Govenia utriculata (Sw.) Lindley (1839

Salazar, Gerardo A., Octaviano-Landa, Víctor I., Jiménez-Machorro, Rolando, Fragoso-Martínez, Itzi, Clase, Teodoro & Ackerman, James D., 2021, Natural history of the often-misunderstood Govenia utriculata (Orchidaceae): discovery of a Mexican population upsets West Indies endemism, Phytotaxa 487 (3), pp. 195-204 : 196-203

Govenia utriculata (Sw.) Lindley (1839 : Misc. p. 46−47).

Limodorum utriculatum Swartz (1788: 119) . TYPE:— JAMAICA. Swartz s.n. (lectotype selected by Ackerman in Ackerman et al. 2014: BM!, isolectotypes UPS!, W photograph!).

Cymbidium utriculatum (Sw.) Swartz (1799: 75) .

Terrestrial herb 45−60 cm in height including the inflorescence. Roots several, arising from the base of the corm, terete, to 150 × 1.5–2.5 mm. Corms asymmetrically globose, dorsiventrally depressed, made up of 3–4 nodes, 2.5–3.5 × 4–5.5 cm, when young covered by 3–4 loose, membranaceous leaf sheaths. Leaves 5–6, lowermost 3–4 of them being bladeless sheaths, obtuse to rounded, 3–10 cm long, the uppermost one much longer, tubular, inflated, greyishgreen with purplish-red suffusion, 19–25 × 3–4 cm, usually filled with rainwater; the upper 2 leaves with elongate petioles fully enclosed by the uppermost bladeless sheath, subquadrate in transverse section, 20–25 × 0.5–1 cm; blades elliptic, acuminate, deep green, plicate, 20−30 × 6–10 cm. Inflorescence racemose; peduncle terete, pale green, 38–42 × 0.4–0.5 cm, with 1–2 membranaceous, tubular, acute to obtuse bracts 3–4 cm long; raceme moderately loose, rachis 5−15 cm long, with 10−25 flowers which open successively. Floral bracts spreading, narrowly lanceolate, attenuate, 10−20 × 2−4 mm. Flowers resupinate, slightly ascending, perianth background colour white, the petals bearing faint, somewhat irregular transverse magenta bars on the distal 2/3 of their inner surface, the labellum with two lanceolate yellow areas on the inner surface extending about 2/3 of its length, three yellowish-brown to dark reddish-brown spots at the apex, sometimes with a less conspicuous additional brownish dot at the tip of each yellow area. Ovary slightly arcuate, subterete, with three rounded longitudinal keels, 7–15 × 1.5–2 mm. Dorsal sepal oblong-lanceolate, subacute, 18–19 × 3.9–4 mm. Lateral sepals oblong, falcate, acute, 12–14 × 4.3–5 mm. Petals narrowly elliptic, falcate, acute, 15–16 × 5.5–6 mm. Labellum versatile (i.e. motile with the union to the column foot acting as a hinge), in natural position ascending and approaching the column, but with weak pressure tipping down and then bouncing back upwards; shortly clawed, then abruptly expanded into a narrowly ovate, acuminate, arching lamina, with a central longitudinal channel bordered by two inconspicuous, rounded keels (which consist of folds that are convex on the upper surface and concave on the lower surface of the labellum), apex shortly acuminate; claw 0.5–1 × ca. 1.2 mm, lamina 9–10.3 × 6–6.5 mm. Column arcuate, truncate at apex, expanded into a broadly triangular, rounded wing at each side above the middle, channeled ventrally, 8–8.5 × 2–3 mm. Anther yellow, galeate, rostrate, ca. 2.5 × 2 mm. Pollinarium ca. 1 × 1 mm, consisting of four yellow, obliquely ovoid pollinia joined through pale yellow, granular caudicles to a short hamular stipe ending into a pointed, whitish viscidium. Rostellum a narrow transverse strip of tissue bearing a small, rounded remnant upon removal of the pollinarium, which is possible to do only shortly before anthesis; when the flowers open the pollinia are already germinating and stuck on the rostellar tissue. Stigma trapezoid, slightly concave, shiny, ca. 1 × 2 mm. Capsules ellipsoidal, pendulous, with six low longitudinal ribs, 2−3 × 0.5−1 cm. Fig. 1 –5.

Phenology: —Flowering from August to December. Well-developed fruits recorded from November to February.

Distribution and habitat: — Bahamas, the Greater Antilles ( Cuba, Dominican Republic, Jamaica, Puerto Rico) and Mexico (Morelos). Terrestrial, with the corms and roots immersed in leaf mould without penetrating the underlying soil. In the Caribbean it inhabits Pinus occidentalis forests and wet broad-leafed tropical forests at 0–1100 m elevation. In Mexico it dwells in partially disturbed tropical deciduous forest at 1350 m elevation. Salazar (2009) speculated that rainwater that accumulates in the sheaths of G. lagenophora Lindley (1839 : Misc. 46–47), the only other species with an inflated sheath similar to that of G. utriculata (see Discussion), may represent a reserve of the liquid in the seasonally dry environments the former dwells in. A similar reasoning may apply to G. utriculata as it concerns its habitat in Mexico (tropical deciduous forest), although the value of such potential adaptation would be less obvious in the moister habitats that the latter occupies in the Greater Antilles ( Ackerman et al. 2014).

Conservation status: —The single population of G. utriculata so far known in Mexico occurs on the edge of the buffer area of the Sierra de Montenegro state reserve, which is about 20 km long and encompasses ca. 7,500 ha of tropical deciduous forest on calcareous terrain at 1000−1775 m elevation, surrounded by valleys where natural vegetation has been eliminated as a result of agriculture and urban expansion, just a few kilometres southeast of the outskirts of the state capital, Cuernavaca (see https://sustentable.morelos.gob.mx/anp/sierra-montenegro). The Govenia population there is subject to occasional disturbance from trampling, as most plants, including all the reproductive individuals observed, grow at the forest edge on the sides of a dirt road and the trails used frequently by farmers from the nearby town on their way to their crop fields and pasturelands (which is often the case in the Greater Antilles; J. D. Ackerman pers. obs.). It is apparent that this species is tolerant to, and perhaps favored by, moderate disturbance. No obvious immediate threats to the Mexican population were noted.

According to the method for assessing risk of extinction for plants of the Mexican norm (MER-Plantas; SEMARNAT 2010), this species qualifies as “Endangered” since it attained a score>2 (2.04), with each of the four criteria rated as follows (maximum value for each = 1): A (characteristics of its geographical distribution) = 1; B (characteristics of its habitat) = 0.78; C (intrinsic vulnerability) = 0.26; and D (impact from human activities) = 0.0. Moreover, this species also qualified as Endangered by two “shortcut” MER-Plantas criteria: (I) Its known area of distribution in Mexico is under 1 km 2 and (II) the number of individuals recorded is less than 500. Likewise, according to the IUCN Red List criteria ( IUCN 2012), at the regional level it qualifies as Endangered by Criterion D (population size estimated to number less than 250 mature individuals). Formal assessments of its risk status in the Bahamas and the Greater Antilles are lacking due to the paucity of information on its distribution, abundance and potential threats ( Ackerman et al. 2014).

Reproductive biology: —Little is known on the reproductive biology of Govenia . The only formal study on the topic published so far is the one by Pansarin (2008). He reported pollination of Brazilian plants attributable to G. gardneri (identified as G. utriculata ) by two species of hoverflies of the genus Salpingogaster (Syrphidae) , which appeared to be deceived by the brown to orange spots on the labellum apex and the column base mimicking pollen clusters. The same fly species were observed visiting flowers of plants belonging to other families that offer pollen as reward. The finding that flowers of G. gardneri do not produce a reward is consistent with our observation of absence of nectar in fresh flowers of G. praecox Salazar & Greenwood (1993: 113–118) , G. lagenophora ( Salazar 2009) , G. polychroma Salazar, Fernández-Díaz & Huerta-Alvízar (2018: 84–84) , G. utriculat a (this work), as well as G. bella Greenwood (1987: 230–232) , G. capitata , G. gardneri , G. liliacea , G. mutica Reichenbach (1852: 856) , G. superba (Lexarza in de la Llave & Lexarza 1825: 13) Lindley (1830 –1840: 153) and G. tingens Poeppig & Endlicher (1837: 5 , t. 107; G. A. Salazar pers. obs.). Hence, the report of nectar for two Venezuelan Govenia species , including one identified there as G. utriculata ( Seres & Ramírez 1995) , should be taken with caution until it can be verified.

All post-anthetic flowers of the Morelos population of G. utriculata we examined underwent self-pollination, showing at anthesis at least some (often all) of the four pollinia stuck to the underlying rostellum tissue because of the apparent germination of the pollen (Fig. F–G). Moreover, all open flowers were at various stages of capsule formation, and in no instance was it possible for us to remove an intact pollinarium once the flower had opened. Thus, that population apparently relies entirely on selfing for sexual reproduction, which may explain the large number of fruits that often form ( Fig. 2H ). Similarly, all the open flowers of the live plant we studied in the Dominican Republic were in various stages of capsule development, although in this case we were unable to verify whether this was the result of auto-pollination. Further studies are required to determine whether cross-pollination occurs at least occasionally in this species or it is fully dependent on auto-pollination.

Vernacular name: — Dominican Republic: Botellitas (Spanish for little bottles). No vernacular names have been recorded elsewhere.

Uses: —In the Dominican Republic, the rainwater that accumulates in the inflated sheath is used locally to refresh the eyes in case of infection (T. Clase pers. obs.).

Taxonomic discussion: — Govenia utriculata is distinguished by the inflated bladeless leaf sheaths, the uppermost of which completely encloses the leaf petioles and, in living condition, is circular in cross section and partially filled with rainwater ( Fig. 1 C−D, 3B, 4A, 5A−D). Such inflated sheath was literally described in Swartz’s protologue of Limodorum utriculatum (“ vagina radicalia inflata;” Swartz 1788: 120) and reflected in the specific epithet (from Latin utriculatus, bladder-like, inflated). Subsequent bona fide reports of G. utriculata have also described and illustrated the unmistakeable sheath. Jacquin (1809: 29, Pl. 32, Fig. 4 ; reproduced here as Fig. 5A) faithfully portrayed the plant and stated that the base of the sheath (“spathe”) contains water, which is evident from the outside up to a height he marked on his figure. Likewise, Hooker (1845: t. 4151) referred to “the bladdery sheath surrounding its scape and the lower part of the leaves,” which was clearly shown in the coloured plate (our Fig. 5B). Further illustrations and descriptions stressing such diagnostic character can be found in Flora of Jamaica (Fawcett & Rendle 1910: 113−114, Pl. 22, Fig. 1 ; our Fig. 5C) and the Orchid Flora of the Greater Antilles ( Ackerman et al. 2014: 203, Fig. 54; reproduced here as Fig. 5D). Florally, G. utriculata is recognized by its relatively small, white flowers with narrowly elliptic, acute petals bearing faint transverse magenta bars above the middle on their inner surface, and the narrowly ovate, acuminate labellum with inconspicuous longitudinal keels below the middle ( Fig. 1F–G , 2 A−B, 3D–E, 4G−I).

The only other species of Govenia possessing a similarly inflated sheath containing rainwater is G. lagenophora , a Mexican endemic that dwells in seasonally dry montane oak forest and xerophilous scrub ( Salazar 2009). Govenia lagenophora differs from G. utriculata in its long, cylindrical raceme with 30−50 flowers, these yellow to yellowish green with the sepals and petals densely spotted and tinged with brown, and the cream-yellow labellum tinged with brown below the middle, which is obtuse to emarginate at apex (see Dressler 1965).

Govenia capitata , a distinctive, large-flowered species from high-elevation conifer-oak forests endemic to the high Mexican cordilleras (see Greenwood 1992b), is still listed in some online compilations as a synonym of G. utriculata (e.g. Govaerts 2021), which likely represents a “relic” of Correll’s (1947) treatment of Govenia . In that work, “offered more for convenience in dealing tentatively with the plants comprising the genus rather than as a final monographic treatment of the genus” on account of the difficulties inherent to its herbarium based taxonomy ( Correll 1947: 219), over 25 nominal species were reduced to five species and two varieties. However, as pointed out by Garay & Romero- González (1999: 483), while herbarium specimens of Govenia are notoriously difficult to determine, difficulties do not mandate wholesale reduction of species to a few names.

Plants of G. gardneri , a widespread South American species originally described from a plant from the Serra dos Órgãos (Organ Mountains), southern Brazil, are often confused in literature with G. utriculata (e.g. Pansarín 2008; Pansarin & Pansarin 2010; Schinini 2010; Zuloaga et al. 2019). Govenia gardneri differs from G. utriculata in its narrow bladeless leaf sheaths 1.5−2 cm in diameter (vs. 3−4 cm), internally spotted (not barred), proportionately short and wide petals 1.8−2 times longer than broad (vs. 2.8−3.2 times longer than broad), and broadly ovate, obtuse labellum with prominent keels over most of its length (vs. keels only on the basal half). Botanical illustrations and descriptions of G. gardneri can be found in Hooker (1839), Cogniaux (1898 –1902) and Hoehne (1942). High-quality colour photographs showing the narrow, tight bladeless sheaths and the characteristic flower colouration of G. gardneri were published by Pansarin & Pansarin (2010, as G. utriculata ).

Representative specimens: — BAHAMAS. Andros: North Andros, Maidenhair Coppice no. 1, ca. 8 miles NW of Fresh Creek , 5 Jan. 1978, Correll et al. 49372 ( NY!) . CUBA. Oriente: Monte Verde, 13 Feb. 1911, Shafer 8678 ( NY!) . DOMINICAN REPUBLIC. San José de Ocoa: municipio Ocoa, La Ciénega, localidad La Laguna, 14.3 km al E de Ocoa , 1232 elev., 28 Nov. 2016, Fragoso-Martínez et al. 543 ( JBSD!) . JAMAICA. without date or collector, donated in 1855 by Hooker [s.n.] ( P!) . MEXICO. Morelos: Sierra Montenegro, municipio Emiliano Zapata, Tetecalita ,

subiendo del poblado hacia el paraje Las Peñas, 23 Aug. 2019, Salazar & Octaviano-Landa 10282 ( HUMO! MEXU!). PUERTO RICO. Utuado: Cerro Morales , 700−950 m, near summit, 5 Nov. 1984, Ackerman & Montero-Oliver 2042 ( UPRRP!) .

Figures

FIGURE 1. Govenia utriculata. A. Clump of plants in situ. B. Base of a plant removed from leaf litter to show the depressed corm from the previous year’s growth and the developing corm enclosed by the sheath bases. C. Inflated sheaths of two adjacent plants. D. One such sheath illuminated from behind to show the accumulation of rainwater. E. Inflorescence. F. Flower, oblique view. G. Flower, front view. H. Labellum and column in natural position, side view. All from Salazar & Octaviano-Landa 10282. Photographs by Gerardo A. Salazar.

FIGURE 2.Govenia utriculata. A. Labellum andcolumn from frontafter tipping the labellumdownwards.B.Perianth dissection,segments flattened. C. Column, side view. D. Column, front view. E. Pollinarium removed from a flower bud just before anthesis, front view. F. Part of a pollinarium of a self-pollinating flower at anthesis; the large pollinium on the right-hand side is swollen because of germination of the pollen tubes. G. Pollinarium of a post-anthetic, self-pollinating flower showing the dried viscidium and the pollinia fussed to the rostellar tissue caused by pollen germination. H. Near-mature capsules. All from Salazar & Octaviano-Landa 10282. Photographs by Gerardo A. Salazar (A−G) and Víctor I. Octaviano-Landa (H).

FIGURE 4. Previously published illustrations of bona fide Govenia utriculata. A. Illustration from Fragmenta Botanica (Jacquin 1809: t. 32, fig. 4). B. Illustration from Botanical Magazine (Hooker 1845: t. 4151). C. Illustration from Flora of Jamaica (Fawcett and Rendle 1910: t. 22, fig. 1−3). D. Illustration by B. Angell. Reproduced with permission of the publisher and illustrator from: James D. Ackerman and Collaborators, Orchid Flora of the Greater Antilles, pg. 202, fig. 54. © 2014, The New York Botanical Garden, Bronx, New York.