Abstract
The natural history and morphology of the immature stages of the butterfly Thereus lomalarga Robbins, Heredia & Busby are described and illustrated. The food plant is Oryctanthus alveolatus (H.B.K.) Kuijt (Loranthaceae). Chaetotaxy of the first instar is described and compared with that of three locally studied Thereus species. Larvae have four instars, and the dorsal nectary organ becomes functional in the third instar. They are facultatively tended by ants belonging to seven genera that are attracted to O. alveolatus by floral disc nectaries, honeydew producing Hemiptera, and secretory wounds produced by Hemiptera on the fleshy inflorescence rachis. The average period from egg to eclosion under lab conditions was 35.68 days. Females emerged before males. Adults of both sexes feed on nectar from the flowers of the food plant and on hemipteran secretions; adults were not observed feeding on other flowers. Campopleginae and Chalcidinae were the most important parasitoids.
References
Ackery, P.R. (1991) Hostplant utilization by African and Australian butterflies. Biological Journal of the Linnean Society, 44 (4), 335–351.
http://dx.doi.org/10.1111/j.1095-8312.1991.tb00624.xAtsatt, P.R. (1981a) Ant-dependent food plant selection by the mistletoe butterfly Ogyris amaryllis (Lycaenidae). Oecologia, 48 (1), 60–63.
http://dx.doi.org/10.1007/BF00346988Atsatt, P.R. (1981b) Lycaenidae butterflies and ants: selection for enemy-free space. American Naturalist, 118, 638–654.
http://dx.doi.org/10.1086/283859Ballmer, G.R. & Pratt, G.F. (1988) A survey of the last instar larvae of the Lycaenidae (Lepidoptera) of California. Journal of Research on the Lepidoptera,27 (1), 1–80
Ballmer, G.R. & Pratt, G.F. (1992) Loranthomitoura, a new genus of Eumaeini (Lepidoptera: Lycaenidae: Theclinae). Tropical Lepidoptera, 3 (1), 37–46.
Ballmer, G.R. (2008) Life history of Purlisa gigantea in South Thailand. Tropical Lepidoptera, 18 (1), 32–39.
Ballmer, G.R. & Wright, D.M. (2008) Life history and larval chaetotaxy of Ahmetia achaja (Lepidoptera, Lycaenidae, Lycaeninae, Theclini, Cheritrina). Zootaxa, 1845, 47–59.
Beccaloni, G.W, Hall, S.K, Viloria, A.L. & Robinson, G.S. (2008) Catalogue of the hostplants of the Neotropical butterflies / Catálogo de las plantas huésped de las mariposas Neotropicales. In: m3m—Monografias Tercer Milenio. Vol. 8. Zaragoza (Spain): S.E.A., RIBES-CYTED, The Natural History Museum, Instituto Venezolano de Investigaciones Científicas.
Caires, C.S. (2012) Estudos taxonômicos aprofundados de Oryctanthus (Griseb.) Eichler, Oryctina Tiegh. e Pusillanthus Kuijt (Loranthaceae). Available from: http://repositorio.unb.br/bitstream/10482/11106/1/2012 Claudenir Simoes Caires.pdf (accessed July 2014)
Congdon, C. & Bampton, I. (2000) Provisional notes on the foodplants of the Iolaini (Lepidoptera, Papilionoidea, Lycaenidae). Metamorphosis, 11 (1), 33–42.
Chen, C., Xia, Q.W., Xiao, H.J., Xiao, L. & Xue, F.S. (2014) A comparison of the life-history traits between diapause and direct development individuals in the cotton bollworm, Helicoverpa armigera. Journal of insect science, 14 (1), 19.
http://dx.doi.org/10.1093/jis/14.1.19D’Araujo e Silva, A.G., Gonçalves, C.R., Galvão, D.M., Gonçalves, A.J.L., Gomes, J., Silva, M.N. & Simoni, L. (1967–1968) Quarto catálogo dos insetos que vivem nas plantas do Brasil. Seus parasitas e predadores. Ministério da Agricultura, Rio de Janeiro, Part I, Vol.1, 422 pp., Vol.2, 906 pp., Part II, Vol.2, 265 pp.
Downey, J.C. & Allyn, A.C. (1981) Chorionic sculpturing in eggs of Lycaenidae. Part I. Bulletin of the Allyn Museum, 61, 1–29.
Downey, J.C. & Allyn, A.C. (1984) Chorionic sculpturing in eggs of Lycaenidae. Part II. Bulletin of the Allyn Museum, 84, 1–44.
Duarte, M., Robbins, R.K. & Mielke, O.H. (2005) Immature stages of Calycopis caulonia (Hewitson, 1887) (Lepidoptera, Lycaenidae, Theclinae, Eumaeini), with notes on rearing detritivorous hairstreaks on artificial diet. Zootaxa 1063, 1–31.
Duarte, M. & Robbins, R.K. (2009) Immature stages of Calycopis bellera (Hewitson) and C. janeirica (Felder)(Lepidoptera, Lycaenidae, Theclinae, Eumaeini): taxonomic significance and new evidence for detritivory. Zootaxa, 2325, 39–61.
Dueñas Gomez, H.D.C. & Franco Roselli, P. (2001) Sinopsis de las Loranthaceae de Colombia. Caldasia, 23 (1), 81–99.
Espinal, L.S. (1968) Visión Ecológica del Departamento del Valle del Cauca. Universidad del Valle, Cali.
Fiedler, K. & Maschwitz, U. (1989) Adult myrmecophily in butterflies: the role of the ant Anoplolepis longipes in the feeding and oviposition behaviour of Allotinus unicolor (Lepidoptera, Lycaenidae). Tyô to Ga, 40 (4), 241–251.
Fiedler, K. (1991) Systematic, evolutionary, and ecological implications of myrmecophily within Lycaenidae (Insecta: Lepidoptera: Papilionoidea). Bonner Zoologische Monographien, 31, 1–210.
Fiedler, K. (1993) The remarkable biology of two Malaysian lycaenid butterflies.Nature Malaysiana, 18 (2), 35–42.
Fiedler, K. (1995) Lycaenid butterflies and plants: is myrmecophily associated with particular hostplant preferences? Ethology ecology & evolution, 7 (2), 107–132.
http://dx.doi.org/10.1080/08927014.1995.9522960Fraser, A.M., Axén, A.H. & Pierce, N.E. (2001) Assessing the quality of different ant species as partners of a myrmecophilous butterfly. Oecologia,129 (3), 452–460.
http://dx.doi.org/10.1007/s004420100744Haskin, J.R. (1933) Thecla halesus, its life cycle and habits. Entomological News 44, 72–74.
Janzen, D.H. & Hallwachs, W. (2015) Dynamic database for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of the Area de Conservacion Guanacaste (ACG), northwestern Costa Rica [Internet]. Philadelphia: University of Pennsylvania. Available from: http://janzen.sas.upenn.edu (accessed september 2015)
Kaminski, L.A. & Freitas, A.V. (2010) Natural history and morphology of immature stages of the butterfly Allosmaitia strophius (Godart) (Lepidoptera: Lycaenidae) on flower buds of Malpighiaceae. Studies on neotropical Fauna and Environment, 45 (1), 11–19.
http://dx.doi.org/10.1080/01650520903495826Kaminski, L.A., Freitas, A.V. & Oliveira, P.S. (2010) Interaction between mutualisms: ant-tended butterflies exploit enemy-free space provided by ant-treehopper associations. The American Naturalist, 176 (3), 322–334.
http://dx.doi.org/10.1086/655427Kaminski, L.A. & Rodrigues, D. (2011) Species-specific levels of ant attendance mediate performance costs in a facultative myrmecophilous butterfly. Physiological Entomology, 36 (3), 208–214.
http://dx.doi.org/10.1111/j.1365-3032.2011.00785.xKaminski, L.A., Rodrigues, D. & Freitas, A.V. (2012) Immature stages of Parrhasius polibetes (Lepidoptera: Lycaenidae): host plants, tending ants, natural enemies and morphology. Journal of Natural History, 46 (11–12), 645–667.
http://dx.doi.org/10.1080/00222933.2011.651630Kattan, G. & Álvarez-López, H. (1996) Preservation and management of biodiversity in fragmented landscapes in the Colombian Andes.pp 3–18 In Schelhas, J. & Greenberg R. (Eds.) Forest Patches in Tropical Landscapes. Island Press, Washington D. C.
Kitching, I.J. (1985) Early stages and the classification of the milkweed butterflies (Lepidoptera, Danainae). Zoological Journal of the Linnean Society,85 (1), 1–97.
http://dx.doi.org/10.1111/j.1096-3642.1985.tb01516.xLohman, D.J. & Samarita, V.U. (2009) The biology of carnivorous butterfly larvae (Lepidoptera: Lycaenidae: Miletinae: Miletini) and their ant-tended hemipteran prey in Thailand and the Philippines. Journal of Natural History, 43 (9–10), 569–581.
http://dx.doi.org/10.1080/00222930802610485Malicky, H. (1970) New aspects of the association between lycaenid larvae (Lycaenidae) and ants (Formicidae, Hymenoptera). Journal of the Lepidopterists’ Society, 24 (3), 190–202.
Maschwitz, U., Dumpert, K. & Sebastian, P. (1985) Morphological and behavioural adaptations of homopterophagous blues (Lepidoptera: Lycaenidae). Entomologia generalis, 85–90.
Maschwitz, U., Nässig, W.A., Dumpert, K. & Fiedler, K. (1988). Larval carnivory and myrmecoxeny, and imaginal myrmecophily in miletine lycaenids (Lepidoptera, Lycaenidae) on the Malay Peninsula. Tyô to Ga, 39 (3), 167–181.
Monteiro, R.F. (1990) Cryptic larval polychromatism in Rekoa marius Lucas and R. palegon Cramer (Lycaenidae: Theclinae). Journal of Research on the Lepidoptera, 29 (1–2), 77–84.
Morbey, Y.E. (2013) Protandry, sexual size dimorphism, and adaptive growth. Journal of theoretical biology, 339, 93–99.
http://dx.doi.org/10.1016/j.jtbi.2013.05.009Newcomer, E.J. (1912) Some observations on the relations of ants and lycaenid caterpillars, and a description of the relational organs of the latter. Journal of the New York Entomological Society, 31–36.
Nickrent, D.L., Malécot, V., Vidal-Russell, R. & Der, J.P. (2010) A revised classification of Santalales. Taxon, 59 (2), 538–558.
Pierce, N.E. & Mead, P.S. (1981) Parasitoids as selective agents in the symbiosis between lycaenid butterfly larvae and ants. Science, 211, 1185–1187.
http://dx.doi.org/10.1126/science.211.4487.1185Pierce, N.E. & Nash, D.R. (1999) The imperial blue, Jalmenus evagoras (Lycaenidae). Monographs on Australian Lepidoptera, 6, 279-315.
Pierce, N.E., Braby, M.F., Heath, A., Lohman, D.J., Mathew, J., Rand, D.B. & Travassos, M.A. (2002) The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annual Review of Entomology, 47 (1), 733–771.
http://dx.doi.org/10.1146/annurev.ento.47.091201.145257Prieto, C. & Dahners, H.W. (2009) Resource utilization and environmental and spatio-temporal overlap of a hilltopping Lycaenid butterfly community in the Colombian Andes. Journal of Insect Science, 9 (1), 16.
http://dx.doi.org/10.1673/031.009.1601Quental, T.B. (2008) Systematics, sexual selection and evolution of secondary sexual charac-ters in Neotropical Eumaeini butterflies (Lepidoptera: Lycaenidae). Dissertation, Harvard University, Cambridge, MA, 226 pp.
Robbins, R.K. & Aiello, A. (1982) Foodplant and oviposition records for Panamanian Lycaenidae and Riodinidae. Journal of the Lepidopterists Society, 36(2), 65–75.
Robbins, R.K. (1991) Evolution, comparative morphology, and identification of the eumaeine butterfly genus Rekoa Kaye (Lycaenidae: Theclinae). Smithsonian Contribution to Zoology, 498, 1–64.
http://dx.doi.org/10.5479/si.00810282.498Robbins, R.K. (2004) Lycaenidae. Theclinae. Eumaeini. In: Lamas G, editor. Checklist: Part 4A. Hesperioidea—Papilionoidea. In Heppner JB, editor. Atlas of Neotropical Lepidoptera. Volume 5A. Gainesville (IL): Association for Tropical Lepidoptera, Scientific Publishers. pp. 118–137.
Robbins, R.K., Busby, R. & Duarte, M. (2010) Phylogeny and Taxonomy of the Neotropical Thepytus (Lepidoptera: Lycaenidae: Theclinae). Arthropod Systematics & Phylogeny, 68 (1), 35–52.
Robbins, R., Heredia, M.D. & Busby, R.C. (2015) Male secondary sexual structures and the systematics of the Thereus oppia species group (Lepidoptera, Lycaenidae, Eumaeini). ZooKeys, 520, 109–130.
http://dx.doi.org/10.3897/zookeys.520.10134Schmid, S., Schmid, V.S., Kamke, R., Steiner, J. & Zillikens, A. (2010) Association of three species of Strymon Hübner (Lycaenidae: Theclinae: Eumaeini) with bromeliads in southern Brazil. Journal of Research on the Lepidoptera, 42, 50–84.
Sepp, J. (1829–1843) Natuurlijke Historie van Surinaamsche Vlinders, naar het leven geteekend. Papillons de Surinam dessinés d'après nature. Amsterdam, Jan Christian Sepp en Zoon. 108 pages, 50 plates.
Singer, M.S., Lichter-Marck, I.H., Farkas, T.E., Aaron, E., Whitney, K.D. & Mooney, K.A. (2014). Herbivore diet breadth mediates the cascading effects of carnivores in food webs. Proceedings of the National Academy of Sciences, 111 (26), 9521–9526.
http://dx.doi.org/10.1073/pnas.1401949111Stehr, F.W. (1987) Order Lepidoptera. In: Stehr FW, editor. Immature insects.Vol. 1. Dubuque (IA): Kendall-Hunt Publishing Company. pp. 288–305.
Uchôa, M.A. & Caires, C.S. (2000) Candidate insects for the biocontrol of the plant phytoparasite Psittacanthus sp.(Loranthaceae) in the region of the Pantanal, Mato Grosso do Sul State, Brazil. In XXI Int. Congress Entomol. Foz do Iguassu, Brazil, Abstract, Vol. 1683.
Uchôa, M.A., Caires, C.S., Nicácio, J.N. & Duarte, M. (2012) Frugivory of Neosilba species (Diptera: Lonchaeidae) and Thepytus echelta (Lepidoptera: Lycaenidae) on Psittacanthus (Santalales: Loranthaceae) in ecotonal cerrado-South Pantanal, Brazil. Florida Entomologist, 95 (3), 630–640.
http://dx.doi.org/10.1653/024.095.0314Vegliante, F. & Hasenfuss, I. (2012) Morphology and diversity of exocrine glands in lepidopteran larvae. Annual review of Entomology, 57, 187–204.
http://dx.doi.org/10.1146/annurev-ento-120710-100646Wagner, D.L. & Gagliardi, B.L. (2015) Hairstreaks (and Other Insects) Feeding at Galls, Honeydew, Extrafloral Nectaries, Sugar Bait, Cars, and Other Routine Substrates. American Entomologist, 61 (3), 160–167.
http://dx.doi.org/10.1093/ae/tmv045Watson, D.M. (2001) Mistletoe-a keystone resource in forests and woodlands worldwide. Annual Review of Ecology and Systematics, 219–249.
http://dx.doi.org/10.1146/annurev.ecolsys.32.081501.114024Watson, D.M. & Herring, M. (2012) Mistletoe as a keystone resource: an experimental test. Proceedings of the Royal Society B-Biological Sciences, 279, 3853–3860.
http://dx.doi.org/10.1098/rspb.2012.0856Whittaker, P.L. (1984a) Population biology of the great purple hairstreak, Atlides halesus, in Texas (Lycaenidae). Journal of the Lepidopterists' Society, 38 (3), 179–185.
Whittaker, P.L.(1984b) The insect fauna of mistletoe (Phoradendron tomentosum, Loranthaceae) in southern Texas. The Southwestern Naturalist, 435–444.
http://dx.doi.org/10.2307/3670996Wiklund, C. & Fagerström, T. (1977) Why do males emerge before females? Oecologia, 31 (2), 153–158.
http://dx.doi.org/10.1007/BF00346917Wolkmann, L. & Núñez Bustos, E. (2014) Observaciones sobre la biología de Thereus pseudarcula (Giacomelli 1914) (Lepidoptera: Lycaenidae: Theclinae). Historia Natural, Vol. 4 (2), 113–121.
Youngsteadt, E. & Devries, P.J. (2005) The effects of ants on the entomophagous butterfly caterpillar Feniseca tarquinius, and the putative role of chemical camouflage in the Feniseca–Ant Interaction. Journal of chemical ecology, 31 (9), 2091–2109.
http://dx.doi.org/10.1007/s10886-005-6079-2Zikán, J.F. (1956) Beitrag zur biologie von 12 Theclinen-arten. Dusenia, 7 (3), 139–148.