Size of and damage on shoots of Passiflora suberosa (Passifloraceae) influence oviposition site selection of Heliconius erato phyllis (Fabricius) (Lepidoptera, Nymphalidae)

Mugrabi-Oliveira, Elna; Moreira, Gilson R.P

doi:10.1590/S0101-81751996000400015

Abstract

Oviposition site selection of Heliconius erato phyllis (Fabricius, 1775) (Lepidoptera, Nymphalidae) was studied when size of and damage on shoots were variable in a natural population of Passiflora suberosa Linnaeus (Passifloraceae), and through sequential and simultaneous choice experiments performed under insectary conditions. Females showed marked oviposition preference for undamaged and largest shoots of P. suberosa. Eggs were mostly laid on the terminal buds of intact shoots under natural conditions. In simultaneous choice trials, females preferred to oviposit on shoots from which leaves (ten) were removed but the terminal bud maintained to those where leaves were kept but the terminal bud was cut out. In sequential choice trials, they did not lay eggs on shoots from which the terminal bud was removed. Females preferred to oviposit on large to short intact shoots in both sequential and simultaneous choice trials. Females laid eggs preferentially on shoots with the greatest leaf area when most plants were intact in the field during early spring. Later in fall, when mostly large, old shoots were damaged or in a reproductive stage (less desirable for oviposition), oviposition intensity was highest on the shortest, youngest shoots of P. suberosa. Thus, females might rank these quality attributes higher than size while selecting shoots for oviposition. The consequences of ovipositing selectively on intact, large shoots of P. suberosa are discussed from the view point of H. erato phyllis larval performance.

Lepidoptera; Heliconius; Passiflora; oviposition behavior; host plant selection

^IPós-graduação em Entomologia, Departamento de Zoologia, Universidade Federal do Paraná. Caixa Postal 19020, 81531-990 Curitiba, Paraná, Brasil

^IICorrespondence to: Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul Avenida Paulo Gama 40 90046-900 Porto Alegre, Rio Grande do Sul, Brasil e-mail: grpm@if.ufrgs.br

ABSTRACT

Oviposition site selection of Heliconius erato phyllis (Fabricius, 1775) (Lepidoptera, Nymphalidae) was studied when size of and damage on shoots were variable in a natural population of Passiflora suberosa Linnaeus (Passifloraceae), and through sequential and simultaneous choice experiments performed under insectary conditions. Females showed marked oviposition preference for undamaged and largest shoots of P. suberosa. Eggs were mostly laid on the terminal buds of intact shoots under natural conditions. In simultaneous choice trials, females preferred to oviposit on shoots from which leaves (ten) were removed but the terminal bud maintained to those where leaves were kept but the terminal bud was cut out. In sequential choice trials, they did not lay eggs on shoots from which the terminal bud was removed. Females preferred to oviposit on large to short intact shoots in both sequential and simultaneous choice trials. Females laid eggs preferentially on shoots with the greatest leaf area when most plants were intact in the field during early spring. Later in fall, when mostly large, old shoots were damaged or in a reproductive stage (less desirable for oviposition), oviposition intensity was highest on the shortest, youngest shoots of P. suberosa. Thus, females might rank these quality attributes higher than size while selecting shoots for oviposition. The consequences of ovipositing selectively on intact, large shoots of P. suberosa are discussed from the view point of H. erato phyllis larval performance.

Key words: Lepidoptera, Heliconius, Passiflora, oviposition behavior, host plant selection

Full text available only in PDF format.

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ACKNOWLEDGMENTS. Thanks are due to FEPAGRO for allowing us to carry out the study at Águas Belas Experimental Station. We are especially grateful to Aldo M. Araújo for encouraging and helping us to start with

Heliconius-Passiflora

studies. We also thank Miriam Becker for some advice on sampling techniques, and Feliciano Flores for the use of the leaf area meter. Comments by Catherine N. Duckett (University of Puerto Rico), Nicoleta T.N. Sabetzki (EPAGRI) and Aldo M. Araújo (UFRGS) improved earlier versions of the manuscript. Financial support for this study came from a CNPq Schoolarship (M.Sc. Thesis) granted to E. Mugrabi-Oliveira.

Recebido em 17.VI.1996; aceito em 28.XII.1996.

¹
Alexander, A.J. 1961. A study of the biology and behavior of the caterpillars, pupae and emerging butterflies of the subfamily Heliconiinae in Trinidad, West Indies. Part I. Some aspects of larval behavior. Zoologica 46:1-24.
Araújo, A.M. 1987. Teoria dos jogos e estratégias evolutivamente estáveis. Actas XVII Congresso Argentino de Genética, Rio Cuarto, p. 27-33.
Benson, W.W. 1978. Resource partitioning in passion vine butterflies. Evolution 32:493-518.
Benson, W.W.; K.S. Brown Jr. & L.E. Gilbert. 1976. Coevolution of plants and herbivores: passion flower butterflies. Evolution 29:659-680.
Bernays, E.A. & R.F. Chapman. 1994. Host-plant selection by phytophagous insects. Chapman & Hall, 312p.
Brown Jr., K.S.. 1981. The biology of Heliconius and related genera. Ann. Rev. Entomol. 26:427-456.
Brown Jr., K.S. & O.H.H. Mielke. 1972. The heliconians of Brazil (Lepidoptera: Nymphalidae). Part II. Introduction and general comments, with a supplementary revision of the tribe. Zoologica 57:1-40.
Cates, R.G. 1980. Feeding patterns of monophagous, oligophagous, and polyphagous insect herbivores: the effect of resource abundance and plant chemistry. Oecologia 46:22-31.
Copp, N.H. & D. Davenport. 1978. Agraulis and Passiflora I. Control of specificity. Biol. Bull. 155:98-112.
Courtney, S.P. & J. Forsberg. 1988. Host use by two pierid butterflies varies with host density. Func. Ecol. 2:67-75.
Crane, J. 1955. Imaginal behavior of a Trinidad butterfly, Heliconius erato hydara Hewitson, with special reference to the social use of color. Zoológica 40:167-195.
Duckett, C.N. 1989. Natural history of Pedilia sp. A and its interactions with other herbivores of Passiflora pittieri. Entomography 6:381-389.
Dunlap-Pianka, H.L; C.L. Boggs & L.E. Gilbert. 1977. Ovarian dynamics in Heliconiine butterflies: programmed senescence versus eternal youth. Science 197:487-490.
Gilbert, L.E. 1972. Pollen feeding and reproductive biology of Heliconius butterflies. Proc. Nat. Acad. Sci. 69:1403-1407.
Gilbert, L.E. 1991. Biodiversity of a Central American Heliconius community: pattern, process, and problems, p. 403-427. In: P.W. Price; T.L. Lewinsohn; G.W. Fernandes & W.W. Benson (Eds). Plant-Animal Interactions: evolutionary ecology in tropical and temperate regions. John Wiley & Sons.
Hamilton, J.G. & M.P. Zalucki. 1993a. Interactions between a specialist herbivore, Crocidosema plebejana, and its host plants Malva parviflora, and cotton, Gossypium hirsutum: larval performance. Entomol. exp. appl. 66:199-205.
Hamilton, J.G. & M.P. Zalucki. 1993b. Interactions between a specialist herbivore, Crocidosema plebejana, and its host plants Malva parviflora, and cotton, Gossypium hirsutum: oviposition preference. Entomol. exp. appl. 66:207-212.
Longino, J.T. 1984. Shoots, parasitoids, and ants as forces in the population dynamics of Heliconius hewitsoni in Costa Rica. Unpublished Ph.D. Dissertation, University of Texas, Austin.
Jaenike, J. 1978. On optimal oviposition behavior in phytophagous insects. Theor. Popul. Biol. 14:350-356.
______. 1990. Host specialization in phytophagous insects. Annu. Rev. Ecol. Syst. 21:243-73.
Jones, R.E. 1991. Host location and oviposition on plants, p. 139-171. In: W.J. Bailey & J. Ridsdill-Smith (Eds). Reproductive behavior of insects: individuals and populations. Chapman & Hall.
Leather, S.R. 1985. Oviposition preferences in relation to larval growth rates and survival in the pine beauty moth, Panolis flammea. Ecol. Entomol. 10:213-217.
Lewis, A.C. 1982. Leaf wilting alters a plant species ranking by the grasshopper Melanoplus differentialis. Ecol. Entomol. 7:391-395.
Lopes, F.S. 1991. Padrões sazonais e evolução do uso de plantas hospedeiras de larvas por Heliconius erato phyllis (L.) (Lepidoptera, Nymphalidae) na Serra do Japi, São Paulo. Unpublished Ph.D. Dissertation, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, 119p.
Lutz, L.V. 1995. Variação e seleção sobre o padrão de coloração das asas de Heliconius erato phyllis (Lepidoptera; Nymphalidae) em populações naturais. Unpublished M.Sc. Thesis, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, 76p.
Menna-Barreto, Y. & A.M. Araújo. 1985. Evidence for host plant preferences in Heliconius erato phyllis from southern Brazil (Nymphalidae). J. Res. Lepid. 24:41-46.
Mugrabi-Oliveira, E & G.R.P. Moreira. 1996. Conspecific mimics and low host plant availability reduce egg laying by Heliconius erato phyllis (Lepidoptera, Nymphalidae). Revta bras. Zool. 13 (4):929-937.
Papaj, D.R. & M.D. Rausher. 1983. Individual variation in host location by phytophagous insects, p. 77-124. In: S. Ahmad (Ed.) Herbivorous insects: host- seeking behavior and mechanisms. Academic Press.
Perico, E. & A.M. Araújo. 1991. Suitability of host plants (Passifloraceae) and their acceptableness by Heliconius erato and Dryas iulia (Lepidoptera; Nymphalidae). Evol. Biol. 5:59-74.
Siegel, S. 1956. Nonparametric statistics: for the behavioral sciences. Freedman and Company.
Singer, M.C. 1983. Determinants of multiple host use by a phytophagous insect population. Evolution 37:389-403.
______. 1986. The definition and measurement of oviposition preference in plant-feeding insects, p. 65-94. In: J. Miller & T. Miller (Eds). Insect-plant interactions. Springer-Verlag.
Smiley, J. 1978. Plant chemistry and the evolution of host specificity: new evidence from Heliconius and Passiflora. Science 201:745-747.
Sokal, R.R. & F.J. Rohlf. 1981. Biometry. W.H. Freeman and Company, 2^nd ed.
Solomon, B.P. 1981. Response of a host-specific herbivore to resource density, relative abundance, and phenology. Ecology 62:1205-1214.
Thomas, CD. 1987. Behavioural determination of diet breadth in insect herbivores: the effect of leaf age on choice of host species by beetles feeding on Passiflora vines. Oikos 48:211-216.
Wiklund, C. 1975. The evolutionary relationship between adult oviposition preferences and larval host plant range in Papilio machaon L. Oecologia 18:185-197.
______. 1981. Generalist vs. specialist oviposition behaviour in Papilio machaon (Lepidoptera) and functional aspects on the hierarchy of oviposition preferences. Oikos 36:163-170.

**Size of and damage on shoots of Passiflora suberosa (Passifloraceae) influence oviposition site selection of Heliconius erato phyllis (Fabricius) (Lepidoptera, Nymphalidae)**

Elna Mugrabi-Oliveira^I; Gilson R.P. Moreira^II

Publication Dates

Publication in this collection
13 July 2009
Date of issue
1996

History

Accepted
28 Dec 1996
Received
17 June 1996

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] ¹
Alexander, A.J. 1961. A study of the biology and behavior of the caterpillars, pupae and emerging butterflies of the subfamily Heliconiinae in Trinidad, West Indies. Part I. Some aspects of larval behavior. Zoologica 46:1-24.

[2] Araújo, A.M. 1987. Teoria dos jogos e estratégias evolutivamente estáveis. Actas XVII Congresso Argentino de Genética, Rio Cuarto, p. 27-33.

[3] Benson, W.W. 1978. Resource partitioning in passion vine butterflies. Evolution 32:493-518.

[4] Benson, W.W.; K.S. Brown Jr. & L.E. Gilbert. 1976. Coevolution of plants and herbivores: passion flower butterflies. Evolution 29:659-680.

[5] Bernays, E.A. & R.F. Chapman. 1994. Host-plant selection by phytophagous insects. Chapman & Hall, 312p.

[6] Brown Jr., K.S.. 1981. The biology of Heliconius and related genera. Ann. Rev. Entomol. 26:427-456.

[7] Brown Jr., K.S. & O.H.H. Mielke. 1972. The heliconians of Brazil (Lepidoptera: Nymphalidae). Part II. Introduction and general comments, with a supplementary revision of the tribe. Zoologica 57:1-40.

[8] Cates, R.G. 1980. Feeding patterns of monophagous, oligophagous, and polyphagous insect herbivores: the effect of resource abundance and plant chemistry. Oecologia 46:22-31.

[9] Copp, N.H. & D. Davenport. 1978. Agraulis and Passiflora I. Control of specificity. Biol. Bull. 155:98-112.

[10] Courtney, S.P. & J. Forsberg. 1988. Host use by two pierid butterflies varies with host density. Func. Ecol. 2:67-75.

[11] Crane, J. 1955. Imaginal behavior of a Trinidad butterfly, Heliconius erato hydara Hewitson, with special reference to the social use of color. Zoológica 40:167-195.

[12] Duckett, C.N. 1989. Natural history of Pedilia sp. A and its interactions with other herbivores of Passiflora pittieri. Entomography 6:381-389.

[13] Dunlap-Pianka, H.L; C.L. Boggs & L.E. Gilbert. 1977. Ovarian dynamics in Heliconiine butterflies: programmed senescence versus eternal youth. Science 197:487-490.

[14] Gilbert, L.E. 1972. Pollen feeding and reproductive biology of Heliconius butterflies. Proc. Nat. Acad. Sci. 69:1403-1407.

[15] Gilbert, L.E. 1991. Biodiversity of a Central American Heliconius community: pattern, process, and problems, p. 403-427. In: P.W. Price; T.L. Lewinsohn; G.W. Fernandes & W.W. Benson (Eds). Plant-Animal Interactions: evolutionary ecology in tropical and temperate regions. John Wiley & Sons.

[16] Hamilton, J.G. & M.P. Zalucki. 1993a. Interactions between a specialist herbivore, Crocidosema plebejana, and its host plants Malva parviflora, and cotton, Gossypium hirsutum: larval performance. Entomol. exp. appl. 66:199-205.

[17] Hamilton, J.G. & M.P. Zalucki. 1993b. Interactions between a specialist herbivore, Crocidosema plebejana, and its host plants Malva parviflora, and cotton, Gossypium hirsutum: oviposition preference. Entomol. exp. appl. 66:207-212.

[18] Longino, J.T. 1984. Shoots, parasitoids, and ants as forces in the population dynamics of Heliconius hewitsoni in Costa Rica. Unpublished Ph.D. Dissertation, University of Texas, Austin.

[19] Jaenike, J. 1978. On optimal oviposition behavior in phytophagous insects. Theor. Popul. Biol. 14:350-356.

[20] ______. 1990. Host specialization in phytophagous insects. Annu. Rev. Ecol. Syst. 21:243-73.

[21] Jones, R.E. 1991. Host location and oviposition on plants, p. 139-171. In: W.J. Bailey & J. Ridsdill-Smith (Eds). Reproductive behavior of insects: individuals and populations. Chapman & Hall.

[22] Leather, S.R. 1985. Oviposition preferences in relation to larval growth rates and survival in the pine beauty moth, Panolis flammea. Ecol. Entomol. 10:213-217.

[23] Lewis, A.C. 1982. Leaf wilting alters a plant species ranking by the grasshopper Melanoplus differentialis. Ecol. Entomol. 7:391-395.

[24] Lopes, F.S. 1991. Padrões sazonais e evolução do uso de plantas hospedeiras de larvas por Heliconius erato phyllis (L.) (Lepidoptera, Nymphalidae) na Serra do Japi, São Paulo. Unpublished Ph.D. Dissertation, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, 119p.

[25] Lutz, L.V. 1995. Variação e seleção sobre o padrão de coloração das asas de Heliconius erato phyllis (Lepidoptera; Nymphalidae) em populações naturais. Unpublished M.Sc. Thesis, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, 76p.

[26] Menna-Barreto, Y. & A.M. Araújo. 1985. Evidence for host plant preferences in Heliconius erato phyllis from southern Brazil (Nymphalidae). J. Res. Lepid. 24:41-46.

[27] Mugrabi-Oliveira, E & G.R.P. Moreira. 1996. Conspecific mimics and low host plant availability reduce egg laying by Heliconius erato phyllis (Lepidoptera, Nymphalidae). Revta bras. Zool. 13 (4):929-937.

[28] Papaj, D.R. & M.D. Rausher. 1983. Individual variation in host location by phytophagous insects, p. 77-124. In: S. Ahmad (Ed.) Herbivorous insects: host- seeking behavior and mechanisms. Academic Press.

[29] Perico, E. & A.M. Araújo. 1991. Suitability of host plants (Passifloraceae) and their acceptableness by Heliconius erato and Dryas iulia (Lepidoptera; Nymphalidae). Evol. Biol. 5:59-74.

[30] Siegel, S. 1956. Nonparametric statistics: for the behavioral sciences. Freedman and Company.

[31] Singer, M.C. 1983. Determinants of multiple host use by a phytophagous insect population. Evolution 37:389-403.

[32] ______. 1986. The definition and measurement of oviposition preference in plant-feeding insects, p. 65-94. In: J. Miller & T. Miller (Eds). Insect-plant interactions. Springer-Verlag.

[33] Smiley, J. 1978. Plant chemistry and the evolution of host specificity: new evidence from Heliconius and Passiflora. Science 201:745-747.

[34] Sokal, R.R. & F.J. Rohlf. 1981. Biometry. W.H. Freeman and Company, 2^nd ed.

[35] Solomon, B.P. 1981. Response of a host-specific herbivore to resource density, relative abundance, and phenology. Ecology 62:1205-1214.

[36] Thomas, CD. 1987. Behavioural determination of diet breadth in insect herbivores: the effect of leaf age on choice of host species by beetles feeding on Passiflora vines. Oikos 48:211-216.

[37] Wiklund, C. 1975. The evolutionary relationship between adult oviposition preferences and larval host plant range in Papilio machaon L. Oecologia 18:185-197.

[38] ______. 1981. Generalist vs. specialist oviposition behaviour in Papilio machaon (Lepidoptera) and functional aspects on the hierarchy of oviposition preferences. Oikos 36:163-170.