Behavioral Ecology and Sociobiology

, Volume 21, Issue 4, pp 237–248 | Cite as

The costs and benefits of cooperation between the Australian lycaenid butterfly, Jalmenus evagoras, and its attendant ants

  • N. E. Pierce
  • R. L. Kitching
  • R. C. Buckley
  • M. F. J. Taylor
  • K. F. Benbow
Article

Summary

The larvae and pupae of the Australian lycaenid butterfly, Jalmenus evagoras associate mutualistically with ants in the genus Iridomyrmex. Four ant exclusion experiments in three field sites demonstrated that predation and parasitism of J. evagoras are so intense that individuals deprived of their attendant ants are unlikely to survive. Larvae and pupae of J. evagoras aggregate, and the mean number of attendant ants per individual increases with larval age and decreases with group size. Field observations showed that young larvae could gain more attendant ants per individual by joining the average size group of about 4 larvae than by foraging alone. Aggregation behaviour is influenced by ant attendance: young larvae and pupating fifth instars aggregated significantly more often on plants with ants than on plants where ants had been excluded. In return for tending and protecting the larvae, ants were rewarded by food secretions that can amount to as much as 409 mg dry biomass from a single host plant containing 62 larvae and pupae of J. evagoras over a 24 h period. Larval development in the laboratory lasted approximately a month, and larvae that were tended by ants developed almost 5 days faster than larvae that were not tended. However, tended individuals, particularly females, pupated at a significantly lower weight than their untended counterparts, and the adults that eclosed from these pupae were also lighter and smaller. On average, pupae that were tended by ants lost 25% more weight than untended pupae, and in contrast with larvae, they took longer to eclose than pupae that were not tended. These experimental results are discussed in terms of costs and benefits of association for both partners, and of aggregation for the lycaenids.

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References

  1. Addicott JF (1984) Mutualistic interactions in population and community processes. In: Price PW, Slobodchikoff CN, Gaud BS (eds) A new ecology: novel approaches to interactive systems. Wiley, New York, pp 437–455Google Scholar
  2. Addicott JF (1986a) On the population consequences of mutualism. In: Diamond J, Case TJ (eds) Community ecology. Harper and Row, New YorkGoogle Scholar
  3. Addicott JF (1986b) Variation in the costs and benefits of mutualism: the interaction between yuccas and yucca moths. Oecologia (Berl) 70:486–494Google Scholar
  4. Atsatt PR (1981) Lycaenid butterflies and ants: selection for enemy-free space. Am Nat 118:638–654Google Scholar
  5. Axelrod R (1984) The evolution of cooperation. Basic Books, New YorkGoogle Scholar
  6. Axelrod R, Hamilton WD (1981) The evolution of cooperation. Science 211:1390–1396Google Scholar
  7. Bhatkar A, Whitcomb WH (1970) Artificial diet for rearing various species of ants. The Fla Entomol 53:230–232Google Scholar
  8. Boucher DH (1985) The idea of mutualism, Past and Future. In: Boucher DH (ed) The biology of mutualisms. Croom Helm, KentGoogle Scholar
  9. Boucher DH, James S, Keeler KH (1982) The ecology of mutualism. Ann Rev Ecol Syst 13:315–347Google Scholar
  10. Common IFB, Waterhouse DF (1981) Butterflies of Australia, 2nd edn. Angus and Robertson, SydneyGoogle Scholar
  11. Cottrell CB (1984) Aphytophagy in butterflies: its relationship to myrmecophily. Zool J Linn Soc 79:1–57Google Scholar
  12. Downey JC (1962) Myrmecophily in Plebejus (Icaricia) icarioides (Lepidoptera: Lycaenidae). Entomol News 73:57–66Google Scholar
  13. Dunn KL (1984) Acacia diffusa Lind.: a new larval foodplant for Jalmenus evagoras evagoras (Donovan) (Lepidoptera: Lycaenidae). Vict Entomol 14:8Google Scholar
  14. Elgar MA, Pierce NE (1987) Mating success and fecundity in an ant-tended lycaenid butterfly. In: Clutton-Brock TH (ed) Reproductive success: studies of selection and adaptation in contrasting breeding systems. Chicago University Press, Chicago (in press)Google Scholar
  15. Hawkeswood TJ (1981) The food plants of Jalmenus evagoras (Donovan) (Lepidoptera: Lycaenidae). Aust Entomol Mag 8:1–2Google Scholar
  16. Henning SF (1983) Chemical communication between lycaenid larvae (Lepidoptera: Lycaenidae) and ants (Hymenoptera: Formicidae). J Entomol Soc South Afr 46:341–366Google Scholar
  17. Hinton HE (1951) Myrmecophilous Lycaenidae and other Lepidoptera — a summary. Proc Soc Lond Entomol Nat Hist Soc 1951:111–175Google Scholar
  18. Hölldobler B (1970) Zur Physiologie der Gast-Wirt-Beziehungen (Myrmecophilie) bei Ameisen. II. Das Gastverhältnis zu Myrmica und Formica. Z Vergl Physiol 66:215–250Google Scholar
  19. Hölldobler B (1971) Communication between ants and their guests. Sci Amer 224:86–93Google Scholar
  20. Janzen DH (1979) How many babies do figs pay for babies? Biotrop 11:48–50Google Scholar
  21. Janzen DH (1985) The natural history of mutualisms. In: Boucher DH (ed) The biology of mutualism. Croom Helm, London, pp 40–99Google Scholar
  22. Keeler KH (1981) A model for a facultative, non-symbiotic mutualism. Am Nat 118:488–498Google Scholar
  23. Keeler KH (1985) Cost: benefit models of mutualism. In: Boucher DH (ed) The biology of mutualism. Croom Helm, London, pp 100–127Google Scholar
  24. Kitching RL (1981) Egg clustering and the Southern Hemisphere lycaenids: comments on a paper by N.E. Stamp. Am Nat 118:423–425Google Scholar
  25. Kitching RL (1983) Myrmecophilous organs of the larvae and pupae of the lycaenid butterfly Jalmenus evagoras (Donovan). J Nat Hist 17:471–481Google Scholar
  26. Kitching RL, Luke B (1985) The myrmecophilous organs of the larvae of some British Lycaenidae (Lepidoptera): a comparative study. J Nat Hist 19:259–276Google Scholar
  27. Kitching RL, Taylor MFJ (1981) The culturing of Jalmenus evagoras (Donovan) and its attendant ant, Iridomyrmex anceps (Roger). Aust Ent Mag 7:71–75Google Scholar
  28. Malicky H (1969) Versuch einer Analyse der ökologischen Beziehungen zwischen Lycaeniden (Lepidoptera) und Formiciden (Hymenoptera). Tijdschr Entomol 112:213–298Google Scholar
  29. Malicky H (1970) New aspects on the association between lycaenid larvae (Lycaenidae) and ants (Formicidae, Hymenoptera). J Lepid Soc 24:190–202Google Scholar
  30. Maschwitz U, Wust M, Schurian K (1975) Blaulingsraupen als Zuckerlieferanten für Ameisen. Oecologia (Berl) 18:17–21Google Scholar
  31. Maynard Smith J (1982) Evolution and the theory of games. Cambridge University Press, CambridgeGoogle Scholar
  32. Morse D (1985) Costs in a milkweed, Asclepias syriaca and bumblebee, Bombus spp. mutualism. Am Nat 125:903–905Google Scholar
  33. Nijhout HF (1975) A threshold size for metamorphosis in the tobacco hornworm, Manduca sexta (L.). Biol Bull 149:214–225Google Scholar
  34. Nijhout HF (1981) Physiological control of molting in insects. Am Zool 21:631–640Google Scholar
  35. Nijhout HF, Williams CM (1974a) Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): Growth of the last-instar larva and the decision to pupate. J Exp Biol 61:481–491Google Scholar
  36. Nijhout HF, Williams CM (1974b) Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (l.): cessation of juvenile hormone secretion as a trigger for pupation. J Exp Biol 61:493–501Google Scholar
  37. Pierce NE (1983) The ecology and evolution of symbioses between lycaenid butterflies and ants. PhD thesis, Harvard University, CambridgeGoogle Scholar
  38. Pierce NE (1984) Amplified species diversity: a case study of an Australian lycaenid butterfly and its attendant ants. In: Vane Wright RI, Ackery PR (eds) Biology of butterflies. XI Symp R Entomol Soc (Lond). Academic Press, London, pp 197–200Google Scholar
  39. Pierce NE (1985) Lycaenid butterflies and ants: selection for nitrogen fixing and other protein rich food plants. Am Nat 125:888–895Google Scholar
  40. Pierce NE (1987) The evolution and biogeography of associations between lycaenid butterflies and ants. Oxford Surv Evol Biol (in press)Google Scholar
  41. Pierce NE, Easteal S (1986) The selective advantage of attendant ants for the larvae of a lycaenid butterfly, Glaucopsyche lygdamus. J Anim Ecol 55:451–462Google Scholar
  42. Pierce NE, Elgar MA (1985) The influence of ants on host plant selection by Jalmenus evagoras, a myrmecophilous lycaenid butterfly. Behav Ecol Sociobiol 16:209–222Google Scholar
  43. Pierce NE, Mead PS (1981) Parasitoids as selective agents in the symbiosis between lycaenid buterfly caterpillars and ants. Science 211:1185–1187Google Scholar
  44. Pierce NE, Young WR (1987) Lycaenid butterflies and ants: two-species stable equilibria in mutualistic, commensal, and parasitic interactions. Am Nat 128 (in press)Google Scholar
  45. Ross GN (1966) Life history studies on Mexican butterflies. IV. The ecology and ethology of Anatole rossi, a myrmecophilous metalmark (Lepidoptera: Riodinidae). Ann Entomol Soc Am 59:985–1004Google Scholar
  46. Roughgarden J (1975) Evolution of marine symbiosis—a simple cost-benefit model. Ecol 56:1201–1208Google Scholar
  47. Schemske DW (1983) Limits to specialization and coevolution in plant-animal mutualisms. In: Nitecki MH (ed) Coevolution. Univ of Chicago Press, ChicagoGoogle Scholar
  48. Templeton AR, Gilbert LE (1985) Population genetics and the coevolution of mutualism. In: Boucher DH (ed) The biology of mutualism. Croom Helm, London, pp 128–144Google Scholar
  49. Trivers RL (1971) The evolution of reciprocal altruism. Q Rev Biol 46:35–57Google Scholar
  50. Vandermeer J (1984) The evolution of mutualism. In: Shorrocks B (ed) Evolutionary ecology. Symp Brit Ecol Soc, 23. Blackwell, London, pp 221–232Google Scholar
  51. Vane Wright RI (1978) Ecological and behavioural origins of diversity in butterflies. In: Mound LA, Waloff N (eds) Diversity of insect faunas. IX Symp R Entomol Soc (Lond). Blackwell, London, pp 56–59Google Scholar
  52. Way MJ, Cammell M (1970) Aggregation behaviour in relation to food utilisation by aphids. In: Watson A (ed) Animal populations in relation to their food resources. Blackwell, Oxford, pp 229–247Google Scholar
  53. Wilson DS (1980) The natural selection of populations and communities. Benjamin/Cummings, Menlo ParkGoogle Scholar
  54. Wilson DS (1983) The effects of population structure on the evolution of mutualism: a field test involving burying beetles and their phoretic mites. Am Nat 121:851–870Google Scholar
  55. Wolin CL (1985) The population dynamics of mutualistic systems. In: Boucher DH (ed) The biology of mutualism. Croom Helm, London, pp 248–269Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • N. E. Pierce
    • 1
    • 2
  • R. L. Kitching
    • 2
  • R. C. Buckley
    • 3
  • M. F. J. Taylor
    • 4
  • K. F. Benbow
    • 2
  1. 1.Museum of Comparative ZoologyHarvard UniversityCambridgeUSA
  2. 2.School of Australian Environmental StudiesGriffith UniversityBrisbaneAustralia
  3. 3.Department of Biogeography and Geomorphology, Research School of Pacific StudiesThe Australian National UniversityCanberraAustralia
  4. 4.Division of EntomologyCSIRO, Longpocket LaboratoriesIndooroopillyAustralia

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