Abstract
Aphid-tending ants protect aphids from natural enemies and collect honeydew secreted by the aphids. However, ants also often prey on the aphids they attend. Aphids, therefore, like social parasites of ants, may well have evolved chemical mimicry as an anti-predation strategy. In this study, we aimed to determine whether the aphid Stomaphis yanonis actively produces cuticular hydrocarbons (CHCs) that resemble those of the tending ant Lasius fuji. In the wild, ants put their CHCs on the aphids that they are tending, so in this study we analyzed “ant-free” aphids. Mature aphids that exuviated in the absence of ant attendance had almost all of the hydrocarbon components that the ants’ CHCs had. Moreover, hydrocarbons artificially applied to the aphids’ body surface were lost by exuviation. Taken together, these findings indicate that mature aphids actively produced ant-like CHCs, and they constitute the first documentation of a chemical resemblance between aphids and ants in a specific aphid–ant association.
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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 (Hymenoptera: Formicidae). Chemoecology 12:83–89
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
Akino T, Yamaoka R (1998) Chemical mimicry in the root aphid parasitoid Paralipsis eikoae Yasumatsu (Hymenoptera: Aphidiidae) of the aphid-attending ant Lasius sakagamii Yamauchi & Hayashida (Hymenoptera: Formicidae). Chemoecology 8:153–161
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 (in Japanese with English abstract)
Akino T, Knapp JJ, Thomas JA, Elmes GW (1999) Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proc R Soc B 266:1419–1426
Akino T, Yamamura K, Wakamura S, Yamaoka R (2004) Direct behavioral evidence for hydrocarbons as nestmate recognition cues in Formica japonica (Hymenoptera: Formicidae). Appl Entomol Zool 39:381–387
Brandt M, Heinze J, Schmitt T, Foitzik S (2005) A chemical level in the coevolutionary arms race between an ant social parasite and its hosts. J Evol Biol 18:576–586
Dani FR, Jones GR, Destri S, Spencer SH, Turillazzi S (2001) Deciphering the recognition signature within the cuticular chemical profile of paper wasps. Anim Behav 62:165–171
Dettner K, Liepert C (1994) Chemical mimicry and camouflage. Annu Rev Entomol 39:129–154
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
Endo S, Itino T (2012) The aphid-tending ant Lasius fuji exhibits reduced aggression toward aphids marked with ant cuticular hydrocarbons. Popul Ecol 54:405–410
Greene MJ, Gordon DM (2007) Structural complexity of chemical recognition cues affects the perception of group membership in the ants Linephithema humile and Aphaenogaster cockerelli. J Exp Biol 210:897–905
Guerrieri FJ, Nehring V, Jørgensen CG, Nielsen J, Galizia CG, d’Ettorre P (2009) Ants recognize foes and not friends. Proc R Soc B 276:2461–2468
Hölldobler B, Wilson EO (1990) The ants. Springer, Berlin
Howard RW (1993) Cuticular hydrocarbons and chemical communication. In: Stanley-Samuelson DW, Nelson DR (eds) Insect lipids: chemistry, biochemistry, and biology. University of Nebraska Press, Lincoln, pp 179–226
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
Howard RW, Stanley-Samuelson DW, Akre RD (1990b) Biosynthesis and chemical mimicry of cuticular hydrocarbons from the obligate predator, Microdon albicomatus Novak (Diptera: Syrphidae) and its ant prey, Myrmica incompleta Provancher (Hymenoptera: Formicidae). J Kansas Entomol Soc 63:437–443
Lohman DJ, Liao Q, Pierce NE (2006) Convergence of chemical mimicry in a guild of aphid predators. Ecol Entomol 31:41–51
Lucas C, Pho DB, Jallon JM, Fresneau D (2005) Role of cuticular hydrocarbons in the chemical recognition between ant species in the Pachycondyla villosa species complex. J Insect Physiol 51:1148–1157
Nixon GEJ (1951) The association of ants with aphids and coccids. Commonwealth Institute of Entomology, London
Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA (2002) The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu Rev Entomol 47:733–771
Pontin AJ (1958) A preliminary note on the eating of aphids by ants of the genus Lasius (Hym., Formicidae). Entomol Mon Mag 94:9–11
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Radchenko A (2005) A review of the ants of the genus Lasius Fabricius, 1804, subgenus Dendrolasius Ruzsky, 1912 (Hymenoptera: Formicidae) from East Palaearctic. Ann Zool 55:83–94
Sakata H (1994) How an ant decides to prey on or to attend aphids. Res Popul Ecol 36:45–51
Sakata H (2000) Mechanisms restricting ant–aphid mutualism: ant foraging strategy and interference among sugar sources. Jpn J Ecol 50:13–22 (in Japanese with English abstract)
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
Silveira HCP, Oliveira PS, Trigo JR (2010) Attracting predators without falling prey: chemical camouflage protects honeydew-producing treehoppers from ant predation. Am Nat 175:261–268
Skinner GJ, Whittaker JB (1981) An experimental investigation of inter-relationships between the wood–ant (Formica rufa) and some tree–canopy herbivores. J Anim Ecol 50:313–326
Stadler B, Dixon AFG (2005) Ecology and evolution of aphid–ant interactions. Annu Rev Ecol Evol Syst 36:345–372
Thomas JA, Elmes GW (1998) Higher productivity at the cost of increased host-specificity when Maculinea butterfly larvae exploit ant colonies through trophallaxis rather than by predation. Ecol Entomol 23:457–464
Vander Meer RK, Morel L (1998) Nestmate recognition in ants. In: Breed MD, Winston ML, Espelie KE, Vander Meer RK (eds) Pheromone communication in social insects. Westview Press, Oxford, pp 79–103
Vander Meer RK, Wojcik DP (1982) Chemical mimicry in the myrmecophilous beetle Myrmecaphodius excavaticollis. Science 218:806–808
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
Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344
Yamaoka R (1990) Chemical approach to understanding interactions among organisms. Physiol Ecol Jpn 27:31–52
Yao I, Akimoto S (2001) Ant attendance changes the sugar composition of the honeydew of the drepanosiphid aphid Tuberculatus quercicola. Oecologia 128:36–43
Yao I, Shibao H, Akimoto S (2000) Costs and benefits of ant attendance to the drepanosiphid aphid Tuberculatus quercicola. Oikos 89:3–10
Acknowledgments
We thank R. Yamaoka, T. Akino, N. Fujiwara-Tsujii, and M.K. Hojo for analytical advice and technical support, M. Maruyama for ant identification, and T. Akino, H. Kuzume and two anonymous reviewers for valuable comments on an earlier draft of this manuscript. This study was supported by a Grant-in-Aid for Scientific Research (C-22570015), a Grant-in-Aid for Exploratory Research (18657008) from the Japan Society for the Promotion of Science, and by Research and Education Funding for Japanese Alps Inter-Universities Cooperative Project, MEXT, Japan.
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Endo, S., Itino, T. Myrmecophilous aphids produce cuticular hydrocarbons that resemble those of their tending ants. Popul Ecol 55, 27–34 (2013). https://doi.org/10.1007/s10144-012-0355-0
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DOI: https://doi.org/10.1007/s10144-012-0355-0