Defensive Strategies of a Noctuid Caterpillar in a Myrmecophytic Plant: are Dyops Larvae Immune to Azteca Ants?
Keywords:Defensive behavior, larval behavior, insect-plant interaction, oral secretion, resource partitioning.
Immature stages of insects are generally susceptive to their natural enemies, but many species developed defensive and evasive mechanisms to circumvent predation. Gregarious larvae of the noctuid moth Dyops cf. cuprescens feed on leaves of young Cecropia pachystachya shrubs colonized by Azteca ants. Ants avoid contact with larval clusters, retreating to the nest when larvae are moving near the stems. Provoked encounters revealed that Dyops caterpillars present several specialized behaviors to avoid and overcome ant attacks, such as fleeing to under leaf, jumping off the leaf, curling and wriggling vigorously the anterior portion of the body, spitting droplets of oral fluids, or killing ants by pouncing them. These mechanisms allow the caterpillars to overcome ant attacks and consume leaves of ant-colonized plants. By feeding on a heavily protected plant, larvae can enjoy not only a competitor-free plant, but possibly also the enemy-free space created by the aggressive ants.
Aguiar, A.P., dos Santos, B.F., Couri, M.S., Rafael, J.A., Costa, C., Ide, S., Duarte, M., Grazia, J., Schwertner, C.F., Freitas, A.V.L. & Azevedo, C.O. (2009). Capítulo 8: Insecta. In R.M. Rocha & W.A.P. Boeger (Eds.), Estado da Arte e Perspectivas para a Zoologia no Brasil (pp. 131-155). Resultados dos Simpósios do XXVII Congresso Brasileiro de Zoologia. Curitiba: Editora UFPR.
Bächtold, A., Del-Claro, K., Kaminski, L.A., Freitas, A.V.L. & Oliveira, P.S. (2012). Natural history of an ant-plant-butterfly interaction in a Neotropical savanna. Journal of Natural History, 46: 943-954. doi: 10.1080/00222933.2011.651649
Bentley, B.L. & Benson, W.W. (1988). The influence of ant foraging patterns on the behavior of herbivores. In J.C. Trager (ed.), Advances in Myrmecology (pp. 297-306), New York: E.J. Brill.
Bernays, E.A. (1997). Feeding by lepidopteran larvae is dangerous. Ecological Entomology, 22: 121-123. doi: 10.1046/j.1365-2311.1997.00042.x
Collins, M.M. (2013). On the finding of dead ants attached to Saturniid caterpillars: Evidence of successful deterrent chemistry? Journal of the Lepidopterists’ Society, 67: 62-63. doi: 10.18473/lepi.v67i1.a10
Dáttilo, W., Aguirre, A., Torre, P.L.L., Kaminski, L.A., Garcia-Chavez, J. & Rico-Gray, V. (2016). Trait-mediated indirect interactions of ant shape on the attack of caterpillars and fruits. Biology Letters, 12: 1-4. doi: 10.1098/rsbl.2016.0401
Davidson, D.W. (2005). Cecropia and its biotic defenses. In C.C. Berg & P.F. Rosselli (Eds.), Cecropia (pp. 214-226). Flora Neotropica Monograph. Bronx New York: The New York Botanical Garden.
DeVries, P.J. (1991). Foam barriers, a new defense against ants for milkweed butterfly caterpillars (Nymphalidae: Danainae). The Journal of Research on the Lepidoptera, 30: 261-266.
Discover Life (2018). Map center of Dyops cuprescens. http://www.discoverlife.org/mp/20m?kind=Dyops+cuprescens (accessed date: 26 March 2018).
Edmunds, M. (1974). Defence in Animals. A Survey of Anti-predator defences. Harlow, UK: Longman Group, 357 p.
Eubanks, M.D., Nesci, K.A., Petersen, M.K., Liu, Z. & Sanchez, A.B. (1997). The exploitation of an ant-defended host plant by a shelter-building herbivore. Oecologia, 109: 454-460. doi: 10.1007/s004420050105
Francini, R.B. (2010). História natural das borboletas do Vale do Rio Quilombo, Santos, SP, 2a. Edição. E-book arquivo PDF, Santos, SP, 550 p. doi: 10.13140/2.1.3862.9441
Freitas, A.V.L. (1996). Population biology of Heterosais edessa (Nymphalidae) and its associated Ithomiinae community. Journal of the Lepidopterists’ Society, 50: 273-289.
Freitas, A.V.L. (1999). An anti-predator behavior in larvae of Libytheana carineta (Nymphalidae, Libytheinae). Journal of the lepidopterists’ Society, 53: 130-131.
Freitas, A.V.L. & Oliveira, P.S. (1992). Biology and behavior of the neotropical butterfly Eunica bechina (Nymphalidae) with special reference to larval defence against ant predation. Journal of Research on the Lepidoptera, 31: 1-11.
Freitas, A.V.L. & Oliveira, P.S. (1996). Ants as Selective Agents on Herbivore Biology: Effects on the Behaviour of a Non-Myrmecophilous Butterfly. Journal of Animal Ecology, 65: 205-210.
Frost, S.W. (1959). Insect Life and Natural History. New York, Dover, 526 p
Gentry, G.L. & Dyer, L.A. (2002). On the conditional nature of neotropical caterpillar defenses against their natural enemies. Ecology, 83: 3108-3119. doi: 10.1890/0012-9658(2002)083[3108:OTCNON]2.0.CO;2
Greeney, H. F. & Jones, M.T. (2003). Shelter building in the Hesperiidae: a classification scheme for larval shelters. Journal of Research on the Lepidoptera, 37: 27-36.
Greeney, H.F., Dyer, L.A. & Smilanich, A.M. (2012). Feeding by lepidopteran larvae is dangerous: A review of caterpillars’ chemical, physiological, morphological, and behavioral defenses against natural enemies. Invertebrate Survival Journal, 9: 7-34. Retrieved from: http://www.isj.unimo.it/articoli/ISJ256.pdf
Heads, P.A. & Lawton J.H. (1985). Braken, ants and extrafloral nectaries. III. How insect hebivores avoid ant predation. Ecological Entomology, 10: 29-42. doi: 10.1111/j.1365-2311.1985.tb00532.x
IBGE, (2012). Manual Técnico da Vegetação Brasileira. Instituto Brasileiro de Geográfica e Estatística Rio de Janeiro: IBGE, 275 p
Ihering, H. (1907). Die Cecropien und ihre Schutzameisen. Engler’s Botanische Jahrbücher, 39: 666-714.
Janzen, D. H. 1969. Allelopathy by myrmecophytes: The ant Azteca as an allelopathic agent of Cecropia. Ecology, 50: 147-153.
Janzen, D.H. & Hallwachs, W. (2017). Dynamic Database for an Inventory of the Macrocaterpillar Fauna, and its Food Plants and Parasitoids, of the Area De Conservacion Guanacaste, Northwestern Costa Rica. University of Pennsylvania, Philadelphia, PA. http://janzen.sas.upenn.edu/caterpillars/database.lasso (accessed date: 28 December 2017).
Jeffries, M.J. & Lawton, J.H. (1984). Enemy free space and the structure of ecological communities. Biological Journal of the Linnean Society, 23: 269-286. doi: 10.1111/j.1095-8312.1984.tb00145.x
Kaminski, L.A., Freitas A.V.L. & Oliveira P.S. (2010). Interaction between mutualisms: Ant-tended butterflies exploit enemy-free space provided by ant-treehopper associations. American Naturalist, 176: 322-334. doi: 10.1086/655427
Lawrence, W.S. (1990). The effects of group-size and host species on development and survivorship of a gregarious caterpillar Halisidota caryae (Lepidoptera, Arctiidae). Ecological Entomology, 15: 53-62. doi: 10.1111/j.1365-2311.1990.tb00783.x
Longino, J.T. (1991). Azteca ants in Cecropia trees: taxonomy, colony structure, and behavior. In D. Cutler & C. Huxley (Eds.), Ant-Plant Interactions (pp. 271-288). Oxford: Oxford University Press.
Machado, G. & Freitas, A.V.L. (2001). Larval defence against ant predation in the butterfly Smyrna blomfildia. Ecological Entomology, 26: 436-439. doi: 10.1046/j.1365-2311.2001.00328.x
McClure, M. & Despland, E. (2011). Defensive responses by a social caterpillar are tailored to different predators and change with larval instar and group size. Naturwissenschaften, 98(5): 425-434. doi: 10.1007/s00114-011-0788-x
Moraes, A.R., Greeney, H.F., Oliveira, P.S., Barbosa, E.P. & Freitas, A.V.L. (2012). Morphology and behavior of the early stages of the skipper, Urbanus esmeraldus, on Urera baccifera, an ant-visited host plant. Journal of Insect Science, 12: 52. doi: 10.1673/031.012.5201
Müller, F. (1881). Die Imbauba und ihre Beschuetzer. Kosmos, 8:109-116.
Oliveira, K.N., Coley, P.D., Kursar, T.A., Kaminski, L.A., Moreira, M.Z. & Campos, R.I. (2015). The effect of symbiotic ant colonies on plant growth: a test using an Azteca-Cecropia System. PLOS ONE 10 (3): e0120351. doi: 10.1371/journal.pone.0120351
Oliveira, P.S. & Freitas, A.V.L. (2004). Ant-plant-herbivore interactions in the Neotropical Cerrado savanna. Naturwissenschaften, 91: 557-570. doi: 10.1007/s00114-004-0585-x
Peterson, S.C., Johnson, N.D. & LeGuyader, J.L. (1987). Defensive regurgitation of allelochemicals derived from host cyanogenesis by eastern tent caterpillars. Ecology, 68: 1268-1272. doi: 10.2307/1939211
Price, P.W., Bouton, C.E., Gross, P., Mcpheron, B.A., Thompson, J.N. & Weis, A.E. (1980). Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics, 11: 41-65. doi: 10.1146/annurev.es.11.110180.000353
Remmel, T., Davison, J. & Tammaru, T. (2011). Quantifying predation on folivorous insect larvae: the perspective of life-history evolution. Biological Journal of the Linnean Society, 104: 1-18. doi: 10.1111/j.1095-8312.2011.01721.x
Rostas, M. & Blassmann, K. (2009). Insects had it first: Surfactants as a defense against predators. Proceedings of the Royal Society B, 276: 633-638. doi: 10.1098/rspb.2008.1281
Salazar, B.A. & Whitman, D.W. (2001). Defensive tactics of caterpillars against predators and parasitoids. In T.N. Ananthakrishnan (Ed.), Insects and Plant Defences Dynamics (pp. 161-207). Plymouth, UK: Science Publishers, Inc.
Sendoya, S.F. & Oliveira, P.S. (2015). Ant-caterpillar antagonism at the community level: interhabitat variation of tritrophic interactions in a neotropical savanna. Journal of Animal Ecology, 84: 442-452. doi: 10.1111/1365-2656.12286
Sendoya, S.F. & Oliveira, P.S. (2017). Behavioural ecology of defence in a risky environment: caterpillars versus ants in a Neotropical savanna. Ecological Entomology, 42: 553-564. doi: 10.1111/een.12416
Schupp, E.W. (1986). Azteca protection of Cecropia: Ant occupation benefits juvenile trees. Oecologia, 70: 379-385. doi: 10.1007/BF00379500
Smedley, S.R., Ehrhardt, E. & Eisner, T. (1993). Defensive regurgitation by a noctuid moth larva (Litoprosopus futilis). Psyche: A Journal of Entomology, 100: 209-221. doi: 10.1155/1993/67950
Singer, M.S., Farkas, T.E., Skorik, C.M. & Mooney, K.A. (2012). Tritrophic interactions at a community level: effects of host plant species quality on bird predation of caterpillars. American Naturalist, 179: 363-374. doi: 10.1086/664080
Turner, G.F. & Pitcher, T.J. (1986). Attack abatement: a model for group protection by combined avoidance and dilution. The American Naturalist, 128: 228-240. doi: 10.1086/284556
Wiltshire, E.P. (1962). Notes on Neotropical Lepidoptera. 1. The early stages and comparative morphology of two species of Dyops (Noctuidae) hitherto confused. Journal of the Lepidopterists’ Society, 16: 47-54.
Zhang, Z.-Q. (2011). Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa, 3148: 1-237.
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