, Volume 138, Issue 4, pp 558–565 | Cite as

Interspecific variation in the defensive responses of obligate plant-ants: experimental tests and consequences for herbivory

  • Emilio M. Bruna
  • David M. Lapola
  • Heraldo L. Vasconcelos
Plant Animal Interactions


The aggressive behavior of ants that protect plants from herbivores in exchange for rewards such as shelter or food is thought to be an important form of biotic defense against herbivory, particularly in tropical systems. To date, however, no one has compared the defensive responses of different ant taxa associated with the same plant species, and attempted to relate these differences to longer-term efficacy of ant defense. We used experimental cues associated with herbivory—physical damage and extracts of chemical volatiles from leaf tissue—to compare the aggressive responses of two ant species obligately associated with the Amazonian myrmecophyte Tococa bullifera (Melastomataceae). We also conducted a colony removal experiment to quantify the level of resistance from herbivores provided to plants by each ant species. Our experiments demonstrate that some cues eliciting a strong response from one ant species elicited no response by the other. For cues that do elicit responses, the magnitude of these responses can vary interspecifically. These patterns were consistent with the level of resistance provided from herbivores to plants. The colony removal experiment showed that both ant species defend plants from herbivores: however, herbivory was higher on plants colonized by the less aggressive ant species. Our results add to the growing body of literature indicating defensive ant responses are stimulated by cues associated with herbivory. However, they also suggest the local and regional variation in the composition of potential partner taxa could influence the ecology and evolution of defensive mutualisms in ways that have previously remained unexplored.


Azteca Crematogaster laevis Myrmecophytes Mutualism Tococa bullifera 



We would like to thank N. Underwood, P. Ward, D. Davidson, J. Rudgers, and two anonymous reviewers for helpful discussions and comments on the manuscript and J.M.S. Vilhena for help with ant identifications. The Biological Dynamics of Forest Fragments Project provided logistical support; permission to conduct the research was provided by the Manaus Free Trade Zone Authority (SUFRAMA). Financial support was provided by an NSF Minority Postdoctoral Fellowship, the NSF AMERICAS program, the University of Florida’s Institute for Food and Agricultural Sciences (E.M.B.), the SUNY-BDFFP Internship Program (D.M.L.), and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (H.L.V.). This is publication number 414 in the BDFFP Technical Series and FAES Publication number R-09881.


  1. Agrawal AA (1998) Leaf damage and associated cues induced aggressive ant recruitment in a neotropical ant-plant. Ecology 79:2100–2112Google Scholar
  2. Agrawal AA, Dubin-Thaler BJ (1999) Induced responses to herbivory in the Neotropical ant-plant association between Azteca ants and Cecropia trees: response of ants to potential inducing cues. Behav Ecol Soc 45:47–54CrossRefGoogle Scholar
  3. Agrawal AA, Rutter MT (1998) Dynamic anti-herbivore defense in ant-plants: the role of induced responses. Oikos 83:227–236Google Scholar
  4. Alonso LE (1998) Spatial and temporal variation in the ant occupants of a facultative ant-plant. Biotropica 30:201–213Google Scholar
  5. Beattie AJ (1985) The evolutionary ecology of ant-plant interactions. Cambridge University Press, Cambridge, UKGoogle Scholar
  6. Benson WW (1985) Amazon ant-plants. In: Prance GT, Lovejoy TE (eds) Amazonia. Pergamon Press, New York, pp 239–266Google Scholar
  7. Bierregaard RO, Gascon C, Lovejoy TE, Mesquita R (eds) (2002) Lessons from Amazonia: the ecology and conservation of a fragmented forest. Yale University Press, New HavenGoogle Scholar
  8. Bronstein JL (1998) The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica 30:150–161Google Scholar
  9. Brouat C, McKey D, Bessiere JM, Pascal L, Hossaert-McKey M (2000) Leaf volatile compounds and the distribution of ant patrolling in an ant-plant protection mutualism: preliminary results on Leonardoxa (Fabaceae: Caesalpinioideae) and Petalomyrmex (Formicidae: Formicinae). Acta Oecol-Int J Ecol 21:349–357Google Scholar
  10. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335Google Scholar
  11. Conover WJ, Iman RL (1981) Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 35:124–129Google Scholar
  12. Crewe RM, Collingwood CA, Blum MS (1972) Comparative analysis of alarm pheromones in ant genus Crematogaster. Compar Biochem Phys 43:703–716CrossRefGoogle Scholar
  13. Davidson DW, McKey D (1993) Ant-plant symbioses: stalking the Chuyachaqui. Trend Ecol Evol 8:326–332CrossRefGoogle Scholar
  14. Do Nascimento RR, et al (1998) Pygidial gland of Azteca nr. bicolor and Azteca chartifex: Morphology and chemical identification of volatile components. J Chem Ecol 24:1629–1637CrossRefGoogle Scholar
  15. Dyer LA, Letourneau DK (1999) Relative strengths of top-down and bottom-up forces in a tropical forest community. Oecologia 119:265–274CrossRefGoogle Scholar
  16. Fearnside PM, Leal Filho N (2002) Soil and development from Amazonia: lessons from the Biological Dynamics of Forest Fragments Project. In: Bierregaard RO Jr, Gascon C, Lovejoy TE, Mesquita R (eds) Lessons from Amazonia: the ecology and conservation of a fragmented forest. Yale University Press, New Haven, pp 291–312Google Scholar
  17. Fiala B, Maschwitz U (1990) Studies on the South East-Asian ant-plant association Crematogaster borneensis/Macaranga: adaptations of the ant partner. Insectes Soc 37:212–231Google Scholar
  18. Fiala B, Maschwitz U, Pong TY, Helbig AJ (1989) Studies of a South East Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia 79:463–470Google Scholar
  19. Fiala B, Grunsky H, Maschwitz U, Linsenmair KE (1994) Diversity of ant-plant interactions: protective efficacy in Macaranga species with different degrees of ant association. Oecologia 97:186–192Google Scholar
  20. Fonseca CR, Ganade G (1996) Asymmetries, compartments and null interactions in an Amazonian ant-plant community. J Anim Ecol 65:339–347Google Scholar
  21. Fowler HG (1993) Herbivory and assemblage structure of myrmecophytous understory plants and their associated ants in the central Amazon. Insectes Soc 40:137–145Google Scholar
  22. Fuente MAS de la, Marquis RJ (1999) The role of ant-tended extrafloral nectaries in the protection and benefit of a Neotropical rainforest tree. Oecologia 118:192–202CrossRefGoogle Scholar
  23. Gaume L, McKey D (1999) An ant-plant mutualisms and its host specific parasite: activity rhythms, young leaf patrolling, and effects on herbivores of two specialist plant-ants inhabiting the same myrmecophyte. Oikos 84:130–144Google Scholar
  24. Heil M (2002) Ecological costs of induced resistance. Curr Opin Plant Biol 5:345–350CrossRefPubMedGoogle Scholar
  25. Heil M, Fiala B, Maschwitz U, Linsenmair KE (2001a) On benefits of indirect defence: short- and long-term studies of antiherbivore protection via mutualistic ants. Oecologia 126:395–403CrossRefGoogle Scholar
  26. Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE (2001b) Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc Nat Acad Sci USA 98:1083–1088CrossRefPubMedGoogle Scholar
  27. Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge, Mass.Google Scholar
  28. Inui Y, Itioka T, Murase K, Yamaoka R, Itino T (2001) Chemical recognition of partner plant species by foundress ant queens in Macaranga-Crematogaster myrmecophytism. J Chem Ecol 27:2029–2040PubMedGoogle Scholar
  29. Itioka T, Nomura M, Inui Y, Itino T, Inoue T (2000) Difference in intensity of ant defense among three species of Macaranga myrmecophytes in a southeast Asian dipterocarp forest. Biotropica 32:318–326Google Scholar
  30. Izzo T, Vasconcelos HL (2002) Cheating the cheater: domatia loss minimizes the effects of ant castration in an Amazonian ant-plant. Oecologia 133:200–205CrossRefGoogle Scholar
  31. Janzen DH (1966) Coevolution of mutualisms between ants and acacias in Central America. Evolution 20:249–275Google Scholar
  32. Janzen DH (1967) Interaction of the bulls-horn acacia (Acacia cornigera L.) with an ant inhabitant (Pseudomyrmex ferruginea F. Smith) in eastern Mexico. Univ Kansas Sci Bull 47:315–558Google Scholar
  33. Karban R, Agrawal AA, Mangel M (1997) The benefits of induced defenses against herbivores. Ecology 78:1351–1355Google Scholar
  34. Lapola DM, Bruna EM, Vasconcelos HL (2003) Contrasting responses to induction cues by ants inhabiting Maieta guianensis (Melastomataceae). Biotropica 35:295–300Google Scholar
  35. Laurent P, Hamdani A, Braekman JC, Daloze D, Isbell LA, de Biseau JC, Pasteels JM (2003) New 1-alk(en)yl-1,3,5-trihydroxycyclohexanes from the Dufour gland of the African ant Crematogaster nigriceps. Tetrahedron Lett 44:1383–1386CrossRefGoogle Scholar
  36. Longino JT (1989) Geographic variation and community structure in an ant-plant mutualism—Azteca and Cecropia in Costa Rica. Biotropica 21:126–132Google Scholar
  37. Mathsoft (1999) S-Plus 2000. Seattle,USAGoogle Scholar
  38. McKey D (1984) Interaction of the ant-plant Leonardoxa africana (Caesalpiniaceae) with its obligate inhabitants in a rainforest in Cameroon. Biotropica 16:81–99Google Scholar
  39. Michelangeli FA (2000) A cladistic analysis of the genus Tococa (Melastomataceae) based on morphological data. Syst Bot 25:211–234Google Scholar
  40. Ness JH (2003) Catalpa bignoniodes alters extrafloral nectar production after herbivory and attracts ant bodyguards. Oecologia 134:210–218PubMedGoogle Scholar
  41. Palmer TM, Young TP, Stanton ML, Wenk E (2000) Short-term dynamics of an acacia ant community in Laikipia, Kenya. Oecologia 123:425–435CrossRefGoogle Scholar
  42. Rankin-de Mérona JM, Prance GT, Hutchings RW, Silva FM, Rodrigues WA, Uehling ME (1992) Preliminary results of large scale tree inventory of upland rain forest in the central Amazon. Acta Amazonica 22:493–534Google Scholar
  43. Rico-Gray V, Garcia-Franco JG, Palacios-Rios M, Diaz-Castelazo C, Parra-Tabla V, Navarro JA (1998) Geographical and seasonal variation in the richness of ant- plant interactions in Mexico. Biotropica 30:190–200Google Scholar
  44. Rocha CFD, Bergallo HG (1992) Bigger ant colonies reduce herbivory and herbivore residence time on leaves of an ant-plant: Azteca muelleri vs Coelomera ruficornis on Cecropia pachystachya. Oecologia 91:249–252Google Scholar
  45. Schupp EW (1986) Azteca protection of Cecropia: ant occupation benefits juvenile trees. Oecologia 70:379–385Google Scholar
  46. SSI (2001) SYSTAT v.8.0 for Windows, 8.0 edn. Systat Software, Richmond, USAGoogle Scholar
  47. Stanton ML, Palmer TM, Young TP (2002) Competition-colonization trade-offs in a guild of African Acacia-ants. Ecol Monogr 72:347–363Google Scholar
  48. Thaler JS (1999) Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–688Google Scholar
  49. Thompson JN (1999) Specific hypotheses on the geographic mosaic of coevolution. Am Nat 153:S1–S14CrossRefGoogle Scholar
  50. Vasconcelos HL (1991) Mutualism between Maieta guianensis Aubl., a myrmecophytic melastome, and one of its ant inhabitants: ant protection against insect herbivores. Oecologia 87:295–298Google Scholar
  51. Vasconcelos HL, Davidson DW (2000) Relationship between plant size and ant associates in two Amazonian ant-plants. Biotropica 32:100–111Google Scholar
  52. Wheeler JW, Evans SL, Blum MS, Torgerson RL (1975) Cyclopentyl ketones: identification and function in Azteca ants. Science 187:254–255PubMedGoogle Scholar
  53. Wood WF, Palmer TM, Stanton ML (2002) A comparison of volatiles in mandibular glands from three Crematogaster ant symbionts of the whistling thorn acacia. Biochem Syst Ecol 30:217–222CrossRefGoogle Scholar
  54. Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle River, N.J.Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Emilio M. Bruna
    • 1
    • 2
    • 5
  • David M. Lapola
    • 3
    • 5
  • Heraldo L. Vasconcelos
    • 4
    • 5
  1. 1.Department of Wildlife Ecology and ConservationUniversity of FloridaGainesvilleUSA
  2. 2.Tropical Conservation and Development ProgramUniversity of FloridaGainesvilleUSA
  3. 3.Departamento de EcologiaUniversidade Estadual PaulistaRio ClaroBrazil
  4. 4.Instituto de BiologiaUniversidade Federal de UberlândiaUberlândiaBrazil
  5. 5.Biological Dynamics of Forest Fragments ProjectINPA-PDBFF ManausBrazil

Personalised recommendations