Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

What happens to the traditional taxonomy when a well-known tropical saturniid moth fauna is DNA barcoded?

Daniel H. Janzen A I , Winnie Hallwachs A , Donald J. Harvey B , Karolyn Darrow B , Rodolphe Rougerie C , Mehrdad Hajibabaei D , M. Alex Smith D , Claudia Bertrand D , Isidro Chacon Gamboa E , Bernardo Espinoza E , J. Bolling Sullivan F , Thibaud Decaens C , Daniel Herbin G , Luis Felipe Chavarria H , Ruth Franco H , Hazel Cambronero H , Sergio Rios H , Freddy Quesada H , Guillermo Pereira H , Johan Vargas H , Adrian Guadamuz H , Roberto Espinoza H , Jorge Hernandez H , Lucia Rios H , Elieth Cantillano H , Roster Moraga H , Calixto Moraga H , Petrona Rios H , Manuel Rios H , Ricardo Calero H , Dinia Martinez H , Duvalier Briceño H , Minor Carmona H , Edwin Apu H , Keiner Aragon H , Cirilo Umaña H , Jose Perez H , Ana Cordoba H , Pablo Umaña H , Gloria Sihezar H , Osvaldo Espinoza H , Carolina Cano H , Elda Araya H , Dunia Garcia H , Harry Ramirez H , Manuel Pereira H , Jose Cortez H , Mariano Pereira H , Waldy Medina H and Paul D. N. Hebert D

A Department of Biology, University of Pennsylvania, Philadelphia, PA 19104, USA.

B Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560-0105, USA.

C Laboratoire ECODIV, Université de Rouen, Batiment IRESE A, Place Emile Blondel, F-76821, Mont Saint Aignan Cedex, France.

D Biodiversity Institute of Ontario, Department of Integrative Biology, University of Guelph, Guelph, Ontario, Canada N1G 2W1.

E INBio, Apartado Postal 22-3100, Domingo de Heredia, Costa Rica.

F 200 Craven Street, Beaufort, NC 28516, USA.

G 7 Lot Clos Lutche, F-31380 GARIDECH, France.

H Area de Conservacion Guanacaste, Apdo. 169-5000, Liberia, Costa Rica.

I Corresponding author. Email: djanzen@sas.upenn.edu

Invertebrate Systematics 26(6) 478-505 http://dx.doi.org/10.1071/IS12038
Submitted: 8 May 2012  Accepted: 22 September 2012   Published: 19 December 2012

Abstract

Biodiversity of tropical Saturniidae, as measured through traditionally described and catalogued species, strongly risks pooling cryptic species under one name. We examined the DNA barcodes, morphology, habitus and ecology of 32 ‘well known’ species of dry forest saturniid moths from Area de Conservacion Guanacaste (ACG) in north-western Costa Rica and found that they contain as many as 49 biological entities that are probably separate species. The most prominent splitting of traditional species – Eacles imperialis, Automeris zugana, Automeris tridens, Othorene verana, Hylesia dalina, Dirphia avia, Syssphinx molina, Syssphinx colla, and Syssphinx quadrilineata – is where one species was believed to breed in dry forest and rain forest, but is found to be two biological entities variously distinguishable by DNA barcodes and morphology, habitus, and/or microecological distribution. This implies that ‘standard’ biological information about each traditional species may be an unconscious mix of interspecific information, and begs renewed DNA barcoding, closer attention to so-called intraspecific variation, and increased museum collection and curation of specimens from more individual and ecologically characterised sites – as well as eventually more species descriptions. Simultaneously, this inclusion of sibling species as individual entities in biodiversity studies, rather than pooled under one traditional name, reduces the degree of ecological and evolutionary generalisation perceived by the observer.


References

Bernays, E. A., and Janzen, D. H. (1988). Saturniid and sphingid caterpillars: two ways to eat leaves. Ecology 69, 1153–1160.
Saturniid and sphingid caterpillars: two ways to eat leaves.CrossRef | open url image1

Brechlin, R., and Meister, F. (2008). Neue Arten der Gattung Ptiloscola Michener, 1949 (Lepidoptera: Saturniidae). Entomo-Satsphingia 1, 21–26. open url image1

Brechlin, R., and Meister, F. (2011a). Vier neue Taxa der Gattung Eacles Hubner, 1819 [“1816”] (Lepidoptera: Saturniidae). Entomo-Satsphingia 4, 94–99. open url image1

Brechlin, R., and Meister, F. (2011b). Funfzig neue Ceratocampinae (Lepidoptera: Saturniidae). Entomo-Satsphingia 4, 5–58. open url image1

Brechlin, R., and Meister, F. (2011c). Neue Taxa der Gattung Automeris Hubner, [1819] (Lepidoptera: Saturniidae). Entomo-Satsphingia 4, 5–89. open url image1

Brechlin, R., and Meister, F. (2011d). Neue Arten der Gattung Dirphia Hubner, 1819 (“1816”) (Lepidoptera: Saturniidae). Entomo-Satsphingia 4, 5–29. open url image1

Burns, J. M., Janzen, D. H., Hajibabaei, M., Hallwachs, W., and 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. open url image1

Burns, J. M., Janzen, D. H., Hajibabaei, M., Hallwachs, W., and Hebert, P. D. N. (2008). DNA barcodes and cryptic species of skipper butterflies in the genus Perichares in Area de Conservación Guanacaste, Costa Rica. Proceedings of the National Academy of Sciences of the United States of America 105, 6350–6355.
DNA barcodes and cryptic species of skipper butterflies in the genus Perichares in Area de Conservación Guanacaste, Costa Rica.CrossRef | 1:CAS:528:DC%2BD1cXlsFyhtLY%3D&md5=f8e56846152c0c4b83f5d6fbaa224e08CAS | open url image1

Burns, J. M., Janzen, D. H., Hallwachs, W., Hajibabaei, M., and Hebert, P. D. N. (2009). Genitalia, DNA barcodes, and life histories synonymize Telles with Thracides – a genus in which Telles arcalaus looks out of place (Hesperiidae: Hesperiinae). Journal of the Lepidopterists’ Society 63, 141–153. open url image1

Burns, J. M., Janzen, D. H., Hallwachs, W., Hajibabaei, M., and Hebert, P. D. N. (2010). Genitalia, DNA barcodes, larval habitus, and foodplants place the mimetic species Neoxeniades molion in Rhinthon (Hesperiidae: Hesperiinae). Journal of the Lepidopterists’ Society 64, 69–78. open url image1

Costa, J. T., Gotzek, D. A., and Janzen, D. H. (2003). Late-instar shift in foraging strategy and trail pheromone use by caterpillars of the neotropical moth Arsenura armida (Cramer) (Saturniidae: Arsenurinae). Journal of the Lepidopterists’ Society 57, 220–229. open url image1

D’Abrera, B. (1998). ‘Saturniidae Mundi. Saturniid Moths of the World. Part 3.’ (Goecke & Evers: Keltern, Germany, and Hill House: Melbourne & London.)

Hajibabaei, M., deWaard, J. R., Ivanova, N. V., Ratnasingham, S., Dooh, R. T., Kirk, S. L., Mackie, P. M., and Hebert, P. D. N. (2005). Critical factors for assembling a high volume of DNA barcodes. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 1959–1967.
Critical factors for assembling a high volume of DNA barcodes.CrossRef | 1:CAS:528:DC%2BD2MXhtlSjsrbE&md5=c3225e33fb170df0244e088aa8791414CAS | open url image1

Hajibabaei, M., Janzen, D. H., Burns, J. M., Hallwachs, W., and Hebert, P. D. N. (2006). DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 103, 968–971.
DNA barcodes distinguish species of tropical Lepidoptera.CrossRef | open url image1

Hausmann, A., Haszprunar, G., and Hebert, P. D. N. (2011). DNA barcoding the geometrid fauna of Bavaria (Lepidoptera): successes, surprises, and questions. PLoS ONE 6, e17134.
DNA barcoding the geometrid fauna of Bavaria (Lepidoptera): successes, surprises, and questions.CrossRef | 1:CAS:528:DC%2BC3MXisFSrs74%3D&md5=81d2a234ff14eb6d8a3f119687d14472CAS | open url image1

Hebert, P. D. N., Cywinska, A., Ball, S. L., and deWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London – B Biological Sciences 270, 313–321.
Biological identifications through DNA barcodes.CrossRef | 1:CAS:528:DC%2BD3sXktVWiu7g%3D&md5=bacde07336013937477a1e8839a85156CAS | open url image1

Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H., and Hallwachs, W. (2004). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101, 14812–14817.
Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator.CrossRef | 1:CAS:528:DC%2BD2cXovVyju7g%3D&md5=0ae4f5812affc4879a365a936524c001CAS | open url image1

Ivanova, N., deWaard, J., and Hebert, P. D. N. (2006). An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6, 998–1002.
An inexpensive, automation-friendly protocol for recovering high-quality DNA.CrossRef | 1:CAS:528:DC%2BD2sXmsl2ksw%3D%3D&md5=61bcb820336b724ae357909d1bde24b1CAS | open url image1

Janzen, D. H. (1982). Guia para la identificación de mariposas nocturnas de la familia Saturniidae del Parque Nacional Santa Rosa, Guanacaste, Costa Rica. Brenesia 19/20, 255–299. open url image1

Janzen, D. H. (1984a). Weather-related color polymorphism of Rothschildia lebeau (Saturniidae). Bulletin of the Entomological Society of America 30, 16–20. open url image1

Janzen, D. H. (1984b). Natural history of Hylesia lineata (Saturniidae: Hemileucinae) in Santa Rosa National Park, Costa Rica. Journal of the Kansas Entomological Society 57, 490–514. open url image1

Janzen, D. H. (1984c). Two ways to be a tropical big moth: Santa Rosa saturniids and sphingids. Oxford Surveys in Evolutionary Biology 1, 85–140. open url image1

Janzen, D. H. (1986). Biogeography of an unexceptional place: what determines the saturniid and sphingid moth fauna of Santa Rosa National Park, Costa Rica, and what does it mean to conservation biology? Brenesia 25/26, 51–87. open url image1

Janzen, D. H. (1987). How moths pass the dry season in a Costa Rican dry forest. Insect Science and Its Application 8, 489–500. open url image1

Janzen, D. H. (1988). Tropical dry forests: the most endangered major tropical ecosystem. In ‘Biodiversity’. (Ed. E. O. Wilson.) pp. 130–137. (National Academy Press: Washington, DC, USA)

Janzen, D. H. (1993). Caterpillar seasonality in a Costa Rican dry forest. In ‘Caterpillars. Ecological and Evolutionary Constraints on Foraging’. (Eds N. E. Stamp and T. M. Casey.) pp. 448–477. (Chapman and Hall: New York.)

Janzen, D. H. (2000). Costa Rica’s Area de Conservación Guanacaste: a long march to survival through non-damaging biodevelopment. Biodiversity 1, 7–20.
Costa Rica’s Area de Conservación Guanacaste: a long march to survival through non-damaging biodevelopment.CrossRef | open url image1

Janzen, D. H. (2002a). Tropical dry forest: Area de Conservación Guanacaste, northwestern Costa Rica. In ‘Handbook of Ecological Restoration. Volume 2. Restoration in Practice’. (Eds M. R. Perrow and A. J. Davy.) pp. 559–583. (Cambridge University Press: Cambridge.)

Janzen, D. H. (2002b). Preface to Lemaire, C. (2002). ‘The Saturniidae of America. Part 4. Hemileucinae’. (Goecke & Evers: Keltern, Germany.)

Janzen, D. H. (2003). How polyphagous are Costa Rican dry forest saturniid caterpillars? In ‘Arthropods of Tropical Forests. Spatio-temporal Dynamics and Resource Use in the Canopy’. (Eds Y. Basset, V. Novotny, S. E. Miller and R. L. Kitching.) pp. 369–379. (Cambridge University Press: Cambridge.)

Janzen, D. H., and Gauld, I. D. (1997). Patterns of use of large moth caterpillars (Lepidoptera: Saturniidae and Sphingidae) by ichneumonid parasitoids (Hymenoptera) in Costa Rican dry forest. In ‘Forests and Insects’. (Eds A. D. Watt, N. E. Stork and M. D. Hunter.) pp. 251–271. (Chapman & Hall: London.)

Janzen, D. H., and Hallwachs, W. (2011). Joining inventory by parataxonomists with DNA barcoding of a large complex tropical conserved wildland in northwestern Costa Rica. PLoS ONE 6, e18123.
Joining inventory by parataxonomists with DNA barcoding of a large complex tropical conserved wildland in northwestern Costa Rica.CrossRef | 1:CAS:528:DC%2BC3MXhtFKmsL3J&md5=d70c478d83a7fb040e3d9312c7377311CAS | open url image1

Janzen, D. H., and Hallwachs, W. (2012). Philosophy, navigation and use of a dynamic database (“ACG Caterpillars yySRNPxxxx”) for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of Area de Conservacion Guanacaste (ACG), northwestern Costa Rica. Available at: http://janzen.bio.upenn.edu/caterpillars/database.lasso

Janzen, D. H., and Waterman, P. G. (1984). A seasonal census of phenolics, fibre and alkaloids in foliage of forest trees in Costa Rica: some factors influencing their distribution and relation to host selection by Sphingidae and Saturniidae. Biological Journal of the Linnean Society. Linnean Society of London 21, 439–454.
A seasonal census of phenolics, fibre and alkaloids in foliage of forest trees in Costa Rica: some factors influencing their distribution and relation to host selection by Sphingidae and Saturniidae.CrossRef | open url image1

Janzen, D. H., Hajibabaei, M., Burns, J. M., Hallwachs, W., Remigio, E., and Hebert, P. D. N. (2005). Wedding biodiversity inventory of a large and complex Lepidoptera fauna with DNA barcoding. Philosophical Transactions of the Royal Society – B Biological Sciences 360, 1835–1845.
Wedding biodiversity inventory of a large and complex Lepidoptera fauna with DNA barcoding.CrossRef | 1:CAS:528:DC%2BD2MXhtlSjsrjI&md5=a3b90d56c68982cfc39d8996d9bd97c7CAS | open url image1

Janzen, D. H., Hallwachs, W., Blandin, P., Burns, J. M., Cadiou, J., Chacon, I., Dapkey, T., Deans, A. R., Epstein, M. E., Espinoza, B., Franclemont, J. G., Haber, W. A., Hajibabaei, M., Hall, J. P. W., Hebert, P. D. N., Gauld, I. D., Harvey, D. J., Hausmann, A., Kitching, I., Lafontaine, D., Landry, J., Lemaire, C., Miller, J. Y., Miller, J. S., Miller, L., Miller, S. E., Montero, J., Munroe, E., Rab Green, S., Ratnasingham, S., Rawlins, J. E., Robbins, R. K., Rodriguez, J. J., Rougerie, R., Sharkey, M. J., Smith, M. A., Solis, M. A., Sullivan, J. B., Thiaucourt, P., Wahl, D. B., Weller, S. J., Whitfield, J. B., Willmott, K. R., Wood, D. M., Woodley, N. E., and Wilson, J. J. (2009). Integration of DNA barcoding into an ongoing inventory of complex tropical biodiversity. Molecular Ecology Resources 9, 1–26.
Integration of DNA barcoding into an ongoing inventory of complex tropical biodiversity.CrossRef | 1:CAS:528:DC%2BD1MXlslOjsb4%3D&md5=b0599c80ef67fa9a139acbb7f2bd9c6aCAS | open url image1

Janzen, D. H., Hallwachs, W., Burns, J. M., Hajibabaei, M., Bertrand, C., and Hebert, P. D. N. (2011). Reading the complex skipper fauna of one tropical place. PLoS ONE 6, e19874.
Reading the complex skipper fauna of one tropical place.CrossRef | 1:CAS:528:DC%2BC3MXhtFKmsL3K&md5=bfa38e7cb95f16169d6d235e8b536a46CAS | open url image1

Lemaire, C. (1978). ‘The Attacidae of America (=Saturniidae). Attacinae.’ (C. Lemaire: 42 Boulevard Victor Hugo, F. 92200, Neuillysur-Seine, France.)

Lemaire, C. (1980). ‘The Attacidae of America (=Saturniidae). Arsenurinae.’ (C. Lemaire: 42 Boulevard Victor Hugo, F. 92200, Neuilly-sur-Seine, France.)

Lemaire, C. (1988). ‘The Saturniidae of America. Ceratocampinae.’ (Museo Nacional de Costa Rica: San Jose, Costa Rica.)

Lemaire, C. (2002). ‘The Saturniidae of America. Part 4. Hemileucinae.’ (Goecke & Evers: Keltern, Germany.)

Pinto-Tomas, A., Uribe-Lorio, L., Blanco, J., Fontecha, G., Rodriguez, C., Mora, M., Janzen, D., Chavarria, F., Diaz, J., and Sittenfeld, A. (2007). Actividades enzimaticas en aislamientos bacterianos de tractos digestivos de larvas y del contenido de pupas de Automeris zugana y Rothschildia lebeau (Lepidoptera: Saturniidae). Revista de Biologia Tropical 55, 401–415. open url image1

Prado, B. R., Pozo, C., Valdez-Moreno, M., and Hebert, P. D. N. (2011). Beyond the colours: discovering hidden diversity in the Nymphalidae of the Yucatan Peninsula in Mexico through DNA barcoding. PLoS ONE 6, e27776.
Beyond the colours: discovering hidden diversity in the Nymphalidae of the Yucatan Peninsula in Mexico through DNA barcoding.CrossRef | 1:CAS:528:DC%2BC3MXhs1ags7fI&md5=933304ea8ffe70a4eb4e1b2e250b2f01CAS | open url image1

Shapiro, A. M. (1984). The genetics of seasonal polyphenism and the evolution of "General Purpose Genotypes" in butterflies. In ‘Population Biology and Evolution’. (Eds K. Woehrmann and V. Loeschke.) pp. 16–30. (Springer-Verlag: Berlin, Germany.)

Smith, M. A., Woodley, N. E., Janzen, D. H., Hallwachs, W., and Hebert, P. D. N. (2006). DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proceedings of the National Academy of Sciences of the United States of America 103, 3657–3662.
DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae).CrossRef | 1:CAS:528:DC%2BD28XivFWju7k%3D&md5=6ca3011e2f91cd90c3a4d3ad6d746dc6CAS | open url image1

Smith, M. A., Wood, D. M., Janzen, D. H., Hallwachs, W., and Hebert, P. D. N. (2007). DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. Proceedings of the National Academy of Sciences of the United States of America 104, 4967–4972.
DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists.CrossRef | 1:CAS:528:DC%2BD2sXjvFKiurw%3D&md5=eda54524b1ef5504ecdc195a37686135CAS | open url image1

Smith, M. A., Rodriguez, J. J., Whitfield, J. B., Deans, A. R., Janzen, D. H., Hallwachs, W., and Hebert, P. D. N. (2008). Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proceedings of the National Academy of Sciences of the United States of America 105, 12359–12364.
Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections.CrossRef | 1:CAS:528:DC%2BD1cXhtVOhtrjN&md5=58ada5b099dc842f18717f0cdc830b03CAS | open url image1

Smith, M. A., Bertrand, C., Crosby, K., Eveleigh, E. S., Fernandez-Triana, J., Fisher, B. L., Gibbs, J., Hajibabaei, M., Hallwachs, W., Hind, K., Hrcek, J., Huang, D.-W., Janda, M., Janzen, D. H., Li, Y., Miller, S. E., Packer, L., Quicke, D., Ratnasingham, S., Rodriguez, J., Rougerie, R., Shaw, M. R., Sheffield, C., Stahlhut, J. K., Steinke, D., Whitfield, J., Wood, M., and Zhou, X. (2012). Wolbachia and DNA barcoding insects: patterns, potenial, and problems. PLoS ONE 7, e36514.
Wolbachia and DNA barcoding insects: patterns, potenial, and problems.CrossRef | 1:CAS:528:DC%2BC38Xntlegtrg%3D&md5=3e2c68efbe02e00be2ccd989579a9158CAS | open url image1



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