Oecologia

, Volume 146, Issue 1, pp 43–49 | Cite as

Ant benefits in a seed dispersal mutualism

  • Nicola Gammans
  • James M. Bullock
  • Karsten Schönrogge
Plant Animal Interactions

Abstract

Myrmecochorous plant seeds have nutrient rich appendages, elaiosomes, which induce some ant species to carry the seeds back to their nest where the elaiosome is consumed and the seed is discarded unharmed. The benefits to plants of dispersal of their seeds in this way have been well documented, but the benefits to the ants from consuming the elaiosomes have rarely been measured and are less clear. Ant benefits from myrmecochory were investigated in a laboratory experiment using the ant Myrmica ruginodis and seeds of Ulex species. To separate the effects of elaiosome consumption on the development of newly produced larvae versus existing larvae, ten ‘Queenright’ colonies containing a queen were compared to ten ‘Queenless’ colonies. Six measures of colony fitness over a complete annual cycle were taken: sexual production, larval weight and number, pupal weight and number, and worker survival. Queenless colonies fed with elaiosomes produced 100.0±29.3 (mean ± SE) of larvae compared to non-elaiosome fed colonies which produced 49.6±19.0; an increase of 102%. Larval weight increased in both Queenright and Queenless colonies. In colonies fed with elaiosomes, larvae weighed 1.02±0.1 mg, but in non-elaiosome fed colonies larvae weighed 0.69±0.1 mg; an increase of 48%. The food supplement provided by Ulex elaiosomes was trivial in energetic terms, under the conditions of an ample diet, suggesting that these effects might be due to the presence of essential nutrients. Chemical analysis of Ulex elaiosomes showed the presence of four essential fatty acids and four essential sterols for ants.

Keywords

Elaiosome Essential nutrients Myrmecochory Myrmica ruginodis Ulex 

Notes

Acknowledgements

This experiment and methodology complies with the current laws of the UK. We would like to thank Graham Elmes, Judith Wardlaw and Michael Fenner for their advice and helpful criticism, Sophie Everett for her advice on chemistry and all the students who helped feed the colonies. This study was funded by the UK Natural Environment Research Council, research studentship to Nicola Gammans, NER/S/A/2002/11078.

References

  1. Andersen AA (1988) Patterns of ant community organisation in mesic south-eastern Australia. Aust J Ecol 11:87–97Google Scholar
  2. Barbehenn RV, Reese JC, Hagens KS (1999) The food of insects. In: Huffaker CB, Gutierrez Ap (eds) Ecol Entomol. Wiley, New YorkGoogle Scholar
  3. Beattie AJ (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, CambridgeGoogle Scholar
  4. Beattie AJ, Culver DC (1983) The nest chemistry of two seed-dispersing ant species. Oecologia 56:99–103CrossRefGoogle Scholar
  5. Begon M, Harper JL, Townsend CR (1996) Ecology. Blackwell, OxfordGoogle Scholar
  6. Behmer ST, Elias DO, Grebenok RJ (1999) Phytosterol metabolism and absorption in the generalist grasshopper, Schistocerca Americana (Orthoptera: Acrididae). Arch Insect Biochem 42:13–25CrossRefGoogle Scholar
  7. Bluthgen N, Gottsberger G, Fiedler K (2004) Sugar and amino acid composition of ant- attended nectar and honeydew sources from an Austral rainforest. Aust Ecol 29:418–429CrossRefGoogle Scholar
  8. Bond WJ, Yeaton R, Stock WD (1991) Myrmecochory in Cape Fynbos. In: Huxley CR, Cutler DF (eds) Ant–plant interactions. Oxford Science publications, Oxford, pp 448–462Google Scholar
  9. Bono JM, Heithaus ER (2002) Sex ratios and the distribution of elaiosomes in colonies of the ant, Aphaenogaster rudis. Insect Soc 49:320–325CrossRefGoogle Scholar
  10. Brew CR, O’Dowd DJ, Rae ID (1989) Seed dispersal by ants—behaviour-releasing compounds in elaiosomes. Oecologia 80:490–497CrossRefGoogle Scholar
  11. Brian MV (1977) Ants. Collins, LondonGoogle Scholar
  12. Brian MV, Abbott A (1977) The control of food flow in a society of the ant Myrmica rubra L. Anim Behav 25:1047–1055CrossRefGoogle Scholar
  13. Brian MV, Rigby C (1978) The trophic eggs of Myrmica rubra L. Insect soc 25(1):89–110CrossRefGoogle Scholar
  14. Brown WD, Keller L, Sundström L (2002) Sex allocation in mound-building ants: The roles of resources and queen replenishment. Ecology 83:1945–1952Google Scholar
  15. Bullock JM (2000) Geographical separation of two Ulex species at three spatial scale: does competition limit species range. Ecography 23:257–271CrossRefGoogle Scholar
  16. Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–638PubMedCrossRefGoogle Scholar
  17. Christie WW (2003) Lipid analysis: Isolation, separation, identification and structural analysis of lipids, 3rd edn. Oily, BridgwaterGoogle Scholar
  18. Dadd RH (1977) Handbook series in nutrition and food. CRC, OhioGoogle Scholar
  19. Elmes GW (1989) The effect of multiple queens in small groups of Myrmica rubra L. Insect Soc 5:137–144Google Scholar
  20. Elmes GW (1991) The social biology of Myrmica ants. Insect Soc 7:17–34Google Scholar
  21. Elmes GW, Wardlaw JC (1981) The quantity and quality of overwintered larvae in five species of Myrmica (Hymenoptera: Formicidae). J Zool 193:429–446CrossRefGoogle Scholar
  22. Elmes GW, Wardlaw JC (1983) A comparison of the effect of temperature on the development of large hibernated larvae of four species of Myrmica (Hym. Formicidae). Insect Soc 30:106–118CrossRefGoogle Scholar
  23. Elmes GW, Wardlaw JC, Schönrogge K, Thomas JA, Clarke RT (2004) Food stress causes differential survival of socially parasitic caterpillars of Maculinea rebeli integrated in colonies of host and non-host Myrmica ant species. Entomol Exp Appl 110:53–63CrossRefGoogle Scholar
  24. Espadaler X, Gómez C (1997) Soil surface searching and transport of Euphorbia characias seeds by ants. Acta Oecologica 18:39–46CrossRefGoogle Scholar
  25. Ferkovich SM, Shapiro J, Carpenter J (2000) Growth of a pupal ectoparasitoid, Diapetimorpha introita, on an artificial diet: stimulation of growth rate by a lipid extract from host pupae. Biocontrol 45:401–413CrossRefGoogle Scholar
  26. Fiedler K, Samm C (1995) Ants benefit from attending facultatively myrmecophilous Lycaenidae caterpillars: evidence form a survival study. Oecologia 104:316–322CrossRefGoogle Scholar
  27. Fischer RC, Richter A, Wanek W, Mayer V (2002) Plants feed ants: food bodies of myrmecophytic Piper and their significance for the interaction with Pheidole bicornis ants. Oecologia 133:186–192CrossRefGoogle Scholar
  28. Gómez C, Espadaler X (1998) Myrmecochorous dispersal distances: a world survey. J Biogeogr 25:573–580CrossRefGoogle Scholar
  29. Hagen KS, Dadd RH, Reese JC (1984) The food insects. In: Huffaker CB (eds) Ecological entomology. Wiley and Sons, New YorkGoogle Scholar
  30. Handel SN, Beattie AJ (1990) Seed dispersal by ants. Sci Am 263:76CrossRefGoogle Scholar
  31. Heil M, Baumann B, Krüger R, Linsenmair KE (2004) Main nutrient compounds in food bodies of Mexican Acacia ant–plants. Chemoecology 14:45–52CrossRefGoogle Scholar
  32. Heinze J, Hölldobler B, Peeters C (1994) Conflict and cooperation in ant societies. Naturwissenschaften 81:489–497CrossRefGoogle Scholar
  33. Holbrook SJ, Schmitt RJ (2004) Population dynamics of a damselfish: effects of a competitor that also is an indirect mutualist. Ecology 85:979–985CrossRefGoogle Scholar
  34. Hölldobler B, Wilson EO (1990) The ants. Belknap, HarvardGoogle Scholar
  35. Horvitz CC (1981) Analysis of how ant behaviours affect germination in a tropical myrmecochore Calathea microcephala (P.& E.) Koernicke (Mantaceae): microsite selection and aril removal by neotropical ants, Odontomachus, Pachycondyla, and Solenopsis (Formicidae). Oecologia 51:47–52CrossRefGoogle Scholar
  36. Hughes L, Westoby M (1992) Effect of diaspore characteristics on removal of seeds adapted for dispersal by ants. Ecology 73:1300–1312CrossRefGoogle Scholar
  37. Kaluzny MA, Duncan LA, Merritt MV, Epps De (1985) Rapid separations of lipid classes in high yield and purity using bonded phase columns. J Lipid Res 26:135–140PubMedGoogle Scholar
  38. Kusmenoglu S, Rockwood LL, Gretz MR (1989) Fatty acids and diacylglycerols from elaiosomes of some ant- dispersed seeds. Phytochemistry 28:2601–2602CrossRefGoogle Scholar
  39. Lanza J, Schmitt MA, Awad AB (1992) Comparative chemistry of elaiosomes of three species of Trillium. J Chem Ecol 18:209–221CrossRefGoogle Scholar
  40. Marshall DL, Beattie AJ, Bollenbacher WE (1979) Evidence for diglycerides as attractants in an ant-seed interaction. J Chem Ecol 5:335–344CrossRefGoogle Scholar
  41. Morales MA, Heithaus ER (1998) Food from seed-dispersal mutualism shifts sex ratios in colonies of the ant Aphaenogaster rudis. Ecology 79:734–739Google Scholar
  42. Ohkawara K, Higashi S, Ohara M (1996) Effects of ants, ground beetles and the seed-fall patterns on myrmecochory of Erythronium japonicum Decne (Liliaceae). Oecologia 106:500–506CrossRefGoogle Scholar
  43. Raine NE, Gammans N, MacFadyen IJ, Scrivner GK, Stone GN (2004) Guards and thieves: antagonistic interactions between two ant species coexisting on the same ant-plant. Ecol Entomol 29:345–352CrossRefGoogle Scholar
  44. Rock GC (1985) The essential dietary fatty acid requirements of the tufted apple budmoth, Platynota idaensalis. J Insect Physiol 31:9–13CrossRefGoogle Scholar
  45. Rudgers JA, Gardener MC (2003) Extrafloral nectar as a resource mediating multispecies interaction. Ecology 85:1495–1502Google Scholar
  46. Ryan BF, Joiner BL, Ryan T (2000) Minitab handbook, 4th edn. Brooks Cole, FlorenceGoogle Scholar
  47. Schmitt RJ, Holbrook SJ (2004) Mutualism can mediate competition and promote coexistence. Ecol Lett 6:898–902CrossRefGoogle Scholar
  48. Sheridan SL, Iversen KA, Itagakis H (1996) The role of chemical senses in seed-carrying behaviour by ants: A behavioural, physiological and morphological study. J Insect Physiol 42:149–159CrossRefGoogle Scholar
  49. Smeeton L (1981) The source of males in Myrmica rubra L. (Hym. Formcidae). Insect Soc 28(3):263–278CrossRefGoogle Scholar
  50. Smeeton L (1982) The effects of the sizes of colony worker and food store on the production of reproductive eggs by workers of Myrmica Rubra L. (Hym. Formicidae). Insect Soc 29:475–484CrossRefGoogle Scholar
  51. Stokes KE, Bullock JM, Watkinson AR (2003) Ulex gallii Planch and Ulex minor Roth. J Ecol 91:1106–1124CrossRefGoogle Scholar
  52. Wardlaw JC, Elmes GW (1996) Exceptional colony size in Myrmica species (Hymenoptera: Formicidea). The Entomol 115:191–196Google Scholar
  53. Wilson MF (1993) Dispersal mode, seed shadows, and colonization patterns. Vegetation 108:261–280Google Scholar
  54. Zettler AJ, Spira TP, Allen CR (2001) Ant-seed mutualisms: can red imported fire ants sour the relationship. Biol Conserv 101:249–253CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Nicola Gammans
    • 1
    • 2
  • James M. Bullock
    • 1
  • Karsten Schönrogge
    • 1
  1. 1.NERC Centre for Ecology and HydrologyWinfrith Technology CentreWinfrith NewburghUK
  2. 2.The University of SouthamptonSouthamptonUK

Personalised recommendations