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==Taxonomic notes==
==Taxonomic notes==
The genus ''Bifrenaria'' has been trditionallt classified under [[Bifrenariinae]] subtribe of tribe [[Maxillariae]], [[Epidendroideae]] subfamily, however, the relationships among the several genera within this tribus are not well defined and changes are foreseen for next years. The genus closest to ''Bifrenaria'' is ''Rudolfiella''. Other related genera are ''[[Teuscheria]]'', ''[[Guanchezia]]'', ''[[Hylaeorchis]]'' and ''[[Horvatia]]'', besides the more distant ''[[Scuticaria]]'' and ''[[Xylobium]]''. Recently is was suggested the unification of subtribes [[Lycastinae]], [[Maxillariinae]] and [[Bifrenariinae]], however, there is no consensus on the path to be followed.<ref><span style="font-variant:small-caps;">Whitten, W. Mark, Williams,  Norris H. &  Chase, Mark W.</span> (2000). Subtribal and generic relationships of Maxillarieae (Orchidaceae) with emphasis on Stanhopeinae: combined molecular evidence. American Journal of Botany. 2000;87:1842-1856. [http://www.amjbot.org/cgi/content/abstract/87/12/1842 Published on the Internet]</ref> Contrary to what was previously thought, the relationship among ''Bifrenaria'' al all these genera from [[Central America]] seems to indicate a primitive origin of ''Bifrenaria'' in [[Central America]] and its posterior dissemination towards the Southeast of Brazil, where it found fertile grounds to its more recent evolution.<ref name="Tese"/>
In 2000, the first more complete molecular analysis on ''Bifrenaria'' species were made.<ref name="Tese"/> Sixteen species of this genus and six of close genera were studied searching for conffirmation of their phylogenetical position, besides the delimitation of each species and each of ''Bifrenaria'''s groups. The obtained results do not allow the acceptance of genus ''Adipe'' and, although they confirm ''Cydoniorchis'' monophyly, they dissuade their use otherwise six other genera should need to be created to fulfill the remaining fifteen species. They discuss also the convenience of splitting two species that are similar to eachother and variable among themselves, with many hard intermediate forms hard to delimitate as ''[[Bifrenaria charlesworthii|B. charlesworthii]]'' and ''B. racemosa''. It is also confirmed the position of ''B. steyermarkii'' out of ''Bifrenaria'' yet no genus name is suggested.
The first species to be described, today classified as a ''Bifrenaria'', was initially denominated ''Dendrobium harrisoniae'' by the author of its description, the English Botanist [[William Jackson Hooker]],<ref><span style="font-variant:small-caps;">Hooker, William Jackson</span> (1824). ''Dendrobium harrisoniae'' in Exotic Flora. 2: t. 120. Edinburgh.</ref> now ''[[Bifrenaria harrisoniae]]''. In 1827, Hooker described the first species of the small ones group, ''B. racemosa'', however, classified it under the genus ''[[Maxillaria]]''.<ref><span style="font-variant:small-caps;">Hooker, William Jackson</span> (1827). ''Maxillaria racemosa'' in Botanical Magazine vol. 54: t. 2789. Curtis Ed., London.</ref> With this two publications started a long series of species descriptions and confusing genera about which many doubts existed during the two following centuries. The [[Royal Botanic Garden]] registers the submission of 69 species or ou varieties under genus ''Bifrenaria'' since the description of the first species.<ref name="Kew"/> Among these, twenty are generally accepted but only seventeen are well established, having no doubts about their true limits and classification. Thirteen species are accepted but now belong to other genera; and four or five, due to deficiencies on their descriptions, possibly will never be solved. The remaining species and varieties are synonyms of the accepted ones.<ref name="Tese"/>
The first species to be described, today classified as a ''Bifrenaria'', was initially denominated ''Dendrobium harrisoniae'' by the author of its description, the English Botanist [[William Jackson Hooker]],<ref><span style="font-variant:small-caps;">Hooker, William Jackson</span> (1824). ''Dendrobium harrisoniae'' in Exotic Flora. 2: t. 120. Edinburgh.</ref> now ''[[Bifrenaria harrisoniae]]''. In 1827, Hooker described the first species of the small ones group, ''B. racemosa'', however, classified it under the genus ''[[Maxillaria]]''.<ref><span style="font-variant:small-caps;">Hooker, William Jackson</span> (1827). ''Maxillaria racemosa'' in Botanical Magazine vol. 54: t. 2789. Curtis Ed., London.</ref> With this two publications started a long series of species descriptions and confusing genera about which many doubts existed during the two following centuries. The [[Royal Botanic Garden]] registers the submission of 69 species or ou varieties under genus ''Bifrenaria'' since the description of the first species.<ref name="Kew"/> Among these, twenty are generally accepted but only seventeen are well established, having no doubts about their true limits and classification. Thirteen species are accepted but now belong to other genera; and four or five, due to deficiencies on their descriptions, possibly will never be solved. The remaining species and varieties are synonyms of the accepted ones.<ref name="Tese"/>


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Bifrenaria
Bifrenaria harrisoniae
Bifrenaria harrisoniae
Scientific classification
Domain: Eukaryota
Kingdom: Plantae
Division: Magnoliophyta
Class: Liliopsida
Order: Asparagales
Family: Orchidaceae
Subfamily: Epidendroideae
Tribe: Cymbidieae
Subtribe: Maxillariinae
Genus: Bifrenaria
Lindl. 1832
Type species
Bifrenaria atropurpurea
Lindl. 1832
Species
Synonyms

Bifrenaria is a genus of orchids formed by twenty species of South America, some among the favorites of orchid growers because of their abundant showy flowers, which are large and very fleshy and at first glance seem artificial flowers made of wax. There are no known uses for them other than ornamental.

Despite the low number of species, they can be split in two clearly distinct groups:[1] one of highly robust plants with large flowers, that encompass the first species to be classified under the genus Bifrenaria; other of more delicate plants with smaller flowers occasionally denominated Stenocoryne or Adipe. There are yet two other species that normally are classified as Bifrenaria but which molecular analysis indicate to belong to different orchid groups. They are Bifrenaria grandis, endemic of Bolívia, which many taxonomists denominate Lacaena grandis,[2] and Bifrenaria steyermarkii, inhabitant of northern Amazon Forest,[3] which does not have an alternative classification as yet.

Distribution

Bifrenaria exist from the north of South America, one species reaching Trinidad, until Rio Grande do Sul, the farther south State in Brazil, however they are split in two isolated areas:[4] Amazon Forest and Atlantic Forest of Brazil. The later, where seventeen species are present, may be considered their recente center of distribution. The montane area of Rio de Janeiro State and Espírito Santo is particularly rich with fifteen species registered. Serra dos Órgãos mountains area, in Rio, is reported as habitat of fourteen Bifrenaria species,[5] however, some of these species are considered synonyms today,[6] being eleven a more realistic number of species existing in the said area.

The species with large flowers are more common on Region Southeast of Brazil, however, they inhabit from the sunnier areas of the seashore to rocky mountain areas of Minas Gerais e Bahia States, from almost sea level up to 2,000 meters of altitude, some species reaching Rio Grande do Sul state.[7] No species of large flowers exist in Amazon Forest. Some species grow directly attached to the famous Sugarloaf Mountain in Rio de Janeiro which can be observed by the commuters in the cable car. The recent centers of irradiation of this group are the seashore close to Serra do Mar chain of mountains, and the high chains of mountains of Minas Gerais.[8] The most common species in this group, spread from Rio Grande do Sul to Bahia, is B. harrisoniae.[9]

The smaller species of Bifrenaria, which some taxonomists classify under the genus Adipe, are more common on less sunny areas and can be found between 300 and about 1,600 meters of altitude.[5] Six species are native in Serra do Mar Chain of mountains and its arms, place considered the center of distribution of the small species. Only three small species inhabit Amazon, Bifrenaria venezuelana, B. longicornis and B. steyermarkii, none found above 1,450 meters of altitude, yet they are much more common on low altitudes.[10] The most common species is B. aureofulva,[11] however, because the geographic characteristic of its territory, without obstacles, B. longicornis is the species spread troughout the largest area, reaching Colombia, Venezuela, Peru, Surinam, Guyanas, Trinidad and all Amazonic area in Brazil.[12]

Two species seem to be endemic in highly restricted areas: B. silvana. discovered in 1987 at Serra da Ouricana mountains, nearby Itororó, in Bahia whch belongs to Adipe group;[13] and B. verboonenii, discovered in September 1995 on Serra do Cipó mountains, close to Diamantina, Minas Gerais, of the large Bifrenara group.[14]

Bifrenaria species inhabit three different environments. The large species generally live in well illuminated areas, occasionally epiphyte on trees of sparse foliage, more often as lithophytes, in campos rupestres, montane rocky areas that exist mostly in Rio and Minas Gerais States of Brazil, or over rocks in jungle's clearances. B. tyrianthina is exclusively lithophyte,[15] B. tetragona and B. wittigii hardly ever do. B. atropurpurea is the only species found living terrestrially, but in rare occasions. The large species always show .[10]

The small species from Southeast Brazil live in cloud montane forests, where the appear in much darker places than the large species. Within this sort of forests the temperature presents noticeable difference between day and night and also through the seasons. These also are plants of caespitous growth, almost all epiphytes, despite there is at least one record of Bifrenaria aureofulva living lithophylically in Chapada Diamantina, Bahia.[16]

The species from Amazon inhabit tropical lowland forests and equatorial forests. Bifrenaria longicornis is mostly found in flood areas along the igapós and igarapés (seasonal flood streams and small rivers of Amazon), and occasionally in open fields where the humidity is high and temperature constant through the year, normally in well iluminated places, although not under direct sunlight.[17] B. venezuelana inhabits forests in higher elevations, closer to the Andes.[18] Amazon species are epiphyte and the only Bifrenaria species with elongated rhyzome and ascendant growth.

Description

Bifrenaria generally are robust plants, of sympodial growth, which measure between ten and sixty centimeters height. Characteristics of an orchid to be classified under this genus are: to show roots of round section with thick vellamen; four angled fleshy pseudobulbs of one internode, often basally protected by dried steaths and with only one apical leaf, except for Bifrenaria steyermarkii, which occasionally has two;[19] plicate enervated leathery leaves, yet malleable and not exceedingly thick, with a pseudopetiole of basal round section; basal inflorescences bearing up to ten flowers, which seldom surpass the leaves length.[8]

Bifrenaria flowers are fragrant or have a strong scent, they have sepals slightly larger than the petals, the lateral ones basally united to the column foot forming a calcar with truncated extremity; labellum variously shaped, often hairy, articulated to the column, with a longitudinal channeled callus often with a basal claw; the column is slightly arching, generally without wings or any other appendages, bearing a foot which the labellum is hinged to; they show two elongated stipes, hardy ever one, at least twice longer than wide, whit salient viscidium, visible caudicles and retinacle in inverted positions; four hard superposed pollinia, protected by a deciduous incumbent anther.[10] The fruits are green, erect or pending, take about eight months to ripe and hold hundreds of thousand yellowish or brownish elongated seeds up to 0.35 mm long.[20] Among all the mentioned, the main characteristic to distinguish Bifrenaria form its related genera is the presence of the calcar on its flowers.[8] Other important qualities are the four sided unifoliated pseudobulbs besides the raceme inflorescence with to to ten flowers.[21]

Few is known about Bifrenaria species pollination. Apparently the only existing records report the presence of some large species' pollinaria observed on the back of male Eufriesea violacea, Euglossinae bees,[22] and of Bombus brasiliensis, Bombini bees.[23] Although there is no information of direct observation flower pollination, a research published in 2006 studied the micromorphology of the labellum of Bifrenaria species searching for substances useful to insects as food:[24] The absence of these substances on the densely pubescent surface of most Bifrenaria labelli in fact seems to indicate possible pollination by large bees as the mentioned before. Other indicator of this possibility is the strong smell emanated by some species, as B. tetragona, similar to the ones of other families flowers which are pollinated by these bees. The smaller species yet pubescent may be pollinated by smaller bees species ant the smooth ones which have strong colored flowers, as B. aureofulva, by hummingbirds.[24]

Bifrenaria are comparatively easy to grow orchids. They should be preferably potted on well drained vegetable fiber because their roots and pseudobulbs get rotten easily when kept humid for long periods. As previously mentioned three different environments are needed in accordance to the species origin to successfully grow these plants. The large species need more light than the rest. The small species from Brazilian Southeast may be cultivated at the same medium temperature but under less 10 to 20% luminosity. Bifrenaria from Amazon forest need higher and more constant temperature and humidity than the other species. All species need more water and fertilizer during their active growth season.[8]

Taxonomic notes

The genus Bifrenaria has been trditionallt classified under Bifrenariinae subtribe of tribe Maxillariae, Epidendroideae subfamily, however, the relationships among the several genera within this tribus are not well defined and changes are foreseen for next years. The genus closest to Bifrenaria is Rudolfiella. Other related genera are Teuscheria, Guanchezia, Hylaeorchis and Horvatia, besides the more distant Scuticaria and Xylobium. Recently is was suggested the unification of subtribes Lycastinae, Maxillariinae and Bifrenariinae, however, there is no consensus on the path to be followed.[25] Contrary to what was previously thought, the relationship among Bifrenaria al all these genera from Central America seems to indicate a primitive origin of Bifrenaria in Central America and its posterior dissemination towards the Southeast of Brazil, where it found fertile grounds to its more recent evolution.[10]

In 2000, the first more complete molecular analysis on Bifrenaria species were made.[10] Sixteen species of this genus and six of close genera were studied searching for conffirmation of their phylogenetical position, besides the delimitation of each species and each of Bifrenaria's groups. The obtained results do not allow the acceptance of genus Adipe and, although they confirm Cydoniorchis monophyly, they dissuade their use otherwise six other genera should need to be created to fulfill the remaining fifteen species. They discuss also the convenience of splitting two species that are similar to eachother and variable among themselves, with many hard intermediate forms hard to delimitate as B. charlesworthii and B. racemosa. It is also confirmed the position of B. steyermarkii out of Bifrenaria yet no genus name is suggested.

The first species to be described, today classified as a Bifrenaria, was initially denominated Dendrobium harrisoniae by the author of its description, the English Botanist William Jackson Hooker,[26] now Bifrenaria harrisoniae. In 1827, Hooker described the first species of the small ones group, B. racemosa, however, classified it under the genus Maxillaria.[27] With this two publications started a long series of species descriptions and confusing genera about which many doubts existed during the two following centuries. The Royal Botanic Garden registers the submission of 69 species or ou varieties under genus Bifrenaria since the description of the first species.[4] Among these, twenty are generally accepted but only seventeen are well established, having no doubts about their true limits and classification. Thirteen species are accepted but now belong to other genera; and four or five, due to deficiencies on their descriptions, possibly will never be solved. The remaining species and varieties are synonyms of the accepted ones.[10]

Few years later, in 1832, John Lindley proposed the genus Bifrenaria when describing its type species, Bifrenaria atropurpurea,[28] previously described by Loddiges as Maxillaria atropurpurea.[29] The name Bifrenaria comes from bi, two, and freno, brake, a reference to the shape of the two pairs of pollinia hold by separated caudicles presented by its flowers.[8]

In 1837, Constantine Samuel Rafinesque, considering the noticeable vegetative difference between the few Bifrenaria known at the time, proposed the genus Adipe, based on B. racemosa morphology, described by Hooker few years before, to which added the description of a supposed new species, today considered its synomym, with the name of Adipe fulva.[30] On next year Lindley received a specimen of B. longicornis from Amazon, which was morphologically even more distant from the known species, however, he described it as Bifrenaria. Five years later, apparently not aware of Rafinesque's previous genus Adipe, changed his mind and suggested that this species should be classified under a new genus, Stenocoryne.[31] While six species were attributed to Lindley's genus Stenocoryne by several taxonomists during following years, the genus Rafinesque proposed remained forgotten until 1990.[4]

Two species similar to Bifrenaria but that show a highly salient claw at the base of the labellum and lateral lobes abruptly divided, were then classified under this genus. In 1914, Rudolf Schlechter, based on Rudolfiella aurantiaca which presented the mentioned differences, suggested they should be classified under the genus Lindleyella, however this genus name was already occupied by plants of Rosaceae family.[32] Just thirthy years later, in 1944, the Botanist Frederico Carlos Hoehne, when working on the first revision of genus Bifrenaria corrected the suggestion of Schlechters. Hoehne initially proposed the genus Schlechterella to these species but, coincidentally, this name was also taken, now by Asclepiadaceae family plants.[33] Finally another name in homage to Schlechter was chosen, Rudolfiella, at the time with the number of species already increased to seven. On this revision, besides Rudolfiella, Hoehne divided Bifrenaria into two genera, therefore accepting the genus Stenocoryne proposed by Lindley but calling attention to the existence of Rafinesque's genus Adipe, which should have name priority over Lindleys and also raised doubts about the identity of several described species.[34] In 1990, Manfred Wolff resurrected the genus Adipe and to it submitted ten Bifrenaria species, besides the two already described by Rafinesque, however, not justifying his critters not revising the species.[35]

Making the picture even more complex, in 1994, Karheinz Senghas, based on several characteristics shared only by B. tetragona and B. wittigii, described the genus Cydoniorchis to accommodate them.[36] In 1996, Gustavo Romero and Germán Carnevali transfered to Bifrenaria a species originally described by Schlechter as Maxillaria petiolaris, now classified as Hylaeorchis petiolaris.[37] On the same year, Vitorino Castro Neto published the most recent revision of Bifrenaria and its five sections, which is the classification used today.[38]

References

  1. ↑ Cogniaux, Celestin A.(1902). Bifrenaria in Flora Brasiliensis K.F.P.von Martius & auct. suc. (eds.) vol.3 p. 5: 476. published on Internet.
  2. ↑ Kraenzlin, Friedrich Wilhelm Ludwig (1928). Lacaena grandis in Repertorium specierum novarum regni vegetabilis. Ed. Selbstverlag des Herausgebers, Berlin, at vol.25: 25.
  3. ↑ Dunsterville, Galfried Clement Keyworth & Garay, Leslie A. (1976). Bifrenaria steyermarkii in Venezuelan Orchids Illustrated vol.6: 56. London.
  4. ↑ 4.0 4.1 4.2 R. Govaerts, M.A. Campacci (Brazil, 2005), D. Holland Baptista (Brazil, 2005), P.Cribb (K, 2003), Alex George (K, 2003), K.Kreuz (2004, Europe), J.Wood (K, 2003, Europe) (Novembro 2008). World Checklist of Orchidaceae. The Board of Trustees of the Royal Botanic Gardens, Kew. Published on the Internet. (Access March 2009).
  5. ↑ 5.0 5.1 Miller, David , Richard Warren, Izabel Moura Miller & Helmut Seehawer (2006). Serra dos Órgãos sua história e suas orquídeas. Rio de Janeiro.
  6. ↑ Koehler, S. & do Amaral, M.D.E. (2004). A taxonomic study of the South American genus Bifrenaria Lindl. (Orchidaceae). Brittonia 56: 314-345.
  7. ↑ Castro Neto, Vitorino P. (2006). Bifrenaria atropurpurea in Icones Orchidacearum Brasilienses. ISBN 8590149447
  8. ↑ 8.0 8.1 8.2 8.3 8.4 Frederico C. Hoehne (1953). Bifrenaria in Flora Brasílica, Vol 12: 7. Instituto de Botânica de São Paulo. Cite error: Invalid <ref> tag; name "FB" defined multiple times with different content
  9. ↑ Castro Neto, Vitorino P. (2006). Bifrenaria harrisoniae in Icones Orchidacearum Brasilienses. ISBN 8590149447
  10. ↑ 10.0 10.1 10.2 10.3 10.4 10.5 Koehler, Samantha (2001). Estudo taxonômico e análise cladástica do complexo Bifrenaria Lindl. (Maxillarieae, Orchidaceae). Universidade Estadual de Campinas. Instituto de Biologia. Published on the Internet
  11. ↑ Lindley, John (1843). Bifrenaria aureofulva in Edwards's botanical register 29: t.52. Ed. James Ridgway, London.
  12. ↑ Lindley, John (1838). Bifrenaria longicornis in Edwards's botanical register 24: t.93. Ed. James Ridgway, London.
  13. ↑ Castro Neto, Vitorino P. (1991). Bifrenaria silvana in Boletim CAOB 3(4): 41.
  14. ↑ Romero, Gustavo A. & Castro Neto, Vitorino P. (2000). Bifrenaria verboonenii in Harvard Papers of Botany 5: 187 Cambridge.
  15. ↑ Toscano de Brito, Antonio & Cribb, Phillip (2005). Bifrenaria tyrianthina in Orquídeas da Chapada Diamantina. Ed. Nova Fronteira. ISBN 8520917828
  16. ↑ Toscano de Brito, Antonio & Cribb, Phillip (2005). Bifrenaria aureofulva in Orquídeas da Chapada Diamantina. Ed. Nova Fronteira. ISBN 8520917828
  17. ↑ Miranda, Francisco (2006). Orquídeas da Amazônia Brasileira. Ed. Expressão e Cultura, 1996. ISBN 8520802087
  18. ↑ Castro Neto, Vitorino P. (2002). Bifrenaria venezuelana in Icones Orchidacearum Brasilienses. ISBN 8590149447
  19. ↑ Foldats, Ernesto (1970). Xylobium steyermarkii em Novedades Cientificas, Contribuciones Occasionales del Museo de Historia Natural La Salle vol.35: 1. Serie Botanica. Caracas.
  20. ↑ Dressler, Robert L. (1993). Phylogeny and classification of the orchid family. Cambridge University Press.
  21. ↑ Campacci, Marcos A. (2003). Coletânea de Orquídeas Brasileiras II, Bifrenaria. Ed. Brasil Orquídeas. ISSN 16785606
  22. ↑ Dressler, Robert L. (1990). The orchids natural history and classification. London: Harvard University Press.
  23. ↑ Singer, Rodrigo B. & Koehler, S. (2004). Pollinarium morphology and floral rewards in Brazilian Maxillariinae (Orchidaceae). Annals of Botany 93: 39–51.
  24. ↑ 24.0 24.1 Davies, K.L. & Stpiczynska, M. (2006). Labellar Micromorphology of Bifrenariinae Dressler (Orchidaceae). Annals of Botany Company. Oxford University Press. published on the Internet
  25. ↑ Whitten, W. Mark, Williams, Norris H. & Chase, Mark W. (2000). Subtribal and generic relationships of Maxillarieae (Orchidaceae) with emphasis on Stanhopeinae: combined molecular evidence. American Journal of Botany. 2000;87:1842-1856. Published on the Internet
  26. ↑ Hooker, William Jackson (1824). Dendrobium harrisoniae in Exotic Flora. 2: t. 120. Edinburgh.
  27. ↑ Hooker, William Jackson (1827). Maxillaria racemosa in Botanical Magazine vol. 54: t. 2789. Curtis Ed., London.
  28. ↑ Lindley, John (1832). Bifrenaria in The Genera and Species of Orchidaceous Plants: 152.
  29. ↑ Loddiges, Conrad L. (1832). Maxillaria atropurpurea em Botanical Cabinet vol.19: t.1877. London.
  30. ↑ Rafinesque, Constantine Samuel (1837). Adipe em Flora Telluriana vol. 2: 101.
  31. ↑ Lindley, John (1843). Stenocoryne in Edwards's botanical register 29(Misc.): 53 Ed. James Ridgway, London.
  32. ↑ Schlechter, Rudolf (1914). Lindleyella in Orchideen: 414.
  33. ↑ Hoehne, Frederico Carlos (1944). Schlechterella in Arquivos de Botânica de Estado São Paulo, n.s., f.m., 2: 13.
  34. ↑ Hoehne, Frederico Carlos (1944). Rudolfiella in Arquivos de Botânica de Estado São Paulo, n.s., f.m., 2: 14.
  35. ↑ Wolff, Manfred (1990). Adipe em Orchidee (Hamburg) 41: 36.
  36. ↑ Senghas, Karlheinz (1994). Cydoniorchis em Journal für den Orchideenfreund 1: 11.
  37. ↑ Romero, Gustavo A. & Carnevali, German (1996). Bifrenaria petiolaris em Richard Spruce: Botanist and Explorer 180.
  38. ↑ Castro Neto, Vitorino P. (1996). Contribution to the study of the genus Bifrenaria. Proceedings of the 15th World Orchid Conference. Turriers, Naturalia Publications, Rio de Janeiro, pp. 376-383.
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