New blueberry and mortiño relatives (Ericaceae) from northwestern Colombia

Abstract The inventory of the vascular plants of one of the richest and least studied floras, the Andean and Chocó regions of northwestern Colombia, targets Las Orquídeas National Park. As a result of field trips to areas never before collected, several epiphytic and small terrestrial shrubs in the family Ericaceae have been discovered in the Park’s humid forests. Five new, morphologically remarkable species of Ericaceae (tribe Vaccinieae), are here described and illustrated. In a separate phylogenetic analysis, Psammisia pinnata Pedraza, Psammisia pseudoverticillata Pedraza, Satyria orquidiensis Pedraza, and Satyria pterocalyx Pedraza, were placed by molecular sequence data within clades of the non-monophyletic genera Psammisia and Satyria; phylogenetic evidence for the placement of Psammisia sophiae Pedraza is still lacking. Their affinities are here discussed, along with their preliminary conservation status.


Introduction
Th e Colombian Western Cordillera and adjacent Chocó region, which belong to the Tropical Andes and Chocó biodiversity hotspots (Mittermeier et al. 1998, Myers et al. 2000, respectively, have the highest angiosperm diversity in N South America (Morawetz and Raedig 2007). Despite their importance, entire lineages endemic to or particularly rich in western Colombia are missing in monographic and phylogenetic works, as collections from this region have not been readily accessible, especially outside of the country. Th is unfortunate situation has silently weakened the scope of botanical research, while also undermining strategic planning for conservation and development in the Tropical Andes and the Chocó biogeographic regions, the world's fi rst and fi fth priority areas for conservation (Churchill et al. 1995, Mittermeier et al. 1998, Mast et al. 1999, Myers et al. 2000, Orme et al. 2005. To bring attention back to one of the richest and least studied fl oras, an inventory of the vascular plants of Las Orquídeas National Park (LONP) was undertaken. LONP is strategically located in the confl uence of the Tropical Andes and Chocó, in the Department of Antioquia (Colombia). Nested in the western slope of the Western Cordillera, LONP (29,118 ha; practically the same size of Grenada) boast an enormous altitudinal gradient (ca. 300-3,450 m) and consequent range of vegetation. In general, the forests below 2,000 m are considered to be part of the Chocó phytogeographic region (Rangel-Ch. et al. 2004) while the remainder is Andean.
Th e ongoing inventory of the vascular plants of LONP particularly targets remote areas that have never been botanically explored before. In addition to trees, collecting is also focused on non-tree plants, especially those that are epiphytic and which are usually omitted from rapid fl oristic and vegetation assessments in the tropics. Th is holistic collecting strategy has resulted in the discovery of several new non-tree plant species, including fi ve members of the family Ericaceae, all placed in the berry producing tribe Vaccinieae. Th ese fi ve new species are all restricted to the Colombian Western Cordillera and Chocó biogeographic region, and three of them are endemic to LONP. Th e new species are here described, illustrated, and discussed. Th eir preliminary conservation status is also included, based on the author's fi eld experience and knowledge of Colombian herbarium collections worldwide.

Vaccinieae diversity in Colombia
Although Vaccinieae is geographically widespread, the greatest species diversity lies in the mountains of Papua New Guinea and the Neotropics, most prominently in the N Andes. In the Neotropics, there are 46 putative genera and more than 800 species of Ericaceae and the great majority belong to the inferior-ovaried tribe Vaccinieae (Luteyn 2002); actually, 27 genera are native to the Neotropics and all are Vaccinieae. Th e members of Vaccinieae are better known by the edible and commercially important blueberry, from North America, and the mortiño [Vaccinium fl oribundum Kunth], from South America.
In the Neotropics, the most extensive radiation of Ericaceae took place in Colombia with 24 genera and 278 species documented, that is ca. 35 % of the neotropical Ericaceae. Notably, about 55 % of the Colombian species are endemic to the country (Pedraza-Peñalosa unpubl.). Within Colombia, the greatest diversity is found in Antioquia, where 18 genera and at least 116 species were recently documented (Pedraza 2011), before the discovery of the fi ve new species from LONP here described. Although Colombia contains already described hyper-diversity, its Ericaceae fl ora still remains poorly known, with many suspected undescribed species from sea level to the páramo.

Placement and phylogenetic affinities of new species
Th e taxonomic placement of new Vaccinieae is diffi cult due to the striking disparity between generic-level phylogenetic relationships and current classifi cation systems (Kron et al. 2002, Powell and Kron 2003, Pedraza-Peñalosa 2009, 2010. Th erefore, to determine the generic placement of the new species, four were included in a comprehensive phylogenetic analysis of neotropical Vaccinieae, based on chloroplast and nuclear sequence data of 91 species (Pedraza-Peñalosa et al. 2015). Unfortunately, amplifi cations of the fi fth new species (Psammisia sophiae Pedraza), which bears the most complex corolla structure, were not successful.
Th e molecular dataset was particularly rich in species of Satyria Klotzsch and Psammisia Klotzsch, both non-monophyletic and broadly defi ned groups, to which the fi ve new species are initially assigned based on their overall morphology (Pedraza-Penalosa et al. 2015). However, the new species possess unusual characters for the genera in which they are provisionally placed: P. sophiae has a corolla morphology unique among neotropical Vaccinieae; P. pinnata Pedraza is among the few Psammisia s.l. with very large and pinnate leaves; P. pseudoverticillata Pedraza is the only species in the group with clustered leaves and one of the few with markedly angled calyces; S. orquidiensis Pedraza is the only species in the group with clustered leaves, while its calyx ribs and constrictions makes it one of two species of Satyria s.l. with ornamented calyces; and lastly, S. pterocalyx Pedraza is the only other species in the group with ornamented calyx and apparently the only one with a corolla throat both dramatically constricted and elongated into a tube.
Eighteen out ca. 24 currently recognized species of Satyria s.l. were analyzed. Th e resulting best ML tree unequivocally placed the two new species described here, S. orquidiensis and S. pterocalyx, within a group that comprises Satyria s.s. (Pedraza-Peñalosa et al. 2015). Despite the fact that S. orquidiensis and S. pterocalyx are endemic to the same region, have similar corolla colors, and are the only Satyria s.s. known to have an ornamented calyx (winged and/or lobed), they are not closely related to each other.
Th e non-monophyletic Psammisia was split in the molecular analysis (Pedraza-Peñalosa et al. 2015). Th e largest of the groupings, Psammisia I clade, was dominated by species from the northern Andes. Psammisia pinnata and P. pseudoverticillata were both placed within one of its subclades, one mostly composed of Colombian species. All the species in this subclade share chartaceous to subcoriaceous leaves with pinnate venation (the majority of Psammisia have plinerved and coriaceous leaves) and short racemes with a rachis typically less than 1.6 cm long, which give infl orescences a fasciculated appearance, their corollas are medium size (8-22 mm long). However, the molecular sequence data show that the newly described Psammisia are not closely related.
Unfortunately, at this time it is not known which clade in the Psammisia complex will retain the generic name, as P. falcata (Kunth) Klotzsch, the type species of the genus has not been sequenced yet. Th us, taxonomic and nomenclatural changes in Psammisia s.l. are anticipated. Moreover, because only 14 out of about 70 spp. of Psammisia species were analyzed, a broader sampling of the group and related genera is needed to better infer the relationships of the new species described here. Names are coined here in order that they may be used in future studies both of phylogeny and conservation of Colombian plants.
Etymology. Th e species name indicates the characteristic pinnate leaf venation. Preliminary conservation status. Psammisia pinnata occupies a large geographic area and ample altitudinal range, therefore there is no concern for its conservation status. However, it must be noted that Colombian Andes have alarming rates of deforestation and transformation, putting its natural vegetation under constant threat.
Specimens examined. COLOMBIA. Antioquia: Municipio Urrao, Corregimiento La Encarnación, Vereda Calles, Parque Nacional Natural Las Orquídeas, fi nca de Alfonso Pino, entre la divisoria de las quebradas La Virola y El Bosque, al NW de la cabaña Calles, 6°31'35"N; 76°15'50"W, 1450-1470 m, 27 Jan 2011 (fl , fr), P. Pedraza-Peñalosa et al. 2015  Diagnosis. Psammisia pseudoverticillata can be easily diff erentiated from all other Psammisia s.l. by its leaves, which are clustered and seemingly verticillate, chartaceous, large, obovate, bullate in vivo, pinnate, decurrent at the base, and subtended by a basally pulvinated petiole. Its congested racemes bear fl owers that are distinctive because of their large size, thickness and fl eshiness; however, it must be noted that the fl owers of this new species shrink signifi cantly upon drying. Th e fl owers of P. pseudoverticillata are also characterized by its color combination and angled calyces and corollas (calyces markedly angled).
Distribution and ecology. Psammisia pseudoverticillata is endemic to Antioquia (Colombia) and it is only known by the type specimen collected in Las Orquídeas National Park. It is known to fl ower in January and February. It grows in humid montane forests at 1600-1850 m.
Etymology. Th e species epithet refers to the clustered tendency of the leaves. Preliminary conservation status. Psammisia pseudoverticillata it is only known by the type specimen collected in montane forests of Las Orquídeas National Park. Only one individual has been observed throughout several years of fi eldwork. Currently, montane forest, and the park in general, suff er from degradation product of human activities (agriculture, selective logging, livestock), therefore I consider this species vulnerable due to the small area it occupies, its perceived scarcity, and current habitat threats.
Discussion. Apparently, Psammisia pseudoverticillata is the only in the genus with seemingly verticillate leaves; only P. oppositifl ora Luteyn has opposite or subopposite leaves. Psammisia pseudoverticillata is morphologically closer to P. orthoneura but the latter is diff erentiated because of its evenly distributed glabrous leaves (vs. leaves clustered, glabrate with minute hairs in P. pseudoverticillata); obscurely articulate pedicels or apparently continuous with the calyx (vs. articulate); shorter (7-8 mm long), cupuliform, terete calyces (vs. 8-11 mm long, ellipsoid, with 5 well-defi ned angles); terete and shorter corollas (12-13 mm long vs. 5-angled, 12-19 mm long); and its staminal connectives with obsolete spurs (according to protologue) (vs. without spurs). A plant collected in La Serranía de los Paraguas (Valle del Cauca, Municipio El Cairo), where several Ericaceae novelties have recently been found (Pedraza-Peñalosa 2008), was identifi ed by James L. Luteyn as P. aff . orthoneura. Th is specimen (Luteyn 12330) may belong to P. pseudoverticillata. However, the fl owers are too immature to make an accurate identifi cation given slight diff erences in leaf shape.
Distribution and ecology. Psammisia sophiae is endemic to Antioquia (Colombia) and it has only been collected in Las Orquídeas National Park. It is known to fl ower in December and July and fruit in January. It grows in conserved humid premontane forests at 1160-1400 m.
Etymology. Named after my daughter, Sofi a Varón, an equally beautiful bloom. Preliminary conservation status. Psammisia sophiae is only known from collections made in Las Orquídeas National Park. Despite collecting in that protected reserve for many years only a few specimens have been procured. Th is species seems to prefer conserved premontane forests. Currently, these forest, and the park in general, specially toward lower elevations, suff er from degradation product of human activities (agriculture, selective logging, livestock). I consider this species vulnerable due to the small area it occupies, its perceived scarcity, and current habitat threats.
Discussion. Although vegetatively similar, P. sophiae can be told apart from P. panamensis, not only because of their strikingly dissimilar fl owers (obconic, terete, and with transversal bands of red, black and white in the latter), but also because the leaves of P. panamensis are glabrous and when dried, the lamina has a black-bluish tint on both sides (vs. hairs present, lamina drying brownish with a distinctive dark marginal band abaxially in P. sophiae), its petioles are not caniculate (vs. caniculate), and its rachis, bracts, bracteoles, and pedicel are longer.
Distribution and ecology. Satyria orquidiensis is endemic to Antioquia (Colombia) and it only known from collections from Las Orquídeas National Park. It is known to fl ower in January and fruit in January and July. Th is species grows in the canopy of humid premontane and montane forests at 880-1470 m, but it is possible that it could be found at lower altitudes as well. [Photos by P. Pedraza-Peñalosa.] Etymology. Named after Las Orquídeas National Park (Colombia), where the species is endemic to.
Preliminary conservation status. Satyria orquidiensis it is only known by specimens collected in Las Orquídeas National Park. It is commonly observed in conserved premontane and montane forests, but because it is a liana normally found high in the canopy, only a few collections exits. Because the observed abundance within the protected area I consider this species of least concern.
Discussion. Morphologically, Satyria orquidiensis and S. pterocalyx stand out within the genus and have more similarities among themselves than with other species; these are the only species in the genus with conspicuous wings and/or ribs on their calyces. Although their large corollas share similar colors and obconic shape, they can be easily diff erentiated because S. orquidiensis has corollas inconspicuously 5-angled (vs. terete in S. pterocalyx), orange with green lobes (vs. red-orange with the tube and lobes green-whitish) that gradually decrease in diameter toward the lobes (vs. dramatically constricted at the throat which is elongated into a tube ca. 8 mm long). Also, the dark or light orange (vs. light green) calyces of S. orquidiensis are conspicuously ribbed on the tube and sharply constricted between the limb and tube (vs. calyces 5-winged, tube with two basal lobes in each of the facets demarked by the wings, not transversally constricted). Vegetetatively, these two new species are even more distinct as S. orquidiensis has leaves that are clustered and seemingly verticillate (vs. not clustered in S. pterocalyx), larger [(14-)18.7-28 cm long vs. 14-18 cm], basally subcordate (vs. obtuse or cuneate), apically acute to acuminate (long acuminate, acumen 1.8-2.8 cm long), and with inconspicuous basal laminar glands (vs. absent).
Distribution and ecology. Satyria pterocalyx is restricted to the biologically rich montane forests of Western Colombia (Antioquia, Choco). It is known to fl ower in December and January.
Etymology. Species named after the rare winged calyces. Preliminary conservation status. Satyria pterocalyx is known from two localities far apart (from adjacent departamentos) that confer it a not so small geographic range. However, after botanizing for several years in Antioquia, this species remains only known by two individuals. Although collected a few miles from Las Orquídeas National Park, S. pterocalyx has not been found within the protected area. Currently, Colombian montane forest suff er from degradation product of human activities (agriculture, selective logging, livestock, mining, etc.), therefore I consider this species vulnerable due to its perceived scarcity and current habitat threats.
Discussion. Th e morphological diff erences and similarities between Satyria pterocalyx and S. orquidiensis are discussed under the latter.