Bol. Mus. Biol. Mello Leitão (N. Sér.) 32:5-11. Setembro de 2013 5 Aristolochia bahiensis (Aristolochiaceae) reaches Espírito Santo: range extension and first description of capsules and seeds Joelcio Freitas1*, Elton John de Lírio2 & Favio González3 ABSTRACT: Aristolochia bahiensis belongs to Aristolochia ser. Hexandrae subser. Anthocaulicae, a subseries characterized by the presence of extremely short and cauliflorous racemes with subtending leaves reduced to small bracts. Hitherto, this is the only species of this subseries found in the Atlantic Forest. Here we report a range extension of A. bahiensis, and complement the original description and illustration, including new morphological traits regarding the perianth variation during flower development, and description of capsules and seeds, which had remained unknown until now. Keywords: Aristolochia ser. Hexandrae, Aristolochia subser. Anthocaulicae, Brazilian Atlantic forests, perianth variation. RESUMO: Aristolochia bahiensis (Aristolochiaceae) atinge Espírito Santo: extensão de alcance e primeira descrição de cápsulas e sementes. Aristolochia bahiensis pertence à Aristolochia ser. Hexandrae subser. Anthocaulicae; esta subsérie é caracterizada pela presença de racemos caulifloros extremamente curtos e com folhas reduzidas a pequenas brácteas. Até o momento, esta é a única espécie desta subsérie encontrada na Mata Atlântica. Neste trabalho são abordadas a ampliação da distribuição de A. bahiensis, e a complementação da descrição e ilustração originais, incluindo novidades morfológicas a respeito da variação do perianto durante o desenvolvimento da flor e a descrição das cápsulas e sementes, antes desconhecidas. Palavras-chave: Aristolochia ser. Hexandrae, Aristolochia subser. Anthocaulicae, floresta tropical, variação do perianto, Mata Atlântica. Museu de Biologia Prof. Mello Leitão. Av. José Ruschi, 04, Centro, Santa Teresa - ES, Brasil. CEP: 29650-000. 2 Programa de Pós-graduação em Botânica, Escola Nacional de Botânica Tropical, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. Rua Pacheco Leão, 2040, Solar da Imperatriz, Horto, Rio de Janeiro – RJ, Brasil. CEP: 22460-030. [email protected]. 3 Instituto de Ciencias Naturales, Universidad Nacional de Colombia, AA 7495, Bogotá, Colombia. [email protected]. * Corresponding author: [email protected] Recebido: 26 out 2012. Aceito: 15 mar 2013. 1 6 Freitas et al.: Aristolochia bahiensis (Aristolochiaceae) in Espírito Santo Introduction The family Aristolochiaceae comprises four genera and about 600 species (González, 1990, 2012; Capellari Jr., 2001). Aristolochia is the largest genus, with about 450 species (González, 2011). The genus is highly diversified in the tropics of the Old and the New World, and it is highly diversified in the Neotropics, mostly in Hispaniola and Brazil (González, 2000), the latter with 87 species according to Barros & Araújo (2013). After the monographic work by Hoehne (1927, 1942), devoted mainly to the Brazilian species, some new taxa have been described from the country (González, 1998, 2000, 2011). One of these new species, Aristolochia bahiensis F. González was described based on two flowering specimens, both from the state of Bahia (González, 1998). This species belongs to Aristolochia ser. Hexandrae subser. Anthocaulicae, which comprises 22 species (González, 1990, 1991, 1997, 1998), all of them characterized by the presence of extremely short and cauliflorous racemes with leaves reduced to small bracts. Until now, A. bahiensis is the only species of this subseries found in the Atlantic Forest. The species of subseries Anthocaulicae are found in western, northern and central Amazonian forests, in wet forests of the Choco, and Magdalena and Cauca valleys of Colombia, in stations of Central America and in the Atlantic Forest Brazil. Here are reported a range extension of A. bahiensis to the state of Espírito Santo, Brazil, collected by one of us (JF), along with the description and ilustration, for the first time, of the capsules and the seeds of this species, which had remained unknown until now, and the perianth variation along the flower development. Material and Methods The descriptions, illustrations and the newly reported morphological traits were made from living specimens of the populations found in the field. Herbarium vouchers were deposited in the herbarium MBML, plus the herbarium specimens of CEPEC, COL and NY (Mun. Una, Reserva Biológica IBAMA, J. Jardim et al. 809, CEPEC, NY, the type collection; and Mun. Porto Seguro, reserva da Brasinheiil Holanda de Industrias S/A, J. G. Jardim et al. 399, COL, NY). The specimens were examined with the aid of a dissecting microscope coupled to the light chamber and directly in the field by naked eye. Descriptions of general morphological characters follow Harris & Harris (2001), except for those characters unique in Aristolochia flowers, which were described according to González (1990, 1991, 1994). Bol. Mus. Biol. Mello Leitão (N. Sér.) 32. 2013 7 Results Aristolochia bahiensis F. González, Brittonia 50: 8. 1998. Type: Brazil. Bahía: Município de Una, Reserva Biológica do Mico-leao (IBAMA), entrada no km 46 da Rod. BA-001 Ilhéus/Una, ramal que 1eva a Faz. Jaqueiral, ca. 8 km da entrada, 15º09’S, 39º05´W, 01 May 1996 (fl), J. Jardim, S. C. Santana & J. L. Paixão 809 (Holotype: CEPEC; isotype: NY). Figures 1 e 2. Glabrescent vines. Stem suberose. Twigs cylindrical, internode 6.8-11.1 cm long. Petiole 1.3-5.1 cm long, the proximal half slightly thicker; lamina ovate-deltoid (narrowly ovate), 10-16 x 5-8.2 cm, base truncate to slightly cordate (and with a sinus to 4 mm deep), slightly peltate, apex acute to acuminate, chartaceous, glabrous above, sparsely puberulous below, especially along the veins, basal primary veins 3(5). Pseudostipules absent. Flowers arranged in short, cauliflorous racemes, 4-13.4 mm long each, with internodes < 1 mm long, up to 8 flowers, each flower subtended by a deltoid, pubescent bract, 2.0-2.5 x 1.6-2.0 mm. Peduncle plus ovary 1.3-2.3 cm long, slender, shortly villous, ovary slightly rostrate at its apex. Perianth glabrous, beige with thick vinaceous grooves on the outside, yellow with whitish indument on the inside, slightly curved at preanthesis, then the curvature between the utricle and the tube becomes more pronounced; utricle obovate, 3.7-8 x 3-5.5 mm; syrinx absent; tube funnel-shape, 1.0-2.3 cm long, 2.0-3.7 mm proximal diameter, 4.5-7.1 mm distal diameter, forming an angle of ca. 110-130o with respect to the utricle; limb broadly ovate to elliptic, 1.1-2 x 0.6-1.4 cm, forming an angle of ca. 180o with respect to the tube, vinaceous to yellow and with white trichomes on the inside, base obtuse, apex obtuse but ending in a very short acumen, margin revolute at anthesis. Ginostemium stipitate, 1.7-4 mm long; anthers 0.9-1.5 mm long. Capsule cylindrical, 2.9-3.8 x 1.6-1.7 cm, hexagonal in transverse section, dehiscence acropetal, septa entire; seeds ovate, concave-convex, 4.25.6 x 3.6-4.6 mm, warty, unwinged, prominulous raphe. Additional specimens examined: Brazil. Bahía: Porto Seguro, reserva da Brasil Holanda de Industrias S/A, entrada no km 22 da rod. Eunapólis/P. Seguro, 9.5 km da entrada, mata higrófila sul Bahíana, mata perturbada, 16º27’45’’S, 39º19’31’’ W, 7 abr 1994 (fl), J. G. Jardim et al. 399 (COL, NY). Espírito Santo: Santa Maria de Jetibá, São José do Rio Claro, prop. Alfredo Renok, interior da capoeira, próxima à caixa d’água grande, 20º00’08’’S, 40º36’59’’W, 21 abr 2009 (fl), J. Freitas 06 (MBML); 01 jun 2012 (fr), J. Freitas & L. Tonini 160 (MBML); Santa Teresa, Valsugana Velha, Estação Biológica de Santa Lúcia, 19º58’4’’S, 40º32’13’’W, 8 fev 2011 (fl) L. Kollmann 12176 et al. (MBML). 8 Freitas et al.: Aristolochia bahiensis (Aristolochiaceae) in Espírito Santo Figure 1. Aristolochia bahiensis F. González (Freitas et al. 06; Kollmann et al. 12176). A Twig. B Leaf base with a detail of the indument. C Perianth at anthesis. D Ginostemium during pollen shed. E Dehisced capsule. F Seeds, adaxial (left) and abaxial (right) views. G Transverse section of capsule before dehiscence. Bol. Mus. Biol. Mello Leitão (N. Sér.) 32. 2013 9 Discussion The fruit of Aristolochia bahiensis is a cylindrical capsule, hexagonal in transverse section (Figure 1G), with dehiscence acropetal and septa entire (Figure 1E). The seeds are ovate, concave-convex, unwinged, warty, and with a prominulous raphe. This suite of traits is characteristic of most species of Aristolochia subser. Anthocaulicae (González, 1990). The fact that the thick, unwinged seeds in capsules located near the ground or in the understory forest stratum, as those found in A. bahiensis (Figure 1E e F), could be an adaptation to short-distance dispersal. These traits strongly contrasts to other new world members of Aristolochia, especially those from series Thyrsicae (e.g. A. maxima Jacq.) and the group Dipharus (e.g. A. ringens Vahl), which have capsules that are exposed to the canopy or to open places, and broad, flat winged seeds, mainly dispersed by wind and/ Figure 2: A-B Young racemes with preanthetic flowers. C Flower at early anthesis, lateral view. D-E Raceme with preanthetic flowers and a flower at late anthesis. 10 Freitas et al.: Aristolochia bahiensis (Aristolochiaceae) in Espírito Santo or fresh water streams (González, 1990; González & Stevenson, 2002). According to the new data reported here, the capsules (Figure 1E) and seeds (Figure 1F) of A. bahiensis are similar in shape with those of its closely related species, A. guentheri O. C. Schmidt and A. klugii O. C. Schmidt, which could not be used to separate these three species. Thus, the main differential traits between these three species are the perianth shape and size (A. guentheri presented tube 1.0-1.3 cm long, limb ovate to broadly ovate; A. klugii presented tube 2.0-2.7 cm long, limb bilobed, unequal, lobe adaxial larger and elliptic to ovate, lobe abaxial smaller and ovate), plus the allopatric distribution, as the geographic range of A. bahiensis does not overlap with that of the other two species, which are distributed in the northwestern and western Amazonian forests (González, 1990, 1994, 1998). The specimens of A. bahiensis newly collected at Espírito Santo during the present study show the following variation compared to the type material of this species: The overall indument is glabrescent (versus glabrous in the type of A. bahiensis); the shape of perianth is ovate to elliptic (versus oblong in the type); and the perianth curvature along the tube, which reaches an angle of ca. 90º during anthesis (versus almost linear in the type). Nevertheless, the variation in all of these traits falls into the expected ranges for Aristolochia species. The variation of the perianth curvature between the type collection and the Espírito Santo specimens, is likely due to flower expansion during anthesis (Figure 2); the young perianth is almost linear (Figure 2 A), but as the flower approaches anthesis, the tube and limb gradually curves to ca. 90° with respect to the utricle (Figures. 1C e 2 B) and remains so until anthesis (Fig. 2 C). At anthesis the tube undergoes further bending (Figures 2 D-E). These gradual changes on the perianth curvature have been reported in a number of species (Costa & Hime, 1981; González & Stevenson, 2000). Acknowledgements The authors would like to thank Alfredo Renok for the proper permits to carry out field observations in situ. Thanks also to the anonymous reviewers for their thoughtful comments. We acknowledge the staff of the Museu de Biologia Prof. Mello Leitão, especially, Hélio de Queiroz Boudet Fernandes, curator of MBML herbarium, for the permission to consult the collection, and Matheus Poubel for the corrections of the English version. Bol. Mus. Biol. Mello Leitão (N. Sér.) 32. 2013 11 Literature Cited Barros, F. & Araújo, A.A.M. 2013. Aristolochiaceae. In: Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. Available in: http:// floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB54 (27-02-2013). Capellari Jr., L. 2001. Aristolochiaceae. In: Rizzo, J.A. (ed.) Flora dos Estados de Goiás e Tocantins. Coleção Rizzo. Goiânia, Universidade Federal de Goiás, vol. 27, 34p. Costa, E. & N. Hime. 1981. Biologia floral de Aristolochia gigantea Mart. & Zucc. (Aristolochiaceae). Rodriguésia, 33(56): 23-44. González, F. 1990. Aristolochiaceae. Flora de Colombia. Universidad Nacional de Colombia, Instituto de Ciencias Naturales, 12: 1-184. González, F. 1991. 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