Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2018-11-20
Page range: 1–32
Abstract views: 99
PDF downloaded: 4

Immature stages of the Rubiaceae-feeding metalmark butterflies (Lepidoptera: Riodinidae), and a new function for the tentacle nectary organs

Aquapro, Km 13 via a Acacias, Villavicencio, Colombia.
Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil.
Lepidoptera Ant-organs chaetotaxy coevolution larval mimicry myrmecophily Psychotria trophobiosis


Metalmark butterfly (Riodinidae) diversity is heavily concentrated in the Neotropical lowland forests but despite their prevalence basic information on immature stages is still scarce. Here we describe the life cycle of seven taxa in the Rubiaceae-feeding section of the Mesosemiina, including three Mesosemia Hübner, [1819], three Leucochimona Stichel, 1909, and the first information for Semomesia Westwood, 1851. Immature stage morphology of Mesosemia cippus Hewitson, 1859 is described in detail through scanning electron microscopy. Generally, eggs are laid singly and caterpillars are folivorous with a cryptic green coloration except for M. cippus which has gregarious caterpillars with a bright yellow color pattern. Immature stages of all analyzed species are morphologically similar and characterized by: oblate spheroid eggs with small spines on the rib intersections; nonmyrmecophilous larvae with sparse long setae on chalazae or pinnacles, perforated cupola organs (PCOs) and tentacle nectary organs (TNOs) in all instars; pupae attached longitudinally to the substrate by the cremaster and a silk girdle that crosses over abdominal segments A1 or A2. Functionality of the TNOs is documented for the first time in the “Mesosemia section” of the Mesosemiina, but they are not used to facilitate symbiotic interactions between caterpillars and ants. When molested, caterpillars everted the TNOs secreting a conspicuous drop of opaque and viscous liquid with a defensive function. A summary of the host plants in the “Mesosemia section” is presented, confirming the preponderance of oligophagy in the Rubiaceae. The morphological and behavioral traits here described are discussed in the context of defense against natural enemies and constitute key information to understanding the evolution of ant-organs and myrmecophily in riodinids.



  1. Aiello, A. (1984) Adelpha (Nymphalidae): deception on the wing. Psyche: A Journal of Entomology, 91, 1–45.

    Altmann, J. (1974) Observational study of behavior: sampling methods. Behaviour, 49, 227–267.

    Ballmer, G.R. & Pratt, G.F. (1992) Loranthomitoura, a new genus of Eumaeini (Lepidoptera: Lycaenidae: Theclinae). Tropical Lepidoptera, 3, 37–46.

    Barcant, M. (1970) Butterflies of Trinidad and Tobago. Collins, London, 314 pp.

    Beccaloni, G.W., Viloria, A.L., Hall, S.K. & Robinson, G.S. (2008) Catalogue of the host plants of the neotropical butterflies/Catálogo de las Plantas Huésped de las Mariposas Neotropicales. m3m-Monografías Tercer Milenio. Vol. 8. Sociedad Entomológica Aragonesa (SEA), Zaragoza, 536 pp.

    Benson, W.W., Brown, K.S. Jr. & Gilbert, L.E. (1975) Coevolution of plants and herbivores: passion vine butterflies. Evolution, 32, 659–680.

    Biezanko, C.M., Mielke, O.H.H. & Wedderhoff, A. (1979) Contribuição ao estudo faunístico dos Riodinidae do Rio Grande do Sul, Brasil (Lepidoptera). Acta Biologica Paranaense, Curitiba, 7, 7–22.

    Brévignon, C. (1992a) Élevage de deux Riodininae guyanais, Napaea beltiana Bates et Cremna thasus Stoll. 1. À propos de la myrmécophilie des chenilles (Lep. Lycaenidae Riodininae). Alexanor, 17 (8), 403–413.

    Brévignon, C. (1992b) Elevage de deux Riodininae Guyanais, Napaea beltiana Bates et Cremna thasus Stoll. 2. Le comportement des imagos. Alexanor, 17 (8), 508–512.

    Brown Jr., K.S. (1987) Chemistry at the Solanaceae ⁄ Ithomiinae interface. Annals of the Missouri Botanical Garden, 74, 359–397.

    Brown Jr., K.S. (1992) Borboletas da Serra do Japi: diversidade, hábitats, recursos alimentares e variação temporal. In: Morellato, L.P.C. (Ed.), História Natural da Serra do Japi: Ecologia e preservação de uma área florestal no sudeste do Brasil. UNICAMP/FAPESP, Campinas, pp. 142–187.

    Burns, J.M., Janzen, D.J., Hajibabaei, M., Hallwachs, W. & Hebert, P.D.N. (2007) DNA barcodes of closely related (but morphologically and ecologically distinct) species of skipper butterflies (Hesperiidae) can differ by only one to three nucleotides. Journal of the Lepidopterists’ Society, 61, 138–153.

    Callaghan, C.J. (1978) Studies on restinga butterflies. II. Notes on the population structure of Menander felsina (Riodininae). Journal of the Lepidopterists’ Society, 32, 87–94.

    Callaghan, C.J. (1991) Notes on the immature biology of two Riodinine butterflies: Metacharis ptolomaeus and Napaea nepos orpheus (Lycaenidae). Journal of Research on the Lepidoptera, 30 (3–4), 221–24.

    Callaghan, C.J. & Lamas, G. (2004) Riodinidae. In: Lamas, G. (Eds.), Checklist: Part 4A. Hesperioidea-Papilionoidea. In: Heppner, J.B. (Ed.), Atlas of Neotropical Lepidoptera. Vol. 5A. Association for Tropical Lepidoptera, Scientific Publishers, Gainesville, FL, pp. 141–170.

    Campbell, D.L. & Pierce, N.E. (2003) Phylogenetic relationships of the Riodinidae: implications for the evolution of ant association. In: Boggs, C.L., Watt, W.B. & Ehrlich, P.R. (Eds.), Butterflies: ecology and evolution taking flight. University of Chicago, Chicago, IL, pp. 395–408.

    D’Abrera, B.L. (1994) Butterflies of the Neotropical Region. Part VI. Riodinidae. Black Rock, Hill House, Victoria, 218 pp. [pp. 879–1096]

    Daniels, H., Gottsberger, G. & Fiedler, K. (2005) Nutrient composition of larval nectar secretions from three species of myrmecophilous butterflies. Journal of Chemical Ecology, 31, 2805–2821.

    Delprete, P.G.P. & Jardim J.G. (2012) Systematics, taxonomy and floristics of Brazilian Rubiaceae: an overview about the current status and future challenges. Rodriguésia, 63, 101–128.

    DeVries, P.J. (1991) Evolutionary and ecological patterns in myrmecophilous riodinid butterflies. In: Huxley, C.R. & Cutler, D.F. (Eds.), Ant-plant interactions. Oxford University Press, Oxford, pp. 143–156.

    DeVries, P.J. (1997) The butterflies of Costa Rica and their natural history. Vol. II. Riodinidae. Princeton University Press, Princeton, NJ, 368 pp.

    DeVries, P.J. (1988) The larval ant-organs of Thisbe irenea (Lepidoptera: Riodinidae) and their effects upon attending ants. Zoological Journal of the Linnean Society, 94, 379–393.

    DeVries, P.J. (1990) Enhancement of symbioses between butterfly caterpillars and ants by vibrational communication. Science, 248, 1104–1106.

    DeVries, P.J. (1991a) Mutualism between Thisbe irenea butterflies and ants, and the role of ant ecology in the evolution of larval–ant associations. Biological Journal of the Linnean Society, 43, 179–195.

    DeVries, P.J. (1991b) Evolutionary and ecological patterns in myrmecophilous riodinid butterflies. In: Huxley, C.R. & Cutler, D.F. (Eds.), Ant-plant interactions. Oxford University Press, Oxford, pp. 143–156.

    DeVries, P.J. (1991c) Call production by myrmecophilous riodinid and lycaenid butterfly caterpillars (Lepidoptera): morphological, acoustical, functional, and evolutionary patterns. American Museum Novitates, 3025, 1–23.

    DeVries, P.J. & Baker, I. (1989) Butterfly exploitation of an ant-plant mutualism: adding insult to herbivory. Journal of the New York Entomological Society, 97, 332–340.

    DeVries, P.J., Chacon, I.A. & Murray, D. (1994) Toward a better understanding of host use biodiversity in riodinid butterflies (Lepidoptera). Journal of Research on Lepidoptera, 31, 103–126.

    DeVries, P.J. & Penz, C.M. (2002) Early stages of the entomophagous metalmark butterfly Alesa amesis (Riodinidae: Eurybiini). Journal of the Lepidopterists’ Society, 56, 265–271.

    DeVries, P.J., Cabral, B.C. & Penz, C.M. (2004) The early stages of Apodemia paucipuncta (Riodinidae): myrmecophily, a new caterpillar ant-organ and consequences for classification. Milwaukee Public Museum Contributions to Biology and Geology, 102, 1–13.

    Downey, J.C. & Allyn, A.C. (1980) Eggs of Riodinidae. Journal of the Lepidopterists’ Society, 34, 133–145.

    Duarte, M., Robbins, R.K. & Mielke, O.H.H. (2005) Immature stages of Calycopis caulonia (Hewitson, 1877) (Lepidoptera, Lycaenidae, Theclinae, Eumaeini), with notes on rearing detritivorous hairstreaks on artificial diet. Zootaxa, 1063 (1), 1–31.

    Dury, G.J., Bede, J.C. & Windsor, D.M. (2014) Preemptive circular defence of immature insects: definition and occurrences of cycloalexy revisited. Psyche: A Journal of Entomology, 2014, 1–13.

    Dussourd, D.E. (2009) Do canal-cutting behaviors facilitate host-range expansion by insect herbivores? Biological Journal of the Linnean Society, 96, 715–731.

    Dussourd, D.E. (2017) Behavioral sabotage of plant defenses by insect folivores. Annual Review of Entomology, 62, 15–34.

    Ebel, E.R., DaCosta, J.M., Sorenson, M.D., Hill, R.I., Briscoe, A.D., Willmott, K.R. & Mullen, S.P. (2015) Rapid diversification associated with ecological specialization in Neotropical Adelpha butterflies. Molecular Ecology, 24, 2392–2405.

    Edger, P.P., Heidel‐Fischer, H.M., Bekaert, M., Rota, J., Glöckner, G., Platts, A.E., Heckel, D.G., Der, J.P., Wafula, E.K., Tang, M., Hofberger, J.A., Smithson, A., Hall, J.C., Blanchette, M., Bureau, T.E., Wright, S.I. dePamphilis, C.W., Schranz, M.E., Barker, M.S., Conant, G.C., Wahlberg, N., Vogel, H., Pires, J.C. & Wheat, C.W. (2015) The butterfly plant arms‐race escalated by gene and genome duplications. Proceedings of the National Academy of Sciences of the United States of America, 112, 8362–8366.

    Ehrlich, P.R. & Raven, P.H. (1964) Butterflies and plants: A study in coevolution. Evolution, 18 (4), 586–608.

    Espeland, M., Hall, J.P.W., DeVries, P.J., Lees, D.C., Cornwall, M., Hsu, Y.F., Wu, L.W., Campbell, D.L., Talavera, G., Vila, R., Salzman, S., Ruehr, S., Lohman, D.J. & Pierce, N.E. (2015) Ancient Neotropical origin and recent recolonisation: phylogeny, biogeography and diversification of the Riodinidae (Lepidoptera: Papilionoidea). Molecular Phylogenetics and Evolution, 93, 296–306.

    Espeland, M., Breinholt, J., Willmott, K.R., Warren, A.D., Vila, R., Toussaint, E.F.A., Maunsell, S.C., Aduse-Poku, K., Talavera, G., Eastwood, R., Jarzyna, M.A., Guralnick, R., Lohman, D.J., Pierce, N.E. & Kawahara, A.Y. (2018) Comprehensive, dated, higher-level phylogeny of butterflies inferred from genomic data. Current Biology, 28, 770–778.

    Fiedler, K. (1991) Systematic, evolutionary, and ecological implications of myrmecophily within the Lycaenidae (Insecta: Lepidoptera: Papilionoidea). Bonner Zoologische Monographien, 31, 1–210.

    Futuyma, D.J. & Agrawal, A.A. (2009) Macroevolution and the biological diversity of plants and herbivores. Proceedings of the National Academy of Sciences of the United States of America, 106,18054–18061.

    Gallard, J.Y. (2017) Les Riodinidae de Guyane. Pensoft, Sofia, 192 pp.

    Greve, R.R., Callaghan, C., Kaminski, L.A. & Freitas, A.V.L. (2013) The rediscovery of Joiceya praeclarus Talbot, 1928 (Lepidoptera: Riodinidae), more than 80 years after its description. Journal of the Lepidopterists’ Society, 67, 56–57.

    Hall, J.P.W. (2003) Phylogenetic reassessment of the five forewing radial-veined tribes of Riodininae ( Lepidoptera : Riodinidae ). Systematic Entomology, 28, 23–37.

    Hall, J.P.W. (2018) A monograph of the Nymphidiina (Lepidoptera: Riodinidae: Nymphidiini): Phylogeny taxonomy, biology, and biogeography. The Entomological Society of Washington, Washington, D.C., 990 pp.

    Hall, J.P.W. & Willmott, K.R. (2000) Patterns of feeding behaviour in adult male Riodinid butterflies and their relationship to morphology and ecology. Biological Journal of the Linnean Society, 69, 11–23.

    Harvey, D.J. (1987) The higher classification of the Riodinidae (Lepidoptera). PhD dissertation, University of Texas, Austin, TX, 215 pp.

    Harvey, D.J. (1989) Perforated cupola organs on larvae of Euselasiinae (Riodinidae). Journal of the Lepidopterists’ Society, 43 (3), 247–249.

    Holdridge L.R. (1967) Life zone ecology. Tropical Science Center, Costa Rica, 206 p.

    Horvitz, C.C., Turnbull, C. & Harvey, D.J. (1987) Biology of immature Eurybia elvina (Lepidoptera: Riodinidae), a myrmecophilous metalmark butterfly. Annals of the Entomological Society of America, 80 (4), 513–519.

    Huang, C.L. & Hsu, Y.F. (2016) Immature biology of Neptis hesione podarces (Lepidoptera: Nymphalidae) in Taiwan, with discussion on its frass chain function. Annals of the Entomological Society of America, 109 (3), 357–365.

    Janzen, D.H. & Hallwachs, W. (2018) Dynamic database for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of Area de Conservacion Guanacaste (ACG), northwestern Costa Rica. Available from: (accessed 26 April 2018)

    Jolivet, P., Vasconcellos-Neto J. & Weinstein, P. (1990) Cycloalexy: a new concept in the larval defense of insects. Insecta Mundi, 4, 133–141.

    Johnson, K. (1986) A new species of Tmolus (Lycaenidae) with notes on the Euptychia westwoodi (Satyridae) mimicry complex. Bulletin of the Allyn Museum, 106, 1–11.

    Kaminski, L.A. (2008) Immature stages of Caria plutargus (Lepidoptera: Riodinidae), with discussion on the behavioral and morphological defensive traits in nonmyrmecophilous riodinid butterflies. Annals of the Entomological Society of America, 101, 906–914.

    Kaminski, L.A. & Rodrigues, D. (2011) Species-specific levels of ant attendance mediate performance costs in a facultative myrmecophilous. Physiological Entomology, 36, 208–214.

    Kaminski, L.A., Rodrigues, D. & Freitas, A.V.L. (2012) Immature stages of Parrhasius polibetes (Lepidoptera: Lycaenidae): host plants, tending ants, natural enemies, and morphology. Journal of Natural History, 46, 645–667.

    Kaminski, L.A., Mota, L.M., Freitas, A.V.L. & Moreira, G.R.P. (2013) Two ways to be a myrmecophilous butterfly: natural history and comparative immature-stage morphology of two species of Theope (Lepidoptera: Riodinidae). Biological Journal of the Linnean Society, 108, 844–870.

    Kaminski, L.A., Soares, G.R., Seraphim, N., Wahlberg, N., Marini-Filho, O.J. & Freitas, A.V.L. (2015) Natural history and systematic position of Rhetus belphegor (n. comb.) (Lepidoptera: Riodinidae), an endangered butterfly with narrow distribution in Southeast Brazil. Journal of Insect Conservation, 19, 1141–1151.

    Kaminski, L.A., Callaghan, C.J., Seraphim, N., Magaldi, L.M., Volkmann, L. & & Freitas, A.V.L. (2017) Sertania gen. nov., a new genus of butterflies (Lepidoptera: Riodinidae) from the South American dry diagonal. Zootaxa, 4312 (1), 165–179.

    Lehtonen, J. & Jaatinen, K. (2016) Safety in numbers: the dilution effect and other drivers of group life in the face of danger. Behavioral Ecology and Sociobiology, 70 (4), 449–58.

    Lopes, S., von Poser, G.L., Kerber, V.A., Farias, F.M., Konrath, E.L., Moreno, P.R.H., Sobral, M., Zuanazzi, J.A. & Henriques, A.T. (2004) Taxonomic significance of alkaloids and iridoid glucosides in the tribe Psychotrieae (Rubiaceae). Biochemical Systematics and Ecology, 32, 1187–1195.

    Mallet, J. & Longino, J.T. (1982) Hostplant records and descriptions of juvenile stages for two rare species of Eueides (Nymphalidae). Journal of the Lepidopterists’ Society, 36, 136–142.

    Matsuura, H.N., Porto, D.D. & Fett-Neto, G.A. (2013) Bioactive alkaloids from South American Psychotria and related Rubiaceae. In: Ramawat, K. & Mérillon, J.M. (Eds.), Natural Products. Springer, Berlin and Heidelberg, pp. 119–47.

    Mosher E. 1916. A classification of the Lepidoptera based on characters of the pupa. Bulletin of the Illinois State Laboratory of Natural History, 12, 17–159.

    Mota, L.L., Silva, A.K., Freitas, A.V.L. & Kaminski, L.A. (2016) Immature stages of Archonias brassolis tereas (Godart) (Pieridae: Pierini), with notes on interspecific interactions between mistletoe butterflies. Journal of the Lepidopterists' Society, 70, 289–294.

    Nielsen, G.J. & Salazar, J.A. (2014) On the presence of certain rare species of Riodinidae (Lepidoptera: Papilionoidea) in a forest fragment on the eastern slope of the Colombian cordillera oriental and a new regional list. Boletín científico. Centro de Museus: Museo de Historia Natural. Universidad de Caldas, 18, 203–226.

    Nishida, K. (2010) Description of the immature stages and life history of Euselasia (Lepidoptera: Riodinidae) on Miconia (Melastomataceae) in Costa Rica. Zootaxa, 2466, 1–74.

    Perry, M. (2006) Comparative evolution and development of the butterfly eyespot and a survey of wing pattern gene expression across butterfly families. MSc Dissertation, University of Florida, Gainesville, FL, 54 pp.

    Peterson, A. (1962) Larvae of Insects: An Introduction to Nearctic Species. Lepidoptera and plant infesting Hymenoptera. Part 1. Ohio State University, Columbus, Ohio, 315 pp.

    Pierce, N.E. (1984) Amplified species diversity: a case study of an Australian lycaenid butterfly and its attendant ants. In: Wane-Wright, R.I. & Ackery, P.R. (Ed.), The biology of butterflies, Symposium of the Royal Entomological Society of London Number 11. Academic Press, London, pp. 197–200.

    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, 733–771.

    Salazar, J.A., Rodríguez, G. & Constantino, L. (2009). Contribución al conocimiento del género Mesosemia Hübner [1819] en Colombia y descripción de nuevos taxa (Lepidoptera: Riodinidae). Boletín científico. Centro de Museus: Museo de Historia Natural. Universidad de Caldas, 13 (2), 174–240.

    Seraphim, N. (2018) Riodinidae Species Checklist: a preliminary species cheklist for the Riodinidae. Available from: (accessed 15 June 2018)

    Seraphim, N., Kaminski, L.A., DeVries, P.J., Penz, C.M., Callaghan, C.J., Wahlberg, N., Silva-Brandão, K.L. & Freitas, A.V.L. (2018) Molecular phylogeny and higher systematics of metalmark butterflies (Lepidoptera: Riodinidae). Systematic Entomology, 43, 407–425.

    Sillén-Tullberg, B. (1988) Evolution of gregariousness in aposematic butterfly larvae: a phylogenetic analysis. Evolution, 42(2), 293–305.

    Singer, M.C., Ehrlich, P.R. & Gilbert, L.E. (1971) Butterfly feeding on lycopsid. Science, 172, 1341–1342.

    Soto-Sobenis, A., Castillo, B., Delgado, A., González, A. & Montenegro, R. (2001) Alkaloid screening of herbarium samples of Rubiaceae from Panama. Pharmaceutical Biology, 39, 161–169.

    Stichel, H.F.E.J. (1923) Beiträge zur Kenntnis der Riodinidenfauna Südamerikas. III: Minas Geraes. Zeitschrift für wissenschaftliche Insektenbiologie, 18 (1/2), 1–9.

    Stehr, F.W. (1987) Order Lepidoptera. In: Stehr, F.W. (Ed.), Immature Insects.Vol. 1. Kendall-Hunt Publishing Company, Dubuque, IA, pp. 288–305.

    Travassos, M.A., DeVries, D.J. & Pierce, N.E. (2008) A novel organ and mechanism for larval sound production in butterfly caterpillars: Eurybia elvina (Lepidoptera: Riodinidae). Tropical Lepidoptera Research, 18 (1), 20–23.

    Valencia, M.C.A., Gil, P.Z.N. & Constantino, L.M. (2005) Mariposas diurnas de la Zona Cafetera Central Colombiana. Guia de campo. Cenicafé, Chinchiná, Colombia, 244 pp.

    Vane-Wright, R.I. (1978) Ecological and behavioural origins of diversity in butterflies. In: Mound, L.A. & Waloff, N. (Eds.), Diversity of Insect Faunas. Symposia of the Royal Entomological Society of London. No. 9. Blackwell Scientific, Oxford, pp. 56–70.

    Vélez-Arango, A. M., Vélez, P. & Wolff, M. (2010) The life cycle of Mesosemia mevania (Hewitson 1857) (Riodinidae) in a lower montane humid forest in Colombia. Journal of the Lepidopterists’ Society, 64 (1), 23–28.

    Willmott, K.R. & Freitas, A.V.L. (2006) Higher-level phylogeny of the Ithomiinae (Lepidoptera: Nymphalidae): classification, patterns of larval hostplant colonisation and diversification. Cladistics, 22, 297–368.

    Willmott, K.R., Elias, M. & Sourakov, A. (2011) Two possible caterpillar mimicry complexes in Neotropical Danaine butterflies (Lepidoptera: Nymphalidae). Annals of the Entomological Society of America, 104 (6), 1108–1118.

    Zanuncio, J.C., Soares, M.A., Zanuncio, T.V., Mielke, O.H.H., Ramalho, F.D., de Assis, S.L. & Wilcken, C.F. (2013b) Euselasia hygenius occulta (Riodininae): first report of feeding on Psidium guajava (Myrtaceae) in Minas Gerais State, Brazil. Journal of the Lepidopterists’ Society, 67, 221–224.

    Zikán, J.F. (1952) Beschreibung neuer Lepidopteren-Arten, Rassen und Varietäten aus Brasilien nebst kritischen Bemerkungen zu bereits bekannten. Dusenia, Curitiba, 3 (1), 11–50.

    Zikán, J.F. (1953) Beiträge zur Biologie von 19 Riodiniden-Arten (Riodinidae - Lepidoptera). Dusenia, Curitiba, 4 (5/6), 403–413.