Abstract
Animals communicate with each other using a variety of signal modalities, any of which can provide useful information to non-intended receivers, or eavesdroppers. Eavesdropping on chemical signals is a widespread phenomenon but its role in shaping the behavior of multi-species assemblages is poorly known. Here, we tested the hypothesis that workers of multiple Neotropical ant species change their behaviors when exposed to odors of the common canopy ant, Azteca trigona. We exposed workers of 16 canopy ant species (five subfamilies) to A. trigona alarm pheromones and compared their behavioral responses to the behavior of ants in control treatments (ambient air). Seven species showed distinct responses to A. trigona odors relative to the control. The most common behavioral responses were increased antennation and running. The results of this study suggest that eavesdropping on heterospecific alarm signals allows ants to avoid generalized threats or negative interactions with aggressive A. trigona workers. Such eavesdropping presumably is selectively advantageous and may determine local arboreal ant species distributions and interspecific differences in access to resources in the forest canopy.
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References
Adams ES (1990) Interaction between the ants Zacryptocerus maculatus and Azteca trigona: interspecific parasitization of information. Biotropica 22:200–206. https://doi.org/10.2307/2388413
Adams ES (1994) Territory defense by the ant Azteca trigona: maintenance of an arboreal ant mosaic. Oecologia 97:202–208. https://doi.org/10.1007/BF00323150
Adams ES (2016) Territoriality in ants (Hymenoptera: Formicidae): a review. Myrmecological News 23:101–118. https://doi.org/10.1016/0095-8956(72)90015-9
Adams BJ, Schnitzer SA, Yanoviak SP (2017) Trees as islands: canopy ant species richness increases with the size of liana-free trees in a Neotropical forest. Ecography 40:1067–1075. https://doi.org/10.1111/ecog.02608
Adams RMM, Wells RL, Yanoviak SP et al (2020) Interspecific eavesdropping on ant chemical communication. Front Ecol Evol 8:24. https://doi.org/10.3389/fevo.2020.00024
Andersen AN, Patel AD (1994) Meat ants as dominant members of Australian ant communities: an experimental test of their influence on the foraging success and forager abundance of other species. Oecologia 98:15–24. https://doi.org/10.1007/BF00326085
Apfelbach R, Blanchard CD, Blanchard RJ et al (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144. https://doi.org/10.1016/j.neubiorev.2005.05.005
Armbrecht I, Jiménez E, Alvarez G et al (2001) An ant mosaic in the Colombian rain forest of Chocó (Hymenoptera: Formicidae). Sociobiology 37:491–509
Attygalle AB, Morgan ED (1984) Chemicals from the glands of ants. The Royal Society of Chemistry London 13:245–278. https://doi.org/10.1039/CS9841300245
Blum MS (1969) Alarm Pheromones. Annu Rev Entomol 14:57–80. https://doi.org/10.1146/annurev.en.14.010169.000421
Bossert WH, Wilson EO (1963) The analysis of olfactory communication among animals. J Theor Biol 5:443–469. https://doi.org/10.1016/0022-5193(63)90089-4
Cárdenas M, Jiroš P, Pekár S (2012) Selective olfactory attention of a specialised predator to intraspecific chemical signals of its prey. Naturwissenschaften 99:597–605. https://doi.org/10.1007/s00114-012-0938-9
Carroll CR, Janzen DH (1973) Ecology of foraging by ants. Annu Rev Ecol Syst 4:231–257. https://doi.org/10.1146/annurev.es.04.110173.001311
Croat TB (1978) Flora of Barro Colorado Island. Stanford University Press, Stanford
Curtis BA (1985) Observations on the natural history and behaviour of the dune ant, Camponotus detritus Emery, in the central Namib Desert. Modoqua 3:279–289
Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153. https://doi.org/10.1086/285308
Feener DH, Jacobs LF, Schmidt JO (1996) Specialized parasitoid attracted to a pheromone of ants. Anim Behav 51:61–66. https://doi.org/10.1006/anbe.1996.0005
Frost CJ, Mescher MC, Carlson JE, de Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824. https://doi.org/10.1104/pp.107.113027
Goodale E, Nieh JC (2012) Public use of olfactory information associated with predation in two species of social bees. Anim Behav 84:919–924. https://doi.org/10.1016/j.anbehav.2012.07.016
Hölldobler B, Wilson EO (1990) The ants. Springer, Berlin
Joint I, Downie JA, Williams P (2007) Bacterial conversations: talking, listening and eavesdropping. An introduction. Phil Trans R Soc B 362:1115–1117. https://doi.org/10.1098/rstb.2007.2038
Jutsum AR, Cherrett JM, Fisher M (1981) Interactions between the fauna of citrus trees in Trinidad and the ants Atta cephalotes and Azteca sp. J Appl Ecol 18:187–195. https://doi.org/10.2307/2402488
Keeling CI, Plettner E, Slessor KN (2004) Hymenopteran semiochemicals. Top Curr Chem 239:133–177. https://doi.org/10.1007/b95452
Leigh EG, Rand AS, Windsor DM (1996) The ecology of a tropical rain forest: seasonal rhythms and long term changes. Smithsonian Press, Washington D.C.
Leonhardt SD, Menzel F, Nehring V, Schmitt T (2016) Ecology and evolution of communication in social insects. Cell 164:1277–1287. https://doi.org/10.1016/j.cell.2016.01.035
Longino JT (2007) A taxonomic review of the genus Azteca (Hymenoptera: Formicidae) in Costa Rica and a global revision of the aurita group. Zootaxa 1491:1–63
Mathis KA, Philpott SM, Moreira RF (2011) Parasite lost: chemical and visual cues used by Pseudacteon in search of Azteca instabilis. J Insect Behav 24:186–199. https://doi.org/10.1007/s10905-010-9247-3
McCann S, Moeri O, Jones T et al (2013) Strike fast, strike hard: the red-throated caracara exploits absconding behavior of social wasps during nest predation. PLoS ONE 8:e84114. https://doi.org/10.1371/journal.pone.0084114
Norman VC, Butterfield T, Drijfhout F et al (2017) Alarm pheromone composition and behavioral activity in fungus-growing ants. J Chem Ecol 43:225–235. https://doi.org/10.1007/s10886-017-0821-4
Obin MS, vander Meer RK, (1985) Gaster flagging by fire ants (Solenopsis spp.): functional significance of venom dispersal behavior. J Chem Ecol 11:1757–1768. https://doi.org/10.1007/BF01012125
Peake TM (2005) Eavesdropping in communication networks. In: McGregor PK (ed) Animal communication networks. Cambridge University Press, Cambridge
Pfeiffer W (1962) The fright reaction of fish. Biol Rev Camb Philos Soc 37:495–511. https://doi.org/10.1111/j.1469-185X.1962.tb01333.x
Pokorny T, Sieber LM, Hofferberth JE, et al (2020) Age-dependent release of and response to alarm pheromone in a Ponerine ant. Journal of Experimental Biology 223:jeb218040. https://doi.org/10.1242/jeb.218040
Roitberg BD, Isman MB (1992) Insect chemical ecology: an evolutionary approach. Chapman and Hall, New York
Stowe MK, Turlings TCJ, Loughrin JH et al (1995) The chemistry of eavesdropping, alarm, and deceit. Proc Natl Acad Sci USA 92:23–28. https://doi.org/10.1073/pnas.92.1.23
Symonds MRE, Elgar MA (2008) The evolution of pheromone diversity. Trends Ecol Evol 23:220–228. https://doi.org/10.1016/j.tree.2007.11.009
Wheeler DE (1986) Polymorphism and division of labor in Azteca chartifex laticeps (Hymenoptera: Formicidae). J Kansas Entomol Soc 59:542–548
Wheeler JW, Evans SL, Blum MS, Torgerson RL (1975) Cyclopentyl ketones: identification and function in Azteca ants. Science 187:254–255. https://doi.org/10.1126/science.1111099
Wilson EO (1965) Trail sharing in ants. Psyche 72:2–7. https://doi.org/10.1155/1965/24875
Wilson EO (1968) The ergonomics of caste in the social insects. Am Nat 102:41–66. https://doi.org/10.1086/282522
Wüst M, Menzel F (2017) I smell where you walked—how chemical cues influence movement decisions in ants. Oikos 126:149–160. https://doi.org/10.1111/oik.03332
Wyatt TD (2014) Pheromones and animal behavior: chemical signals and signatures, 2nd edn. Cambridge University Press, Cambridge
Yanoviak SP, Kaspari M (2000) Community structure and the habitat templet: ants in the tropical forest canopy and litter. Oikos 89:259–266. https://doi.org/10.1034/j.1600-0706.2000.890206.x
Acknowledgements
Noah Gripshover and Aspen Workman assisted in the lab; Benjamin Adams, Jelena Bujan, and Daniella Prince assisted in the field; Evan Gora provided statistical advice. Comments from Benjamin Adams, Natalie Christian, Perri Eason, Evan Gora, Kane Lawhorn, Daniella Prince, and Jeannine Richards improved the manuscript. We thank Melissa Cano and the staff of the Smithsonian Tropical Research Institute for logistical support in Panama. This work was supported by the National Science Foundation grants GRF-2018265609 to RLW, IOS-1656625 and IOS-2101059 to CJF, and DEB-1252614 to SPY.
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This work was supported by the National Science Foundation grants GRF-2018265609 to RLW, IOS-1656625 and IOS-2101059 to CJF, and DEB-1252614 to SPY.
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All authors contributed to the study conception and design. Material preparation, data collection, and analyses were performed by RLW. All authors contributed to the writing, and read and approved the final version.
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Wells, R.L., Frost, C.J. & Yanoviak, S.P. Effects of Azteca trigona alarm pheromones on heterospecific ant behavior. Insect. Soc. 68, 359–365 (2021). https://doi.org/10.1007/s00040-021-00836-2
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DOI: https://doi.org/10.1007/s00040-021-00836-2