Habenaria cruegeri Rchb.f. var. flaviflora J.A.N.Bat. & Bianch., 2018

Batista, João A. N., Reis, André F. De S., Leite Junior, Josefran L. & Bianchetti, Luciano De Bem, 2018, Phylogeny and taxonomy of Habenaria leprieurii, H. alpestris and H. sect. Microdactylae (Orchidaceae), with descriptions of two new taxa, Phytotaxa 373 (4), pp. 241-271 : 262-265

Habenaria cruegeri Rchb.f. var. flaviflora J.A.N.Bat. & Bianch. var. nov. ( Figs. 4H, N )

Similar to H. cruegeri , but distinct for growing in dry areas, having plants, on average, higher (33–44 cm including the inflorescence), inflorescence with 10–13 flowers, a shorter pedicellate ovary (8.0–10.0 mm long), shorter spur (6.0– 7.5 mm long), and yellow to greenish-yellow petals and lip.

Type: — BRAZIL. Distrito Federal: Brasília, Setor de Mansões do Lago Norte, base das encostas logo após o Varjão, em direção ao Paranoá, 15º42’54.77”S, 47º52’13.54”W, 1032 m, campo limpo seco, área queimada durante a seca, observada uma pequena população no local com cerca de 12 indivíduos em floração, sépalas verdes, pétala e labelo amarelados, 26 February 1990, A. H. Salles, L. B. Bianchetti & J. A. N. Batista 1547 (holotype HEPH! [6918-3] mixed with H. cruegeri ).

Etymology:—From the Latin words flavi (yellow) and floris (flower), in reference to the yellowish corolla of the variety, contrasting with the green color of H. cruegeri .

Distribution and Conservation Status:— Habenaria cruegeri var. flaviflora is currently known only from the Distrito Federal (Federal District), the administrative capital of Brazil, located in the core area of the cerrado biome in the central region of that country. The taxon is known from three collections, and possibly only two populations. The population in Setor de Mansões do Lago Norte (Salles et al. 1547) was encountered in February 1990 when approximately 10 flowering individuals were observed. This area was later occupied by an irregular residential settlement and the population no longer exists. As far as it was possible to evaluate this site is probably the same as that of the Irwin et al. 15364 collection, made in 1966. Based on the IUCN Red List Categories and Criteria, and guidelines ( IUCN 2012, 2016), Habenaria cruegeri var. flaviflora can be tentatively classified as Critically Endangered CR (criteria B1ab(iii) + 2ab(iii); D).

Habitat, phenology, and ecology:— Habenaria cruegeri var. flaviflora grows in dry grassy fields (campo limpo seco), on clayey-sandy, shallow soils, about 1,000 m a.s.l. Flowering occurs from the peak to the end of rainy season (February to May). On the one occasion that we observed them, the plants were growing and flowering in an area that had burned during the previous dry season.

Notes:— Habenaria cruegeri var. flaviflora is similar in terms of its vegetative and floral morphology to H. cruegeri , but differs by the yellow or greenish-yellow color of its petals and lip, and by growing in dry campo limpo vegetation, while H. cruegeri always has green or greenish-brown flowers and grows in seasonally to permanently humid grasslands. Other differences are that Habenaria cruegeri var. flaviflora grows taller (33–44 cm including the inflorescence vs mean of 9–30 cm tall in H. cruegeri ), has larger numbers of flowers (10–13 flowers vs (1–)2–6(–9) flowers in H. cruegeri ), a shorter pedicellate ovary (8–10 mm long vs (11–) 13–16 mm long in H. cruegeri ), and a shorter spur (6.0– 7.5 mm long vs (7–) 8–11 mm long in H. cruegeri ) ( Table 2). Habenaria cruegeri var. flaviflora was originally discovered from a single population comprising approximately a dozen plants, with all of the specimens sharing the same distinctive characteristics. Since the species is sympatric and morphologically similar to H. cruegeri , we followed Stace (1989) in defining its varietal taxonomic rank as “a population of one or several biotypes, forming more or less distinct local races of a species”. Collections of more material and additional field observations should allow better comparisons of both taxa.

Habenaria cruegeri var. flaviflora is a rare taxon, known only from two sites in the Distrito Federal. Unfortunately, the type collection site was destroyed, and extensive searches in neighboring areas have not located additional populations. It is expected, however, to occur in other places in the Distrito Federal and surrounding areas. The new variety is mixed with H. cruegeri in the type collection, but the latter taxon was collected in another nearby location. A specimen from Mato Grosso, Andrade-Lima 79-8675 (IPA 45699!), is very similar to H. cruegeri var. flaviflora , and most likely corresponds to that species. We were unable, however, to examine details of its floral morphology and confirm identification. If correct, it will greatly expand the known distribution of the variety.

Additional specimens examined:— BRAZIL. Distrito Federal : near Ribeirão Torto, N. E. of Lago Paranoá, 26 Apr 1966, H. S. Irwin et al. 15364 ( UB!) ; Brasília , Parque Nacional de Brasília, 100 m após a estação meteorológica, em direção ao despenhadeiro, 15º38’14”S, 47º59’33”W, 1212 m, 13 May 2008, Santos 2993 ( CEN!) .

Habenaria heptadactyla Reichenbach (1850: 812) . Syntypes:— VENEZUELA. [Amazonas], Orinoco, Esmeraldas, [21–23 May 1800], A.J.A. Bonpland & F.W.H.A. von Humboldt 1005 (lectotype, designated here: B! [B-W 16857 -01 0], W-R! [51242] drawing and fragment of the lectotype); reg. alpina Meridensis & Caracas, July [1865], J. W. K. Moritz 615 ( BM! [ BM000032574 ], HBG! [500775], W-R! [51219], RENZ! [14371] photocopy and drawing from W-R). GUYANA: Pirara, January 1842, R. Schomburgk 634 ( AMES! [00099866 drawing and fragment from B], B [destroyed], W-R! [51218], RENZ! [14369] photocopy from W-R). ( Figs. 5A–F ). Habenaria viridiaurea Lindl. ex Kränzlin (1892: 102) , as synonym. Based upon: BRAZIL. Prov. Rio Negro [Amazonas], near Barra

[Manaus], December-March 1850–1851, R. Spruce s.n. (AMES! photo, BM! [32707], K! [000363833], LE, M!, MG! [19354], P!

[00408683], W-R! [51236, 51220 drawing from M], RENZ! [14373] photocopy from W-R); Campo de Janauarí , January 1851, R .

Spruce 1222 (K! [000363830], K-L! [000363789], P! [00408682], RENZ! [14366] drawing). Habenaria leprieurii Rchb.f. var. heptadactyla (Rchb.f.) Schultes (1956: 193) .

Distribution and Conservation Status:— H. heptadactyla is widely distributed from Panama to Colombia, Guyana, Suriname, Trinidad, Venezuela, northern and central Brazil (AM, DF, GO, MS, MT, RR, TO), and Bolivia. It would be expected to be found in Pará State Brazil, and other states with cerrado vegetation, such as western Bahia and northwestern and central Minas Gerais. The specimen reported for Argentina (Spruce s.n. [K! 000363833]) by Szlachetko et al. (2017) is one the specimens upon which the name H. viridiaurea is based and, in fact, is from Brazil, from Province of Rio Negro [= Amazonas]. Based on the IUCN Red List Categories and Criteria and guidelines ( IUCN 2012, 2016), H. heptadactyla can be tentatively classified as of least concern (LC), due to its wide geographic distribution and large numbers of known populations.

Habitat, phenology and ecology:— Similar to H. omissa , the species grows in both dry and humid grasslands. We have encountered H. heptadactyla most often on rocky, dry fields in the cerrado of central Brazil. In Roraima, in northern Brazil, H. heptadactyla is found on water logged sites that dry completely during the dry season. Flowering occurs from the middle to the near end of the rainy season; in central Brazil from February to April.

Notes:—The most distinctive characteristic of H. heptadactyla is its short, congested, somewhat cylindrical inflorescence (fig. 5A), with an average of 2.1–4.9 flowers/cm of inflorescence ( Table 2). Even plants with fewer flowers gather them more closely than observed in the other species of the section. Another difference is the usually bright-yellow color of their flowers. This character was noted by Reichenbach (1850) in the species protologue. The dorsal sepal is usually yellow, the lateral sepals yellowish-green, and the petals and lip bright yellow with a whitish base. However, as illustrated here (fig. 5E) and by Kenny (1992), its flowers can occasionally be greenish-yellow or completely green. The pinkish-purple color of the flowers mentioned by Schultes (1960) is clearly a mistake. Similar to H. leprieurii , the width of the petals and the lateral segments of the lip are variable. The materials we examined from central Brazil had linear lateral segments, but they were broader in the illustrations prepared by Ames (1910), Dunsterville & Garay (1972), Snuverink & Westra (1983), and Kenny (1992), all of whom misidentified material from Trinidad, Venezuela, and the Guianas as H. leprieurii .

Habenaria heptadactyla has been treated as a variety ( Schultes 1956, 1960, Schweinfurth 1967) or a synonym ( Foldats 1969, Dunsterville & Garay 1972, Snuverink & Westra 1983) of H. leprieurii . As Renz (1992) pointed out, however, the species is very distinctive and those proposals are clearly unwarranted. In fact, the morphology of the perianth is very similar to H. omissa , but it can be distinguished from that species (and other species of the section) by the characteristics outlined above. Herbarium specimens with few flowers (1–2) appear similar, however, and are difficult to distinguish from H. omissa .

Reichenbach (1850) recorded three syntypes in the protologue of H. heptadactyla . We select here as lectotype the specimen Bonpland & Humboldt 1005 located in Herbarium B, as it is one of the best conserved syntypes and the only one with a handwritten identification label by Reichenbach himself. In the protologue of H. heptadactyla ( Reichenbach 1850) the collection Moritz 615 is assigned to Caripe, a locality in the state of Monagas, Venezuela. However, the duplicates at BM and HBG do not make any mention of this locality. In the sample located in HBG, which has the most complete data, the material is quoted for reg. (regionem) alpina Meridensis and Caracas, and we follow this data here.

Illustrations: — Ames (1910, plate 70, fig. 2, as H. leprieurii ), Hoehne (1940, tab. 94, fig. 1, based on Kuhlmann 786), Dunsterville & Garay (1972, pg. 135, as H. leprieurii ), Dunsterville & Garay (1979, pg. 339, as H. leprieurii ), Pabst & Dungs (1975, pg. 253, fig. 124, as H. leprieurii , based on Black & Lobato 51-12774 [IAN!]), Snuverink & Westra (1983, fig. 8, based on Oldenburger et al. 927 [U!], as H. leprieurii ), Kenny (1992, pg. 17, as H. leprieurii ; pg. 18, as H. leprieurii var. heptadactyla ), Foldats et al. (2003, fig. 351), Léotard et al. (2017, fig. 9), Szlachetko et al. (2016, fig. 65, reproduction from Dunserville & Garay (1979); fig. 66, based on Spruce 3650 [P!])), Szlachetko et al. (2017, fig. 209, reproduction from Dunsterville & Garay (1979); fig. 210, based on Spruce 3650 [P!]; fig. 211, based on Riaño & Duron 190 [COAH, FMB!]; fig. 212, based on Cabrera 2329 [COL!]; figs. 214 & 215, based on Langenheim 3255 [ US, COL!], as H. leprieurii ).

Additional specimens examined:— BOLIVIA: Santa Cruz, Velasco Province, Parque Nacional Noel Kempff Mercado, Huanchaca, 13º53’41”S, 60º48’46”W, 500 m, 23 January 1997, Soto et al. 332 (G!, MO, SI!); Apolo [Franz Tamayo Province, La Paz Department], 6000 ft, 20 February 1902, Williams 129 (BM!, K!, NY!); Santa Cruz, Chiquitos, Serrania de Santiago de Chiquitos, E of pass on road to Sunsas, 18º19’S, 59º34’W, 900 m, 25 January 2001, Wood & Goyder 16960 (K!). BRAZIL. Amazonas. Humaitá, margem da rodovia Humaitá-Porto velho, a 5 km de Humaitá, km 8 da BR-319, Irina & Gentchujnicov s.n. (HB 70454!); Humaitá, campo natural ao leste da BR 319, km 670, 23 December 1979, Janssen & Gemtchujnicov 62 (INPA!, M!); Distrito Federal. Paranoá, São Bartolomeu , 2 March 1993, Batista 414 (CEN!); Brasília, Setor de Mansões do Lago Norte, 12 February 1997, Batista 674 (CEN!); Brazlândia, RA IV, Chapada da Contagem, Fazenda Dois Irmãos, 28 February 2005, Bertioli s.n. (BHCB 97467!); Brasília, Estação Ecológica Jardim Botânico de Brasília - Área do Cristo Redentor, depois da manilha à direita, 12 February 2009, Chacon et al. 507 (HEPH!); Brasília, Estação Ecológica Jardim Botânico de Brasília, Área do Cristo Redentor, após o córrego, 13 February 2012, Chacon & Rodrigues 910 (HEPH!); Gama, aproximadamente na altura do km 8 da DF-290, 8 February 1996, Gonçalves s.n. (CEN 25380!); Brasília, Paranoá, São Bartolomeu , 4 March 1980, Heringer et al. 3665 (IBGE!); Paranoá, São Bartolomeu , 5 March 1980, Heringer et al. 3713 (IBGE!); Paranoá, São Bartolomeu , 11 March 1980, Heringer et al. 3778 (IBGE!); Paranoá, São Bartolomeu , quadricula 141, 17 March 1980, Heringer et al. 3953 (AMES!, IBGE!); Ceilândia, adjacência da barragem do Descoberto, 3 February 2004, Pastore 864 (CEN!). Goiás. Cavalcante, Chapada dos Veadeiros, 5 km após Cavalcante, em direção ao entroncamento com a GO-118, 22 February 1997, Batista et al. 718 (CEN!); Alto Paraíso de Goiás, Chapada dos Veadeiros, em direção a Colinas, cerca de 39 km do entroncamento com a GO-118, 23 March 1997, Batista et al. 727 (CEN!); Pirenópolis, Fazenda do Lázaro, 11 km NE de Pirenópolis. Reserva Ecológica Vargem Grade, nas encostas do lado direito do rio um pouco antes da Cachoeira do Lázaro, 6 February 2000, Batista & Proite 1043 (CEN!); Cocalzinho de Goiás, km 55.5 da rodovia Brasília—Corumbá de Goiás, Fazenda Santa Rita da Contagem Velha, 2 March 1993, Bianchetti 1473 (CEN!); Santo Antonio do Descoberto, Morro a aprox. 1 Km do centro da cidade, 26 February 1980, Heringer et al. 3457 (HB!, IBGE!, K!); Santo Antônio do Descoberto, 26 February 1980, Heringer 3472 (HB!, IBGE!, NY!); Girassol, Vale do São Gerônimo , loteamento chácara da montanha, caminho para a lagoa do pato selvagem, em frente a entrada da fazenda Recanto da Paz, 12 February 2000, Miranda 26 (CEN!); Cavalcante, área à margem esquerda da pista, cerca de 5 km após Cavalcante, em direção ao entroncamento com a GO-118, 22 February 1997, Oliveira et al. s.n. (UB0018781!); Serra dos Caiapos, 40 km de Amorinópolis para Rio Verde, 22 February 1972, Rizzo & Barbosa 6260 (UFG!); Mossâmedes, Serra Dourada, 17 March 1994, Rizzo et al. 11103 (UFG!); Santo Antônio do Descoberto, 27 March 1980, Salles 144 (BHCB! mixed with H. tamanduensis and H. obtusa Lindl. (1835: 315)) ; Cocalzinho de Goiás, Fazenda Santa Rita da Contagem Velha, 3 April 1992, Salles 1859 (HEPH!). Mato Grosso. Parque Nacional, Chapada dos Guimarães, próximo à cachoeira Véu de Noiva, 1 March 1983, Cunha et al. 751 (INPA!); Chapada dos Guimarães, Parque Nacional Chapada dos Guimarães, trilha do Véu da Noiva, em direção ao vale da mata do Véu da Noiva, 28 February 2011, Mota 2061 (BHCB!); Chapada dos Guimarães, Parque Nacional Chapada dos Guimarães, trilha do Morro de São Gerônimo , 3 March 2011, Mota 2131 (BHCB!); Cuiabá, entroncamento das rodovias Cuiabá/Santarém e Porto Velho, arredores do aeroporto, 4 February 1979, Silva & Pinheiro 4434 (INPA!, MG!); Diamantino, December 1844, Weddell 3074 (BR! fragment, P!); Serra Ricardo Franco, próximo fronteira com a Bolívia, 7 February 1978, Windisch 1547-A (HB!); Serra Ricardo Franco, 4 February 1978, Windisch 1574 (HB!). Mato Grosso do Sul. São Gabriel do Oeste, estrada de São Gabriel a Rio Negro, 1 March 1994, Pott & Pott 6767 (CPAP!). Roraima. Boa Vista, em campo de lavrado próximo a EMBRAPA, 17 July 2002, Bianchetti 1719c (CEN!); Boa Vista, Igarapé Caranã, 20 August 1951, Black 51-12774 (IAN!); Boa Vista, localidade Monte Cristo, chácara do Sr. Cleber Barroso, 12 October 1991, Silva 246 (MG!); Rio Branco, 6 July 1937, Ducke s.n. (RB! 37467); Boa Vista, Rio Branco, August 1913, Kuhlmann 786 (AMES!, RB!, SP!). Tocantins. Porto Nacional, setor campus dos Ipês Centro universitário Porto Nacional, 13 March 1995, Alves s.n (HTINS! 2160); Miracema do Tocantins, acesso à fazenda Sérgio a partir da est. do cór. Santa Luzia para Barrolândia, 13 January 1999, Arbocz 6493 (HTINS, IBGE!); Estrada de terra para Pindorama, ca. de 2 km do entroncamento com a BR-010, 26 March 2011, Bringel & Moreira 716 (IBGE!, UB!); Ponte Alta do Tocantins, Bacia do Tocantins, 10º49’48”S, 47º30’00”W, 19 November 2008, Fagg & Oliveira 1998 (CEN!, IBGE); Palmas, próximo a entrada para a fazenda Ecotropical, 4 February 2012, Faria et al. 2276 (UB!). COLOMBIA: Altillanuras, altillanura plana, cerca del hato La Bengala, al est del rio Manacacías, 6 June 1963, Blydenstein 1028 (COL!); Comisaría Del Vichada, 20 June 1972, Cabrera 2329 (COL!); Guaviare, San José Del Guaviare, ciudad de piedra, 2º28’1.4”N, 72º42’35.1”W, 423 m, 17 May 2014, Castro et al. 192 (COL!); Vichada, Puerto Carreno, Vda. Cano Negro, Finca La Pedregoza, 6º4’11.8”N, 67º45’14.3”W, 47 m, 4 July 2012, Córdoba & Castro 7612 (FMB!); Departamento Del Vichada, El Viento, Centro Las Gaviotas, 4 June 1995, Cortés & Dueñas 221 (COL!); El Vichada, to North of R. Vichada, near San José de Ocune, 1 May 1939, Haught 2798 (AMES!, COL!, NY!, US); Santander, about 1 km south of Floridablanca on road to Piedecuesta, 9 July 1953, Langenheim 3255 (COL!, US); Comissaria da Arauca, 30April 1937, Renz 4109 (RENZ!); Dep. Boyaca, 5 May 1937, Renz 4110 (RENZ!); Commissaria Vaupes, April 1938, Renz 4113 (RENZ!); comisaría del Vichada, Margen derecha Cño Blanco, SW Pto. Carreño, valle inferior del R. Vita, 12 July 1979, Salamanca 386 (COL!); Vichada, Parque Nacional Natural Tuparro, Riaño & Duron 190 (COAH, FMB! 8033, 37538). GUYANA: Rupununi Distr., Manari, 3 o 28’N, 59º41’W, 22 October 1979, Maas & Westra 3763 (U!). PANAMA. Bouche 7 (AMES!); 21 July1938, Woodson et al. 1406 (AMES!). TRINIDAD: Aripo Savana, 27 July 1943, Beard 142 (AMES!); Aripo Savana, 21 April 1920, Britton et al. s.n. (NY!); Aripo Savana, 16 April 1908, Broadway 2337 (AMES!); Broadway 2903 (AMES! mixed with H. cruegeri ); Aripo Savannah, 16 August 1922, Broadway s.n. (TRIN! 10181); Aripo, Crueger (?) s.n. (TRIN! 884); Aripo Savana, 22 May 1956, Doures & Aitken 97 (AMES!); Aripo Savannah, 13 February 1915, Freeman s.n. (TRIN! 8775); Johnson et al. 758 (TRIN! 32514); Savannah de Aripo, July 1848, Purdie 119 (K!); Aripo Savanna, 17 July 1983, Quesnel s.n. (TRIN! 28645); Aripo savanna, 13 August 1959, Richardson 663 (K!); Aripo savanna, 10 August 1961, Richardson 969 (K!); Aripo Savanna, near Cumuto, 14 August 1959, Webster et al. 9655 (S! mixed with H. cruegeri ); Aripo Savannah, 7 August 1925, Williams & Freeman s.n. (AMES 70134, TRIN! 113220); Aripo Savannah, Wright s.n. (TRIN! 35080). VENEZUELA: 23 February 1951, Cowan & Wurdack 32072 (NY!); Alto Orinoco, 14 July 1951, Croizat 71 (NY!); Cumaná, S. Augustin, August 1843, Füncke 630 (BM!, G!, K!, OXF!, P!, RENZ! photocopy from W-R, W-R! drawing); Salvajito, Haut Orénoque, 3 July 1887, Gaillard 53 (P!); Gran Sabana, 20 June 1983, Huber & Alarcon 7504 (NY!); Gran Sabana, 23 March 1952, Maguire 33544A (NY!); 27-28 March 1952, Maguire 33638 (NY!); Ter. Amazonas, Alto Orinoco, 23 March 1953, Maguire & Wurdack 34655 (NY!); Est. Tachira, 7 June 1949, Renz 5434 (RENZ!); Est. Merida, 31 July 1949, Renz 5707 (RENZ!); Est. Merida, 31 July 1949, Renz 5709 (RENZ!); Est. Merida, 29 July 1949, Renz 5710 (RENZ!); Est. Merida, 2 August 1949, Renz 5789 (RENZ!); prope Maypures, ad flumen Orinoco, June 1854, Spruce 3650 (BM!, BR!, K!, P!, W-R!); Estado Bolivar, 30 April 1953, Steyermark 75315 (NY!); WITHOUT LOCALITY: January 1866, Pearce s.n. (K000363831!).

Figures

FIGURE 4. Habenaria cruegerii. A. Habit. B. Leaf. C–G. Dissected perianth, bract, pedicellate ovary, gynostemium and spur. I. Inflorescence. J. Flower, lateral view. K–L. Flower, front view. M. Gynostemium, front view. Habenaria cruegeri var. flaviflora. H. Dissected perianth, bract, pedicellate ovary, gynostemium and spur. N. Flower, front view. A. Mota 3363 (BHCB). B. Batista et al. 701 (CEN). C, I, K. Bianchetti & Batista 843 (CEN). D.?. E. Batista 778 (CEN). F. Batista & Salles 69 (CEN). G. Batista 1595 (BHCB). H, N. Salles 1547 (HEPH). J, L, M. Batista 2810 (BHCB). Photographs by J.A.N. Batista.

FIGURE 5. Habenaria heptadactyla. A. Habit. B. Leaf. C–D. Dissected perianth, bract, pedicellate ovary, gynostemium and spur. E. Inflorescence. F. Flowers, front view. Habenaria alpestris. G. Habit. H–I. Leaf. J–K. Dissected perianth, bract, pedicellate ovary, gynostemium and spur. L. Inflorescence. M. Flowers, front view. B, F. Batista 674 (CEN). C. Batista 414 (CEN). D. Batista et al. 727 (CEN). E. Salles 1859 (HEPH). H, K, N. Batista et al. 1810 (BHCB). I, J, L. Batista 2505 (BHCB). Photographs by J.A.N. Batista.