Tropical and temperate: evolutionary history of paramo flora.
The vascular plant flora of the tropical high Andes between tree-line and permanent snow-line, paramo, comprises over 3,500 species and is by far the richest of tropical alpine floras (Table 1). High species richness of paramo has been attributed to the large geographic extension of the Andes, connections to temperate zones via continuous mountain chains, and age of the mountains (Simpson, 1983; Smith & Cleef, 1988; Hedberg, 1992; Simpson & Todzia, 1990). Several plant groups diversified profusely in the equatorial Andes, of which the perhaps best known example is the composite subtribe Espeletiinae with some 140 species of varied growth forms in paramos and montane forests of Venezuela, Colombia, and Ecuador (Cuatrecasas, 1986; Diazgranatos, pers. comm.). Other species-rich paramo taxa, such as Valeriana, Gentianella, and Lupinus, are equally fascinating examples of adaptive radiation in the northern Andes (von Hagen & Kadereit, 2001; Bell & Donoghue, 2005; Hughes & Eastwood, 2006). Repeated isolation and expansion of plant populations due to climatic oscillations during the Plio-Pleistocene, interaction with pollinators leading to diversified flower morphology, and habitat heterogeneity have been suggested as possible mechanisms that enhanced species evolution within paramo groups (Cuatrecasas, 1986; Molau, 1988; Simpson & Todzia, 1990; Luteyn, 2002; Kadereit & von Hagen, 2003; Hughes & Eastwood, 2006).
A varied origin of the paramo flora was documented already three decades ago (Cleef, 1979). A significant proportion of taxa in the paramo flora belong to autochthonous plant groups that evolved in the Neotropics and subsequently--through local adaptations--gave rise to species that were adapted to the high altitude environment as it emerged over the past 5-10 My of mountain building. Another important group of paramo taxa are allochthonous, temperate plant groups that immigrated--often through long-distance dispersal--to the tropics from higher latitudes after environments suitable for species adapted to temperate conditions became available (Cleef, 1979; Simpson, 1983; van der Hammen & Cleef, 1983). In previous biogeographic analyses of the paramo flora, these two elements were further subdivided into endemic, Andean alpine, neotropical montane, and wide tropical elements for tropical groups, and Austral-Antarctic, Holarctic, and wide-temperate elements for temperate ones. This multiple origin of the paramo flora was studied using a chorological approach that assessed relative proportions of these geographic flora elements in different paramo sites (e.g., Cleef, 1979; van der Hammen & Cleef, 1986; Smith & Cleef, 1988; Sklenar & Balslev, 2007). The high importance of temperate taxa that had immigrated into paramo and contributed to its plant diversity was demonstrated through the chorological studies which documented that between one-half and two-thirds of the genera were of temperate origin (Cleef, 1979, 1981, 2005; van der Hammen & Cleef, 1986; Cleef & Chaverri, 1992; Ramsay, 1992; Salamanca, 1992).
The chorological approach, however, has clear limitations because geographic distribution of a taxon and its area of origin may not be congruent, i.e. patterns are in conflict with processes (Hedberg, 1965; Cleef, 1979; Ito et al., 2000; Sklenar & Balslev, 2007). The majority of species of Halenia, for instance, occur in paramos of the northern Andes (Allen, 1933; Luteyn, 1999), but a molecular phylogeny of the genus shows that high species richness of Halenia in the Andes resulted from rapid speciation following repeated immigrations from Central America (von Hagen & Kadereit, 2003). A parallel situation was found in chorological studies of the African flora in which species of several Afro-montane genera are phylogenetically nested within clades from the Cape floristic region, suggesting a northward migration from South Africa and rejecting hypotheses assuming dispersal in the opposite direction and of a relictual distribution (Galley & Linder, 2006). On a global scale, molecular phylogenetic studies have refuted the vicariance model for many southern hemisphere plant groups with disjunct distribution and instead revealed complex transoceanic dispersal patterns (Winkworth et al., 2002; Meudt & Simpson, 2006; Wagstaff et al., 2006). Phylogenetic studies using molecular markers thus provide an important tool for analyzing distribution patterns of taxa and for testing explicit biogeographic hypotheses regarding their origin, evolutionary history, migration routes, etc. (e.g., Winkworth et al., 2002, 2005; Comes & Kadereit, 2003; McDaniel & Shaw, 2003; Vargas, 2003; Albach et al., 2005b; de Queiroz, 2005; Gehrke & Linder, 2009).
In this paper, published molecular phylogenies that include paramo species are reviewed. Conclusions drawn from molecular phylogenies are compared with those based on previous chorological analyses. Finally current knowledge of geographic origin of the neotropical paramo flora based on the combined chorological and phylogenetic studies is summarized. Circumscription of the paramo flora is based upon Luteyn (1999) for species and Sklenar et al. (2005) for genera.
Geology and Paleoecology of the Tropical High Andes
The Andean South American cordillera is a nearly 9,000 km long complex mountain system with three latitudinal segments, i.e., the southern, central, and northern Andes (Clapperton, 1993; Graham, 2009). Geographical delimitation of paramo generally corresponds to the northern Andes with only minor oveflaps to the central Andes in northern Peru and to the Central American cordillera in Panama and Costa Rica. The northern Andes stretch from Venezuela and Colombia to the Amotape-Huancabamba zone in northern Peru (Fig. 1) and comprise a structurally varied system of cordilleras and deep valleys with different tectonic histories (Clapperton, 1993; Weigend, 2002). Their uplift resulted from a combination of multiple tectonic events acting in different geological periods. In the Colombian cordilleras, for example, uplift started during the Late Cretaceous/Paleocene with rise of the Western and Central Cordillera, whereas uplift of the Eastern Cordillera mostly occurred in the Pliocene (Kroonenberg et al., 1990; Clapperton, 1993; Coltorti & Ollier, 2000; Gregory-Wodzicki, 2000; Graham, 2009). It has been estimated that the northern Andes reached 40% of modern elevation by middle Miocene/early Pliocene and that they rose to current heights through rapid final uplift only by around 2.7 Mya (Gregory-Wodzicki, 2000).
The northern Andes are built of both volcanic and non-volcanic rocks. The Venezuelan Andes, the Colombian Eastern Cordillera along with the Sierra Nevada de Santa Marta, and some parts of the Central Cordillera are of non-volcanic origin, whereas the Colombian Western and Central Cordilleras and most of the Ecuadorian Andes are built of volcanic rocks (Clapperton, 1993; Graham, 2009). Hence volcanism is an important factor in formation of northern Andean ecosystems and affects distribution and population dynamics of many species (Salamanca, 1992; Sklenar et al., 2010). Many of the highest peaks in the northern Andes are volcanoes, including the highest mountain in the region, Chimborazo volcano (6,310 m), in central Ecuador.
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Evolution of the paramo biota is tightly linked to Andean orogeny. The northern Andes emerged above tree-line near the end of the Pliocene (3-5 Mya), which provides an approximate date for conditions suitable for development of the paramo ecosystem (van der Hammen et al., 1973; van der Hammen, 1974; van der Hammen & Cleef, 1986). During uplift, a semi-open vegetation is believed to have occurred on hilltops in the Andean region, determined by local climate or edaphic conditions. This hypothetical preparamo vegetation contained elements of savanna and subandean forest and might have been an important source of the neotropical element in modern paramo. By Late Pliocene/Early Pleistocene (1-2 Mya), the so-called protoparamo, a floristically poor early paramo vegetation, occupied large areas between 2,000 and 3,000 m. Its pollen spectrum (Poaceae, Valeriana, Plantago, Aragoa, Ranunculaceae, and with a later arrival of Caryophyllaceae, Geranium, Gunnera, Gentianella, Lysipomia) confirms presence of modern paramo taxa and a continually increasing proportion of genera with temperate distribution. By gradual enrichment of protoparamo the modern paramo ecosystem evolved during the Pleistocene.
During the Pleistocene, as many as 20 glacial cycles of various intensity occurred in the northern Andes (van der Hammen, 1974; van der Hammen & Cleef, 1986). Vegetation zones were shifted altitudinally by as much as 1,500-2,000 m, many of the isolated paramos merged, and the ecosystem as a whole covered an area many times larger than the present one (Fig. 2). During interglacial periods, paramo shrank and split into small islands. Such repeated pulses of expansion and contraction of the paramo ecosystem are believed to have affected diversity and distribution of biota of the high Andes. The Holocene period (since about 12,000 years ago) was characterized by two thermal optima when forest advanced to altitudes 300-400 in higher than today. Expansion of forest reduced extension of paramo and several paramo "islands" on smaller mountains may have disappeared.
Tropical Elements in the Paramo Flora
Tropical paramo elements comprise those taxa that entered high-altitude habitats from lower elevations of the (neo)tropical region by adapting to environmental conditions as mountains rose to present height (Smith & Cleef, 1988). One necessary step in that adaptive process must have been evolution of the ability to survive subzero temperatures, which is a year-round phenomenon in high-altitude paramo (Sarmiento, 1986; Rundel et al., 1994). Evolution of new adaptations by tropical plant lineages, such as frost resistance, is believed to have been the limiting factor in colonization of paramo habitats (Donoghue, 2008). Nevertheless, about three-fifths of vascular plant genera found in paramo have been classified as tropical paramo elements (Table 2).
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The endemic element in the paramo flora includes genera confined to the paramo ecosystem and radiating within it, although occasionally some species may be found in montane forest. In the chorologically-based analyses this element included 17 genera.
Aragoa (Plantaginaceae) is a distinct shrubby genus of 19 species endemic to paramos of Colombia and Venezuela, although some species may also occur in upper montane forest (Cleef, 1979; Fernandez-Alonso, 1995; Luteyn, 1999). Even if traditionally treated in the family Scrophulariaceae, molecular phylogenetic studies employing nuclear and plastid DNA markers found the nearly cosmopolitan, predominantly herbaceous Plantago as the sister taxon of Aragoa which justified its reclassification into Plantaginaceae (Bello et al., 2002; Ronsted et al., 2002; Albach et al., 2005a). The split of Aragoa and Plantago, estimated at 7.1 Mya, predates the Plio-Pleistocene occurrence of paramo habitats. Pollen of both genera is present in Plio-Pleistocene lake sediments in the Colombian Eastern Cordillera (van der Hammen & Cleef, 1986). This dating along with the contrasting geographical distribution of the genera raises a question as to their occurrence in paramo (van der Hammen & Cleef, 1986; Bello et al., 2002; Ronsted et al., 2002).
Albach et al. (2005a) suggested an Old World origin of Aragoa ancestors which would later become adapted to a newly evolving paramo environment. Xylem in Aragoa lacks rays and rayless wood appears related to secondary woodiness (Carlquist, 1988). Therefore, it was suggested that the woody habit of Aragoa is secondary, implying a herbaceous status of its ancestor (Fernandez-Alonso, 1995). Further evolution within Aragoa might have lead from a hypothetical arborescent form of montane forest towards paramo shrubs. Monophyly of the genus is supported, but a limited DNA sequence divergence suggests a recent diversification among the species and does not allow further biogeographic inference (Fernandez-Alonso, 1995; Bello et al., 2002).
Blakiella, Floscaldasia, Hinterhubera, Laestadia, and Westoniella (Asteraceae) are genera with a diversity of habits, ranging from low, prostrate herbs to tall shrubs, which belong to the predominantly southern hemisphere subtribe Hinterhuberinae (Nesom, 1994; Nesom & Robinson, 2007). The former four genera are mostly (Blakiella and Floscaldasia exclusively) confined to the northern Andes, but Hinterhubera is also reported from Chile and Laestadia from the central Andes, Costa Rica, and Hispaniola. Westoniella is endemic to the high mountains of Costa Rica and Panama (Karaman-Castro & Urbatsch, 2009). Twenty species in these genera occur in paramo (Luteyn, 1999; Sklenar et al., 2005). Molecular phylogeny using combined nuclear markers rejects monophyly of Hinterhuberinae, although it suggests monophyly, moderately to strongly supported, in Hinterhubera, Laestadia, and Westoniella. Monotypic Blakiella is sister to Laestadia-Hinterhubera, although support is weak. Floscaldasia, with two species of which only one was analyzed, occurs in a polytomy with Blakiella-Laestadia-Hinterhubera and other South and Central American subclades. Westoniella occurs in a well-supported subclade with Mexican Laennecia schiedeana as sister taxon (Karaman-Castro & Urbatsch, 2009). Neotropical (Central American in Westoniella) affinity of the group is evident but the polytomy of and poor support within subclades do not allow further conclusions as regards origin of the genera in paramo. Geographic distribution of Blakiella and Floscaldasia, limited to paramo, however, warrants their classification in the endemic element (Cuatrecasas, 1969; Sklenar & Robinson, 2000).
Espeletia s.1. (Asteraceae) is a complex of ca. 140 species endemic to the northern Andes. Major species richness is found in the Venezuelan Andes and the Colombian Eastern Cordillera (Cuatrecasas, 1979, 1986). Most species (>120) are confined to paramo habitats, ranging from shrubby subparamo thickets to high-elevation superparamo (Cuatrecasas, 1986; Luteyn, 1999). Based on synflorescence structure and life forms, Cuatrecasas (1976, 1979, 1986) divided this group into eight genera, six of them restricted to Venezuela and the Colombian Eastern Cordillera. One of the segregate genera, Libanothamnus, also reaches the Sierra Nevada de Santa Marta (Colombia), Sierra de Perija (Colombia/Venezuela), and the Cordillera de Avila (central coastal Venezuela). Espeletia s.s., with the largest geographical range, occurs also in the Central and Western Colombian Cordilleras and in Ecuador (see, e.g., Hooghiemstra et al., 2006, Fig. 8 for distribution map).
Cuatrecasas (1986) suggested that the common ancestor of the subtribe may have been a perennial, evergreen, branched shrub with xeromorphic foliage inhabiting mesic climates of semi-open montane forest scrub. This ancestor could have diversified into trees on the one hand and into monocaule of sessile rosettes on the other, and from polycarpic to monocarpic growth. Cuatrecasas further suggested an evolutionary relationship among the genera with expected evolution from montane forest-shrubby subparamo to superparamo belts. Based on geographic distribution of the genera and patterns of species diversity, he hypothesized migration from Venezuela and the Colombian Eastern Cordillera to the remaining parts of the northern Andes during the last glacial.
Monophyly of Espeletiinae, with the neotropical genus Ichtyothere asa possible sister taxon, is supported by two molecular studies using chloroplast and nuclear DNA markers (Panero et al., 1999; Rauscher, 2002). Poor species sampling and weak support of branches within clades, however, prevent inference about relationships within the group. For instance, Panero et al. (1999) found Espeletia pycnophylla, the only species reaching Ecuador, in the basal position of the group, which would contradict the scenario proposed by Cuatrecasas (1986). Rauscher (2002), in contrast, placed E. pycnophylla together with Colombian Espeletiopsis jimenez-quesadae and Paramiflos glandulosa, as sister group to the Venezuelan Coespeletia moritziana. In spite of the limited resolution of the two studies, they do suggest that at least some of Cuatrecasas' segregate genera may not be monophyletic and that evolutionary history of the group in the northern Andes has been more complicated than envisioned by Cuatrecasas (1986). It appears Espeletiinae underwent repeated migration, speciation, and hybridization events between populations inhabiting different paramo areas.
Molecular phylogeny supports the apparent neotropical origin of the Espeletia complex. However, much more representative sampling, covering the entire geographical range, is needed to disentangle its evolutionary history and to reveal the route that paramo was colonized by this group.
Although molecular phylogenies significantly improve our knowledge about evolution of paramo endemic taxa, they do not provide a clear picture of their origin in this altitudinal belt. The relationships within Espeletiinae and Hinterhuberinae remain insufficiently understood. Generic limits need to be revisited in the Espeletia complex to clarify colonization of paramo presumably from montane forest. Lineages endemic to paramo can be expected to be identified after more detail sampling. Confirmation of the Blakiella-Laestadia-Hinterhubera relationship would point to a paramo origin in the latter two genera and provide the first evidence about emigration of paramo lineages outside the neotropical region. Restricted geographic distribution in the northern Andes of Aragoa, Blakiella, and Floscaldasia justifies their placement in the endemic paramo category, although phylogenetic relationships and/or the route by which their ancestors entered paramo remain to be identified.
Neotropical Alpine and Montane Elements
Neotropical alpine and montane elements include genera that besides paramo occur in either (sub)alpine habitats outside the tropical Andes or also inhabit montane forest. As many as 242 genera have been classified in this element.
Areytophyllum (Rubiaceae) includes 15 species of small erect shrubs and prostrate subshrubs distributed at high elevations from Costa Rica to Bolivia with all except one species reported from paramo (Mena, 1990; Luteyn, 1999). Most Andean Rubiaceae have their closest relatives in tropical South America and they are thought to have originated through local speciation as a response to rise of the Andes. Arcytophyllum, in contrast, has its closest relatives in North America (Andersson & Rova, 1999) and in addition, is present in Central America, which suggests that the genus arrived to the Andes from the north. Molecular phylogenetic analysis using chloroplast DNA confirms monophyly of the genus after the Mexican A. serpyllaceum is excluded (Terrell, 1999; Andersson et al., 2002). The widespread American Houstonia and Hedyotis clade is a sister group to Arcytophyllum, and a South American origin of the Arcytophyllum-Houstonia clade seems most likely (Andersson et al., 2002). This suggests that Arcytophyllum originated in the Andes, but poor resolution within Arcytophyllum does not provide enough evidence to determine precisely where it originated. So, although initial molecular phylogenies suggested Arcytophyllum could have immigrated to the Andes from the north, more detailed studies confirm the assumption that it is a tropical Andean genus, as suggested in original chorological analyses.
The Centropogon clade (Siphocampylus, Centropogon--Campanulaceae) with over 600 species is particularly well developed in montane forests, but occasionally reaches above the tree-line--11 species of Siphocampylus and six of Centropogon are reported from paramo (Luteyn, 1999). Unlike Lysipomia (see below), which conserved the presumed ancestral herbaceous habit, shrubs, subshrubs, and occasionally treelets evolved in the speciose Centropogon clade. Most Siphocampylus and all Centropogon species together form a monophyletic group although the two genera are paraphyletic (Knox et al., 2008; Timmermann, Antonelli & Gustafsson, unpublished data). Among species of Centropogon and Siphocampylus that occur in paramo, several are fairly closely related, but probably not forming a monophyletic group, and available evidence is too weak for firm conclusion (Gustafsson, pers. comm.). Molecular evidence supports previous classification of these genera in the neotropical element. It appears that paramo species originated in several colonization events, but poor representation of paramo species in the analyses prevents further conclusions.
Chusquea and Neurolepis (Poaceae) are conspicuous neotropical bamboo genera inhabiting lowland to montane forests and high-altitude grasslands. Chusquea has some 140 species distributed in Central and South America (mostly SE Brazil and the Andes) and the West Indies. Neurolepis comprises 21 species distributed mostly in the Andes between Venezuela and Bolivia, with disjunct occurrence in Costa Rica, Panama, the Guayana Highland, and Trinidad (Clark, 1997; Judziewicz et al., 1999). Each genus is represented by ten species in paramo (Luteyn, 1999). Studies of a single chloroplast DNA marker supported monophyly of Chusquea with paramo species N. aperta as a sister taxon (Kelchner & Clark, 1997). However, later analysis employing five chloroplast markers revealed that Chusquea formed a well-supported clade nested between two Neurolepis clades, one of them containing paramo species (Fisher et al., 2009). Molecular phylogeny thus suggests that at least two lineages of Chusquea s.l., which now comprises also the two Neurolepis clades (Fisher et al., 2009), independently colonized paramo flora montane forest, and that chorological classification of Chusquea in the neotropical element is supported.
Chuquiraga (Asteraceae) is an Andean genus of 23 shrubby species distributed from Chile and Argentina to Colombia (Ezcurra, 1985) with three species reported in paramo (Luteyn, 1999). Based on morphological and molecular (nuclear DNA) data, two species groups are supported and characterized by leaf morphology and size and color of capitula and flowers (Gustafsson et al., 2001; Ezcurra, 2002). Paramo representatives belong to the group of hummingbird-pollinated species distributed in the central and northern Andes. A southern South America origin of Chuquiraga is suggested by phylogenetic studies, which imply a south to north migration into paramo.
Disterigma (Ericaceae) comprises 37 species of small shrubs distributed in Central and South America mostly in cloud forests but with eight species in paramo (Luteyn, 1999). Nuclear and plastid markers indicate that Disterigma is polyphyletic (Pedraza-Penalosa, 2009). The six sampled paramo species occur in a well-supported Disterigma s.s. clade to which neotropical montane forest Sphyrospermum and central Andean Disterigma species are sister. Based on the evidence, it may be concluded that Disterigma entered paramo from cloud forest. The poor resolution within the Disterigma s.s. clade, however, does not allow inference as to the number of colonization events (Pedraza-Penalosa, 2009). Nevertheless, classification of Disterigma in the neotropical element is justified by molecular data.
Halenia (Gentianaceae) is a herbaceous genus with tetramerous, mostly spurred flowers distributed in high-altitude areas of Asia and the Americas. While there are two species in eastern Asia, one species in temperate USA, and 15 species in Central America, about 50 species were reported in South America, although the real number may be lower (Allen, 1933; von Hagen & Kadereit, 2003), with 39 species being reported from paramo (Luteyn, 1999). Based on pattern of species richness and presence of spurless species, the Andes were thought to be the center of origin of the genus and consequently Halenia was considered a neotropical element (Allen, 1933; Cleef, 1979). Molecular phylogenetic analyses employing nuclear and chloroplast DNA, however, show that Halenia originated in eastern Asia and then immigrated via North and Central America to South America (Fig. 3). There is evidence for three independent dispersal events that occurred approximately 1 Mya, 0.8 Mya, and 0-0.2 Mya (von Hagen & Kadereit, 2003). Two of these colonization events gave rise to recent diversity of paramo species with an accelerated speciation rate in the group containing spurred flowers (Kadereit & von Hagen, 2003).
Jamesonia and Eriosorus (Pteridaceae), fern genera with about 20 and 25 species, respectively, of predominantly Andean distribution (Tryon, 1962, 1970), are together represented with 32 species in paramo (Luteyn, 1999). Jamesonia, with distinctly coriaceous leaves and highly reduced pinnae representing specialization to the paramo habitat, was believed to be derived from Eriosorus, which has variously pinnate leaves (Tryon 1962, 1970). Phylogenetic analyses using chloroplast and nuclear markers confirm monophyly of the Jamesonia-Eriosorus clade, but within that clade both morphologically defined Jamesonia and Eriosorus are paraphyletic (Fig. 4) (Sanchez-B., 2004). The Jamesonia-Eriosorus clade is sister to Guayana shield species of Pterozonium. Within this clade, Brazilian E. myriophyllus is sister to the remaining, largely Andean species that form three subclades suggesting three independent radiations, although two of the subclades have only moderate support. Brazilian E. insignis is nested among two Andean subclades, which would suggest two colonizations of the high Andes by Brazilian ancestors accompanied with a repeated evolution of the "jamesonia" growth form (Sanchez-B., 2004). This view of a widespread neotropical Jamesonia-Eriosorus clade, which gave rise to several immigrations and radiations in the paramo ecosystem with convergent evolution of the compact "jamesonia" form, is in contrast to the previous more simple scenario of a neotropical-montane Eriosorus with more branched fronds, which gave rise to compact Jamesonia that subsequently radiated in paramo.
Lachemilla (Rosaceae) is a genus of about 80 morphologically variable species, which includes perennial herbs and small shrubs. Lachemilla is distributed in South and Central America from Mexico and the Greater Antilles (Hispaniola) to the Andes of northern Chile and Argentina, at 2,200-5,000 m elevation: 34 species are reported from paramo (Luteyn, 1999; Romoleroux, 2004). A molecular phylogeny of Alchemillinae based on analysis of chloroplast and nuclear markers (Gehrke et al., 2008) shows that Lachemilla is monophyletic and forms a clade separate from Eurasian and African clades of Alchemilla (so called Eualchemilla and Afromilla clades, respectively) and a clade of a widespread Aphanes. The four clades are well-supported which, except for Aphanes, suggests a single dispersal event between geographic areas. However, direction of arrival of Lachemilla in the Andes remains to be clarified.
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Lasiocephalus (Asteraceae) is a genus of approximately 25 species distributed in the Andes from Venezuela to Bolivia and Peru with the highest species richness in Ecuador (Cuatrecasas, 1978; Sklenar et al., unpublished data). In this genus, two main growth forms are recognized, i.e., broad-leaved suffrutescent climbers of montane forest and tree-line ecotone and erect or ascending herbs or subshrubs with narrow subcoriaceous leaves of high-altitude paramo. Considering the relatively recent development of paramo habitats, evolution of paramo species from forest species is implied with growth form change reflecting adaptive radiation during colonization of paramo habitats (Cuatrecasas, 1978). Molecular analysis based on ITS data of three species of Lasiocephalus suggested a close relationship of Lasiocephalus to Culcitium which together were nested within Senecio s.s. (Pelser et al., 2007). ITS sequences of 14 species revealed two clades within Lasiocephalus (Duskova et al., 2010). Ecuadorian paramo species occurred along with the high-altitude Culcitium nivale in the first clade, whereas the Venezuelan paramo species L. longipenicillatus is nested within montane forest species in the second. These preliminary results thus suggest two paramo lineages. Further study using more markers is underway to provide a more robust phylogeny of Lasiocephalus.
Lysipomia (Campanulaceae) includes about 40 low-rosulate herbaceous species that occur predominantly in paramo of the northern Andes with a few species reaching southern Peru and Bolivia (Ayers, 1999; Luteyn, 1999). The genus is monophyletic (West & Ayers, 2006) and sister to a clade including the shrubby lobelioid genera Siphocampylus, Centropogon, and Burmeistera (Antonelli, 2008, 2009; Knox et al., 2008). Highest species diversity of Lysipomia is found on both sides of the Amotape-Huancabamba zone, i.e., in southern Ecuador and northern Peru. The genus comprises two subgenera, Rhizocephalum and Lysipomia, distinguished by size of corolla and presence/absence of nectar guides (Ayers, 1999; West & Ayers, 2006). Based on geographic distribution of the species, Ayers (1999) hypothesized that both subgenera as well as the entire genus may have originated south of the Amotape-Huancabamba zone. Whereas one dispersal event north across the Amotape-Huancabamba zone was suggested for subgen. Rhizocephalum, there may have been repeated migration events in subgen. Lysipomia. Molecular evidence thus supports the previous classification of Lysipomia as a neotropical element, but it appears it has reached paramo by repeated independent colonizations from the south.
Munnozia and Chrysactinium (Asteraceae) are herbs or subshrubs from the neotropical tribe Liabeae, subtribe Munnoziinae (Kim et al., 2003), of which seven and five species, respectively, are found in paramo (Luteyn, 1999). Molecular phylogenetic analysis employing nuclear DNA, which involved four paramo species of Munnozia and one species of Chrysactinium, supports a close relationship of the two genera (Kim et al., 2003). However, relationships between them are not completely understood as Chrysactinium occurs nested within Munnozia, although with only moderate support. Although additional sampling within the group is needed to reconstruct the exact biogeographic pattern, position of paramo species in the phylogenetic tree may suggest repeated entries into paramo within Munnoziinae. Previous chorologically-based assignments placed these genera in the neotropical element and molecular and phylogenetic evidence do not change their positions.
Perezia (Asteraceae) has about 30 species with southern South America--Andean distribution, of which three species are reported from paramo, although only two may be valid (Vuilleumier, 1970; Luteyn, 1999; Simpson et al., 2009). Molecular phylogeny employing chloroplast and nuclear markers showed the genus is not monophyletic, since two species are more closely related to other genera primarily from southern South America (Simpson et al., 2009). It is suggested that Perezia originated in temperate South America and that high-elevation species are the most derived (Simpson et al., 2009). Among paramo species, P. multiflora, which is widespread almost throughout the genus' distribution range, occurs in an derived position in a small subclade that is basal to the rest of the genus. Sister to P. multiflora in this subclade are two species from SE Brazil and western Argentina and Uruguay. Perezia pungens, the other paramo species, occurs in a distal position within the phylogenetic tree with species from the central Andes as sister taxa. Thus two independent arrivals in paramo from the south are suggested, which modifies the earlier ideas of the neotropical origin of the genus.
In several of the above discussed examples of paramo genera molecular data modify our views concerning their origin in paramo. Based on molecular evidence, independent colonizations of paramo habitats are implied in Lasiocephalus. Neurolepis is now merged within Chusquea, but still represents an independent genetical lineage in paramo. A similar situation is found in the Jamesonia-Eriosorus complex. The two genera together likely represent three lineages in paramo, which involved repeated evolution of the compact "jamesonia" growth form. Chuquiraga and Perezia were treated in the neotropical element but molecular data suggest their origin in the south temperate South America. Halenia provides one of the most striking examples of incongruence between the area of highest species richness and the area of likely origin. Contrary to the chorological pattern of the geographical distribution of species richness, molecular phylogeny indicates that the genus did not originate in the Neotropics but instead repeatedly immigrated there from the north.
Wide Tropical Element
This element includes 58 genera (Table 2) that are not only widely distributed in tropical and subtropical habitats of the New World, but also occur in the Palaeotropics and occasionally reach the temperate zone.
Elaphoglossum (Dryopteridaceae) is a large fern genus of some 600 species widely distributed in the tropics, especially in the New World, with a few species reaching temperate regions (Rouhan et al., 2004). Although Elaphoglossum is primarily a montane and cloud forest genus, with 65 species reported in paramo, it belongs to the most diverse genera of this ecosystem (Luteyn, 1999). Molecular phylogenetic analyses based on various chloroplast markers strongly support monophyly of Elaphoglossum, but its relationships to other fern genera remain unclear (Rouhan et al., 2004; Skog et al., 2004). Paramo species occur scattered in four and five well-supported clades, and mostly in distal positions within these clades. This suggests repeated colonizations into paramo. Rouhan et al. (2004) found evidence for a repeated long-distance dispersal from the Neotropics to the Indian Ocean area. Although evidence for dispersal towards South America was not found it cannot be ruled out provided that only a subset of species was analyzed.
Elaphoglossum was considered a wide tropical element in chorological analyses, but molecular data identified more precisely the origin of its species that occur in paramo. Elaphoglossum seems to have colonized paramo repeatedly from the neotropical montane forest. Relationships to other tropical regions might be revealed upon further taxon sampling. In such a case Elaphoglossum would represent a true wide tropical element in paramo.
Temperate Elements in the Paramo Flora
Temperate zones of the northern and southern hemispheres are important source areas for the paramo flora (Cleef, 1979; Smith & Cleef, 1988). Some genera that were restricted to the Austral-Antarctic regions migrated from the south temperate zones along the Andes as they rose from the lowlands, whereas several important herbaceous genera of the Holarctic region, such as Cerastium, Hypochaeris, Draba, and Lupinus arrived to paramo along the northern migration route after formation of the Isthmus of Panama. In many cases, a massive speciation followed their arrival into the neotropical region which made the (northern) Andes a secondary center of diversity for these genera. Finally the paramo was populated by species belonging to genera that were widely distributed in temperate regions of both hemispheres. As many as 151 paramo genera are classified as temperate elements (Table 2).
Continuous mountain chains connecting the south temperate and northern tropical Andes provided a suitable migration route for plants since the Andean uplift (Simpson, 1983). Both forest and non-forest genera have migrated into paramo from the southern Andes (Smith & Cleef, 1988). Similarity between the aseasonal, humid paramo climate and the mild oceanic climate of the south temperate zone has allowed establishment of these southern elements in the equatorial Andes (Cleef, 1978; Simpson & Todzia, 1990). In the chorological classification 34 genera were classified in this element.
Azorella (Apiaceae) is a conspicuous genus of 26 cushion- or mat-forming species distributed from Tierra del Fuego and sub-Antarctic islands to paramos of the northern Andes and Costa Rica (Martinez, 1993). Employing three chloroplast markers, Andersson et al. (2006) showed that the genus is not monophyletic and within the Azorella clade are nested other genera, such as Shizeilema (New Zealand and Australia with one species in Chile and the Falkland Islands), Stilbocarpa (sub-Antarctic islands of New Zealand), and the Argentinean-Chilean genera Huanaca and Laretia. In paramo there are nine species of Azorella (Luteyn, 1999), which form two moderately supported subclades. Sister taxon to them, although weakly supported, is A. lycopodioides from Argentina and Chile, suggesting that Azorella immigrated to the equatorial Andes from temperate South America, possibly in two independent events.
Calceolaria (Calceolariaceae) with more then 250 species is distributed along the Andes from Chile and Argentina to Central America and Mexico with disjunct outliers in Brazil and the Falkland Islands (Molau, 1988; Ehrhart, 2000; Andersson, 2006). Molecular phylogenetic studies, using nuclear and plastid DNA markers, along with studies of floral morphology, confirm that Jovellana, distributed in Chile and New Zealand, is sister to Calceolaria (Andersson, 2006; Mayer & Weber, 2006). In paramo there are 65 species of Calceolaria, occurring mostly in shrubby subparamo but with specialized representatives reaching high-altitude super-paramo (Molau, 1988; Luteyn, 1999). Although molecular analyses do not provide a strong support, species from temperate South America appear in the basal position of the phylogenetic tree (Andersson, 2006; Cosacov et al., 2009). This suggests a south temperate distribution as the ancestral situation and a later migration towards the northern Andes, which is in agreement with the previous chorological classification. Molecular data support Molau's (1988) hypothesis of a barrier effect imposed by the Amotape-Huancabamba zone for the migration of Calceolaria between paramos of northern Peru and southern Ecuador and imply independent dispersal events towards the northern Andes.
Gunnera (Haloragaceae) is an old genus of 40 recent species with a disjunct Gondwana distribution in Africa, Australasia, New Zealand, and South America, but also reaching Central America, Mexico, and the Hawaiian Islands. Late Cretaceous and Early Tertiary fossil records are known from North America, India, and Antarctica (Wanntorp & Wanntorp, 2003). Eleven species are reported from paramo (Luteyn 1999); nevertheless, most species enter paramo only marginally and the only true paramo species is G. magellanica, an Andean species widespread from Patagonia to Colombia. Phylogenetic analyses, combining morphological and molecular (nuclear and plastid DNA markers) data, indicate that New Zealand-Australasian taxa are sister to the South American subgenera Misandra and Panke, from which paramo species are derived. Subgenus Misandra, which includes G. magellanica, occurs in the basal position and is sister to the remainder of American and Hawaiian species of subgen. Panke (Wanntorp & Wanntorp, 2003). Since the second species of subgen. Misandra, G. lobata, is confined to southern Patagonia, it may be assumed that G. magellanica migrated to paramo from the south temperate Andes. The history of subgen. Panke, with the remainder of the paramo species, may have involved a late Cretaceous colonization of North America, a tertiary dispersal to Hawaii, and later southward recolonization of South America along the Andes during which several species entered paramo (Wanntorp & Wanntorp, 2003).
Nertera (Rubiaceae) is a small genus of six herbaceous species distributed in New Zealand, Tristan da Cunha, South and Central America, and the Antilles (Andersson, 1993, 2000). A polymorphic species, N. granadensis, widespread from Chile and Argentina to Mexico, is reported from paramo (Andersson, 1993; Luteyn, 1999). Molecular phylogenetic analyses using nuclear and plastid markers show that Nertera is monophyletic within a moderately supported subclade and is sister to a well-supported subclade comprising Coprosma (New Zealand, Australia, Fiji, and Hawaii) and Normandia (New Caledonia) (Anderson et al., 2001). The two subclades together form a strongly supported clade with the Australian Durringtonia paludosa as their sister taxon (Fig. 5). A biogeographic reconstruction suggests an Australasian origin of Nertera and a subsequent migration to other regions of the southern hemisphere including South America via a long-distance dispersal (Anderson et al., 2001). It may be assumed that the dispersal abilities successful in the transoceanic migration to South America also allowed dispersal of N. granadensis in the New World. However, phylogeographic relationships of the Andean plants remain to be studied to clarify the history of paramo populations.
[FIGURE 5 OMITTED]
Oreobolus (Cyperaceae) is a genus of about 15 species of trans-Pacific distribution in Malaysia, Australia, New Zealand, Tahiti, the Hawaiian Islands, the Andes, and Central America (Seberg, 1988; Morris, 2001; Chacon et al., 2006). They are cushion forming plants in boggy habitats from low to alpine elevations; five species occur in paramo (Luteyn, 1999). Nuclear and chloroplast DNA markers indicate that South American Oreobolus species form a monophyletic group that is sister to O. pumilio from Australia and New Zealand (Chacon et al., 2006). It has been estimated that the genus arrived in South America from Australasia 5.5-6 Mya by means of long-distance dispersal. The establishment of the genus in the temperate southern part of the continent was followed by migration towards the developing northern Andes and to Costa Rica, which was accompanied with a moderate species diversification (Fig. 6).
Oreomyrrhis (Apiaceae), a genus of ca. 25 herbaceous species of which O. andicola is found in paramo, provides another example of a disjunct trans-Pacific distribution (Mathias & Constance, 1955; Luteyn, 1999). Since mericarps of Oreomyrrhis do not posses any apparent adaptations to dispersal (Mathias & Constance, 1955; Chung et al., 2005), long-distance trans-oceanic dispersal was doubted in favor of ancient land migration and vicariance events (Mathias & Constance, 1955; van Steenis, 1962). Nevertheless, phylogeny of Oreomyrrhis, based on nuclear DNA markers, suggests a late Tertiary to Quatemary origin and diversification of the genus, rejecting the vicariance scenarios (Chung et al., 2005) in favour of a long-distance dispersal between South America and Australasia/New Zealand. Oreomyrrhis appears nested within Eurasian-North American Chaerophyllum sect. Chaerophyllum, with North American species most closely related. However, relationship within Oreomyrrhis remains unresolved. Several equally parsimonious scenaria may explain the trans-Pacific distribution of Oreomyrrhis, which prevents biogeographic reconstruction and leaves the origin of O. andicola in paramo unclear (Chung et al., 2005).
[FIGURE 6 OMITTED]
Ourisia (Plantaginaceae) includes 28 herbaceous and sub-woody species at high-elevations in New Zealand, Tasmania, and the Andes (Meudt & Simpson, 2006). Two herbaceous species occur in paramo, where they usually grow in humid habitats (Luteyn, 1999). Molecular phylogeny based on nuclear and chloroplast DNA markers, suggests a temperate South America origin with the suffruticose species appearing in the basal position (Meudt & Simpson, 2006). A subsequent dispersal to Tasmania and New Zealand is implied although the relationship of Australasian species with the clade of South American herbaceous species is not clarified by the analyses. Paramo species are nested in a distal position within the herbaceous South American clade (Fig. 7). This suggests that the occurrence of Ourisia in paramo resulted from immigration from the southern Andes, possibly during the Plio-Pleistocene (Meudt & Simpson, 2006).
Except for Gunnera and Oreomyrrhis, molecular phylogenies support the earlier chorology based ideas about origins of southern genera in paramo. A pattern of south to north speciation, such as that documented for the Andean lizard Proctoporus (Doan, 2003), is found in Oreobolus and Ourisia. This pattern of species evolution may be consistent with the south to north progression of Andean uplift, although calibration of speciation events is only available for the former. Long-distance, trans-Pacific dispersal is implied for Nertera, Oreobolus, and Ourisia. This suggests that availability of suitable habitats may be more important than distance in determining distribution patterns of high-Andean plants (Simpson & Todzia, 1990; Sklenar & Balslev, 2005, 2007). Arrival in the equatorial Andes from both south and north is found in Gunnera, because at least two lineages of that genus are present in paramo. Although Oreomyrrhis has a disjunct trans-Pacific distribution similar to Oreobolus and Ourisia, the manner in which it migrated to paramo remains unclear.
This element includes 41 genera with a north temperate and Mediterranean distribution, although sometimes a few species are found in temperate regions elsewhere. Their presence in the paramo ecosystem implies north to south long-distance dispersals via land bridges along Central America and the Isthmus of Panama.
[FIGURE 7 OMITTED]
Astragalus (Fabaceae), with about 2,500 species widely distributed mostly in Mediterranean habitats, has over 100 species in South America inhabiting usually semiarid environments in the south. Three species are reported in paramo (Luteyn, 1999), one of which, A. garbancillo, was included in a molecular study using nuclear rDNA ITS and two chloroplast spacers (Scherson et al., 2008). The South American Astragalus species form two recently evolving clades that are nested within the North American species, suggesting two immigrations from North America (Scherson et al., 2008). The single paramo species of Astragalus is found in a clade with an estimated age of 1.89[+ or -]0.18 Mya. The geographical pattern of species richness with the majority of species found in the central and southern part of the continent, and the ecological preference for arid habitats, which is a habitat type with quite a limited extension in the equatorial Andes, suggest that paramo actually might have been colonized from the south by Astragalus, in the same way as happened with Hypochaeris (see below). More detailed sampling is needed to test this hypothesis, however.
Cerastium (Caryophyllaceae) has some 120 species distributed mostly in temperate regions of the northern hemisphere, but reaching into temperate South America via high elevations of the equatorial and subequatorial Andes (Baumann, 1988). In paramo there are about 16 Cerastium species (Luteyn, 1999; Sklenar, unpublished data), but species richness of the genus in South America peaks in the central Andes of Peru and Bolivia. Taxonomy of paramo species is not completely understood and phylogeny of the South American species has yet to be studied. However, a phylogenetic study using three non-coding plastid DNA regions that sampled a few South American (and paramo) species suggested that they are derived from temperate North American species (Sheen et al., 2004) with the age of the colonization of the South American continent via the Isthmus of Panama estimated at 2.22-1.31 Mya. A north to south American biogeographic relationship is suggested also for Silene (Caryophyllaceae), although the evidence is less clear than the one found in Cerastium (Popp & Oxelman, 2007).
Draba (Brassicaceae) is a genus of ca. 350 herbaceous and suffrutescent species with a mostly northern hemisphere distribution, but also reaching the Andes and southern hemisphere (Jordon-Thaden & Koch, 2008). About 80 species are found in Central and South America, 46 of which have been recorded in paramo (Al-Shehbaz, 1987; Luteyn, 1999 ; Al-Shehbaz & Sklenar 2010). Molecular phylogenetic analyses employing both nuclear and chloroplast DNA of the American representative of the genus indicate that Central and South American Draba probably evolved from northern hemisphere groups and that the genus arrived in South America repeatedly after multiple hybridization in North and Central America (Koch & Al-Shehbaz, 2002; M. Koch, pers. comm.). Molecular data also suggest extensive cross relationships among taxa from various geographical regions within the genus' distribution range, which complicates a biogeographical interpretation. Most paramo Draba are found in a large clade together with species from central-southern South America and North America, while a few Colombian species are found in a separate small clade (Koch & Al-Shehbaz, 2002). Whereas the evolutionary relationships among species are apparently very complex, it seems unequivocal that the origin of the genus in the Andes is due to immigration from the north.
Hypochaeris (Asteraceae) is a genus of about 60 species in the Mediterranean region, Europe, Asia, and South America (Tremetsberger et al., 2006). Nuclear ribosomal DNA and karyological data show that a South American monophyletic clade most likely resulted from a morphological and ecological diversification of a common ancestor which arrived on the continent via a long-distance dispersal from NW Africa no more than 3.5 Mya (Samuel et al., 2003; Tremetsberger et al., 2005, 2006). Of the 45 South American Hypochaeris species, 11 occur in paramo (Luteyn, 1999). Although phylogenetic relationships are not reliably resolved, AFLP data suggests that two groups of species from the southern part of the continent appear in the basal position of the South American clade (Fig. 8) (Tremetsberger et al., 2006). This suggests that the occurrence of the genus in paramo can be explained by immigration from temperate South America, although the number of migration events remains to be determined.
[FIGURE 8 OMITTED]
Lathyrus (Fabaceae) comprises ca. 160 species distributed in all continents except Australia. Twenty-four species belonging to sect. Notolathyrus are found in South America, mostly in the south temperate zone, but two species, including L. magellanicus widespread between Colombia and Chile, reach equatorial paramo (Luteyn, 1999). Molecular phylogeny based on chloroplast DNA suggests that the essentially Holarctic sect. Orobus is basal to the South American Notolathyrus (Asmussen & Liston, 1998). This phylogenetic pattern indicates that Lathyrus arrived in South America from the north, although a date for this event is not available. Since only four of the South American species were analyzed (Asmussen & Liston, 1998), relationships within Notolathyrus remain unknown. Similar to Astragalus, upon more intensive sampling it may eventually be found that Lathyrus arrived in paramo from the south.
Lupinus (Fabaceae) is a genus of 275 species distributed in both the Old and New Worlds, but with highest species richness in western North America and the Andes (Hughes & Eastwood, 2006). A phylogenetic analysis employing nuclear ITS and CYCLOIDEA gene sequences showed that Lupinus arrived in South America from North America at least twice (Fig. 9). One of the colonization events gave rise to a large monophyletic group of species of varied life forms and ecology which rapidly radiated in the Andes probably within the last ca. 1.5 My (Hughes & Eastwood, 2006). Although the real species richness is likely lower (Luteyn, 1999), the 56 species reported from paramo all belong to this Andean clade, which is sister group to Mexican species (Hughes & Eastwood, 2006).
[FIGURE 9 OMITTED]
Molecular phylogenies of genera from the holarctic element treated above are fully consistent with the previous chorological classification and confirm the north temperate migration route. North America is usually determined as the source area, although dispersal from other cool regions of the northern hemisphere is also possible, such as the one documented for Hypochaeris. Another distinct pattern is revealed by Hypochaeris--although the north temperate zone is confirmed as the source area for the South American Hypochaeris, the genus arrived in paramo from the south. This example points to the temporal scale dependence of biogeographic events. Such pattern may be found in other genera from the holarctic element, e.g., in Astragalus and Lathyrus, once more representative taxon sampling has been done.
An astonishing feature among some north-temperate immigrants is the variety of paramo growth forms. Whereas certain groups, such as Cerastium and Silene, retained their herbaceous growth form upon arrival in paramo, massive speciation of Draba and Lupinus, along with Gentianella and Valeriana (see below), was accompanied by an impressive radiation of growth forms which also involved evolution of a (sub)woody habit.
Wide Temperate Element
This element includes 76 paramo genera that primarily occur in temperate and cool regions of both hemispheres.
Caltha (Ranunculaceae) is a small genus of terrestrial herbs of marshy and wet habitats. They are distributed in temperate zones of the northern hemisphere, disjunctly in the central and equatorial Andes, and in southern South America, New Zealand, and Australia (Hoffmann, 1999). The only paramo species, C. sagittata (Luteyn, 1999), has a fragmented distribution in Patagonia, at Lake Titicaca, and in the high Andes of Ecuador. The phylogenetic analysis based on nuclear and plastid DNA suggests a north temperate origin of the genus in North America from where Caltha migrated to South America possibly as early as late Cretaceous or early Paleocene (Fig. 10) (Schuettpelz & Hoot, 2004). This suggested scenario raises a question regarding the origin of paramo populations of C. sagittata. Paramo and Titicaca populations could be relicts from migration of the genus to temperate South America. However, since C. sagittata is confined to open, cold and wet habitats, it seems unlikely that it could have survived in the equatorial zone during the late Cretaceous-early Paleocene period. More probably, the species arrived in equatorial paramo from the south along the Andes after suitable alpine habitats were formed in Plio-Pleistocene. To confirm either of the two scenaria, paramo populations must be analyzed.
Gentianella s.s. (Gentianaceae) is a genus of 250 herbaceous species distributed mostly in alpine habitats of the north temperate zone, but reaching into Central and South America, northwest Africa, Australia, and New Zealand (von Hagen & Kadereit, 2001). There are 48 species in paramo and some are narrowly distributed endemics (Pringle, 1995; Luteyn, 1999). Molecular phylogenetic analyses, employing nuclear and chloroplast markers, indicate that Gentianella s.s. is monophyletic. Two morphologically distinct species groups, i.e., species with fimbriate or efimbriate petals, form moderately supported clades (von Hagen & Kadereit, 2001). The South American and thus paramo species of Gentianella all belong to the efimbriate group within which further relationships remained unresolved. Nevertheless, molecular and morphological features suggest that efimbriate Gentianella s.s. originated in Asia and then dispersed to other north temperate regions (von Hagen & Kadereit, 2001; Kadereit & von Hagen, 2003). Colonization of South America likely occurred via North America, supposedly after formation of treeless high-Andean habitats, but the number of colonization events remains to be determined. Speciation of Gentianella s.s. in South America may be linked to its flower diversification (Kadereit & von Hagen, 2003).
[FIGURE 10 OMITTED]
Plantago (Plantaginaceae) is a virtually cosmopolitan genus with 200 species of which 11 are found in paramo (Luteyn, 1999). Neither morphological (Rahn, 1996) nor molecular (Ronsted et al., 2002) phylogenetic studies have elucidated the geographic origin of the paramo species. Of the two paramo species sampled by Ronsted et al. (2002), P. sericea occurs in a basal position of a clade containing North and South American species with Mediterranean region sister species. The other species, the cushion forming P. rigida, occurs in an unresolved group with one clade of mostly South American species, and another clade with species from Asia and Europe, and the cosmopolitan P. major. Sister to this group are species mostly from Australia and New Zealand. It seems that paramo representatives of Plantago are derived from at least two sources of different (temperate) geographic affinity, but this must be confirmed by additional sampling.
Valeriana (Valerianaceae) with 250 species is distributed in Eurasia, North America and South America, where the genus underwent remarkable morphological and ecological diversification (Baumann, 1988; Eriksen, 1989). Fifty-five species are reported from paramo (Luteyn, 1999). Phylogenetic analyses based on chloroplast and nuclear DNA markers and sampling of one-third of the paramo species, suggest an Asian origin of the genus (and family) and subsequent migration via Europe to North America (Bell, 2004; Bell & Donoghue, 2005). From North America there may have been two colonization events of the South American continent. Paramo species of Valeriana along with non-paramo ones are found in a weakly supported clade (Fig. 11). Whether the high paramo species richness resulted from a single colonization event of this habitat or from repeated colonizations must be clarified by further sampling (Bell & Donoghue, 2005).
The wide temperate category that harbors genera that occur in both temperate zones is apparently meaningful only in the chorological approach. Once a sufficiently resolved molecular phylogeny is available, the source area, either south or north temperate zone, for paramo species is determined. This is the case for Gentianella and Valeriana, for which molecular data suggest the northern migration route. So phylogenetically the wide temperate category should be redundant. Nevertheless, there is some indication that Plantago arrived in paramo from temperate regions of both hemispheres, which in fact conforms with the chorological pattern. It remains to be clarified whether Caltha arrived in the equatorial Andes from north or south.
This element includes 41 genera (Table 2) that have a worldwide, or nearly so, distribution.
Huperzia (Lycopodiaceae) comprises 300 terrestrial and epiphytic species distributed throughout the world (Ollgaard, 1992) of which some 60 species occur in paramo (Luteyn, 1999). Phylogenetic studies based on chloroplast DNA result in a strongly supported tree showing that terrestrial species of Huperzia from the north temperate zone are basal to two large neotropical and paleotropical clades comprising primarily epiphytic species (Wikstrom et al., 1999, Wikstrom & Kenrick 2000). In the neotropical clade, the great majority of paramo species forms a large monophyletic group of terrestrial species that is nested within species of montane forest epiphytes, and a single terrestrial paramo species is found within another group of epiphytes (Fig. 12). This suggests that paramo Huperzia are derived from epiphytic ancestors and that at least two events of reversal to the terrestrial habit occurred in the high Andes. Diversification within paramo Huperzia occurred about 15 Mya and would thus be contemporary to Andean orogeny and formation of open, treeless habitats (Wikstrom et al., 1999). Compared with previous views of Huperzia as a cosmopolitan element in the paramo flora, molecular phylogenies clearly show that paramo Huperzia, which are all terrestrial, originated from at least two events from epiphytic neotropical montane species.
[FIGURE 11 OMITTED]
Similar to wide temperate, the cosmopolitan element is a chorological category. Based on molecular phylogenies, Huperzia is now believed to have established in the neotropical region well before major uplift of the northern Andes. After the paramo habitat was formed, it was colonized already by the neotropical lineages, probably repeatedly. Accordingly, it should be considered neotropical element in the paramo flora.
[FIGURE 12 OMITTED]
Species Richness of Paramo Elements
The 34 genera (the paraphyletic groups of Siphocampylus-Centropogon, Chusquea-Neurolepis, Jamesonia-Eriosorus, and Munnozia-Chrysactinium treated together) with supported tropical, northern, and southern origin in paramo together comprise 827 paramo species--the genera having about 6400 species worldwide. This represents about 7% of total generic and 23% of total species paramo diversity, respectively. Genera from tropical and temperate elements contribute, on average, 26 and 23 species, respectively, to paramo diversity (Table 3). The two elements do not differ in their generic species richness (Kruskal-Wallis ANOVA by ranks, H=0.43, p=0.51, df=l). However, a considerable variation among elements is revealed when the temperate category is split into northern and southern elements (Fig. 13). Genera from the northern element have, on average, ca. 31 species in paramo, whereas genera from the southern element have ca. 13 species (Table 3). Test for difference among tropical, northern, and southern elements remains insignificant (Kruskal-Wallis ANOVA by ranks, H= 4.17, p=0.12, df=2), but this is only due to outlying values of Espeletia s.1. and Calceolaria in tropical and southern elements, respectively (values marked with dots in Fig. 13).
Only a limited sample of plant groups that inhabit neotropical paramo have been subjected to phylogenetic studies. Often the studied plant groups are conspicuous by their disjunct geographical ranges, such as the amphi-Pacific Oreobolus and Ourisia, or they are remarkably diverse with numerous endemic species, such as the Espeletia complex and Valeriana. Phylogeny of many species-rich Andean genera, such as Baccharis, Diplostephium, Pentacalia and Senecio (Asteraceae), Puya (Bromeliaceae), and Geranium (Geraniaceae), remains to be studied. Asteraceae, the most diverse family in the high Andes (Funk et al., 1995; Luteyn, 1999), is under-represented in the phylogenetic studies covering paramo. Scarce knowledge is available about paramo grasses and ferns, and woody plant groups are often overlooked in favor of herbaceous ones. Despite these apparent limitations of our sample, some major biogeographical trends seem to be emerging.
[FIGURE 13 OMITTED]
Molecular phylogenies that include species from the paramo ecosystem mostly support findings of the previous chorological approach, although conflicts are also encountered (e.g., Halenia, Perezia). Consistent with other tropical alpine regions, temperate zones are confirmed as important source areas for the evolution of the paramo flora (van der Hammen & Cleef, 1986; Smith & Cleef, 1988; Katinas et al., 1999; Gehrke & Linder, 2009). Nearly half of the paramo species are derived through immigrations from temperate zones. Gentianella, Draba, Valeriana, Cerastium, Lupinus, etc. immigrated to South America from the north. Their arrival in the northern Andes was followed by adaptive radiation resulting in a remarkable diversity of species and often growth forms. Molecular phylogenies also confirm immigration from the south temperate Andes, even if the south temperate element represented by, e.g., Ourisia, Oreobolus, Calceolaria, and Azorella, contributed much less to species diversity of paramo than the north temperate element.
The southern Andes probably host the oldest alpine flora of South America and this region could have acted as the initial source of immigrants to the equatorial Andes (Simpson, 1983; van der Hammen & Cleef, 1986). In spite of that, we find equal or smaller proportion of the south temperate element in paramo (in contrast to the north temperate element), both at the generic (e.g., Cleef, 1979; Sklenar & Balslev, 2007) and species level (this study). Since the north temperate zone is a much larger and richer source of potential immigrants than the southern one, there may be higher propagule pressure from the north than from the south. Hence, we find a slightly higher proportion of genera of north temperate origin in paramo. The numbers clearly show that north temperate genera have, on the average, more species in paramo than south temperate genera. Among the south temperate genera, only Calceolaria matches the species richness of north temperate genera, such as Gentianella, Halenia, Valeriana, and Lupinus. In contrast to, e.g., the relatively species-poor Oreobolus and Azorella, both with small, inconspicuous flowers, Calceolaria has conspicuous bilabiate flowers and diversified pollination biology (Molau, 1988; Cosacov et al., 2009). Interaction with pollinators may have been an important factor in speciation of Calceolaria, similar to some north temperate genera (Kadereit & von Hagen, 2003; Cosacov et al., 2009).
Donoghue (2008) suggested that migration from temperate zones into newly formed paramo habitats was more important than evolution of new adaptations among tropical plants. It seems, however, that the contribution of tropical genera to paramo species richness has been no lower than contribution of temperate genera (averaging the northern and southern genera). Knowledge of paramo plant ecology is mostly limited to several conspicuous groups, such as giant rosettes (Espeletia) and tree-line trees (Polylepis), and otherwise remains insufficiently known (Rundel et al., 1994). Evolutionary-based studies of high-Andean plant ecology are needed to test to what degree evolution of new adaptations among tropical plants allowed them to colonize the paramo habitats. For instance, Sklenar et al. (unpublished data) found evolutionary based differences in the resistance of the paramo plants to freezing temperatures.
The two main sources of the paramo flora, i.e., neotropical and temperate genetic stocks with the latter divided into northern and southern temperate stock, are evident. Other patterns, however, are less clearly marked as the complex history of the Andean flora and novel insights into its evolution are revealed. Phylogenetic data document paraphyly and repeated arrivals in several paramo taxa. Multiple lineages of some neotropical groups, such as Chusquea-Neurolepis, Lasiocephalus, Huperzia, and Elaphoglossum, independently colonized paramo from montane forests. However, repeated arrivals are also found in temperate groups, such as Halenia migrating to paramo from the north, and Gunnera and likely also Plantago arriving in the northern Andes from the north as well as from the south. Numbers of colonization events apparently vary within paramo elements which makes further conclusions difficult.
Moreover, biogeographic events are spatially and temporally scale-dependent, and similar general patterns may represent different individual histories (Ito et al., 2000; Comes & Kadereit, 2003). A distinction must be made between arrivals in the Andes before and after suitable alpine habitats were available. Arrivals before formation of the paramo habitats in the Plio-Pleistocene imply that immigrants established in tropical (lowland or montane) conditions and only later colonized paramo after it had been formed. Such taxa as Huperzia have been considered neotropical element even though its basal lineages may occur outside the tropics (Wikstrom et al., 1999). Post Plio-Pleistocene arrivals should then be classified by the original source area. For instance, although Hypochaeris colonized paramo from the southern and central Andes, the genus can hardly be considered as south temperate since it arrived in South America from the northern hemisphere only during Plio-Pleistocene (Tremetsberger et al., 2005). In contrast to Hypochaeris, Caltha has a similar general migration pattern between the northern and southern hemispheres, but the colonization of South America occurred much earlier, i.e., in late Cretaceous or early Paleocene (Schuettpelz & Hoot, 2004). If migration of Caltha sagittata from the southern parts of the continent to the northern Andes is confirmed, Caltha should be considered south temperate element in the paramo flora. Time estimates of taxon arrival in the paramo are available for some genera (e.g., Oreobolus, Halenia), but additional data is needed before a realistic and more detailed picture can be made for the evolutionary history of the paramo flora.
Plio-Pleistocene climatic fluctuations and polyploidization are believed important mechanisms for species evolution in mountain floras (Winkworth et al., 2005; Abbott, 2008). Although radiation of the rich paramo plant genera is also often linked to the Pleistocene climatic oscillations (e.g., Cuatrecasas, 1986; Wikstrom et al., 1999), exact tests of this scenario are lacking. Polyploidy was found in about half the Afroalpine and two-thirds of the Mt. Wilhelm (New Guinea) species (Borgmann, 1962; Hedberg, 1986; Smith, 1986). Higher ploidy levels have been found in paramo populations of Draba, Lasiocephalus, Valeriana, and Oritrophium (Jordon-Thaden & Koch, 2008; Dugkova et al., 2010 and unpublished data). Nevertheless, the proportion of polyploids in the paramo flora and the role of polyploidization and genome size-change in the evolution of paramo plant diversity remain to be studied. The evolutionary picture of the flora may be further complicated by hybridization and reticulate evolution, as has been found in the Afroalpine flora and paramo Draba and Lasiocephalus (Hedberg, 1986; Koch & Al-Shehbaz, 2002; Duskova et al., unpublished data).
Conclusions and Directions for Future Work
Parallel to tropical alpine Africa and New Guinea (Albach et al., 2005b; Wagstaff et al., 2006; Gehrke & Linder, 2009), the reviewed molecular phylogenies confirm the composite character of the neotropical paramo flora. Furthermore, molecular studies generally confirm the pattern suggested by the chorological approach. The paramo flora is derived flora neotropical and temperate stocks, and the two sources may have had similar impacts on modern paramo species diversity. Immigration occurred flora temperate regions of both hemispheres, but northern hemisphere genera gave rise to a significantly higher proportion of species found in paramo than genera flora the southern hemisphere.
Biogeographical generalization that would go beyond tropical and temperate origins is difficult, as paramo taxa have particular evolutionary and migration histories. In the same way as in east-African mountains (Gehrke & Linder, 2009), there is evidence of repeated arrivals of genera into paramo. But unlike the African mountains, a few genera likely arrived in paramo from both the northern and the southern hemispheres.
No direct dispersal has yet been found between paramo and other tropical alpine regions (Gehrke & Linder, 2009). Genera that are shared with tropical alpine New Guinea (Oreobolus, likely also Oreomyrrhis) arrived in paramo via migration along the cordilleras. So far, no evidence has been provided for generic migration flora tropical paramo to the temperate zone. Such pattern has been rejected for Halenia, and remains to be verified for Hinterhubera and Laestadia.
Several pertinent questions remain open as regards the evolutionary history and species diversity of the paramo flora.
* Were tropical lineages handicapped in the process of colonization of the paramo environment with the year-round risk of subzero temperatures and physiological dryness against the presumably preadapted temperate lineages arriving flora the highly seasonal climate?
* Some genera, such as Gentianella, Valeriana and Lupinus, underwent rapid diversification after their arrival in paramo (Andes), whereas other groups, such as Silene, originating in the same ancestral area, did not. A contrasting pattern in this regard is seen between north and south temperate genera. Were the drivers for species diversification biological, such as interaction with pollinators, or historical, such as different arrival time in paramo?
* What factor(s) triggered evolution of the spectrum of growth forms within species-rich genera? In genera comprising both woody and herbaceous forms, is the woody habit ancestral and the herbaceous habit derived or vice versa?
* How much did hybridization and polyploidization contribute to evolution of paramo species richness relative to allopatric speciation implied by Plio-Pleistocene contraction-expansion pulses of plant populations?
* The age difference between montane forest and paramo habitats implies a forest-to-paramo direction of evolution in tropical elements. Dial an opposite direction of speciation occur in the equatorial Andes, i.e., that paramo taxa (of either geographic origin) colonized montane forest?
Additional phylogenetic studies combined with eco(physio)logical research are needed especially among autochthonous neotropical taxa to provide a more complete picture of the history and processes that lead to evolution of the paramo flora (Simpson, 1988; Bello et al., 2002). This kind of research, however, should be firmly supported by monographic works that would determine species limits and their geographic distribution.
Acknowledgments Work was supported by the Czech Science Foundation (project no. 206/07/0273), Grant Agency of the Academy of Sciences of the Czech Republic (project no. KJB601110710), and partly by Ministry of Education, Youth and Sports of the Czech Republic (project no. MSMT 0021620828). The University of Aarhus supported Petr Sklenar's research visit during which an early draft of the manuscript was prepared (Grant no. 220945-0057 to H. Balslev). Jim Luteyn and an anonymous reviewer are thanked for valuable comments on an earlier draft of the manuscript, Jim Luteyn also kindly revised the English.
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Petr Sklenar (1,3) * Eva Duskova (1) * Henrik Balslev (2)
(1) Department of Botany, Charles University, Benatska 2, 128 01 Prague, Czech Republic
(2) Department of Biology, University of Aarhus, Build. 1540, Ny Munkegade, 8000 Aarhus C., Denmark
(3) Author for Correspondence; e-mail: firstname.lastname@example.org
Published online: 17 November 2011
[c] The New York Botanical Garden 2010
Table 1 Vascular plant diversity in tropical alpine floras of Central and South America (paramo), Africa (Afroalpine), and New Guinea with estimated ages in Mya of respective alpine habitats (Smith, 1986; van der Hammen & Cleef, 1986; Hedberg, 1992). Counts include true tropical alpine species and some montane forest species that are occasionally found above the tree-line. Introduced taxa are excluded. Data extracted from Hedberg (1957); van Royen (1980-83); Luteyn (1999); Sklenar et al. (2005), with an unpublished update for the Afroalpine flora (Hedberg & Hedberg, unpublished) Paramo Afroalpine New Guinea Families 127 44 84 Genera 509 139 226 Species 3,564 371 1,118 Estimated age 3-5 Mya 0.1-23 Mya ~1.8 Mya Table 2 Generic composition of the paramo and their classification in the geographic flora elements as suggested by Cleef (1979); van der Hammen and Cleef (1986); Cleef and Chaverri (1992); Ulloa and Jorgensen (1993); Islebe and Kappelle (1994); Luteyn (1999), and Sklenar and Balslev (2007), with modifications when sources were not congruent. Genera in bold are treated in this text Element Definition Genus Tropical Paramo Confined Aragoa, Ascidiogyne, endemic (almost) Blakiella, Bucquetia, exclusively Castratella, Cotopaxia, to paramo Espeletia, Floscaldasia, Hinterhubera, Laestadia, Myrrhidendron, Nephropteris, Neurolepis, Perissocoeleum, Phutarchia, Raouliopsis, Westoniella Neotropical Genera Aa, Acautimalva, Aciachne, that range Aegopogon, Aetanthus, from Aequatorium, Ageratina, lowlands Alloispermum, Alloplectus, to the Alonsoa, Altensteinia, alpine Antidaphne, Aphanactis, zone, Aphanelytrum, Arcytophyllum, distributed Aristeguietia, Aristida, also Arracacia, Arthrostylidium, outside Aulonemia, Axinaea, paramo Baccharis, Badilloa, Barbosella, Barnadesia, Bejaria, Bomarea, Bowlesia, Brachionidium, Brachyotum, Brayopsis, Brunellia, Cabreriella, Cacosmia, Caiophora, Campyloneurum, Cavendishia, Centropogon, Ceradenia, Ceratostema, Cestrum, Chaetolepis, Chaptalia, Chersodoma, Chevreulia, Chionolaena, Chromolaena, Chrysactinium, Chuquiraga, Chusquea, Clinanthus, Clusia, Cochlidium, Colignonia, Cologania, Columellia, Columnea, Corynaea, Cranichis, Cremolobus, Critoniopsis, Cronquistiantus, Cuatrecasasiella, Cuphea, Cyathea, Cybianthus, Cyclopogon, Dalea, Dendrophthora, Deprea, Diplostephium, Dissanthelium, Disterigma, Distichia, Dorobaea, Drymaria, Eccremocarpus, Echeandia, Echeveria, Elleanthus, Epidendrum, Erato, Eriosorus, Eudema, Excremis, Facelis, Ferreyranthus, Flosmutisia, Freya, Freziera, Gaiadendron, Galinsoga, Gamochaeta, Gaylussacia, Geissanthus, Gomphichis, Greigia, Grosvenoria, Guevaria, Guzmania, Gynoxys, Halenia, Halimolobos, Heliopsis, Helogyne, Heppiella, Hesperomeles, Hierobotana, Holodiscus, Idiopappus, Isidrogalvia, Iltisia, Jaltomata, Jamesonia, Jalcophila, Jaramilloa, Jessea, Joseanthus, Jungia, Laccopetalum, Lachemilla, Laennecia, Lamourouxia, Lasiocephalus, Lellingeria, Lepanthes, Lepechinia, Liabum, Llerasia, Lophosoria, Loricaria, Lourteigia, Lucilia, Luciliocline, Lysipomia, Macleania, Macrocarpaea, Manettia, Margyricarpus, Masdevallia, Maxillaria, Meriania, Miconia, Micropleura, Minthostachys, Mniodes, Monactis, Monnina, Monochaetum, Moritzia, Munnozia, Mutisia, Myrcianthes, Myrosmodes, Nasa, Nassella, Neonelsonia, Nierembergia, Niphidium, Niphogeton, Noticastrum, Nototriche, Novenia, Obtegorneria, Odontoglossum, Oligactis, Oncidium, Onoseris, Ophryosporus, Opuntia, Oreopanax, Oreithales, Oveobolopsis, Oritrophimn, Ortachne, Ottoa, Oxylobus, Pachyphyllum, Pappobolus, Paragynoxys, Paranephelius, Pecluma, Pentacalia, Perezia, Phalacrea, Philibertia, Philoglossa, Phylloscirpus, Piptochaetium, Pitcairnia Plagiocheilus, Platystele, Pleopeltis, Pleurothallis, Poidium, Polylepis, Psammisia, Pterichis, Puya, Racinaea, Radiovittaria, Rhynchotheca, Romanschulzia, Roupala, Sabazia, Salpichroa, Salpistele, Saracha, Scrobicaria, Selloa, Semiramisia, Siphocampylus, Smallanthus, Stelis, Stenomesson, Stenorrhynchos, Stevia, Stuckertiella, Tagetes, Talamancalia, Telipogon, Terpsichore, Themistoclesia, Thibaudia, Tibouchina, Ticoglossum, Tillandsia, Tournonia, Trichocline, Trichosalpinx, Tridax, Triniochloa, Tropaeolum, Vallea, Verbesina, Viguiera, Villadia, Villanova, Vittaria, Weberbauera Werneria, Xenophyllum Wide Widely Achyrocline, Begonia, tropical distributed Bothriochloa, Buddleja, in Bulbostylis, Cheilanthes, tropical Clethra, Conyza, Cyperus, America, Diehondra, Dicksonia, occurring Dioscorea, Elaphoglossum, also in Enterosora, Eragrostis, the Eriocaulon, Grammitis, Palaeotropics Hedyosmum, Histiopteris, Hybanthus, Hymenophyllum, Hypolepis, Hypoxis, Ilex, Lippia, Maytenus, Melpomene, Micropolypodium, Mikania, Myrsine, Ocotea, Oldenlandia, Otholobium, Paepalanthus, Paspalum, Passiflora, Peperomia, Persea, Pilea, Piper, Phytolacca, Pityrogramma, Plagiogyria, Pseudognaphalium, Pteris, Schefflera, Schizachyrium, Sigesbeckia, Spermacoce, Sporobolus, Stenandrium, Stycherus, Symplocos, Syngonanthus, Ternstroemia, Tournefortia, Xyris, Zygophlebia Temperate Austral- South Acaena, Azorella, Antarctic temperate Calandrinia, Calceolaria, distribution Colobanthus, Cortaderia, Cotula, Desfontainia, Drimys, Dysopsis, Escallonia, Fuchsia, Gaultheria, Gunnera ([dagger]), Libertia, Lilaea, Lilaeopsis, Lomatia, Muehlenbeckia, Myriactis, Myrteola, Nertera, Oreobolus, Oreocallis, Oreomyrrhis, Orthrosanthus, Ourisia, Pernettya, Prumnopitys, Rostkovia, Tristerix, Ugni, Uncinia, Weinmannia Holarctic North Antennaria, Astragalus, temperate and Bartsia, Berberis, Castilleja, mediterranean Cerastium, Cinna, Cirsium, distribution Clinopodium, Coreopsis, Comarostaphylis, Draba, Erigeron, Erysimum, Garrya, Geum, Hackelia, Helianthemum, Hypochaeris, Lathyrus, Lithospermum, Lupinus, Muhlenbergia, Oenothera, Parietaria, Pedicularis, Phacelia, Potentilla, Ribes, Rhamnus, Salvia, Saxifraga, Sibthorpia, Silene, Stachys, Thalictrum, Trichophorum, Vaccinium, Verbena, Viburnum, Vicia Wide Temperate and Agrostis, Alopecurus, temperate cool regions Anemone, Aphanes, Arenaria, of both Brachypodium, Bromus, hemispheres Calamagrostis, Callitriche, Caltha, Cardamine, Cardionema, Carex, Crassula, Coriaria, Cynoglossum, Cystopteris, Danthonia, Daucus, Deschampsia, Descurainia, Dryopteris, Elatine, Elodea, Elymus, Ephedra, Epilobium, Festuca, Galium, Gentiana, Gentianella, Geranium, Glandularia, Glyceria, Gnaphalium, Gratiola, Hieracium, Hierochloe, Hordeum, Hypericum, Isoetes, Isolepis, Juncus, Lepidium, Limosella, Luzula, Lysimachia, Melica, Mimulus, Montia, Myosotis, Paronychia, Pilularia, Pingjuicula, Plagiobothrys, Plantago, Poa, Polypogon, Polystichum, Potamogeton, Puccinellia, Ranunculus, Rubus, Rumex, Senecio, Sedum, Sisyrinchium, Spergularia, Stellaria, Stipa, Thelypteris, Trisetum, Urtica, Valeriana, Veronica, Viola Cosmopolitan Worldwide, or Adianthum, Anagallis, nearly so, Asplenium, Athyrium, Azolla, distribution Bidens, Blechnum, Botrychium, Eleocharis, Chamaesyce, Culcita, Cuscuta, Cynanchum, Drosera, Equisetum, Eryngium, Euphorbia, Habenaria, Huperzia, Hydrocotyle, Lobelia, Lemna, Lycopodiella, Lycopodium, Malaxis, Morella, Myriophyllum, Nicotiana, Ophioglossum, Oxalis, Pellaea, Polypodium, Pteridium, Rhynchospora, Scirpus, Selaginella, Solanum, Stuckenia, Utricularia, Wahlenbergia, Woodsia Table 3 Species richness of paramo genera with tropical, north temperate, and south temperate origin, and their contribution to paramo species diversity; Siphocampylus and Centropogon, Chusquea and Neurolepis, Jamesonia and Eriosorus, and Munnozia and Chrysactinium are treated together due to paraphyly; Gunnera, Oreomyrrhis, Caltha, and Plantago are excluded due to unclear origin in paramo Element Tropical Number of Genera 18 Paramo Species Richness 464 Mean Species Richness 25.8 [+ or -] 29.6 ([+ or -] SD) Proportion per Genus (%) 3.1 [+ or -] 3.58 Element Temperate (north/south) Number of Genera 16 (9/7) Paramo Species Richness 363 (275/88) Mean Species Richness 22.7 [+ or -] 23.1 (30.6 ([+ or -] SD) [+ or -] 21.1/12.6 [+ or -] 21.5) Proportion per Genus (%) 2.7 [+ or -] 2.79 (3.7 [+ or -] 2.55/1.5 [+ or -] 2.6) Element Total Number of Genera 34 Paramo Species Richness 827 Mean Species Richness 24.3 [+ or -] 26.8 ([+ or -] SD) Proportion per Genus (%) 2.9 [+ or -] 3.24
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|Author:||Sklenar, Petr; Duskova, Eva; Balslev, Henrik|
|Publication:||The Botanical Review|
|Date:||Jun 1, 2011|
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