Abstract
Ants attack and exclude natural enemies of aphids in ant–aphid mutualisms. However, larvae of the green lacewing, Mallada desjardinsi, prey on the cowpea aphid, Aphis craccivora, without exclusion by aphid-tending ants. Lacewing larvae are protected from ants by carrying aphid carcasses on their backs. Here, we tested whether cuticular hydrocarbons (CHCs) of aphid carcasses affected the aggressiveness of aphid-tending ants. Aphid carcasses were washed with n-hexane to remove lipids. Lacewing larvae with washed aphid carcasses were attacked by aphid-tending ants more frequently than those with untreated aphid carcasses. We measured the aggressiveness of aphid-tending ants to lacewing larvae that were either carrying a piece of cotton wool (a dummy aphid carcass) treated with CHCs from aphids or lacewing larvae, or carrying aphid carcasses. The rates of attack by ants on lacewing larvae carrying CHCs of aphids or aphid carcasses were lower than that of attack on lacewing larvae with conspecific CHCs. Chemical analysis by gas chromatography/mass spectrometry showed similarity of CHCs between aphids and aphid carcasses. These results suggest that aphid carcasses on the backs of lacewing larvae function via chemical camouflage to limit attacks by aphid-tending ants.
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References
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, 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-Biol Sci 266:1419–1426
Bonavita-Cougourdan A, Clément JL, Lange C (1987) Nestmate recognition: the role of cuticular hydrocarbons in the ant Camponotus vagus Scop. J Entomol Sci 22:1–10
Breton LM, Addicott JF (1992) Density-dependent mutualism in an aphid-ant interaction. Ecology 73:2175–2180
Carlson DA, Bernier UR, Sutton BD (1998) Elution patterns from capillary GC for methyl-branched alkanes. J Chem Ecol 24:1845–1865
Choe D-H, Rust MK (2006) Homopteran chemical signatures reduce aggression of tending ants. Chemoecology 16:175–178
Dettner K, Liepert C (1994) Chemical mimicry and camouflage. Annu Rev Entomol 39:129–154
Eisner T, Hicks K, Eisner M, Robson DS (1978) “Wolf-in-sheep’s-clothing” strategy of a predaceous insect larva. Science 199:790–794
Elgar MA, Allan RA (2004) Predatory spider mimics acquire colony-specific cuticular hydrocarbons from their ant model prey. Naturwissenschaften 91:143–147
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
Endo S, Itino T (2013) Myrmecophilous aphids produce cuticular hydrocarbons that resemble those of their tending ants. Popul Ecol 55:27–34
Gibbs AG (1998) The role of lipid physical properties in lipid barriers. Am Zool 38:268–279
Glinwood R, Willekens J, Pettersson J (2003) Discrimination of aphid mutualists by an ant based on chemical cues. Acta Agric Scand B-S P 53:177–182
Godeau J-F, Hemptinne J-L, Dixon AFG, Verhaeghe J-C (2009) Reaction of ants to, and feeding biology of, a congeneric myrmecophilous and non-myrmecophilous ladybird. J Insect Behav 22:173–185
Hayashi M, Nomura M (2011) Larvae of the green lacewing Mallada desjardinsi (Neuroptera: Chrysopidae) protect themselves against aphid-tending ants by carrying dead aphids on their backs. Appl Entomol Zool 46:407–413
Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–453
Howard RW, McDaniel CA, Blomquist GJ (1978) Cuticular hydrocarbons of the eastern subterranean termite, Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae). J Chem Ecol 4:233–245
Kaneko S (2002) Aphid-attending ants increase the number of emerging adults of the aphid’s primary parasitoid and hyperparasitoids by repelling intraguild predators. Entomol Sci 5:131–146
Kaneko S (2007) Predator and parasitoid attacking ant-attended aphids: effects of predator presence and attending ant species on emerging parasitoid numbers. Ecol Res 22:451–458
Kaplan I, Eubanks MD (2005) Aphids alter the community-wide impact of fire ants. Ecology 86:1640–1649
Katayama N, Suzuki N (2002) Cost and benefit of ant attendance for Aphis craccivora (Hemiptera: Aphididae) with reference to aphid colony size. Can Entomol 134:241–249
Katayama N, Suzuki N (2003a) Changes in the use of extrafloral nectaries of Vicia faba (Leguminosae) and honeydew of aphids by ants with increasing aphid density. Ann Entomol Soc Am 96:579–584
Katayama N, Suzuki N (2003b) Bodyguard effects for aphids of Aphis craccivora Koch (Homoptera: Aphididae) as related to the activity of two ant species, Tetramorium caespitum Linnaeus (Hymenoptera: Formicidae) and Lasius niger L. (Hymenoptera: Formicidae). Appl Entomol Zool 38:427–433
Lang C, Menzel F (2011) Lasius niger ants discriminate aphids based on their cuticular hydrocarbons. Anim Behav 82:1245–1254
Liepert C, Dettner K (1993) Recognition of aphid parasitoids by honeydew-collecting ants: the role of cuticular lipids in a chemical mimicry system. J Chem Ecol 22:695–707
Liepert C, Dettner K (1996) Role of cuticular hydrocarbons of aphid parasitoids in their relationship to aphid-attending ants. J Chem Ecol 19:2143–2153
Liere H, Perfecto I (2008) Cheating on a mutualism: Indirect benefits of ant attendance to a coccidophagous coccinellid. Environ Entomol 37:143–149
Lohman DJ, Liao Q, Pierce NE (2006) Convergence of chemical mimicry in a guild of aphid predators. Ecol Entomol 31:41–51
Mochizuki A, Naka H, Hamasaki K, Mitsunaga T (2006) Larval cannibalism and intraguild predation between the introduced green lacewing, Chrysoperla carnea, and the indigenous trashcarrying green lacewing, Mallada desjardinsi (Neuroptera: Chrysopidae), as a case study of potential nontarget effect assessment. Environ Entomol 35:1298–1303
Monnin T (2006) Chemical recognition of reproductive status in social insects. Ann Zool Fenn 43:515–530
Nakahira K, Arakawa R (2006) Defensive functions of the trashpackage of a green lacewing, Mallada desjardinsi (Neuroptera: Chrysopidae), against a ladybird, Harmonia axyridis (Coleoptera: Coccinellidae). Appl Entomol Zool 41:111–115
Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Y, Nisimura T, Yamaoka R (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309:311–314
Schwartzberg EG, Haynes KF, Johnson DW, Brown GC (2010) Wax structures of Scymnus louisianae attenuate aggression from aphid-tending ants. Environ Entomol 35:1298–1303
Sloggett JJ, Majerus MEN (2003) Adaptations of Coccinella magnifica, a myrmecophilous coccinellid to aggression by wood ants (Formica rufa group). II. Larval behaviour, and ladybird oviposition location. Eur J Entomol 100:337–344
Sloggett JJ, Völkl W, Schulze W, von der Schulenburg JH, Majerus MEN (2002) The ant-associations and diet of the ladybird Coccinella magnifica (Coleoptera: Coccinellidae). Eur J Entomol 99:565–569
Stadler B, Dixon AFG (2005) Ecology and evolution of aphid-ant interactions. Annu Rev Ecol Evol Syst 36:345–372
Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc B Biol Sci 274:151–164
Völkl W (1992) Aphids or their parasitoids: who actually benefits from ant-attendance? J Anim Ecol 61:273–281
Völkl W, Mackauer M (1993) Interactions between ants attending Aphis fabae ssp. cirsiiacanthoidis on thistles and foraging parasitoid wasps. J Insect Behav 6:301–312
Völkl W, Vohland K (1996) Wax covers in larvae of two Scymnus species: Do they enhance coccinellid larval survival? Oecologia 107:498–503
Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–343
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
Yao I, Shibao H, Akimoto S-I (2000) Costs and benefits of ant attendance to the drepanosiphid aphid Tuberculatus quercicola. Oikos 89:3–10
Acknowledgments
We are grateful to J. Millar of the University of California, Riverside for reviewing the manuscript. We also thank H. Shimoji of Hokkaido University and S. Endo of Shinshu University for technical advice. This work was supported by grants from the Japan Society for the Promotion of Science for Young Scientists to M. H. (24–4473).
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Hayashi, M., Choh, Y., Nakamuta, K. et al. Do Aphid Carcasses on the Backs of Larvae of Green Lacewing Work as Chemical Mimicry against Aphid-Tending Ants?. J Chem Ecol 40, 569–576 (2014). https://doi.org/10.1007/s10886-014-0451-z
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DOI: https://doi.org/10.1007/s10886-014-0451-z