THE EPIPHYTIC BRYOPHYTE FLORA OF THE COLOMBIAN AMAZON Los briófitos epífitos de la región amazónica de Colombia

An inventory of 384 plots on 64 trees, in four localities across the Colombian Amazon region (Amazonas, Caquetá, Putumayo, Vaupés), yielded 160 species of epiphytic bryophytes (116 of liverworts, 44 of mosses), in 64 genera and 26 families. Sampling was carried out in four non-seasonally flooded forests (Terra Firme), where bryophytes where collected from the base to the outer canopy, of 16 trees per locality. The flora is characterized by dominance of liverworts, especially Lejeuneaceae. The families with the highest number of records were Lejeuneaceae (55%), Calymperaceae (10%), Lepidoziaceae (8%), Octoblepharaceae (6%) and Sematophyllaceae (5%). The most common genera in number of records were Cheilolejeunea (11%), Pycnolejeunea (8%), Archilejeunea (8%) Ceratolejeunea (8%) and Syrrhopodon (7%). Syrropodon and Lejeunea were the most species-rich genera, followed by Ceratolejeunea and Cheilolejeunea. In average, the localities had 102 species in sixteen phorophytes. In terms of species richness and composition there were no significant differences between the four localities.


INTRODUCTION
Bryophytes are important in terms of species richness and cover in many habitats, as well as for ecosystem functioning (Goffinet & Shaw, 2009).Bryophytes are the first colonizers of various different types of substrates, and in several landscapes produce a major part of the biomass.In addition, epiphytic bryophytes are an integral component of forest ecosystems and represent a significant part of the plant species diversity (Lesica et al., 1991).They have important ecosystem functions as they increase structural complexity, influence nutrient cycles and moisture retention, and provide habitats for plants and animals (Rhoades, 1995).
Tropical forests harbor a rich diversity of bryophytes, because of their complexity and variety of microhabitats (Gradstein, 1992).In the Colombian Amazon nearly of 221 species of bryophytes have been recorded, including 114 liverworts distributed in eleven families and 44 genera, and 107 mosses, distributed among 23 families and 49 genera (Churchill, in press; Gradstein & Uribe, in press).For the Amazon region an estimated 188 genera and 700 species of mosses and liverworts have been reported (Gradstein et al., 2001).In Colombia, inventories and floristic studies on bryophytes in Colombia have principally focused on the Andean area.There are very few studies on bryophyte diversity patterns in the Colombian Amazon, only one of these (Ruiz & Aguirre, 2004) sampled the trees, and studied the vertical distribution of bryophyte diversity on different types of phorophytes in several landscapes of Tarapacá (Amazonas).Other studies in the Colombian Amazon (Benavides et al., 2004;Benavides et al., 2006) have focused on the bryophyte diversity in flooded and non-flooded forests along the Caquetá river, and two areas of the Chiribiquete and Araracuara regions.
Here we provide the most updated inventory of the epiphytic bryophyte flora along of 64 trees distributed in four localities across the Colombian Amazon.Epiphytic bryophytes were sampled on mature rainforest trees, from the base to the outer canopy.All the species were collected in the framework of the project "Diversity of epiphytic bryophytes in the Colombian Amazon".

Study area.
Fieldwork was carried out in four non-flooded forests in the Colombian Amazon.This forest is the dominant forest type in the region and covers ca.80% of the total area of the Amazon basin (ter Steege et al., 2000), occupies fairly well drained and non-flooded clayey soils.The forests have an average annual rainfall of ca.3.300 millimeters.December -January has the lowest monthly means whereas the maximum monthly means are from May to June.The average temperature in the region is 25.3°C, with a minimum level of 21°C and a maximum level of 30.2°C.June and August have the lowest minimum values while the maximum values are in December and January.Some dominant Angiosperm families in the forest are Fabaceae, Rubiaceae, Melastomataceae, Moraceae, Annonaceae, Araceae, Euphorbiaceae, Clusiaceae, Lauraceae, Arecaceae (SINCHI 2007).Canopy height of upland forest in the study sites varied from 30 to 40 m.Four study sites were selected; their location and characteristics are showed in Tab. 1 fueron los géneros más diversos, seguidos por Ceratolejeunea y Cheilolejeunea.El promedio de especies por localidad fue de 102.En términos de riqueza y composición de especies, no hubo diferencias significativas entre las cuatro localidades.
Data collection.Epiphytic bryophytes were sampled on mature trees, from the base to the outer canopy.Epiphylls were not included.To climb trees a static rope technique was used as described by Perry (1978), ter Steege & Cornelissen (1988) and ter Steege (1998).The communities of bryophytes were sampled on 64 trees (16 trees in each site study), using six plots of 40 cm 2 per tree, as described by Mota de Oliveira et al., (2009).Thus, there were 96 plots per study site and a total of 384 for the Colombian Amazon.
Samples of all species were collected for identification in the laboratory and subsequently deposited in the Herbario Nacional Colombiano (COL) with some duplicated in the Herbario Amazonico Colombiano (COAH).Nomenclature of bryophytes was based on Gradstein & Uribe (in press), and Churchill (in press).Data analysis.Species presence-absence matrices were prepared for all localities per tree as well as per plot.Species abundance was not measured due to the difficulty of separating the small individuals and to the variations in plant size.To quantify community structure (species accumulation curves per locality and abundance distribution for the complete dataset) we used frequency, viz.number of plots per site in which each species was present, as a surrogate for abundance.Frequency values ranged from 1 to 96, being the maximum number of plots per locality.Species richness per tree in each locality was compared using the Shannon Index and by calculating evenness (Magurran, 2004;Chao et al., 2005).The floristic similarity of epiphytic bryophytes in each study site was tested with the Jaccard Similarity Coefficient (Magurran, 2004).

RESULTS
Eighteen liverworts species new to Colombia were collected (Campos et al., 2014)  From 160 species identified, 51 (32%) occur in all sites, 35 (22%) in three localities, 28 (18%) in two localities and 46 (28%) were restricted to one locality (Appendix).The highest proportion of species recorded from only one locality was found in Putumayo (15.6%).The number of bryophytes species per tree varied from 18 to 42 and the average number of species per plot (40 cm 2 ) was eight.The mean number of species per tree was highest in the Putumayo site with 30.4±4.66, followed by Vaupes with 28.3±5.8,Amazonas 26.5±4.0 and Caquetá with 25.8±4.72 (P<0.01).The Shannon index was slightly higher in Putumayo (H´= 4.2) than in Amazonas (H´= 4.0), Caquetá (H´= 3.9) and Vaupes (H´= 3.9), but evenness was similar in all localities (E = 0.5).In terms of species richness there were no significant differences between the localities (AMOVA; F = 2.52; p = 0.066).
The percentage of floristic similarity between the four sites in the Colombian Amazon was 53%, with a coefficient correlation of 0,69.The highest floristic similarity was found between Caquetá -Vaupés and between Putumayo -Amazonas (59% and 57% each one), and Putumayo-Vaupes was the lower similarity with 49%.
Families, genera and species recorded are listed in Tab. 4 and 5, and in Appendix.The families with the highest number of records were Lejeuneaceae with 1556 (=55% of the total), followed by Calymperaceae (294, 10%), Lepidoziaceae (224, 8%), Octoblepharaceae (157, 6%) and Sematophyllaceae (138, As shown in Fig. 2 (SAD -species abundance distribution) these nine species included the 36% of the records in the complete data set.

DISCUSSION
With 160 species recorded from 64 trees sampled from the base to the canopy, this study is the first inventory of epiphytic bryophytes across the entire Colombian Amazon.Most of the species recorded are widespread in the Amazon basin and also occur in Brazil, Colombia, French Guiana, Guyana, and Ecuador (e.g., Benavides et al., 2004;Benavides et al., 2006;Churchill, 1994;Churchill, in & Ilkiu-Borges, 2007).Nevertheless, there is also a high number of new records for the Colombian Amazon, especially in the Lejeuneaceae (Campos et al., 2014).Many of these new records are from the forest canopy.Since the canopy of the Amazonian forests of Colombia had been little studied, the high number of new records found was to be expected.
Our results are consistent with the recent bryophyte inventory of the Amazon region by Mota de Oliveira & ter Steege (2013),   Gradstein (1995) with 70%, and Gradstein (2006) with 75%.These results and our data show the importance of this family in the flora of tropical lowland forests (Schuster, 1983;Richards, 1984).It can be related with the consideration that Lejeuneaceae is the most advanced and most highly specialized family among the leafy liverworts (e.g., Heinrichs et al., 2007;Wilson et al., 2007).
There were floristic similarities between localities in the Colombian Amazon.The localities share a high percentage of species, 72% presents in more than one site (32% in all sites, 22% in three sites and 18% in two sites) and 28% of species restricted to one site.Species richness (number of species per site) was rather similar among sites, except for Putumayo where the number of species was slightly higher.This could be related to the influence of the northern Andes.Putumayo is the site with the highest elevation in the study (230 m).This condition may favor the presence of Andean species.Surprisingly, most of the species found only in Putumayo (80%) have a predominant Andean distribution (Churchill, in press; Gradstein & Uribe, in press).The northern Andes has a highly diverse vegetation and flora, due to the variation in climate and elevation (Gradstein et al., 2001).Mota de Oliveira & ter Steege (2013), in their study, of nine localities, also reported a higher number of species in the locality with the highest elevation, which was also adjacent to the Andes.

Figure 2 .
Figure 2. SAD -Species abundance distribution based on the complete dataset.(Orange points are representing the nine species that recorded the 36% of the records in the data set).

Figure 3 .
Figure 3. Summary of the species richness per family in four localities of the Colombian Amazon: Amazonas AM, Caquetá CA, Putumayo PU, and Vaupés VA

Table 2 .
Distribution of species richness at family and genera level, and genera richness at family level in Colombian Amazon.

Table 3 .
Species diversity by locality.

Table 4 .
Family richness in the four sites in the Colombian Amazon.

Table 5 .
Number of species per genus in the 4 sites of the Colombian Amazon.

Table 6 .
The most abundant families in the four localities and the proportional distribution of records (in percent).