Skip to main content
SpringerLink
Log in

Alkaloid Venom Weaponry of Three Megalomyrmex Thief Ants and the Behavioral Response of Cyphomyrmex costatus Host Ants

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Social parasites exploit other societies by invading and stealing resources. Some enter protected nests using offensive chemical weaponry made from alkaloid-based venom. We characterized the venoms of three Megalomyrmex thief ant species (M. mondabora, M. mondaboroides, and M. silvestrii) that parasitize the fungus-growing ants, and developed an ethogram to describe host ant reactions to raiding M. mondaboroides and M. silvestrii parasites. We compared piperidine, pyrrolidine, and pyrolizidine venom alkaloid structures with synthetic samples from previous studies, and describe the novel stereochemistry of trans 2-hexyl-5-[8-oxononyl]-pyrrolidine (3) from M. mondabora. We showed that workers of Cyphomyrmex costatus, the host of M. mondaboroides and M. silvestrii, react to a sting by Megalomyrmex parasites mainly with submissive behavior, playing dead or retreating. Host submission also followed brief antennal contact. The behavior of C. costatus ants observed in this study was similar to that of Cyphomyrmex cornutus, host of M. mondabora, suggesting that the alkaloidal venoms with pyrrolidines from M. mondabora, piperidines from M. mondaboroides, and pyrolizidines from M. silvestrii may function similarly as appeasement and repellent allomones against host ants, despite their different chemical structure. With the use of these chemical weapons, the Megalomyrmex thief ants are met with little host resistance and easily exploit host colony resources.

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
Scheme 1
Fig. 3

Similar content being viewed by others

References

  • Adams ES, Traniello JFA (1981) Chemical interference competition by Monomorium minimum (Hymenoptera: formicidae). Oecologia 51:265–270. doi:10.1007/BF00540612

    Article  Google Scholar 

  • Adams RMM, Liberti J, Illum AA, Jones TH, Nash DR, Boomsma JJ (2013) Chemically armed mercenary ants protect fungus-farming societies. Proc Natl Acad Sci U S A 110:15752–15757. doi:10.1073/pnas.1311654110

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Adams RMM, Longino JT (2007) Nesting biology of the arboreal fungus-growing ant Cyphomyrmex cornutus and behavioral interactions with the social-parasitic ant Megalomyrmex mondabora. Insects Soc 54:136–143. doi:10.1007/s00040-007-0922-0

    Article  Google Scholar 

  • Adams RMM, Mueller UG, Holloway AK, Green AM (2000a) Garden sharing and garden stealing in fungus-growing ants. Naturwissenschaften 87:491–493

    Article  CAS  PubMed  Google Scholar 

  • Adams RMM, Mueller UG, Schultz TR, Norden B (2000b) Agro-predation: usurpation of attine fungus gardens by Megalomyrmex ants. Naturwissenschaften 87:549–554

    Article  CAS  PubMed  Google Scholar 

  • Adams RMM, Shah K, Antonov LD, Mueller UG (2012) Fitness consequences of nest infiltration by the mutualist-exploiter Megalomyrmex adamsae. Ecol Entomol 37:453–462. doi:10.1111/j.1365-2311.2012.01384.x

    Article  Google Scholar 

  • Akino T (2008) Chemical strategies to deal with ants: a review of mimicry, camouflage, propaganda, and phytomimesis by ants (Hymenoptera: formicidae) and other arthropods. Myrmecol News 11:173–181

    Google Scholar 

  • Allies AB, Bourke AFG, Franks NR (1986) Propaganda substances in the cuckoo ant Leptothorax kutteri and the slave-maker Harpagoxenus sublaevis. J Chem Ecol 12:1285–1293

    Article  CAS  PubMed  Google Scholar 

  • Anderson AN, Blum MS, Jones TH (1991) Venom alkaloids in Monomorium “rothsteini” Forel repel other ants: is this the secret to success by Monomorium in Australian ant communities? Oecologia 88:157–160

    Article  Google Scholar 

  • Barke J, Seipke RF, Gruschow S, Heavens D, Drou N, Bibb MJ, Goss RJ, Yu DW, Hutchings MI (2010) A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biol 8:109. doi:10.1186/1741-7007-8-109

    Article  PubMed Central  PubMed  Google Scholar 

  • Blum MS, Jones TH, Hölldobler B, Fales HM, Jaouni T (1980) Alkaloidal venom mace: offensive use by a thief ant. Naturwissenschaften 67:144–145

    Article  CAS  Google Scholar 

  • Boudinot BE, Sumnicht TP, Adams RMM (2013) Central American ants of the genus Megalomyrmex Forel (Hymenoptera: Formicidae): six new species and keys to workers and males. Zootaxa 3732:1–82

    Article  PubMed  Google Scholar 

  • Carlin NF, Hölldobler B (1987) The kin recognition system of carpenter ants (Camponotus spp.). Behav Ecol Sociobiol 20:209–217. doi:10.1007/BF00299735

    Article  Google Scholar 

  • Crewe RM, Blum MS (1972) Alarm pheromones of the Attini: their phylogenetic significance. J Insect Physiol 18:31–42. doi:10.1016/0022-1910(72)90062-5

    Article  CAS  Google Scholar 

  • Currie C, Scott J, Summerbell R, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–705

    Article  CAS  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. doi:10.1007/PL00001815

    Article  Google Scholar 

  • Daly J (1995) The chemistry of poisons in amphibian skin. Proc Natl Acad Sci U S A 92:9–13

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • De Souza DJ, Soares IMF, Della Lucia TMC (2007) Acromyrmex ameliae sp. n. (Hymenoptera: formicidae): a new social parasite of leaf-cutting ants in Brazil. Insect Sci 14:251–257. doi:10.1111/j.1744-7917.2007.00151.x

    Article  Google Scholar 

  • Dijkstra MB, Boomsma JJ (2003) Gnamptogenys hartmani wheeler (Ponerinae: ectatommini): an agro-predator of Trachymyrmex and Sericomyrmex fungus-growing ants. Naturwissenschaften 90:568–571. doi:10.1007/s00114-003-0478-4

    Article  CAS  PubMed  Google Scholar 

  • Escoubas P, Blum MS (1990) The biological activities of ant-derived alkaloids. In: Vander Meer RK, Jaffe K, Cedeno A (eds) Applied myrmecology. Westview Press, Boulder, Colorado, pp 482–489

    Google Scholar 

  • Francke W, Schröder F, Walter F, Sinnwell V, Baumann H, Kaib M (1995) New alkaloids from ants: identification and synthesis of (3R,5S,9R)-3-butyl-5-(1-oxopropy1)indolizidine and (3R,5R,9R)-3-butyl-5-(1-oxopropyl)indolizidine, constituents of the poison gland secretion in Myrmicaria. Liebigs Ann 6:965–977

    Article  Google Scholar 

  • Garraffo HM, Simon L, Daly J, Spande TF, Jones TH (1994) Cis- and trans-configurations of α, α’-disubstituted piperidines and pyrrolidines by GC-FTIR; application to decahydroquinoline stereochemistry. Tetrahedron 50:11329–11338

    Article  CAS  Google Scholar 

  • Gorman J, Jones T, Spande T, Snelling R, Torres J, Garraffo H (1998) 3-hexyl-5-methylindolizidine isomers from thief ants, Solenopsis (Diplorhoptrum) species. J Chem Ecol 24:933–943

    Article  CAS  Google Scholar 

  • Guillem R, Drijfhout F, Martin S (2014) Chemical deception among ant social parasites. Curr Zool 60:62–75

    Google Scholar 

  • Hermann H, Moser J, Hunt A (1970) The hymenopterous poison apparatus. X. Morphological and behavioral changes in Atta texana (Hymenoptera: Formicidae). Ann Entomol Soc Am 63:1552–1558

    Article  Google Scholar 

  • Hölldobler B (1973) Chemische strategie beim nahrungserwerb der diebsameise (Solenopsis fugax Latr.) und der Pharaoameise (Monomorium pharaonis L.). Oecologia 11:371–380

    Article  Google Scholar 

  • Hölldobler B, Wilson E (1990) The ants. Belknap Press of Harvard University Press, Cambridge, p 198

    Book  Google Scholar 

  • Ishak HD, Miller JL, Sen R, Dowd SE, Meyer E, Mueller UG (2011) Microbiomes of ant castes implicate new microbial roles in the fungus-growing ant Trachymyrmex septentrionalis. Sci Rep 1:204. doi:10.1038/srep00204

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jones T, Blum M, Howard R (1982a) Venom chemistry of ants in the genus Monomorium. J Chem Ecol 8:285–300

    Article  CAS  PubMed  Google Scholar 

  • Jones T, Highet R, Blum M, Fales H (1984) (5Z, 9Z)-3-alkyl-5-methylindolizidines from Solenopsis (Diplorhoptrum) species. J Chem Ecol 10:1233–1249

    Article  CAS  PubMed  Google Scholar 

  • Jones TH, Blum MS, Fales HM (1982b) Ant venom alkaloids from Solenopsis and Monomorium species recent developments. Tetrahedron 38:1949–1958

    Article  CAS  Google Scholar 

  • Jones TH, Blum MS, Fales HM, Brandão CRF, Lattke J (1991a) Chemistry of venom alkaloids in the ant genus Megalomyrmex. J Chem Ecol 17:1897–1908. doi:10.1007/BF00993736

    Article  CAS  PubMed  Google Scholar 

  • Jones TH, DeVries PJ, Escoubas P (1991b) Chemistry of venom alkaloids in the ant Megalomyrmex foreli (Myrmicinae) from Costa Rica. J Chem Ecol 17:2507–2518

    Article  CAS  PubMed  Google Scholar 

  • Jones TH, Torres J, Spande T, Garraffo H, Blum M, Snelling R (1996) Chemistry of venom alkaloids in some Solenopsis (Diplorhoptrum) species from Puerto Rico. J Chem Ecol 22:1221–1236

    Article  CAS  PubMed  Google Scholar 

  • Jones TH, Wojciechowski T, Snelling R, Torres J, Chacón P, DeVreis P (1999) Dialkylpyrrolidines from the ants Megalomyrmex cyendyra Brandão and M. latreillei Emery. Caribb J Sci 35:310–311

    Google Scholar 

  • Jouvenaz DP, Blum MS, MacConnell JG (1972) Antibacterial activity of venom alkaloids from the imported fire ant, Solenopsis invicta Buren. Antimicrob Agents Chemother 2:291–293

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kang S, Kim W, Moon B (1985) An effective method for the preparation of ω-bromoalkanols from α, ω-diols. Synthesis 12:1161–1162

    Article  Google Scholar 

  • Leclercq S, Braekman JC, Daloze D, Pasteels JM, Van der Meer RK (1996) Biosynthesis of the Solenopsins, venom alkaloids of the fire ants. Naturwissenschaften 83:222–225

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li S, Jin X, Chen J (2012) Effects of piperidine and piperideine alkaloids from the venom of red imported fire ants, Solenopsis invicta Buren, on Pythium ultimum Trow growth in vitro and the application of piperideine alkaloids to control cucumber damping-off in the greenhouse. Pest Manag Sci 68:1546–1552. doi:10.1002/ps.3337

    Article  CAS  PubMed  Google Scholar 

  • Longino JT (2010) A taxonomic review of the ant genus Megalomyrmex Forel (Hymenoptera: Formicidae) in Central America. Zootaxa 2720:35–58

    Google Scholar 

  • Martin SJ, Drijfhout FP (2009) Nestmate and task cues are influenced and encoded differently within ant cuticular hydrocarbon profiles. J Chem Ecol 35:368–374. doi:10.1007/s10886-009-9612-x

    Article  CAS  PubMed  Google Scholar 

  • Morgan ED (2004) Biosynthesis in insects. R Soc Chem Cambridge. doi:10.1039/9781847550262

    Google Scholar 

  • Mori A, Visicchio R, Sledge M (2000) Behavioural assays testing the appeasement allomone of Polyergus rufescens queens during host-colony usurpation. Ethol Ecol Evol 12:315–322

    Article  Google Scholar 

  • Mueller UG (2012) Symbiont recruitment versus ant-symbiont co-evolution in the attine ant-microbe symbiosis. Curr Opin Microbiol 15:269–277. doi:10.1016/j.mib.2012.03.001

    Article  PubMed  Google Scholar 

  • Mueller UG, Rehner SA, Schultz TR (1998) The evolution of agriculture in ants. Science 281:2034–2038

    Article  CAS  PubMed  Google Scholar 

  • Obin MS, Vander Meer RK (1985) Gaster flagging by fire ants (Solenopsis spp.): functional significance of venom dispersal behavior. J Chem Ecol 11:1757–1768

    Article  CAS  PubMed  Google Scholar 

  • Rabeling C, Cover SP, Johnson RA, Mueller UG (2007) A review of the North American species of the fungus-gardening ant genus Trachymyrmex (Hymenoptera: formicidae). Zootaxa 1664:1–53

    Google Scholar 

  • Rashid T, Chen J, McLeod P (2013) Toxicity of newly isolated piperideine alkaloids from the red imported fire ant, Solenopsis invicta Buren, against the green peach aphid, Myzus persicae (Sulzer). Adv Entomol 01:20–23. doi:10.4236/ae.2013.12005

    Article  Google Scholar 

  • Regnier FE, Wilson EO (1971) Chemical communication and “propaganda” in slave-maker ants. Science 172:267–269

    Article  CAS  PubMed  Google Scholar 

  • Ruano F, Devers S, Sanllorente O, Errard C, Tinaut A, Lenoir A (2011) A geographical mosaic of coevolution in a slave-making host-parasite system. J Evol Biol 24:1071–1079. doi:10.1111/j.1420-9101.2011.02238.x

    Article  CAS  PubMed  Google Scholar 

  • Saporito RA, Garraffo HM, Donnelly MA, Edwards AL, Longino JT, Daly JW (2004) Formicine ants: an arthropod source for the pumiliotoxin alkaloids of dendrobatid poison frogs. Proc Natl Acad Sci U S A 101:8045–8050. doi:10.1073/pnas.0402365101

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schoenian I, Spiteller M, Ghaste M, Wirth R, Herz H, Spiteller D (2011) Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proc Natl Acad Sci U S A 108:1955–1960. doi:10.1073/pnas.1008441108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci USA 105:5435–5440

  • Schultz TR, Bekkevold D, Boomsma JJ (1998) Acromyrmex insinuator new species: an incipient social parasite of fungus-growing ants. Insects Soc 45:457–471. doi:10.1007/s000400050101

    Article  Google Scholar 

  • Seipke RF, Barke J, Brearley C, Hill L, Yu DW, Goss RJM, Hutchings MI (2011) A single Streptomyces symbiont makes multiple antifungals to support the fungus farming ant Acromyrmex octospinosus. PLoS ONE 6:e22028. doi:10.1371/journal.pone.0022028

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shik JZ, Kaspari M (2010) More food, less habitat: how necromass and leaf litter decomposition combine to regulate a litter ant community. Ecol Entomol 35:158–165. doi:10.1111/j.1365-2311.2009.01165.x

    Article  Google Scholar 

  • Snyder AJ, Jones TH, Snelling GC, Snelling RR (2009) Venom alkaloids from some Monomorium species. J Hymenopt Res 18:145–150

    Google Scholar 

  • Soler J, Martínez J, Soler M, Møller A (2001) Life history of magpie populations sympatric or allopatric with the brood parasitic great spotted cuckoo. Ecology 82:1621–1631

    Article  Google Scholar 

  • Svensson EI, Råberg L (2010) Resistance and tolerance in animal enemy-victim coevolution. Trends Ecol Evol 25:267–274. doi:10.1016/j.tree.2009.12.005

    Article  PubMed  Google Scholar 

  • Termonia A, Pasteels JM, Windsor DM, Milinkovitch MC (2002) Dual chemical sequestration: a key mechanism in transitions among ecological specialization. Proc R Soc B Biol Sci 269:1–6. doi:10.1098/rspb.2001.1859

    Article  CAS  Google Scholar 

  • Vander Meer RK (2012) Ant interactions with soil organisms and associated semiochemicals. J Chem Ecol 38:728–745. doi:10.1007/s10886-012-0140-8

    Article  CAS  PubMed  Google Scholar 

  • Ward PS, Brady SG, Fisher BL, Schultz TR (2015) The evolution of myrmicine ants: phylogeny and biogeography of a hyperdiverse ant clade (Hymenoptera: formicidae). Syst Entomol 40:61–81. doi:10.1111/syen.12090

    Article  Google Scholar 

  • Wheeler WM (1907) The fungus-growing ants of North America. Bull Am Mus Nat Hist 23:669–807

    Google Scholar 

  • Zamora-Munoz C, Ruano F, Errard C, Lenoir A, Hefetz A, Tinaut A (2003) Coevolution in the slave-parasite system Proformica longiseta-Rossomyrmex minuchae (Hymenoptera: formicidae). Sociobiology 42:299–317

    Google Scholar 

Download references

Acknowledgments

We thank the Smithsonian Tropical Research Institute and the Organization for Tropical Studies and La Selva Biological Station in Costa Rica for providing facilities and logistical help; the Autoridad Nacional del Ambiente y el Mar and Ministerio de Ambiente, Energía y Telecomunicaciones for permission to sample ants and to export them. We thank Rozlyn E. Haley for illustrations in Fig. 1. This work was funded by a Marie Curie International Incoming Fellowship (237266 – ANCEPS) and National Science Foundation DDIG award DEB-0508698 to RMMA and DEB-0072702 (Project ALAS) to JTL. THJ acknowledges the support of the VMI Chemistry Department. Some collections and field assistance were generously provided by Janni Larson, Christian Peeters, Hermógenes Fernández-Marín, Adam Kay, and Gaspar Bruner, while Janni Larson and Astrid Blok van Witteloostuijn cared for the live colonies. Phil Lester and two anonymous reviewers provided helpful comments.

Author information

Authors and Affiliations

  1. Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark

    Rachelle M. M. Adams

  2. Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC, 20560, USA

    Rachelle M. M. Adams

  3. Department of Chemistry, Virginia Military Institute, Lexington, VA, 24450, USA

    Tappey H. Jones & Robert G. Weatherford

  4. Department of Biology, University of Utah, Salt Lake City, UT, 84112, USA

    John T. Longino

  5. Section of Integrative Biology, University of Texas at Austin, Austin, TX, 78712, USA

    Ulrich G. Mueller

Authors
  1. Rachelle M. M. Adams
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tappey H. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John T. Longino
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert G. Weatherford
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ulrich G. Mueller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rachelle M. M. Adams.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Adams, R.M.M., Jones, T.H., Longino, J.T. et al. Alkaloid Venom Weaponry of Three Megalomyrmex Thief Ants and the Behavioral Response of Cyphomyrmex costatus Host Ants. J Chem Ecol 41, 373–385 (2015). https://doi.org/10.1007/s10886-015-0565-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-015-0565-y

Keywords

Search

Navigation