An up-to-date survey of tropical forest lianas
December 07, 2016
By Noêmia Lopes | Agência FAPESP – The tribe Bignonieae, a large, morphologically diverse grouping of lianas and an important component of tropical forests, has won a privilege rarely granted to Brazil’s rich biodiversity – a complete, up-to-date survey of its 21 genera and 393 species, providing details of morphology, taxonomy, geographic distribution and genetics, as well as data on the tribe’s evolutionary history and biogeography.
This is the outcome of the project “Systematics of the tribe Bignonieae (Bignoniaceae)”, supported by FAPESP. The principal investigator is Lúcia Garcez Lohmann, affiliated with the University of São Paulo’s Bioscience Institute (IB-USP).
“We have some 250 plant families in Brazil, and very few have been surveyed in such detail,” Lohmann told Agência FAPESP. “Systematic surveys are fundamental to an understanding of the processes that led to the formation of our flora as a whole, and to the prioritization of conservation areas, management plans, and sustainable use of biodiversity.”
Lohmann has spent the last 24 years refining the classification of Bignoniaceae, the trumpet creeper or catalpa family of the mint order of flowering plants (Lamiales). The tribe Bignonieae is the largest group in the family and includes the most diverse lineage of tropical forest lianas.
“It’s a very important group,” Lohmann said. “The presence of lianas is precisely what distinguishes Old World forests from Neotropical forests. Because the species of Tribe Bignonieae represent the most diverse and abundant group of lianas in the Neotropics, an understanding of their evolutionary history gives us important information on the origin and diversification of Neotropical forests as a whole. In addition, the species of this tribe are intensively used by indigenous communities for their medicinal properties, so their pharmacological potential is considerable.”
The first step toward a better understanding of the past of certain ecosystems and in a search for new chemical compounds for drug development was to learn exactly how many species of lianas the clade contains, where each one is to be found, how they evolved, and which are their closest relatives.
This survey was the central goal of the study, resulting in the description of ten new species, 190 proposed new nomenclatural combinations, and almost 100 new lectotypes (specimens designated as the type of a species or subspecies on which to base its redescription). Countless taxonomic problems were also resolved.
Thanks to all this new knowledge, Tribe Bignonieae became one of the models used in the Thematic Project “Structure and evolution of the Amazonian biota and its environment: an integrative approach”, for which Lohmann is also principal investigator.
A collaboration between FAPESP’s Research Program on Biodiversity Characterization, Conservation, Restoration & Sustainable Use (BIOTA-FAPESP) and the US National Science Foundation’s Dimensions of Biodiversity Program, the Thematic Project is investigating the origins of biodiversity in the Amazon, where lianas arrived some 40 million years ago – 10 million years after they emerged in the Atlantic Rainforest on Brazil’s eastern seaboard.
According to Lohmann, lineages continued to migrate and diversify, reaching dry areas of the Cerrado (Brazilian savanna) approximately 30 million years ago. Several million years later, they evolved to become trees, losing their tendrils – modifications of leaflets into filaments that spiral up tree trunks toward the forest canopy – and developing seeds with a rounded shape that enabled them to fly through large open areas like frisbees. As time passed, species of Bignonieae continued to spread through the Americas as far as Mexico and the southern United States.
The project has also produced new knowledge in terms of whether occupation of new environments or changes in morphology came first in each case. “We constructed a phylogenetic tree tracing the genealogical history of each species and enabling us to determine when certain characteristics changed,” Lohmann said. “The evolution of characteristics before the occupation of a new area we call a key innovation: a new characteristic enabled the group to occupy a new environment and diversify. Changes that occurred after occupation of a new environment were adaptations.”
From collection to the lab
Throughout the project Lohmann and students she supervised traveled all over Brazil collecting samples in the field and visiting herbariums. Their itinerary included 12 states (Acre, Amazonas, Bahia, Ceará, Espírito Santo, Goiás, Mato Grosso, Minas Gerais, Pará, Paraíba, Piauí and Rio de Janeiro) as well as São Paulo State.
“Some sites we chose because very few lianas had been collected there,” Lohmann explained. “Other sites were known to have lianas, but by collecting more specimens there, we increased the number of reported occurrences and obtained fresh material for DNA extraction and for anatomical and phytochemical analysis.”
In addition to providing information with which to identify a great deal of previously unclassified material, their visits to herbariums enabled the students who were working with Lohmann to network with local undergraduate and graduate students. “Young researchers contacted me throughout the project saying they wanted to study the flora of their region in more depth. Now, I’m supervising students and partnering with academics in several Brazilian states,” Lohmann said. “Interaction is mutual with students from São Paulo, who were always made very welcome at all the institutions we visited.”
They also visited other countries, including Austria, Belgium, France, Germany, Russia, Spain, Sweden, the UK and the US. There, they perused classical collections and a large amount of type material required for taxonomic revisions.
The material amassed in all these visits and field trips was analyzed at a transition point. Earlier in the project, in 2012, genetic sequencing was performed using the Sanger method, using only a few molecular markers. The original proposition, therefore, was to sequence three markers for multiple individuals from all species of Tribe Bignonieae. “However, in mid-project, we had the opportunity to use next-generation sequencing, which is high throughput and can sequence entire genomes,” Lohmann said. “So we were able to reconstruct relationships between genera and species with a far higher level of confidence.”
Given its vast scope, many students took part in the project, with the support of FAPESP scholarships ranging from scientific initiation to postdoc: Alexandre Rizzo Zuntini, Alison Nazareno, Annelise Frazão Nunes, Beatriz Machado Gomes, Eric Yasuo Kataoka, Fabiana Firetti Leggieri, Jéssica Nayara Carvalho Francisco, Luiz Henrique Fonseca, Maila Beyer, Maria Claudia Medeiros, Maria Fernanda Calió, Miriam Kaehler (PhD and postdoc) and Verônica Thode.
“We all used the same methodology and conducted the research in a standardized manner, enabling us to assemble a large database full of photographs and information on the morphology, geographic distribution and genetics of the species studied. We’re also pursuing the best way to make the data and images available on the internet,” Lohmann said.
Another planned outcome is an understanding of how the tribe will react to climate change. On this topic, Lohmann is supervising the PhD research of Juan Pablo Narváez Gómez, a Colombian student. “The goal is to find the areas with the greatest diversity and endemism of species in Tribe Bignonieae, model species distribution using current and future scenarios, and propose conservation strategies on that basis,” Lohmann said.
The project “Systematics of the tribe Bignonieae (Bignoniaceae)” has so far resulted in the 18 scientific articles listed below, besides five others submitted for publication:
Iamonico, D., E. Banfi, G. Galasso, L.G. Lohmann, J.A. Lombardi & N.M.G. Ardenghi. 2015. Typification of the Linnaean name Bignonia peruviana (Vitaceae). Phytotaxa 236(3): 283-286. http://biotaxa.org/Phytotaxa/article/view/phytotaxa.236.3.10
Fonseca, L.H.M.F. & L.G. Lohmann. 2015. Biogeography and evolution of Dolichandra (Bignonieae, Bignoniaceae). Botanical Journal of the Linnean Society 179: 403-420. http://onlinelibrary.wiley.com/doi/10.1111/boj.12338/abstract
Nazareno, A.G., M. Carlsen & L.G. Lohmann. 2015. Complete chloroplast genome of Tanaecium tetraganolobum: The first Bignoniaceae plastome. PLOS One 10(6): e0129930. http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0129930
Zuntini, A.R., C.M. Taylor & L.G. Lohmann. 2015. Problematic specimens turn out to be two undescribed species of Bignonia (Bignoniaceae). Phytokeys 56: 7-18. http://phytokeys.pensoft.net/articles.php?id=5423
Zuntini, A.R., C.M. Taylor & L.G. Lohmann. 2015. Deciphering the Neotropical Bignonia binata species complex (Bignoniaceae). Phytotaxa 219(1): 69-77. http://biotaxa.org/Phytotaxa/article/view/phytotaxa.219.1.5
Firetti-Leggieri, F. D. Demarco & L.G. Lohmann. 2015. A new species of Anemopaegma (Bignonieae, Bignoniaceae) from the Atlantic Forest of Brasil. Phytotaxa 219(2): 174-182. http://biotaxa.org/Phytotaxa/article/view/phytotaxa.219.2.7
Fonseca, L.H.M.F., S.M. Cabral, M.F. Agra & L.G. Lohmann. 2015. Taxonomic updates in Dolichandra (Bignonieae, Bignoniaceae). Phytokeys 46: 35-43. http://phytokeys.pensoft.net/articles.php?id=4671
Medeiros, M.C.M.P., A. Guisan & L.G. Lohmann. 2015. Climate niche conservatism does not explain restricted distribution patterns in Tynanthus (Bignonieae, Bignoniaceae). Bot. J. Linn. Soc. 179: 95-109. http://onlinelibrary.wiley.com/doi/10.1111/boj.12300/abstract
Medeiros, M.C.P. & L.G. Lohmann. Taxonomic revision of Tynanthus (Bignonieae, Bignoniaceae). Phytotaxa 216(1): 1-60. http://biotaxa.org/Phytotaxa/article/view/phytotaxa.216.1.1
Medeiros, M.C.P. & L.G. Lohmann. 2015. Phylogeny and biogeography of Tynanthus Miers (Bignonieae, Bignoniaceae). Molecular Phylogenetics and Evolution 85: 32-40. https://www.ncbi.nlm.nih.gov/pubmed/25659336
Medeiros, M.C.P. & L.G. Lohmann. 2014. Two new species of Tynanthus Miers (Bignonieae, Bignoniaceae) from Brazil. Phytokeys 42: 77-85. http://phytokeys.pensoft.net/articles.php?id=4192
Lohmann, L.G & C.M. Taylor. 2014. A new generic classification of Tribe Bignonieae (Bignoniaceae). Annals of the Missouri Botanical Garden 99(3): 348-489. http://www.bioone.org/doi/abs/10.3417/2003187
Zuntini, A.R., C.M. Taylor & L.G. Lohmann. 2014. Proposal to conserve the name Bignonia magnifica (Bignoniaceae) with a conserved type. Taxon 63(6): 1376-1377. http://www.ingentaconnect.com/contentone/iapt/tax/2014/00000063/00000006/art00025
Zuntini, A.R. & L.G. Lohmann. 2014. Synopsis of Martinella Baill. (Bignonieae, Bignoniacee), with the description of a new species from the Atlantic Forest of Brazil. Phytokeys 37: 15-24. http://phytokeys.pensoft.net/articles.php?id=1526
Firetti-Leggieri, F., L.G. Lohmann, J. Semir, D. Demarco & M.M. Castro. 2014. Using leaf anatomy to solve taxonomic problems within the Anemopaegma arvense species complex (Bignonieae, Bignoniaceae). Nordic Journal of Botany 32: 620-631. http://onlinelibrary.wiley.com/doi/10.1111/j.1756-1051.2013.00275.x/pdf
Zuntini, A.R., L.H.M. Fonseca & L.G. Lohmann. 2013. Primers for phylogeny reconstruction in Bignonieae (Bignoniaceae) using herbarium samples. Applications in Plant Sciences 1(9): 1300018. https://www.ncbi.nlm.nih.gov/pubmed/25202586
Lohmann, L.G., C. Bell, M.F. Calió, and R.C. Winkworth. 2013. Pattern and timing of biogeographical history in the neotropical Tribe Bignonieae (Bignoniaceae). Botanical Journal of the Linnean Society 171: 154-170. http://onlinelibrary.wiley.com/doi/10.1111/j.1095-8339.2012.01311.x/abstract
Kaehler, M., F. Michelangeli & L.G. Lohmann. 2012. Phylogeny of Lundia based on ndhF and PepC sequences. Taxon 61(2): 368-380. http://www.ingentaconnect.com/content/iapt/tax/2012/00000061/00000002/art00008
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