A new species of () from northeastern Brazil

ALAIN CHAUTEMS, GEORGE S. BARACHO, AND JOSE A. SIQUEIRA FILHO

Chautems, A. (Conservatoire et Jardin botaniques de la Ville de Gen~ve, C. P. 60, CH-1292 Chamb6sy, Switzerland), G. S. Baracho & J. A. Siqueira Filho (Herbarium UFP, Depto. de Boffmica, CCB, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego s/n, Cidade Universit~ia, Recife-PE, CEP 50670-901, Brazil). A new species of Sinningia (Gesneriaceae) from northeastern Brazil. Brit- tonia 52: 49-53. 2000.~inningia nordestina is described and illustrated. Mor- phological and molecular characters are discussed. It is a new species endemic to northeastern Brazil and is distinguished from other members of the by its vestigial tubers, ascending pedicels with pendent flowers, small corollas, and deviating flowering period. Key words: Gesneriaceae, Sinningia, , northeastern Brazil, molec- ular phylogenetics, pollination.

Chautems, A. (Conservatoire et Jardin botaniques de la Ville de Gen~ve, C. P. 60, CH-1292 Chamb6sy, Switzerland), G. S. Baracho & J. A. Siqueira Filho (Herbarium UFP, Depto. de BotS_nica, CCB, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego s/n, Cidade Universit&ria, Recife-PE, CEP 50670-901, Brazil). A new species of Sinningia (Gesneriaceae) from northeastern Brazil. Brit- tonia 52: 49-53. 2000.--Sinningia nordestina 6 descrita e ilustrada. S~o discu- tidos caracteres morfol6gicos e moleculares, t~ uma esp6cie nova endSmica do nordeste do Brasil, distinta dos outros membros do genero pela presenoa de tub- 6rculos vesfigiais, pedicelos ascendentes corn totes pendentes, corolas pequenas e pela fenologia diferente.

Sinningia is a genus of neotropical Ges- (Paxt.) Regel. An illustration of the same neriaceae with approximately 65 species. species, based on a collection from the state The genus is characterized by a mostly ru- of Paraiba (Moraes s.n.) was posthumously picolous habit, usually perennial tubers or published in Hoehne (1970: pl. 185) under basal stem portion producing annual flow- the same identification. The correct name ering shoots, and axillary or terminal inflo- for this is Smithiantha zebrina (Paxt.) rescences with usually ornithophilous or Kuntze, as the genus Naegelia Regel 1847, melittophilous flowers. A revision of the non Rabenhorst 1844, must be substituted genus is currently under investigation due to the homonymy (Farr et al., 1979). (Chautems, 1990, 1991, 1995; Chautems & The genus Smithiantha Kuntze includes Weber, 1999). about five species restricted to southern During a visit to the herbarium of the Mexico and belonging to tribe Gloxinieae "Empresa pernambucana de pesquisa e (Wiehler, 1983). The presence of scaly rhi- agropecu~ia" (IPA) in 1984, the first au- zomes is the key character for this tribe. thor saw some specimens collected by An- The above-mentioned material from Brazil drade Lima in Pernambuco and annotated is strikingly reminiscent of the nodding po- in 1958 by Hoehne as Naegelia zebrina sition of the flowers and the red and yellow

Brittonia, 52(1), 2000, pp. 49-53. ISSUED: 21 Mar 2000 2000, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A. 50 BRITTONIA [VOL. 52 corolla of the Mexican genus, but leaf Smithiantha appears unambiguously nested shape and coloration, flower size, and the in a separate clade including the genera opposite instead of alternate disposition of sampled for the tribe Gloxinieae. the flowers along the inflorescence axis dif- fer from Smithiantha (Paxton, 1841; Regel, Sinningia nordestina Chautems, Baracho 1878). In the absence of subterranean or- & Siqueira Filho, sp. nov. (Fig. 2) gans, it was difficult to assign the Brazilian TYPE: BRAZIL. Pernambuco: Mun. Mar- specimens to genus. In the following years, aial, Engenho Curtume, margens do Rio similar material from several locations in Pirangi, 08~ 35~ 260 m, 5 Sep northeastern Brazil was encountered in dif- 1997, G. S. Baracho & J. A. Siqueira Filho ferent herbaria in Brazil, but none bore 663/704 (HOLOTYPE: UFP; ISOTYPE: G). complete subterranean organs or observa- Plantae Brasiliam boreali-orientalem incolentes, ha- tions of this important character. All collec- bitu gregariae, ab omnibus congeneribus tubero parvo tions, because of their habit and red tubular (0.5-1.5 cm diam), pedicellis ascendentibus, floribus corolla, pointed to Sinningia, a genus well- cernuis, corollae parvae (2-2.5 cm) cinnabarinae tubo diversified in southeastern and southern gradatim ampliato ad ventrem flavum rnbro maculato, Brazil but of limited distribution in the diversae. northeast region. In 1996, the second and Terrestrial herb, arising from fibrous third authors located a population in Per- roots and occasionally forming small tu- nambuco, growing in the municipality of bers, 0.5-1.5 cm wide~ stem 40-70 era, cy- Maraial. Detailed examination of the sub- lindric-angular, simple or rarely branched, terranean organs was done and small tubers green to purplish red, glandular-puberulous, were found hidden in the organic litter, glutinous and aromatic, internodes 5-7 cm; among fibrous roots. Another excursion to leaves decussate, subequal, often bearing the same locality was organized in 1998 shoots in the axils, petioles 3-6 cm, pur- and we gathered new morphological and plish red, pubescent, blades 6-9(-12) x 4- ecological observations. 7.5 cm, ovate, cordate at base, acute at DNA was extracted from dried leaves apex, margin irregularly toothed, teeth 3-6 sent by the second and third authors and X 3-9 mm, abaxial face green, puberulous, included in an ongoing molecular phylo- adaxial face pale green, glabrescent, 4-7 genetic study of the genus Sinningia (Per- lateral veins; 1-2 flowers borne in the upper ret, Savolainen, Chautems & Spichiger, un- axils and in bracts along an axis 12-25 cm publ. data). In the present work, we have long, pending from ascending pedicels, the selected a subset of the Perret et al. data set pedicels 2-3(-4) cm, glandular-pubescent, (viz., representing all tribes of the neotrop- calyx subeampanulate, glandular-pubescent, ical Gesneriaceae) and analyzed them in or- fused for 2 ram, lobes lanceolate, 4 x 2 der to define the position of this taxon from mm, puberulous, margin entire. Corolla tu- northeastern Brazil. Based on the cladistic bular, 2-2.8 cm long, with a 3 mm wide combined analysis of noncoding plastid annular swelling at base, abruptly narrowed DNA sequences, i.e., the two intergenes to 2 mm above, gradually widened to 7-8 atpB-rbcB and trnL-trnF and the rpll6 in- mm in throat, slightly grooved laterally to- tron, Sinningia nordestina emerges clearly ward base, yellow-orange in bud, at matu- nested among other congeneric species and rity scarlet-orange above, yellow with small within the tribe Sinningieae Fritsch (Fig. 1). red dots below, puberulent, throat yellow Although its relative position among the with dark red dots and glabrous, the lobes neighboring species is not yet clearly estab- erect to slightly spreading, subequal, 5 • 4 lished, there is enough evidence that this ram, the ventral one slightly larger, red out- species belongs to genus Sinningia. Select- side, yellow with red dots inside; ed species from all the tribes composing the 4, included, filaments white, glabrous, an- neotropical Gesneriaceae segregate into thers 2 X 1.5 mm, nectary a bilobed dorsal clades with high branch-support values gland, ovary conic, style and stigma slight- (bootstrap with 500 replicates) according to ly exserted. Fruit a capsule, conic, ca. 1 cm, the current classification (WieNer, 1983). ellipsoid, striate. 2000] CHAUTEMS ET AL.: GESNERIACEAE 51

Sinningia aggregata Sinningia valsuganensis Sinningia barbata Sinningia nordestina Sinningia harleyi 85 m I Sinningia elatior A 100 prasinata I , Paliavana sericiflora ! calcarata Sinningia buibosa purpurascens "--" I00 100 ~ " Koeilikeria erinoides B Smithiantha laui admirabilis 71 humilis __C cupreata j villosus ]~ mefittifofius reitzii -'qE i melancholica ""7IF saxorum Nicotiana FIG. 1. Strict consensus cladogram based on a phylogenetic analysis of the two intergenes atpB-rbcL and trnL-trnF, and the rpl-16 iutron combined: Sinningia nordestina nests among other congeneric species and within tribe Sinningieae. A = Sinningieae, B = Gloxinieae, C = Gesnerieae, D = Episcieae, E = Napeantheae, F = Beslerieae), G = subfam. Cyrtandroideae with Nicotiana as the outgroup; bootstrap values, based on 500 replicates, are indicated.

Additional specimens examined: BRAZIL. Alagoas: (IPA); Quipapfi, Engenho Brejinho, 15 Sep 1972, An- Quebr~ngulo, Reserva Biol6gica Pedra Talhada, drade Lima 72-7003 (IPA); Quipap~i, Eng. Pelada, 12 09~ 36~ 750 m, Oct 1994, Cervi et aL Jul 1950, Leal & Otavio 234 (RB); Ipojuca, Eng. Agua 6017 (G). Bahia: Praia de Monte Cristo, Bom Jesus Fria, 25 Jun 1968, Lira 68-269 (IPA); Maraial, Engen- dos Passos, terra~o de urea fal6sia de arenito, Jul 1995, ho Curtume, pr6ximo rio Pirangi, 08~ 35~ Santos 05 (ALCB). Cearfi: Unknown locality [label 260 m, 25 Aug 1996, Siqueira Filho & Baracho 096 unreadable], Jun 1854, Fr. Allemdo & Cysneiros 911 (UFP); Jaqueira, Serra do Espelho, Mata do Jasmim, (R); Serra de Baturit6, sftio B. Inficio de Azevedo, 26 Aug 1998, Siqueira Filho 815 (UFP); Maraial, af- 1938-39, Eugenio 1073 (RB); Viqosa Fragusso, 550 loramentos rochosos pr6ximos at rio, 5 Sep 1997, m, 21 Jun 1972, Sucre & da Silva 9268 (CEPEC, RB). Wanderley et aL 2248 (SP). Sergipe: Frei Paulo, 18 Paral'ba: Areia, ?~s margens da estrada para Alagoa Aug 1981, Viana 001 (ASE); Nossa Senhora da G16ria, Grande, 15 Jun 1992, Agra et aL 1461 (G); Areia, orla Viana 016 da mata, 28 Aug 1956, Moraes s.n. (SPSF); Areia, 21 Aug 1981, (ASE); Simao Dias, 3 Sep capoeira, 11 Aug 1957, Moraes s.n. (SPF). Pernam- 1981, Viana 042 (ASE); Frei Paulo, Faz. Serras Pretas, buco: Quipapfi, Usina Agua Branca, Faz. Pelada, 12 11 Aug 1982, Viana 613 (ASE); Serra de Itabaiana, 4 Jul 1950, Andrade Lima 50-597a (IPA); Caruaru, 10 Oct 1982, Viana 652 (ASE); Canhoba, Faz. Borda da Sep 1971, Andrade Lima 71-6468 (IPA); Altinho, Fa- Mata, 18 Sep 1984, Viana 1026 (ASE); Nossa Senhora zenda Tabocas, 29 Aug 1980, Andrade Lima et al. 20 da G16ria, Faz. Olbos d'./~gua, 1 Aug 1986, Viana 52 BRITTONIA [VOL. 52 2mm[ B

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FIG. 2. Sinningia nordestina. A. Habit: at left is upper portion of the plant, at right is the basal portion of stem with subterranian organs. B. Flower, side view. C. Flower, front view. D. Basal portion of corolla tube. E. Detail of calyx lobe. F. Anthers, dorsal view. G. Anthers, ventral view. H. Position of nectary. (A-H, Baracho & Siqueira Filho 663/704; details of subterranean organs based on slides taken in 1998 in the type locality).

1549 (ASE); S~o Miguel do Aleixo, Faz. Tanquinho, Distribution and ecology.--Sinningia 2 Aug 1986, Viana 1599 (ASE); Nossa Senhora da G16ria, Faz. Olhos d'Agua, 25 Aug 1987, Viana 1999 nordestina occurs in northeastern Brazil, (ASE). between and including the states of Ceani 2000] CHAUTEMS ET AL.: GESNERIACEAE 53 and Bahia, covering a range of some 1000 Sinningia nordestina differs from all re- km. The species has been found within lated species by having vestigial tubers, "caatinga" or "campos rupestre" vegeta- long ascending pedicels combined with tion type as well as in forested areas, on pendent fowers and rather short scarlet and rocky outcrops or arenitic soil, in semi- yellow corolla. It shares some characters shady and humid locations, at elevations with S. aggregata (Ker Gawl.) Wiehler, between 250 and 1050 m. It is frequently such as the glutinous and aromatic indu- associated with a kind of vegetation known ment, red and tubular corollas, but the latter as "brejos de altitude" in northeastern Bra- differs by having larger tubers (5-10 cm), zil (Sales et at., 1998). horizontally held flowers arranged in denser Etymology.--The specific epithet refers to inflorescences (usually 2-10 per axil), lon- its peculiar distribution in the northeastern re- ger corollas (2.5-4 cm) and distribution gion of Brazil, in contrast to the majority of from southeastern Brazil to Paraguay. species of Sinningia that occur in the south- eastern and southern region of Brazil. Acknowledgments Phenology.--Flowers from June to Oc- We are grateful to the curators of the her- tober. This is again in contrast with most baria indicated in the text for courtesies ex- other species of Sinningia whose flowering tended while studying their collections. We period extends from October to March in thanks the reviewers for constructive com- southeastern and southern Brazil, relative to ments on the manuscript. The Latin diag- the respective rainy seasons. nose was kindly revised by Rupert Barneby. Sinningia nordestina occurs as a rupico- The first author was partly supported for lous herb, growing in thin pockets of or- this research by the Swiss National Science ganic litter, forming dense populations in Foundation, grant 31-5238.97. patches. Numerous seedlings were ob- served suggesting that its survival during Literature Cited the dry season essentially relics on heavy Chautems, A. 1990. Taxonomic revision of Sinningia production. Preliminary experiments Nees: nomenclatural changes and new synonymies. on cultivated material revealed that, unlike Candollca 45: 381-388. all the other known Sinningia species, the . t991. Taxonomic revision of Sinningia Nees tubers were unable to resprout after a dry (Gcsneriaceae) 1I: new species from Brazil. Can- period (M. Peixoto, pers. comm.). If this dollca 46:411-425. 1995. Taxonomic revision of Sinningia Nees fact is confirmed by further observations, S. (Gesncriaceae) llI: new species from Brazil and nordestina would be the first species in the new combinations. Gesneriana I: 8-14. genus completely lacking perennial struc- --& A. Weber. 1999. Shoot and inflorescence ture. It would then behave as an annual in architecture in the neotropical genus Sinningia response to the northeastern Brazil climate, (Gesneriaceae). Pages 305-322. In: M. Kurmann & A. Hcmsley, editors. The Evolution of Plato Ar- where the rainy season takes place between chitecture. Royal Botanic Gardens, Kew. May and October, tollowed by a severe dry Faegri, K. & L. Van der Pijl. 1979. The principles period between November and April. of pollination ecology. Ed. 3. Pergamon Press, Ox- The shining red (almost fluorescent) co- ford. rollas, the lax inflorescence with obliquely Farr, E. F., J. A. I.eussink & F. Stafleu (eds.). 1979. Index Nominum Genericum (Plantarum). Vol. 2. pendent flowers, the production of nectar Bohn, Scheltema & Holkema, Utrecht. and the absence of floral odor agree with lloehne, F. C. 1970. lconografia dos Gesneriaceae do the syndrome typical for hummingbird pol- Brasil. lnstituto de Bot~nica, SSo Paulo, Brazil. lination (Faegri & Van der Pijl, 1979). Dur- Paxton, J. 1841. Gesnera zebrina. Paxton's Mag. Bot. 8: 271-272. ing field studies in the Maraial area (Per- Regel, E. 1878. Neue und empfehlenswerthc Zierp- nambuco), visits of Phaethornis ruber were flmlzen. Gartenflora 27: 278-288. recorded by the third author. Besides Sin- Sales, M. F., S. J. Mayo & M. J. N. Rod',d. 1998. ningia nordestina, few other in flow- Plantas vasculares das florestas serranas de i~crnam - er were available for . There- buco: um check-list da flora amea~ada dos brejos de altitude de Pernambucc>--Brasil. Universidade fore, this species of Gesneriaceae may well Federal Rural de Pernambuco, Recife. represent a key resource h~r the humming- Wiehler, H. 1983. A synopsis of neotropical Gesner- bird community during its flowering period. iaceac. Selbyana 6: 1-219.