Thismia paradisiaca S.Guzm.

Guzmán-Guzmán, Santiago & Plata-Torres, Angelo, 2023, A flower in paradise: citizen science helps to discover Thismia paradisiaca (Thismiaceae), a new species from the Chocó Biogeographic region in Colombia, Phytotaxa 603 (1), pp. 27-42 : 29-38

Thismia paradisiaca S.Guzm. -Guzm., sp. nov. ( Fig. 2–5 ).

Diagnosis — Thismia paradisiaca is similar to T. panamensis mainly because it has the distal portion of the stamen connective bearing a tuft of trichomes, free ellipsoid thecae and the stigma proximally puberulous and distally hispid. The new species differs from the latter by hypanthium color (dark purple vs whitish tinged with greenish–brown to colorless or pinkish) ( Fig. 5A, B ), shape of outer tepals (upper outer tepal incurved, lateral outer tepals declinate and slightly twisted laterally outside vs outer tepals reflexed) ( Fig. 5C, D ), dimorphic (vs homomorphic) stamens ( Fig. 5E, F ) and conical (vs cylindrical) stigma.

Type: — COLOMBIA. Valle del Cauca: Dagua municipality, La Cascada village, El Paraíso Natural Reserve , El Danubio River , tributary of Anchicayá River , located approximately 50 meters from the river, on the right side of the path towards the reserve, 716 m, 3°37’40.66”N, 76°50’1.47”W, 10 February 2023 (fl., fr.), B. C. Corrales Restrepo, S. Guzmán-Guzmán & E. Restrepo 001 (Holotype: FAUC!, in alcohol+glycerine) .

Terrestrial achlorophyllous herb, 3.7–5.0 cm tall, generally glabrous (where not stated otherwise) ( Fig. 2A 1 ; 3A ). Tuber obovoid, 7.0–11.0 × 4.0–8.0 mm, cream (rapidly turning tawny after being collected) ( Fig. 2A2 ); roots filiform, up to 60.0 mm long, cream ( Fig. 2A2 ). Stem 1 or 2, erect to flexuous, longitudinally bisulcate, 16.0–20.0 × 1.2–1.5 mm, cream at the base turning chestnut towards the apex, basally ensheathed by an inconspicuous triangular volva 1.0 × 1.0 mm ( Fig. 2A 1–A 2 ; 3A ). Involucral bracts 4, crowded at apex of stem, surrounding the base of ovary, sessile, decussate, appressed, navicular, ovate–lanceolate, 2.5–3.0 × 4.5–5.0 mm, chestnut-coloured, margin entire, base truncate, apex acute, venation hyphodromous ( Fig. 2A 1 ; 3A ). Flower terminal, zygomorphic, solitary, sessile ( Fig. 2A–C ; 3A–B ). Hypanthium gibbous, 10.0–16.0 × 7.0–10.0 mm (largest diam.); outer surface vesicular, indigo to black with 12 flattened vertical veins slightly darker than surrounding tissue (surrounding tissue turns light green in backlight) ( Fig. 2A 3; 3C 2 ); inner surface papillose with papillae to 0.5 mm long, indigo to dark purple, dorsally with five prominent cream to mauve vertical veins densely covered by tiny gland-like protrusions, ventrally with seven prominent indigo to dark purple vertical veins at base suddenly flattening distally and densely papillose with papillae to 0.5 mm long ( Fig. 2D 1 ; 3C 1–C 4 ); bases of all veins forming a prominent cream-coloured crenate ring ( Fig. 2E ; 3G ). Tepals 6, inserted more or less at the same level in the distal portion of the hypanthium, heteromorphic. Outer tepals alternate with the segments of the annulus; upper outer tepal incurved, elliptic, 7.0–7.5 × 4.0– 4.5 mm, indigo to dark purple, vesicular, margin entire, base subcordate, apex rounded, venation hyphodromous ( Fig. 3D 1 ); lateral outer tepals declinate and slightly twisted laterally outside, elliptic, 6.0–6.5 × 4.0– 4.5 mm, indigo to dark purple, vesicular, margin entire, base slightly revolute, apex rounded, venation hyphodromous ( Fig. 3D 2 ). Inner tepals opposite to segments of the annulus, assurgent, narrowly triangular, 5.0–7.0 × 1.5–3.0 mm, dark violet, vesicular, apex tapering abruptly into a cauda; cauda 30.0–57.0 × 0.5 mm, tawny turning cream, apex slightly acute ( Fig. 2A 1 ; 3A ). Annulus consisting into three connate segments opposite to inner tepals, reclinate, each segment 4.0–5.0 × 2.0– 2.5 mm, lavender to brilliant white, ornamented with three finely raised crests on the upper side, arranged parallel to the orifice, outer crest 0.6–1.0 mm high, middle crest 0.3–0.4 mm high and inner crest 0.3 mm high, separated by gaps 0.5–0.6 mm wide ( Fig. 2B–D ; 3C 1 ). Orifice of annulus circular, ca. 2.5 mm diam. ( Fig. 2C ; 3B ). Stamens 6, dimorphic, arranged in the radii of tepals, inserted along the inner edge of annulus segments, pendulous and hanging into the hypanthium; bases of stamen filament expanded laterally and fused into a ring ca. 0.4 mm in diam. ( Fig. 2D ; 3C 1 ). Dorsal stamens 3 ( Fig. 2D2 ; 3E ; 5E ); each with filament laminar, 0.7 × 1.0 mm, coral to white ( Fig. 3E 1 ); connective dilated, bilobed basally and apically (apical lobes branching off immediately below the point of insertion of thecae), 1.0 × 1.0 mm (including apical lobes), rufous, distal portion bearing a tuft of trichomes at the point of insertion with the thecae; trichomes unicellular, erect, 0.4–0.9 mm long ( Fig. 3E 2 ); basal lobes of connective appressed to the filament, linear, 1.0 × 0.4 mm, rufous ( Fig. 3E 1 ); apical lobes of connective narrowly ovate, 0.3–0.4 × 0.5–0.6 mm, dark purple, apex rounded to truncate, papillose; papillae 0.09–0.12 mm long, dark purple ( Fig. 3E3 ); interstaminal lobes inserted ca. 0.5 mm below the filaments, mammiliform to shortly triangulate, 0.3–0.5 × 0.3–0.5 mm, dark purple ( Fig. E1 ). Ventral stamens 3; 2 lateral stamens each with filament laminar, 1.0 × 1.0 mm, coral to white ( Fig. 3F 1 ); connective dilated, at the margin adjacent to dorsal stamen lobed basally and apically, at the margin adjacent to central stamen lobed laterally lobed by fusion of basal and apical lobe (apical and lateral lobes branching off immediately below the point of insertion of the thecae), 1.0 × 0.8 mm, rufous, distal portion bearing a tuft of trichomes at the point of insertion with thecae; trichomes unicellular, erect, 0.4–0.9 mm long ( Fig. 3F 2 ); basal lobe, appresed to the filament, linear, 1.0 × 0.4 mm, rufous ( Fig. 3F 1 ); apical lobe narrowly ovate, 0.3–0.4 × 0.5–0.6 mm, dark purple, apex rounded to truncate, papillose; papillae 0.09–0.12 mm long, dark purple; lateral lobe divaricate, falcate, 1.0 × 0.7 mm, rufous, outer margin proximally papillose; papillae 0.09–0.12 mm long ( Fig. 3F 1 ); single central stamen with filament laminar, 1.0 × 1.0 mm, coral to white ( Fig. 3F 2 ); connective dilated, laterally lobulated by fusion of basal and apical lobe, 1.0 × 0.8 mm, rufous, distal portion bearing a tuft of trichomes at the point of insertion with thecae; trichomes unicellular, erect, 0.4– 0.9 mm long ( Fig. 3F 2 ); lateral lobes 2, divaricate, falcate, 1.0 × 0.7 mm, rufous, outer margin proximally papillose; papillae 0.09–0.12 mm long ( Fig. 3F 2–F 3 ); interstaminal lobes inserted ca. 0.5 mm below the filament, linear, 1.0 × 0.3 mm, dark purple ( Fig. 3F 1 ). Thecae 2, inserted at the distal part of the connective, free, ellipsoid, 1.0–1.2 × 0.5– 0.7 mm, longitudinally dehiscent, white ( Fig. 3E 2 ; 3F 2 ). Pollen in monades, bilaterally symmetrical, isopolar, amb circular to slightly elliptic, spheroidal shape, (22.0–)23.2(–24.0) µm in diam., monoporate with simple circular pore; exine intectate, 1.0 µm thick; sculpture psilate ( Fig. 4 , Table 1 ). Ovary inferior, broadly obconical, 2.0–2.5 × 3.7–4.0 mm, unilocular; placentation parietal; placentas 3, inserted in the basal part of the locule, bearing numerous ovules; style erect, cylindrical to shortly conical, 0.6–0.7 × 0.6–1.0 mm, dark purple ( Fig. 2E ; 3G ); stigma divaricate, trilobed, each conical lobe, 1.0–1.3 × 0.9 mm, dark purple and covered abaxially by multicellular uniseriate simple trichomes; proximally densely puberulous with 0.1–0.3 mm long trichomes, dark purple and distally hispid with 0.3–0.5 mm long trichomes, light green ( Fig. 2E ; 3G ). Immature fruit cupuliform, 3.6 × 5.3 mm, dark purple, surrounded by persistent involucral bracts ( Fig. 2A–2F ).

Additional specimen examined (paratype): — COLOMBIA. Valle del Cauca: Buenaventura municipality, El Paraíso Natural Reserve, Danubio Stream , tributary of El Danubio River , located approximately seven meters from the river, among leaf litter, 737 m, 3°37’55.09”N, 76°49’59.37”W, 10 February 2023, B. C . Corrales Restrepo , S . Guzmán-Guzmán & E . Restrepo 002 ( FAUC) .

Photographic records examined: — COLOMBIA. Valle del Cauca: Cali municipality, 3°26’48.8”N, 76°39’23.9”W (approximate coordinates), 9 February 2018, Sasha Robinson, Recorded in iNaturalist (https://www. inaturalist.org/observations/10252116) ; Valle del Cauca: Dagua municipality, 384 m, 3°36’0.3”N, 76°51’0.2”W, 8 January 2021, Mauricio Morales, Recorded in iNaturalist (https://www.inaturalist.org/observations/81910064) .

Etymology: —The specific epithet of Thismia paradisiaca refers to the Latin word “ paradisiacus ” which means “belonging to paradise”. In turn, this word derives from the Latin term “ paradisus ” which is related to “garden of sublime exuberance and beauty”. This name is a tribute to the El Paraíso Natural Reserve.

Distribution and habitat: — Thismia paradisiaca is found in the Pacific Domain, specifically in Chocó –Darién Moist Forests Ecoregion on the Pacific slope of the Western Cordillera of the Andes ( Fig. 1A ; 6 ) ( Olson et al. 2001, Rangel 2004, Morrone 2022), located in the immeasurable and ineffable diversity of the Biogeographic Chocó, where the reserve owners are currently working hard to conserve this area through endangered species conservation plans, such as Lehmann’s poison frog ( Oophaga lehmannii , Dendrobatidae ), the long-wattled umbrellabird ( Cephalopterus penduliger , Cotingidae ) and now the thismia of paradise ( Thismia paradisiaca ). This species inhabits elevations of 710–750 m in riparian forests near the Danubio River and Danubio Stream ( Fig. 1B ), with the two known localities placed in approximately 470 m from each other.

The first (holotype) locality is in about 50 m from the Danubio River, next to a little-traveled path that leads to the cabin of the El Paraíso Nature Reserve ( Fig. 1D ). A total of five individuals were recorded in this locality, two of which had flower buds, one had an anthetic flower and immature fruit, one had an in immature fruit, and the last one had no flowering stem (only the tuber was observed). Additionally, two abscised hypanthia were recorded on the ground, right next to the immature fruits. These individuals were located in a layer of leaf litter 3 to 5 cm deep dominated by leaves of Ficus tonduzii Standley (Moraceae) and Inga sp. Miller ( Fabaceae ) in a small (2 m 2) landslide. This landslide was possibly formed after heavy rains that occurred days before the collection; it was composed mainly of small rocks, soil, and small shrubs.

In an area of 5 m 2 in the first locality, the herbaceous layer between 0.5 to 1 m in height comprised Diplazium macrodictyon (Baker)Diels(Athyriaceae) , Mickelia nicotianifolia (Sw.)R.C.Moran ,Labial&Sundue( Dryopteridaceae ), Campyloneurum sphenodes Fée (Polypodiaceae) , Dicranopygium sp. (Cyclanthaceae) , Costus sp. (Costaceae) , Pilea pteropodon Wedd. and P. umbriana Killip. (Urticaceae) . The lower tree layer is dominated by Inga psittacorum L.Uribe (Fabaceae) and Saurauia sp. (Actinidiaceae) with heights between 5 to 7 m, and by an upper tree layer between 20 to 25 m in height consisting of F. tonduzii and Inga sp.

The second (paratype) locality is located in approximately 7 meters from the Danubio Stream. It had a layer of leaf litter between 5 to 7 cm deep, mainly composed of leaves of F. tonduzii and two lianas, Coussapoa contorta Cuatrec. (Urticaceae) and Clusia hirsuta Hammel (Clusiaceae) . In this locality, the leaf litter was accumulated in cavities formed by thick superficial roots above ground of Turpinia occidentalis (Sw.) G.Don (Staphyleaceae) and Guatteria alta R.E.Fr. (Annonaceae) ( Fig. 1C ), right next to a runoff drain that flows from the top of the mountain. Only two individuals were found for this locality: one in anthesis and the other one with immature fruit and its corresponding abscised hypanthium on the ground.

In an area of 5 m 2 in the second locality, the herbaceous layer between 0.5to 1 m in height comprised Campyloneurum sphenodes (Polypodiaceae) , Anthurium spp. and Xanthosoma daguense Engl. (Araceae) , Dicranopygium sp. (Cyclanthaceae) , Costus sp. (Costaceae) and Pilea umbriana (Urticaceae) . The lower tree layer comprised Eugenia victoriana Cuatrec. (Myrtaceae) and G. alta with heights between 7 to 9 m and a upper tree layer dominated by F. tonduzii and T. occidentalis . Of the mentioned species, E. victoriana and G. alta are endemic to Colombia ( Bernal et al. 2019), and along with C. contorta and C. hirsuta , they have a restricted distribution to the Chocó –Darién Moist Forests Ecoregion (Bert et al. 1990, Luján et al. 2018).

Phenology: —Both populations were collected in flower and fruit on February 10, however, according to the reports in iNaturalist and the monitoring and photographic recording by the reserve’s tour guides, the flowering season take place from January to March in both locations.

Ecological interactions: —The knowledge about the floral biology of Thismia was for a long time limited to various hypotheses based on its floral morphology and particularly on the arrangement of androecial and gynoecial organs inside the floral chamber, the presence of nectaries at the base of the perianth or on the anthers, the presence of osmophores and filiform appendages in the tepals, and narrowly spaced filaments of the stamens. These features correspond to a myiophilous pollination syndrome. Various lineages of flies, and mainly fungus gnats and scuttle flies, were identified as possible pollinators ( Poulsen 1890, Groom 1895, Faegri & Van Der Pijil 1979, Stone 1980, Maas et al. 1986). Only recently the first direct observations on floral visitors and/or pollinators were conducted, thereby confirming some of these hypotheses. All the hitherto published observations were made in Asian species of the genus.

Li & Bi (2013) recorded a dipteran species visiting a flower of T.gongshanensis Li & Bi (2013: 25) during collection of the type specimen. Subsequently, Mar & Saunders (2015) reported the presence of a fungus gnat ( Mycetophilidae or Sciaridae , Diptera ) and a scuttle fly wing ( Phoridae , Diptera ) inside the floral chamber of T. hongkongensis Mar & R.M.K.Saunders (2015: 23) . Both records, while being significant, did not provide insight into the role of these visitors and their role in pollination.

Guo et al. (2019) conducted a remarkable study on the reproductive biology of T. tentaculata Larsen & Averyanov (2007: 16) , where they recorded insects from various families and other invertebrates as floral visitors. They identified a species of fungus gnats from the genus Corynoptera ( Sciaridae : Diptera ) as the pollinator of this species, observing that the gnats are retained inside the floral chamber for a significant time, interact with the stigmatic region, and carry pollen grains on their bodies. Likewise, Yudina et al. (2021) recorded 35 floral visitors from various insect and other invertebrate families in T. puberula Nuraliev (2015: 135) (16 visitors), T. mucronata Nuraliev (2014: 246) (18 visitors) and T. annamensis Larsen & Averyanov (2007: 13) (one visitor). Among them, they highlighted the scuttle flies and parasitic wasps from the families Braconidae , Diapriidae and Scelionidae (Hymenoptera) as potential pollinators since these insects were demonstrated to carry pollen grains of Thismia . These studies support the earlier hypotheses based on floral morphology and demonstrate sapromyophilous pollination especially by fungus gnats and scuttle flies.

To date, no floral visitors have ever been recorded for the Neotropical species of Thismia , i.e. subgenus Ophiomeris . During dissection of an alcohol-stored flower of T. paradisiaca , a small dipteran was found inside the floral chamber ( Fig. 1E ), firmly retained between the inner surface of the hypanthium and the dorsal stamens. It is impossible to determine whether it was actually interacting with the stamens, as not a single fly approaching the flowers or interacting with them was recorded during observation and specimen collection. Nevertheless, the record of this dipteran within the flower suggests an evident floral visitation, especially considering the reported close relationship between Diptera and the Asian species mentioned above, as well as a combination of floral characters of T. paradisiaca consistent with the typical pattern of sapromyophilous pollination syndrome. This is the first record of floral visitors for subgen. Ophiomeris , and further studies focused on the floral biology of T. paradisiaca may provide additional insights into its pollination mechanisms and the role of floral visitors.

The relationship between the dimorphic stamens and pollination of T. paradisiaca is noteworthy. The stamen dimorphism has not been reported for any other species of family Thismiaceae . The dorsal stamens, lose to which the dipteran was found, forms a barrier due to the proximity of the stamens (including the basal lobes of the connectives) to the interstaminal lobes ( Fig. 3E ). The ventral stamens, in contrast, are more distantly spaced, and the lateral lobes of the connectives form openings ( Fig. 3F ). As a result, the dorsal stamens possibly act as a barrier that directs floral visitors to pass through the openings between the ventral stamens, hindering their exit and ensuring interaction with pollen grains before leaving the floral chamber.

Taxonomic relationships: —We assign Thismia paradisiaca to the subgen. Ophiomeris sect. Ophiomeris , because of its underground part represented by a tuber, sulcate stem, sessile flower, laminar staminal filament and parietal placentas inserted in the basal part of the ovary. With T. paradisiaca , sect. Ophiomeris comprises 15 species ( Kumar et al. 2017). Thismia paradisiaca differs from all the other species of the section by having dimorphic (vs homomorphic) stamens, incurved (vs reflexed to patent) upper outer tepal and lateral outer tepals slightly revolute (vs truncate or cordate) at base.

Thismia paradisiaca occurs in the Chocó –Darién Moist Forests Ecoregion ( Olson et al. 2001) along with T. luetzelburgii K.I.Goebel & Suess. (1924: 56) and T. panamensis . The new species differs from T. luetzelburgii by having not swollen (vs swollen) apex of the cauda of the external tepals, the distal portion of the stamen connective bearing a tuft of trichomes (vs. glabrous) and the free (vs fused) stamen thecae inserted at the apex (vs middle) of the connective ( Maas et al. 1986). Palynological analysis suggests that the pollen of T. paradisiaca is like that of T. luetzelburgii and T. panamensis previously cited by Maas & Maas-van de Kamer (1988), however, T. paradisiaca probably has an intermediate pollen size, being the smallest of T. luetzelburgii and the largest of T. panamensis .

Thismia paradisiaca is the second species of Thismia newly reported from Colombia since the revision of Maas & Maas-van de Kamer (1988) in the Flora de Colombia, bringing the number of species of the genus known for the country to four ( Fig. 6 ). Of the Colombian species, T. paradisiaca differs from the recently described T. andicola by having an indigo to black (vs light blue, densely punctate with sky-blue metallic dots) outer surface of the hypanthium and conical (vs obovoid) stigma lobe. It also differs from T. glaziovii Poulsen (1889: 549) by having a gibbous (vs campanulate) hypanthium and an annulus in the shape of three connate segments (vs of a single disc). Finally, it differs from T. panamensis (in addition to the characters mentioned in the diagnosis) by having prominent (vs flat) dorsal veins towards the interior of the hypanthium densely covered by small gland-like protrusions (vs papillae), connective trichomes 0.4–0.9 mm (vs up to 0.4 mm) long and dimorphic (vs homomorphic) interstaminal lobes ( Fig. 5D, E ).

Figures

FIGURE 1. Habitat and ecology of Thismia. A. Mountains of the Pacific slope of the Western Cordillera of the Andes. B. Riparian forests of the Danubio Stream. C. Litter accumulated in cavities formed by surface roots above ground. D. Trail towards the Danubio River (arrow indicating the area where the type locality is found). E. Fly (Diptera) recorded in the floral chamber. Photographs by Santiago Guzmán- Guzmán (A, B. D and E) and Dairo Utima (C).

FIGURE 2. Thismia paradisiaca. A1. Individual with anthetic flower and immature fruit. A2. Tuber. A3. Outer surface of hypanthium. B. Flower (3/4 view). C. Flower (top view). D1. Flower with longitudinally dissected hypanthium. D2. Dorsal stamens (inner=abaxial view). E. Stigma (top view). F. Immature fruit (side view). B.C. Corrales Restrepo, S. Guzmán-Guzmán & E. Restrepo 001. Photographs and plate by Eugenio Restrepo.

FIGURE 3. Thismia paradisiaca. A. Habit. B. Flower (top view). C1. Longitudinal dissection of flower. C2. Outer surface of the hypanthium. C3. Inner surface of hypanthium, showing papillae. C4. Glandular-like surface of the dorsal veins of the hypanthium. D1. Upper outer tepal (adaxial view). D2. Lateral outer tepal (abaxial view). E1. Dorsal stamens (inner=abaxial view). E2. Dorsal stamen (outer=adaxial view). E3. Papillae of the dorsal stamen apical lobe. F1. Ventral stamens (inner=abaxial view). F2. Ventral stamen (outer=adaxial view). F3. Papillae of the ventral stamen lateral lobe. G. Style and stigma. B.C. Corrales Restrepo, S. Guzmán-Guzmán & E. Restrepo 001. Illustration by Maria José Rodriguez.

FIGURE 4. Pollen morphology of Thismia paradisiaca; LM (A–D) and SEM (E–H) images. A. pollen grain without fuchsin staining (showing amb circular and thin intectate exine). B–D. Fuchsin-stained pollen grains (showing psilate sculpture and a single simple circular pore). E–F. Pollen grains (showing an amb circular to slightly elliptic, spherical shape and a single pore) H. Dehydrated pollen grains.

FIGURE 5. Comparison between Thismia paradisiaca and T. panamensis. A, C. B.C. Corrales Restrepo et al. 001. E. B.C. Corrales Restrepo et al. 002. B, D, F. Santiago Guzmán-Guzmán 593.A–B. Lateral view of the flower. C–D. 3/4 view of the flower. E–F. Inner view of the flower, showing annulus and stamens. Photographs by Brayan Camilo Restrepo (C), Mauricio Morales (B and D) and Santiago Guzmán-Guzmán (A, E and F).

FIGURE 6. A. Distribution of Thismia in Colombia. B–C. Distribution of T. paradisiaca.