Insectes Sociaux

, Volume 62, Issue 2, pp 121–132 | Cite as

Ectaheteromorph ants also host highly diverse parasitic communities: a review of parasitoids of the Neotropical genus Ectatomma

Review Article


Despite the diversity of ant-myrmecophile associations, there are few examples of primary parasitism of ants and these are poorly documented, particularly in genera with only a few species such as the genus Ectatomma. We identified 18 associations that involve at least 16 taxa of primary parasitoids distributed in three families belonging to two invertebrate classes, and five of the 15 valid Ectatomma species. Among these, we report for the first time an endoparasitoid fly (probably a phorid) that attacks E. ruidum larvae and constitutes the second record of ant-larva endoparasitism by a dipteran. We provide a brief account of the interactions of these organisms with their hosts and their possible impact at the colonial or population level. Ectatomma ants, though being a small group, serve as a remarkable resource for the evolution of a wide variety of parasitoid organisms which, comparatively, are much more important than those associated with better-studied ant genera such as Myrmica or Formica. Considering the lack of studies dedicated to their parasites and parasitoids, the available information (almost limited to the three most studied Ectatomma species) suggests that, in spite of both their carnivorous diet and the aggressiveness typical of their workers, the diversity of these associations with Ectatomma might be much more important than previously expected. We stress the urgency of performing detailed inventories focused on these associations, not only for the genus Ectatomma, but for all the poorly studied ant communities (ectaheteromorphs, poneromorphs, arboreal ants) and endangered species.


Host-parasitoid interactions Ectatomma Phoridae Eucharitidae Mermithidae Inventory 

Supplementary material

40_2015_390_MOESM1_ESM.docx (98 kb)
Supplementary material 1 (DOCX 99 kb)


  1. AntWeb. Available from Accessed 17 November 2014
  2. Arias-Penna T.M. 2008. Subfamilia Ectatomminae. In: Sistemática, Biogeografía y Conservación de las Hormigas Cazadoras de Colombia (Jiménez E., Fernández F., Arias T.M. and Lozano-Zambrano F.H., Eds), Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá. pp 53–107Google Scholar
  3. Baker G.L. and Poinar G.O. Jr. 1995. Agamermis catadecaudata n. sp. (Nematoda: Mermithidae), a parasitoid of Orthoptera in south-eastern Australia. Fundam. Appl. Nematol. 18: 139–148Google Scholar
  4. Bolton B. 2003. Synopsis and classification of Formicidae. Mem. Am. Entomol. Inst. 71: 1–370Google Scholar
  5. Brady S.G., Schultz T.R., Fisher B.L. and Ward P.S. 2006. Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc. Natl Acad. Sci. USA 103: 18172–18177Google Scholar
  6. Breed M.D., Cook C. and Krasnec M.O. 2012. Cleptobiosis in social insects. Psyche 2012: Article ID 484765, 7 pagesGoogle Scholar
  7. Brown B.V. 2000. Revision of the “Apocephalus miricauda-group” of ant-parasitizing flies (Diptera: Phoridae). Contrib. Sci. 482: 1–62Google Scholar
  8. Brown B.V. and Feener D.H. Jr. 1991. Behavior and host location cues of Apocephalus paraponerae (Diptera: Phoridae), a parasitoid of the giant tropical ant, Paraponera clavata (Hymenoptera: Formicidae). Biotropica 23: 182–187Google Scholar
  9. Brown B.V. and Feener D.H. Jr. 1998. Parasitic phorid flies (Diptera: Phoridae) associated with army ants (Hymenoptera: Formicidae: Ecitoninae, Dorylinae) and their conservation biology. Biotropica 30: 482–487Google Scholar
  10. Brown B.V., Bragança M.A.L., Gomes D.S., Queiros J.M. and Teixeira M.C. 2012. Parasitoid phorid flies (Diptera: Phoridae) from the threatened leafcutter ant Atta robusta Borgmeier (Hymenoptera: Formicidae). Zootaxa 3385: 33–38Google Scholar
  11. Brown W.L. Jr. 1958. Contributions toward a reclassification of the Formicidae. II. Tribe Ectatommini (Hymenoptera). Bull. Mus. Comp. Zool. 118: 175–362Google Scholar
  12. Carey B., Visscher K. and Heraty J. 2012. Nectary use for gaining access to an ant host by the parasitoid Orasema simulatrix (Hymenoptera, Eucharitidae). J. Hym. Res. 27: 47–65Google Scholar
  13. Clausen C.P. 1941. The habits of the Eucharidae. Psyche 48: 57–69Google Scholar
  14. Cockerell T.D.A. 1909. A new braconid of the genus Elasmosoma. Proc. Entomol. Soc. Washington 10: 168–169Google Scholar
  15. Coman D. 1953. Mermithide freatice în fauna Republicii Populare România, Studii cercet. ştiinţ. 4: 123–152Google Scholar
  16. Cook O.F. 1904. Notes on the habits of the Kelep, or Guatemalan cotton-boll-weevil ant. USDA Bull. # 49, pp 15Google Scholar
  17. Cook O.F. 1905. The social organization and breeding habits of the cotton-protecting Kelep of Guatemala. USDA Techn. Ser. 10: 1–55Google Scholar
  18. Coovert G.A. 2005. The ants of Ohio (Hymenoptera: Formicidae). Ohio Biol. Survey Bull. N.S. 15: 1–196Google Scholar
  19. Csősz S. 2012. Nematode infection as significant source of unjustified taxonomic descriptions in ants (Hymenoptera: Formicidae). Myrmecol. News 17: 27–31Google Scholar
  20. Csősz S. and Majoros G. 2009. Ontogenic origin of mermithogenic Myrmica phenotypes (Hymenoptera, Formicidae). Insect. Soc. 56: 70–76Google Scholar
  21. Czechowski W., Czechowska W. and Radchenko A. 2007a. Strikingly malformed host morphology: Myrmica rugulosa Nyl. and Myrmica sabuleti Mein. (Hymenoptera: Formicidae) parasitised by mermithid nematodes. Fragm. Faun. 50: 139–148Google Scholar
  22. Czechowski W., Radchenko A. and Czechowska W. 2007b. Mermithid infestation strikingly alters the morphology of Myrmica rubra (L.) (Hymenoptera: Formicidae): possible taxonomical involvements. Ann. Zool. 57: 325–330Google Scholar
  23. Darling D.C. 2009. A new species of Smicromorpha (Hymenoptera, Chalcididae) from Vietnam, with notes on the host association of the genus. ZooKeys 20: 155–163Google Scholar
  24. Davidson D.W. and Fisher B.L. 1991. Symbiosis of ants with Cecropia as a function of light regime. In: AntPlant Interactions (Huxley C.R. and Cutler D.F., Eds), Oxford University Press, Oxford. pp 289-309Google Scholar
  25. Disney R.H.L. 1979. Natural history notes on some British Phoridae (Diptera) with comments on a changing picture. Entomol. Gaz. 30: 140–150Google Scholar
  26. Disney R.H.L. 1994. Scuttle Flies: The Phoridae. Chapman and Hall, LondonGoogle Scholar
  27. Disney R.H.L. 2000. Revision of European Pseudacteon Coquillet (Diptera, Phoridae). Bonn. Zool. Beitr. 49: 79–91Google Scholar
  28. Disney R.H.L. 2002. Revisionary notes and new key to Aenigmatias Meinert (Diptera, Phoridae). Fragm. Faun. 45: 67–72Google Scholar
  29. Donisthorpe H.St.J.K. 1910. Myrmecophilous notes for 1909. Entomol. Rec. J. Var. 22: 15–17Google Scholar
  30. Donisthorpe H.St.J.K. 1913a. Aenigmatias blattoides Meinert, captured in Scotland. Entomol. Rec. J. Var. 25: 277–278Google Scholar
  31. Donisthorpe H.St.J.K. 1913b. Rare myrmecophilous Diptera. Proc. Entomol. Soc. Lond. 1913: lxxv-lxxvi.Google Scholar
  32. Donisthorpe H.St.J.K. 1914. Some notes on the genera Platyphora and Aenigmatias and a species new to Britain. Entomol. Rec. J. Var. 26: 276–278Google Scholar
  33. Donisthorpe H.St.J.K. 1915. British Ants, Their Life-History & Classification. William Brendon and Son Limited, PlymouthGoogle Scholar
  34. Donisthorpe H.St.J.K. 1927. The Guests of British Ants: Their Habits and Life-Histories. G. Routledge and Sons, LondonGoogle Scholar
  35. Dupont S. and Pape T. 2007. Fore tarsus attachment device of the male scuttle fly, Aenigmatias lubbockii. J. Insect Sci. 7:54.Google Scholar
  36. Eggleton P. and Belshaw R. 1992. Insect parasitoids: an evolutionary overview. Phil. Trans. R. Soc. Lond. B 337: 1–20Google Scholar
  37. Eggleton P. and Gaston K.J. 1990. “Parasitoid” species and assemblages: convenient definitions or misleading compromises? Oikos 59: 417–421Google Scholar
  38. Emery C. 1890. Studii sulle formiche della fauna neotropica. I. Formiche di Costa Rica. Boll. Soc. Entomol. Ital. 22: 33–80Google Scholar
  39. Fahringer J. 1936. Opuscula braconologica. Band 4. Palaearktischen Region. Lieferung 1-3. Opusc. Braconol. 1935: 1–276Google Scholar
  40. Falk S.J. and Chandler P.J. 2005. A review of the scarce and threatened flies of Great Britain. Part 2: Nematocera and Aschiza not dealt with by Falk (1991). Species Status 2: 1–189Google Scholar
  41. Feener D.H. Jr. 2000. Is the assembly of ant communities mediated by parasitoids? Oikos 90: 79–88Google Scholar
  42. Feener D.H. Jr. and Brown B.V. 1997. Diptera as parasitoids. Annu. Rev. Entomol. 42: 73–97Google Scholar
  43. Feener D.H. Jr., Jacobs L.F. and Schmidt J.O. 1996. Specialized parasitoids attracted to a pheromone of ants. Anim. Behav. 51: 61–66Google Scholar
  44. Fénéron R., Poteaux C., Boilève M., Valenzuela J. and Savarit F. 2013. Discrimination of the social parasite Ectatomma parasiticum by its host sibling species (E. tuberculatum). Psyche 2013: Article ID 573541, 11 pagesGoogle Scholar
  45. Fernández F. 1991. Las hormigas cazadoras de género Ectatomma (Formicidae: Ponerinae) en Colombia. Caldasia 16: 551–564Google Scholar
  46. Folgarait P.J. 2013. Leaf-cutter ant parasitoids: current knowledge. Psyche 2013: Article ID 539780, 10 pagesGoogle Scholar
  47. Forel A. 1874. Les fourmis de la Suisse. Systématique. Notices anatomiques et physiologiques. Architecture. Distribution géographique. Nouvelles expériences et observations de moeurs. Neue Denkschriften der Allgemeinen Schweizerischen Gesellschaft für di gesammten Naturwissenschaften 26: 1–452Google Scholar
  48. Forel A. 1890. Un parasite de la Myrmecia forficata Fabr. Ann. Soc. Entomol. Belg. 34: 8–10Google Scholar
  49. Gahan A.B. 1940. A contribution to the knowledge of the Eucharidae (Hymenoptera: Chalcidoidea). Proc. U.S. Natl Mus. 88: 425–458Google Scholar
  50. Gaston K.J. 1991. The magnitude of global insect species richness. Conserv. Biol. 5: 283–296Google Scholar
  51. Gaulle J. de 1907. Catalogue systématique & biologique des Hyménoptères de France, suite. Feuille Jeunes Nat. 37: 185–189Google Scholar
  52. Giraud J. 1871. Note sur l’Elasmosoma berolinense et description d’une espèce nouvelle (viennense) du même genre. Ann. Soc. Entomol. Fr. 1871: 299–302Google Scholar
  53. Goater T.M., Goater C.P. and Esch G.W. 2014. Parasitism: The Diversity and Ecology of Animal Parasites, 2nd edn. Cambridge University Press, CambrigeGoogle Scholar
  54. Godfray H.C.J. 1994. Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, New JerseyGoogle Scholar
  55. Godfray H.C.J. 2007. Parasitoids. In: Encyclopedia of Biodiversity (Levin S. Ed.), Academic Press. pp 1–13Google Scholar
  56. Gómez Durán J.-M. and van Achterberg C. 2011. Oviposition behaviour of four ant parasitoids (Hymenoptera, Braconidae, Euphorinae, Neoneurini and Ichneumonidae, Hybrizontinae), with the description of three new European species. ZooKeys 125: 59–106Google Scholar
  57. González C.T., Wcislo W.T., Wheeler T., Cambra R. and Fernández-Marín H. 2014. Pseudogaurax sp. (Chloropidae) a novel ectoparasitoid fly to ants, attacking the fungus-growing ant, Apterostigma dentigerum (Hymenoptera: Formicidae). In: Memorias 41° Congreso de la Sociedad Colombiana de Entomología (Rodríguez J., Ed.), SOCOLEN 2014, Cali, Colombia. p. 40Google Scholar
  58. González V.V.E., Gómez L.L.A., and Mesa C.N.C. 2004. Observaciones sobre la biología y comportamiento del ácaro Macrodinychus sellnicki (Mesostigmata: Uropidae) ectoparasitoide de la hormiga loca Paratrechina fulva (Hymenoptera: Formicidae). Rev. Colomb. Entomol. 30: 143–149Google Scholar
  59. Gösswald K. 1930. Weitere Beiträge zur Verbreitung der Mermithiden bei Ameisen. Zool. Anz. 90: 13–21Google Scholar
  60. Gösswald K. 1934. Über Ameisengäste und –schmarotzer des mittleren Maingebiets. Entomol. Z. 48: 125–127Google Scholar
  61. Gösswald K. 1938. Über bisher unbekannte, durch den Parasitismus der Mermithiden (Nemat.) verursachte Formveränderungen bei Ameisen. Z. Parasit. 10: 138–151Google Scholar
  62. Gösswald K. 1950. Pflege des Ameisenparasiten Tamiclea globula Meig. (Dipt.) durch den Wirt mit Bemerkungen über den Stoffwechsel in der parasitierten Ameise. Verhandl. Deutsch. Zool. 1949: 256–264Google Scholar
  63. Guénard B., Weiser M.D. and Dunn R.R. 2012. Global models of ant diversity suggest regions where new discoveries are most likely are under disproportionate deforestation threat. Proc. Natl Acad. Sci. USA 109: 7368–7373Google Scholar
  64. Hagmeier A. 1912. Beitrage zur Kenntnis der Mermithiden. I. Biologische Notizen und systematische Bechreibung einiger alter und neuer Arten. Zool. Jahrb. Abt. Syst. Geogr. Biol. Tiere 32: 521–612Google Scholar
  65. Hamilton A.J., Basset Y., Benke K.K., Grimbacher P.S., Miller S.E., Novotný V., Samuelson G.A., Stork N.E., Weible G.D. and Yen J.D.L. 2010. Quantifying uncertainty in estimation of tropical arthropod species richness. Am. Nat. 176: 90–95Google Scholar
  66. Heraty J.M. 1998. The genus Dilocantha (Hymenoptera: Eucharitidae). Proc. Entomol. Soc. Washington 100: 72–87Google Scholar
  67. Heraty J.M. 2002. A revision of the genera of Eucharitidae (Hymenoptera: Chalcidoidea) of the world. Mem. Am. Entomol. Inst. 68: 1–367Google Scholar
  68. Heraty J.M. 2009. Parasitoid biodiversity and insect pest management. In: Insect Biodiversity: Science and Society (Foottit R.G. and Adler P.H. Eds), Wiley-Blackwell, Chichester. pp 445–462Google Scholar
  69. Hölldobler B. and Wilson E.O. 1990. The Ants. Harvard University Press, Cambridge, MassachusettsGoogle Scholar
  70. Howard R.W., Pérez-Lachaud G. and Lachaud J.-P. 2001. Cuticular hydrocarbons of Kapala sulcifacies (Hymenoptera: Eucharitidae) and its host, the ponerine ant Ectatomma ruidum (Hymenoptera: Formicidae). Ann. Entomol. Soc. Am. 94: 707–716Google Scholar
  71. Huddleston T. 1976. A revision of Elasmosoma Ruthe (Hymenoptera, Braconidae) with two new species from Mongolia. Ann. Hist.-Nat. Mus. Nation. Hung. 68: 215–225Google Scholar
  72. Hughes D.P., Pierce N.E. and Boomsma J.J. 2008. Social insect symbionts: evolution in homeostatic fortresses. Trends Ecol. Evol. 23: 672–677Google Scholar
  73. Ibarra-Núñez G., García J.A., López J.A. and Lachaud J.-P. 2001. Prey analysis in the diet of some ponerine ants (Hymenoptera: Formicidae) and web-building spiders (Araneae) in coffee plantations in Chiapas, Mexico. Sociobiology 37: 723–755Google Scholar
  74. Jaffe K., Pavis C., Vansuyt G. and Kermarrec A. 1989. Ants visit extrafloral nectaries of the orchid Spathoglotis plicata Blume. Biotropica 21: 278–279CrossRefGoogle Scholar
  75. Kathirithamby J. 2009. Host-parasitoid associations in Strepsiptera. Annu. Rev. Entomol. 54: 227–249Google Scholar
  76. Keller L. 1995. Parasites, worker polymorphism, and queen number in social insects. Am. Nat. 145: 842–847Google Scholar
  77. Kistner D.H. 1982. The social insects’ bestiary. In: Social Insects, vol. 3 (Hermann H.R. Ed.), Academic Press, New York, New York. pp 1–244Google Scholar
  78. Kloft W. 1949. Ü-ber den Einfluss von Mermisparasitismus auf den Stoffwechsel und die Organbildung bei Ameisen. Z. Parasit. 14: 390–422Google Scholar
  79. Komatsu T. and Konishi K. 2010. Parasitic behaviors of two ant parasitoid wasps (Ichneumonidae: Hybrizontinae). Sociobiology 56: 575–584Google Scholar
  80. Lachaud J.-P. and Pérez-Lachaud G. 2009. Impact of natural parasitism by two eucharitid wasps on a potential biocontrol agent ant in southeastern Mexico. Biol. Control 48: 92–99Google Scholar
  81. Lachaud J.-P. and Pérez-Lachaud G. 2012. Diversity of species and behavior of hymenopteran parasitoids of ants: a review. Psyche 2012: Article ID 134746, 24 pagesGoogle Scholar
  82. Lachaud J.-P., Cerdan P. and Pérez-Lachaud G. 2012a. Poneromorph ants associated with parasitoid wasps of the genus Kapala Cameron (Hymenoptera: Eucharitidae) in French Guiana. Psyche 2012: Article ID 393486, 6 pagesGoogle Scholar
  83. Lachaud J.-P., Lenoir A. and Hughes D.P. (eds.). 2013. Ants and Their Parasites 2013. Psyche Special Issue. Hindawi Publishing Corporation, New York, New YorkGoogle Scholar
  84. Lachaud J.-P., Lenoir A. and Witte V. (eds.). 2012b. Ants and Their Parasites. Psyche Special Issue. Hindawi Publishing Corporation, New York, New YorkGoogle Scholar
  85. Lachaud J.-P., López Méndez J.A., Schatz B., De Carli P. and Beugnon G. 1996. Comparison de l’impact de prédation de deux ponérines du genre Ectatomma dans un agroécosystème néotropical. Actes Coll. Insect. Soc. 10: 67–74Google Scholar
  86. Lachaud J.-P., Pérez-Lachaud G. and Heraty J.M. 1998. Parasites associated with the ponerine ant Ectatomma tuberculatum (Hymenoptera: Formicidae): First host record for the genus Dilocantha (Hymenoptera: Eucharitidae). Fla Entomol. 81: 570–574Google Scholar
  87. Lapola D.M., Antonialli Júnior W.F. and Giannotti E. 2003. Arquitetura de ninhos da formiga neotropical Ectatomma brunneum F. Smith, 1858 (Formicidae, Ponerinae) em ambientes alterados. Rev. Bras. Zooci. 5: 177–188Google Scholar
  88. Le Breton J., Takaku G. and Tsuji K. 2006. Brood parasitism by mites (Uropodidae) in an invasive population of the pest-ant Pheidole megacephala. Insect. Soc. 53: 168–171Google Scholar
  89. Lima L.D. and Antonialli-Junior W.F. 2013. Foraging strategies of the ant Ectatomma vizottoi (Hymenoptera, Formicidae). Rev. Bras. Entomol. 57: 392–396Google Scholar
  90. Longino J. 2014. AntWeb. Available from: Accessed 17 November 2014.
  91. Marshall T.A. 1899. I. A monograph of British Braconidae. Part VIII. Trans. Entomol. Soc. Lond. 47: 1–79Google Scholar
  92. Moreau C.S. and Bell C.D. 2013. Testing the museum versus cradle tropical biological diversity hypothesis: phylogeny, diversification, and ancestral biogeographic range evolution of the ants. Evolution 67: 2240–2257Google Scholar
  93. Morehead S.A. and Feener D.H. Jr. 2000a. An experimental test of potential host range in the ant parasitoid Apocephalus paraponerae. Ecol. Entomol. 25: 332–340Google Scholar
  94. Morehead S.A. and Feener Jr. D.H. 2000b. Visual and chemical cues used in host location and acceptance by a dipteran parasitoid. J. Insect Behav. 13: 613–625Google Scholar
  95. Morehead S.A., Seger J., Feener Jr. D.H. Jr. and Brown B.V. 2001. Evidence for a cryptic species complex in the ant parasitoid Apocephalus paraponerae (Diptera: Phoridae). Evol. Ecol. Res. 3: 273–284Google Scholar
  96. Morley C. 1909. Notes on Braconidae, X.: On the Pachylommatinae, with descriptions of new species. Entomol. Month. Mag. 45: 209–214Google Scholar
  97. Muesebeck C.F.W. 1941. A new ant parasite (Hymenoptera, Braconidae). Bull. Brooklyn Entomol. Soc. 36: 200–201Google Scholar
  98. Naug D. and Camazine S. 2002. The role of colony organization on pathogen transmission in social insects. J. Theor. Biol. 215: 427–439Google Scholar
  99. Nickle W.R. and Jouvenaz D.P. 1987. Tetradonema solenopsis n. sp. (Nematoda: Tetradenomatidae) parasitic on the red imported fire ant Solenopsis invicta Buren from Brazil. J. Nematol. 19: 311–313Google Scholar
  100. Olivier E. 1893. Notes entomologiques. Bull. Séanc. Bull. Bibliogr. Soc. Entomol. Fr. 1: lxx-lxxiGoogle Scholar
  101. Parmentier T., Dekoninck W. and Wenseleers T. 2014. A highly diverse microcosm in a hostile world: a review on the associates of red wood ants (Formica rufa group). Insect. Soc. 61: 229–237Google Scholar
  102. Passera L. 1976. Origine des intercastes dans les sociétés de Pheidole pallidula (Nyl.) (Hymenoptera Formicidae) parasitées par Mermis sp. (Nematoda Mermithidae). Insect. Soc. 23: 559–576Google Scholar
  103. Passera L., Lachaud J.-P. and Gomel L. 1994. Individual food source fidelity in the neotropical ponerine ant Ectatomma ruidum Roger (Hymenoptera Formicidae). Ethol. Ecol. Evol. 6: 13–21Google Scholar
  104. Pérez-Lachaud G. and Lachaud J.-P. 2014. Arboreal ant colonies as ‘hot-points’ of cryptic diversity for myrmecophiles: the weaver ant Camponotus sp. aff. textor and its interaction network with its associates. PLoS ONE 9:e100155.Google Scholar
  105. Pérez-Lachaud G., Gates M.W. and Lachaud J.-P. 2013. New host record for Camponotophilus delvarei (Hymenoptera: Eurytomidae), a parasitoid of microdontine larvae (Diptera: Syrphidae), associated with the ant Camponotus sp. aff. textor. Psyche 2013: Article ID 230601, 6 pagesGoogle Scholar
  106. Pérez-Lachaud G., Heraty J.M., Carmichael A. and Lachaud J.-P. 2006a. Biology and behavior of Kapala (Hymenoptera: Eucharitidae) attacking Ectatomma, Gnamptogenys, and Pachycondyla (Formicidae: Ectatomminae and Ponerinae) in Chiapas, Mexico. Ann. Entomol. Soc. Am. 99: 567–576Google Scholar
  107. Pérez-Lachaud G., Jervis M.A., Reemer M. and Lachaud J.-P. 2014. An unusual, but not unexpected, evolutionary step taken by syrphid flies: the first record of true primary parasitoidism of ants by Microdontinae. Biol. J. Linn. Soc. 111: 462–472Google Scholar
  108. Pérez-Lachaud G., López-Méndez J.A. and Lachaud J.-P. 2006b. Eucharitid parasitism of the Neotropical ant Ectatomma tuberculatum: parasitoid co-occurrence, seasonal variation, and multiparasitism. Biotropica 38: 574–576Google Scholar
  109. Pérez-Lachaud G., López-Méndez J.A., Beugnon G., Winterton P. and Lachaud J.-P. 2010. High prevalence but relatively low impact of two eucharitid parasitoids attacking the Neotropical ant Ectatomma tuberculatum (Olivier). Biol. Control 52: 131–139Google Scholar
  110. Pérez-Lachaud G., Noyes J. and Lachaud J.-P. 2012. First record of an encyrtid wasp (Hymenoptera: Chalcidoidea) as a true primary parasitoid of ants (Hymenoptera: Formicidae). Fla Entomol. 95: 1066–1076Google Scholar
  111. Pérez-Lachaud G., Valenzuela J.E. and Lachaud J.-P. 2011. Is increased resistance to parasitism at the origin of polygyny in a Mexican population of the ant Ectatomma tuberculatum (Hymenoptera: Formicidae)? Fla Entomol. 94: 677–684Google Scholar
  112. Philpott S.M., Perfecto I., Vandermeer J. and Uno S. 2009. Spatial scale and density dependence in a host parasitoid system: an arboreal ant, Azteca instabilis, and its Pseudacteon phorid parasitoid. Environ. Entomol. 38: 790–796Google Scholar
  113. Pie M.R. 2004. Foraging ecology and behaviour of the ponerine ant Ectatomma opaciventre Roger in a Brazilian savannah. J. Nat. Hist. 38: 717–729Google Scholar
  114. Poinar G. Jr. 2004. Behaviour and development of Elasmosoma sp. (Neoneurinae: Braconidae: Hymenoptera), an endoparasite of Formica ants (Formicidae: Hymenoptera). Parasitol. 128: 521–531Google Scholar
  115. Poinar G. Jr. 2012. Nematode parasites and associates of ants: past and present. Psyche 2012: Article ID 192017, 13 pagesGoogle Scholar
  116. Poinar G. Jr. and Yanoviak S.P. 2008. Myrmeconema neotropicum n. g., n. sp., a new tetradonematid nematode parasitising South American populations of Cephalotes atratus (Hymenoptera: Formicidae), with the discovery of an apparent parasite-induced host morph. Syst. Parasitol. 69: 145–153Google Scholar
  117. Poinar Jr. G., Lachaud J.-P., Castillo A. and Infante F. 2006. Recent and fossil nematode parasites (Nematoda: Mermithidae) of Neotropical ants. J. Invertebr. Pathol. 91: 19–26Google Scholar
  118. Poteaux C., Prada-Achiardi F.C., Fernández F. and Lachaud J.-P. (in press). Diversidade genética e fenotípica no gênero Ectatomma. In: Poneromorfas do Brasil (Delabie J.H.C., Feitosa R., Serrão J.E., Mariano C. and Majer J., Eds)Google Scholar
  119. Quicke D.L.J. 1997. Parasitic Wasps. Chapman and Hall, LondonGoogle Scholar
  120. Rettenmeyer C.W., Rettenmeyer M.E., Joseph J. and Berghoff S.M. 2011. The largest animal association centered on one species: the army ant Eciton burchellii and its more than 300 associates. Insect. Soc. 58: 281–292Google Scholar
  121. Reuter O.M. 1913. Lebensgewohnheiten und Instinkte der Insekten bis zum Erwachen der Sozialen Instinkte. R. Friedländer & Sohn, BerlinGoogle Scholar
  122. Rocha F.H., Lachaud J.-P. and Pérez-Lachaud G. 2014. Fine individual specialization and elitism among workers of the ant Ectatomma tuberculatum for a highly specific task: intruder removal. Ethology 120: 1185–1198Google Scholar
  123. Ruschka F. 1924. Die europäisch-mediterranen Eucharidinae und Perilampinae. (Hym. Chalc.). [Der Chalcididenstudien IV. und V. Teil.]. Deutsche Entomol. Z. 41: 82–96Google Scholar
  124. Ruthe J.F. 1858. Beiträge zur Kenntniss der Braconiden. Berl. Entomol. Z. 2: 1–10Google Scholar
  125. Schmid-Hempel P. 1998. Parasites in Social Insects. Monographs in Behavior and Ecology. Princeton University Press, Princeton, New JerseyGoogle Scholar
  126. Schmiedeknecht O. 1914. Die Schlupfwespen (Ichneumonidea). In: Die Insekten Mitteleuropas insbesondere Deutschlands. Zweiter Band. Hymenopteren Zweiter Teil (Schröder C., Ed.), Franckh’sche Verlagshanlung, Stuttgart, Germany. pp 113–256Google Scholar
  127. Schmitz H. 1914. Die myrmecophilen Phoriden der Wasmann’schen Sammlung. Zool. Jahrb. 37: 509–566Google Scholar
  128. Schmitz H. 1941. Zwei neue Aenigmatistes aus Abessinien, nebst einem Verzeichnis aller bisher beschriebenen Aenigmatiinae. Natuurhist. Maandbl. 30: 104–108Google Scholar
  129. Shaw S.R. 1992. Seven new North American species of Neoneurus (Hymenoptera: Braconidae). Proc. Entomol. Soc. Washington 94: 26–47Google Scholar
  130. Shaw S.R. 1993. Observations on the ovipositional behavior of Neoneurus mantis, an ant-associated parasitoid from Wyoming (Hymenoptera: Braconidae). J. Insect Behav. 6: 649–658Google Scholar
  131. Shaw S.R. 2007. A new species of Elasmosoma Ruthe (Hymenoptera: Braconidae: Neoneurinae) from the northwestern United States associated with the western thatching ants, Formica obscuripes Forel and Formica obscuriventris clivia Creighton (Hymenoptera: Formicidae). Proc. Entomol. Soc. Washington 109: 1–8Google Scholar
  132. Tang C., Gu J., Li Q. 1999. Observation on the mermithid larvae from Formica gagates and Amphimermis chinensis in ant colony soil in Korquing pasture of inner Mongolia. Sichuan J. Zool. 18: 152–156Google Scholar
  133. Tobias V.I. 1971. Obzor naezdnikov-brakonid (Hymenoptera) fauny SSSR. Trud. Vsesoy. Entomol. Obshch. 54: 156–268Google Scholar
  134. Torréns J. 2013. A review of the biology of Eucharitidae (Hymenoptera: Chalcidoidea) from Argentina. Psyche 2013: Article ID 926572, 14 pagesGoogle Scholar
  135. Torréns J. and Heraty J.M. 2012. Description of the species of Dicoelothorax Ashmead (Chalcidoidea, Eucharitidae) and biology of D. platycerus Ashmead. ZooKeys 165: 33–46Google Scholar
  136. Vandel A. 1930. La production d’intercastes chez la fourmi Pheidole pallidula sous l’action des parasites du genre Mermis. 1. Étude morphologique des individus parasites. Bull. Biol. Fr. Belg. 64: 457-494Google Scholar
  137. Vander Meer R.K., Jouvenaz D.P. and Wojcik D.P. 1989. Chemical mimicry in a parasitoid (Hymenoptera: Eucharitidae) of fire ants (Hymenoptera: Formicidae). J. Chem. Ecol. 15: 2247–2261Google Scholar
  138. Varone L., Heraty J.M. and Calcaterra L.A. 2010. Distribution, abundance and persistence of species of Orasema (Hym: Eucharitidae) parasitic on fire ants in South America. Biol. Control 55: 72–78Google Scholar
  139. Wagner H.C., Koschuh A., Schatz I. and Stalling T. 2012. Die Myrmecophilen einer Lawinenrinne im Nationalpark Gesäuse (Steiermark). Abhandl. Zool.-Bot. Gesellsch. Österreich 38: 147–161Google Scholar
  140. Wasmann E. 1894. Kritisches Verzeichniss der myrmekophilen und termitophilen Arthropoden. Mit Angabe der Lebensweise und mit Beschreibung neuer Arten. Verlag von Felix L. Dames, Berlin, GermanyGoogle Scholar
  141. Wasmann E. 1899. Die psychischen Fähigkeiten der Ameisen. Zoologica 11: 1-133 (1909).Google Scholar
  142. Wasmann E. 1908. Weitere Beiträge zum sozialen Parasitismus und der Sklaverei bei den Ameisen. Biol. Zentralbl. 28: 726–731Google Scholar
  143. Watanabe C. 1935. On two hymenopterous guests of ants in Japan. Ins. Matsumurana 9: 90–94Google Scholar
  144. Weber N.A. 1946. Two common ponerine ants of possible economic significance, Ectatomma tuberculatum (Olivier) and E. ruidum Roger. Proc. Entomol. Soc. Washington 48: 1–16Google Scholar
  145. Wheeler G.C. and Wheeler J. 1952. The ant larvae of the subfamily Ponerinae—Part I. Am. Midl. Nat. 48: 111–144Google Scholar
  146. Wheeler G.C. and Wheeler J.N. 1986. The Ants of Nevada. Natural History Museum of Los Angeles County, Los Angeles, CaliforniaGoogle Scholar
  147. Wheeler W.M. 1907. The polymorphism of ants, with an account of some singular abnormalities due to parasitism. Bull. Am. Mus. Nat. Hist. 23: 1–93Google Scholar
  148. Wheeler W.M. 1910. Ants, Their Structure, Development and Behavior. The Columbia University Press, New York, New YorkGoogle Scholar
  149. Wheeler W.M. 1930. Two mermithergates of Ectatomma. Psyche 37: 48–54Google Scholar
  150. Wilson E.O. 1971. The Insect Societies, Harvard University Press, Cambridge, MassachusettsGoogle Scholar
  151. Wise de Valdez M.R. 2006. Parasitoid-induced behavioral alterations of Aedes aegypti mosquito larvae infected with mermithid nematodes (Nematoda: Mermithidae). J. Vector Ecol. 31: 344–354Google Scholar
  152. Witek M., Barbero F. and Markó B. 2014. Myrmica ants host highly diverse parasitic communities: from social parasites to microbes. Insect. Soc. 61: 307–323Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2015

Authors and Affiliations

  1. 1.Departamento de Conservación de la BiodiversidadEl Colegio de la Frontera SurChetumalMexico
  2. 2.Centre de Recherches sur la Cognition AnimaleUniversité de Toulouse, Université Paul SabatierToulouse Cedex 09France
  3. 3.Centre National de la Recherche Scientifique, UMR 5169, CRCAToulouse Cedex 09France

Personalised recommendations