Insectes Sociaux

, Volume 61, Issue 3, pp 229–237 | Cite as

A highly diverse microcosm in a hostile world: a review on the associates of red wood ants (Formica rufa group)

Review Article

Abstract

The importance of Eurasian red wood ants (RWAs) (Formica rufa group) in forest and heath ecosystems has long been recognized. One key function of RWAs is the role of their nests in supporting an intriguing ecosystem of a highly diverse group of obligate myrmecophiles and facultative guests. In this review we list 125 obligate arthropod myrmecophiles that occur in RWA mounds or in the near vicinity of the mounds. More than 40 % of them are Coleoptera, but also Hemiptera, Diptera, Hymenoptera, Acari and Araneae are well represented. RWAs are estimated to be the primary hosts for 49 species. 24 species were hitherto only recorded to be associated with RWAs, 12 with both RWAs and other mound-building Formica species and 9 were found to be associated with both mound-building and non-mound-building Formica species. The remaining associates are less specific and can be found with other ant genera or ant subfamilies. Other mound-building Formica ants (Coptoformica, F. uralensis and F. truncorum) support fewer species, most of which are known to also occur with RWAs. We discuss the biology of the different obligate myrmecophilous groups and give general notes on the facultative guests found in RWA mounds. We stress the importance of the conservation of RWAs as hosts of one of the richest and diverse associations known to date in insects.

Keywords

Red wood ants Formicidae Formica rufa group Myrmecophiles Ant guests Symbionts 

Supplementary material

40_2014_357_MOESM1_ESM.pdf (402 kb)
Supplementary material 1 (PDF 403 kb)

References

  1. 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: 173-181Google Scholar
  2. Andersson H. 1974. Studies on the myrmecophilous fly, Glabellula arctica (Zett.) (Dipt. Bombyliidae). Insect Syst. Evol. 5: 29-38Google Scholar
  3. Boer P. 2013. De Nederlandse mieren - species found in wood ant mounds in the Netherlands. <http://www.nlmieren.nl/websitepages/woodant%20mounds.html>, retrieved on 1 February 2014
  4. Bagnères A.-G. and Lorenzi M.C. 2010. Chemical deception/mimicry using cuticular hydrocarbons. In: Insect Hydrocarbons: Biology, Biochemistry and Chemical Ecology (Blomquist G.J. and Bagnères A.-G., Eds), Cambridge: Cambridge University Press. pp 282-324Google Scholar
  5. Brooks J.L. 1942. Notes on the ecology and the occurrence in America of the myrmecophilous sowbug, Platyarthus hoffmanseggi Brandt. Ecology 23: 427-437Google Scholar
  6. Chopard L. 1951. Faune de France Orthoptéroïdes. Paul Lechevalier, ParisGoogle Scholar
  7. Coenen-Stass D., Schaarschmidt B. and Lamprecht I. 1980. Temperature distribution and calorimetric determination of heat production in the nest of the wood ant, Formica polyctena (Hymenoptera, Formicidae). Ecology 61: 238-244Google Scholar
  8. Cushing P.E. 1997. Myrmecomorphy and myrmecophily in spiders: a review. Florida Entomol. 80: 165-193Google Scholar
  9. Davidson M. 2011. Some observations on the wood ant spider (Dipoena torva). <www.woodants.org.uk>, retrieved on 5 February 2014
  10. Dekoninck W., Lock K. and Janssens F. 2007. Acceptance of two native myrmecophilous species, Platyarthrus hoffmannseggii (Isopoda: Oniscidea) and Cyphoderus albinus (Collembola: Cyphoderidae) by the introduced invasive garden ant Lasius neglectus (Hymenoptera: Formicidae) in Belgium. Eur. J. Entomol. 104: 159-161Google Scholar
  11. Dekoninck W., Hendrickx F., Grootaert P. and Maelfait J. 2010. Present conservation status of red wood ants in north-western Belgium: Worse than previously, but not a lost cause. Eur. J. Entomol. 107: 209-218Google Scholar
  12. Dettner K. and Liepert C. 1994. Chemical mimicry and camouflage. Annu. Rev. Entomol. 39: 129-154Google Scholar
  13. Domisch T., Ohashi M. and Finér L. 2008. Decomposition of organic matter and nutrient mineralisation in wood ant (Formica rufa group) mounds in boreal coniferous forests of different age. Biology and Fertility of soils 44: 539-545Google Scholar
  14. Donisthorpe H.S.J.K. 1927. The Guests of British Ants, their Habits and Life-Histories. George Routledge and Sons, LondonGoogle Scholar
  15. Ebermann E. 1980. Zur Kenntnis der Ostalpinen Milbenfauna (Acari, Fam. Scutacaridae). Mitt. Naturwiss. Ver. Steiermark 110: 143-149Google Scholar
  16. Elmes G.W., Barr B., Thomas J.A. and Clarke R.T. 1999. Extreme host specifcity by Microdon mutabilis (Diptera: Syrphidae), a social parasite of ants. Proc. R. Soc. Lond. B 266: 447-453Google Scholar
  17. Evans G.O. and Till W.M. 1966. Studies on the British Dermanyssidae (Acari: Mesostigmata). Part II. Classification. Bulletin of The British Museum (Natural History) Zoology 14: 107-370Google Scholar
  18. Fain A. and Chmielewski W. 1987. The phoretic hypopi of two acarid mites described from ants’ nest: Tyrophagus formicetorum Volgin, 1948 and Lasioacarus nidicolus Kadzhaja and Sevastianov, 1967. Acarologia 28: 53-61Google Scholar
  19. Fowles A.P. 1994. A review of the ecology of the red wood ant Formica rufa L. (Hymenoptera, Formicidae) and its status in Wales. Cons. Ecol. Wales 1: 1-22Google Scholar
  20. Freude H., Harde K.W. and Lohse G.A. 1974. Die Käfer Mitteleuropas. Band 5, Staphylinidae II (Hypocyphtinae und Aleocharinae). Pselaphidae. Krefeld: Goecke et Evers VerlagGoogle Scholar
  21. Frouz J. 2000. The effect of nest moisture on daily temperature regime in the nests of Formica polyctena wood ants. Insect. Soc. 47: 229-235Google Scholar
  22. Frouz J., Kalcik J. and Cudlín P. 2005. Accumulation of phosphorus in nests of red wood ants Formica s. str. Annal. Zool. Fenn. 42: 269-275Google Scholar
  23. Godeau J.-F. 1997. Les stratégies écologiques de la coccinelle myrmécophile Coccinella magnifica Redtenbacher. Doctoral thesis, Faculté Universitaire des Sciences Agronomiques de GemblouxGoogle Scholar
  24. 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 106: 59-106Google Scholar
  25. Goropashnaya A. V, Fedorov V.B. and Pamilo P. 2004. Recent speciation in the Formica rufa group ants (Hymenoptera, Formicidae): inference from mitochondrial DNA phylogeny. Mol. Phylogen. Evol. 32: 198-206Google Scholar
  26. Gosswald K. 1989. Die Waldameise. Band 2. Die Waldameise im Ökosystem Wald, ihr Nutzen und ihre Hege. Aula-Verlag WiesbadenGoogle Scholar
  27. Gyllenstrand N. and Seppä P. 2003. Conservation genetics of the wood ant, Formica lugubris, in a fragmented landscape. Mol. Ecol. 12: 2931-2940Google Scholar
  28. Härkönen S. and Sorvari J. 2014. Species richness of associates of ants in the nests of a red wood ant Formica polyctena. Insect Cons. Diversity: 1-11Google Scholar
  29. Heimer S. and Nentwig W. 1991. Spinnen Mitteleuropas. Verlag Paul Parey, Berlin und HamburgGoogle Scholar
  30. Henderickx H. 2011. A new myrmecophilous Allochernes from ant nests in the high altitude of the eastern Spanish Pyrenees (Arachnida: Pseudoscorpiones: Chernetidae). Bulletin S.R.B.E/K.B.V.E. 147: 79-83Google Scholar
  31. Hlavac P. and Lackner T. 1998. Contribution to the knowledge of myrmecophilous beetles of Slovakia. Entomofauna carpathica 10: 1-9Google Scholar
  32. Hlavac P. 2005. Revision of the myrmecophilous genus Lomechusa (Coleoptera: Staphylinidae: Aleocharinae). Sociobiology 46: 203–250Google Scholar
  33. Hölldobler B. 1967. Zur Physiologie der Gast-Wirt-Beziehungen (Myrmecophilie) bei Ameisen I. Das Gastverhältnis der Atemeles- und Lomechusa-Larven (Col. Staphylinidae) zu Formica (Hym. Formicidae). Z. vergl. Physiol. 56: 1-21Google Scholar
  34. Hölldobler B. 1970. Zur Physiologie der Gast-Wirt-Beziehungen (Myrmecophilie) bei Ameisen II.1 Das Gastverhältnis des imaginalen Atemeles pubicolis Bris. (Col. Staphylinidae) zu Myrmica und Formica (Hym. Formicidae). Z. vergl. Physiol. 66: 215-250Google Scholar
  35. Hölldobler B. and Wilson E.O. 1990. The Ants. Harvard University Press Cambridge, MassachusettsGoogle Scholar
  36. Hovestadt T., Thomas J.A., Mitesser O. and Elmes G.W. 2012. Unexpected benefit of a social parasite for a key fitness component of its ant host. Amer. Nat. 179: 110-123Google Scholar
  37. Howard R.W., Akre R.D. and Garnett W.B. 1990a. Chemical mimicry in an obligate predator of carpenter ants (Hymenoptera: Formicidae). Annals Entomol. Soc. Am. 83: 607-661Google Scholar
  38. Howard R.W., Stanley-Samuelson D.W. and Akre R.D. 1990b. Biosynthesis and chemical mimicry from the obligate predator Microdon albicomatus and its ant prey, Myrmica incompleta Provancher (Hymenoptera: Formicidae). J. Kansas Entomol. Soc. 63: 437-443Google Scholar
  39. Huhta V. and Karg W. 2010. New species in genera Hypoaspis (s. lat.) Canestrini, 1884, Dendrolaelaps (s. lat.) Halbert, 1915, and Ameroseius Berlese, 1903 (Acari, Gamasina) from Finland. Soil Organisms 82: 325-349Google Scholar
  40. IUCN 2013. The IUCN red list of threatened species. <http://www.iucnredlist.org/>, retrieved on 15 February 2014
  41. Janet C. 1897. Etudes sur les fourmis, les guêpes et les abeilles. Note 14: Rapports des animaux myrmécophiles avec les fourmis. Ducourtieux, LimogesGoogle Scholar
  42. Junker E.A. 1997. Untersuchungen zur Levensweise und Entwicklung von Myrmecophilus acervorum (PANZER, 1799) (Saltatoria, Myrmecophilidae). Articulata 12: 93-106Google Scholar
  43. Junker E.A. and Ratschker U.M. 2000. Zur Verbreitung der Ameisengrille, Myrmecophilus acervorum (Panzer, 1799), in Sachsen (Insecta; Ensifera; Myrmecophilidae). Faun. Abh. Staatlich. Mus. Tierkunde Dresden 22: 11-21Google Scholar
  44. Karafiat H. 1959. Systematik und Ökologie der Scutacariden. In: Uppstrom K. A. 2010. Mites (Acari) associated with the ants (Formicidae) of Ohio and the harvester ant, Messor pergandei, of ArizonaGoogle Scholar
  45. Kärcher M.H. and Ratnieks F.L.W. 2010. Honey bee guards recognise allospecific intruders via “different odours” not “harmful-intruder odours.” J. Apicult. Res. 49: 270-277Google Scholar
  46. Kielczewski B. and Wisniewski J. 1962. Z badań nad akarofauną gniazd Formica rufa L. i Formica polyctena Forst. na tle pozostałych stawonogów towarzyszących (From studies on the Acarofauna of Formica rufa L. Formica polyctena Först. nests on the background of other accompanying Arthropoda). Prace z Zakresu Entomologii Lesnej 13: 3-14Google Scholar
  47. Laakso J. and Setälä H. 1997. Nest mounds of red wood ants (Formica aquilonia): hot spots for litter-dwelling earthworms. Oecologia 111: 565-569Google Scholar
  48. Lachaud J.-P. and Pérez-Lachaud G. 2012. Diversity of Species and Behavior of Hymenopteran Parasitoids of Ants: A Review. Psyche: A Journal of Entomology 2012: 1-24Google Scholar
  49. Lapeva A. and Simov N. Xylocoris formicetorum (Bohemann, 1844) (Heteroptera: Anthocoridae), a new member of the myrmecophilous fauna of the Balkan Peninsula. Hist. Nat. Bulgarica 12, 29-31Google Scholar
  50. Lapeva-Gjonova A. and Rücker W.H. 2011. Latridiidae and Endomychidae beetles (Coleoptera) from ant nests in Bulgaria. Latridiidae 8: 5-8Google Scholar
  51. Lapeva-Gjonova A. and Lieff O. 2012. Ant-associated rove beetles (Coleoptera: Staphylinidae) in Bulgaria. Acta Entomol. Slovenica 20: 73-84Google Scholar
  52. Lapeva-Gjonova A. 2013. Ant-associated beetle fauna in Bulgaria: A Review and New Data. Psyche: J. Entomol. 2013: 1-14Google Scholar
  53. Lehtinen P.T. 1987. Association of uropodid prodinychid polyaspidid antennophorid sejid microgynid and zerconid mites with ants. Entomol. Tidskr. 2: 13-20Google Scholar
  54. Lommelen E., Johnson C.A., Drijfhout F.P., Billen J., Wenseleers T. and Gobin B. 2006. Cuticular hydrocarbons provide reliable cues of fertility in the ant Gnamptogenys striatula. Journal of Chemical Ecology 32: 2023-2034Google Scholar
  55. Mäki-Petäys H., Zakharov A., Viljakainen L., Corander J. and Pamilo P. 2005. Genetic changes associated to declining populations of Formica ants in fragmented forest landscape. Mol. Ecol. 14: 733-42Google Scholar
  56. Mahunka S. 1967. Beiträge zur kenntnis der Tschechoslowakischen Tarsonemini- fauna. Věstník Česk. Spol. Zool. 31: 240-244. In: Uppstrom, K. A. 2010. Mites (Acari) associated with the ants (Formicidae) of Ohio and the harvester ant, Messor pergandei, of Arizona. Master thesis Ohio State UniversityGoogle Scholar
  57. Mahunka S. 1970. Zwei neue Heterodispus- Arten und einige interessante in Ameisenhaufen lebende milben aus Ungarn (Acari: Tarsonemina). Folia Entomol. Hung. 23: 313-331. In: Uppstrom K. A. 2010. Mites (Acari) associated with the ants (Formicidae) of Ohio and the harvester ant, Messor pergandei, of Arizona. Master thesis Ohio State UniversityGoogle Scholar
  58. Martin S.J., Jenner E. and Drijfhout F.P. 2007. Chemical deterrent enables a socially parasitic ant to invade multiple hosts. Proc. R. Soc. B 274: 2717-2722.Google Scholar
  59. O’Keefe S. 2000. Ant-like stone beetles, ants, and their associations (Coleoptera: Scydmaenidae; Hymenoptera: Formicidae; Isoptera). J. N.Y. Entomol. Soc. 108: 273-303Google Scholar
  60. Päivinen J., Ahlroth P., Kaitala V., Kotiaho J.S., Suhonen J. and Virola T. 2003. Species richness and regional distribution of myrmecophilous beetles. Oecologia 134: 587-595Google Scholar
  61. Päivinen J., Ahlroth P., Kaitala V., Kotiaho J.S. and Suhonen J. 2004. Species richness, abundance and distribution of myrmecophilous beetles in nests of Formica aquilonia ants. Ann. Zool. Fenn. 41: 447-454Google Scholar
  62. Reemer M., Renema W., van Steenis W., Zeegers T., Barendregt A., Smit J.T., van Veen M.P., van Steenis J. and van der Leij L.J.J.M. 2009. De Nederlandse zweefvliegen (Diptera: Syrphidae). - Nederlandse Fauna 8. Leiden. Nationaal Natuurhistorisch Museum Naturalis, KNNV Uitgeverij, European Invertebrate Survey – NederlandGoogle Scholar
  63. Renneson J.-L., Drumont A., Grotz R. and Dekoninck W. 2012. A propos de Protaetia (Potosia) metallica (Herbst, 1782) en Belgique et au Grand-Duché de Luxembourg (Coleoptera, Scarabaeidae, Cetoniinae). Lambillionea 3: 263-279Google Scholar
  64. Rettenmeyer C.W., Rettenmeyer M.E., Joseph J. and Berghoff S.M. 2010. 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
  65. Robinson N.A. and Robinson E.J.H. 2013. Myrmecophiles and other invertebrate nest associates of the red wood ant Formica rufa (Hymenoptera: Formicidae) in north-west England. Brit. J. Entomol. Nat. Hist. 26: 67-88Google Scholar
  66. Rolstad J., Løken B. and Rolstad E. 2000. Habitat selection as a hierarchical spatial process: the green woodpecker at the northern edge of its distribution range. Oecologia 124: 116-129Google Scholar
  67. Rosengren R., Fortelius W., Lindström K. and Luther A. 1987. Phenology and causation of nest heating and thermoregulation in red wood ants of the Formica-rufa group studied in coniferous forest habitats in southern Finland. Ann. Zool. Fenn. 24: 147-155Google Scholar
  68. Shamble P.S., Beatus T., Cohen I. and Hoy R. 2013. Terrestrial locomotor mimicry at the kinematic level: Does the ant-mimicking jumping spider Myrmarachne formicaria walk like an ant? SICB Annual Meeting 2013 January 3-7, 2013 San Francisco, CAGoogle Scholar
  69. Simon U. 1997. On the biology of Dipoena torva (Araneae: Theridiidae). Arachnol. Mitt. 13: 30-41Google Scholar
  70. Seifert B. 2007. Die Ameisen Mittel- und Nordeuropas. lutra Verlags- und Vertriebsgesellschaft, GörlitzGoogle Scholar
  71. Skinner G. 1980. The feeding habits of the wood-ant, Formica rufa (Hymenoptera: Formicidae), in limestone woodland in north-west England. J. Anim. Ecol. 49: 417-433Google Scholar
  72. Sloggett J.J., Wood R.A. and Majerus M.E.N. 1998. Adaptations of Coccinella magnifica Redtenbacher,, a myrmecophilous coccinellid, to aggression by wood ants (Formica rufa group). I. Adult behavioral adaptation, its ecological context and evolution. Evolution 11: 889-904Google Scholar
  73. Sorvari J. and Hakkarainen H. 2005. Deforestation reduces nest mound size and decreases the production of sexual offspring in the wood ant Formica aquilonia. Ann. Zool. Fenn. 42: 259-267Google Scholar
  74. Sorvari J. and Hakkarainen H. 2007. Wood ants are wood ants: deforestation causes population declines in the polydomous wood ant Formica aquilonia. Ecol. Entomol. 32: 707-711Google Scholar
  75. Staniec B. and Zagaja M. 2008. Rove-beetles (Coleoptera, Staphylinidae) of ant nests of the vicinities of Leżajsk. Ann. Univ. Mariae Curie-Sklodowska Lublin - Polonia 63: 111-127Google Scholar
  76. Stoev P. and Lapeva-Gjonova A. 2005. Myriapods from ant nests in Bulgaria (Chilopoda, Diplopoda). Peckiana 4: 131-142Google Scholar
  77. Storey M. BioInfo (UK) 2014. <www.bioinfo.org.uk>, retrieved on 5 March 2014
  78. Storkan J. 1940. Myrmekofiln Acari z Cech. Vestnik Cesk. Zool. Spol. 8: 166-172Google Scholar
  79. Tykarski P. 2013. Coleoptera Poloniae - Information System about Beetles of Poland. <http://coleoptera.ksib.pl/index.php?id=cretl=en>, retrieved on 10 February 2014
  80. Uppstrom K. A. 2010. Mites (Acari) associated with the ants (Formicidae) of Ohio and the harvester ant, Messor pergandei, of Arizona. Master thesis Ohio State UniversityGoogle Scholar
  81. Wachmann E., Melber A. and Deckert J. 2007. Wanzen. Goecke et Evers, KelternGoogle Scholar
  82. Wardle D., Hyodo F. and Bardgett R. 2011. Long-term aboveground and belowground consequences of red wood ant exclusion in boreal forest. Ecology 92: 645-656Google Scholar
  83. Wasmann E. 1894. Kritisches Verzeichniss der myrmekophilen und termitophilen Arthropoden. Berlin: F. L. Dames, xvGoogle Scholar
  84. Wasmann E. 1898. Erster Nachtrag zu den Ameisengästen von Holländisch Limburg, mit biologischen Notizen. Tijdschr. Entomol. 41: 1-19Google Scholar
  85. Wasmann E. 1899. Weitere nachträge zum Verzeichniss der Ameisengäste von Holländisch Limburg. Tijdschr. Entomol. 42: 158-171Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2014

Authors and Affiliations

  1. 1.Laboratory of Socioecology and SocioevolutionLeuvenBelgium
  2. 2.Entomology DepartmentRoyal Belgian Institute of Natural SciencesBrusselsBelgium

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