Rediscovery of Banisteriopsis magdalenensis ...

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Rediscovery of Banisteriopsis magdalenensis (Malpighiaceae): Notes on morphology, distribution, and ecology of an endemic and threatened species from the Atlantic Forest of Brazil RAFAEL FELIPE DE ALMEIDA1, RAQUEL NEGRÃO2, PATRÍCIA ROSA2, CAIO BAEZ2, DANIEL MAURENZA2, AND GUSTAVO MARTINELLI2 1

Instituto de Ciências Biológicas, Departamento de Botânica, Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Minas Gerais, Avenida Antonio Carlos 6627, Pampulha, Belo Horizonte, Minas Gerais 31270-901, Brazil; e-mail: [email protected] 2 Centro Nacional de Conservação da Flora, Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão 915, Rio de Janeiro, RJ 22460-030, Brazil

Abstract. We present the rediscovery of Banisteriopsis magdalenensis, including an updated morphological description, illustrations, distribution map, and notes on conservation, ecology and taxonomic affinities. The species is endangered and appears to be confined to rocky outcrops in the Atlantic Forest of Northern state of Rio de Janeiro, Brazil, where two populations were found growing apart within the limits of Desengano State Park. Keywords: endemism, IUNC Red List, Malpighiales, Neotropical flora, Rio de Janeiro.

Banisteriopsis C.R.Rob. is one of the largest genera of Neotropical Malpighiaceae comprising ca. 60 species, distributed from Mexico to Argentina (Gates, 1982; Davis & Anderson, 2006). The genus can be recognized by its leaves bearing extra-floral nectaries abaxially, inflorescences usually of 4-flowered umbels, and flowers bearing stamens with enlarged and glandular connectives (Almeida et al., 2016). About 75% of its species (i.e. 46 spp.) are known to occur in Brazil, being widely distributed in all phytogeographic domains, but especially diverse in the Cerrado and Atlantic Forest domains (BFG, 2015; Gates, 1 9 82 ) . T h e la t t e r ho l ds 1 4 s p ec i es o f Banisteriopsis, 11 of which are represented by endemics (Almeida et al., 2016). Banisteriopsis magdalenensis B. Gates is the rarest species of the informal B. parviflora group proposed by Gates (1982). It was hitherto known from only three specimens, collected between 1934 and 1936, in the municipality of Santa Maria Madalena, state of Rio de Janeiro (Gates, 1982). Consequently, it was categorized as endangered on the last Brazilian red list of plants due to its restricted distribution and habitat loss (Martinelli & Moraes, 2013). This species is characterized by its shrubby habit, subsessile, abaxially sericeous

leaves, with silver hairs and large basal glands, large flowers, erect and subequal styles, and umbels born in dichasia (Gates, 1982). Nothing is known about its habitat and ecology in nature, besides its probable rupicolous habit, and altitudinal range varying from 1200 to 1700 m (Gates, 1982). We recently discovered new populations of B. magdalenensis during the course of fieldwork conducted for the BProcura-se^ (Wanted) project of the National Center for Flora Conservation of the Rio de Janeiro Botanical Garden (CNCFlora/JBRJ). This ongoing project aims to recollect threatened plant species from the state of Rio de Janeiro with fewer than three records and/or last collected more than 30 years ago. Here, we report the rediscovery of B. magdalenensis 80 years after its latest collection and provide notes on its morphology, distribution, and ecology.

Material and Methods The taxonomic treatment and illustrations that follow are based on herbarium study (GUA, MBM, R, RB, RBR, and RFA; acronyms according to Thiers, 2017 and continuously updated) and field observation. Terminology used in the

Brittonia, DOI 10.1007/s12228-018-9526-4 ISSN: 0007-196X (print) ISSN: 1938-436X (electronic) © 2018, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.

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morphological description was adopted from several sources [i.e., indumentum: Anderson (1981); laminar morphology: Radford et al. (1974); inflorescence morphology: Weberling (1965, 1989); fruit morphology: Spjut (1994) and Anderson (1981)]. The conservation status was re-assessed following the IUCN methodology, according IUCN Red List Categories and Criteria, Version 3.1 (IUCN, 2001). Maps were prepared using ArcGIS 9.3 (ESRI, 2010) from point data from geographical coordinates obtained from herbarium specimens or estimated from locality data. The classification of vegetation types follows IBGE (2012). Taxonomic Treatment Banisteriopsis magdalenensis B. Gates. Fl. Neotrop. Monogr. 30: 163. 1982. Type: BRAZIL. Rio de Janeiro: Santa Maria Magdalena, Pedra do Abreuzinho, May 1936 (fl), A. Santos Lima 350 (holotype: RB barcode 540,699!). (Figs. 1 and 2). Shrubs or vines; stems striated, laterally flattened, sericeous to glabrescent at age; stipules 0.4–0.6 × 0.8–10 mm, triangular, interpetiolar, sericeous, deciduous. Leaves opposite, reduced in inflorescences; petioles 3–4 mm long, sericeous to glabrescent at age, 2-glandular at apex, glands 1.5– 1.8 mm diam., discoid, sessile; leaf blades 2.7– 11.5 × 1.8–5.2 cm, flat, ovate to elliptic or rotund, base cordate, margin slightly revolute, apex emarginate to mucronate, adaxially sparsely sericeous to glabrescent at age, abaxially densely sericeous to glabrescent at age, hairs white, eglandular; midvein adaxially impressed, abaxially prominent, 10–12 pairs of secondary veins, subopposite to alternate, adaxially impressed, abaxially prominent, reticulum conspicuous on both sides. Umbels axillary to terminal, 4-flowered, disposed in dichasia, axillary to terminal; main axis 10–24 cm long, laterally flattened, longitudinally striated, sericeous; bracts and bracteoles 1–1.5 × 0.6–1 mm, triangular, sessile, parallel to peduncle, papery, eglandular, sparsely sericeous, persistent; peduncle sessile. Flowers 1.1–2 cm diam. at anthesis; floral buds 4–6 mm diam.; pedicels 11–23 × 0.5–0.9 mm, sparsely sericeous. Sepals 1.8–2.2 × 2.5–3 mm, ovate to narrowly ovate, not appressed to the androecium, apex rounded, straight, adaxially glabrous, abaxially sericeous; glands green, 1–2 × 0.7–2 mm. Petals yellow, not turning darker at age, margin dentate; lateral petals patent to

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deflexed at anthesis, limb 10–12 mm diam., orbicular to obovate, glabrous on both sides; claw 1.5– 2.5 × 0.4–0.5 mm, glabrous on both sides; posterior petal erect at anthesis, limb 8–8.5 × 5.5–6 mm, obovate, base truncate, glandular at base, glabrous on both sides; claw 4.2–4.5 × 0.6–0.8 mm, glabrous on both sides. Stamens 10, those opposite to the anterior sepals longer than the others; filaments 2.9–3.4 mm long, heteromorphic, connate ca. 1 mm long at base, glabrous; anthers 0.7–1 × 0.4–0.6 mm, heteromorphic, straight with a glandular connective, glabrous. Ovary 1.2–1.4 × 0.9– 1.1 mm, sparsely sericeous at apex, glabrous at middle and base; styles 3, 2–2.4 mm long, cylindrical, straight, parallel at base, slightly divergent at apex, glabrous, anterior style slightly longer and curved, apex truncate; stigma terminal, discoid. Samaras unknown. Distribution and habitat.—Banisteriopsis magdalenensis was found growing apart in two small subpopulations on rocky outcrops and altitudinal grasslands of the Desengano State Park in northern Rio de Janeiro (RJ), Brazil. This conservation unit comprises 22,400 ha of native vegetation growing on granitic and gneissic massifs, dated from 650 to 480 Mya (Instituto Estadual de Florestas 1991). The altitudinal grassland of this region are regarded as one of the best remaining examples of this vegetation type in RJ due to its intact condition and high rate of plant endemism. Among the vegetation types in the Northwest Region of Rio de Janeiro, altitudinal grasslands are the phytophysiognomy that is most threatened by human activities (Martinelli, 1996, 2007). Phenology.—Encountered with flowers from February to March and in May and August. Conservation status.—Banisteriopsis magdalenensis meets the requirements of the more restricted forms of rarity (Rabinowitz et al., 1986; Caiafa & Martins, 2010), as evidenced by its very small geographic distribution, high habitat specificity, and very small population size in Desengano State Park. Even though Desengano State Park comprises one of the largest Atlantic Forest remnants in RJ, it is impacted by the cultivation of sugarcane, livestock grazing, and skyrocketing tourism in the surrounding region (Moreno et al., 2003). The species was classified as BEndangered – EN^ in the Official List of Endangered Species from the Brazilian Flora (MMA, 2014). That assessment was made based on the IUCN (2001) B1 criterion Extent of Occurrence (EOO=536.37 km2), but that estimate

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ALMEIDA ET AL.: BANISTERIOPSIS MAGDALENENSIS (MALPIGHIACEAE)

FIG. 1. Banisteriopsis magdalenensis. A. Rocky outcrop vegetation in the Desengano State Park, municipality of São Fidelis. B. Habit, showing scandent (sometimes lianescent) stem on the left. C. Flowering branch, showing the dichasioid inflorescence. D. Adaxial side of a leaf, showing the sericeous deciduous indumentum in the extremities of the leaf blade. E. Flower in frontal view. (Photographs by C. Baez.)

was based on imprecise knowledge of the collection localities. Our results provide new information on population size, accuracy of localities, ecology, and the severity of local threats, thus resulting in a more robust assessment of the conservation status. We estimate that the Extent of Occurrence (EOO) is 54.32 km2; the Area of Occupancy (AOO) 12 km2; and the number of mature individuals in the two known subpopulations n=6 and n=5,

respectively. Following the IUCN (2001) categories and criteria, B. magdalenensis should remain in the Endangered – EN category [B2ab (i, ii, iii, iv)]. Currently, this species is part of a scientific divulgation campaign within the local community in the surroundings of the Desengano State Park. This campaign is led by the CNCFlora/JBRJ project BWanted^ that aims to locate new subpopulations of rare plant species within the state of Rio the Janeiro.

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FIG. 2. Distribution of Banisteriopsis magdalenensis.

Additional Specimens examined. BRAZIL. Rio de Janeiro: Santa Maria Magdalena, Pedra Dubois, 28 February 1934 (fl), A. Santos Lima 1328 (RB); loc. Cit., Serra da Furquilha, 4 March 1935 (fl), A. Santos Lima 14,239 (RB); loc. Cit., Pedra Dubois, picada para a direita durante a subida final, 21°56′33^S, 41°59′33^W, 1161 m, 30 August 2016 (fl), C. Baez 1000 (RB). São Fidélis, Parque Estadual do Desengano, Serra do Itacolomi, cume entre a Pedra do Macaco e Morro das Orquídeas, 21°50′58^S, 41°52′13^W, 1494 m, 31 August 2016 (fl), C. Baez 1023 (RB).

Affinities and morphological notes.— Banisteriopsis magdalenensis is part of the informal B. parviflora group proposed by Gates (1982), comprising six additional species: B. basifixa B. Gates, B. parviflora (A. Juss.) B. Gates, B. parviglandula B. Gates, B. pseudojanusia (Nied.) B. Gates, B. salicifolia (DC.) B. Gates, and B. scutellata (Griseb.) B. Gates. Those species are endemic to the Atlantic Forest domain of eastern Brazil, ranging from the state of Bahia (Northeastern Brazil) to the state of Santa Catarina (Southeastern Brazil) (BFG, 2015, Gates, 1982). All

species share the scandent habit, leaf blades with stalked glands abaxially (eglandular in B. magdalenensis), 4-flowered umbels arranged in thyrsi (or reduced to dichasia in B. magdalenensis), bracts and bracteoles papery, flowers usually small, and anterior style slightly longer than the posterior ones (Gates, 1982). Gates (1982) did not formally include B. magdalenensis in the informal B. parviflora group due to its supposedly shrubby habit (versus lianescent habit in the remaining species) and 4-flowered umbels disposed in dichasia (versus 4-flowered umbels disposed in thyrsi). Despite having its flowers disposed in dichasia, B. magdalenensis fits perfectly into the morphological description proposed by Gates (1982) for the B. parviflora group. The B. parviflora group was recovered as monophyletic in the last molecular phylogeny of Malpighiaceae (Davis & Anderson, 2010) and by unpublished data from the first author (Almeida et al., unpubl.). The abovementioned morphological characters are putative synapomorphies for this natural group. A

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key for the species of the B. parviflora group can be found in Gates (1982). Acknowledgements RFA would like to thank Capes for his postdoc fellowship and CNPq (DEB #422747/2016-5) for supporting field and herbarium studies. The authors would like to thank Thalis Pereira Lima (JBRJ) for helping with the field work; the Environmental State Secretary of Rio de Janeiro ( S E A - R J ) f o r s u p p o r t i n g t h e BWa n t e d expeditions^ as part of the project BState Conservation Units of Rio de Janeiro: analysis and strategies for conservation of threatened endemic flora – Complementary Project for data consolidation on the flora of the Rio de Janeiro state, especially in State Protected Areas"; and the managers of Desengano State Park, especially João Marins and Carlos Dário, for support provided during the field expeditions.

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ESRI-Environmental Systems Research Institute. 2010. ArcGIS, version 9.3.1. Environmental Systems Research Institute, Redlands, California. Gates, B. 1982. Banisteriopsis, Diplopterys (Malpighiaceae). Flora Neotropica 30: 1–238. IBGE. 2012. Manual técnico da vegetação Brasileira. Série Manuais Técnicos em Geociências 1, 2ª edição revista e ampliada. Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro. IUCN. 2001. IUCN Red List categories and criteria: Version 3.1. IUCN Species Survival Commission, Gland, Switzerland and Cambridge, U.K. Instituto Estadual de Florestas. 1991. Plano de Manejo Diretor Parque Estadual do Desengano. Secretaria Estadual do Meio Ambiente, Rio de Janeiro. Martinelli, G. 1996. Campos de altitude – High mountain grasslands. 2nd ed. Editora Index. Rio de Janeiro. ———. 2007. Mountain biodiversity in Brazil. Revista Brasileira de Botânica 30: 587–597. ——— & M. A. Moraes. 2013. Livro Vermelho da Flora do Brasil. Instituto Pesquisas Jardim Botânico do Rio de Janeiro & Andrea Jacobson, Rio de Janeiro. MMA. 2014. Portaria No 443, De 17 de Dezembro de 2014. Lista Nacional Oficial de Espécies da Flora Ameaçadas de Extinção". Diário Oficial da República Federativa do Brasil. Moreno, M. R., M. T. Nascimento & B. C. Kurtz. 2003. Estrutura e composição florística do estrato arbóreo em duas zonas altitudinais na Mata Atlântica de encosta da região do Imbé, RJ. Acta Botanica Brasilica 17: 371–386. Rabinowitz, D., S. Cairns & T. Dillon. 1986. Seven forms of rarity and their frequency in the flora of the British Isles. In: Conservation biology: the science of scarcity and diversity. Sinauer Associates, Massachusetts. Radford, A. E., W. C. Dickison, J. R. Massey & C. R. Bell. 1974. Vascular plant systematics. Harper & Row, New York. Spjut, R. W. 1994. A systematic treatment of fruit types. Memoirs of the New York Botanical Garden, vol. 70. New York Botanical Garden, Bronx, New York. Thiers, B. continuously updated. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden's Virtual Herbarium. Available at: http:// sweetgum.nybg.org/ih/ (Accessed: 15 May 2017). Weberling, F. 1965. Typology of inflorescences. Botanical Journal of the Linnean Society 59: 15–221. ———. 1989. Morphology of flowers and inflorescences. Cambridge University Press, Cambridge, UK