Abstract
Honeydew collectors of Formica pratensis taken from the nature (control) and laboratory-reared “naïve” ants, which had never met either “mature” workers or aphids and aphidophages, were observed during their interactions with various aphid enemies: adults and larvae of ladybirds and lacewings, and larvae of syrphid flies. The naïve ants were significantly more aggressive towards adults than towards larvae of aphidophages. More than 70% of the naïve ants treated ladybirds and lacewings as enemies at their first encounter and attacked them immediately without any prior antennation. The frequency of aggressive reactions (body jerking and bites) towards larvae was significantly higher in the control group, whereas the percentage of ants showing explorative behavior was significantly higher in the naïve ants. Overall, experience proved to be not important for displaying the key behavioral reactions towards adult ladybirds and lacewings underlying the protection of trophobionts from these natural enemies. However, accumulation of experience is assumed to play an important role in the recognition of aphidophage larvae and formation of aggressive behavior towards them.
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References
Addicott, J.F., “Competition for Mutualists: Aphids and Ants,” Canad. J. Zool. 56, 2093–2096 (1978).
Akino, T., “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 (2008).
Bishop, D.B. and Bristow, C.M., “Effects of the Presence of the Allegheny Mound Ant (Hymenoptera: Formicidae) in Providing Enemy-Free Space to Myrmecophilous Aphid and Soft Scale Populations,” Ann. Entomol. Soc. 96 (3), 202–210 (2003).
Bristow, C.M., “Differential Benefits from Ant Attendance to Two Species of Homoptera on New York Ironweed,” J. Anim. Ecol. 53, 715–726 (1984).
Buckley, R. and Gullan, P., “More Aggressive Ant Species (Hymenoptera: Formicidae) Provide Better Protection for Soft Scales and Mealybugs,” Biotropica 23, 282–286 (1991).
Delabie, J.H.C., “Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an Overview,” Neotrop. Entomol. 30 (4), 501 (2001).
Delattre, O., Châline, N., Chameron, S., et al., “Opportunist Slave-Making Ants Myrmoxenus ravouxi Discriminate Different Host Species from a Non-Host Species,” Ins. Soc. 60 (1), 7–13 (2013).
d'Ettorre, P. and Lenoir, A., “Nestmate Recognition,” in Ant Ecology, Ed. by L. Lach, C. Parr, and K. Abbott (Oxford Univ. Press, Oxford, 2010), pp. 194–209.
Dlussky, G.M., Ants of the Genus Formica (Nauka, Moscow, 1967) [in Russian].
Dorosheva, E.A. and Reznikova, Zh.I., “Ethological Mechanisms of Spatial Competition between Red Wood Ants and Ground Beetles,” Zh. Obshch. Biol. 67 (3), 190–206 (2006).
Dorosheva, E.A., Yakovlev, I.K., and Reznikova, Zh.I., “An Innate Template for Enemy Recognition in Red Wood Ants,” Zool. Zh. 90 (2), 184–191 (2011) [Entomol. Rev. 91 (2), 274-280 2011].
Douglas, J.M. and Sudd, J.H., “Behavioral Coordination between an Aphid (Symydobius oblongus Heyden; Hemiptera: Callaphidae) and the Ant that Attends It (Formica lugubris Zetterstedt; Hymenoptera: Formicidae): an Ethological Analysis,” Animal Behav. 28, 1127–1139 (1980).
Fischer, M.K., Hoffman, K.H., and Völkl, W., “Competition for Mutualists in an Ant-Homopteran Interaction Mediated by Hierarchies of Ant Attendance,” Oikos 92 (3), 531–541 (2001).
Gavrilyuk, A.V. and Novgorodova, T.A., “Efficiency of Aphid Protection by Different Species of Ants,” Doklady Ross. Akad. Nauk 417 (3), 427–429 (2007).
Gibernau, M. and Dejean, A., “Ant Protection of Heteropteran Trophobionts against a Parasitoid Wasp,” Oecologia 126, 53–57 (2001).
Gromysz-Kalkowska, K. and Unkiewicz-Winiarczyk, A., “Ethological Defense Mechanisms in Insects. II. Active Defense,” Ann. Univ. Mariae Curie-Sklod. Sec. C 66 (1), 143–153 (2011).
Grostal, P. and Dicke, M., “Direct and Indirect Cues of Predation Risk Influence Behavior and Reproduction of Prey: a Case for Acarine Interactions,” Behav. Ecol. 10, 422–427 (1999).
Hölldobler, B. and Wilson, E.O., The Ants (Springer-Verlag, Bern, 1990).
Hübner, G., “Differential Interactions between an Aphid Endohyperparasitoid and Three Honeydew-Collecting Ant Species: a Field Study of Alloxysta brevis (Thomson) (Hymenoptera: Alloxystidae),” J. Ins. Behav. 13 (5), 771–784 (2000).
Itioka, T. and Inoue, T., “The Alternation of Mutualistic Ant Species Affects the Population Growth of Their Trophobiont Mealybug,” Ecography 22, 169 (1999).
Katayama, N. and Suzuki, N., “Bodyguard Effects for Aphids of Aphis craccivora Koch (Homoptera: Aphididae) as Related to the Activity of Two Ant Species, Tetramorium caespitum L. (Hymenoptera: Formicidae) and Lasius niger L. (Hymenoptera: Formicidae),” Appl. Entomol. Zool. 38, 427–433 (2003).
Karhu, K.J., “Effects of Ant Exclusion during Outbreaks of a Defoliator and a Sap Sucker on Birch,” Ecol. Entomol. 23, 185–194 (1998).
Lahav, S., Soroker, V., Hefetz, A., and Vander Meer, R.K., “Direct Behavioral Evidence for Hydrocarbons as Ant Recognition Discriminators,” Naturwiss. 86, 246–249 (1999).
Lohman, D.J., Liao, Q., and Pierce, N.E., “Convergence of Chemical Mimicry in a Guild of Aphid Predators,” Ecol. Entomol. 31 (1), 41–51 (2006).
Majerus, M.E.N., Sloggett, J.J., Godeau, J.-F., and Hemptinne, J.L., “Interactions between Ants and Aphidophagous and Coccidophagous Ladybirds,” Popul. Ecol. 49, 15–27 (2007).
Mordvilko, A.K., “On Biology and Morphology of Aphids,” Trudy Russ. Entomol. O-va 33, 418 (1901).
Nagy, C., Markó, V., and Cross, J., “Effects of Exclusion or Supplementary Honey Feeding of the Common Black Ant, Lasius niger (L.), on Aphid Populations and Natural Enemies on Apple,” IOBC/WPRS Bull. 30, 43–50 (2007).
Nixon, G.F.J., The Association of Ants with Aphids and Coccids (Commonwealth Inst. of Entomology, London, 1951).
Novgorodova, T.A., “Ant-Aphid Interactions in Multi-Species Ant Communities: Some Ecological and Ethological Aspects,” Eur. J. Entomol. 102 (3), 495 (2005a).
Novgorodova, T.A., “Relative Influence of the Members of a Multi-Species Ant Association on the Potential Abundance of the Common Aphid Symbionts,” Doklady Ross. Akad. Nauk 401 (6), 848–849 (2005b).
Novgorodova, T.A., “Specialization in Groups of Worker Ants during Trophobiosis with Aphids,” Zh. Obshch. Biol. 69 (4), 284–293 (2008).
Novgorodova, T.A. and Gavrilyuk, A.V., “The Degree of Protection Different Ants (Hymenoptera: Formicidae) Provide Aphids (Hemiptera: Aphididae) against Aphidophages,” Eur. J. Entomol. 109, 187–196 (2012).
Novgorodova, T.A. and Gavrilyuk, A.V., “How to Avoid Ant Aggression: Some Behavioral Traits of Aphidophages,” Trudy Russ. Entomol. O-va 84 (2), 80–87 (2013).
Novgorodova, T.A. and Reznikova, Zh.I., “Ecological Aspects of Interactions of Ants and Aphids in the Recreational Forest Zone of Akademgorodok, Novosibirsk,” Sibir. Ekol. Zh., Nos. 3–4, 239–245 (1996).
Oliver, T.H., Leather, S.R., and Cook, J.M., “Macroevolutionary Patterns in the Origin of Mutualisms Involving Ants,” J. Evol. Biol. 21, 1597–1608 (2008).
Phillips, D. and Willis, C.K.R., “Defensive Behavior of Ants in a Mutualistic Relationship with Aphids,” Behav. Ecol. Sociobiol. 59, 321–325 (2005).
Reznikova, Zh.I. and Novgorodova, T.A., “Individual Roles and Information Exchange in Groups of Ant Workers,” Uspekhi Sovrem. Biol. 118 (3), 345 (1998a).
Reznikova, Zh.I. and Novgorodova, T.A., “Individual and Social Experience of Ants in Their Interaction with Symbiotic Aphids,” Doklady Ross. Akad. Nauk 359 (4), 572–574 (1998b).
Rotheray, G.E., “Color, Shape and Defense in Aphidophagous Syrphid Larvae (Diptera),” Zool. J. Linn. Soc. 88, 201–216 (1986).
Shingleton, A.W. and Foster, W.A., “Ant Tending Influences Soldier Production in a Social Aphid,” Proc. Royal Soc. B 267, 1863–1868 (2000).
Szentkirályi, F., “Ecology and Habitat Relationships,” in Lacewings in the Crop Environment, Ed. by P. McEwen, T.R. New, and A.E. Whittington (Cambridge Univ. Press, Cambridge, 2001), pp. 82–115.
Tilles, D.A. and Wood, D.L., “The Influence of the Carpenter Ant (Camponotus modoc) (Hymenoptera: Formicidae) Attendance on the Development and Survival of Aphids (Cinara spp.) (Homoptera: Aphididae) in a Giant Sequoia Forest,” Canad. Entomol. 114, 1133–1142 (1982).
Way, M.J., “Mutualism between Ants and Honeydew Producing Homoptera,” Ann. Rev. Entomol. 8, 307 (1963).
Yakovlev, I.K., Candidate's Dissertation in Biology (Novosibirsk, 2010).
Zakharov, A.A., Ant, Family, Colony (Nauka, Moscow, 1978) [in Russian].
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Original Russian Text © T.A. Novgorodova, 2015, published in Zoologicheskii Zhurnal, 2015, Vol. 94, No. 10, pp. 1190–1199.
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Novgorodova, T.A. Interaction of ants with aphid enemies: Do inexperienced ants specializing in honeydew collection recognize aphidophages at their first contact?. Entmol. Rev. 95, 1182–1190 (2015). https://doi.org/10.1134/S0013873815090055
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DOI: https://doi.org/10.1134/S0013873815090055