Partnerships for enhanced engagement in research (PEER) Cycle 4 (2015 Deadline)
Mapping and conserving butterfly biodiversity in the Brazilian Amazon
PI: André Freitas (baku@unicamp.br), Universidade Estadual de Campinas (UNICAMP) U.S. Partner: Keith Willmott, University of Florida Project Dates: January 2016 - December 2019
Project Overview
The project team has produced a short video about the new genus Nhambikuara (subtitles in English available)
The Amazon has some of the most diverse biological communities in the world, including butterflies, and recent expeditions by Dr. Freitas and his collaborators have found numerous poorly known or undescribed species. The PI and his team are involved in several projects on butterfly classification and evolution (systematics), but the Amazon is very poorly known in comparison with other regions of Brazil due to its sheer size and difficulties of transport. Given the insufficient knowledge of distribution and biology, conservation of faunas and species is currently not possible for the great majority of butterflies. In this project, the Brazilian research team will collaborate with a National Science Foundation-supported project at the Florida Museum of Natural History on the systematics of euptychiine butterflies, a highly diverse and abundant group in Amazonian forests, to sample new regions, build collections and provide vital capacity for research and conservation of Brazilian Amazonian butterflies. The researchers will compile data from numerous sources, including literature, databases, and specimens in major world museums, to improve our knowledge of Amazonian butterfly distribution. Poorly known groups or those containing species with restricted distributions, which are important both for understanding evolution and for conservation, will be targeted. A major goal of the project is to conduct up to eight expeditions to poorly sampled or unexplored areas of the Brazilian Amazon, including access by boat or light aircraft. Approximately 20,000 specimens will be collected during these expeditions, and these will be processed and databased. Mitochondrial cytochrome C oxidase 1 (COI) genes will be sequenced for some specimens to enable identification of cryptic species, where morphology alone is inconclusive.
Deforestation, exploitation for oil and gas, and climate change all threaten Brazilian Amazon biological communities. Butterflies are used as indicators of biodiversity and ecosystem health, as monitors of climate change, and as key species in biodiversity conservation. Butterfly distribution data therefore have great potential in identifying priority areas for conservation of Amazonian biodiversity, as has been done in many temperate countries. With the Brazilian Amazon playing a vital role in controlling South American and global climate, such data also provide a baseline for measuring future climate change in the region. This project will build capacity for research on Brazilian Amazonian butterflies by training graduate students and a postdoc and by strengthening collaborations among researchers and students in Brazil and with foreign institutions. The project will build substantial collections and online resources for future taxonomic, biogeographic, and conservation research, including enhancing major Brazilian butterfly collections with new material, archiving tissue samples for DNA study, and databasing specimens. The data collected will also be made available online via iDigBio, a major initiative for aggregating specimen data and sharing it with the public.
Final Summary of Project Activities
Now that this project has concluded as of the end of 2019, the PI Dr. Freitas stresses that the financial support provided by PEER has been extremely important in facilitating the collection of new data from some remote, under-sampled regions in the Amazon. In total, he and his team visited 67 localities during the project, gathering data that they will continue to study during the coming years. Based on this material, as of February 2020 they have already published 17 papers describing more than 20 new taxa (species and genera) based on morphological and molecular data. They have achieved a better picture of some processes of diversification in the Amazon region, including the role of the large rivers and hybrid zones. By involving all students on the team in activities related to the project, some nice outreach projects were conceived and developed during the four years. Finally, the project helped to strengthen an existing international collaboration with the U.S. partner and to start a new collaboration. Following are details on the project results in various categories.
DATABASE OF BRAZILIAN AMAZONIAN BUTTERFLIES During the final year of the project in 2019, postdocs Leila T. Shirai and Jessie P. Santos received continued training from NSF-funded collaborator Dr. Keith R. Willmott in the use of a Microsoft Access database developed for recording butterfly specimen data. This relational database contains a table of 17,218 localities, a table of Neotropical butterfly species-group names (28,412 records) based on the Lamas (2004) Neotropical butterfly checklist, and a form for entering new specimen records, with dropdown menus linked to both locality and taxon tables. In addition, Dr. Freitas and his colleagues completed a compilation of records from multiple databases available to them, resulting in 27,332 locality records for 36,203 specimens of Brazilian butterflies (21,854 from Amazonian states), including 752 species from 170 genera.
The team carried out sampling expeditions to Tumucumaque, which often involved early morning travel by river (photo courtesy of Dr. Freitas).
MORPHOLOGICAL RESEARCH During the four years of project, morphological research on key butterfly genera (those containing poorly known and often endemic Amazonian species), contributed to eight research papers (including those published, submitted and in preparation). These research activities were greatly facilitated after Dr. Freitas used PEER funds to acquire a stereomicroscope for his lab. The data gathered will also result in several additional publications, including taxonomic revisions and descriptions of new taxa (genera and species). The main researchers involved in these studies in 2019 included Dr. Mario Marín, Dr. Eduardo P. Barbosa, and Dra. Thamara Zacca, and they were assisted by undergraduate student Julia Ramos and Master’s student Tamara Aguiar.
MOLECULAR RESEARCH The molecular team on the project sequenced DNA for more than 800 specimens during the four years of project. They continue to use the data in their ongoing projects on the systematics and evolution of Neotropical butterflies, with a principal focus on Brazil. The results are partly available in their recently published papers. An ongoing molecular study of Heliconius hermathena, a sand forest specialist, is advancing based on data gathered from eight populations representing five out of the six known subspecies. The first publication describing a new subspecies has been completed, and two additional genomic studies are being carried out, one of them a collaboration with Dr. Marcus Kronforst (University of Chicago). All these studies involve the collaboration of Dra. Karina Silva-Brandão (Center of Molecular Biology - Unicamp).
Mario Marín continued with broad scale sequencing of specimens of Pareuptychia, including several recently collected specimens in Amapá, Roraima, Amazonas and Pará; most of the recently sequenced material comes from field trips supported by the present project. In addition, Mario is now sequencing specimens of Taygetis from several localities in the Amazon to unveil the species complexes in this genus (in collaboration with Keith Willmott). Leila T. Shirai prepared a genetic diversity bank with tissues of most of the 2,300 butterfly specimens collected in the central Amazon (see above). This material will be used in several ongoing projects in Dr. Freitas’s lab, and in particular in a collaborative project between Unicamp, Harvard University, and the University of York, United Kingdom.
TAXONOMIC DESCRIPTIONS During the project, the PI and his group published 17 papers and described more than 20 new taxa, including a new subspecies of Heliconius hermathena from South Pará State, based on morphological and molecular data. Other studies in collaboration with postdocs Thamara Zacca, Eduardo Barbosa, and Mario Marín focused on the poorly known satyrines. These studies included several published and submitted papers, including broad taxonomic revisions of key genera of Satyrinae butterflies with description of several new taxa.
OUTREACH During the four years of project, six students from Unicamp participated as instructors training local people in sampling protocols for residents and future implementers of the program “Biodiversity Monitoring in Conservation Units” in the Cabo Orange National Park, Amapá, during field work in this Conservation Unit in September 2016 and in Tumucumaque National Park in September 2017. With support from the National Geographic Society, the team appeared in a documentary to be released in 2020. They also produced and released several other videos on their YouTube page at https://www.youtube.com/channel/UC6S1BrU3brYzW_XqeESrixg. In addition, during the expedition to Tefé and Iranduba (September-October 2018) a television crew accompanied the team to record a popular Brazilian TV program called “Profissão Reporter.” The objective was to illustrate to the public the challenges faced by researchers in Brazil. Videos from the program are available at: https://globoplay.globo.com/v/7112455/programa/.
PARTICIPATORY MONITORING Dr. Freitas and his colleagues have collaborated in activities of the Brazilian Biodiversity Monitoring Program in several Amazon Conservation Units. In August 2017, they took part in an expedition to Tumucumaque Mountains National Park, a Conservation Unit that is integrated with the Monitoring Program. The Tumucumaque Park did not have any previous records from butterfly surveys, with its butterfly diversity still unknown. Therefore, the team’s expedition aimed to survey across the entire butterfly fauna and develop a species list for Tumucumaque Park (in preparation as of February 2020). Over the course of one week, they collected with entomological nets along the monitoring transects. The local monitoring team provided substantial logistical assistance, as well as reports on their experience of butterfly sampling in the region. Similarly, the researchers helped the monitoring crew with species identification and other relevant information about the butterfly fauna. All images of specimens collected during monitoring events that could not be confidently identified were reviewed and resolved. The biological material brought from this expedition is still in the process of identification, and several undescribed species of Satyrini will be described in future taxonomic publications.
Overall, the data gathered during the four years of the project are now an invaluable source of information for a better knowledge of the Amazon region, especially in areas not previously sampled. In addition, several new taxa have been already described, and some additional new species are being now studied to be described in the near future. The project was also important to strengthen the collaboration of Dr. Freitas and his team with Dr. Keith Willmott of the University of Florida. In 2020 and beyond, they will continue studying the collected material, with some support provided by the Brazilian National Council for Scientific and Technological Development. The PI has also submitted a proposal to the São Paulo Research Foundation (FAPESP) to study the evolution of the Amazonian butterflies. Useful Links:
Short course on the biology of butterflies, July 23-27, 2018 (link to Part 1 of 7 may be found at https://youtu.be/1VhFYINFepY with links to the subsequent sections at the end of the first video)
Doré, M., Willmott, K., Leroy, B., Chazot, N., Mallet, J., Freitas, A. V. L., Hall, J. P. W., Lamas, G., Dasmahapatra, K. K., Fontaine, C., & Elias, M. (2022). Anthropogenic pressures coincide with Neotropical biodiversity hotspots in a flagship butterfly group. Diversity and Distributions, 28, 2912–2930. https://doi.org/10.1111/ddi.13455
Mota, L.L., Boddington, S.J., Brown Jr., K.S., Callaghan, C.J., Carter, G., Carter, W., Dantas, S.M., Dolibaina, D.R., Garwood, K., Hoyer, R.C., Robbins, R.K., Soh, A., Willmott, K.R., Freitas, A.V.L. (2022). The butterflies of Cristalino Lodge, in the Brazilian southern Amazonia: An updated species list with a significant contribution from citizen science. Biota Neotropica 22(3): e20221367. https://doi.org/10.1590/1676-0611-BN-2022-1367
Moraes SS, Murillo-Ramos L, Machado PA, et al. (2021). A double-edged sword: Unrecognized cryptic diversity and taxonomic impediment in Eois (Lepidoptera, Geometridae). Zool Scr. 2021;50:633–646. https://doi.org/10.1111/zsc.12488
Rosser, N., Shirai, L.T., Dasmahapatra, K.K., Mallet, J., and Freitas, A. (2021). The Amazon river is a suture zone for a polyphyletic group of co-mimetic heliconiine butterflies. Ecography 44:177-187. https://doi.org/10.1111/ecog.05282
Zacca, T., Casagrande, M.N., Mielke, O.H.H., Huertas, B., Freitas, A., Marin, M.A., Espeland, M., and Willmott, K.R. (2021). A new euptychiine butterfly species from south Brazil and taxonomic rearrangements for Taydebis Freitas, 2013 and Hermeuptychia Forster, 1964 (Lepidoptera: Nymphalidae: Satyrinae). Zootaxa 5023 (4):555–570. https://doi.org/10.11646/zootaxa.5023.4.5
Moraes SS, Montebello Y, Stanton MA, Yamaguchi LF, Kato MJ, Freitas AVL. (2021). Description of three new species of Geometridae (Lepidoptera) using species delimitation in an integrative taxonomy approach for a cryptic species complex. PeerJ 9:e11304, DOI 10.7717/peerj.11304
Moraes Magaldi, L., Kaminski, L.A., Seraphim, N., Azeredo-Espin, A.M., Lucas Silva-Brandao, K., and Freitas, A.V.L. (2021). Hidden in the wing dots: Disentangling mimetic sister species of butterflies (Riodinidae: Stalachtis) with an integrative approach. Zoologischer Anzeiger 294 (2021) 92-99. https://doi.org/10.1016/j.jcz.2021.07.009
Matos-Maravi, P., Wahlberg, N., Freitas, A.V.L., Devries, P., Antonelli, A., and Penz, C.M. (2021). Mesoamerica is a cradle and the Atlantic Forest is a museum of Neotropical butterfly diversity: insights from the evolution and biogeography of Brassolini (Lepidoptera: Nymphalidae). Biological Journal of the Linnean Society, 2021, 133, 704–724. https://doi.org/10.1093/biolinnean/blab034
Gueratto, P.E., Machado, P.A., Aguiar, T.M.C., Barbosa, E.P., Dias, F.M.S., Oliveira-Neto, J.F., Casagrande, M.M., and Freitas, A.V.L. (2020). Identifying Memphis: A comprehensive and comparative description of the immature stages and natural history of Memphis acidalia victoria (H. Druce, 1877) (Lepidoptera: Nymphalidae). Austral Entomology, 59:127– 141. https://doi.org/10.1111/aen.12431
Zacca, T., Casagrande, M.M., Mielke, O.H.H., Huertas, B., Espeland, M., Freitas, A.V.L., Willmott, K.R., Nakahara, S., and Lamas, G. (2020). Revalidation of Vareuptychia Forster, 1964, description of Vanima gen. nov., and notes on Euptychia cleophes Godman & Salvin, 1889 (Lepidoptera: Nymphalidae:Satyrinae). Zootaxa 4858 (1): 001-34. https://doi.org/10.11646/zootaxa.4858.1.1
Zacca, T., Casagrande, M.M., Mielke, O.H.H., Huertas, B., Barbosa, E.P., Freitas, A.V.L., and Willmott, K.R. (2020). Description of Emeryus Zacca, Mielke & Casagrande gen. nov. (Lepidoptera: Nymphalidae) to accommodate three species formerly placed in Paryphthimoides Forster, 1964. Austral Entomology (2020) 59, 505–523. https://doi.org/10.1111/aen.12479
Mota, L.Ll, Kaminski, L.A., and Freitas, A.V.L. (2020). The tortoise caterpillar: carnivory and armoured larval morphology of the metalmark butterfly Pachythone xanthe (Lepidoptera: Riodinidae), Journal of Natural History, 54:5-6, 309-319. https://doi.org/10.1080/00222933.2020.1759720
Massardo, D., VanKuren, N.W., Nallu, S. et al. (2020). The roles of hybridization and habitat fragmentation in the evolution of Brazil’s enigmatic longwing butterflies, Heliconius nattereri and H. hermathena. BMC Biol 18, 84. https://doi.org/10.1186/s12915-020-00797-1
Willmott, K.R., Marin, M.A., Nakahara, S., Pomerantz, T., Lamas, G., Huertas, B., Espeland, M., Xiao, L., Hall, J.P.W., Robinson Willmott, J.I., and Freitas, A.V.L. (2019). A revision of the new Andean butterfly genus Optimandes Marín, Nakahara & Willmott, n. gen., with the description of a new species (Nymphalidae: Satyrinae: Euptychiina). Trop. Lepid. Res., 29(1): 29-44. htpps://doi.org/10.5281/zenodo.2650482
Freitas, A.V.L., Ramos, R.R., Silva-Brandão, K.L. et al. (2019). A New Subspecies of Heliconius hermathena (Nymphalidae: Heliconiinae) from Southern Amazonia. Neotrop Entomol 48, 467–475. https://doi.org/10.1007/s13744-018-0658-8
Rosser, N., Freitas, A.V.L., Huertas, B., Joron, M., Lamas, G., Mérot, C., Simpson, F., Willmott, K.R., Mallet, J., and Dasmahapatra, K.K. (2019). Cryptic speciation associated with geographic and ecological divergence in two Amazonian Heliconius butterflies. Zoological Journal of the Linnean Society, Volume 186, Issue 1, May 2019, 233–249. https://doi.org/10.1093/zoolinnean/zly046
Dias, F.M.S., Siewert, R.R., Freitas, A.V.L., Lamas, G., Magaldi, L.M., Mielke, O.H.H. and Casagrande, M.M. (2019). An integrative approach elucidates the systematics of Sea Hayward and Cybdelis Boisduval (Lepidoptera: Nymphalidae: Biblidinae). Syst Entomol, 44: 226-250. https://doi.org/10.1111/syen.12327
Zacca, T., Casagrande, M., Mielke, O., Huertas, B., Barbosa, E., Freitas, A., Magaldi, L., Espeland, M., Nakahara, S., and Willmott, K. (2018). Systematics of the butterfly genus Cissia Doubleday, 1848 (Lepidoptera: Nymphalidae: Satyrinae) using an integrative approach. Arthropod Systematics and Phylogeny 76(2):349-376.
Seraphim, N., Kaminski, L.A., Devries, P.J., Penz, C., Callaghan, C., Wahlberg, N., Silva-Brandao, K.L. and Freitas, A.V.L. (2018). Molecular phylogeny and higher systematics of the metalmark butterflies (Lepidoptera: Riodinidae). Syst Entomol, 43: 407-425. https://doi.org/10.1111/syen.12282
Freitas, A.V.L., Barbosa, E.P., Zacca, T., Marin, M.A., Beirao, M.V., Silva, A.R.M., Casagrande, M.M., Espeland, M., and Willmott, K. (2018). Before it is too late: description of a new genus and species of butterfly from a highly threatened Brazilian biome. Revista Brasileira de Entomologia 62 (2018) 148–158. https://doi.org/10.1016/j.rbe.2018.02.003
Morin, M., Pena, C., Uribe, S.I., and Freitas, A.L. (2017). Morphology agrees with molecular data: phylogenetic affinities of Euptychiina butterflies (Nymphalidae: Satyrinae). Syst Entomol, 42: 768-785. https://doi.org/10.1111/syen.12245
Seixas, R.R., Santos, S.E., Okada, Y.,, and Freitas, A.V.L. (2017). Population Biology of the Sand Forest Specialist Butterfly Heliconius hermathena hermathena (Hewitson) (Nymphalidae: Heliconiinae) in Central Amazonia). The Journal of the Lepidopterists' Society 71(3), 133-140, (1 September 2017). https://doi.org/10.18473/lepi.71i3.a2
