Breakdown of scavina resistance in Bahia caused by the evolution of Moniliophthora perniciosa

Resistant clones to witches' broom disease of cacao (WBD), caused by the basidiomycete fungus Moniliophthora perniciosa (Mp) is the most practical and cost efficient strategy for WBD management, but their use is currently restricted to very limited clones, mostly, Scavina's descendants. Scavina resistance has proved inadequate or unstable, as, for example, in Rondônia in the Amazon basin, in Ecuador during the 1980s, and in Bahia in 2002. In this paper, we present evidences, through several independent studies, that the Scavinas' resistance have been overcome because of changes in the pathogen population. Using molecular markers in studies of 40 isolates of the fungus, collected from brooms from five resistant and two susceptible cocoa genotypes, a clear genetic differentiation was observed between fungal isolates from primarily resistant clones and from susceptible ones. Further, a study carried out to characterize temporal genetic variability of Mp populations in Bahia, Brazil, over four consecutive years (2001 to 2004), in several locations, have shown that there was a shift in the genetic composition of the Mp populations. Pathogenic variability through cross inoculation experiments using -isolates derived from Scavinas (Scavina 6 and descendants), non scavina, and from SIC, a susceptible clone, showed that Scavina isolates caused more disease on the Scavinas genotypes, whereas the isolate derived from SIC was less pathogenic on the Scavinas and more pathogenic on its respective host. These results allowed us to conclude that the increase in susceptibility in Scavina descendants was the result of the buildup of resistance-breaking pathogen's strains capable of overcoming the resistance of Scavina. Also, temporal observations of natural infections between 2003 and 2010 in a F2 Scavina 6 x ICS1 showed that the major QTL identified in the LG9 had its effect decreased year by year; moving from a LOD of 9 in 2003 to a non significant LOD in 2010. The same results were found under artificial inoculations with specific strains of Mp and using a new F2 population created in 2007. The present study provides the first evidences that Scavinas WB resistance breakdown is due to the adaptation of the Mp field populations. These studies, besides proving the change in the Mp population in Bahia, they are also a warning call that the efficiency of resistant cultivars in WBD management is limited by Mp variability and an incentive to design breeding programs for durable resistance. Different sources of resistance have been identified and are being used in the cacao breeding program to associate distinct genes of resistance. (Résumé d'auteur

External Morphology Of The Immature Stages Of Neotropical Heliconines: Vi. Dione Moneta Moneta Hübner (lepidoptera, Nymphalidae, Heliconiini) [morfologia Externa Dos Estágios Imaturos De Heliconíneos Neotropicais: Vi. Dione Moneta Moneta Hübner (lepidoptera, Nymphalidae, Heliconiinae)]

The external features of the egg, larva and pupa of Dione moneta moneta Hübner, 1825 are described and illustrated, based upon light and scanning electron microscopy.5211323Antunes, F.A., Menezes Jr., A.O., Tavares, M., Moreira, G.R.P., Morfologia externa dos estágios imaturos de heliconíneos neotropicais: I. Eueides isabella dianasa (Hübner, 1816). (2002) Revista Brasileira de Entomologia, 46, pp. 601-610Araújo, A.M., Valente, V.L.S., Observaçõ es sobre alguns lepidópteros e drosofilídeos do Parque Estadual do Turvo. (1981) Ciência e Cultura, 33, pp. 1485-1490Beebe, W., Crane, J., Fleming, H., A comparison of eggs, larvae and pupae in fourteen species of heliconiine butterflies from Trinidad, W. I (1960) Zoologica, 45, pp. 111-154Benson, W.W., Brown Jr., K.S., Gilbert, L.E., Coevolution of plants and herbivores: Passion vine butterflies (1975) Evolution, 32, pp. 659-680Biezanko, C.M., Acraeidae, Heliconiidae et Nymphalidae de Pelotas e seus arredores (contribuição ao conhecimento da fisiografia do Rio Grande do Sul) (1949) Pelotas, Livraria do Globo, , 16pBiezanko, C.M., Ruffinelli, A., Link, D., Catálogo de lepidópteros do Uruguai. (1978) Revista do Centro de Ciências Rurais, 8, pp. 1-84Brown, F.M., The egg, larva and chrysalis of Dione moneta Huebner (1944) Bulletin of the Brooklyn Entomological Society, 39, pp. 132-134Brown Jr., K.S., The biology of Heliconius and related genera (1981) Annual Review of Entomology, 26, pp. 427-456Brown, K. S. Jr. 1992. Borboletas da Serra do Japi: diversidade, hábitats, recursos alimentares e variação temporal, p. 142-187. In: L. P. C. Morellato (ed.). História Natural da Serra do Japí: Ecologia e preservação de uma área florestal no sudeste do Brasil. Campinas, UNICAMP/FAPESP, 322 pBrown Jr., K.S., Mielke, O.H.H., The heliconians of Brazil (Lepidoptera: Nymphalidae). Part II. Introduction and general comments, with a supplementary revision of the tribe (1972) Zoologica, 57, pp. 1-40D'Abrera, B. 1984. Butterflies of the Neotropical region. Part II. Danaidae, Ithomiidae, Heliconidae & Morphidae. Victoria, Hill House, vii + 173-384 pDell'Erba, R., Kaminski, L.A., Moreira, G.R.P., O estágio de ovo dos Heliconiini (Lepidoptera: Nymphalidae) do Rio Grande do Sul, Brasil. (2005) Iheringia, Série Zoologia, 95, pp. 29-46DeVries, P.J., The butterflies of Costa Rica and their natural history (1987) Papilionidae, Pieridae, Nymphalidae, , Princeton, Princeton University, 327 pDuarte, M.R. K. Robbins & O. H. H. Mielke. 2005. Immature stages of Calycopis caulonia (Hewitson, 1877) (Lepidoptera, Lycaenidae, Theclinae, Eumaeini), with notes on rearing detritivorous hairstreaks on artificial diet. Zootaxa 1063: 1-31Emsley, M.G., A morphological study of imagine Heliconiinae (Lep.: Nymphalidae) with a consideration of the group (1963) Zoologica, 48, pp. 85-130Fleming, H., The first instar larvae of the Heliconiinae (Butterflies) of Trinidad, W. I (1960) Zoologica, 45, pp. 91-110Freitas, A.V.L., Description of a new genus for "Euptychia" peculiaris (Nymphalidae: Satyrinae): immature stages and systematic position (2003) Journal of the Lepidopterists' Society, 57, pp. 100-106García-Barros, E., Cano, J.M., Morfología de los tubérculos mesotorácicos de las pupas de algunos lepidópteros (Lepidoptera: Nymphalidae, Hesperiidae, Sphingidae). (1994) SHILAP Revista de Lepidopterologia, 22, pp. 249-258Garcias, G.L., (1983) Aspectos da biologia de cinco espécies de heliconíneos do anel mimético laranja, , Dissertação de Mestrado. Porto Alegre, UFRGS, 88 pGilbert, L.E., On the ecology of natural dispersal: Dione moneta poeyii in Texas (Nymphalidae) (1969) Journal of the Lepidopterists' Society, 23, pp. 177-185Gilbert, L.E., Butterfly-plant coevolution: Has Passiflora adenopoda won selectional race with heliconiine butterflies? (1971) Science, 172, pp. 585-586Harvey, D. J. 1991. Higher classification of the Nymphalidae. Appendix B, p. 255-273. In: H. F. Nijhout (ed.). The development and evolution of butterfly wing patterns. Washington, Smithsonian Institution, xvi + 297 pHinton, H.E., On the homology and nomenclature of the setae of lepidopteran larvae, with some notes on the phylogeny of the Lepidoptera (1946) Transactions of the Royal Entomological Society of London, 97, pp. 1-37Kaminski, L.A., Tavares, M., Ferro, V.G., Moreira, G.R.P., Morfologia externa dos estágios imaturos de heliconíneos neotropicais: III (2002) Heliconius erato phyllis, , Fabricius, Lepidoptera: Nymphalidae: Heliconiinae, Revista Brasileira de Zoologia 19: 977-993Kitching, I.J., The use of larval chaetotaxy in butterfly systematics, with special reference to the Danaini (Lepidoptera: Nymphalidae) (1984) Systematic Entomology, 9, pp. 49-61Lamas, G., Checklist: Part 4A. Hesperioidea - Papilionoidea (2004) Atlas of Neotropical Lepidoptera, 5 A. , J. B. Heppner ed, Gainesville, Association for Tropical Lepidoptera, Scientific Publishers, xxxiv, 428 pMcCaffrey, J., Dione moneta poeyii Butler [1873] in New Mexico (Lepidoptera: Nymphalidae) (1984) Journal of Research on the Lepidoptera, 23, pp. 106-107Miller, J.S., Cladistics and classification of the Notodontidae (Lepidoptera: Noctuoidea) based on larval and adult morphology (1991) Bulletin of the American Museum of Natural History, 204, pp. 1-230Mosher, E., A classification of the Lepidoptera based on characters of the pupa (1916) Bulletin of the Illinois State Laboratory of Natural History, 12, pp. 1-165Motta, P. C. 2003. Phylogenetic relationships of Ithomiinae based on first-instar larvae, p. 409-429. In: C. L. BoggsW. B. Watt & P. R. Ehrlich (eds.). Butterflies: ecology and evolution taking flight. Chicago, University of Chicago, 739 pMüller, W., Südamerikanische Nymphalidenraupen. Versuch eines naturlichen Systems der Nymphaliden. (1886) Zoologischen Jahrbüchern, 1, pp. 417-678Murray, D., Immatures stages and biology of Taygetis Hübner (Lepidoptera: Nymphalidae) (2001) Proceedings of the Entomological Society of Washington, 103, pp. 932-945Nakanishi, A., Study on the first instar larvae of the subfamily Nymphalinae (Lepidoptera, Nymphalidae) (1988) Special Bulletin of the Lepidopterological Society of Japan, 6, pp. 83-99Paim, A.C., Kaminski, L.A., Moreira, G.R.P., Morfologia externa dos estágios imaturos de heliconíneos neotropicais. IV. Dryas iulia alcionea (Lepidoptera: Nymphalidae: Heliconiinae). (2004) Iheringia, Série Zoologia, 94, pp. 25-35Paluch, M., Casagrande, M.M., Mielke, O.H.H., Estágios imaturos de Actinote carycina Jordan (Lepidoptera, Nymphalidae, Acraeinae). (2001) Revista Brasileira de Zoologia, 18, pp. 883-896Penz, C.M., Higher level phylogeny for the passion-vine butterflies (Lepidoptera: Heliconiinae) based on early stage and adult morphology (1999) Zoological Journal of the Linnean Society, 127, pp. 277-344Peterson, A., Larvae of insects. An introduction to Neartic species (1962) Part I Lepidoptera and plant infesting Hymenoptera, , Ann Arbor, Edwards Brothers Inc, 315 pSilva, da, D.S., Dell'Erba, R., Kaminski, L.A., Moreira, G.R.P., Morfologia externa dos estágios imaturos de heliconíneos neotropicais: V. Agraulis vanillae maculosa (Lepidoptera, Nymphalidae, Heliconiinae). (2006) Iheringia, Série Zoologia, 96, pp. 219-228Snedecor, G.W., Cochran, W.G., (1980) Statistical methods, , Ames, Iowa State University, 507 pStehr, F. W. 1987. Order Lepidoptera, p. 288-305. In: F. W. Stehr, (ed.). Immature insects. I. Dubuque, Kendall/ Hunt Publishing Company, 975 pTavares, M., Kaminski, L.A., Moreira, G.R.P., Morfologia externa dos estágios imaturos de heliconíneos neotropicais: II (2002) Dione juno juno, , Cramer, Lepidoptera: Nymphalidae: Heliconiinae, Revista Brasileira de Zoologia 19: 961-976Toledo, Z.D.A., Fauna del noroeste argentino. Contribucion al conocimiento de los lepidopteros argentinos. X. Agraulis vanilla maculosa (Stichel) (Lepidoptera, Rhopalocera, Heliconiidae) (1991) Acta Zoologica Lilloana, 40, pp. 21-3

Variation In Nectar And Pollen Availability, Sucrose Preference, And Daily Response In The Use Of Flowers By Heliconius Erato Phyllis

The mechanisms mediating the use of flowers in the butterfly Heliconius erato phyllis (Nymphalidae) are poorly understood. Availability of nectar and pollen, nectar concentration, and abundance of Stachytarpheta cayennensis and Lantana camara (Verbenaceae), two flower species commonly used by H. erato phyllis in the Neotropics, as well as flower use by this butterfly species in the field were examined in southern Brazil. Under insectary conditions, the preference of H. erato phyllis for different sucrose concentrations (0, 10, 20, 40, and 80%) and the ability to associate sucrose concentrations with preferred and non-preferred flower colors were evaluated through choice tests. Lantana camara inflorescences were less abundant, but contained larger amounts of pollen and nectar than S. cayennensis, and H. erato phyllis utilized the flowers of the former species with higher frequency compared to the latter. In the choice tests, butterflies fed more intensely on 20 and 40% sucrose solutions, an interval in which the nectars of L. camara and S. cayennensis are situated, and were able to associate preferred sucrose concentrations with flower color efficiently within the color spectrum of L. camara flowers (i.e., preferred colors), but not within that of S. cayennensis (non-preferred colors). Thus, the greater use of L. camara flowers by H. erato phyllis is related to the plant's superior floral rewards and not flower abundance, and to the cognitive abilities of these butterflies to adjust their feeding to the availability of pollen and nectar. To our knowledge, this is the first report showing sucrose preferences in a butterfly species. © 2010 Springer Science+Business Media, LLC.243200219Altmann, J., Observational study of behavior: sampling methods (1974) Behaviour, 49, pp. 227-267Andersson, S., Dobson, H.E.M., Behavioral foraging responses by the butterfly Heliconius melpomene to Lantana camara floral scent (2003) J Chem Ecol, 29, pp. 2303-2318Antonini, Y., Souza, H.G., Jacobi, C.M., Mury, F.B., Diversidade e comportamento dos insetos visitantes florais de Stachytarpheta glabra Cham. (Verbenaceae), em uma área de campo ferruginoso, Ouro Preto, MG (2005) Neotrop Entomol, 34, pp. 555-564Baker, H.B., Baker, I., A brief historical review of the chemistry of floral nectar (1983) The Biology of Nectarines, pp. 126-152. , B. Bentley and T. Elias (Eds.), New York: Columbia University PressBarp, E.A., (2006) Ecologia Comportamental de Heliconius erato phyllis (LepidopteraNymphalidae) Frente à Variação Espaço-Temporal dos Recursos Florais, , Ph. D. Dissertation, Universidade Federal do Rio Grande do Sul, Porto AlegreBarrows, E.M., Nectar robbing and pollination of Lantana camara (Verbenaceae) (1976) Biotropica, 8, pp. 132-135Bernays, E.A., Chapman, R.F., (1994) Host Plant Selection by Phytophagous Insects, , New York: Chapman and HallBlackiston, D.J., (2007) Learning and memory in larval and adult Lepidoptera, , Ph. D. Dissertation, Georgetown University, Washington, DCBrack, P., Rodrigues, R.S., Sobral, M.G., Leite, S.L.C., Árvores e arbustos na vegetação natural de Porto Alegre (1998) Iheringia, Sér Bot, 51, pp. 139-166Cerveira, J.F., Baldissera, R., Kerpel, S.M., Bianchi, V., Gauer, E.A.B., Horn, G., Beatrici, A., Moreira, G.R.P., Efeito da distribuição espacial sobre a agregação dos adultos em Heliconius erato phyllis (Lepidoptera: Nymphalidae) (2003) Anais Do VI Congresso De Ecologia Do Brasil, pp. 270-272. , Sociedade de Ecologia do Brasil, São Paulo: SEBCorbet, S.A., Nectar sugar content: estimating standing crop and secretion rate in the field (2003) Apidologie, 34, pp. 1-10Corrêa, C.A., Irgang, B.E., Moreira, G.R.P., Estrutura floral das angiospermas usadas por Heliconius erato phyllis (Lepidoptera, Nymphalidae) no Rio Grande do Sul (2001) Iheringia, Sér Zool, 90, pp. 71-84Courtney, S.P., The ecology of pierid butterflies: dynamics and interactions (1986) Adv Ecol Res, 15, pp. 51-131Crane, J., Imaginal behavior of a Trinidad butterfly, Heliconius erato hydara Hewitson, with special reference to the social use of color (1955) Zoologica, 40, pp. 167-196Crepet, W.L., The role of insect pollination in the evolution of the angiosperms (1983) Pollination Biology, pp. 29-50. , L. E. Real (Ed.), Orlando: AcademicDafni, A., (1992) Pollination Ecology: A Practical Approach, , New York: Oxford University PressDelph, F.L., The evolution of floral color change: pollinator attraction versus physiological constraints in Fuchsia excorticata (1989) Evolution, 43, pp. 1252-1262Dias-Filho, M.B., How is fecundity affected by mowing in the tropical weed Stachytarpheta cayennensis (Verbenaceae) (1994) Pesqui Agropecu Bras, 29, pp. 1675-1679Dunlap-Pianka, H., Boggs, C.L., Gilbert, L.E., Ovarian dynamics in Heliconiine butterflies: programmed senescence versus eternal youth (1977) Science, 197, pp. 487-490Eberhard, S., Hrassnigg, N., Crailsheim, K., Krenn, H.W., Evidence of protease in the saliva of the butterfly Heliconius melpomene (L.) (Nymphalidae, Lepidoptera) (2007) J Insect Physiol, 53, pp. 126-131Fægri, K., Pijl, L.V., (1971) The Principles of Pollination Ecology, , Oxford: PergamonFerro, V.G., (1998) Criação de Heliconius erato phyllis (Fabricius) (Lepidoptera, Nymphalidae) em Condições Semi-Naturais, , Senior Thesis, Universidade Federal do Rio Grande do Sul, Porto AlegreFuturo, D.O., (1992) Estudo Comparativo de Duas Populações de Stachytarpheta cayennensis (Rich) Vahl Gervão Roxo, , M. Sc. Thesis, Universidade Federal do Rio de Janeiro, Rio de JaneiroGaletto, L., Bernardello, G., Floral nectarines, nectar production dynamics and chemical composition in six Ipomoea species (Convolvulaceae) in relation to pollinators (2004) Ann Bot, 94, pp. 269-280Gardener, M.C., Gillman, M.P., The taste of nectar-a neglected area of pollination ecology (2002) Oikos, 98, pp. 552-557Ghisalberti, E.L., Lantana camara L. (Verbenaceae) (2000) Fitoterapia, 71, pp. 467-486Gilbert, L.E., Pollen feeding and reproductive biology of Heliconius butterflies (1972) Proc Natl Acad Sci, 69, pp. 1403-1407Gilbert, L.E., Ecological consequences of a coevolved mutualism between butterflies and plants (1975) Coevolution of Animals and Plants, pp. 210-240. , L. E. Gilbert and P. H. Raven (Eds.), Austin: University of Texas PressGori, D.F., Floral change in Lupinus argenteus (Fabaceae): why should plants advertise the location of unrewarding flowers to pollinators? (1989) Evolution, 43, pp. 870-881Goulson, D., Cory, J.S., Flower constancy and learning in foraging preferences of the green-veined white butterfly Pieris napi (1993) Ecol Entomol, 18, pp. 315-320Grant, V., Pollination systems as isolating mechanisms in angiosperms (1949) Evolution, 3, pp. 82-97Grimaldi, D., The co-radiations of pollinating insects and angiosperms in the Cretaceous (1999) Ann Mo Bot Gard, 86, pp. 373-406Herrera, C.M., Floral traits and plant adaptation to insect pollinators: a devil's advocate approach (1996) Floral Biology: Studies on Floral Evolution in Animal Pollinated Plants, pp. 65-87. , D. G. Lloyd and S. C. H. Barrett (Eds.), New York: Chapman and HallHolzinger, H., Holzinger, R., (1994) Heliconius and Related Genera, , Venette: Sciences NaturellesIlse, D., New observations on responses to colours in egg-laying butterflies (1937) Nature, 25, pp. 544-545Kearns, C.A., Inouye, D.W., (1993) Techniques for Pollination Biologists, , Niwot: University Press of ColoradoKelber, A., Colour learning in the hawkmoth Macroglossum stellatarum (1996) J Exp Biol, 199, pp. 1127-1131Kelber, A., Innate preferences for flower features in the hawkmoth Macroglossum stellatarum (1997) J Exp Biol, 200, pp. 827-836Kelber, A., Pattern discrimination in a hawkmoth: innate preferences, learning performance and ecology (2002) Proc R Soc Lond B, 269, pp. 2573-2577Kelber, A., Pfaff, M., Spontaneous and learned preferences for visual flower features in a diurnal hawkmoth (1997) Isr J Plant Sci, 45, pp. 235-245Kerpel, S.M., Moreira, G.R.P., Absence of learning and local specialization on host plant selection by Heliconius erato (2005) J Insect Behav, 18, pp. 433-451Kingsolver, J.D., Daniel, T.L., Mechanics of food handling by fluid-feeding insects (1995) Regulatory Mechanisms in Insect Feeding, pp. 32-73. , R. F. Chapman and G. Boerde (Eds.), New York: Chapman and HallKinoshita, M., Shimada, N., Arikawa, K., Colour vision of the foraging swallowtail butterfly Papilio xuthus (1999) J Exp Biol, 202, pp. 95-102Koptur, S., Extrafloral nectary-mediated interactions between insects and plants (1992) Insect-Plant Interactions, pp. 81-130. , E. A. Bernays (Ed.), Boca Raton: CRCKrenn, H.W., Penz, C.M., Mouthparts of Heliconius butterflies (Lepidoptera: Nymphalidae): a search for anatomical adaptations to pollen-feeding behavior (1998) Int J Insect Morphol Embryol, 27, pp. 301-309Lincoln, R., Boxshall, G., Clark, P., (1998) A Dictionary of Ecology, Evolution and Systematics, , 2nd edn., Cambridge: Cambridge University PressLorenzi, H., (2000) Plantas Daninhas Do Brasil: Terrestres, Aquáticas, Parasitas, Tóxicas E Medicinais, , 3rd edn., Nova Odessa: PlantarumMabberley, D.J., (1997) The Plant-Book, a Portable Dictionary of the Vascular Plants, , London: Cambridge University PressMathur, G., Mohan Ram, H.Y., Floral biology and pollination of Lantana camara (1986) Phytomorphology, 36, pp. 79-100Mesia-Vela, S., Souccar, C., Lima-Landman, M.T.R., Lapa, A.J., Pharmacological study of Stachytarpheta cayennensis Vahl in rodents (2004) Phytomedicine, 11, pp. 616-624Mohan Ram, H.Y., Mathur, G., Flower colour changes in Lantana camara (1984) J Exp Bot, 35, pp. 1656-1662Motulsky, H., (1999) Analysing Data with GraphPad Prism Software, , San Diego: GraphPad SoftwareNicolson, L.M., Fleming, P.A., Nectar as food for birdsthe physiological consequences of drinking dilute sugar solutions (2003) Plant Syst Evol, 238, pp. 139-153Pellmyr, O., Pollination by animals (2002) Plant-Animal Interactions: An Evolutionary Approach, pp. 157-184. , C. M. Herrera and O. Pellmyr (Eds.), Malden: BlackwellPenz, C.M., Krenn, H.W., Behavioral adaptations to pollen-feeding in Heliconius butterflies (Nymphalidae, Heliconiinae): an experiment using Lantana flowers (2000) J Insect Behav, 13, pp. 865-880van der Pijl, L., Ecological aspects of flower evolution. II. Zoophilous flower classes (1961) Evolution, 15, pp. 44-59Raguso, R.A., Floral scent, olfaction, and scent-driven foraging behavior (2001) Cognitive Ecology of Pollination: Animal Behavior and Floral Evolution, pp. 83-105. , L. Chittka and J. D. Thomson (Eds.), New York: Cambridge University PressRaguso, R.A., Flowers as sensory billboards: progress toward an integrated understanding of floral advertisement (2004) Curr Opin Plant Biol, 7, pp. 434-440Ramos, R.R., Freitas, A.V.L., Population biology and wing color variation in Heliconius erato phyllis (Nymphalidae) (1999) J Lepid Soc, 53, pp. 11-21Rodrigues, D., Goodner, B.W., Weiss, M.R., Reversal learning and risk-averse foraging behavior in the monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae) (2010) Ethology, 116, pp. 270-280Romanowsky, H.P., Gus, R., Araújo, A.M., Studies on the genetics and ecology of Heliconius erato (Lepid.Nymph:). III. Population size, preadult mortality, adult resources and polymorphism in natural populations (1985) Rev Bras Biol, 45, pp. 563-569Rusterholz, H.P., Erhardt, A., Can nectar properties explain sex-specific flower preferences in the adonis blue butterfly Lysandra bellargus? (2000) Ecol Entomol, 25, pp. 81-90Ruszczyk, A., Hábitos alimentares de borboletas adultas e sua adaptabilidade ao meio urbano (1986) Rev Bras Biol, 46, pp. 419-427Sanders, R.W., The genera of Verbenaceae in the Southeastern United States (2001) Harv Pap Bot, 5, pp. 303-358Santos, C.G., (2002) Aspectos do Comportamento e Morfologia Envolvidos na Alimentação dos Adultos de Dryas iulia alcionea e Heliconius erato phyllis, , (Lepidoptera: Nymphalidae) M. Sc. Thesis, Universidade Federal do Rio Grande do Sul, Porto AlegreSchapoval, E.E.S., Vargas, M.R.W., Chaves, C.G., Bridi, R., Zuanazzi, J.A., Henriques, A.T., Antiinflammatory and antinociceptive activities of extracts and isolated compounds from Stachytarpheta cayennensis (1998) J Ethnopharmacol, 60, pp. 53-59Schemske, D.W., Pollinator specificity in Lantana camara and L. trifolia (Verbenaceae) (1976) Biotropica, 8, pp. 260-264Scherer, C., Kolb, G., Behavioral experiments on the visual processing of color stimuli in Pieris brassicae L. (Lepidoptera) (1987) J Comp Physiol, 160, pp. 645-656Sharp, M.A., Parks, D., Plant resources and butterfly habitat selection (1974) Ecology, 55, pp. 870-875Sinha, S., Sharma, A., Lantana camara L.-a review (1984) Feddes Repert, 95, pp. 621-633Sokal, R.R., Rohlf, F.J., (1995) Biometry, , 3rd edn., New York: W.H. Freeman and CompanySwihart, S.L., The neural basis of colour vision in butterfly, Papilio troilus (1970) J Insect Physiol, 16, pp. 1623-1636Swihart, C.A., Colour discrimination by the butterfly Heliconius charitonius Linn (1971) Anim Behav, 19, pp. 156-164Waddington, K.D., Bumblebees do not respond to variance in nectar concentration (1995) Ethology, 101, pp. 33-38Wadlington, M.C., (2007) Innate preferences and learning abilities for floral patterns by monarch butterflies, , (Danaus plexippus). Senior Thesis, Georgetown University, Washington, DCWaser, N.M., Pollinator behavior and plant speciation: looking beyond the "ethological isolation" paradigm (2001) Cognitive Ecology of Pollination: Animal Behavior and Floral Evolution, pp. 318-335. , L. Chittka and J. D. Thomson (Eds.), New York: Cambridge University PressWeiss, M.R., Floral colour changes as cues for pollinators (1991) Nature, 354, pp. 227-229Weiss, M.R., Associative colour learning in a nymphalid butterfly (1995) Ecol Entomol, 20, pp. 298-301Weiss, M.R., Floral color change: a widespread functional convergence (1995) Am J Bot, 82, pp. 167-185Weiss, M.R., Innate colour preferences and flexible colour learning in the pipevine swallowtail (1997) Anim Behav, 53, pp. 1043-1052Weiss, M.R., Vision and learning in some neglected pollinators: beetles, flies, moths, and butterflies (2001) Cognitive Ecology of Pollination: Animal Behavior and Floral Evolution, pp. 171-190. , L. Chittka and J. D. Thomson (Eds.), New York: Cambridge University PressWyatt, R., Broyles, S.B., Ecology and evolution of reproduction in milkweeds (1994) Annu Rev Ecol Syst, 25, pp. 423-441Zar, J.H., (1999) Biostatistical Analysis, , 4th edn., New Jersey: Prentice Hal

External Morphology Of The Immature Stages Of Neotropical Heliconians: Vii. Dryadula Phaetusa (linnaeus) (lepidoptera, Nymphalidae, Heliconiinae) [morfologia Externa Dos Estágios Imaturos De Heliconíneos Neotropicais: Vii. Dryadula Phaetusa (linnaeus) (lepidoptera, Nymphalidae, Heliconiinae)]

The external features of egg, larva and pupa of Dryadula phaetusa (Linnaeus, 1758) are described and illustrated, based upon light and scanning electron microscopy.524500509Antunes, F.A., Menezes Jr., A.O., Tavares, M., Moreira, G.R.P., Morfologia externa dos estágios imaturos de heliconíneos neotropicais: I. Eueides isabella dianasa (Hübner, 1806). (2002) Revista Brasileira de Entomologia, 46, pp. 601-610Araújo, A.M., Valente, V.L.S., Observaçõ es sobre alguns lepidópteros e drosofilídeos do Parque Estadual do Turvo. (1981) Ciência e Cultura, 33, pp. 1485-1490Beebe, W., Crane, J., Fleming, H., A comparison of eggs, larvae and pupae in fourteen species of heliconiine butterflies from Trinidad, W. I (1960) Zoologica, 45, pp. 111-154Benson, W.W., Brown Jr., K.S., Gilbert, L.E., Coevolution of plants and herbivores: Passion vine butterflies (1975) Evolution, 32, pp. 659-680Brown Jr., K.S., The biology of Heliconius and related genera (1981) Annual Review of Entomology, 26, pp. 427-456Brown, K. S., Jr. 1992. Borboletas da Serra do Japi: diversidade, hábitats, recursos alimentares e variação temporal, p. 142-187. In: L. P. C. Morellato (ed.). História Natural da Serra do Japí: Ecologia e preservação de uma área florestal no sudeste do Brasil. Campinas, UNICAMP/FAPESP, 322 pBrown Jr., K.S., Mielke, O.H.H., The heliconians of Brazil (Lepidoptera: Nymphalidae). Part II. Introduction and general comments, with a supplementary revision of the tribe (1972) Zoologica, 57, pp. 1-40Daly, H.V., Insect morphometrics (1985) Annual Review of Entomology, 30, pp. 415-438Dell'Erba, R., Kaminski, L.A., Moreira, G.R.P., O estágio de ovo dos Heliconiini (Lepidoptera: Nymphalidae) do Rio Grande do Sul, Brasil. (2005) Iheringia, Série Zoologia, 95, pp. 29-46DeVries, P.J., The butterflies of Costa Rica and their natural history (1987) Papilionidae, Pieridae, Nymphalidae, , Princeton, Princeton University, 327 pDowney, J.C., Allyn Jr., A.C., Chorionic sculpturing in eggs of Lycaenidae. Part I (1981) Bulletin of the Allyn Museum, 61, pp. 1-29Duarte, M.R. K. Robbins & O. H. H. Mielke. 2005. Immature stages of Calycopis caulonia (Hewitson, 1877) (Lepidoptera, Lycaenidae, Theclinae, Eumaeini), with notes on rearing detritivorous hairstreaks on artificial diet. Zootaxa 1063: 1-31Emsley, M.G., A morphological study of imagine Heliconiinae (Lep.: Nymphalidae) with a consideration of the group (1963) Zoologica, 48, pp. 85-130Fleming, H., The first instar larvae of the Heliconiinae (Butterflies) of Trinidad, W. I (1960) Zoologica, 45, pp. 91-110Freitas, A.V.L., Brown Jr., K.S., Phylogeny of the Nymphalidae (Lepidoptera) (2004) Systematic Biology, 53, pp. 363-383Freitas, A.V.L., Oliveira, P.S., Ants as selective agents on herbivore biology: Effects on the behaviour of a nonmyrmecophilous butterfly (1996) Journal of Animal Ecology, 65, pp. 205-210Harvey, D. J. 1991. Higher classification of the Nymphalidae. Appendix B, p. 255-273. In: H. F. Nijhout (ed.). The development and evolution of butterfly wing patterns. Washington, Smithsonian Institution, xvi + 297 pKaminski, L.A., Tavares, M., Ferro, V.G., Moreira, G.R.P., Morfologia externa dos estágios imaturos de heliconíneos neotropicais: III. Heliconius erato phyllis (Fabricius) (Lepidoptera, Nymphalidae, Heliconiinae). (2002) Revista Brasileira de Zoologia, 19, pp. 977-993Kaminski, L.A., Dell'Erba, R., Moreira, G.R.P., Morfologia externa dos estágios imaturos de heliconíneos neotropicais: VI. Dione moneta moneta Hübner (Lepidoptera, Nymphalidae, Heliconiinae). (2008) Revista Brasileira de Entomologia, 52, pp. 13-23Kitching, I.J., The use of larval chaetotaxy in butterfly systematics, with special reference to the Danaini (Lepidoptera: Nymphalidae) (1984) Systematic Entomology, 9, pp. 49-61Kitching, I.J., Early stages and the classification of the milkweed butterflies (Lepidoptera: Danainae) (1985) Zoological Journal of the Linnean Society, 85, pp. 1-97Lamas, G., Checklist: Part 4A. Hesperioidea - Papilionoidea (2004) Atlas of Neotropical Lepidoptera, 5 A. , J. B. Heppner ed, Gainesville, Association for Tropical Lepidoptera, Scientific Publishers, xxxiv, 428 pMiller, J.S., Cladistics and classification of the Notodontidae (Lepidoptera: Noctuoidea) based on larval and adult morphology (1991) Bulletin of the American Museum of Natural History, 204, pp. 1-230Mosher, E., A classification of the Lepidoptera based on characters of the pupa (1916) Bulletin of the Illinois State Laboratory of Natural History, 12, pp. 1-165Motta, P. C. 2003. Phylogenetic relationships of Ithomiinae based on first-instar larvae, p. 409-429. In: C. L. BoggsW. B. Watt & P. R. Ehrlich (eds.). Butterflies: ecology and evolution taking flight. Chicago, University of Chicago, 739 pMüller, W., Südamerikanische Nymphalidenraupen. Versuch eines naturlichen Systems der Nymphaliden. (1886) Zoologischen Jahrbüchern, 1, pp. 417-678Paim, A.C., Kaminski, L.A., Moreira, G.R.P., Morfologia externa dos estágios imaturos de heliconíneos neotropicais: IV. Dryas iulia alcionea (Lepidoptera, Nymphalidae, Heliconiinae). (2004) Iheringia, Série Zoologia, 94, pp. 25-35Penz, C.M., Higher level phylogeny for the passion-vine butterflies (Lepidoptera: Heliconiinae) based on early stage and adult morphology (1999) Zoological Journal of the Linnean Society, 127, pp. 277-344Peterson, A., Larvae of insects. An introduction to Neartic species (1962) Part I Lepidoptera and plant infesting Hymenoptera, , Ann Arbor, Edwards Brothers Inc, 315 pSilva, da, D.S., Dell'Erba, R., Kaminski, L.A., Moreira, G.R.P., Morfologia externa dos estágios imaturos de heliconíneos neotropicais: V. Agraulis vanillae maculosa (Lepidoptera, Nymphalidae, Heliconiinae). (2006) Iheringia, Série Zoologia, 96, pp. 219-228Snedecor, G.W., Cochran, W.G., (1980) Statistical methods, , Ames, Iowa State University, 507 pStehr, F. W. 1987. Order Lepidoptera, p. 288-305. In: F. W. Stehr, (ed.). Immature insects. I. Dubuque, Kendall/ Hunt Publishing Company, 975 pTavares, M., Kaminski, L.A., Moreira, G.R.P., Morfologia externa dos estágios imaturos de heliconíneos neotropicais: II (2002) Dione juno juno, , Cramer, Lepidoptera: Nymphalidae: Heliconiinae, Revista Brasileira de Zoologia 19: 961-97