Skip to main content
SpringerLink
Log in

Arthropods Associate with their Red Wood ant Host without Matching Nestmate Recognition Cues

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

Abstract

Social insect colonies provide a valuable resource that attracts and offers shelter to a large community of arthropods. Previous research has suggested that many specialist parasites of social insects chemically mimic their host in order to evade aggression. In the present study, we carry out a systematic study to test how common such chemical deception is across a group of 22 arthropods that are associated with red wood ants (Formica rufa group). In contrast to the examples of chemical mimicry documented in some highly specialized parasites in previous studies, we find that most of the rather unspecialized red wood ant associates surveyed did not use mimicry of the cuticular hydrocarbon recognition cues to evade host detection. Instead, we found that myrmecophiles with lower cuticular hydrocarbon concentrations provoked less host aggression. Therefore, some myrmecophiles with low hydrocarbon concentrations appear to evade host detection via a strategy known as chemical insignificance. Others showed no chemical disguise at all and, instead, relied on behavioral adaptations such as particular defense or evasion tactics, in order to evade host aggression. Overall, this study indicates that unspecialized myrmecophiles do not require the matching of host recognition cues and advanced strategies of chemical mimicry, but can integrate in a hostile ant nest via either chemical insignificance or specific behavioral adaptations.

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
Fig. 3

Similar content being viewed by others

References

  • Akino T (2002) Chemical camouflage by myrmecophilous beetles Zyras comes (Coleoptera: Staphylinidae) and Diaritiger fossulatus (Coleoptera: Pselaphidae) to be integrated into the nest of Lasius fuliginosus (hymenoptera: Formicidae). Chemoecology 12:83–89. doi:10.1007/s00049-002-8330-4

    Article  CAS  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. Myrmecological News 11:173–181

    Google Scholar 

  • Akino T, Knapp J (1999) Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proc Roy Soc B Biol Sci 266:1419–1426

    Article  CAS  Google Scholar 

  • Akino T, Yamaoka R (1998) Chemical mimicry in the root aphid parasitoid Paralipsis eikoae Yasumatsu (hHymenoptera : Aphidiidae) of the aphid-attending ant Lasius sakagamii. Chemoecology 161:153–161

    Article  Google Scholar 

  • Akino T, Mochizuki R, Morimoto M, Yamaoka R (1996) Chemical camouflage of myrmecophilous cricket Myrmecophilus sp. to be integrated with several ant species. Jpn J Appl Entomol Zool 40:39–46. doi:10.1303/jjaez.40.39

    Article  CAS  Google Scholar 

  • Akino T, Nakamura KI, Wakamura S (2004a) Diet-induced chemical phytomimesis by twig-like caterpillars of Biston robustum Butler (Lepidoptera: Geometridae). Chemoecology 14:165–174. doi:10.1007/s00049-004-0274-4

    Article  CAS  Google Scholar 

  • Akino T, Yamamura K, Wakamura S, Yamaoka R (2004b) Direct behavioral evidence for hydrocarbons as nestmate recognition cues in Formica japonica (hymenoptera : Formicidae). Appl Entomol Zool 39:381–387. doi:10.1303/aez.2004.381

    Article  CAS  Google Scholar 

  • Allan R, Elgar M (2001) Exploitation of the green tree ant, Oecophylla smaragdina, by the salticid spider Cosmophasis bitaeniata. Aust J Zool 49:129–137

    Article  Google Scholar 

  • von Beeren C, Schulz S, Hashim R, Witte V (2011) Acquisition of chemical recognition cues facilitates integration into ant societies. BMC Ecol 11:30. doi:10.1186/1472-6785-11-30

    Article  PubMed  Google Scholar 

  • von Beeren C, Hashim R, Witte V (2012a) The social integration of a myrmecophilous spider does not depend exclusively on chemical mimicry. J Chem Ecol 38:262–271. doi:10.1007/s10886-012-0083-0

    Article  CAS  Google Scholar 

  • von Beeren C, Pohl S, Witte V (2012b) On the use of adaptive resemblance terms in chemical ecology. Psyche 2012. doi:10.1155/2012/635761

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300. doi:10.2307/2346101

    Google Scholar 

  • Blomquist GJ, Bagnères AG (2010). Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press

  • Bos N, Grinsted L, Holman L (2011) Wax on, wax off : Nest soil facilitates indirect transfer of recognition cues between ant nestmates. PLoS One 6:2–7. doi:10.1371/journal.pone.0019435

    Article  Google Scholar 

  • Buschinger A (2009) Social parasitism among ants : a review (Hymenoptera : Formicidae). Myrmecological News 12:219–235

    Google Scholar 

  • Carlson DA, Roan CS, Yost RA, Hector J (1989) Dimethyl disulfide derivatives of long chain alkenes, alkadienes, and alkatrienes for gas chromatography/mass spectrometry. Anal Chem 61:1564–1571. doi:10.1021/ac00189a019

    Article  CAS  Google Scholar 

  • Carlson DA, Bernier UR, Sutton BD (1998) Elution patterns from capillary GC for methyl-branched alkanes. J Chem Ecol 24:1845–1865

    Article  CAS  Google Scholar 

  • Cervo R, Dani FR, Cotoneschi C, Scala C, Lotti I, Strassmann JE, Queller DC, Turillazzi S (2008) Why are larvae of the social parasite wasp Polistes sulcifer not removed from the host nest? Behav Ecol Sociobiol 62:1319–1331. doi:10.1007/s00265-008-0560-1

    Article  Google Scholar 

  • Dekoninck W, Hendrickx F, Grootaert P, 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 107:209–218

    Article  Google Scholar 

  • Di Giulio A, Maurizi E, Barbero F, Sala M, Fattorini S, Balletto E, Bonelli S (2015) The pied piper: a parasitic beetle’s melodies modulate ant behaviours. PLoS One 10:e0130541. doi:10.1371/journal.pone.0130541

    Article  PubMed  PubMed Central  Google Scholar 

  • Dinter K, Paarmann W, Peschke K, Arndtab E (2002) Ecological, behavioural and chemical adaptations to ant predation in species of Thermophilum and Graphipterus (Coleoptera: Carabidae) in the Sahara desert. J Arid Environ 50:267–286. doi:10.1006/jare.2001.0850

    Article  Google Scholar 

  • Donisthorpe HSJK (1927) The guests of British ants, their habits and life-histories. George Routledge and Sons, London

    Google Scholar 

  • Eberhard W (1977) Aggressive chemical mimicry by a bolas spider. Science 198:1173–1175

    Article  CAS  PubMed  Google Scholar 

  • Elgar M, Allan R (2004) Predatory spider mimics acquire colony-specific cuticular hydrocarbons from their ant model prey. Naturwissenschaften 91:143–147. doi:10.1007/s00114-004-0507-y

    Article  CAS  PubMed  Google Scholar 

  • Elgar MA, Allan RA (2006) Chemical mimicry of the ant Oecophylla smaragdina by the myrmecophilous spider Cosmophasis bitaeniata : is it colony-specific ? J Ethol:239–246. doi:10.1007/s10164-005-0188-9

  • Elmes GW, Akino T, Thomas JA, Clarke RT, Knapp JJ (2002) Interspecific differences in cuticular hydrocarbon profiles of Myrmica ants are sufficiently consistent to explain host specificity by Maculinea (large blue) butterflies. Oecologia 130:525–535. doi:10.1007/s00442-001-0857-5

    Article  CAS  PubMed  Google Scholar 

  • El-Sayed AM (2016) The Pherobase: Database of insect pheromones and semiochemicals <http://www.pherobase.com>

  • Gerhardt H, Betz O, Albert K, Lämmerhofer M (2016) Insect adhesion secretions: similarities and dissimilarities in hydrocarbon profiles of tarsi and corresponding tibiae. J Chem Ecol 42:725–738

    Article  CAS  PubMed  Google Scholar 

  • Gösswald K (1989) Die Waldameise Band 1 Biologische Grundlagen. Ökologie und Verhalten, Aula-Verlag Wiesbaden

    Google Scholar 

  • Guerrieri FJ, Nehring V, Jørgensen CG, Nielsen J, Galizia CG, D’Ettorre P (2009) Ants recognize foes and not friends. Proc Roy Soc B 276:2461–2468. doi:10.1098/rspb.2008.1860

    Article  CAS  Google Scholar 

  • Hojo MK, Wada-katsumata A, Akino T, Yamaguchi S, Ozaki M, Yamaoka R (2009) Chemical disguise as particular caste of host ants in the ant inquiline parasite Niphanda fusca (Lepidoptera : Lycaenidae). Proc Roy Soc B 276:551–558. doi:10.1098/rspb.2008.1064

    Article  CAS  Google Scholar 

  • Hojo MK, Yamamoto A, Akino T, Tsuji K, Yamaoka R (2014) Ants use partner specific odors to learn to recognize a mutualistic partner. PLoS One 9:4–11

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press Cambridge, Massachusetts

    Book  Google Scholar 

  • Howard RW (1976) Observations on behavioral interactions between Trichopsenius frosti (Coleoptera: Staphylinidae) and Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae). Sociobiology 2:189–192

    Google Scholar 

  • Howard RW (1978) Proctodeal feeding by termitophilous Staphylinidae associated with Reticulitermes virginicus (Banks). Science 201:541–543

    Article  CAS  PubMed  Google Scholar 

  • Howard RW, Kistner DH (1978) The eggs of Trichopsenius depressus and T. frosti (Coleoptera, Staphylinidae, Trichopseniinae) with a comparison to those of their host termites Reticulitermes vriginicus and R. flavipes. Sociobiology 3:99–106

    Article  Google Scholar 

  • Howard RW, McDaniel CA, Blomquist GJ (1980) Chemical mimicry as an integrating mechanism: Cuticular hydrocarbons of a termitophile and its host. Science 210:431–433

    Article  CAS  PubMed  Google Scholar 

  • Howard RW, McDaniel CA, Blomquist GJ (1982) Chemical mimicry as an integrating mechanism for three termitophiles associated with Reticulitermes virginicus (Banks). Psyche 89:157–168

    Article  Google Scholar 

  • Howard RW, Akre RD, Garnett WB (1990a) Chemical mimicry in an obligate predator of carpenter ants (hymenoptera: Formicidae). Ann Entomol Soc Am 83:607–616. doi:10.1093/aesa/83.3.607

    Article  CAS  Google Scholar 

  • Howard RW, Stanley-Samuelson DW, Akre RD (1990b) Biosynthesis and chemical mimicry from the obligate predator Microdon albicomatus and its ant prey, Myrmica incompleta Provancher (hymenoptera: Formicidae). J Kansas Entomol Soc 63:437–443

    Google Scholar 

  • Howard RW, Pérez-Lachaud G, Lachaud JP (2001) Cuticular hydrocarbons of Kapala sulcifacies (hymenoptera: Eucharitidae) and its host, the ponerine ant Ectatomma ruidum (hymenoptera: Formicidae). Ann Entomol Soc Am 94:707–716. doi:10.1603/0013-8746(2001)094[0707:CHOKSH]2.0.CO;2

    Article  CAS  Google Scholar 

  • Ichinose K, Lenoir A (2010) Hydrocarbons detection levels in ants. Insect Soc 57:453–455

    Article  Google Scholar 

  • Joel DM (1988) Mimicry and mutualism in carnivorous pitcher plants (Sarraceniaceae, Nepenthaceae, Cephalotaceae, Bromeliaceae). Biol J Linn Soc 35:185–197. doi:10.1111/j.1095-8312.1988.tb00465.x

    Article  Google Scholar 

  • Kather R, Drijfhout FP, Shemilt S, Martin SJ (2015) Evidence for passive chemical camouflage in the parasitic mite Varroa destructor. J Chem Ecol 41:178–186. doi:10.1007/s10886-015-0548-z

    Article  CAS  PubMed  Google Scholar 

  • Kistner DH (1979) Social and evolutionary significance of social insect symbionts. Soc Insects 1:339–411

    Google Scholar 

  • Kistner DH (1982) The social insects’ bestiary. In: social insects. Academic Press, London, pp 1–244

    Google Scholar 

  • Kronauer DJC, Pierce NE (2011) Myrmecophiles. Curr Biol 21:208–209. doi:10.1016/j.cub.2011.01.050

    Article  Google Scholar 

  • Le Conte Y, Huang ZY, Roux M, Zeng ZJ, Christidès J-P, Bagnères A-G (2015) Varroa destructor changes its cuticular hydrocarbons to mimic new hosts. Biol Lett 11:20150233-. doi: 10.1098/rsbl.2015.0233

  • Lenoir A, D’Ettorre P, Errard C (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:537–599

    Article  Google Scholar 

  • Lenoir A, Depickère S, Devers S, Christidès J-P, Detrain C (2009) Hydrocarbons in the ant Lasius niger: from the cuticle to the nest and home range marking. J Chem Ecol 35:913–921. doi:10.1007/s10886-009-9669-6

    Article  CAS  PubMed  Google Scholar 

  • Lenoir A, Chalon Q, Carvajal A, Ruel C, Barroso Á, Lackner T, Boulay R (2012) Chemical integration of myrmecophilous guests in Aphaenogaster ant nests. Psyche 2012:1–12. doi:10.1155/2012/840860

    Article  Google Scholar 

  • Lenoir A, Háva J, Hefetz A, Dahbi A, Cerdá X, Boulay R (2013) Chemical integration of Thorictus myrmecophilous beetles into Cataglyphis ant nests. Biochem Syst Ecol 51:335–342. doi:10.1016/j.bse.2013.10.002

    Article  CAS  Google Scholar 

  • Liepert C, Dettner K (1996) Role of cuticular hydrocarbons of aphid parasitoids in their relationship to aphid-attending ants. J Chem Ecol 22:695–707

    Article  CAS  PubMed  Google Scholar 

  • Linstrom PJ, Mallard WG (eds) (2016) NIST chemistry webbook, NIST standard reference database number 69, National Institute of Standards and Technology, Gaithersburg, MD, 20899. <http://webbook.Nist.Gov>

  • Lohman DJ, Liao Q, Pierce NE (2006) Convergence of chemical mimicry in a guild of aphid predators. Ecol Entom 31:41–51

    Article  Google Scholar 

  • Martin SJ, Bayfield J (2014) Is the bee louse Braula coeca (Diptera) using chemical camouflage to survive within honeybee colonies? Chemoecology 24:165–169. doi:10.1007/s00049-014-0158-1

    Article  CAS  Google Scholar 

  • Martin C, Salvy M, Provost E, Bagnères A-G, Roux M, Crauser D, Clèment J-L, Le Conte Y (2001) Variations in chemical mimicry by the ectoparasitic mite Varroa jacobsoni according to the developmental stage of the host honey- bee Apis mellifera. Insect Biochem Mol Biol 31:365–379

    Article  CAS  PubMed  Google Scholar 

  • Martin SJ, Helanterä H, Drijfhout FP (2008a) Evolution of species-specific cuticular hydrocarbon patterns in Formica ants. Biol J Linnean Soc 95:131–140

    Article  Google Scholar 

  • Martin SJ, Takahashi J-I, Ono M, Drijfhout FP (2008b) Is the social parasite Vespa dybowskii using chemical transparency to get her eggs accepted? J Insect Physiol 54:700–707. doi:10.1016/j.jinsphys.2008.01.010

    Article  CAS  PubMed  Google Scholar 

  • Martin SJ, Vitikainen E, Helanterä H, Drijfhout FP (2008c) Chemical basis of nest-mate discrimination in the ant Formica exsecta. Proc Roy Soc B 275:1271–1278. doi:10.1098/rspb.2007.1708

    Article  CAS  Google Scholar 

  • Maruyama M, Akino T, Hashim R, Komatsu T (2009) Behavior and cuticular hydrocarbons of myrmecophilous insects (Coleoptera: Staphylinidae; Diptera : Phoridae; Thysanura) associated with Asian Aenictus army ants (Hymenoptera; Formicidae). Sociobiology 54:19–35

    Google Scholar 

  • Messadi D, Helaimia F, Ali-Mokhnache S, Boumahraz M (1990) Accurate determination of retention indices in programmed temperature gas chromatography. Chromatographia 29:429–434

    Article  CAS  Google Scholar 

  • Moritz RFA (1991) Chemical camouflage of the Death’s head hawkmoth (Acherontia atropos L.) in honeybee colonies. Naturwissenschaften 78:179–182

    Article  CAS  Google Scholar 

  • Nash DR, Boomsma JJ (2008) Communication between hosts and social parasites. In: sociobiology of communication: an interdisciplinary perspecftive. Oxford University Press, p 55-80

  • Nash DR, Als TD, Maile R, Jones GR, Boomsma JJ (2008) A mosaic of chemical coevolution in a large blue butterfly. Science 319:88–90

    Article  CAS  PubMed  Google Scholar 

  • Nehring V, Dani FR, Calamai L, Turillazzi S, Bohn H, Klass K-D, d’Ettorre P (2016) Chemical disguise of myrmecophilous cockroaches and its implications for understanding nestmate recognition mechanisms in leaf-cutting ants. BMC Ecol 16:35. doi:10.1186/s12898-016-0089-5

    Article  PubMed  PubMed Central  Google Scholar 

  • Nielsen J, Boomsma JJ, Oldham NJ, Petersen HC, Morgan ED (1999) Colony-level and season-specific variation in cuticular hydrocarbon profiles of individual workers in the ant Formica truncorum. Insect Soc 46:58–65

    Article  Google Scholar 

  • Parker J (2016) Myrmecophily in beetles (Coleoptera): evolutionary patterns and biological mechanisms. Myrmecological News 22:65–108

    Google Scholar 

  • Parmentier T, Dekoninck W, 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 61:229–237. doi:10.1007/s00040-014-0357-3

    Article  Google Scholar 

  • Parmentier T, Bouillon S, Dekoninck W, Wenseleers T (2016a) Trophic interactions in an ant nest microcosm: a combined experimental and stable isotope (δ13C/δ15N) approach. Oikos 125:1182–1192. doi:10.1111/oik.02991

  • Parmentier T, Dekoninck W, Wenseleers T (2016b) Do well-integrated species of an inquiline community have a lower brood predation tendency? A test using red wood ant myrmecophiles. BMC Evol Biol 16:12. doi:10.1186/s12862-016-0583-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Parmentier T, Dekoninck W, Wenseleers T (2016c) Survival of persecuted myrmecophiles in laboratory nests of different ant species can explain patterns of host use in the field (hymenoptera : Formicidae). Myrmecological News 23:71–79

  • Pérez-Lachaud G, Bartolo-Reyes JC, Quiroa-Montalván CM, Cruz-Lopez L, Lenoir A, Lachaud JP (2015) How to escape from the host nest: imperfect chemical mimicry in eucharitid parasitoids and exploitation of the ants’ hygienic behavior. J Insect Physiol 75:63–72. doi:10.1016/j.jinsphys.2015.03.003

    Article  PubMed  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Found. Stat. Comput. Vienna Austria 0:{ISBN} 3–900051–07-0

  • Richard FJ, Poulsen M, Drijfhout F, Jones G, Boomsma JJ (2007) Specificity in chemical profiles of workers, brood and mutualistic fungi in Atta, Acromyrmex and Sericomyrmex fungus-growing ants. J Chem Ecol 33:2281–2229

    Article  CAS  PubMed  Google Scholar 

  • Salazar A, Fürstenau B, Quero C, Pérez-hidalgo N, Carazo P, Font E (2015) Aggressive mimicry coexists with mutualism in an aphid. Proc Natl Acad Sci U S A 112:1101–1106. doi:10.1073/pnas.1414061112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlick-Steiner BC, Steiner FM, Höttinger H, Nikiforov A, Mistrik R, Schafellner C, Baier P, Christian E (2004) A butterfly’s chemical key to various ant forts: intersection-odour or aggregate-odour multi-host mimicry? Naturwissenschaften 91:209–214. doi:10.1007/s00114-004-0518-8

    Article  CAS  PubMed  Google Scholar 

  • Schönrogge K, Wardlaw JC, Peters AJ, Everett S, Thomas JA, Elmes GW (2004) Changes in chemical signature and host specificity from larval retrieval to full social integration in the myrmecophilous butterfly Maculinea rebeli. J Chem Ecol 30:91–107

    Article  PubMed  Google Scholar 

  • Seifert B (2007) Die Ameisen Mittel- und Nordeuropas. Tauer: lutra Verlags- und Vertriebsgesellschaft, Görlitz

  • Sloggett JJ, Wood RA, Majerus M (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. J Insect Behav 11:889–904. doi:10.1023/A:1020820428820

    Article  Google Scholar 

  • Sorvari J, Theodora P, Turillazzi S, Hakkarainen H, Sundström L (2008) Food resources, chemical signaling, and nest mate recognition in the ant Formica aquilonia. Behav Ecol 19:441–447. doi:10.1093/beheco/arm160

    Article  Google Scholar 

  • Stoeffler M, Tolasch T, Steidle JLM (2011) Three beetles—three concepts. Different defensive strategies of congeneric myrmecophilous beetles. Behav Ecol Sociobiol 65:1605–1613. doi:10.1007/s00265-011-1171-9

    Article  Google Scholar 

  • Sutton PA, Wilde MJ, Martin SJ, Cvačka J, Vrkoslav V, Rowland SJ (2013) Studies of long chain lipids in insects by high temperature gas chromatography and high temperature gas chromatography-mass spectrometry. J Chromatogr A 1297:236–240. doi:10.1016/j.chroma.2013.05.006

    Article  CAS  PubMed  Google Scholar 

  • Thomas J, Knapp JJ, Akino T, Gerty S, Wakamura S, Simcox DJ, Wardlaw JC, Elmes GW (2002) Parasitoid secretions provoke ant warfare. Nature 417:505–506. doi:10.1038/417505a

    Article  CAS  PubMed  Google Scholar 

  • Uboni A, Lorenzi MC (2013) Poor odors, strength, and persistence give their rewards to Mutilla europaea visiting dangerous wasp nests. J Insect Behav 26:246–252. doi:10.1007/s10905-012-9362-4

    Article  Google Scholar 

  • Uboni A, Bagnères A-G, Christidès J-P, Lorenzi MC (2012) Cleptoparasites, social parasites and a common host : chemical insignificance for visiting host nests, chemical mimicry for living in. J Insect Physiol 58:1259–1264. doi:10.1016/j.jinsphys.2012.06.013

    Article  CAS  PubMed  Google Scholar 

  • Van Oystaeyen A, Oliveira RC, Holman L, van Zweden JS, Romero C, Oi CA, D’Ettorre P, Khalesi M, Billen J, Wackers F, Millar JG, Wenseleers T (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343:287–290. doi:10.1126/science.1244899

    Article  PubMed  Google Scholar 

  • Van Oystaeyen A, van Zweden JS, Huyghe H, Drijfhout F, Bonckaert W, Wenseleers T (2015) Chemical strategies of the beetle Metoecus paradoxus, social parasite of the wasp Vespula vulgaris. J Chem Ecol 41:1137–1147. doi:10.1007/s10886-015-0652-0

    Article  PubMed  Google Scholar 

  • Vander Meer RK, Wojcik DP (1982) Chemical mimicry in the myrmecophilous beetle Myrmecaphodius excavaticollis. Science 218:806–808

    Article  CAS  Google Scholar 

  • 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. doi:10.1007/BF01014113

    Article  CAS  PubMed  Google Scholar 

  • Vantaux A, Roux O, Magro A, Ghomsi NT, Gordon RD, Dejean A (2010) Host-specific myrmecophily and myrmecophagy in the tropical coccinellid Diomus thoracicus in French Guiana. Biotropica 42:622–629

    Article  Google Scholar 

  • Wasmann E (1894) Kritisches Verzeichniss der myrmekophilen und termitophilen Arthropoden. F. L. Dames, Berlin

    Book  Google Scholar 

  • Witek M, Pietro CL, Barbero F, Patricelli D, Sala M, Bossi S, Maffei M, Woyciechowski M, Balletto E, Bonelli S (2013) Interspecific relationships in co-occurring populations of social parasites and their host ants. Biol J Linn Soc 109:699–709. doi:10.1111/bij.12074

    Article  Google Scholar 

  • Witte V, Leingärtner A, Sabaß L, Hashim R, Foitzik S (2008) Symbiont microcosm in an ant society and the diversity of interspecific interactions. Anim Behav 76:1477–1486. doi:10.1016/j.anbehav.2008.05.010

    Article  Google Scholar 

  • Witte V, Foitzik S, Hashim R, Maschwitz U, Schulz S (2009) Fine tuning of social integration by two myrmecophiles of the ponerine army ant, Leptogenys distinguenda. J Chem Ecol 35:355–367. doi:10.1007/s10886-009-9606-8

    Article  CAS  PubMed  Google Scholar 

  • Włodarczyk T (2011) Recognition of individuals from mixed colony by Formica sanguinea and Formica polyctena ants. J Insect Behav 25:105–113. doi:10.1007/s10905-011-9280-x

    Article  Google Scholar 

  • Wyatt TD (2012) Pheromones and animal behavior: chemical signals and signatures, Cambridge University Press

  • van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Insect hydrocarbons biology, biochemistry and chemical ecology. Cambridge University Press, New York, pp 222–243

    Chapter  Google Scholar 

Download references

Acknowledgements

This project was supported by Fonds Wetenschappelijk Onderzoek Vlaanderen, grant TP no.11D6414N and Kuleuven (grant TP 253 PDM/16/099). We are grateful for the constructive comments of David Nash and three anonymous referees.

Author information

Authors and Affiliations

  1. Laboratory of Socioecology and Socioevolution, KU Leuven, Naamsestraat 59, B-3000, Leuven, Belgium

    Thomas Parmentier & Tom Wenseleers

  2. Entomology Department, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, B-1000, Brussels, Belgium

    Thomas Parmentier & Wouter Dekoninck

Authors
  1. Thomas Parmentier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wouter Dekoninck
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tom Wenseleers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Parmentier.

Electronic supplementary material

ESM 1

Supplementary Material 1 Identified hydrocarbons based on Kovats indices and diagnostic ions. Gas chromatograms of cuticular volatiles of red wood ants and associated myrmecophiles. Ant figures were adapted from www.AntWeb.org, myrmecophile figures were adapted from pictures kindly provided by Lech Borowiec or by the first author (PPTX 3.85 MB)

ESM 2

Supplementary Material 2: Surface estimation of ants and myrmecophiles. Mean cuticle surface of myrmecophiles and red wood ants and estimated concentration of cuticular hydrocarbons (ng/mm2). (DOCX 19 kb)

ESM 3

Supplementary Material 3: Percent composition of cuticular hydrocarbons found in red wood ants and associated myrmecophiles. (DOCX 65.6 kb)

ESM 4

Supplementary Material 4: Hierachical cluster analyses of subsets of the cuticular hydrocarbon profile: n-alkanes, n-alkenes, methyl-branched alkanes, dimethyl-branched alkanes. (PPTX 238 kb)

ESM 5

Supplementary Material 4: Post-hoc tests of cuticular hydrocarbon concentration. Table S2. Wilcoxon rank sum tests to compare the hydrocarbon concentration between different myrmecophile species and red wood ant workers. (DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Parmentier, T., Dekoninck, W. & Wenseleers, T. Arthropods Associate with their Red Wood ant Host without Matching Nestmate Recognition Cues. J Chem Ecol 43, 644–661 (2017). https://doi.org/10.1007/s10886-017-0868-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-017-0868-2

Keywords

Search

Navigation