Systematic Botany (2009), 34(3): pp. 505–509 © Copyright 2009 by the American Society of Taxonomists

A New of Rhipsalis (Cactaceae) from

Maria de Fátima Freitas,1, 3 Alice de Moraes Calvente ,2 and João Marcelo Alvarenga Braga1 1 Instituto de Pesquisas Jardim Botânico do , Diretoria de Pesquisa Científica, Rua Pacheco Leão 915, CEP 22460-030, Rio de Janeiro, RJ, Brazil 2 Laboratório de Sistemática Vegetal, Departamento de Botânica - IB, Universidade de São Paulo, Rua do Matão 277, CEP 05508-090, São Paulo-SP, Brazil 3 Author for correspondence ([email protected])

Communicating Editor: Daniel Potter

Abstract— A new species of Rhipsalis (Cactaceae) from Rio de Janeiro State, in southwestern Brazil, is described and illustrated. The new Rhipsalis aurea is circumscribed in the subgenus Erythrorhipsalis and is morphologically most similar to R. pulchra Loefgr., but is distinct by the smaller, sub- erect habit, smaller secondary stem segments of determinate growth, golden yellow , depressed-globose fruit, and epidermis and pollen grain features. Following the IUCN criteria this new species is vulnerable due to its restricted area of occurrence and reduction of the quality of habitat observed in the pres- ent and projected for the future. A taxonomic key to the subgenus Erythrorhipsalis is included. Keywords— Atlantic forest , endemic , neotropical , new species , .

Cactaceae is composed of more than 1,500 neotropical spe- the subgenus Erythrorhipsalis together with the most simi- cies. Only (J.S. Muell.) Stearn exceeds this lar species R. pulchra Loefgr., based on the arrangement and distribution, occurring in and part of Asia ( Barthlott shape of the flowers. 1987). The main centers of biodiversity and endemism of Cactaceae are located in Mexico and the southwestern U. S. A., Materials and Methods the Andes, and Brazil. In Brazil two centers of endemism can be found, the northeastern Brazilian arid region and the The morphological descriptions and comparisons are based on obser- Brazilian Atlantic Forest, which is remarkable for the diver- vations of Rhipsalis specimens in herbaria HB, HBR, MBM, R, RB, SP, SPF ( Holmgren et al. 1990 ), and of fresh specimens using a stereomicroscope. sity and endemism of epiphytic cacti ( Taylor and Zappi 2004 ). Materials preserved in 70% ethanol (Rhipsalis pulchra : Calvente 231 , 232 ; The most representative epiphytic in this region R. aurea : Calvente 156, 157 ; SPF) were used for scanning electron micros- is Rhipsalis with 37 species, 30 of which occur there as endem- copy (SEM) analysis. For the preparation of the epidermis samples the ics ( Barthlott and Taylor 1995 ). material was kept for 72 hr in chloroform to remove the epicuticular wax and critical point dried before metallization. The Brazilian Atlantic Forest is an endangered biodiversity and endemism hotspot (Mittermeier et al. 2000). The grow- ing deforestation and accelerated urbanization of this forest Taxonomic Treatment is threatening the maintenance of the genetic diversity of sev- eral groups of organisms and in some cases even the survival Rhipsalis aurea M. F. Freitas & J. M. A. Braga, sp. nov.— of many species. That is the case for many Rhipsalis species, TYPE: BRAZIL. Estado do Rio de Janeiro, município de which are commonly even more restricted to specific altitude Nova Friburgo, Macaé de Cima, estrada de acesso pela ′ ′ or climatic conditions inside their areas of occurrence. Eight BR 116, 22°21 50”S, 42°30 08”W, 1201 m alt., 27 Oct 2004, Rhipsalis species are already listed as threatened in the Atlantic J. M. A. Braga 7494 (holotype: RB!; isotype: R!). Forest and ten do not yet have conservation status defined Haec species a R. pulchra Loefgr. similis, sed ab ea habito sub- ( Taylor 1997 ; Calvente et al. 2005 ). Thus, increasing the knowl- erecto minore, segmentis secundariis caulis minoribus, crescen- edge of the Atlantic Forest flora is one important step to encour- tia definita, perigonio flavo-aureo, fructu adpresso et globoso age its conservation and the maintenance of its biodiversity. distinguitur. The circumscription of Rhipsalis is mostly unchanged fol- Rupicolous or epiphytic, 60–80 cm long. Roots stiff, grayish lowing the synopsis proposed by Barthlott and Taylor (1995 ), white, adventitious roots absent. Branches suberect to almost but three new species of Rhipsalis have been described and one horizontal or slightly pendent, erect when young, branching rediscovered since then ( Taylor and Zappi 1997 ; Taylor 2003 ; subacrotonically or mesotonically. Stem segments cylindri- Calvente and Andreata 2007). The species are distributed in five cal; primary of indeterminate growth, basal 15–45 cm long, subgenera, Rhipsalis , Calamorhipsalis K. Schum., Epallagogonium 4–6 mm diam, suberect, stiff, woody; subsequent 3–4, 14–20 cm K. Schum., Phyllarthrorhipsalis Buxb., and Erythrorhipsalis A. long, 3.7–4.7 mm diam, suberect, stiff but succulent, dark Berger, based on a combination of vegetative and reproduc- green; secondary smaller, of determinate growth, 2–9 cm tive morphological features. The shape of the stem segments, long, 1.2–3 mm diam, pendent, succulent, dark green. Areoles branching patterns, and the position and shape of flowers are ca. 0.5 mm diam, green, reddish or brown; scales 1–2, ca. 0.5 × the main characters used for separation of the subgenera, while 1 mm, triangular; hairs absent in mature segments and pres- differences in relative lengths of primary and secondary stem ent in young segments. Flowers 1.6–1.7 × 1.5–2 cm at anthe- segments, and colors, shapes and sizes of flowers and fruits sis, campanulate, not conspicuously immersed in the areoles; are used to separate species. Recent studies have pointed out absent to 1 per areole, diurnal, inodorous, mostly subapical that epidermal features provide important information for the or lateral, oblique to slightly perpendicular to the stems; peri- separation of Rhipsalis taxa (Calvente et al. 2008). carpel 0.2–0.3 × 0.4 mm, green to yellow, turbinate, distinctly In this work we describe Rhipsalis aurea, a new species from truncate; perigonium segments golden yellow, immaculate, Rio de Janeiro State distinguished by its unique combination membranaceous, 0.2–1.3 × 0.3–0.6 mm, gradually longer and of morphological characters. The new taxon is positioned in thinner towards the center, suborbicular, triangular to oblong,

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Fig . 1. Line drawing of Rhipsalis aurea M. F. Freitas and J. M. A. Braga. A. Suberect habit. B. Branches with flowers and immature fruits. C. Young stem segment displaying areoles with hairs. D. Disposition of hairs in young areoles. E. not conspicuously immersed in the areole. F. Longitudinal section of flower. G. Immature, cupulate, strongly truncate fruit (Braga 7494 ). 2009] FREITAS ET AL.: NEW SPECIES OF RHIPSALIS 507

Janeiro State, located in the Serra dos Órgãos. It occurs in high altitude forest between 1,200 and 1,700 m elevation. The vegetation of this region is the Brazilian Atlantic Forest where epiphytic Cactaceae are an important component (Calvente et al. 2005). Rhipsalis is particularly well represented in the epiphytic flora of this vegetation and in the Nova Friburgo region nine species are found (Freitas 1996; Fontoura et al. 1997; Calvente et al. 2005). In addition to housing a state park, Nova Friburgo area is known for its rural activities and many agricultural and cattle raising farms are found there. Two of the locations where the new species was found show no ade- quate conservation conditions. One of them is adjacent to an access road (Braga 7494) and the other one is next to a pas- ture inside the main site of the park (Calvente 156 , 157 ). These populations should be monitored to have their conservation assured. Following the IUCN (2001 ) criteria this new spe- cies is vulnerable (VU, B1abiii, iv) due to its restricted area of occurrence and reduction of the quality of habitat observed in the present and projected for the future. The newly described species belongs the subgenus Eryth- rorhipsalis, which is morphologically distinct in having cam- panulate flowers not conspicuously immersed in the areoles ( Barthlott and Taylor 1995 ). Wihtin this subgenus, R. aurea is most similar to R. pulchra, having mesotonically to subacro- tonically branched stem segments, the primary of indeter- Fig . 2. Photographs of Rhipsalis aurea M. F. Freitas and J. M. A. Braga. minate growth (i.e. with variable length), and characteristic A. Epiphytic plant with flowers and immature fruits. B. Golden-yellow flower. C. Floral bud. D. Mature fruit. Note that the fruit is transluscent oblique campanulate flowers. However, R. aurea is distinct ( Braga 7494 ). in having the primary stem segments stiff and the second- ary stem segments smaller and with determinate growth apex rounded, external spreading to suberect, internal erect. (Figs. 1– 2 ). These stem characters are also reflected in a quite dis- polystichous spreading or with a discrete separation tinct habit: while R. pulchra is long pendent, R. aurea is smaller of the internal facing outwards and external facing inwards, and suberect. In addition, R. aurea is markedly different in its yellow; filaments 4–7 mm long; anthers 0.5–0.6 mm long. golden yellow flowers and by the depressed-globose trans- Ovary 1.7–2 mm long, turbinate; style 8 mm, yellow; stigma lucent green fruits. Rhipsalis pulchra has pinkish-white flow- 4–6 lobed, 2 mm long, yellow, oblong, patent. Fruit indehis- ers and dark purple to white fruits ( Table 1 ). Loefgren (1915 ) cent, glabrous: when immature cupulate, strongly truncate, described R. pulchra originally from Serra da Mantiqueira, but green; when mature 6–7.7 × 6–8 mm, depressed-globose, it can also be found in the Serra dos Órgãos. translucent green. Figures 1 – 2 The mesotonic to subacrotonic branching pattern of both Additional Specimens Examined—BRAZIL. Estado do Rio de Janeiro, R. aurea and R. pulchra are characteristic of species of Lepis- município de Nova Friburgo, Macaé de Cima, pr. Friburgo, 1,600 m alt., mium Pfeiffer as defined by Barthlott (1987). However, nei- 4 Oct 1959, G. F. J. Pabst 5178 (HB, HBR); Sítio Sophronites, 5 Oct 1987, ther species has the connate petals forming a floral tube and G. Martinelli 12252 (RB); Parque Estadual dos Três Picos, Sítio Vale dos Sonhos, 22°19′43.6”S, 42°43′27.5”W, 1,702 m alt., 23 Nov 2005, A. M. Calvente the angular pericarpel considered to be diagnostic features and L. M. Versieux 156, 157 (RB, SPF). for Lepismium species ( Barthlott 1987 ). The flowers of R. aurea are similar to the flowers of salicornioides (Haw.) Britton & Rose in shape and color. However, the morphologi- Discussion cal characters of R. aurea do not match the features of Hatiora Rhipsalis aurea is a microendemic, rare plant. It is known Britton & Rose, all species of which have all stem segments only from five collections from three different localities in with determinate growth and terminal flowers ( Barthlott and the Três Picos State Park in the city of Nova Friburgo, Rio de Taylor 1995 ).

Table 1. Morphological comparison between R. aurea and R. pulchra .

R. aurea R. pulchra Habit Smaller and suberect Long pendent Stems Primary stiff, with indeterminate growth; secondary smaller, with All long, with indeterminate growth determinate growth Flower Golden-yellow White to pinkish Stamens Polystichous spreading or with discrete separation of the internal Inner stamens faced outwards, outer stamens facing inwards facing outwards and external facing inwards Fruit Depressed-globose, translucent green Globose to elongate-globose, dark purple to whitish Epidermis With smaller stomata at the same level as epidermis cells Sunken bigger stomata complex Pollen grains Isolated with exine spiculate Isolated or in tetrads, with exine punctate, without spicula 508 SYSTEMATIC BOTANY [Volume 34

Fig . 3. Scanning electron micrographs. A-D. Rhipsalis aurea ( Calvente 156 , 157). A. Epidermis 60×; B. Epidermis with stomata 500×; C. Pollen grain 3,000×; D. Pollen grain with spiculate exine 5,000×. E-H. R. pulchra ( Calvente 231 , 232 ); E. Epidermis 60×; F. Epidermis with sunken stomata complex 500×; G. Pollen tetrad 1,000×; H. Pollen grain with punctate exine 5,000×.

Epidermis anatomy has proved useful for separating closely onym of R. floccosa subsp. pulvinigera (G. A. Lindb.) Barthlott allied Rhipsalis species (Calvente et al. 2008). Epidermis and & N. P. Taylor. and the specimen at HBR was labeled R. rigida pollen grain features also segregate R. aurea from R. pulchra. Loefgr., a synonym of R. dissimilis (G. A. Lindb.) K. Schum. The epidermis of R. aurea has smaller stomata located at the Both identifications are erroneous since these specimens do same level as the regular epidermal cells, differing from the not have the morphological features of either R. floccosa or bigger sunken stomata complex found in R. pulchra ( Fig. 3 ). R. dissimilis, two species that belong to subgenus Epallagogonium In addition, pollen grains of R. aurea are solitary and the and have flowers conspicuously immersed in the areoles. exine is conspicuously spiculate, unlike the pollen grains on Later, three new collections made it possible to describe R. pulchra , which are isolated or in tetrads. The exine of the lat- R. aurea as a new species and enabled the link with the collec- ter species is punctate and does not possess spicules (Fig. 3). tion of Pabst 5178. The specific epithet aurea was chosen as an The first collection of R. aurea was made in 1959 (Pabst 5178 ) allusion to the golden yellow flowers, not found in any other and was kept in the herbaria HB and HBR. The specimen in HB Rhipsalis species. The flowering period of R. aurea is during was originally identified as R. gibberula F. A. C. Weber, a syn- the spring and early summer from October to November.

Key to the Subgenus E RYTHRORHIPSALIS 1. Terminal stem-segments angled/ribbed or cylindric, stem areoles bristly and hairy yet ...... 2 2. Terminal stem-segment short, branched, erect, 2–3 cm long, pericarpel naked, fruit white ...... R. cereuscula Haw. 2. Terminal stem-segment long, pendent, up to 3 cm long, pericarpel with long bristles, fruit pink ...... R. pilocarpa Loefr. 1. Terminal stem-segments cylindric or clavate, areoles naked or with minute trichomes when young ...... 3 3. Stem-segments clavate, fruit white to pale pink ...... R. clavata F. C. A. Weber 3. Stem segments cylindric, fruit whitish green to red ...... 4 4. segments white and stamens red at base ...... R. campos-portoana Loefg. 4. Perianth segments white, yellow or pinked, and stamens yellow to orange ...... 5 5. Perianth segments golden yellow; fruits depressed globose, translucent ...... R. aurea M. F. Freitas & J. M. A. Braga 5. Perianth segments white or pink; ovoid, fruits purplish or whitish ...... 6 6. Branching mesotonic, flowers lateral, filaments orange ...... R. pulchra Loefr. 6. Branching acrotonic, flowers apical, filaments white to purplish ...... 7 7. Stem-segments purplish, fruit brilliant purplish magenta ...... R. burchellii Britton & Rose 7. Stem-segments green, fruit green tinged maroon-purplish ...... 8 8. Perianth segments all white ...... R. juengeri Barthollot & N. P. Taylor 8. External perianth segments magenta ...... R. ormindoi N. P. Taylor & Zappi

Acknowledgments . The authors wish to thank Programa Mata Leonardo Versieux for suggestions on the manuscript and field assistance; Atlântica, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Brazil, Paulo Ormindo for the line drawing; and Laboratório de Microscopia for the support on field studies; Dr. Jorge Fontella Pereira for the assis- Eletrônica of the Instituto de Biociências of the Universidade de São tance in the Latin diagnosis; Fapesp for the grant to the second author; Paulo. 2009] FREITAS ET AL.: NEW SPECIES OF RHIPSALIS 509

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