M, Elbers J, Longdoz B, Epron D, Guehl J-M, Granier A (2008) Impact of severe dry season on net ecosystem exchange in the Neotropical rainforest of French Guiana. Glob Change Biol 14:1917–1933CrossRefGoogle Scholar
  13. Burnham KP, Anderson DR (1998) Model selection and inference: a practical information theoretic approach. Springer, New YorkCrossRefGoogle Scholar
  14. Coley PD (1980) Effects of leaf age and plant life-history patterns on herbivory. Nature 284:545–546CrossRefGoogle Scholar
  15. Coley PD, Kursar TA (1996) Anti-herbivore defenses of young tropical leaves: physiological constraints and ecological tradeoffs. In: Mulkey SS, Chazdon R, Smith AP (eds) Tropical forest plant ecophysiology. Springer, Berlin, pp 305–337CrossRefGoogle Scholar
  16. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899PubMedCrossRefGoogle Scholar
  17. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608CrossRefGoogle Scholar
  18. Feeny P (1976) Plant apparency and chemical defense. In: Wallace J, Mansell R (eds) Biochemical interaction between plants and insects. Springer, Berlin, pp 1–40CrossRefGoogle Scholar
  19. Fine PVA, Mesones I, Coley PD (2004) Herbivores promote habitat specialization by trees in amazonian forests. Science 305:663–665PubMedCrossRefGoogle Scholar
  20. Fine PVA, Miller ZJ, Mesones I, Irazuzta S, Appel HM, Stevens MHH, Saaksjarvi I, Schultz LC, Coley PD (2006) The growth defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87:S150–S162PubMedCrossRefGoogle Scholar
  21. Fine PVA, Metz MR, Lokvam J, Mesones I, Zuniga JMA, Lamarre GPA, Pilco MV, Baraloto C (2013) Insect herbivores, chemical innovation, and the evolution of habitat specialization in Amazonian trees. Ecology 94:1764–1775PubMedCrossRefGoogle Scholar
  22. Fortunel C, Paine CET, Fine PVA, Kraft NJB, Baraloto C (2014) Environmental factors predict community functional composition in Amazonian forests. J Ecol 102:145–155Google Scholar
  23. Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspect Plant Ecol Evol Syst 8:157–178CrossRefGoogle Scholar
  24. Heil M, Kost C (2006) Priming of indirect defences. Ecol Lett 9:813–817PubMedCrossRefGoogle Scholar
  25. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  26. Kursar TA, Coley PD (1992) Delayed greening in tropical leaves: an antiherbivore defense. Biotropica 24:256–262CrossRefGoogle Scholar
  27. Kursar TA, Coley PD (2003) Convergence in defense syndromes of young leaves in tropical rainforests. Biochem Syst Ecol 31:929–949CrossRefGoogle Scholar
  28. Lamarre GPA, Baraloto C, Fortunel C, Davila N, Mesones I, Grandez Rios J, Rios M, Valderrama E, Vasquez Pilco M, Fine PVA (2012) Herbivory, growth rates, and habitat specialization in tropical tree lineages: implications for Amazonian beta-diversity. Ecology 93:S195–S210CrossRefGoogle Scholar
  29. Legendre P, Legendre L (1998) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
  30. Lieberman D, Lieberman M (1984) The causes and consequences of synchronous flushing in a dry tropical forest. Biotropica 16:193–201CrossRefGoogle Scholar
  31. Macauley BJ, Fox LR (1980) Variation in total phenols and condensed tannins in Eucalyptus: leaf phenology and insect grazing. Aust J Ecol 5:31–35CrossRefGoogle Scholar
  32. Marquis RJ (1984) Leaf herbivores decrease fitness of a tropical plant. Science 226:537–539PubMedCrossRefGoogle Scholar
  33. McKey D (1975) The ecology of coevolved seed dispersal systems. In: Gilbert LE, Raven PH (eds) Coevolution of plants and animals. University of Texas, Austin, pp 159–191Google Scholar
  34. McKey D (1989) Interactions between ants and leguminous plants. In: Stirton CH, Zarucchi JL (eds) Advances in legume biology. Monographs in Systematic Botany from the Missouri Botanical Garden, vol 29, pp 673–718Google Scholar
  35. Molino JF, Sabatier D, Prévost MF, Frame D, Gonzalez S, Bilot-Guérin V (2009) Etablissement d’une liste des espèces d’arbres de la Guyane française. IRD, CayenneGoogle Scholar
  36. Mooney KA, Halitschke R, Kessler A, Agrawal AA (2010) Evolutionary trade-offs in plants mediate the strength of trophic cascades. Science 327:1642–1644PubMedCrossRefGoogle Scholar
  37. Novotny V, Drozd P, Miller SE, Kulfan M, Janda M, Basset Y, Weiblen GD (2006) Why are there so many species of herbivorous insects in tropical rainforests? Science 313:1115–1118PubMedCrossRefGoogle Scholar
  38. Pennec A, Gond V, Sabatier D (2010) Tropical forest phenology in French Guiana from MODIS time series. Remote Sens Lett 2:337–345CrossRefGoogle Scholar
  39. Pennington TD, Gasson P, Hanson L, Kite G, Harborne J (1997) The genus Inga: botany. Royal Botanic Gardens, Richmond, UK, 844 ppGoogle Scholar
  40. Poorter L, Bongers L, Bongers F (2006) Architecture of 54 moist-forest tree species: traits, trade-offs, and functional groups. Ecology 87:1289–1301PubMedCrossRefGoogle Scholar
  41. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  42. Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annu Rev Ecol Evol Syst 40:245–269CrossRefGoogle Scholar
  43. van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu Rev Entomol 52:37–55PubMedCrossRefGoogle Scholar
  44. van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24:353–377CrossRefGoogle Scholar
  45. Wagner F, Rossi V, Stahl C, Bonal D, Hérault B (2013) Asynchronism in leaf and wood production in tropical forests: a study combining satellite and ground-based measurements. Biogeosci Discuss 10:8247–8281CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Greg P. A. Lamarre
    • 1
    • 2
  • Irene Mendoza
    • 3
    • 4
  • Paul V. A. Fine
    • 5
  • Christopher Baraloto
    • 2
    • 6
  1. 1.Université Antilles Guyane, UMR Ecologie des Forêts de GuyaneKourouFrench Guiana
  2. 2.INRA, UMR Ecologie des Forêts de GuyaneKourouFrench Guiana
  3. 3.Plant Phenology and Seed Dispersal Research Group, Departamento de Botânica, Instituto de BiocienciasUniversidade Estadual Paulista (UNESP)Rio ClaroBrazil
  4. 4.UMR 7179 CNRS-MNHN, Departement d’Ecologie et Gestion de la BiodiversitéMuséum National d’Histoire NaturelleBrunoyFrance
  5. 5.Department of Integrative BiologyUniversity of CaliforniaBerkeleyUSA
  6. 6.Department of BiologyUniversity of FloridaGainesvilleUSA

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