Bauhinia proboscidea P. Juárez, R., 2018

Juárez, Pedro, Flores, Rodolfo & Blanco, Mario A., 2018, Bauhinia proboscidea (Fabaceae: Cercidoideae), a new species from Costa Rica and Panama, with notes on B. beguinotii, B. gorgonae and B. pansamalana, Phytotaxa 361 (1), pp. 25-40 : 27-32

Bauhinia proboscidea P. Juárez, R. Flores & M.A. Blanco, sp. nov. ( Figs. 1 , 2 )

Similar to Bauhinia pansamalana but differs from that species by its shorter petioles, more elongate leaf blades, inflorescences with 2 (rarely up to 8) flowers, larger flowers, longer fruits and allopatric, more southern geographic distribution.

Type:— COSTA RICA. Prov. Puntarenas: cantón Osa, distrito Drake, poblado Rancho Quemado , cerca de la toma de agua, bosque primario, ribera de una quebrada, 210 m, 8°40’58.30’’ N, 83°33’36.85’’ W, 4 May 2014 (fr.), Juárez 420 (holotype: USJ!; isotypes: CR!, MO!) .

Shrubs or small trees (occasionally reportedly semiscandent), conforming to Troll’s architectural model, 4–12(–21) m tall (but see comments) × 10–25 cm at breast height when reproductive, andromonoecious. Stems plagiotropic, with distichous, alternate phyllotaxy; green, slightly compressed, fractiflex and glabrous when young; becoming cylindrical with age; bark smooth to striate, lenticelate, light brownish-gray. Leaves simple; petiole bituminous, 10–20 × 1–3 mm; blade chartaceous, entire, ovate, (2.5–) 5–30 × (1.2) 2–9 cm, basally cuneate to rounded, sub-truncate, obtuse, or slightly acute, apically acuminate or bifid, glabrous on both surfaces, margin entire; venation acrodromous, primary nerves 5, the 3 central ones reaching the blade apex, secondary nerves irregularly perpendicular to the primaries, tertiary venation reticulate; stipules ovate, subulate, acute, up to 1 × 0.5 mm, early-caducous; intrastipular spines subconical, acute, up to 1.5 mm long × 0.4 mm in diameter on the dorsal (upper) side of branches, up to 2.5 mm long × 0.8 mm in diameter on the ventral (lower) side of branches. Inflorescences both axillary and terminal; terminal ones occasionally displaced laterally by the axillary branch of the last leaf and thus appearing leaf-opposed, racemose, rarely branched, sequentially flowered, with 1–2 (–8) flowers, usually only the first flower hermaphroditic, the subsequent flowers staminate; rachis 1–3 cm long; floral bracts broadly triangular, 1 × 3 mm, minutely strigose; bracteoles ovate, 1.5 × 1.3 mm, minutely strigose, located at the base of the pedicel, adjacent to the floral bract. Flowers zygomorphic to slightly asymmetric, either hermaphroditic or staminate. Pedicel 3–6 mm long × 1.5–2.5 mm in diameter, minutely strigose. Flower buds botuliform, up to 5 cm long × 4–5 mm in diameter just before anthesis, pale green. Hypanthium tubular, 8–15 mm long × 4.5–5 mm in diameter externally, 7 mm long × 2 mm in diameter internally. Calyx spathaceous, formed by 5 connate sepals, 2.5–5.5 × 0.6–1.2 cm, straight or reflex, minutely striate, minutely strigose abaxially, glabrous adaxially, dehiscing along one or two sepal margins (usually one of the lowermost 3 sepals, and thus opening obliquely in relation to the rest of the flower), occasionally dehiscing along an additional sepal margin, and frequently splitting incompletely along the basal margins of other sepals. Petals 5, erect to suberect, subequal or the 2 lowermost ones smaller, 28–63 × 1.5–5 mm, narrowly spathulate, apically acute, glabrous, white with a green middle vein and yellowish secondary veins, becoming pink on the second day of anthesis. Stamens 10, heterodynamous, in 2 whorls of 5 each; the 3 lowermost of the external whorl fertile, the rest staminodial; filaments dark red, glabrous, connate, forming a staminal tube 15–20 mm long × 3–3.5 mm in diameter; filaments of fertile stamens projecting 30–42 mm beyond staminal tube, those of hermaphroditic flowers strongly recurved to coiled so that the anthers lie under (or to the side of) staminal tube, those of staminate flowers straight, slightly incurved apically so that the anthers face the tip of the pistillode; filaments of staminodes projecting 1–11 mm beyond staminal tube; fertile anthers linear, dorsifixed, introrsely longicidal, margins minutely villous, grayish pink externally, white internally, 7 × 1 mm each, connate, forming an oblong pseudosynanther 7 × 3 mm; abortive anthers (of staminodia) narrowly ellipsoid to sagittate or absent, minutely villous when present, up to 1.5 × 0.5 mm; pollen white. Gynoecium of 1 carpel, stipitate; fertile pistil (of hermaphroditic flowers) 30–62 mm long; gynophore ca. 10 mm long, glabrate; ovary narrowly oblong, strigillose, whitish, 18–20 × 2–3 mm deep × 1 mm thick; style ca. 5 mm, glabrate, incurved; stigma facing the flower base due to the curvature of the style, oblong, green, ventrally papillose, dorsally glabrous, 6–7 × 2 mm; pistillode (of staminate flowers) linear, whitish with green margins, 15–30 × 1.5–2 mm. Fruits ensiform to falcate, flattened, basally obtuse to acute, stipitate (gynophore 2.5–3 cm), apically rostrate with the persistent style, (12–)20–35 × 3 cm, glabrous, pendulous, green when immature, drying brown to blackish when mature, with 8–12 seeds, dehiscing through both the ventral and dorsal sutures, valves becoming helically coiled. Seeds sub-elliptic, slightly lenticular, ca. 1.5–2 × 1–1.5 cm, dark brownish, shiny. Seedling erect; cotyledons unknown; eophylls (first leaves after cotyledons) opposite, blade chartaceous, sub-quadrate, 4.2–4.5 × 5.1–5.3 cm, 5-nerved, each of the 4 lateral nerves terminating in a 2.2–3.5 cm long acumen extending from the blade, the central nerve terminating in a 1–2 mm long apiculus.

Distribution and habitat:— Bauhinia proboscidea occurs on the Pacific slope of central and southern Costa Rica and extreme western Panama. It has been collected in many localities in the Costa Rican provinces of Puntarenas and San José, and from a single locality in the Panamanian province of Chiriquí, in the Burica Peninsula, adjacent to the Costa Rican border ( Figure 3 ). Unaware of the recent Panamanian collections, Zamora (2010) considered B. proboscidea (as Bauhinia sp. B ) as a Costa Rican endemic. Bauhinia proboscidea grows in primary and secondary moist forest and rain forest at elevations of 200–1300 m, frequently near streams.

Phenology:—Flowering has been recorded during both dry and rainy seasons, from January to May and August to September. Fruiting specimens have been collected from January to August. A small tree now in cultivation at Lankester Botanic Garden has flowered more or less continuously after reaching a height of ca. 70 cm. Presence of seedlings has been documented in July (based on the seedling included in Valverde 1060, US).

Observations on reproductive biology:—Anthesis apparently begins during the night or just before dawn. The petals stay erect and in good condition for ca. 15–20 h (if protected from the sun or heavy rain), and then shrivel, turning pinkish or magenta before falling (in hermaphroditic flowers). On the second day of anthesis the anthers (in hermaphrodite flowers) shrivel, but the stigma remains in good condition and apparently receptive. Flowers abscise on the third day of anthesis.

Most inflorescences in Bauhinia proboscidea are two-flowered. Observations made on numerous inflorescences produced by the small tree cultivated at Lankester Botanic Garden indicate that most flowers are staminate, and when hermaphroditic flowers are produced, they are usually the first of the pair to open. Very rarely two hermaphroditic flowers are produced on the same inflorescence.

Pollinators are unknown, but the floral morphology suggests adaptation to either hawk-moths or hummingbirds. Flowers of the related Bauhinia pansamalana , which have the same basic morphology, are visited by hummingbirds, according to Wendt et al. 3399 (MEXU). Bauhinia curvula Bentham in Martius (1870: 194), which has flowers with a similar morphology, is pollinated by hawk-moths in Brazil ( Munin et al. 2008). As in other species of Bauhinia , fruits of B. proboscidea are explosively dehiscent, and several herbarium specimens show open fruits with coiled valves.

Etymology:—The specific epithet refers to the prominent staminal tube and the projecting pistil (the latter in hermaphroditic flowers), which together resemble a snout or proboscis of an animal. The recurved fertile stamens of hermaphroditic flowers also bear a superficial resemblance to the tusks of elephants Loxodonta spp. , order Proboscidea ).

Comments:—Although at least two dozen previous Costa Rican herbarium collections of Bauhinia proboscidea are known, the earliest dating from 1989, few of them have flowers and these are poorly preserved. During a plant collecting trip to the Osa Peninsula in 2014, a fruiting specimen of this taxon was collected (P. Juárez 420). One seed of that specimen was planted and eventually grew; two years later the young plant (vouchered by Juárez 1241) started blooming, and provided plenty of flower material for a detailed description. This plant is now in cultivation at Lankester Botanic Garden of the University of Costa Rica.

Bauhinia proboscidea is apparently not rare, judging from the quantity of available herbarium specimens. As in other arborescent species of Bauhinia , the vegetative morphology and development of B. proboscidea conform to Troll´s architectural model ( Hallé et al. 1978). Valverde 1060 describes the plant as a 21 m tree, which would make it one of the tallest arborescent Bauhinia in Central America; however, we suspect this could be an error, as all other specimens of B. proboscidea describe the plant height as 4– 12 m. The seedling description is based on the one included with the specimen Valverde 1060 at US (image available at https://collections.nmnh.si.edu/search/botany/).

The “intrastipular spines” of Bauhinia proboscidea and those of some other species of Bauhinia s.s. are glandular and secrete tiny drops of nectar (van der Pijl 1951, Dubey et al. 1990, Rezende et al. 1994, P. Juárez & M.A. Blanco, personal observation), possibly as a reward for ants that defend the plants against herbivores. Marazzi et al. (2012: Fig. 2 ) documented this phenomenon for B. macranthera Bentham ex Hemsley (1880: 49) but confused the structures with stipules. In his detailed review of the morphology of Bauhinia s.l., Urban (1885: 82–85) stated that these projections, seemingly unique among seed plants, originate from the axil of the true stipules (which are often caducous), and considered them to be derived from the intrastipular trichomes (colleters) present in other species of the genus. However, González & Marazzi (2018) showed that the corresponding structures (which they call prickles) in B. forficata Link (1821: 404) subsp. pruinosa ( Vogel 1839: 301) Fortunato & Wunderlin (in Fortunato 1986: 550) do not arise from the axils of the stipules (which are occupied by colleters), but arise from each side of the leaf base instead, just below the stipules. Thus, the homology of the “intrastipular spines” of Bauhinia remains unsettled. In this regard, it is interesting to note that similar, paired, spinescent projections borne from either side of the petiole base, adjacent to stipules (and often confused with them), occur in some unrelated members of Fabaceae (e.g., Prosopis juliflora ( Swartz 1788: 85) de Candolle (1825: 447) and most other species of Prosopis section Algarobia de Candolle (1825: 446) , Robinia pseudoacacia Linnaeus (1753: 722) , Vachellia seyal ( Delile 1813: 286) Hurter (in Mabberley 2008: 1021); Burkart 1937, Bell & Bryan 2008, Sharma & Kumar 2012), and may represent modified short, leafless shoots produced by accessory, collateral, displaced axillary buds (sensu Bell & Bryan 2008; also Burkart 1937).

As in other species of Bauhinia , B.proboscidea produces both hermaphroditic and staminate flowers (see Wunderlin 1983, Tucker 1988, Torres Colín 1999). Bauhinia s.l. shows a variety of floral morphologies and arrangements of stamens and staminodes ( Urban 1885, Endress 1994); we provide a floral diagram of B. proboscidea ( Fig. 1F ) for comparison with Figs. 11–19 in Urban (1885). The petals of B. proboscidea fall easily if the flower-bearing branch is cut; this probably explains why herbarium collections with complete flowers in good condition are scarce in this species.

Conservation status:—With an EOO of 8,347.21 km 2, an AOO of 52 km 2, and known from 11 localities (10 in Costa Rica, one in Panama), of which four are protected areas (three in Costa Rica, one in Panama), our global-level assessment for Bauhinia proboscidea shows that this species fits the category of Least Concern (LC) of the IUCN Red List. Our national-level assessment for Costa Rica also places it in the LC category (EOO= 6,075.06 km 2, AOO= 48 km 2).

For Panama, however, the national-level assessment categorizes this species as Endangered [EN B2ab (ii, iii, iv)] because of its restricted AOO (4 km 2) and the severe threats facing its only known population. The El Chorogo forest, which extends for ca. 10 km in a narrow strip on the Panamanian side of the Burica Peninsula along the border with Costa Rica, is in an isolated hilly area (150–689 m elevation) and contains the largest forest remnant (ca. 800 ha) of the Pacific slope lowlands in extreme western Panama ( Flores et al. 2016). This is the only place in Panama where 12 species of birds globally restricted to the South Central American Pacific Slope Endemic Bird Area (BirdLife International 2017) occur; thus, it has been designated a National and Global Important Bird Area ( Angehr 2003). It also contains a population of the similarly restricted and globally endangered Red-Backed (or Central American) Squirrel Monkey ( Angehr 2003). The only part of this forest under official protection is that within the Audubon-El Chorogo (178 ha) and San Bartolo (105 ha) Private Nature Reserves. The remaining forest is privately owned by various farmers, has no formal protection and is in danger of being deforested for cattle ranching and other agricultural pursuits, or for selective logging.

Additional specimens examined (paratypes):— COSTA RICA. Cultivated: [Germinated from seeds of the type collection; cultivated at San Rafael de Heredia, later planted at Lankester Botanic Garden], 1 July 2016, Juárez 1241 (USJ-spirit). Puntarenas: Buenos Aires , Cuenca Térraba-Sierpe , Potrero Grande , La Lucha , alrededores de Rancho Amuo, 1000–1100 m, 9º06’ N, 83º06’ W, 18 February 2008 (fr.), Santamaría 6989 ( CR, CR-INB, PMA) ; same locality, 3 November 2010 (sterile), González et al. 1862 ( CR-INB) ; same locality, 3 November 2010 (sterile), González et al. 1863 ( CR-INB) ; same locality, 3 November 2010 (sterile), González et al. 1864 ( CR-INB) ; same locality, 3 November 2010 (sterile), González et al. 1865 ( CR-INB) ; Bueno Aires, Cuenca Térraba-Sierpe. Potrero Grande, Lodge Monte Amou , La Lucha, Sendero Quiero a 2.5 km de La Lucha, 1100 m, 9º06’ N, 83º06’ W, 22 Febrary 2000 (fl., fr.), Aguilar 5989 ( CR, CR-INB, MO) ; Golfito, Dos Brazos de Río Tigre, Jiménez , Cerro Müller , bajando por la fila a los afluentes de Río Niño , 400–744 m, 8º30’ N, 83º28’ W, 30 August 1990 (fr.), Herrera & Fallas 4173 ( CR, CR-INB, MO) ; Osa, Parque Nacional Corcovado, Sirena , Los Patos , Mirador Trail , 200–300 m, 8º41’40” N, 83º34’48” W, 26 October 1989 (fl.), Kernan 1303 ( CR-INB, K) ; Osa, Aguabuena, cuenca superior de la Quebrada El Campo , Rincón , 300 m, 8º42’35” N, 83º31’50” W, 1 October 1990 (fl., fr.), Herrera 4421 ( CR, K, USJ) ; Osa, Rancho Quemado, Sierpe. siguiendo el camino a Drake , cabeceras de Río Drake , 400 m, 8º41’ N, 83º35’ W, 18 June 1990 (fr.), Herrera 4204 ( CR, CR-INB, MEXU, USJ) ; Osa, Reserva Forestal Golfo Dulce, Rancho Quemado centro, 300 m, 8º41’40” N, 83º33’35” W, 15 December 1991 (fr.), Aguilar 751 ( CR, CR-INB, MO) ; Osa, Sierpe, Agua Buena , bosques al Noreste de la Fundación Neotrópica , 290 m, 8º42’36.31” N, 83º31’21.30” W, 15 September 2013 (sterile), Jiménez & Juárez 1733 ( USJ) ; Osa, Sierpe, Campo de Aguabuena , Parcela Proyecto BDEF, 95 m, 8º42’11” N, 83º31’05” W, 30 January 2013 (sterile), Chacón et al. 1613 ( USJ) ; Osa, Palmar Norte, bosque aledaño a la toma de agua potable, faldas de Fila Retinto, 700 m, 08°57’36”N, 83°27’36”W, 13 May 1992 (fl., fr.), Jiménez 1077 ( CR, CR-INB, MEXU, MO, USJ). San José: Acosta , cuenca del Pirrís-Damas, Fila Ayarales, falda NE, Quebrada Ayarales, camino al Cornelio, 1250–1300 m, 9º43’ N, 84º12’ W, 13 May 2001 (fl.), Morales 8050 ( CR-INB, K, MO, USJ) ; Acosta, Fila Bustamante , 3 km NO Hacienda Tiquires, Cerro El Cornelio, faldas Fila Aguabuena , 1300 m, 9º42’ N, 84º13’ W, 16 December 1994 (sterile), Jiménez 1699 ( CR, CR-INB) ; Acosta, Fila Bustamante, Tiquires , bosque primario en el camino a Zoncuaco, cerca del paso sobre la quebrada El Ayaral , hasta cerca del cruce, 1100–1250 m, [9°43’N 84°12’W], 4 June 1995 (sterile), Morales 4343 ( CR-INB, MO) ; Aguirre, Londres, estribaciones de Cerro Nara , 800 m, 9º29’30” N, 84º01’30” W, 13 May 1994 (fr.), Herrera 7030 ( CR) ; Aserrí, cuenca del Pirrís-Damas, Fila Agua Buena , Quebrada Laja , 1100–1200 m, 9º40’ N, 84º11’ W, 23 January 2003 (fr.), Morales & Hammel 9060 ( CR-INB) ; Aserrí, cuenca del Pirrís-Damas, entre Escuadra y Zoncuano por Hacienda Tiquires , 1000–1500 m, 9º40’ N, 84º11’ W, 28 June 1995 (fr.), Hammel 19896 ( CR, CR-INB, K, MO) ; Dota, San Isidro, Zona Protectora Cerros Nara , 900–1000 m, 9º29’40” N, 84º00’50” W, 21 July 1998 (fl., fr.), Valverde 1060 ( CR, US, USJ) ; Dota, Copey, área no protegida, La Chaqueta , márgenes de Río Savegre , 750 m, 9º29’55” N, 83º54’50” W, 16 May 2002 (fr.), Estrada & Bustamante 3271 ( CR, K, MO, US) ; Tarrazú, San Lorenzo, área no protegida, Cerro Diamante , 600–900 m, 9º32’40” N, 82º02’30” W [erroneous coordinates; actual approximate coordinates: 9.554985 -84.043280], 9 February 1992 (fr.), Estrada 2097 ( CR) ; Tarrazú, cuenca del Naranjo y Paquita , 2.5 Sur de Napoles, sobre la carretera de San Marcos de Quepos , 1300 m, 9º35’ N, 84º04’ W, 17 February 1998 (fl., fr.), Rodríguez et al. 3039 ( CR, CR-INB, MO). PANAMA. Chiriquí: Distrito de Barú , Corregimiento de Puerto Armuelles , Reserva Natural Privada Audubon-El Chorogo, 547 m, 8°17’26.4” N, 82°59’52.4” W, 1 April 2016 (fl, fr) Flores et al. 3835 ( PMA, SCZ, UCH) ; same locality, 1 April 2016 (sterile), Flores et al. 3836 ( PMA, SCZ) ; Punta Burica, El Chorogo, desde la finca de Fernando Chavarría hacia la trocha en límite fronterizo, altos de la Laguna, Finca Audubon , 16 May 2007 (fr.), Aranda et al. 3921 ( SCZ) .

Figures

FIGURE 1. Bauhinia proboscidea. A. Fruiting branch. B. Perfect (hermaphrodite) flower; note recurved fertile stamens and incurved style. C. Staminate flower; note apically incurved fertile stamens. D. Apex of staminodes and bases of free portion of filaments of fertile stamens in staminate flower. E. Apex of fertile stamen filaments and anthers of staminate flower. F. Floral diagram of perfect flower. G. Pair of intrastipular spines at a node (leaf scar on opposite side of stem, not visible), with liquid secretion. A based on type specimen (Juaìrez 420, USJ, CR, MO); B–F based on photographs of Juárez 1241 (USJ). Drawn by P. Juaìrez.

FIGURE 2. Bauhinia proboscidea. A. Staminate flower. B. Perfect (hermaphrodite) flower. C. Apex of fertile stamens of staminate flower with incurved filaments and open anthers. D. Detail of perfect flower, showing recurved fertile anthers and pistil with incurved style. E. Detail of staminodes (red and yellow, with white abortive anthers), filaments of fertile stamens (dark red) and pistillode (green) in staminate flower. F. Immature fruits. G. Two-flowered inflorescence, with one perfect flower and one staminate flower; the perfect flower (left) has already shed its petals. H. Detail of stem node showing intrastipular spine with liquid secretion. F from Flores et al. 3835 (PMA) by R. Flores; all other photos from Juárez 1241 (USJ) by P. Juárez.

FIGURE 3. Distribution map of Bauhinia beguinotii, B. gorgonae, B. pansamalana and B. proboscidea, according to the localities of available herbarium collections with geographic coordinates (indicated or inferred, see text).