Advertisement

Behavioral Ecology and Sociobiology

, Volume 64, Issue 8, pp 1219–1228 | Cite as

Waste management in the leaf-cutting ant Acromyrmex echinatior: the role of worker size, age and plasticity

  • Sarah J. Waddington
  • William O. H. Hughes
Original Paper

Abstract

Division of labour is the hallmark of the success of many social animals. It may be especially important with regard to waste management because waste often contains pathogens or hazardous toxins and worker specialisation can reduce the number of group members exposed to it. Here we examine waste management in a fungus-farming, leaf-cutting ant, Acromyrmex echinatior, in which waste management is necessary to protect their vulnerable fungal crop. By marking ants with task-specific paint colours, we found clear division of labour between workers that engage in waste management and those that forage, at least during the fine timescale of the 3-day marking period. This division of labour was influenced by both age and size, with waste management workers tending to be smaller and younger than foragers. The role of preventing contaminated ants from entering the colony was fulfilled mainly by medium-sized workers. When the level of waste was experimentally increased, most of the ants that responded to remove the waste were workers previously engaged in tasks inside the nest rather than external waste workers or foragers. These responding workers tended to be young and medium-sized. Surprisingly, the responding ants were subsequently able to revert back to working within the fungus garden, but the probability of them doing so depended on their age and the length of time they were exposed to waste. The results demonstrate the importance of division of labour with regard to waste management in A. echinatior and show that this is adaptable to changing needs.

Keywords

Social insect Hygiene Caste Polyethism Stimulus-response threshold 

Notes

Acknowledgements

We thank the Smithsonian Tropical Research Institute for facilities in Gamboa, the Autoridad Nacional del Ambiente (ANAM) for permission to collect and export the ants, J.J. Boomsma for providing the ant colonies, L. A. Santorelli, C. L. Frost, F. R. Ryan and A. Reynolds for technical assistance, the referees for their constructive comments and the Leverhulme Foundation for funding. The work described in this article complies with the current laws of the countries in which it was performed. The authors declare that they have no conflict of interest.

References

  1. Ballari S, Farji-Brener A, Tadey M (2007) Waste management in the leaf-cutting ant Acromyrmex lobicornis: division of labour, aggressive behaviour, and location of external refuse dumps. J Ins Behav 20:87–98CrossRefGoogle Scholar
  2. Benton TG, Foster WA (1992) Altruistic housekeeping in a social aphid. Proc R Soc Lond B 247:199–202CrossRefGoogle Scholar
  3. Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440CrossRefPubMedGoogle Scholar
  4. Beshers SN, Robinson GE, Mittenthal J (1999) Response thresholds and division of labor in insect colonies. In: Detrain C, Deneubourg JL, Pasteels JM (eds) Information processing in social insects. Birkhauser, Basel, pp 115–140Google Scholar
  5. Bonabeau E, Theraulaz G (1999) Role and variability of response thresholds in the regulation of division of labor in insect societies. In: Detrain C, Deneubourg JL, Pasteels JM (eds) Information processing in social insects. Birkhauser, Basel, pp 141–164Google Scholar
  6. Bonabeau E, Theraulaz G, Deneubourg J-L (1996) Quantitative study of the fixed threshold model for the regulation of division of labour in insect societies. Proc R Soc Lond B 263:1565–1569CrossRefGoogle Scholar
  7. Bot ANM, Currie CR, Hart AG, Boomsma JJ (2001) Waste management in leaf-cutting ants. Ethol Ecol Evol 13:225–237Google Scholar
  8. Breed MD, Williams DB, Queral A (2002) Demand for task performance and workforce replacement: undertakers in honeybee, Apis mellifera, colonies. J Ins Behav 15:319–329CrossRefGoogle Scholar
  9. Brown MJF, Bot ANM, Hart AG (2006) Mortality rates and division of labor in the leaf-cutting ant Atta colombica. J Ins Sci 6:18Google Scholar
  10. Camargo RS, Forti LC, Lopes JFS, Andrade APP, Ottati ALT (2007) Age polyethism in the leaf-cutting ant Acromyrmex subterraneus brunneus Forel, 1911 (Hym., Formicidae). J Appl Entomol 131:139–145Google Scholar
  11. Chapman NC, Oldroyd BP, Hughes WOH (2007) Differential responses of honeybee (Apis mellifera) patrilines to changes in stimuli for the generalist tasks of nursing and foraging. Behav Ecol Sociobiol 61:1185–1194CrossRefGoogle Scholar
  12. Currie CR (2001) Prevalence and impact of a virulent parasite on a tripartite mutualism. Oecologia 128:99–106CrossRefGoogle Scholar
  13. Currie CR, Stuart AE (2001) Weeding and grooming of pathogens in agriculture by ants. Proc R Soc Lond B 268:1033–1039CrossRefGoogle Scholar
  14. Currie CR, Mueller UG, Malloch D (1999a) The agricultural pathology of ant fungus gardens. Proc Natl Acad Sci U S A 96:7998–8002CrossRefPubMedGoogle Scholar
  15. Currie CR, Scott JA, Summerbell RC, Malloch D (1999b) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–704CrossRefGoogle Scholar
  16. Currie CR, Wong B, Stuart AE, Schultz TR, Rehner SA, Mueller UG, Sung GH, Spatafora JW, Straus NA (2003) Ancient tripartite coevolution in the attine ant–microbe symbiosis. Science 299:386–388CrossRefPubMedGoogle Scholar
  17. Detrain C, Pasteels JM (1991) Caste differences in behavioral thresholds as a basis for polyethism during food recruitment in the ant Pheidole pallidula (Nyl.) (Hymenoptera: Myrmicinae). J Insect Physiol 4:157–176Google Scholar
  18. Dornhaus A (2008) Specialization does not predict individual efficiency in an ant. PLoS Biol 6:e285CrossRefPubMedGoogle Scholar
  19. Feener DH, Moss KAG (1990) Defense against parasites by hitchhikers in leaf-cutting ants—a quantitative assessment. Behav Ecol Sociobiol 26:17–29CrossRefGoogle Scholar
  20. Fewell JH, Bertram SM (1999) Division of labor in a dynamic environment: response by honeybees (Apis mellifera) to graded changes in colony pollen stores. Behav Ecol Sociobiol 46:171–179CrossRefGoogle Scholar
  21. Forti LC, Camargo RS, de Matos CAO, de Andrade APP, Lopes JFS (2004) Aloetismo em Acromyrmex subterraneus brunneus Forel (Hymenoptera, Formicidae), durante o forrageamento, cultivo do jardim de fungo e devolução dos materials forrageados. Rev Bras Ent 48:59–63Google Scholar
  22. Gordon DM (1996) The organization of work in social insect colonies. Nature 380:121–124CrossRefGoogle Scholar
  23. Gordon DM, Mehdiabadi NJ (1999) Encounter rate and task allocation in harvester ants. Behav Ecol Sociobiol 45:370–377CrossRefGoogle Scholar
  24. Hart AG, Ratnieks FLW (2001) Task partitioning, division of labour and nest compartmentalisation collectively isolate hazardous waste in the leafcutting ant Atta cephalotes. Behav Ecol Sociobiol 49:387–392CrossRefGoogle Scholar
  25. Hart AG, Ratnieks FLW (2002) Waste management in the leaf-cutting ant Atta colombica. Behav Ecol 13:224–231CrossRefGoogle Scholar
  26. Hölldobler B, Wilson EO (1990) The Ants. Belknap, CambridgeGoogle Scholar
  27. Hughes WOH, Boomsma JJ (2007) Genetic polymorphism in leaf-cutting ants is phenotypically plastic. Proc R Soc Lond B 274:1625–1630CrossRefGoogle Scholar
  28. Hughes WOH, Eilenberg J, Boomsma JJ (2002) Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc R Soc Lond B 269:1811–1819CrossRefGoogle Scholar
  29. Hughes WOH, Goulson D (2001) Polyethism and the importance of context in the alarm reaction of the grass-cutting ant, Atta capiguara. Behav Ecol Sociobiol 49:503–508CrossRefGoogle Scholar
  30. Hughes WOH, Howse PE, Vilela EF, Goulson D (2001) The response of grass-cutting ants to natural and synthetic versions of their alarm pheromone. Physiol Entomol 26:165–172CrossRefGoogle Scholar
  31. Hughes WOH, Sumner S, Van Borm S, Boomsma JJ (2003) Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proc Natl Acad Sci U S A 100:9394–9397CrossRefPubMedGoogle Scholar
  32. Hughes WOH, Thomsen L, Eilenberg J, Boomsma JJ (2004) Diversity of entomopathogenic fungi near leaf-cutting ant nests in a Neotropical forest, with particular reference to Metarhizium anisopliae var. anisopliae. J Invertebr Pathol 85:46–53CrossRefPubMedGoogle Scholar
  33. Jackson DE, Hart AG (2009) Does sanitation facilitate sociality? Anim Behav 77:e1–e5CrossRefGoogle Scholar
  34. Jeanson R, Clark RM, Holbrook CT, Bertram SM, Fewell JH, Kukuk PF (2008) Division of labour and socially induced changes in response thresholds in associations of solitary halictine bees. Anim Behav 76:593–602CrossRefGoogle Scholar
  35. Julian GE, Cahan S (1999) Undertaking specialization in the desert leaf-cutter ant Acromyrmex versicolor. Anim Behav 58:437–442CrossRefPubMedGoogle Scholar
  36. Linksvayer TA, McCall AC, Jensen RM, Marshall CM, Miner JW, McKone MJ (2002) The function of hitchhiking behavior in the leaf-cutting ant Atta cephalotes. Biotropica 34:93–100Google Scholar
  37. Little AEF, Currie CR (2008) Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants. Ecology 89:1216–1222CrossRefPubMedGoogle Scholar
  38. Michener CD (1974) The social behavior of bees. Harvard University Press, CambridgeGoogle Scholar
  39. Mikheyev AS, Vo T, Mueller UG (2008) Phylogeography of post-Pleistocene population expansion in a fungus-gardening ant and its microbial mutualists. Mol Ecol 17:4480–4488CrossRefPubMedGoogle Scholar
  40. Mueller UG, Dash D, Rabeling C, Rodrigues A (2008) Coevolution between attine ants and actinomycete bacteria: a reevaluation. Evolution 62:2894–2912CrossRefPubMedGoogle Scholar
  41. Orr MR (1992) Parasitic flies (Diptera, Phoridae) influence foraging rhythms and caste division of labor in the leaf-cutter ant, Atta cephalotes (Hymenoptera, Formicidae). Behav Ecol Sociobiol 30:395–402CrossRefGoogle Scholar
  42. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, PrincetonGoogle Scholar
  43. Page RE, Robinson GE, Britton DS, Fondrk MK (1992) Genotypic variability for rates of behavioral development in worker honeybees (Apis mellifera L). Behav Ecol 3:173–180CrossRefGoogle Scholar
  44. Pankiw T, Page RE (1999) The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Physiol A 185:207–213CrossRefPubMedGoogle Scholar
  45. Ravary F, Lecoutey E, Kaminski G, Chaline N, Jaisson P (2007) Individual experience alone can generate lasting division of labor in ants. Curr Biol 17:1308–1312CrossRefPubMedGoogle Scholar
  46. Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665CrossRefPubMedGoogle Scholar
  47. Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, PrincetonGoogle Scholar
  48. Seid M, Traniello J (2006) Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants. Behav Ecol Sociobiol 60:631–644CrossRefGoogle Scholar
  49. Smith CR, Toth AL, Suarez AV, Robinson GE (2008) Genetic and genomic analyses of the division of labour in insect societies. Nature Rev Gen 9:735–748CrossRefGoogle Scholar
  50. Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New YorkGoogle Scholar
  51. Theraulaz G, Bonabeau E, Deneubourg JL (1998) Response threshold reinforcement and division of labour in insect societies. Proc R Soc Lond B 265:327–332CrossRefGoogle Scholar
  52. Uribe-Rubio J, Guzmán-Novoa E, Vázquez-Peláez C, Hunt G (2008) Genotype, task specialization, and nest environment influence the stinging response thresholds of individual Africanized and European honeybees to electrical stimulation. Behav Genet 38:93–100CrossRefPubMedGoogle Scholar
  53. Walker TN, Hughes WOH (2009) Adaptive social immunity in leaf-cutting ants. Biol Lett 5:446–448CrossRefPubMedGoogle Scholar
  54. Weidenmuller A (2004) The control of nest climate in bumblebee (Bombus terrestris) colonies: interindividual variability and self reinforcement in fanning response. Behav Ecol 15:120–128CrossRefGoogle Scholar
  55. Wetterer JK (1999) The ecology and evolution of worker size-distribution in leaf-cutting ants (Hymenoptera: Formicidae). Sociobiology 34:119–144Google Scholar
  56. Wilson EO (1980a) Caste and division of labor in leaf-cutter ants (Hymenoptera, Formicidae, Atta). 2. The ergonomic optimization of leaf cutting. Behav Ecol Sociobiol 7:157–165CrossRefGoogle Scholar
  57. Wilson EO (1980b) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). I. The overall pattern in A. sexdens. Behav Ecol Sociobiol 7:143–156CrossRefGoogle Scholar
  58. Winston ML (1995) The biology of the honey bee. Harvard University Press, LondonGoogle Scholar
  59. Yackulic CB, Lewis OT (2007) Temporal variation in foraging activity and efficiency and the role of hitchhiking behaviour in the leaf-cutting ant, Atta cephalotes. Ent Exp Appl 125:125–134CrossRefGoogle Scholar
  60. Yanagawa A, Yokohari F, Shimizu S (2008) Defense mechanism of the termite, Coptotermes formosanus Shiraki, to entomopathogenic fungi. J Invertebr Pathol 97:165–170CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Institute of Integrative and Comparative BiologyUniversity of LeedsLeedsUK

Personalised recommendations