“O Check List weir tote af ey | J . Fr. NOTES ON GEOGRAPHIC DISTRIBUTION Check List 14 (2): 335-339 B https://doi.org/10.15560/14.2.335 PENSUFT. Hippeastrum angustifolium Pax (Amaryllidaceae): first record for a biodiversity hotspot in the Mato Grosso do Sul, Brazil Berinaldo Bueno,' Suzana Neves Moreira,’ Vali Joana Pott? 1 Programa de Pés-Graduacao em Ecologia e Conserva¢aéo, Departamento de Biologia, Universidade Federal de Mato Grosso do Sul, P.O. Box 549, CEP 79.070-900, Campo Grande, MS, Brazil. 2 Universidade Estadual do Mato Grosso do Sul, Rua General Mendes Morais, 370, Jardim Aeroporto, CEP 79.400-000, Coxim, MS, Brazil. 3 Programa de Pdés-Gradua¢ao em Biologia Vegetal, Instituto de Biociéncias, Universidade Federal de Mato Grosso do Sul, CEP 79.070-900, P.O. Box 549, Campo Grande, MS, Brazil. Corresponding author: Berinaldo Bueno, bio_bere@hotmail.com Abstract Hippeastrum angustifolium Pax a bulbous perennial in the family Amaryllidaceae, occurs in Argentina, Paraguay, and south-southeastern Brazil in the Pampa and Atlantic Forest domains. In this work, we present the first record of this species for the Cerrado domain in the state of Mato Grosso do Sul, Brazil. We also comment on its biology and ecology. Key words Bulbous herbs; Cerrado; distribution; South America; wetlands. Academic editor: Mayara K. Caddah | Received 13 September 2017 | Accepted 23 January 2018 | Published 16 March 2018 Citation: Bueno B, Moreira SN, Pott VJ (2018) Hippeastrum angustifolium Pax (Amaryllidaceae): first record for a biodiversity hotspot in the Mato Grosso do Sul, Brazil. Check List 14 (2): 335-339. https://doi.org/10.15560/14.2.335 Introduction Hippeastrum Herb., which presents the greatest spe- cies richness in this group (Meerow and Snijyman 1998, Meerow et al. 2000). Hippeastrum has about 50 species throughout North and South America (Meerow 2004). In Brazil, Hippeastrum is a major genus and many species are native, occurring throughout the country; species are epiphytes or terrestrial in grasslands, forests, caatinga, The family Amaryllidaceae J.St.-Hil. is distributed worldwide and its taxonomy is complex (Oliveira 2012). In Brazil, 18 genera are recognized, comprising 135 native species (Dutilh and Oliveira 2015a). Amarylli- doideae Burnett is distributed from temperate to tropical areas; South America, South Africa, and the Mediterra- nean region are the 3 main centers of diversity (Arroyo marshes, and near the sea (Dutilh 1989, Schultz 1990, and Cutler 1984, Meerow 2004). This subfamily consists Dutilh 2005a). Plants of the genus are popularly known of bulbous herbs, with strap-shaped leaves, umbellate 4S amaryllis and lilies and have great economic impor- inflorescences, bisexual flowers, inferior ovaries, and tance worldwide because many are used as ornamentals capsule-shaped fruits (Meerow 2004). or have pharmacological potential (Dutilh 2005a). According to APG IV (2016), Amaryllidoideae is 1 of Hippeastrum angustifolium Pax is 1 of the 34 spe- 3 subfamilies of Amaryllidaceae and is part of the clade cies of Hippeastrum known from Brazil. It is distributed Hippeastroide. This clade includes the tribe Hippeast- through Argentina, Paraguay and south-southeastern reae Herb. ex Sweet, with 7 genera, including the genus __ Brazil, in the states of Rio Grande do Sul and Sdo Paulo, Copyright Bueno et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 336 Paraguay_<<\ Check List 14 (2) ©. Cerrado Atlantic Forest @G& Pampa (Pantanal es Territory boundaries Datum: WGS&4 River system, boundaries, domains, IBGE 2014 90 180 360 540 Figure 1. Geographic distribution of H. angustifolium in South America. * = previously known occurrences; A = first species record in the Cerrado of Mato Grosso do Sul, Brazil. in the Pampa and Atlantic Forest domains, respectively (Dutilh and Oliveira 2015b). This species is widely marketed as an ornamental plant by collectors of bul- bous plants around the world (Dutilh 2005b), but little is known about this species distribution in Brazil because many natural populations are disappearing and citations in lists of local floras are scarce (Dutilh 2005a, Dutilh et al. 2013). In this work, we present the first record of H.. angustifolium for the Cerrado domain in the state of Mato Grosso do Sul, Brazil, along with comments about its biology and ecology. Methods The species was collected during the “Aquatic Commu- nities Monitoring Program” in the areas around the Sao Fernando Sugarcane Mill, Dourados, Mato Grosso do Sul (Fig. 1). Here, typical Cerrado phytophysiognomies predomi- nate, Submontane Semi-deciduous Forest and Atlantic Forest formations interspersed (IBGE 2012). The climate is Cfa according to the Koeppen climate classification system, with a warm summer, average annual tempera- ture between 20 and 22 °C and an annual rainfall between 1600 and 1900 mm (Alvares et al. 2013). The collected specimen was deposited in the Her- barium of the Federal University of Mato Grosso do Sul, Campo Grande (CGMS). The geographic distribution map (Fig. 1) was prepared using the available information in the SpeciesLink (http:// www.splink.org.br) and Global Biodiversity Information Facility (http://www. gbif.org) databases, as well as unpub- lished data from Julie Henriette Antoinette Dutilh (pers. comm.). When the geographic coordinates of collection sites were not explicit, for mapping purposes, we used the most specific locality (hence, the nearest town). Records for which a set of coordinates could not be derived from the data are recorded 1n (Table 1) but not mapped. Results New records. Brazil: Mato Grosso do Sul. Dourados, wet- land next to MS-379 road, near Sao Fernando Sugarcane Mill (22°19'41"S, 054°56'14" W), 7-X-2016, (B. Bueno, CGMS 57124). Dourados, wetland next to MS-379 road, near junction with MS-463 road (22°15'32"S, 054°52'41" W), 7-X-2016, (B. Bueno, no voucher speci- men collected). The specimens were collected in a vereda (a typical wetland of the Cerrado, with water table above the sur- Bueno et al. | Hippeastrum angustifolium: first record in Mato Grosso do Sul, Brazil 337 Table 1. List of H. angustifolium available, including the data for each sample. Asterisks (*) indicate geographic coordinates determined by authors. MBM = Herbario do Museu Botanico Municipal, Sl and AS = Instituto de Botanica Darwinion, MO = Missouri Botanical Garden, C = University of Copenhagen, F = Field Museum, B = Botanischer Garten und Botanisches Museum Berlin-Dahlem, MACN = Museo Argentino de Ciencias Naturales, CGMS = Herbario da Fundacao Universidade Federal de Mato Grosso do Sul, HDCF = Herbario do Departamento de Ciéncias Florestais, UEC = Herbario da Universidade Estadual de Campinas, BHCB = Herbario da Universidade Federal de Minas Gerais, ESA = Herbario da Escola Superior de Agricultura Luiz de Queiroz, S = Swedish Museum of Natural History, NY = The New York Botanical Garden, SPF = Universidade de Sao Paulo, SP = Instituto de Botanica, U = Naturalis Biodiversity Center, K = Royal Botanic Gardens Kew, BM = British Museum of Natural History, MVJB = Museo y Jardin Botanico, MVM = Museo Nacional de Historia Natural, MVFQ = Universidad de Date Herbarium number Collector/Collection number 21-IX-2004 MBM 322847 M.E.M. Romero 3797 et al. 21-IX-2004 SI 145417; SI 145418 M.E.M. Romero s/n° 15-X-2000 SI 19106 F.O. Zuloaga 7145 22-X-1996 SI 1408; MO 2188178 O. Morrone 1822 13-X-1977_ Sl A.L. Cabrera 28761 12-X-1977 S167351 A.L. Cabrera 28626 25-X-1959 C T.M. Pedersen 5230 XII-1950 SI 19106; MO 2452834 R.A. Spegazzini 1 1907 SI 10037 A. de Llamas 26616 27-X-1886 F G. Niederlein 1893 27-X-1886 B9971 G. Niederlein 1893 13-X-1886 MACN 16771 G. Niederlein 655 $1 67350 A.L. Cabrera s/n° MO 3029368 G. Niederlein 1893 7-X-2016 CGMS 57124 B. Bueno s/n° 13-X-2009 HDCF 6517 K.P. Soares s/n° 23-X-2001 UEC 170541 J.H.A. Dutilh s/n° 5-XI-1995 UEC 77762;BHCB 31158 J.R. Stehmann 1986 et al. 5-XI-1995 UEC 77238 J.R. Stehmann 1987 et al. 3-XI-1995 ESA 39648;UEC 77752; = J.R. Stehmann 2004 et al. BHCB 31329 3-X-1944 S A. Macedo 513 13-XIl-1936 MO 3029316; NY 886273 W.A. Archer 4435; J.H.A. Dutilh s/n° 21-X-1936 SPF 72966; SP 36534 F.C. Hoehne s/n®; F.C. Hoehne & A. Gehrt 1938 12-XII-1956 U 1065423 A.L. Woolston 732 IX-1931 S P. Jorgensen 4540 IX-1898 AS 34146 E. Hassler 4591 27-IX-1874 K B. Balansa 529 MO 2492272 E. Hassler 4591 BM 526566 E. Hassler 6.1864; d.1937; Hassl. 4591 MVJB 38317 C. Brussa 1292 XI-1898 SI 179273; MVM J. Arechavaleta 3993c; M.B. Berro la Republica. Locality Latitude Longitude Argentina, Misiones, Apdstoles 27°49'00"S 055°46’00" W Argentina, Misiones, Ruta Provincial 1 27°49'23"S 055°46'12”W Argentina, Misiones, Posadas 27°28'48"S = 055°55'12"”W Argentina, Corrientes, Santo Tomé 28°04'59"S = 055°42’00"” W Argentina, Misiones, Apdstoles* 27°54'53”S = 055°45'18" W Argentina, Misiones, Gral Guemes 27°39'00"S = 055°33’36" W Argentina, Misiones* 27°15'29"S 055°32'05”W Argentina, Misiones, Posadas 27°22'59"S = 055°54’00"” W Argentina, Misiones, Candelaria 27°26'24"S = 055°35’24"W Argentina, La Pampa, Ruta Provincial 11* 35°23'12”S 064°55'14” W Argentina Argentina, Misiones* 27°27'47"S — 055°51'50” W Argentina, Misiones, Apdstoles 27°46'48"S = 055°43'12”W Argentina Brazil, MS, Dourados 22°19’41"S_ 054°56'14"W Brazil, RS, Mata 29°34'59"S = 054°29'07" W Brazil, SP, Avaré 23°05’24"S = 048°55'12"” W Brazil, RS, Quarai 30°23'15”S 056°27'5”W Brazil, RS, Candiota 31°26'56"S 053°40’55”W Brazil, RS, Santana do Livramento 30°53'26"S 055°31'58” W Brazil, MG, Ituiutaba* 18°58'41"S = 049°27'45" W Brazil, RS, Santana do Livramento* 30°48'11"S_ — 055°37'33"W Brazil, SP, Andradina* 20°37’47"S = 051°05’59" W Paraguay, San Pedro* 24°05’26"S_ = 057°4’33”W Paraguay, Gauira, Itapé* 25°51'05”S 056°36’49" W Paraguay, Canindeyu, Curuguaty 24°28'14"S 055°41'35”"W Paraguay Paraguay, Paraguari* 25°37'11"S_ — 57°9'00"” W Paraguay, Central, Aregua* 25°18'20"S = 57°24'33”W Uruguay, Rivera, Ruta 27* 31°2’31"S 55°29'11"W Uruguay, Tacuaremboé 31°19'37"S — 55°59'15”W Uruguay, Rivera, Tranqueras 31°9’24"S 55°55'55"W face, abundant organic matter, and many filiform species of Poaceae and Cyperaceae; Moreira et al. 2015). The Vereda is located within an area of cultivated pasture (Urochloa spp.) surrounded by sugarcane. Two natural populations of H. angustifolium were recorded in 2 sepa- rate wetlands, about 9 km apart. Identification. Hippeastrum individuals with flowers and fruits were collected for their identification in labora- tory. The flowers were analyzed with stereomicroscope and flower features were identified according to the iden- tification key for Hippeastrum species (Dutilh 200S5a). According to Dutilh (2005a), the flower features required to identify species are: a) 3 lower tepals wrapping the filaments base, b) thick corona of fimbriae and c) stamens 5957 MVFQ 621; MVM J. Arechavaleta 3998 and style longly exserted (Fig. 2B). Hippeastrum angus- tifolium is characterized as a bulbous herb with annual green leaves and long erect hollow scape that can sustain up to twelve dark red and green-tinged flowers, which give rise to fruit containing semi-discoid and flattened seeds (Dutilh 2005a). It is a terrestrial plant that usu- ally occurs in wet open grasslands (Dutilh and Oliveira 2015b) and its pollination is certainly performed by birds and seed dispersion by wind (Piratelli 1997, Oliveira 2012, Fig. 2). Discussion The Cerrado is a global biodiversity hotspot with over 4800 plant and vertebrate species found nowhere else, Check List 14 (2) Figure 2. General appearance of H. angustifolium from Dourados, Mato Grosso do Sul, Brazil. A. Habit. B. Inflorescence. C. Fruit. but public protected areas cover only 7.5% of the area this biome and deforestation threatens about 480 endemic plant species (Strassburg et al. 2017). The vereda wet- lands are important in maintaining animal and plant diversity (Moreira et al. 2015), but, unfortunately, the vereda subsystem is one of the most vulnerable in Brazil because it is under high anthropogenic pressure and has little capacity for regeneration (Carvalho 1991). Since 2011, H. angustifolium has been recorded tn the surveys of the Sao Fernando Mill. The 2 natural popula- tions recorded are located inside private rural properties, but the specimens were collected only in the mill area because we did not have authorization to collect them in the other area. All specimens recorded in the last 5 years were observed blooming in September and October, and their flowers were visited by hummingbirds, bees, and butterflies (Berinaldo Bueno, pers. obs.). The clos- est known occurrence where this species was previously documented is in Sao Paulo state, Brazil (/.H.A. Dutilh, UEC 170541), about 520 km northwest from our record. The species is classified as Vulnerable in Brazil, but is not protected (Dutilh et al. 2013). It is considered extirpated in the state of Sao Paulo (SNA 2016). In the states of Sao Paulo and Minas Gerais, records of H. angustifolium were mainly made in the 1930s and 1940s, respectively (Table 1). In both states, plant records were in specific habitats (Fig. 1) and tts occurrence is unlikely nowadays, as the habitats needed by this species have drastically changed in the last several decades due to expansion of agriculture, natural resource extraction, and infrastructure projects (MMA 2008). Based on the data available to us, this species is restricted in some habitats in south-southeastern in South America and the its popu- lations seem to be very scarce (Fig. 1), which makes them more susceptible to several threats. According to Dutilh et al. (2013), H. angustifolium is rapidly disappearing due to dam construction, opening of drainage channels, and agricultural and urban expansion on wetlands. In the southern region of Brazil, for example, flooded areas, previously considered unhealthy and unproductive, were drained for growing rice. Agrochemicals, applied on rice crops, cause soil and water contamination and put the flora in jeopardy (Carvalho and Ozorio 2007). The gen- eration time of H. angustifolium is a limiting factor that hinders the recovery of populations because it 1s at least 3-4 years (CNCFlora 2017). Thus, habitat preservation is very important for sur- vival of H. angustifolium. Because this species is still Data Deficient (MMA 2008), new studies on its repro- ductive biology and ecology are needed. Bueno et al. | Hippeastrum angustifolium: first record in Mato Grosso do Sul, Brazil 339 Acknowledgements We are grateful to the Citta Urban and Environmental Planning Company for the logistical support. We also thank Julie Henriette Antoinette Dutilh for making avail- able unpublished personal data of the species and Arnildo Pott for the English proofreading. Finally, we thank the anonymous reviewers and the academic editor for your contributions and critical comments, which helped us to improve the manuscript. Authors’ Contributions BB collected the data. SNM and VJP identified the species. BB, SNM and VJP wrote the text and produced the map. References Alvares CA, Stape JL, Sentelhas PC, Goncalves JLM, Sparovek G (2013) Koppen’s climate classification map for Brazil. Meteo- rologische Zeitschrift 22: 711-728. https://doi.org/10.1127/0941- 2948/2013/0507 APG IV (2016) An update of the Angiosperm Phylogeny Group clas- sification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1-20. https://doi. org/10.1111/boj.12385 Arroyo SC, Cutler DF (1984) Evolutionary and taxonomic aspects of the internal morphology in Amaryllidaceae from South America and southern Africa. Kew Bulletin 39 (3): 467-498. https://doi. org/10.2307/4108592 Carvalho PGS (1991) As veredas e sua importancia no dominio dos cerrados. Informe Agropecuario. Belo Horizonte 15 (168): 54—56. Carvalho ABP, Ozorio CP (2007) Avaliagéo sobre os banhados do Rio Grande do Sul, Brasil. Revista de Ciéncias Ambientais 1 (2): 83-95. https://doi.org/10.18316/171 CNCFlora (2017) Hippeastrum angustifolium in Lista Vermelha da flora brasileira versio 2012.2 Centro Nacional de Conserva¢ao da Flora. http://cncflora.jbrj.gov.br/portal/pt-br/profile/Hippeastrum- angustifolium. Accessed on 2017-5-16. Dutilh JHA (1989) As coloridas acucenas brasileiras. Boletim Informa- tivo da Sociedade Brasileira de Floricultura e Plantas Ornamentais, IAC, Campinas, SP, Boletim Informativo 1: 4—5. Dutilh JHA (2005a) Amaryllidaceae. In: Wanderley MGL, Shepherd GJ, Melhem TSA, Giulietti AM, Martins SE, Kirizawa M (Eds) Flora fanerogamica do Estado de Sao Paulo. FAPESP:RiMa, Sao Paulo, 4: 244-256. Dutilh JHA (2005b) Ornamental bulbous plants of Brazil. Acta Horticul- turae 683: 37-42. https://doi.org/10.17660/ActaHortic.2005.683.3 Dutilh JHA, Oliveira RS (2015a) Amaryllidaceae in Lista de Espécies da Flora do Brasil. Jardim Botanico do Rio de Janeiro. http:// floradobrasil jbrj.gov.br/jabot/floradobrasil/FB43. Accessed on: 2017-11-11. Dutilh JHA, Oliveira RS (2015b) Amaryllidaceae. In: Flora do Brasil 2020 em constru¢ao. Jardim Botanico do Rio de Janeiro. http:// floradobrasil.jbrj.gov. br/reflora/floradobrasil/FB33479. Accessed on: 2017-5-21. Dutilh JH, Fernandez EP, Penedo TSA, Moraes MMV, Messina T (2013) Amaryllidaceae. In: Martinelli G, Moraes MA (Eds) Livro Verme- lho da Flora do Brasil. CNCFLORA, Rio de Janeiro, 130-130. IBGE (2012) Manual Técnico da Vegetacao Brasileira. Série Manuais Técnicos em Geociéncias 1, 2° edi¢ao revista e ampliada. Rio de Janeiro, IBGE, 275 pp. Meerow AW (2004) Alliaceae, Amaryllidaceae. In: Smith N, Mori SA, Henderson A, Stevenson DW, Heald SV (Eds) Flowering Plants of the Neotropics. The New York Botanical Garden, New York, 410-412. Meerow AW, Sniyman DA (1998) Amaryllidaceae. In: Kubitzki K (Ed.) The Families and Genera of Vascular Plants. Springer-Verlag, Ber- lin, 141-190. Meerow AW, Guy CL, Li Q-B, Yang S-L (2000) Phylogeny of the American Amaryllidaceae based on nrDNA ITS sequences. Sys- tematic Botany 25 (4): 708-726. https://doi.org/10.2307/2666729 MMA (2008) Espécies da flora brasileira ameacadas de extin¢ao e com deficiéncia de dados. Instrucéo Normativa 06/2008. Ministério do Meio Ambiente. Moreira SN, Eisenlohr PV, Pott A, Pott VJ, Oliveira-Filho AT (2015) Similar vegetation structure in protected and non-protected wetlands in central Brazil: conservation significance. Environmental Conser- vation 42: 1—7. https://doi.org/10.1017/S03768929 15000107 Oliveira RS (2012) O género Hippeastrum Herb. (Amaryllidaceae) no Brasil: evidéncia de evolucao reticulada e analise de caracteres florais. PhD thesis, Universidade Estadual de Campinas, Campinas, 240 pp. Piratelli AJ (1997) Feeding behavior of hummingbirds in two sympatric Hippeastrum species. Revista Brasileira de Biologia 57: 261-273. Schultz A (1990) Introduc¢ao a Botanica Sistematica. Vol. 2. 6 ed. Editora da Universidade Federal de Rio Grande do Sul, Porto Alegre, 414 pp. SNA (2016) Espécies da flora ameagadas de extin¢ao no Estado de Sao Paulo. Resolugao SNA 057/2016. Secretaria de Estado do Meio Ambiente. Strassburg BBN, Brooks T, Feltran-Barbieri R, Iribarrem A, Crouzeilles R, Loyola R, Latawiec AE, Filho FJBO, Scaramuzza CAM, Sca- rano FR, Soares-Filho B, Balmford A (2017) Moment of truth for the Cerrado hotspot. Nature Ecology & Evolution 1: 1-3. https:// doi.org/10.1038/s41559-017-0099