Checklist and molecular phylogenetics reveal three taxonomic novelties in Habenaria (Orchidaceae, Orchidoideae) from Chapada dos Veadeiros, Goiás, Brazil

  • João A. N. Batista Universidade Federal de Minas Gerais, Instituto de Ciências Biológicas, Departamento de Botânica https://orcid.org/0000-0003-4640-0942
  • Gabriela Cruz-Lustre Universidade Federal de Minas Gerais, Instituto de Ciências Biológicas, Departamento de Botânica https://orcid.org/0000-0003-0094-2594
  • Aline A. do Vale Secretaria de Educação do Estado de São Paulo, Programa Ensino Integral-Escola Henrique Rocha, Rua José dos Santos Garcia, 2-15-Bairro Nova Bauru, Bauru, 17022-144, São Paulo, Brazil
  • Luciano B. Bianchetti Embrapa Recursos Genéticos e Biotecnologia, Parque Estação Biológica, Final Av. W5 Norte, Brasília, 70770-901, Distrito Federal, Brazil
Keywords: Biodiversity, Cerrado, grasslands, habenariinae, taxonomy

Abstract

A comprehensive checklist of Habenaria from Chapada dos Veadeiros, State of Goiás, was performed alongside morphologic and molecular phylogenetic studies, revealing three new taxa endemic to this region. A total of 61 taxa (59 species and two varieties) of Habenaria are recorded for Chapada dos Veadeiros, representing a two-fold increase compared to previous lists and comprising one of the greatest diversities of the genus in Brazil. Of this total, four taxa are locally endemic. Habenaria cultellifolia, until recently known only from the type collection, was rediscovered in the region after 127 years without records and represents this species’ only known extant population. Three proposed new taxa of Habenaria (H. minuticalcar J.A.N. Bat. & Bianch. sp. nov., H. proiteana J.A.N. Bat., A.A. Vale & Bianch. sp. nov., and H. lavrensis var. xanthodactyla J.A.N. Bat. & Bianch. var. nov.) are corroborated by molecular phylogenetic analyses based on nuclear and plastid markers. They are described, illustrated, tentatively assessed as threatened, and compared to phylogenetically and morphologically related species. Since some areas of this mountain range have not yet been floristically sampled, additional taxonomic novelties and new records are still expected in the future.

References

Bachman S., Moat J., Hill A.W., de la Torre J. & Scott B. 2011. Supporting red list threat assessments with GeoCAT: Geospatial conservation assessment tool. ZooKeys 150: 117–126. https://doi.org/10.3897/zookeys.150.2109

Barbosa Rodrigues J. 1877. Genera et Species Orchidearum Novarum I. C. & H. Fleiuss, Rio de Janeiro.

Barbosa Rodrigues J. 1882. Genera et Species Orchidearum Novarum II. Typographia Nacional, Rio de Janeiro.

Batista J.A.N. & Bianchetti L.B. 2003. Lista atualizada das Orchidaceae do Distrito Federal, Brasil. Acta Botanica Brasilica 17 (2): 183–201. https://doi.org/10.1590/S0102-33062003000200003

Batista J.A.N., Bianchetti L.B., Nogueira R.E., Pellizzaro K.F. & Ferreira F.E. 2004. The genus Habenaria (Orchidaceae) in the Itacolomi state park, Minas Gerais, Brazil. Sitientibus Série Ciências Biológicas 4 (1–2): 25–36.

Batista J.A.N., da Silva J.B.F. & Bianchetti L.B. 2008. The genus Habenaria (Orchidaceae) in the Brazilian Amazon. Brazilian Journal of Botany 31 (1): 105–134. https://doi.org/10.1590/S0100-84042008000100011

Batista J.A.N., Bianchetti L.B., R. González-Tamayo R., Figueroa X.M.C. & Cribb P.J. 2011a. A synopsis of new world Habenaria (Orchidaceae) I. Harvard Papers in Botany 16: 1–47. https://doi.org/10.3100/025.016.0101

Batista J.A.N., Bianchetti L.B., R. González-Tamayo R., Figueroa X.M.C. & Cribb P.J. 2011b. A synopsis of new world Habenaria (Orchidaceae) II. Harvard Papers in Botany 16: 233–273. https://doi.org/10.3100/0.25.016.0202

Batista J.A.N., Borges K.S., Faria M.W., Proite K., Ramalho A.J., Salazar G.A. & van den Berg C. 2013. Molecular phylogenetics of the species-rich genus Habenaria (Orchidaceae) in the New World based on nuclear and plastid DNA sequences. Molecular Phylogenetics and Evolution 67: 95–109. https://doi.org/10.1016/j.ympev.2013.01.008

Batista J.A.N., Proite K., Carvalho B.M., Vale A.A. & Felix L.P. 2014. From Cuba to most of the Neotropic: Habenaria Bicornis (Orchidaceae) is widespread from Mexico to Southeastern Brazil. Lankesteriana 13: 165–184. https://doi.org/10.15517/lank.v13i3.14351

Batista J.A.N., Vale A.A., Carvalho B.M., Proite K., Ramalho A.J., Munhoz A.C.D., van den Berg C. & Bianchetti L.B. 2016. Four new species in Habenaria (Orchidaceae) from the Espinhaço Range, Brazil. Systematic Botany 41: 275–292. https://doi.org/10.1600/036364416X691858

Batista J.A.N., Proite K. & Bianchetti L.B. 2017. Descriptions and phylogenetic relationships of four new species and a new name of Habenaria (Orchidaceae) from the cerrado and campos rupestres of Brazil. Plant Systematics and Evolution 303: 873–899. https://doi.org/10.1007/s00606-017-1415-x

Batista J.A.N., Reis A.F.S., Leite J.L.Jr. & Bianchetti L.B. 2018. Phylogeny and taxonomy of Habenaria leprieurii, H. alpestris and H. sect. Microdactylae (Orchidaceae), with descriptions of two new taxa. Phytotaxa 373: 241–271. https://doi.org/10.11646/phytotaxa.373.4.1

Batista J.A.N., Ferreira V.L., Alves C.I.G. & Stehmann J.R. 2022a. A new species of Habenaria (Orchidaceae, Asparagales) and a checklist of Orchidaceae from limestone outcrops of Brazil. European Journal of Taxonomy 828: 16–44. https://doi.org/10.5852/ejt.2022.828.1855

Batista J.A.N., Lau B.L., Costa I.G.C.M., Massensini Junior A., Mota R.C. & Borba E.L. 2022b. Description of four new species of the Habenaria repens complex (Orchidaceae) from Brazil based on a biosystematic and molecular phylogenetic approach. Systematic Botany 47: 215–231. https://doi.org/10.1600/036364422X16442668423536

Brade A.C. 1951. O Gênero Habenaria (Orchidaceae) no Itatiaia. Rodriguésia 14 (26): 7–21.

Carvalho B.M., Ramalho A.J. & Batista J.A.N. 2013. O gênero Habenaria (Orchidaceae) na Serra da Canastra, Minas Gerais, Brasil. Rodriguésia 64 (2): 223–245. https://doi.org/10.1590/S2175-78602013000200003

Cogniaux A. 1893–1896. Orchidaceae. In: Martius C.F.P., Eichler A.G. & Urban I. (eds) Flora brasiliensis, vol. 3: 1–672. F. Fleischer, München.

Cogniaux A. 1906. Notes sur les orchidées du Brésil et des régions voisines. Bulletin de la Société Royale de Botanique de Belgique 43: 266–350.

Cribb P.J. 2001. Habenaria. In: Pridgeon A.M., Cribb P.J., Chase M.W. & Rasmussen F.N. (eds) Genera orchidacearum, vol. 2, Orchidoideae (part1) : 298–303. Oxford University Press Inc., Oxford.

Cruz-Lustre G., Batista J.A.N., Radins J.A., González A. & Borba E.L. 2020. Morphometric analysis of the Habenaria parviflora complex (Orchidaceae). Plant Systematics and Evolution 306: 37. https://doi.org/10.1007/s00606-020-01634-2

Cruz-Lustre G., Castro C., Borba E.L. & Batista J.A.N. 2022. Phylogenetics and taxonomy of Habenaria sect. Micranthae (Orchidaceae), with the description of an overlooked new species from the Espinhaço mountain range, Eastern Brazil. Systematics and Biodiversity 20 (1): 2030424. https://doi.org/10.1080/14772000.2022.2030424

Doyle J.F. & Doyle J.L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15.

Erixon P., Svennblad B., Britton T. & Oxelman B. 2003. Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. Systematic Biology 52: 665–673. https://doi.org/10.1080/10635150390235485

ESRI (2016) ArcGIS Desktop: Release 10. Environmental Systems Research Institute, Redlands. [Computer software]. https://www.redlands.edu/study/schools-and-centers/css/resources/arcgis-desktop/

Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

Fitch W.M. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Zoology 20: 406–416. https://doi.org/10.1093/sysbio/20.4.406

Flora e Funga do Brasil 2022. Orchidaceae. Jardim Botânico do Rio de Janeiro. Available from https://floradobrasil.jbrj.gov.br/FB11639 [accessed 12 August 2022].

Govaerts R., Nic Lughadha E., Black N., Turner R. & Paton A. 2021. The World Checklist of Vascular Plants, a continuously updated resource for exploring global plant diversity. Scientific Data 8: 215. https://doi.org/10.1038/s41597-021-00997-6

Harder L.D. & Johnson S.D. 2009. Darwin’s beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytologist 183(3): 530–545. https://doi.org/10.1111/j.1469-8137.2009.02914.x

IUCN 2012. IUCN red list categories and criteria version 3.1. Ed. 2. IUCN, Gland, Switzerland and Cambridge, UK. Available from https://www.iucnredlist.org/technical-documents/categories-and-criteria [accessed 9 February 2017].

IUCN 2016. Guidelines for using the IUCN red list categories and criteria version 12. Prepared by the standards and petitions subcommittee. IUCN Species Survival Commission. IUCN, Gland, Switzerland and Cambridge, UK. Available from https://www.iucnredlist.org/documents/RedListGuidelines.pdf [accessed 9 Feb. 2017].

Jin W.-T., Schuiteman A., Chase M.W., Li J.-W., Chung S.-W., Hsu T.-C. & Jin X.-H. 2017. Phylogenetics of subtribe Orchidinae s.l. (Orchidaceae; Orchidoideae) based on seven markers (plastid matK, psaB, rbcL, trnL-F, trnH-psba, and nuclear nrITS, Xdh): implications for generic delimitation. BMC Plant Biology 17: 222. https://doi.org/10.1186/s12870-017-1160-x

Katoh K. & Standley D.M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010

Kränzlin F. 1892. Beitrage zu einer monographie der gattung Habenaria Willd. Botanisch Jahrbücher für Systematik 16: 52–223.

Kränzlin F. 1911. Beitrage zur Orchideenflora Südamerikas. Kongliga Svenska Vetenskapsakademiens Handlingar 46: 1–105.

Kress W.J., Prince L.M. & Williams K.J. 2002. The phylogeny and a new classification of the gingers (Zingiberaceae): evidence from molecular data. American Journal of Botany 89: 1682–1696. https://doi.org/10.3732/ajb.89.10.1682

Lau B.L., Batista J.A.N., Massensini Junior A., Whitten W.M. & Borba E.L. 2021. Unravelling the Habenaria repens (Orchidaceae) complex in Brazil: a biosystematic and molecular phylogenetic approach. Botanical Journal of the Linnean Society 197: 229–248. https://doi.org/10.1093/botlinnean/boab

Lima P.C.A. & Franco J.L.A. 2014. As RPPNs como estratégia para a conservação da biodiversidade: O caso da chapada dos veadeiros. Sociedade & Natureza (Uberlândia) 26 (1): 113–125. https://doi.org/10.1590/1982-451320140108

Lindley J. 1830–1840. The genera and species of Orchidaceous plants. Ridgways, London.

Madeira F., Park Y.M., Lee J., Buso N., Gur T., Madhusoodanan N., Basutkar P., Tivey A.R.N., Potter S.C., Finn R.D. & Lopez R. 2019. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Research 47: W636–W641. https://doi.org/10.1093/nar/gkz268

Mendonça R.C., Filgueiras T.S. & Fagg C.W. 2007. Análise florística da Chapada dos Veadeiros. In: Felfili J.M., Rezende A.V. & Silva-Junior M.C. (eds) Biogeografia do bioma Cerrado: vegetação e solos da Chapada dos Veadeiros: 119–237. Editora da Universidade de Brasília/Finatec, Brasília.

Meneguzzo T.E.C. 2013. 752. Sacoila cerradicola: Orchidaceae. Curtis’s Botanical Magazine 30 (1): 18–27. https://doi.org/10.1111/curt.12013

Menezes L.C. 1992. Encyclia chapadensis. Orchid Digest 56 (3): 133.

Miller M.A., Pfeiffer W. & Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE): 1–8. Gateway Computing, New Orleans. https://doi.org/10.1145/2016741.2016785

Monteiro S.H.N., Selbach-Schnadelbach A., Oliveira R.P. & van den Berg C. 2010. Molecular phylogenetics of Galeandra (Orchidaceae : Catasetinae) based on plastid and nuclear DNA sequences. Systematic Botany 35: 476–486. https://doi.org/10.1600/036364410792495944

Mota R.C. 2006. Orchidaceae na Serra do Caraça, Minas Gerais: Levantamento florístico com ênfase no estudo taxonômico da subfamília Epidendroideae. Masters thesis, Universidade Federal de Minas Gerais, Brazil.

Munhoz C.B.R. & Proença C.E.B. 1998. Composição florística do Município de Alto Paraíso de Goiás na Chapada dos Veadeiros. Boletim do Herbário Ezechias Paulo Heringer 3: 102–150.

Ngugi G., Péchon T., Martos F., Paillere T., Bellstedt D.U. & Bytebier B. 2020. Phylogenetic relationships amongst the African genera of subtribe Orchidinae s.l. (Orchidaceae; Orchideae): Implications for subtribal and generic delimitations. Molecular Phylogenetics and Evolution 153: 106946. https://doi.org/10.1016/j.ympev.2020.106946

Nylander, J.A.A. 2004. MrModeltest v2. Program distributed by the author. Uppsala: Evolutionary Biology Centre, Uppsala University.

Pansarin E.R. 2004. Cleistes pusilla (Orchidaceae): A new species from central Brazil. Kew Bulletin 59 (4): 555–558. https://doi.org/10.2307/4110910

Pedron M., Buzatto C.R., Singer R.B., Batista J.A.N. & Moser A. 2012. Pollination biology of four sympatric species of Habenaria (Orchidaceae: Orchidinae) from southern Brazil. Botanical Journal of the Linnean Society 170: 141–156. https://doi.org/10.1111/j.1095-8339.2012.01285.x

Pedron M., Buzatto C.R., Ramalho A.J., Carvalho B.M., Radins J.A., Singer R.B. & Batista J.A.N. 2014. Molecular phylogenetics and taxonomic revision of Habenaria section Pentadactylae (Orchidaceae, Orchidinae). Botanical Journal of the Linnean Society 175: 47–73. https://doi.org/10.1111/boj.12161

Reichenbach f. H.G. 1847. Orchidiographische Beiträge. Linnaea 19: 369–379.

Reichenbach f. H.G. 1881. VII–Novitiae Orchidaceae Warmingianae. Otia Botanica Hamburgensia 2: 48–65.

Renz J. 1992. The genus Habenaria (Orchidaceae) in the Guianas. Candollea 47: 483–512.

Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MRBAYES 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029

Santos I.S. & Silva M.J. 2019. O gênero Bulbophyllum Thouars (Orchidaceae, Epidendroideae) no Parque Nacional da Chapada dos Veadeiros, Goiás, Brasil. Hoehnea 46: e872018. https://doi.org/10.1590/2236-8906-87/2018

Santos I.S. & Silva M.J. 2020. Epidendrum L. (Orchidaceae, Epidendroideae) no Parque Nacional da Chapada dos Veadeiros, Estado de Goiás, Brasil. Hoehnea 47: e202020. https://doi.org/10.1590/2236-8906-20/2020

Simon M.F. & Proença C. 2000. Phytogeographic patterns of Mimosa (Mimosoideae, Leguminosae) in the Cerrado biome of Brazil: an indicator genus of high-altitude centers of endemism? Biological Conservation 96: 279–296. https://doi.org/10.1016/S0006-3207(00)00085-9

Simpson M.G. 2006. Plant Systematics. Elsevier Academic Press, Burlington, San Diego, and London.

Stace C.A. 1989. Plant taxonomy and biosystematics. 2nd Ed. Edward Arnold, Hodder and Stoughton Limited, London.

Staden R. 1996. The Staden sequence analysis package. Molecular Biotechnology 5: 233–241. https://doi.org/10.1007/BF02900361

Stearn W.T. 1992. Botanical Latin. 4th Ed. Timber Press, Portland, Oregon.

Swofford D.L. 2002. PAUP* Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland.

Thiers B. 2022. [continuously updated] Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available from https://sweetgum.nybg.org/science/ih/ [accessed 12 August 2022].

Toscano de Brito A.L.V. 1995. Orchidaceae. In: Stannard B.L. (ed) Flora of the Pico das Almas, Chapada Diamantina – Bahia, Brazil: 725–767. Royal Botanic Gardens, Kew.

Trovó M. & Echternacht L. 2022. The Paepalanthoideae (Eriocaulaceae) of the Chapada dos Veadeiros National Park, Brazil: taxonomic novelties, identification key, and illustrated list of species. European Journal of Taxonomy 834: 58–93. https://doi.org/10.5852/ejt.2022.834.1899

Vieira T.L & Barros F. 2017. Orchidaceae na Serra do Ouro Branco, Minas Gerais, Brasil. Rodriguésia 68(2): 691–747. https://doi.org/10.1590/2175-7860201768224

Warming E. 1892. Lagoa Santa: Et Bidrag til den biologiske Plantegeografi. Kongelige Danske videnskabernes Selskabs Skrifter, Naturvidenskabeli Mathematisk Afdeling 6: 159–455.

Published
2023-09-15
How to Cite
Batista, J. A. N., Cruz-Lustre, G., do Vale, A. A., & Bianchetti, L. B. (2023). Checklist and molecular phylogenetics reveal three taxonomic novelties in Habenaria (Orchidaceae, Orchidoideae) from Chapada dos Veadeiros, Goiás, Brazil. European Journal of Taxonomy, 891(1), 51-86. https://doi.org/10.5852/ejt.2023.891.2271
Section
Research article