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Type: Article
Published: 2022-05-11
Page range: 415-425
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Redescription and oviposition behavior of an orb-weaver spider parasitoid Hymenoepimecis cameroni Townes, 1966 (Hymenoptera: Ichneumonidae)

Programa de Pós-Graduação em Ciências Ambientais, Universidade do Estado de Minas Gerais, Frutal, MG, Brazil.
Programa de Pós-Graduação em Entomologia, Instituto Nacional de Pesquisas da Amazônia, Amazonas, Manaus, Brazil.
Graduação em Ciências Biológicas, Universidade do Estado de Minas Gerais, Ubá, MG, Brazil.
Graduação em Ciências Biológicas, Universidade do Estado de Minas Gerais, Ubá, MG, Brazil.
Programa de Pós-Graduação em Ciências Ambientais, Universidade do Estado de Minas Gerais, Frutal, MG, Brazil. Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.
Hymenoptera Atlantic forest Darwin wasp ectoparasitoid koinobiont orb-web Pimplinae polysphinctine

Abstract

Strategies to invade and exploit hosts for survival are an essential part of the parasitic lifestyle. Species of the Polysphincta genus group (Hymenoptera: Ichneumonidae), which utilize spiders as hosts, are examples of parasitoids that present several behavioral strategies in host immobilization and egg laying. In this study, we characterized the oviposition behavior of the Darwin wasp Hymenoepimecis cameroni Townes, 1966 (Hymenoptera: Ichneumonidae) on their host spider, performed the taxonomic description of the female, and redescribed the male parasitoid. We observed eight H. cameroni females endeavoring to parasitize young Leucauge volupis (Keyserling, 1893) spiders. Each female made up to 12 successive attempts at oviposition, totaling 36 observed attacks, with only two successful attacks. The main oviposition behavior of H. cameroni individuals consists of flying close to the web and performing a direct attack on the spider, which often results in the spider escaping into the vegetation. We observed that in seven events where the spiders fled into the vegetation, the individuals of H. cameroni adopted a second strategy, which consisted of hanging from the hind legs in the web hub. This observation showed that the females of H. cameroni have the ability to modulate the oviposition strategy after a failure in the initial attack. The pattern observed for the attack of H. cameroni indicates that the ability to adjust the approach could be specific to the behavioral habits of L. volupis.

 

References

  1. Blamires, S.J., Hou, C., Chen, L.F., Liao, C.P. & Tso, I.M. (2013) Three-dimensional barricading of predatory trap reduces predation and enhances prey capture. Behavioral Ecology and Sociobiology, 67 (5), 709­­–714. https://doi.org/10.1007/s00265-013-1493-x
    Cameron, P. (1911) On the Hymenoptera of the Georgetown Museum, British Guiana. Part I. Timehri, 1, 152–186.
    Choi, J.K., Kolarov, J. & Lee, J.W. (2019) Description of two new species of Brachyzapus Gauld & Dubois (Hymenoptera: Ichneumonidae: Pimplinae) from South Korea with key to a Paleartic species. Zootaxa, 4711 (2), 293–306. https://doi.org/10.11646/zootaxa.4711.2.4
    Eberhard, W.G. (2000) The natural history and behavior of Hymenoepimecis argyraphaga (Hymenoptera: Icheneumonidae) a parasitoid of Plesiometa argyra (Araneae: Tetragnathidae. Journal of Hymenoptera Research, 9 (2), 220–240.
    Eberhard, W.G. (2019) Hunting behavior of the wasp Polysphincta gutfreundi and related polysphinctine wasps (Hymenoptera, Ichneumonidae). Journal of the Kansas Entomological Society, 91 (3), 177‒191. https://doi.org/10.2317/0022-8567-91.3.177
    Eberhard, W.G. & Gonzaga, M.O. (2019) Evidence that Polysphincta-group wasps (Hymenoptera: Ichneumonidae) use ecdysteroids to manipulate the web-construction behaviour of their spider hosts. Biological Journal of the Linnean Society, 127 (2), 429–471. https://doi.org/10.1093/biolinnean/blz044
    Elizalde, L. & Folgarait, P.J. (2012) Behavioral strategies of phorid parasitoids and responses of their hosts, the leaf-cutting ants. Journal of Insect Science, 12 (1), Article ID 135. https://doi.org/10.1673/031.012.13501
    Gauld, I.D. (1991) The Ichneumonidae of Costa Rica I. Memoirs of the American Entomological Institute, 47, 1–589.
    Gauld, I.D. (2000) The Re-definition of Pimplinae Genus Hymenoepimecis (Hymenoptera: Ichneumonidae) with a Description of a Plesiomorphic New Costa Rican Species. Journal of Hymenoptera Research, 9 (2), 213–219.
    Gauld, I.D. & Dubois, J. (2006) Phylogeny of the Polysphincta group of genera (Hymenoptera: Ichneumonidae; Pimplinae): a taxonomic revision of spider ectoparasitoids. Systematic Entomology, 31 (3), 529–564. https://doi.org/10.1111/j.1365-3113.2006.00334.x
    Gilhuis, J.P. (1986) [Vegetation survey of the Parque Florestal Estadual do Rio Doce, MG, Brazil]. Universidade Federal de Viçosa, Viçosa, 86p.
    Gonzaga, M.O., Moura, R.R., Pêgo, P.T., Bang, D.L. & Meira, F.A. (2015) Changes to web architecture of Leucauge volupis (Araneae: Tetragnathidae) induced by the parasitoid Hymenoepimecis jordanensis (Hymenoptera: Ichneumonidae). Behaviour, 152 (2), 181–193. https://doi.org/10.1163/1568539X-00003238
    Gonzaga, M.O. & Sobczak, J.F. (2007) Parasitoid-induced mortality of Araneus omnicolor (Araneae, Araneidae) by Hymenoepimecis sp. (Hymenoptera, Ichneumonidae) in southeastern Brazil. Naturwissenschaften, 94 (3), 223–227. https://doi.org/10.1007/s00114-006-0177-z
    Harvey, J.A., Kadash, K. & Strand, M.R. (2000) Differences in larval feeding behavior correlate with altered developmental strategies in two parasitic wasps: implications for the size-fitness hypothesis. Oikos, 88 (3), 621–629. https://doi.org/10.1034/j.1600-0706.2000.880319.x
    Higa, P.T. & Penteado-Dias, A.M. (2020) Altitudinal effects on diversity of Pimplinae (Hymenoptera, Ichneumonidae) from Southeast Brazil and description of new species. Brazilian Journal of Biology, 80 (2), 377–385. https://doi.org/10.1590/1519-6984.210438
    Higgins, L. (1992) Developmental changes in barrier web structure under different levels of predation risk in Nephila clavipes (Araneae: Tetragnathidae). Journal of Insect Behavior, 5 (5), 635–655. https://doi.org/10.1007/BF01048010
    IEF [Instituto Estadual de Florestas] (2002) Plano de Manejo do Parque Estadual do Rio Doce. Instituto Estadual de Florestas de Minas Gerais e Projeto Doces Matas, Belo Horizonte.
    Available from: http://www.ief.mg.gov.br/component/content/article/306 (accessed 15 October 2021)
    Klopfstein, S., Santos, B.F., Shaw, M.R., Alvarado, M., Bennett, A. M. R., Dal Pos, D., Giannotta, M., Florez, A.F.H., Karlsson, D., Khalaim, A. I., Lima, A.R., Mikó, I., Sääksjärvi, I.E., Shimizu, S., Spasojevic, T., van Noort, S., Vilhelmsen, L. & Broad G.R. (2019) Darwin wasps: a new name heralds renewed efforts to unravel the evolutionary history of Ichneumonidae. Entomological Communications, 1, Article ID ec01006. https://doi.org/10.37486/2675-1305.ec01006
    Kloss, T.G., Gonzaga, M.O., Roxinol, J.A.M. & Sperber, C.F. (2016) Attack behavior of two wasp species of the Polysphincta genus group (Hymenoptera, Ichneumonidae) on their orb-weaver spider hosts (Araneae, Araneidae). Journal of Insect Behavior, 29 (3), 315–324. https://doi.org/10.1007/s10905-016-9560-6
    Kloss, T.G., Pádua, D.G., Lacerda, F.G., Oliveira, L.S., Cossolin, J.F.S., Serrão, J.E. & Gonzaga, M.O. (2018) Suppression of orb-web building behavior of the spider Metazygia laticeps (O. Pickard-Cambridge, 1889) (Araneae: Araneidae) by a new parasitoid wasp. Zoologischer Anzeiger, 276, 100–106. https://doi.org/10.1016/j.jcz.2018.06.005
    Kumagai, A.F. & Graf, V. (2002) Biodiversidade de Ichneumonidae (Hymenoptera) e monitoramento das espécies de Pimplinae e Poemeniinae do Capão da Imbuia, Curitiba, Paraná. Revista Brasileira de Zoologia, 19 (2), 445–452. https://doi.org/10.1590/S0101-81752002000200010
    Kuris, A.M. & Lafferty, K.D. (2000) Parasite-host modeling meets reality: Adaptive peaks and their ecological attributes. In: Poulin, R., Morand, S. & Skorping, A. (Eds.), Evolutionary Biology of Host-Parasite Relationships: Teory Meets Reality: Developments in Animal and Veterinary Sciences. Vol. 32. Elsevier Science, Amsterdam, pp. 9–26.
    Loffredo, A.P.S. & Penteado-Dias, A.M. (2009) New species of Hymenoepimecis Viereck (Hymenoptera, Ichneumonidae, Pimplinae) from Brazilian Atlantic forest. Revista Brasileira de Entomologia, 53 (1), 11–14. https://doi.org/10.1590/S0085-56262009000100004
    Matsumoto, R. (2009) “Veils” against predators: modified web structure of a host spider induced by an Ichneumonid parasitoid, Brachyzapus nikkoensis (Uchida) (Hymenoptera). Journal of Insect Behavior, 22 (1), 39‒48. https://doi.org/10.1007/s10905-008-9152-1
    Matsumoto, R. (2016) Molecular phylogy and systematics of the Polysphincta group of genera (Hymenoptera, Ichneumonidae, Pimplinae). Systematic Entomology, 41 (4), 854‒864. https://doi.org/10.1111/syen.12196
    Nimer, E. (1989) Climatologia do Brasil. IBGE, Rio de Janeiro, 421 pp.
    Pádua, D.G. & Kloss, T.G. (2020) A new species of Acrotaphus Townes (Hymenoptera: Ichneumonidae: Pimplinae) from the Brazilian Amazon, with notes on its host spider behavioral modification. Zootaxa, 4810 (1), 161–168. https://doi.org/10.11646/zootaxa.4810.1.10
    Pádua, D.G., Oliveira, M.L., Onody, H.C., Sobczak, J.F., Sääksjärvi, I.E. & Gómez, I.C. (2015) The Brazilian Amazonian species of Hymenoepimecis Viereck, 1912 (Hymenoptera: Ichneumonidae: Pimplinae). Zootaxa, 4058 (2), 175–194. https://doi.org/10.11646/zootaxa.4058.2.2
    Pádua, D.G., Sääksjärvi, I.E., Monteiro, R.F. & Oliveira, M.L. (2020a) Seven new species of spider-attacking Hymenoepimecis Viereck (Hymenoptera, Ichneumonidae, Pimplinae) from Ecuador, French Guiana, and Peru, with an identification key to the world species. ZooKeys, 935, 57‒92. https://doi.org/10.3897/zookeys.935.50492
    Pádua, D.G., Sääksjärvi, I.E., Monteiro, R.F. & Oliveira, M.L. (2020b) Review of the New World genus Acrotaphus Townes, 1960 (Hymenoptera: Ichneumonidae: Pimplinae) with descriptions of fifteen new species. Zootaxa, 4719 (1), 1‒62. https://doi.org/10.11646/zootaxa.4719.1.1
    Pádua, D.G., Sääksjärvi, I.E., Spasojevic, T., Kaunisto, K.M., Monteiro, R.F. & Oliveira, M.L. (2021) A review of the spider-attacking Polysphincta dizardi species-group (Hymenoptera, Ichneumonidae, Pimplinae), with descriptions of seven new species from South America. ZooKeys, 1041, 137–165. https://doi.org/10.3897/zookeys.1041.65407
    Snodgrass, R.E. (1941) The male genitalia of Hymenoptera. Smithsonian Miscellaneous collections, 99, 1–86.
    Sobczak, J.F. (2013) Biological and ecological studies of the interaction between Nephila clavipes (Araneae, Nephilidae) and the parasitoid Hymenoepimecis bicolor (Hymenoptera, Ichneumonidae, Pimplinae). Universidade de São Carlos, São Carlos, 110 pp. [in Portuguese]
    Sobczak, J.F., Loffredo, A.P.S., Penteado-Dias, A.M. & Gonzaga, M.O. (2009) Two new species of Hymenoepimecis (Hymenoptera: Ichneumonidae: Pimplinae) with notes on their spider hosts and behaviour manipulation. Journal of Natural History, 43 (43–44), 2691–2699. https://doi.org/10.1080/00222930903244010
    Sobczak, J.F., Pádua, D.G., Costa, L.F.A., Carvalho, J.L.V.R., Sobczak, J.C.M.S.M. & Messas, Y.F. (2018) The parasitoid wasp Eruga unaliabiana Pádua & Sobczack, sp. nov. (Hymenoptera: Ichneumonidae) induces behavioral modification in its spider host. Entomological Science, 21 (1), 59‒65. https://doi.org/10.1111/ens.12278
    Sobczak, J.F., Pádua, D.G., Villanueva-Bonilla, G.A., Nóbrega, F.A.S. & Messas, Y.F. (2019) Two new species of Zatypota (Hymenoptera: Ichneumonidae, Pimplinae) sharing the same host spider in Northeast Brazil. Zootaxa, 4609 (1), 169‒177. https://doi.org/10.11646/zootaxa.4609.1.9
    Takasuka, K., Fritzén, N.R., Tanaka, Y., Matsumoto, R., Maeto, K. & Shaw, M.R. (2018) The changing use of the ovipositor in host shifts by ichneumonid ectoparasitoids of spiders (Hymenoptera, Ichneumonidae, Pimplinae). Parasite, 25, Article ID 17. https://doi.org/10.1051/parasite/2018011
    Takasuka, K. & Matsumoto, R. (2011a) Lying on the dorsum: unique host-attacking behaviour of Zatypota albicoxa (Hymenoptera, Ichneumonidae). Journal of Ethology 29 (2), 203–207. https://doi.org/10.1007/s10164-010-0263-8
    Takasuka, K. & Matsumoto, R. (2011b) Infanticide by a solitary koinobiont ichneumonid ectoparasitoid of spiders. Naturwissenschaften, 98 (6), 529–536. https://doi.org/10.1007/s00114-011-0797-9
    Takasuka, K., Matsumoto, R. & Maeto, K. (2019) Oviposition behaviour by a spider-ectoparasitoid, Zatypota maculata, exploits the specialized prey capture technique of its spider host. Journal of Zoology, 308 (3), 221–230. https://doi.org/10.1111/jzo.12668
    Takasuka, K., Matsumoto, R. & Ohbayashi, N. (2009) Oviposition behavior of Zatypota albicoxa (Hymenoptera, Ichneumonidae), an ectoparasitoid of Achaearanea tepidariorum (Araneae, Theridiidae). Entomological Science, 12 (3), 232–237. https://doi.org/10.1111/j.1479-8298.2009.00338.x
    Triana-Cambronero, E., Barrantes, G., Cuyckens, E. & Camacho, A. (2011) Function of the upper tangle in webs of young Leucauge argyra (Araneae: Tetragnathidae). Journal of Arachnology, 39 (3), 519–522. https://doi.org/10.1636/Hi11-36.1
    Varga, O. & Reshchikov, A. (2018) Schizopyga alinae, a genus of pimplinae parasitoid wasps (Hymenoptera: Ichneumonidae: Pimplinae) new to the Afrotropical region. Zootaxa, 4422 (2), 291‒295. https://doi.org/10.11646/zootaxa.4422.2.9
    Varga, O., Reshchikov, A. & Di Giovanni, F. (2018) First record of the genus Brachyzapus Gauld & Dubois, 2006 (Hymenoptera: Ichneumonidae: Pimplinae) from the Afrotropical region, with descriptions of two new species. Zootaxa, 4377 (4), 581‒586. https://doi.org/10.11646/zootaxa.4377.4.8
    Weng, J.L. & Barrantes, G. (2007) Natural history and larval behavior of the Zatypota petronae (Hymenoptera: Ichneumonidae). Journal of Hymenoptera Research, 16 (2), 326‒335.
    Yu, D.S.K. (2019) Taxapad Ichneumonoidea. In: Roskov, Y., Ower, G., Orrell, T., Nicolson, D., Bailly, N., Kirk, P.M., Bourgoin, T., DeWalt, R.E., Decock, W., Nieukerken, E., Zarucchi, J. & Penev, L. (Eds.), Species 2000 & ITIS Catalogue of Life. Available from: http://www.catalogueoflife.org/col (accessed 1 November 2021)

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