Abstract
Crop wild relatives (CWR) are a key component of the world’s biota since they have the potential to contribute traits for crop improvement. The rich flora of the Brazilian Cerrado harbours a large number of CWR, but little is known about their distribution and conservation status. This study focused on the conservation of cassava (Manihot) wild relatives in the Cerrado. To accomplish this, we performed herbarium and field surveys to assess species conservation status based on geographic distribution, population density estimates, and rates of habitat loss. We found 75 species of Manihot occurring in the Cerrado, including 59 endemics. Among the endemic taxa, 24 are at some level of threat according to IUCN classification (14% Vulnerable, 22% Endangered, 5% Critically endangered), mostly owing to narrow geographic range and habitat loss. Most species are locally abundant, ranging from 55 to 1493 mature individuals per hectare. A quarter of the species recorded have been described over the past 5 years, indicating that the diversity of Manihot in the Cerrado is still underestimated. Areas of high species richness and endemism coincided mostly with Cerrado highlands, particularly in northern Goiás state. Field surveys in 16 reserves indicate that 54% of Cerrado endemics are not represented in these protected areas. We believe that the patterns of distribution and conservation status uncovered here for Manihot are representative of many plant groups that are particularly diverse in high-altitude areas in the Cerrado. This calls for expansion of the network of protected areas to cover a wider range of environments, particularly those with a concentration of rare and endemic species, to ensure the effective in situ conservation of CWR present in the Cerrado flora.
Similar content being viewed by others
References
Allem AC (1989) Four new species of Manihot (Euphorbiaceae) from Brazil. Rev Bras Biol 49:649–662
Allem AC (1994) The origin of Manihot esculenta Crantz (Euphorbiaceae). Genet Res Crop Evol 41:133–150
Amaral AG, Munhoz CB, Walter BMT, Aguirre-Gutiérrez J, Raes N, De Cáceres M (2017) Richness pattern and phytogeography of the Cerrado herb–shrub flora and implications for conservation. J Veg Sci 28:848–858
Brummitt NA, Bachman SP, Griffiths-Lee J, Lutz M, Moat JF, Farjon A, Donaldson JS, Hilton-Taylor C, Meagher TR, Albuquerque S, Aletrari E (2015) Green plants in the red: a baseline global assessment for the IUCN sampled Red List Index for plants. PLoS ONE 10(8):e0135152
Carmo Júnior C, Sodré RC, Silva MJ, Sales MFD (2013) Manihot in Serra Dourada State Park, Goiás, Brazil. Rodriguésia 64:727–746
Carvalho LJCB, Vieira EA, Fialho JF, Souza CRB (2011) A genomic assisted breeding program for cassava to improve nutritional quality and industrial traits of storage root. Crop Breed Appl Biotechnol 11:289–296
Castañeda-Álvarez NP, Khoury CK, Achicanoy HA, Bernau V, Dempewolf H, Eastwood RJ, Guarino L, Harker RH, Jarvis A, Maxted N, Müller JV, Ramirez-Villegas J, Sosa CC, Struik PC, Vincent H, Toll J (2016) Global conservation priorities for crop wild relatives. Nat Plants 2:16022
Cavalcanti TB (2007) Diversidade e distribuição em Diplusodon Pohl (Lythraceae). Fontqueria 55:397–404
Chacón J, Madriñán S, Debouck D, Rodriguez F, Tohme J (2008) Phylogenetic patterns in the genus Manihot (Euphorbiaceae) inferred from analyses of nuclear and chloroplast DNA regions. Mol Phylogen Evol 49:260–267
Cordeiro I, Secco R, Silva MJ, Sodré RC, Martins MLL (2016) Manihot in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB36155. Accessed 15 Dec 2016
Duputié A, Salick J, McKey D (2011) Evolutionary biogeography of Manihot (Euphorbiaceae), a rapidly radiating Neotropical genus restricted to dry environments. J Biogeogr 38:1033–1043
Echternacht L, Trovó M, Oliveira CT, Pirani JR (2011) Areas of endemism in the Espinhaço range in Minas Gerais, Brazil. Flora 206:782–791
Esquinas-Alcázar J (2005) Protecting crop genetic diversity for food security: political, ethical and technical challenges. Nat Rev Genet 6:946–953
Fernandes GW, Coelho MS, Machado RB, Ferreira ME, Aguiar LMS, Dirzo R, Scariot A, Lopes CR (2016) Afforestation of savannas: an impending ecological disaster. Nat Conserv 14:146–151
Françoso RD, Brandão RA, Nogueira CC, Salmona Y, Machado RB, Colli GR (2015) Habitat loss and the effectiveness of protected areas in the Cerrado biodiversity hotspot. Nat Conserv 13:35–40
Françoso RD, Haidar RF, Machado RB (2016) Tree species of South America central savanna: endemism, marginal areas and the relationship with other biomes. Acta Bot Bras 30:78–86
Goodwin ZA, Harris DJ, Filer D, Wood JR, Scotland RW (2015) Widespread mistaken identity in tropical plant collections. Curr Biol 25:R1066–R1067
Hershey C (2008) A global conservation strategy for cassava (Manihot esculenta) and wild Manihot species. Summary of stakeholder deliberations and recommendations prepared for the Global Crop Diversity Trust. http://isa.ciat.cgiar.org/urg/urgweb_folder/files/unitfiles/A%20Global%20Conservation%20Strategy%20for%20Manihot%20%20August%202008-2.pdf. Accessed 15 Oct 2016
Irwin HS, Barneby RC (1982) The American Cassiinae: a synoptical revision of Leguminosae tribe Cassieae subtribe Cassiinae in the New World. Mem NY Bot Gard 35:455–918
IUCN (2014) Guidelines for Using the IUCN Red List Categories and Criteria. Version 11. Prepared by the Standards and Petitions Subcommittee. http://www.iucnredlist.org/documents/RedListGuidelines.pdf. Accessed 15 Dec 2016
IUCN (2016) The IUCN Red List of Threatened Species. Version 2016-2 http://www.iucnredlist.org. Accessed 15 Dec 2016
Jarvis A, Lane A, Hijmans RJ (2008) The effect of climate change on crop wild relatives. Agric Ecosyst Environ 126:13–23
Loeuille B, Semir J, Lohmann LG, Pirani JR (2015) A phylogenetic analysis of Lychnophorinae (Asteraceae: Vernonieae) based on molecular and morphological data. Syst Bot 40:299–315
Martinelli G, Moraes MA (2013) Livro Vermelho da Flora do Brasil. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro
Martinelli G, Messina T, Santos Filho L (2014) Livro Vermelho da Flora do Brasil – Plantas Raras do Cerrado. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro
Martins MLL, Ledo CAS (2015) Manihot cezarii (Euphorbiaceae), a new species from Central-Western Brazil. Novon 24:179–181
Martins MLL, Carvalho PCL, Ledo CAS, Amorim AM (2014) What’s new in Manihot (Euphorbiaceae)? Syst Bot 39:485–489
Martins MLL, Ledo CAS, Carvalho PCL, Amorim AM, Silva DCS (2017) Wild relatives of cassava: conservation and use. In: Klein C (ed) Handbook on cassava: production, potential uses and recent advances. Nova Science Publishers, New York, pp 373–405
Maxted N, Kell SP (2009) Establishment of a global network for the in situ conservation of crop wild relatives: status and needs. FAO Commission on Genetic Resources for Food and Agriculture, Rome
Maxted N, Kell S, Toledo Á, Dulloo E, Heywood V, Hodgkin T, Hunter D, Guarino L, Jarvis A, Ford-Lloyd B (2010) A global approach to crop wild relative conservation: securing the gene pool for food and agriculture. Kew Bull 65:561–576
Meilleur BA, Hodgkin T (2004) In situ conservation of crop wild relatives: status and trends. Biodiv Conserv 13:663–684
Mendoza FJM, Cavalcanti TB (2015) Three new endemic species of Manihot (Euphorbiaceae) from Central Brazil. Q’euña 6:7–22
Mendoza FJM, Simon MF, Cavalcanti TB (2015) Three new endemic species of Manihot (Euphorbiaceae) from the Chapada dos Veadeiros, Brazil. Arnaldoa 22:297–312
Mendoza FJM, Simon MF, Reis TS, Fidelis A, Cavalcanti TB (2016) New endemic species of Manihot (Euphorbiaceae) from Serra do Tombador in Goiás, Central Brazil. Phytotaxa 273:147–157
Mendoza FJM, Simon MF, Arquelão TKM, Cavalcanti TB (2018) Novas espécies de Manihot Mill. (Euphorbiaceae) do Brasil Central. Rodriguésia 69:915–932
Miller JS, Krupnick GA, Stevens H, Porter-Morgan H, Boom B, Acevedo-Rodríguez P, Ackerman J, Kolterman D, Santiago E, Torres C, Velez J (2013) Toward target 2 of the global strategy for plant conservation: an expert analysis of the Puerto Rican flora to validate new streamlined methods for assessing conservation status 1. Ann Missouri Bot Gard 99:199–205
MMA (2015) Mapeamento do uso e cobertura do Cerrado: Projeto Terraclass Cerrado 2013. Ministério do Meio Ambiente/Secretaria de Biodiversidade e Florestas, Brasília
Monteiro L, Brum FT, Pressey RL, Morellato LPC, Soares-Filho B, Lima-Ribeiro MS, Loyola R (2018) Evaluating the impact of future actions in minimizing vegetation loss from land conversion in the Brazilian Cerrado under climate change. Biodiv Conserv. https://doi.org/10.1007/s10531-018-1627-6
Murphy BP, Andersen AN, Parr CL (2016) The underestimated biodiversity of tropical grassy biomes. Philos Trans R Soc B 371:20150319
Nassar NM (2006) Cassava genetic resources: extinct everywhere in Brazil. Genet Res Crop Evol 53:975–983
Neves RJ, Carvalho PCL, Alves AAC, Ledo CAS, Martins MLL (2014) Wild species of Manihot Mill. (Euphorbiaceae) in the Embrapa Cassava and Fruit Collection, Cruz das Almas, Bahia, Brazil. Iheringia Série Bot 69:245–256
Olsen KM, Schaal BA (1999) Evidence on the origin of cassava: phylogeography of Manihot esculenta. Proc Natl Acad Sci USA 96:5586–5591
Pennington RT, Lavin M (2016) The contrasting nature of woody plant species in different neotropical forest biomes reflects differences in ecological stability. New Phytol 210:25–37
Rando JG, Zuntini AR, Conceição AS, van den Berg C, Pirani JR, Queiroz LP (2016) Phylogeny of Chamaecrista ser. Coriaceae (Leguminosae) unveils a lineage recently diversified in Brazilian campo rupestre vegetation. Int J Plant Sci 177:3–17
Ratter JA, Ribeiro JF, Bridgewater S (1997) The Brazilian Cerrado vegetation and threats to its biodiversity. Ann Bot 80:223–230
Ribeiro PL, Rapini A, Silva UCSE, Konno TUP, Damascena LS, van den Berg C (2012) Spatial analyses of the phylogenetic diversity of Minaria (Apocynaceae): assessing priority areas for conservation in the Espinhaço Range, Brazil. Syst Biodiv 10:317–331
Ribeiro-Silva S, Medeiros MB, Lima VVF, Peixoto MR, Aona LYS (2016) Patterns of Cactaceae species distribution in a protected area in the semiarid Caatinga biome of north-eastern Brazil. Edinburgh J Bot 73:157–170
Rivera VL, Panero JL, Schilling EE, Crozier BS, Moraes MD (2016) Origins and recent radiation of Brazilian Eupatorieae (Asteraceae) in the eastern Cerrado and Atlantic Forest. Mol Phylogen Evol 97:90–100
Rivers MC, Bachman SP, Meagher TR, Lughadha EN, Brummitt NA (2010) Subpopulations, locations and fragmentation: applying IUCN Red List criteria to herbarium specimen data. Biodivers Conserv 19:2071–2085
Rogers DJ, Appan SG (1973) Manihot and Manihotoides (Euphorbiaceae). A computer-assisted study. Flora Neotropica Monograph 13. Hafner Press, New York
Sano ES, Rosa R, Brito JLS, Ferreira LG (2010) Land cover mapping of the tropical savannah region in Brazil. Environ Monit Assess 166:113–124
Secco RS, Cordeiro I, Fernandez EP, Monteiro NP, Messina T, Borges RAX, Santos-Filho LAF (2013) Extinction risk assessments of the Brazilian flora. Martinelli G, Moraes MA (orgs) Livro Vermelho da Flora do Brasil. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro, pp 85–102
Silva MJ (2014) Manihot veadeirensis (Euphorbiaceae s.s.): a new species from the Brazilian Cerrado, Brazil. Syst Bot 39:1161–1165
Silva MJ (2015a) Manihot appanii (Euphorbiaceae s.s.): a new species from Brazil, and a key to the species with unlobed or very shortly lobed leaves. Syst Bot 40:168–173
Silva MJ (2015b) Two new wild cassava species (Manihot, Euphorbiaceae) from the Brazilian Cerrado. Phytotaxa 213:131–139
Silva MJ (2016) Manihot gratiosa and M. lourdesii spp. nov. (Manihoteae, Euphorbiaceae) from the Brazilian Cerrado. Nordic J Bot 34:66–74
Silva MJ, Sodré R (2014) A dwarf species of Manihot Mill. (Euphorbiaceae s.s.) from the highlands of Goiás, Brazil. Syst Bot 39:222–226
Silva MJ, Sodré R, Almeida LC (2013) A new endemic species of Manihot (Euphorbiaceae s. str.) from the Chapada dos Veadeiros, Goiás, Brazil. Phytotaxa 131:53–57
Silva GHL, Bringel JBA Jr, Teles AM (2016a) A new species of Calea (Asteraceae-Neurolaeneae) from Goiás State, Brazil. Phytotaxa 265:279–284
Silva MJ, Alonso A, Sodré R (2016b) Manihot pachycaulis sp. nov. (Euphorbiaceae) from the Brazilian Cerrado. Nordic J Bot 34:60–65
Simon MF, Pennington T (2012) Evidence for adaptation to fire regimes in the tropical savannas of the Brazilian Cerrado. Int J Plant Sci 173:711–723
Simon MF, Proença C (2000) Phytogeographic patterns of Mimosa (Mimosoideae, Leguminosae) in the Cerrado biome of Brazil: an indicator genus of high-altitude centers of endemism? Biol Conserv 96:279–296
Sousa-Baena MS, Garcia LC, Peterson AT (2014) Completeness of digital accessible knowledge of the plants of Brazil and priorities for survey and inventory. Divers Distrib 20:369–381
Souza ÉR, Lewis GP, Forest F, Schnadelbach AS, van den Berg C, Queiroz LP (2013) Phylogeny of Calliandra (Leguminosae: Mimosoideae) based on nuclear and plastid molecular markers. Taxon 62:1200–1219
Steege H, Pitman NC, Killeen TJ, Laurance WF, Peres CA, Guevara JE, Salomão RP, Castilho CV, Amaral IL et al (2015) Estimating the global conservation status of more than 15,000 Amazonian tree species. Sci Adv 1:e1500936
Strassburg BB, Brooks T, Feltran-Barbieri R, Iribarrem A, Crouzeilles R, Loyola R, Latawiec AE, Oliveira Filho FJB, Scaramuzza CAM, Scarano FR, Soares-Filho B, Balmford A (2017) Moment of truth for the Cerrado hotspot. Nat Ecol Evol 1:99
Trovó M, Andrade MJG, Sano PT, Ribeiro PL, van den Berg C (2013) Molecular phylogenetics and biogeography of Neotropical Paepalanthoideae with emphasis on Brazilian Paepalanthus (Eriocaulaceae). Bot J Linnean Soc 171:225–243
Vincent H, Wiersema J, Kell S, Fielder H, Dobbie S, Castañeda-Álvarez NP, Guarino L, Eastwood R, Leόn B, Maxted N (2013) A prioritized crop wild relative inventory to help underpin global food security. Biol Conserv 167:265–275
VMA-Bioversity (2010) Los parientes silvestres del cultivo de la yuca en Bolivia: Estado de conocimiento, grado de conservación y acciones de conservación propuestas. Imprenta Sagitario, La Paz
Walter KS, Gillett HJ (1997) IUCN Red list of threatened plants. Compiled by the World Conservation Monitoring Centre. IUCN-The World Conservation Union, Gland
Warschefsky E, Penmetsa RV, Cook DR, von Wettberg EJ (2014) Back to the wilds: tapping evolutionary adaptations for resilient crops through systematic hybridization with crop wild relatives. Am J Bot 101:1791–1800
Acknowledgements
We thank the curators of the herbaria visited, as well as Aécio Amaral, Alessandra Fidelis, Anderson Sevilha, Glocimar Pereira-Silva, and the managers of reserves surveyed for support during fieldwork. ICMBio authorized us to carry out research in national parks (permit SISBIO 42461). We acknowledge financial support from CNPq (Project “Conservação de Recursos Genéticos Nativos e Parentes Silvestres da Flora do Cerrado”; n. 457438/2012-6) under the Rede de Pesquisa Biota Cerrado, the Brazilian Ministry of Environment/GEF Cerrado Project, and Embrapa.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Guarino Rinaldi Colli.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Simon, M.F., Reis, T.S., Mendoza F., J.M. et al. Conservation assessment of cassava wild relatives in central Brazil. Biodivers Conserv 29, 1589–1612 (2020). https://doi.org/10.1007/s10531-018-1626-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-018-1626-7