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Ant larvae regulate worker foraging behavior and ovarian activity in a dose-dependent manner

Behavioral Ecology and Sociobiology volume 70, pages 1011–1018 (2016)Cite this article

Abstract

Division of labor in insect societies relies on simple behavioral rules, whereby individual colony members respond to dynamic signals indicating the need for certain tasks to be performed. This in turn gives rise to colony-level phenotypes. However, empirical studies quantifying colony-level signal-response dynamics are lacking. Here, we make use of the unusual biology and experimental amenability of the queenless clonal raider ant Cerapachys biroi to jointly quantify the behavioral and physiological responses of workers to a social signal emitted by larvae. Using automated behavioral quantification and oocyte size measurements in colonies of different sizes and with different worker-to-larvae ratios, we show that the workers in a colony respond to larvae by increasing foraging activity and inhibiting ovarian activation in a progressive manner and that these responses are stronger in smaller colonies. This work adds to our knowledge of the processes that link plastic individual behavioral/physiological responses to colony-level phenotypes in social insect colonies.

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References

  • Amdam GV, Norberg K, Fondrk MK, Page RE (2004) Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc Natl Acad Sci U S A 101:11350–11355

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Arnold G, Le Conte Y, Trouiller J, Hervet H, Chappe B, Masson C (1994) Inhibition of worker honeybee ovaries development by a mixture of fatty-acid esters from larvae. Cr Acad Sci Iii-Vie 317:511–515

    CAS  Google Scholar 

  • Cassill DL, Tschinkel WR (1995) Allocation of liquid food to larvae via trophallaxis in colonies of the fire ant, Solenopsis invicta. Anim Behav 50:801–813

    Article  Google Scholar 

  • Cassill DL, Tschinkel WR (1999) Effects of colony-level attributes on larval feeding in the fire ant, Solenopsis invicta. Insectes Soc 46:261–266

    Article  Google Scholar 

  • Creemers B, Billen J, Gobin B (2003) Larval begging behaviour in the ant Myrmica rubra. Ethol Ecol Evol 15:261–272

    Article  Google Scholar 

  • den Boer S, Duchateau MJHM (2006) A larval hunger signal in the bumblebee Bombus terrestris. Insectes Soc 53:369–373

    Article  Google Scholar 

  • Dolezal AG, Johnson J, Hoelldobler B, Amdam GV (2013) Division of labor is associated with age-independent changes in ovarian activity in Pogonomyrmex californicus harvester ants. J Insect Physiol 59:519–524

    CAS  Article  PubMed  Google Scholar 

  • Dornhaus A, Powell S, Bengston S (2012) Group size and its effects on collective organization. Annu Rev Entomol 57:123–41

    CAS  Article  PubMed  Google Scholar 

  • Duarte A, Weissing FJ, Pen I, Keller L (2011) An evolutionary perspective on self-organized division of labor in social insects. Annu Rev Ecol Evol S 42:91–110

    Article  Google Scholar 

  • Field J, Paxton RJ, Soro A, Bridge C (2010) Cryptic plasticity underlies a major evolutionary transition. Curr Biol 20:2028–31

    CAS  Article  PubMed  Google Scholar 

  • Gautrais J, Theraulaz G, Deneubourg JL, Anderson C (2002) Emergent polyethism as a consequence of increased colony size in insect societies. J Theor Biol 215:363–373

    Article  PubMed  Google Scholar 

  • Heinze J (2008) The demise of the standard ant (Hymenoptera: Formicidae). Myrmecological News 11:9–20

    Google Scholar 

  • Heinze J, Trunzer B, Oliveira PS, Holldobler B (1996) Regulation of reproduction in the neotropical ponerine ant, Pachycondyla villosa. J Insect Behav 9:441–450

    Article  Google Scholar 

  • Holbrook CT, Barden PM, Fewell JH (2011) Division of labor increases with colony size in the harvester ant Pogonomyrmex californicus. Behav Ecol 22:960–966

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (2008) The superorganism: the beauty, elegance, and strangeness of insect societies, 1st edn. W.W. Norton, New York

    Google Scholar 

  • Kawatsu K (2013) Effect of nutritional condition on larval food requisition behavior in a subterranean termite Reticulitermes speratus (Isoptera: Rhinotermitidae). J Ethol 31:17–22

    Article  Google Scholar 

  • Keller L, Vargo EL (1993) Reproductive structure and reproductive roles in colonies of eusocial insects. In: Keller L (ed) Queen Number and Sociality in Insects. Oxford University Press, pp 16–44

  • Kronauer DJC, Pierce NE, Keller L (2012) Asexual reproduction in introduced and native populations of the ant Cerapachys biroi. Mol Ecol 21:5221–5235

    Article  PubMed  Google Scholar 

  • Le Conte Y, Mohammedi A, Robinson GE (2001) Primer effects of a brood pheromone on honeybee behavioural development. P Roy Soc B-Biol Sci 268:163–168

    Article  Google Scholar 

  • Leoncini I, Le Conte Y, Costagliola G, Plettner E, Toth AL, Wang MW, Huang Z, Becard JM, Crauser D, Slessor KN, Robinson GE (2004) Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees. Proc Natl Acad Sci U S A 101:17559–17564

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Mohammedi A, Paris A, Crauser D, Le Conte Y (1998) Effect of aliphatic esters on ovary development of queenless bees (Apis mellifera L.). Naturwissenschaften 85:455–458

    CAS  Article  Google Scholar 

  • Morel L, Vandermeer RK (1988) Do ant brood pheromones exist. Ann Entomol Soc Am 81:705–710

    Article  Google Scholar 

  • Oldroyd BP, Wossler TC, Ratnieks FLW (2001) Regulation of ovary activation in worker honey-bees (Apis mellifera): larval signal production and adult response thresholds differ between anarchistic and wild-type bees. Behav Ecol Sociobiol 50:366–370

    Article  Google Scholar 

  • Oxley PR, Ji L, Fetter-Pruneda I, McKenzie SK, Li C, Hu HF, Zhang GJ, Kronauer DJC (2014) The genome of the clonal raider ant Cerapachys biroi. Curr Biol 24:451–458

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Pankiw T, Huang Z-Y, Winston ML, Robinson GE (1998a) Queen mandibular gland pheromone influences worker honey bee (Apis mellifera L.) foraging ontogeny and juvenile hormone titers. J Insect Physiol 44:685–692

    Article  PubMed  Google Scholar 

  • Pankiw T, Page RE, Fondrk MK (1998b) Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behav Ecol Sociobiol 44:193–198

    Article  Google Scholar 

  • Ravary F (2002) The reproductive cycle of thelytokous colonies of Cerapachys biroi Forel (Formicidae, Cerapachyinae). Insectes Soc 49:114–119

    Article  Google Scholar 

  • Ravary F, Jaisson P (2004) Absence of individual sterility in thelytokous colonies of the ant Cerapachys biroi Forel (Formicidae, Cerapachyinae). Insectes Soc 51:67–73

    Article  Google Scholar 

  • Ravary F, Jahyny B, Jaisson P (2006) Brood stimulation controls the phasic reproductive cycle of the parthenogenetic ant Cerapachys biroi. Insectes Soc 53:20–26

    Article  Google Scholar 

  • Schafer RJ, Holmes S, Gordon DM (2006) Forager activation and food availability in harvester ants. Anim Behav 71:815–822

    Article  Google Scholar 

  • Siegel S, Castellan NJ (1988) In: Nonparametric statistics for the behavioural sciences. MacGraw Hill Int, New York, pp 213–214

    Google Scholar 

  • Teseo S, Kronauer DJC, Jaisson P, Chaline N (2013) Enforcement of reproductive synchrony via policing in a clonal ant. Curr Biol 23:328–332

    CAS  Article  PubMed  Google Scholar 

  • Thomas ML, Elgar MA (2003) Colony size affects division of labour in the ponerine ant Rhytidoponera metallica. Naturwissenschaften 90:88–92

    CAS  PubMed  Google Scholar 

  • Traynor KS, Le Conte Y, Page RE (2014) Queen and young larval pheromones impact nursing and reproductive physiology of honey bee (Apis mellifera) workers. Behav Ecol Sociobiol 68:2059–2073

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsuji K, Yamauchi K (1995) Production of females by parthenogenesis in the ant, Cerapachys Biroi. Insectes Soc 42:333–336

    Article  Google Scholar 

  • Villalta I, Angulo E, Devers S, Cerdá X, Boulay R (2015) Regulation of worker egg laying by larvae in a fission-performing ant. Anim Behav 106:149–156

    Article  Google Scholar 

  • Waters JS, Holbrook CT, Fewell JH, Harrison JF (2010) Allometric scaling of metabolism, growth, and activity in whole colonies of the seed-harvester ant Pogonomyrmex californicus. Am Nat 176:501–10

    Article  PubMed  Google Scholar 

  • Weidenmuller A (2004) The control of nest climate in bumblebee (Bombus terrestris) colonies: interindividual variability and self reinforcement in fanning response. Behav Ecol 15:120–128

    Article  Google Scholar 

  • West-Eberhard MJ (1996) Natural history and evolution of paper wasp. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper wasp. Oxford Univ. Press, New York, pp 290–317

    Google Scholar 

Download references

Acknowledgments

This work was supported by grant 1DP2GM105454-01 from the NIH, a Klingenstein-Simons Fellowship Award in the Neurosciences, and a Searle Scholar Award to D.J.C.K. Y.U. was supported by a Swiss National Science Foundation Advanced Postdoc Mobility Fellowship (P300P3-147900) and a Rockefeller University Women & Science Fellowship. D.B. was supported by the Rockefeller University Summer Undergraduate Research Fellowship Program. R.L. was supported by a Marie Curie International Outgoing Fellowship (PIOF-GA-2012-327992). Jonathan Saragosti helped design and build the setup used to acquire behavioral data.

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Authors and Affiliations

  1. Laboratory of Social Evolution and Behavior, The Rockefeller University, New York, NY, USA

    Yuko Ulrich, Dominic Burns, Romain Libbrecht & Daniel J. C. Kronauer

  2. Ant Lab, School of Biological Sciences, University of Bristol, Bristol, UK

    Dominic Burns

  3. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

    Romain Libbrecht

Authors
  1. Yuko Ulrich
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  2. Dominic Burns
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  3. Romain Libbrecht
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  4. Daniel J. C. Kronauer
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Corresponding author

Correspondence to Yuko Ulrich.

Additional information

This manuscript is a contribution to the special issue Integrative Analysis of Division of Labor—Guest Editors: Simon K. Robson, James F.A. Traniello.

Communicated by W. Hughes

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Ulrich, Y., Burns, D., Libbrecht, R. et al. Ant larvae regulate worker foraging behavior and ovarian activity in a dose-dependent manner. Behav Ecol Sociobiol 70, 1011–1018 (2016). https://doi.org/10.1007/s00265-015-2046-2

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  • DOI: https://doi.org/10.1007/s00265-015-2046-2

Keywords

  • Division of labor
  • Ovarian development
  • Automated behavioral analysis
  • Larvae
  • Social behavior
  • Social communication