Skip to main content
SpringerLink
Log in

Do these eggs smell funny to you?: an experimental study of egg discrimination by hosts of the social parasite Polyergus breviceps (Hymenoptera: Formicidae)

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Social parasites exploit the behaviours of other social species. Infiltration of host systems involves a variety of mechanisms depending on the conditions within the host society and the needs of the social parasite. For many species of socially parasitic ants, colony establishment entails the usurpation of colonies of other species. This frequently involves the eviction or death of the host colony queen and the subsequent adoption of the invading queen. The social parasite queen achieves host worker acceptance by either manipulating the nest-mate recognition processes of the host or undergoing chemical modification. Little is known, however, about how host workers respond to social parasite eggs or whether host species defend against brood parasitism during parasite invasions. Host species are believed to adopt social parasite offspring because the recent common ancestry between many social parasites and their hosts may grant the sharing of certain characteristics such as chemical cues. Use of multiple host species, however, suggests other processes are needed for the social bond between host and parasite young to form. This study reports the findings of adoption bioassays in which eggs from a slave-maker ant, Polyergus breviceps, were offered to workers of two of its host species from unparasitised or newly parasitised nests to determine whether P. breviceps eggs generally elicit rearing behaviours from multiple host species. Comparisons of parasite egg survival until adulthood with conspecific egg survival reveal that workers of both host species, free-living or newly enslaved, do not typically accept slave-maker eggs. Both host species thus have sufficient discriminatory power to reject social parasite eggs although our hydrocarbon analysis indicates parasite eggs may be adapted to their local host species. Combined these results suggest that host rearing of P. breviceps eggs may reflect an evolutionary equilibrium that is maintained by probability and cost of recognition errors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Figure 3
Fig. 4

Similar content being viewed by others

References

  • Agosti D (1994) A new inquiline ant (Hymenoptera: Formicidae) in Cataglyphis and its phylogenetic relationship. J Nat Hist 28:913–919

    Google Scholar 

  • Akino T, Knapp JJ, Thomas JA, Elmes GW (1999) Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proc R Soc Lond B 266:1419–1426

    Article  CAS  Google Scholar 

  • Alloway TM (1982) How the slave-making ant Harpagoxenus americanus (Emery) affects the pupa-acceptance behavior of its slaves. In: Breed MD, Michener CD, Evans HE (eds) The biology of social insects. Westview, Boulder, Colo., pp 261–265

  • Ayasse M, Paxton RJ (2002) Brood protection in social insects. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell, Berlin, pp 117–148

  • Bagnères AG, Lorenzi MC, Dusticier G, Turillazzi S, Clement JL (1996) Chemical usurpation of a nest by paper wasp parasites. Science 272:889–892

    PubMed  Google Scholar 

  • Bhatkar A, Whitcomb WH (1970) Artificial diet for rearing various species of ants. Fla Entomol 53:229–232

    Google Scholar 

  • Bourke AFG (1994) Indiscriminate egg cannibalism and reproductive skew in a multiple-queen ant. Proc R Soc Lond 255:55–59

    Google Scholar 

  • Bourke AFG, Franks NR (1991) Alternative adaptations, sympatric speciation and the evolution of parasitic, inquiline ants. Biol J Linnean Soc 43:157–178

    Google Scholar 

  • Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton, N.J.

  • Breed MD, Snyder LE, Lynn TL, Morhart JA (1992) Acquired chemical camouflage in a tropical ant. Anim Behav 44:519–523

    Google Scholar 

  • Cox DR (1972) Regression models and life-tables with discussion. J R Stat Soc B 34:187–220

    Google Scholar 

  • Crozier RH, Dix MW (1979) Analysis of two genetic models for the innate components of colony odor in social Hymenoptera. Behav Ecol Sociobiol 47:217–224

    Google Scholar 

  • Davies NB, Brooke MdL (1989) An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination. J Anim Ecol 58:207–224

    Google Scholar 

  • Davies NB, Bourke AFG, Brooke MdL (1989) Cuckoos and parasitic ants: interspecific brood parasitism as an evolutionary arms race. Trends Evol Ecol 4:274–278

    Article  Google Scholar 

  • Dawkins R (1982) The extended phenotype. Oxford University Press, Oxford

  • D’Ettorre P, Errard C (1998) Chemical disguise during colony founding in the dulotic ant Polyergus rufescens Latr. (Hymenoptera, Formicidae). Insect Soc Life 2:71–77

    Google Scholar 

  • D’Ettorre P, Heinze J (2001) Sociobiology of slave-making ants. Acta Ethol 3:67–82

    Article  Google Scholar 

  • D’Ettorre P, Errard C, Ibarra F, Francke W, Hefetz A (2000) Sneak in or repel your enemy: Dufour’s gland repellent as a strategy for successful usurpation in the slave-maker Polyergus rufescens. Chemoecology 10:135–142

    Google Scholar 

  • D’Ettorre P, Mondy N, Lenoir A, Errard C (2002) Blending in with the crowd: social parasites integrate into their host colonies using a flexible chemical signature. Proc R Soc Lond B 269:1911–1918

    Article  PubMed  Google Scholar 

  • Elmes GW, Barr B, Thomas JA, Clarke RT (1999) Extreme host specificity by Microdon mutabilis (Diptera: Syrphidae), a social parasite of ants. Proc R Soc Lond B 266:447–453

    Article  Google Scholar 

  • Emery C (1909) Über den Ursprung der dulotischen, parasitischen und myrmekophilen Ameisen. Biol Zentralbl 29:352–362

    Google Scholar 

  • Errard C, D’Ettorre P (1998) Camouflage chimique chez la reine de Polyergus rufescens lors de la fondation. Actes Colloq Insect Soc 11:137–144

    Google Scholar 

  • Foitzik S, Herbers JM (2001) Colony structure of a slave-makig ant. II. Frequency of slave raids and impact on the host population. Evolution 55:316–323

    CAS  PubMed  Google Scholar 

  • Foitzik S, DeHeer CJ, Hunjan DN, Herbers JM (2001) Coevolution in host–parasite systems: behavioural strategies of slave-making ants and their hosts. Proc R Soc Lond 268:1139–1146

    Article  CAS  Google Scholar 

  • Franks N, Blum M, Smith RK, Allies AB (1990) Behavior and chemical disguise of the cuckoo ant Leptothorax kutterii in relation to its host Leptothorax acervorum. J Chem Ecol 16:1431–1444

    CAS  Google Scholar 

  • Gause GF (1935) The struggle for existence. Williams and Wilkins, Baltimore

  • Gladstone DE (1981) Why there are no ant slave rebellions. Am Nat 117:779–781

    Article  Google Scholar 

  • Goodloe L, Topoff H (1987) Pupa acceptance by slaves of the socially-parasitic ant Polyergus (Hymenoptera: Formicidae). Psyche 94:293–302

    Google Scholar 

  • Hannonen M, Sundström L (2003) Worker nepotism among polygynous ants. Nature 421:910

    Article  CAS  PubMed  Google Scholar 

  • Howard RW, Stanley-Samuelson DW, Akre R (1990) Biosynthesis and chemical mimicry of cuticular hydrocarbons from the obligate predator, Microdon albicomatus Novak (Diptera: Syrphidae) and its ant prey, Myrmica incompleta Provancher (Hymenoptera: Formicidae). J Kans Entomol Soc 63:437–443

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Belknap, Cambridge, Mass.

  • Isingrini M, Lenoir A, Jaisson P (1985) Preimaginal learning as a basis of colony–brood recognition in the ant Cataglyphis cursor. Proc Nat Acad Sci USA 82:8545–8547

    Google Scholar 

  • Jaisson P (1987) The construction of fellowship between nestmates in social Hymenoptera. Experientia [Suppl] 54:313–331

  • Jaisson P, Fresneau D (1978) The sensitivity and responsiveness of ants to their cocoons in relation to age and methods of measurement. Anim Behav 26:1064–1071

    Google Scholar 

  • Johnson CA, Vander Meer RK, Lavine B (2001) Changes in the cuticular hydrocarbon profile of the slave-maker ant queen, Polyergus breviceps Emery, after killing a Formica host queen (Hymenoptera: Formicidae). J Chem Ecol 27:1787–1804

    Google Scholar 

  • Johnson CA, Topoff H, Vander Meer RK, Lavine B (2002) Host queen killing by a slave-maker ant queen: when is a host queen worth attacking? Anim Behav 64:807–815

    Article  Google Scholar 

  • Kaib M, Heinze J, Ortius D (1993) Cuticular hydrocarbon profiles in the slave-making ant Harpagoxenus sublaevis and its hosts. Naturwissenschaften 80:281–285

    CAS  Google Scholar 

  • Lahav S, Soroker V, Hefetz A, Vander Meer RK (1999) Direct behavioral evidence for hydrocarbons as ant recognition discriminators. Naturwissenschaften 86:246–249

    Article  CAS  Google Scholar 

  • Lawes MJ, Marthews TR (2003) When will rejection of parasite nestlings by hosts of nonevicting avian brood parasites be favored? A misimprinting-equilibrium model. Behav Ecol 14:757–770

    Article  Google Scholar 

  • Lenoir A, Fresneau D, Errard C, Hefetz A (1999) Individuality and colonial identity in ants: the emergence of the social representation concept. In: Detrain C, Deneubourg JL, Pasteels J (eds) Information processing in social insects. Birkhäuser, Basel, pp 219–237

  • Lenoir A, D’Ettorre P, Errard C (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599

    Article  CAS  PubMed  Google Scholar 

  • Lorenzi M C, Filippone F (2000) Opportunistic discrimination of alien eggs by social wasps (Polistes biglumis, Hymenoptera Vespidae): a defense against social parasitism? Behav Ecol Sociobiol 48:402–406

    Article  Google Scholar 

  • Lotem A, Nakamura H, Zahavi A (1995) Constraints on egg discrimination and cuckoo-host co-evolution. Anim Behav 49:1185–1209

    Article  Google Scholar 

  • Monnin T, Peeters C (1997) Cannibalism of subordinates’ eggs in the monogynous queenless ant Dinoponera quadriceps. Naturwissenschaften 84:499–502

    Article  CAS  Google Scholar 

  • Mori A, D’Ettorre P, Le Moli F (1995) Host nest usurpation and colony foundation in the European amazon ant, Polyergus rufescens Latr. (Hymenoptera: Formicidae). Insectes Soc 42:279–286

    Google Scholar 

  • Mori A, Grasso DA, Visicchio R, Le Moli F (2000a) Colony founding in Polyergus rufescens: the role of the Dufour’s gland. Insectes Soc 47:7–10

    Article  Google Scholar 

  • Mori A, Visicchio R, Sledge MF, Grasso DA, Le Moli F, Turillazzi S, Spencer S, Jones GR (2000b) Behavioral assays testing the appeasement allomone of Polyergus rufescens queens during host-colony usurpation. Ethol Ecol Evol 12:315–322

    Google Scholar 

  • Oliveira PS, Hölldobler B (1991) Agonistic interactions and reproductive dominance in Pachycondyla obscuricornis. Psyche 98:215–225

    Google Scholar 

  • Otto M (1999) Chemometrics. Wiley, New York

  • Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc R Soc Lond B 266:1323–1327

    Article  CAS  Google Scholar 

  • Plateaux L (1985) Adoption expérimentale entre des formis de genres différents Myrmica laevinodis Nylanderi et Anergates atratulus Schenk. Insectes Soc 32:221–226

    Google Scholar 

  • Ratnieks FLW (1995) Evidence for a queen-produced egg-marking pheromone and its use in worker policing in the honey bee. J Apic Res 34:31–37

    Google Scholar 

  • Savolainen R, Vepsäläinen K (2003) Sympatric speciation through intraspecific social parasitism. Proc Natl Acad Sci USA 100:7169–7174

    Article  CAS  PubMed  Google Scholar 

  • Schumann R, Buschinger A (1991) Selective acceptance of alien host species pupae by slaves of the dulotic ant, Harpagoxenus sublaevis (Hymenoptera, Formicidae, Myrmicinae). Ethology 88:154–162

    Google Scholar 

  • Singer TL (1998) Roles of hydrocarbons in the recognition systems of insects. Am Zool 38:394–405

    CAS  Google Scholar 

  • Sumner S, Aanen DK, Delabie J, Boomsma JJ (2004) The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery’s rule. Insectes Soc 51:37–42

    Article  Google Scholar 

  • Thompson JN (1994) The coevolutionary process. The University of Chicago Press, Chicago

  • Topoff H, Cover S, Greenberg L, Goodloe L, Sherman P (1988) Colony founding by queens of the obligatory slave-making ant, Polyergus breviceps: the role of the Dufour’s gland. Ethology 78:209–218

    Google Scholar 

  • Topoff H, Weickert T, Zimmerli EJ (1990) A comparative study of colony takeover between queens of facultative and obligatory slave-making ants (Hymenoptera: Formicidae). J Insect Behav 3:813–817

    Google Scholar 

  • Vander Meer RK, Morel L (1998) Nestmate recognition in ants. In: Vander Meer RK, Breed M, Winston M, Espelie KE (eds) Pheromone communication in social insects. Westview, Boulder, Colo., pp 79–103

  • Vander Meer RK, Jouvenaz DP, Wojcik DP (1989) Chemical mimicry in a parasitoid (Hymenoptera: Eucharitidae) of fire ants (Hymenoptera: Formicidae). J Chem Ecol 15:2247–2261

    Google Scholar 

  • Vienne C, Soroker V, Hefetz A (1995) Congruency of hydrocarbon patterns in heterospecific groups of ants: transfer and/or biosynthesis? Insectes Soc 42:267–277

    Google Scholar 

  • Wagner D, Brown MJF, Broun P, Cuevas W, Moses LE, Chao DL, Gordon DM (1998) Task-related differences in the cuticular hydrocarbon composition of harvester ants, Pogonomyrmex barbatus. J Chem Ecol 24:2021–2037

    Article  CAS  Google Scholar 

  • Yamaoka R (1990) Chemical approach to understanding interactions among organisms. Physiol Ecol Jpn 27:31–52

    Google Scholar 

  • Zimmerli EJ, Mori A (1993) The role of an attractive brood pheromone in the obligatory, slavemaking ant, Polyergus breviceps (Hymenoptera: Formicidae). J Insect Behav 6:761–770

    Google Scholar 

Download references

Acknowledgements

Field research was conducted at the Southwestern Research Station (SWRS) of the American Museum of Natural History, Portal, Ariz. Behavioural tests were conducted at SWRS, Hunter College, New York, N.Y. and the American Museum of Natural History, New York, N.Y. The chemical analyses were carried out at the Medical and Veterinary Entomology Research Laboratory of the United States Department of Agriculture. We thank Michele Hosack for her assistance in the chemical laboratory, Erica Gallegos for her assistance with initial nest egg monitoring, James Carpenter for comments on an early version of the manuscript, and David Nash, Lotta Sundström, Alain Lenoir, two anonymous reviewers and Joan Herbers and her laboratory for comments on a later version of the manuscript. Parts of this research were aided by grants from the Animal Behavior Society, Sigma Xi, Southwestern Research Station Student Support Fund, Theodore Roosevelt Memorial Fund and by a fellowship from the Biopsychology subprogram at Hunter College to C.A. Johnson.

Author information

Author notes

  1. Christine A. Johnson

    Present address: Department of Evolution Ecology and Organismal Biology, The Ohio State University, 314 Aronoff Laboratory, 318 W 12th Street, Columbus, OH 43210, USA

Authors and Affiliations

  1. Department of Psychology, The Graduate School and University Center of the City University of New York, New York, USA

    Christine A. Johnson & Howard Topoff

  2. Medical and Veterinary Entomology Research Laboratory, Agricultural Research Service, United States Department of Agriculture, Gainesville, Florida, USA

    Robert K. Vander Meer

  3. Department of Chemistry, Clarkson University, Potsdam, New York, USA

    Barry Lavine

Authors
  1. Christine A. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Howard Topoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert K. Vander Meer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Barry Lavine
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christine A. Johnson.

Additional information

Communicated by L. Sundström

Rights and permissions

Reprints and permissions

About this article

Cite this article

Johnson, C.A., Topoff, H., Vander Meer, R.K. et al. Do these eggs smell funny to you?: an experimental study of egg discrimination by hosts of the social parasite Polyergus breviceps (Hymenoptera: Formicidae). Behav Ecol Sociobiol 57, 245–255 (2005). https://doi.org/10.1007/s00265-004-0851-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-004-0851-0

Keywords

Search

Navigation