Eur. J. Entomol. 102 (2): 201-208, 2005 | DOI: 10.14411/eje.2005.032

Host-plant flowering status and the concentration of sugar in phloem sap: Effects on an ant-treehopper interaction

Tiago B. QUENTAL*, José R. TRIGO, Paulo S. OLIVEIRA**
Departamento de Zoologia, C.P. 6109, Universidade Estadual de Campinas, 13083-970 Campinas SP, Brasil

Host-plant mediation in ant-hemipteran mutualisms requires three conditions. First, hemipteran attractiveness to ants should vary with plant quality. Second, ants should preferentially tend those Hemiptera that produce the most nutritious attractant. Third, increased ant attendance based on a richer food reward should have a significant effect on some measure of hemipteran fitness. A field experiment is used to test these conditions. This is the first study to simultaneously test these three conditions, and the first to test the effect of plant flowering status on the ant-derived benefits for a honeydew-producing hemipteran. It is hypothesized that membracids (Guayaquila xiphias) feeding on plants (Didymopanax vinosum) with flowers ingest phloem sap of higher quality (higher sugar concentration), produce a higher-quality honeydew and, as a result, are attended by more ants and are better protected compared to those on plants without flowers. Total nitrogen content of the phloem sap of plants with or without flowers did not differ significantly, whereas the sugar concentration was higher in the sap of plants with flowers. Honeydew sugar concentration, honeydew production, and ant tending levels did not vary significantly with flowering status. Membracid survival increased, and natural enemy abundance decreased when ants were present. Plant flowering status did not affect the ant-derived protection afforded to treehoppers, but plants with flowers accumulated more natural enemies through time than plants without flowers. The results suggest that a trade-off between feeding on a higher-quality food and running increased risk of predation on flowering plants could underlie this ant-hemipteran interaction. Based on the parameters measured in this study it is concluded that host-plant mediation does not occur in the ant-Guayaquila system. The results suggest, however, that the way in which the host-plant could affect ant-Guayaquila interactions is complex and likely to involve other species.

Keywords: Ant-treehopper association, honeydew, host-plant mediation, host-plant quality, Membracidae, mutualism, phloem sugar, tritrophic interaction, cerrado savanna

Received: September 1, 2004; Revised: December 17, 2004; Accepted: March 7, 2005; Published: May 3, 2005  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
QUENTAL, T.B., TRIGO, J.R., & OLIVEIRA, P.S. (2005). Host-plant flowering status and the concentration of sugar in phloem sap: Effects on an ant-treehopper interaction. EJE102(2), 201-208. doi: 10.14411/eje.2005.032
Download citation

References

  1. AUCLAIR J.L. 1963: Aphid feeding and nutrition. Annu. Rev. Entomol. 8: 439-490 Go to original source...
  2. BRISTOW C.M. 1984: Differential benefits from ant attendance to two species of Homoptera on New York ironweed. J. Anim. Ecol. 53: 715-726 Go to original source...
  3. BRISTOW C.M. 1991: Are ant-aphid association a tritrophic interaction? Oleander aphids and Argentine ants. Oecologia 87: 514-521 Go to original source...
  4. BRISTOW C.M. & YANITY E. 1999: Seasonal response of workers of the Allegheny mound ant, Formica exsectoides (Hymenoptera: Formicidae) to artificial honeydews of varying nutritional content. Great Lakes Entomol. 32: 15-27 Go to original source...
  5. BRONSTEIN J.L. & BARBOSA P. 2002: Multitrophic/multispecies mutualistic interactions: The role of non-mutualists in shaping and mediating mutualisms. In Tscharntke T. & Hawkins B.A. (eds): Multitrophic Level Interactions. Cambridge University Press, Cambridge, pp. 44-66 Go to original source...
  6. BUCKLEY R.C. 1987: Interactions involving plants, Homoptera, and ants. Annu. Rev. Entomol. 18: 111-138 Go to original source...
  7. CAMPBELL B.C. 1986: Host-plant oligosaccharins in the honeydew of Schizaphis graminum (Rondani) (Insecta, Aphididae). Experientia 42: 451-452 Go to original source...
  8. CUAUTLE M. & RICO-GRAY V. 2003: The effect of wasps and ants on the reproductive success of the extrafloral nectaried plant Turnera ulmifolia (Turneraceae). Funct. Ecol. 17: 417-423 Go to original source...
  9. CUSHMAN J.H. 1991: Host-plant mediation of insect mutualisms: variable outcomes in herbivore-ant interactions. Oikos 61: 138-144 Go to original source...
  10. CUSHMAN J.H. & ADDICOTT J.F. 1989: Intra- and interspecific competition for mutualists: ants as a limited and limiting resource for aphids. Oecologia 79: 315-321 Go to original source...
  11. CUSHMAN J.H. & ADDICOTT J.F. 1991: Conditional interactions in ant-plant-herbivore mutualisms. In Huxley C.R. & Cutler D.F. (eds): Ant-Plant Interactions. Oxford University Press, Oxford, pp. 92-103 Go to original source...
  12. CUSHMAN J.H. & WHITHAM T.G. 1989: Conditional mutualism in a membracid-ant association: temporal, age-specific, and density-dependent effects. Ecology 70: 1040-1047 Go to original source...
  13. DAVIDSON D.W., COOK S.C., SNELLING R.R. & CHUA T.H. 2003: Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300: 969-972 Go to original source...
  14. DEL-CLARO K. & OLIVEIRA P.S. 1993: Ant-homoptera interaction: do alternative sugar sources distract tending ants? Oikos 68: 202-206 Go to original source...
  15. DEL-CLARO K. & OLIVEIRA P.S. 1996: Honeydew flicking by treehoppers provides cues to potential tending ants. Anim. Behav. 51: 1071-1075 Go to original source...
  16. DEL-CLARO K. & OLIVEIRA P.S. 1999: Ant-Homoptera interactions in a neotropical savanna: The honeydew-producing treehopper Guayaquila xiphias (Membracidae) and its associated ant fauna on Didymopanax vinosum (Araliaceae). Biotropica 31: 135-144 Go to original source...
  17. DEL-CLARO K. & OLIVEIRA P.S. 2000: Conditional outcomes in a neotropical treehopper-ant association: temporal and speciesspecific effects. Oecologia 124: 156-165 Go to original source...
  18. DIXON A.F.G. 1985: Aphid Ecology. Blackie, London, 136 pp
  19. DOUGLAS A.E. 1993: The nutritional quality of phloem sap utilized by natural aphid populations. Ecol. Entomol. 18: 31-38 Go to original source...
  20. DOUGLAS A.E. 2003: The nutritional physiology of aphids. Adv. Insect Physiol. 31: 73-140 Go to original source...
  21. FISCHER M.K. & SHINGLETON A.W. 2001: Host plant and ants influence the honeydew sugar composition of aphids. Funct. Ecol. 15: 544-550 Go to original source...
  22. HACKER S.D. & BERTNESS M.D. 1995: A herbivore paradox: why salt marsh aphids live on poor-quality plants. Am. Nat. 145: 192-210 Go to original source...
  23. HENDRIX D.L., WEI Y. & LEGGERR J.E. 1992: Homopteran honeydew sugar composition is determined by both the insect and plant species. Comp. Biochem. Physiol. (B) 101: 23-27 Go to original source...
  24. HOLLDOBLER B. & WILSON E.O. 1990: The Ants. Harvard University Press, Cambridge, MA, 732 pp Go to original source...
  25. JACKSON R.R., POLLARD S.D., NELSON X.J., EDWARDS G.B. & BARRION A.T. 2001: Jumping spiders (Araneae: Salticidae) that feed on nectar. J. Zool. 255: 25-29 Go to original source...
  26. JERVIS M.A. & KIDD N.A.C. 1996: Phytophagy. In M.A. Jervis & Kidd N.A.C. (eds): Insect Natural Enemies: Practical Approaches to Their Study and Evaluation. Chapman and Hall, London, pp. 375-394 Go to original source...
  27. KEARNS C.A. & INOUYE D.W. 1993: Techniques for Pollination Biologists. University Press of Colorado, Niwot, 583 pp
  28. KING R.W. & ZEEVAART J.A. 1974: Enhancement of phloem exudation from cut petioles by chelating-agents. Plant Physiol. 53: 96-103 Go to original source...
  29. KISS A. 1981: Melezitose, aphids and ants. Oikos 37: 382 Go to original source...
  30. KREBS J.R. & DAVIES N.B. 1993: An Introduction to Behavioural Ecology. Blackwell Science, Oxford, 464 pp
  31. LANZA J. 1988: Ant preferences for Passiflora nectar mimics that contain amino acids. Biotropica 20: 341-344 Go to original source...
  32. MATTSON W.J. 1980: Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst . 11: 119-161 Go to original source...
  33. MCEVOY P.B. 1979: Advantages and disadvantages to group living in treehoppers (Homoptera: Membracidae). Misc. Pub. Entomol. Soc. Am. 11: 1-13 Go to original source...
  34. OLIVEIRA P.S. & DEL-CLARO K. 2005: Multitrophic interactions in a neotropical savanna: ant-hemipteran systems, associated insect herbivores, and a host plant. In Burslem D.F.R.P., Pinard M.A. & Hartley S.E. (eds): Biotic Interactions in the Tropics. Cambridge University Press, Cambridge (in press)
  35. OLIVEIRA P.S. & FREITAS A.V.L. 2004: Ant-plant-herbivore interactions in the neotropical cerrado savanna. Naturwissenschaften 91: 557-570
  36. OLIVEIRA P.S., FREITAS A.V.L. & DEL-CLARO K. 2002: Ant foraging on plant foliage: contrasting effects on the behavioral ecology of insect herbivores. In Oliveira P.S. & Marquis R.J. (eds): The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna. Columbia University Press, New York, pp. 287-305. Go to original source...
  37. OLIVEIRA-FILHO A.T. & RATTER J.A. 2002: Vegetation physiognomies and woody flora of the cerrado biome. In Oliveira P.S. & Marquis R.J. (eds): The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna. Columbia University Press, New York, pp. 91-120 Go to original source...
  38. PIERCE N.E. 1985: Lycaenid butterflies and ants: selection for nitrogen fixing and other protein rich food plants. Am. Nat. 125: 888-895 Go to original source...
  39. PIERCE N.E., KITCHING R.L., BUCKLEY R.C., TAYLOR M.F.J. & BENBOW K.R. 1987: The costs and benefits of cooperation between the Australian lycaenid butterfly, Jalmenus evagoras, and its attendant ants. Behav. Ecol. Sociobiol . 21: 237-248 Go to original source...
  40. PRICE P.W., BOUTON C.E., GROSS P., MCPHERON B.A., THOMPSON J.N. & WEIS A.E. 1980: Interactions among three trophic levels: influence of plant on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11: 41-65 Go to original source...
  41. PRICE P.W. & CARR T.G. 2000: Comparative ecology of membracids and tenthredinids in a macroevolutionary context. Evol. Ecol. Res. 2: 645-665
  42. QUEIROZ J.M. & OLIVEIRA P.S. 2001: Tending-ants protect honeydew-producing whiteflies (Homoptera: Aleyrodidae). Environ. Entomol. 30: 295-297 Go to original source...
  43. RICO-GRAY V. 1993: Use of plant-derived food resources by ants in the dry tropical lowlands of coastal Veracruz, Mexico. Biotropica 25: 301-315 Go to original source...
  44. RIECHERT S.E. 1992: Spiders as representative "sit-and-wait" predators. In Crawley M.J. (eds): Natural Enemies: The population Biology of Predators, Parasites, and Diseases. Blackwell, Oxford, pp. 313-328 Go to original source...
  45. SALISBURY F.B. & ROSS C.W. 1992: Plant Physiology. Wadsworth Publishing Company, Belmont, 682 pp
  46. STADLER B. & DIXON A.F.G. 1998: Costs of ant attendance for aphids. J. Anim. Ecol. 67: 454-459 Go to original source...
  47. STRONG, D.R., LAWTON J.H. & SOUTHWOOD T.R.E. 1984: Insects on Plants: Community Patterns and Mechanisms. Harvard University Press, Cambridge, MA, 313 pp
  48. VOGEL A.I. 1989: Textbook of Quantitative Chemical Analysis. Longman, London, 372 pp
  49. VOLKL W., WOODRING J., FISCHER M., LORENZ M.W. & HOFFMANN K.H. 1999: Ant-aphid mutualisms: the impact of the honeydew production and honeydew sugar composition on ant preferences. Oecologia 118: 483-491 Go to original source...
  50. WAY M.J. 1963: Mutualism between ants and honeydewproducing Homoptera. Annu. Rev. Entomol. 8: 307-344 Go to original source...
  51. WHITE T.C.R. 1984: The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63: 90-105 Go to original source...
  52. WOOD T.K. 1980: Divergence in the Enchenopa binotata Say complex (Homoptera: Membracidae) effected by host plant adaptation. Evolution 34: 147-160 Go to original source...
  53. WOODRING J., WIEDEMANN R., FISCHER M.K., HOFFMANN K.H. & VOLKL W. 2004: Honeydew amino acids in relation to sugars and their role in the establishment of ant-attendance hierarchy in eight species of aphids feeding on tansy (Tanacetum vulgare). Physiol. Entomol. 29: 311-319 Go to original source...
  54. ZAR J.H. 1999: Biostatistical Analysis. 4th ed. Prentice Hall, New Jersey, 663 pp

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.