Abundance and diversity patterns of terrestrial bryophyte species in secondary and planted montane forests in the northern portion of the Central Cordillera of Colombia Adriana Corrales1,5, Alvaro Duque2, Jaime Uribe3, and Victor Londoño4 1 Maestrı́a en Bosques y Conservación Ambiental, Universidad Nacional de Colombia Sede Medellı́n, Medellı́n, Colombia; 2 Departamento de Ciencias Forestales, Universidad Nacional de Colombia sede Medellı́n. Medellı́n, Colombia; 3 Instituto de Ciencias Naturales, Universidad Nacional de Colombia sede Bogotá. Bogotá, Colombia; 4 Instituto de Biologı́a, Universidad de Antioquia. Medellı́n, Colombia ABSTRACT. Patterns of diversity and distribution of bryophytes were surveyed across three different forest types: secondary montane forest and tree plantations of Cupressus lusitanica and of Pinus patula, in the Andean Central Cordillera of Colombia. A stratified sample design was employed to distribute 40 transects (50 3 40 m each) across forest types, each one conforming to a minimum of ten randomly selected plots of 1 m2. One-Way ANOVA and rarefaction curves were employed to analyze species richness. Species richness was weighted by the total number of plots surveyed in each transect with a minimum of 10 plots with bryophytes present. Detrended Correspondence Analysis (DCA) was used to analyze the patterns of distribution of bryophyte species among forest types. Correlation analyses were employed to test the influence of environmental and spatial factors for species richness and distribution. A total of 151 species were recorded. Weighted species richness was higher in secondary montane forests and cypress plantations than in pine plantations. Bryophyte abundances differed among forest types, with the highest level recored for the cypress plantations. The DCA showed a high floristic similarity among forest types. Soil pH, slope and light availability were the principle factors explaining bryophyte distribution, which support habitat specialization as the main mechanism addressing species distribution within forest types. At a mesoscale level, however, a continuous dispersal of propagules among forest types was considered the main mechanism determining the regional pattern of bryophyte distribution. KEYWORDS. Mosses, Liverwort, Ecology, Diversity, Forest Types, Northern Andes, Ordination Analysis. ¤ The Andean region in Colombia represents roughly 25% of the country (Chaves & Santamarı́a 2006). This region has the highest bryophyte diversity 5 Corresponding author e-mail: acorral0@unal.edu.co DOI: 10.1639/0007-2745-113.1.8 ¤ ¤ with nearly 90% of all moss species and 80% of all liverwort species reported for the country (Churchill 1991; Uribe & Gradstein 1998). Approximately 50% of all bryophytes have been recorded for the elevational range between 2000 and 3000 m (Churchill 1991; Churchill & Linares The Bryologist 113(1), pp. 8–21 Copyright E2010 by The American Bryological and Lichenological Society, Inc. 0007-2745/10/$1.55/0 Corrales et al.: Terrestrial bryophytes in Colombian forests 1995; Churchill et al. 1995; Gradstein 1995; Wolf 1993). Bryophyte composition and richness in tropical forest have been related to a high variability of microhabitats (Holz et al. 2002). The influence of several environmental factors such as light, temperature, humidity and pH have been correlated with patterns of species richness and distribution (Asada et al. 2003; Gradstein et al. 2001; Proctor 2000; Sonesson et al. 2002; Weibull & Rydin 2005). However, Sporn et al. (2009) showed that there was not any correlation between species richness and microclimate in tropical forests. In the Colombian Andes, low temperature, continuous precipitation and constant solar radiation, have been found to favor the growth and development of epiphytic bryophytes (Wolf 1993). However, other factors such as the canopy tree structure and composition, which modifies the throughfall and litter quality, could also affect the establishment of bryophyte species (Weibull & Rydin 2005). At a regional scale, forest and soil type were successfully employed as predictive variables of the bryophyte species richness in temperate regions (Vanderpoorten & Engels 2003). In montane forests located in the Colombian Central Cordillera of the Antioquia region, where different forest types such as secondary montane forest and tree plantations of Cupressus lusitanica and Pinus patula are the dominant vegetation types (cypress and pine hereafter), bryophytes are a very important component. Terrestrial bryophytes have received less attention than their epiphytic counterparts. However, the higher availability of open soil and water along with a lower temperature in tropical montane forests have promoted a higher abundance of bryophytes in the understory than that reported for lowlands (Holz & Gradstein 2005; van Reenen & Gradstein 1983). For this reason, the forest floor of montane forests appears as an appropriate habitat to test hypothesis about the environmental filtering effect on species diversity and distribution (Tuomisto et al. 2003). The main research questions addressed in this study include: Are there any differences in the main patterns of abundance, richness and distribution of bryophytes among secondary montane forests, pine 9 and cypress plantations? Are there any differential patterns of distribution within taxonomic groups when divided by mosses and liverworts? Answers to these questions may help to identify strategies and opportunities for the conservation for bryophyte species in tropical Andean ecosystems. METHODS Study site. The study site comprises about 5000 ha, situated in the Santa Elena area ca. 17 km east of the city of Medellı́n, ca. 6u129–6u189N and 75u259– 75u329W. The entire area is part of a regional protected area administered by the environmental bureau of the Corporación Autonoma Regional del Centro y Norte de Antioquia (CORANTIOQUIA). The whole Santa Elena area encompasses the watersheds of Santa Elena and Piedras Blancas. The soils have been classified as Andisols, with low pH, contents of phosphorous and total bases (Jaramillo 1995). The average relative humidity is 83%, daily solar brightness about 3.55 hours, average temperature is 15uC (range 5–20uC), and wind speed is ca. 0.0029 mh21 (Bedoya et al. 2002). The average annual precipitation has been calculated ca. 1800 mm (Blandon 2002). This regional protected area, which is part of the Parque Arvı́, is composed of small scale farms (averaging less than 1 ha), vacational houses and forested areas. The latter is composed of a mosaic of remnant secondary montane forests that in the past were exploited for charcoal, and tree plantations of exotic coniferous species (Cupressus lusitanica and Pinus patula), which were never managed. The tree plantations belong to the local power company Empresas Públicas de Medellı́n (EEPPM). In the early 1900s and before charcoal exploitation, most of the lands were mined for gold and then for salt. Tree plantations were established about 50 years ago in an attempt to recover soil and increase water quality and availability for human use. Bryophyte sampling. Forest types were defined on vegetation maps produced by CORANTIOQUIA, which were obtained by means of digital and visual interpretation of aerial photographs and satellital images (LANDSAT TM). Three different forest types were defined: secondary montane forests, cypress (Cupressus lusitanica) and pine (Pinus patula) 10 The Bryologist 113(1): 2010 plantations. A stratified sampled design was employed to distribute 40 transects (50 3 40 m each) across the three different forest types. We assumed that the location of each transect was done under homogeneous forest stand conditions, such as successional stage or plantation development age. Thirty transects were in the cypress plantation forests, five in secondary montane forests and five in pine plantation forests. We used this unbalanced sampling design since the data were part of larger research project (Corrales & Duque 2007) also focusing on growth only under the cypress plantations. However, we employed statistical methods, such as rarefaction, to make the sample sizes comparable as discussed below. Each transect was divided by means of an imaginary grid of 50 3 40 m, which was divided every five meters, producing a total of 99 possible sampling points. Ten of these sampling points were chosen by means of a table of random numbers, and a plot of 1 m2 was established. When a selected plot did not have any bryophytes present, it was replaced by another random point from the grid. Once we reached ten random plots of 1 m2 each with bryophytes present the plot selection was considered complete. Thus, among transects, there could be different sample sizes (area). Bryophyte abundance was estimated by using a 1 m2 grid with a mesh size of 10 3 10 cm. The bryophyte profiles in the grid were drawn by hand on a scaled sheet in the field and the drawings were digitalized in Arc View 3.x (ESRI) to quantify the cover per species in each plot. Bryophytes growing on soil, felled branches, rocks or woody debris were collected within each plot. All species were stored and determined at the Herbario de la Universidad de Antioquia (HUA) and the Herbario Nacional Colombiano (COL). Mosses generally follow the botanical classification used by the Missouri Botanical Garden (www.tropicos.org, 9 Dec 2008) and liverworts follow Uribe and Gradstein (1998). Environmental characterization. The slope of the terrain, canopy openness and soil pH were the main abiotic factors used to explain richness and distribution patterns of bryophytes across forest types. The slope was measured with a clinometer SUUNTO; each transect was calculated as the average of ten different measurements carried out in 10 different plots that conformed to each transect. To estimate the canopy gap density the ‘‘Crown illumination index’’ (Brown et al. 2000) was employed; calculated by means of the average of ten values associated with the same plots. Soil pH was calculated as the average of three random samples, surveyed in three 1 m2 plots located within each transect. Due to problems with five samples we could only analyze 35 out of the 40 soil samples. Soil analyses were carried out in the Laboratory of Ecology and Environmental Conservation (LECA) of the Universidad Nacional de Colombia, Medellı́n branch. The geographical coordinates of each transect, latitude and longitude, were estimated using a portable GPS taking as a reference the initial point of each transect. Data analysis. Floristic composition and species richness.—Species richness and abundance were measured by the number of species and the cover area (m2), respectively. In each transect the total number of species was calculated from the sum of all the species found in a minimum of ten 1 m2 plots; however, due to the fact that in some transects we surveyed more than ten plots in all, we weighted the total species richness taking into account the total surveyed area. For example, when in a transect all the first ten plots contained bryophytes, we divided the total number of species by one; however when the total number of plots were, for example, fourteen, we divided the species richness by 1.4. Hereafter, it will be referred in the text as weighted species richness when necessary. Likewise, the total species cover, either one, individually or together, was divided by the total area surveyed in each transect. One way ANOVA and a subsequent TukeyKramer test between forest types were employed to analyze significant differences in species richness. We used a randomization approach for testing the significance due to the unbalanced sampling design and the lack of normality in the abundance data; this approach allowed us to overcome the condition of normality (Gotelli & Graves 1996). The null model employed to test for significant differences in the ANOVA analysis was based on 1000 iterations. ANOVA analysis was done employing ECOSIM Corrales et al.: Terrestrial bryophytes in Colombian forests (Gotelli & Entsminger 2004). Post-hoc Tukey’s honestly significant difference was tested assuming a minimal probability of 0.05 (Sokal & Rohlf 1995), and using the JMP 5 software (SAS 2002). Species-area curves among forest types were compared using rarefaction analysis (Gotelli & Colwell 2001). Due to the unbalanced sample employed we compared the species richness found in secondary forests and pine plantations with the expected richness in cypress plantations based on the average of 1000 iterations of five transects randomly selected. Three different types of curves were analyzed according to the taxonomic group as follows: all bryophytes, mosses and liverworts. Rarefaction analyses were conducted using the software ECOSIM (Gotelli & Entsminger 2004). To assess sampling completeness the Chao 1 estimator was calculated, which estimates the true expected number of species richness based on the number of rare species in the sample (Chao 1984). This was done using the freely available software Estimates (Colwell 2004). Patterns of species distribution.—Patterns in species composition of understory bryophytes, mosses and liverworts were explored using the Detrended Correspondence Analysis (DCA, ter Braak 1987) applying transect data of presence-absence and abundance. The species-transect abundance matrices were transformed using the function Yi9 5 arcseno!yi, as suggested for percentages (Legendre & Legendre 1998; Sokal & Rohlf 1995). The analyses were performed with the CANOCO 4.5 software (ter Braak & Smilauer 1998), using the default option without any additional transformation. Environmental and spatial correlation with species richness and distribution.—To analyze the incidence of abiotic and spatial factors measured on the species richness and distribution patterns we used a pairwise correlation analysis (Sokal & Rohlf 1995). We used a null model based on 1000 iterations to test for significance (Gotelli & Graves 1996). Latitude and longitude were used to test the influence of biological spatial structured processes such as dispersal (Duque et al. 2002; Tuomisto et al. 2003). The environmental variables (Crown illumination index, slope and soil pH) and the spatial template (latitude and longitude), were first correlated with the weighted 11 species richness found in each transect. Likewise, the plot coordinates of the first and second axes obtained from the DCA ordination analyses, both for presence-absence and abundance, were correlated with the same environmental and spatial variables described above; this was done also for all bryophytes, and for liverworts and mosses, following the same approach as that based on a null model for testing significance. Pairwise correlation analyses were performed using ECOSIM (Gotelli & Entsminger 2004). RESULTS Floristic composition and bryophyte species richness. A total of 1230 bryophyte collections were made, representing 38 families, 81 genera and 151 species; 63 mosses and 88 liverworts (Appendix). We could not assign 5 species (mosses) to any family and 19 (13%) could be identified beyond the genus. There were 21 families and 36 genera of mosses and 17 families and 45 genera of liverworts. The most diverse bryophyte family was the Lejeuneaceae (Fig. 1), while the most diverse genera were Campylopus (Dicranaceae) and Plagiochila (Plagiochilaceae). Regarding forest types, 130 species were recorded in cypress plantations, 86 in secondary montane forests and 40 in pine plantations. In total 32 species were found in all forest types, 34 species were present in both secondary montane forests and cypress plantations, 7 were found both in the cypress and pine plantations, and no species were exclusively shared between secondary montane forests and pine plantations. In total 63 species were exclusively found in cypress plantations, 23 in secondary montane forests and one in pine plantations (see Appendix 1). The most frequent moss species within transects was Thuidium peruvianum (Thuidiaceae), while Calypogeia rhombifolia (Calypogeiaceae) was the most frequent liverwort species. The most abundant moss was Hypnum amabile (Hypnaceae), while Frullania sp. (Frullaniaceae) was the most abundant liverwort (Fig. 2). We found 112 species growing only on soil, 81 species growing on wood (10 as epiphytes) and 25 species growing both on soil and wood. Species such as Acroporium estrellae, Frullania caulisequa, Polytrichum juniperinum, and 12 The Bryologist 113(1): 2010 Figure 1. The ten most diverse families in the inventory (40 transects) for the three forest types. Values between brackets equal the number of species encountered for each family. Squamidium livens, were found growing only on wood. On the other hand, species such as Hypnum amabile, Lepidozia cupressina, Leptodontium luteum, Leucobryum antillarum, Sematophyllum sp. 1, and Thuidium peruvianum, were found both on soil and wood, while only Riccardia smaragdina was found growing on stones, but not exclusively. Weighted bryophyte species richness showed significant differences among all forest types; secondary montane forests had more species per transect in average than cypress and pine plantations, respectively (Fig. 3). Species abundance differed between forest types, with the cypress plantations exhibiting the greatest bryophytes cover compared to the other two forest types (Table 1). Sample based rarefaction curves showed a higher bryophyte species diversity in secondary montane forests than in tree plantations. (Fig. 3). The expected total number and percentage of species estimated by the Chao 1 Index were 163 species (53%) for secondary montane forest, 202 (64%) for cypress plantations and 80 (50%) for pine plantations. Pooling all samples together, the expected species richness according to the same estimator was 205, which means a sampling completeness of 74% of the total species richness. Pattern of species distribution between forest types. According to DCA analyses, neither bryophyte species nor independently mosses or hepatics showed any pattern of species distribution clearly related to forest types (Fig. 4). A unique and slight exception to this assertion was found when bryophyte species were analyzed based on incidence data (presence-absence). Therefore, species turnover between forest types was extremely low. This result was confirmed by the length of gradient, which was never greater than four standard deviations, except for liverworts. The liverwort species showed higher eigenvalues and length of gradient when presenceabsence data were employed, this was mainly due to one plot having very few species and behaved as an outlier, which makes it difficult to consider this result as conclusive. In general, the length of gradient and the eigenvalues were higher when the bryophyte and moss species abundance was considered (Table 2). Explanatory factors of species richness and distribution. Canopy openness, which roughly represents the amount of incident light in each transect, showed a negative, though, significant correlation with bryophyte and liverwort species richness. In contrast, the slope had a positive and significant relationship with these two taxonomic groups. Mosses did not show any significant relationship with either environmental or spatial variables (Table 3). In this way, the total number of liverworts species showed a reduction with an increase in canopy openness; on the other hand, an increase in the slope of the terrain seemed to favors an increase in the number of liverwort species. Regarding the patterns of distribution of species based on incidence data, soil pH, slope and light were important factors determining the floristic patterns of bryophytes. The first two variables were also important for moss distribution; this taxonomic group, in terms of the floristic composition, had a strong spatial structured pattern. Floristic patterns of liverworts did not have any significant correlation with anyone of the environmental or spatial variables employed (Table 4). Therefore, microhabitat features along with spatially structured processes might play an important role on structuring bryophyte distribution patterns, particularly for mosses. Species distribution across forest types based on abundance showed light conditions as a key factor for all taxonomic groups. However, light conditions played a completely opposite role for mosses than liverworts; in the former the correlation was positive and significant with the second axis, while in the latter it was negative and significant with the first axis. Soil pH showed a negative and significant Corrales et al.: Terrestrial bryophytes in Colombian forests 13 Figure 2. The most abundant species in all forest types. The frequency refers to the number of occurrences of each species in all 40 transects surveyed. The species cover is defined as the total area occupied by each species (m2) in surveyed area. correlation with the second axis of the DCA based on mosses abundance; this result was strongly supported by the higher and significative differences in soil pH and abundance found in cypress plantations. On the other hand, liverwort distributions based on abundance data were significantly correlated with the slope of the terrain (Table 4). DISCUSSION Bryophyte species richness and abundance. In the Colombian Central Cordillera, our research site, previous studies reported a bryophyte diversity peak at altitudes of 2500–3200 m (Churchill 1991; Wolf 1993). This distribution pattern, which is opposite to the one reported for woody vascular plants (Gentry 1982; Rosenzweig 1995), supports the idea that low evapotranspiration rates caused by high humidity, along with a low to medium temperature, favor bryophyte establishment (Proctor 2003). The environmental features of our study site, where the relative humidity has been estimated at 83%, the annual precipitation around 1800 mm, an altitudinal range of 2500–2600 m and the average temperature at 15uC, should thus be considered favorable to induce high species diversity of brophytes. The high species number recorded in the present study (151) confirms the high bryophyte diversity associated with tropical Andean montane forests. Even though we only focused on terrestrial species, the total number of species reported exceeds prior records established for this area (66 spp.), which included epiphytes and epiphylls (Parra et al. 1999). In similar studies carried out in cloud forests in Costa Rica, where a higher number of species was reported (199 and 206; Gradstein et al. 2000 and Holz et al. 2002, respectively), most of the species (184; Holz et al. 2002) were found growing in the forest understory as well (including base of trunks, debris and soil). The number of bryophyte species encountered here notably exceeded those reported in the Colombian Amazon (84 spp.), where the authors employed a relatively similar sample design (Benavides et al. 2006). Our findings pinpoint the importance of secondary montane forests and plantations as a bryophyte habitat in the Andes. Weighted species richness was higher in secondary montane forests than in cypress and pine plantations, respectively. Light availability, and thus local humidity, appeared as the most important factors promoting species coexistence at a very local scale. This means that more light increases local 14 The Bryologist 113(1): 2010 Figure 3. Rarefaction curves by forest type. a. Bryophyte. b. Mosses. c. Liverworts. Corrales et al.: Terrestrial bryophytes in Colombian forests 15 Table 1. One way ANOVA results of weighted bryophyte species richness and abundance in the three forest types. Values denotes the mean and standard deviation. Significant differences were denoted by: ns 5 non significant; * 5 0.05 # p # 0.01; ** 5 0.01 # p # 0.001; *** 5 p , 0.001. + 5 denotes the mean with a significant difference according to the Tukey-Kramer test (p # 0.05). The analyses of soil pH based on a sample size of 35 transects: cypress: 29, pine: 4 and secondary montane forests: 2. Variables Number of transects Weighted species richness Abundance (%) pH Slope ( u ) Ilumination Index Cypress 25.3 509.017 4.45 15.13 1.96 30 6 6 6 6 6 6.76+ 157.48+ 0.31 5.05 0.45 evaporation and reduces humidity, decreasing the number of species. Since there were not significant differences in the level of canopy openness among forest types, this result simply demonstrated that a closed canopy would in principle be able to harbor more bryophyte species independently of whether a Figure 4. Detrended Correspondence Analisis ordination diagrams. A-1. DCA based on bryophyte abundance. A-2. DCA based on bryophyte presence-absence. B-1. DCA based on moss abundance. B-2. DCA based on moss presence-absence. C-1. DCA based on liverwort abundance.C-2. DCA based on liverwort presence-absence. Pine 15.8 222.78 3.94 18.21 2.33 5 6 6 6 6 6 4.49+ 155.15 0.35 6.37 0.42 Natural secondary forest F 5 6 6 6 6 6 7.84*** 22.97*** 10.25*** 0.71 n.s 1.61 n.s. 34.4 77.96 3.7 18.78 1.97 8.67+ 30.52 0 7.07 0.17 secondary montane forest or not as has been shown by Holz and Gradstein (2005) in their comparison of species richness in primary and secondary montane forests of Costa Rica. Furthermore, structural variability seemed to be another relevant factor explaining species richness patterns. In secondary montane forests, structural variability might provide a higher variety of light environments and substrates such as wood, litter, and debris (Acebey et al. 2003; Holz & Gradstein 2005; Sastre-De Jesús 1992). For example, a more densely populated understory such as that found in secondary montane forests might decrease wind incidence and desiccation (Pharo et al. 2005), which favors species establishment as it was shown in this study. Environmental factors similar to those reported here, such as light, pH of the bark and litter decomposition rates, were directly correlated with bryophyte richness and abundance in other studies (Acebey et al. 2003; Holz & Gradstein 2005; Weibull 2001; Weibull & Rydin 2005). Nevertheless, the results obtained here were in contrast to those found in Indonesia where there was no difference in species richness between cacao plantations and natural forest (Sporn et al. 2009). These differences suggest that more physiological studies of bryophytes are needed in order to understand better structural responses to changes in habitat type and climatic variation. Bryophyte species abundances differed among forest types, being higher in the cypress plantations. In this type of forest ca. 50% of the soil was covered by mosses. Some possible reasons that could explain such a high abundance of bryophytes in cypress plantations are: 1) there is a high availability of bare 16 113(1): 2010 The Bryologist Table 2. Detrended Correspondence Analysis (DCA) results based on presence-absence and abundance data in 40 transects. The length of gradient units is given in standard deviations. Separate 2 groups clearly Axis 1 Axis 2 Inertia total Eigenvalues Length of gradient Mosses 0.367 2.813 0.252 2.464 4.886 Eigenvalues Length of gradient Liverworts 0.395 3.081 0.193 1.921 3.095 Eigenvalues Length of gradient 0.466 6.023 0.363 3.885 7.020 0.442 0.291 4.250 Length of gradient Mosses 3.633 2.886 Eigenvalues Length of gradient Liverworts 0.441 3.400 0.239 2.566 2.919 Eigenvalues Length of gradient 0.589 4.337 0.504 4.723 8.259 Presence-absence Bryophytes Abundance Bryophytes Eigenvalues soil not covered by cypress leaves, enabling the establishment of bryophytes. This contrasts with that in the pine plantations and secondary montane forests where there is a thick layer of litter constraining the colonization of bryophytes on the forest floor. 2) A higher soil pH in the cypress plantations could promote the establishment and growth of those very dominant species, as shown in the results. Patterns of species distribution across forest types. The results of the present study pinpoint two main mechanisms that depend on the spatial scale as the major forces addressing bryophyte species composition in these montane forests. First, at a local scale, bryophyte species showed a positive response to microhabitat variation rather than macroecological features associated to forest types. Type and quality of microsites within the forests, which here mainly concern with features such as soil pH, slope and light availability, were determinant factors explaining bryophyte distributions (see also Mills & MacDonald 2005). Thus, habitat specialization appears as the main mechanism addressing species distribution within forest types. Second, at a mesoscale, which means among forest types, terrestrial bryophytes were widely distributed, and beta diversity was quite low. Therefore we hypothesized that the understory of both tree plantations and secondary montane forests provides the basic ecological requirements for the establishment of most terrestrial bryophytes. We proposed that at a mesoscale level a continuous dispersal of propagules could be defined as the main mechanism determining the regional pattern of distribution of bryophyte species in these montane forests. The long tail of rare species in very diverse ecosystems is a well-known structural characteristic that could easily arise because of undersampling (Hubbell 2001). Dispersal as the major mechanism determining the low beta diversity among forest types could find support in the youthfulness of the forest plantations, which do not exceed 50 years. In this case, it seems quite improbable that all bryophyte species found exclusively in one or both forest plantations come from outside of the oldest neighboring secondary montane forests. Therefore, even when assuming that a small proportion of the species found in the Santa Elena region have come from other surrounding habitats, most of the bryophyte species found in the forest plantations may have come from the local secondary montane forests. Table 3. Pairwise correlation analysis between weighted species richness by trasnect, and spatial and environmental variables. Significant differences were denoted by: ns 5 non significant; * 5 0.05 # p # 0.01; ** 5 0.01 # p # 0.001; *** 5 p , 0.001, and were calculated by mean of a null model based on 1000 permutations. In total, we expect by chance that at least 5% of the correlations to be significant at a probability of 95%. No. Spp Longitude Bryophytes Mosses Liverworts 0.0898 0.1821 0.0343 n.s. n.s. n.s. Latitude 20.1022 20.0158 20.1211 n.s Ilumination Index . n.s. n.s. 20.4724 **** 20.2514 n.s. 20.4828**** pH 20.2130 20.1350 20.2085 Slope n.s. n.s. n.s. 0.2729 * 0.0498 n.s. 0.3199* Corrales et al.: Terrestrial bryophytes in Colombian forests 17 Table 4. Pairwise correlation analyses between DCA scores of the first two axes derived from presence-absence and abundance data, and the spatial and environmental variables. Significant differences were denoted by: ns 5 non significant; * 5 0.05 # p # 0.01; ** 5 0.01 # p # 0.001; *** 5 p , 0.001. and were calculated by mean of a null model based on 1000 permutations. In total, we expect by chance that at least 5% of the correlations to be significant at a probability of 95%. Presence - Absence Variable Axis 1 Abundance Axis 2 Axis 1 Axis 2 Bryophytes Longitude Latitude Ilumination Index pH Slope 20.1758 n.s. 0.0346 n.s. 20.2895* 20.2879* 0.3640* 0.0549 20.0322 0.1351 20.1249 20.2006 n.s. 20.3399* 20.0754 n.s. 20.2154 n.s. 20.3075* 0.3309* 0.2674* 20.0078 n.s. 0.0316 n.s. 0.2492 n.s. 20.1579 n.s. n.s. n.s. n.s. n.s. 0.0631 20.0920 20.2568 20.1518 0.2716 n.s. 0.0962 20.1155 20.2229 20.0127 0.1685 n.s. n.s. n.s. n.s. n.s. 0.0820 n.s. 20.0490 n.s. 0.3674 ** 20.2952* 0.1713 n.s. Mosses Longitude Latitude Ilumination Index pH Slope n.s. n.s. n.s. n.s. 20.1196 n.s. 20.0389 n.s. 0.3614** 20.5006** 0.2689 n.s. Liverwort Longitude Latitude Ilumination Index pH Slope 0.1656 0.0851 20.2543 20.0949 0.2072 n.s. n.s. n.s. n.s. n.s. Disturbance, dispersal and niche theory have been rejected and supported by different studies regarding bryophytes. In Australia, Pharo et al. (2004) found a high bryophyte species assemblage similarity between Eucalyptus natural forests and Pinus radiata plantations. Likewise, Pharo and Vitt (2000) did not find any significant relationship between environmental variables such as age stand, canopy density, plot slope, elevation, number of micro habitats within the plot, local topography, and the patterns of distribution of terrestrial lichen and bryophyte communities in Pinus contorta forests in Canada. Dispersal ability as well as the rate of disturbance within these forests were the main factors explaining the bryophyte composition. Forest disturbance intensity and environmental features also contributed to differentiate bryophyte species diversity between logged natural forests and tree plantations in Canada (Mills & MacDonald 2005; Ross-Davis & Frego 2002). In our study, we basically propose that habitat specialization and dispersal are complementary rather than mutually exclusive 20.1564 20.0195 0.1516 20.1797 0.1525 n.s. n.s. n.s. n.s. n.s. 0.0214 n.s. 0.0425 n.s. 20.3408* 20.0186 n.s. 0.1879 n.s. 20.0409 n.s. 20.0752 n.s. 20.0098 n.s. 20.2399 n.s. 0.2819* processes structuring bryophyte species assemblages in these tropical montane forests. Although mosses and liverworts in tropical mountain forests have different environmental requirements and dispersal strategies (Holz et al. 2002; van Reenen & Gradstein 1983), the diversity patterns in both groups seem to be similar; hence the larger gradient length found for liverworts may be explained by the high diversity and low frequency of liverworts mainly represented by the family Lejeuneaceae (Gradstein 1994). The Lejeuneaceae are the most diverse bryophyte family in the tropics accounting for almost 45% of the liverworts species in montane forests (Gradstein et al. 2001). Studies in tropical forests found the opposite in epiphytic bryophytes: mosses have higher beta diversity than liverworts; this difference has been explained by the low frequency and specialization of different moss species (Wolf 1993). Additional studies of bryophyte diversity are needed in order to understand the mechanisms maintaining species coexistence and species distribution in tropical ecosystems. 18 The Bryologist 113(1): 2010 ACKNOWLEDGMENTS The present study was supported by the Corporación Regional del Centro y Norte de Antioquia (CORANTIOQUIA) and Empresas Públicas de Medellı́n (EPM). We want to thank the people from the region of Santa Elena for their hospitality. Members of the Herbario de la Universidad de Antioquia (HUA) and Herbario Nacional Colombiano (COL) who shared with us their kindness and knowledge during the identification of bryophyte species. Additionally we thank the members from the Corporación Académica Ambiental (CAA) of the Universidad de Antioquia who helped us manage the project. We are strongly indebted to Rob Gradstein and Steve Churchill, who kindly helped us to improve this document in all possible ways. The Departamento de Ciencias Forestales of the Universidad Nacional de Colombia provided accommodation in the Piedras Blancas research station. Finally Fernando Colorado, Jose David Sierra, Juan C. Benavides, Juan L. Toro and Ricardo Callejas provided assistance during the development of the present project. LITERATURE CITED Acebey, A., S. R. Gradstein & T. Krömer. 2003. Species richness and habitat diversification of bryophytes in submontane rain forest and fallows of Bolivia. Journal of Tropical Ecology 19: 9–18. Asada, T., B. G. Warner & A. Banner. 2003. Growth of mosses in relation to climate factors in a hypermaritime coastal peatland in British Columbia, Canada. The Bryologist 106: 516–527. Bedoya, A. M., V. Hernández, G. C. Mejı́a, A. Largacha & L. A. Velez. 2002. Formas y Procesos de Ocupación del Suelo, Corregimiento de Santa Elena en el Contexto de la Ordenación Territorial, Bases para un Análisis Ambiental. Tesis, Escuela de Planeación Urbano Regional. Facultad Arquitectura, Universidad Nacional Sede, Medellı́n, Colombia. Benavides, J. C., A. J. Duque, J. F. Duivenvoorden & A. Cleef. 2006. Species richness and distribution of understorey bryophytes in different forest types in Colombian Amazonia. Journal of Bryology 28: 182–189. Blandon, L. A. 2002. Valoración del patrimonio natural: El caso de la cuenca de Piedras Blancas. VII Seminario Internacional de Control Fiscal Ambiental. Villa de Leyva, Colombia. Brown, N., S. Jennings, P. Wheeler & J. Nabe-Nielsen. 2000. An improved method for rapid assessment of forest understorey light environments. Journal of Applied Ecology 37: 1044–1053. Chao, A. 1984. Non–parametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11: 265–270. Chaves, M. E. & M. Santamarı́a. 2006. Informe sobre el Avance en el Conocimiento y la Información de la Biodiversidad 1998–2004. Instituto de Investigaciones de Recursos Biológicos Alxander von Homboldt, Bogotá, Colombia. Churchill, S. P. 1991. The floristic composition and elevational distribution of Colombian mosses. The Bryologist 94: 157–167. ———, D. Griffin II & M. Lewis. 1995. Moss diversity in the tropical Andes. Pages 335–346. In S. P. Churchill, H. Balslev, E. Forero & J. L. Luteyn (eds.), Biodiversity and Conservation of Neotropical Montane Forests. New York Botanical Garden, Bronx. ——— & E. L. Linares. 1995. Prodromus Bryologiae NovoGranatensis. Biblioteca José Jerónimo Triana 12: 1–924. Colwell, R. K. 2004. Estimates, Version 7.5: Statistical Estimation of Species Richness and Shared Species from Samples (Software and User’s Guide). Corrales, A. & A. Duque. 2007. Biomasa y crecimiento de seis especies de briofitos aprovechadas por la comunidad de Santa Elena. Pages 57–75. In A. Duque, T. Lobo, J. G. Marı́n, C. Zarate, J. L. Toro & F. Colorado (eds.), Introducción al Aprovechamiento Sostenible de los Musgos en el Área de Piedras Blancas (Antioquia). Medellı́n, Colombia. Duque, A., M. Sánchez, J. Cavelier & J. Duivenvoorden. 2002. Differential floristic patterns among understory and canopy woody plants in Colombian Amazonia. Journal of Tropical Ecology 18: 499–525. Gentry, A. H. 1982. Neotropical floristic diversity: Phytogeographical connections between Central and South America. Pleistocene climatic fluctuations, or an accident of the Andean orogeny? Annals of the Missouri Botanical Garden 69: 557–593. Gotelli, N. J. & R. K. Colwell. 2001. Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4: 379–391. ——— & G. L. Entsminger. 2004. EcoSim: Null Models Software for Ecology. Version 7. Acquired Intelligence Inc. & Kesey-Bear, Jericho, VT 05465. http://garyentsminger. com/ecosim/index.htm. ——— & G. R. Graves. 1996. Null Models in Ecology., Smithsonian Institution Press, Washington, D.C., U.S.A. Gradstein, S. R. 1994. Lejeuneaceae: Ptychantheae, Brachiolejeuneae. Flora Neotropica Monograph 62: 1–216. ———. 1995. Diversity of Hepaticae and Anthocerotae in montane forests of the tropical Andes. Pages 321–334. In S. P. Churchill, H. Balslev, E. Forero & J. L. Luteyn (eds.), Biodiversity and Conservation of Neotropical Montane Forests. New York Botanical Garden, Bronx. ———, S. P. Churchill & N. Salazar-Allen. 2001. Guide to the bryophytes of tropical America. Memories of the New York Botanical Garden 86: i–viii + 1–571. ———, D. Griffin, M. I. Morales & N. M. Nadkarni. 2000. Diversity and habitat differentiation of mosses and liverworts in the cloud forest of Monteverde, Costa Rica. Caldasia 23: 203–212. Corrales et al.: Terrestrial bryophytes in Colombian forests Holz, I. & S. R. Gradstein. 2005. Cryptogamic epiphytes in primary and recovering upper montane oak forests of Costa Rica—species richness, community composition and ecology. Plant Ecology 178: 89–109. ———, ——— & J. Heinrichs. 2002. Bryophyte diversity, microhabitat differentiation and distribution of life forms in Costa Rican upper montane Quercus forest. The Bryologist 105: 334–348. Hubbell, S. P. 2001. The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press, Princeton, NJ. Jaramillo, D. F. 1995. Andisoles del Oriente Antioqueño: Caracterización Quı́mica y Fertilidad. Editorial Ecográficas Ltda, Medellı́n, Colombia. Legendre, P. & L. Legendre. 1998. Numerical Ecology. 2nd ed. Elsevier, Amsterdam. Mills, S. E. & E. MacDonald. 2005. Factors influencing bryophyte assemblage at different scales in the western Canadian boreal forest. The Bryologist 108: 86–100. Parra, J. D., J. A. Posada & R. Callejas. 1999. Guı́a Ilustrada de los Briofitos del Parque Arvı́. Corporación Autónoma Regional del Centro de Antioquia (CORANTIOQUIA), Medellı́n, Colombia. Pharo, E. J., J. B. Kirkpatrick, L. Gilfedder, L. Mendel & P. A. M. Turner. 2005. Predicting bryophyte diversity in grassland and eucalypt-dominated remnants in sub-humid. Tasmania. Journal of Biogeography 32: 2015–2024. ———, D. B. Lindenmayer & N. Taws. 2004. The effects of large-scale fragmentation on bryophytes in temperate forest. Journal of Applied Ecology 41: 910–921. ——— & D. H. Vitt. 2000. Local variation in bryophyte and macro-lichen cover and diversity in montane forest of western Canada. The Bryologist 103: 455–466. Proctor, M. C. F. 2000. Physiological ecology. Pages 225–246. In A. J. Shaw & B. Goffinet (eds.), Bryophyte Biology. Cambridge University Press, Cambridge & New York. ———. 2003. Experiments on the effect of different intensities of desiccation on bryophyte survival, using chlorophyll fluorescence as an index of recovery. Journal of Bryology 25: 201–210. Rosenzweig, M. L. 1995. Species Diversity in Space and Time. Cambridge University Press, Cambridge. Ross-Davis, A. L. & K. A. Frego. 2002. Comparison of plantations and naturally regenerated clearcuts in the Acadian Forest: forest floor bryophyte community and habitat features. Canadian Journal of Botany 80: 21–32. SAS (Statistical Analysis Software) Institute. 2002. JMP Statistic and Graphics Guide. SAS Institute Inc., Cary, NC. Sastre-De Jesús, I. 1992. Comunidades de briófitos sobre troncos en descomposición en el bosque subtropical mojado de Puerto Rico. Tropical Bryology 5: 181–191. Sokal, R. R. & F. J. Rohlf. 1995. Biometry. 3rd ed. W. H. Freeman & Co., NewYork. 19 Sonesson, M., B. A. Carlsson, T. V. Callaghan, S. Halling, L. O. Björn, M. Bertgren & U. Johanson. 2002. Growth of two peat-forming mosses in subartic mires: Species interactions and effects of simulated climate change. Oikos 99: 151–160. Sporn, S. G., M. Bos, M. Hoffstätter-Müncheberg, M. Kessler & S. R. Gradstein. 2009. Microclimate determines community composition but not richness of epiphytic bryophytes of rainforest and cacao agroforest in Indonesia. Functional Plant Biology 36: 171–179. ter Braak, C. J. K. 1987. Ordination. Pages 91–173. In R. G. H. Jongman, C. J. F. ter Braak & O. F. R. van Tongeren (eds.), Data Analysis in Community and Landscape Ecology. Pudoc, Wageningen, The Netherlands. ——— & P. Smilauer. 1998. CANOCO Reference Manual and User’s Guide to CANOCO for Windows: Software for Canonical Community Ordination version 4. Microcomputer Power, Ithaca, NY. Tuomisto, H., K. Ruokolainen & M. Yli–Halla. 2003. Dispersal, environment, and floristic variation of western Amazonian forests. Science 299: 241–244. Uribe, J. & S. R. Gradstein. 1998. Catalogue of the Hepaticae and Anthocerotae of Colombia. Bryophytorum Bibliotheca 53: 1–99. Vanderpoorten, A. & P. Engels. 2003. Patterns of bryophyte diversity and rarity at a regional scale. Biodiversity and Conservation 12: 545–553. van Reenen, G. B. A. & S. R. Gradstein. 1983. Studies in Colombian cryptogams XX. A transect analysis of the bryophytes vegetation along an altitudinal gradient on the Sierra Nevada de Santa Marta, Colombia. Acta Botanica Neerlandica 32: 163–175. Weibull, H. 2001. Influence of tree species on the epilithic bryophyte flora in deciduous forest of Sweden. Journal of Bryology 23: 55–66. ——— & H. Rydin. 2005. Bryophytes species richness on boulders: relationship to area, habitat diversity and canopy tree species. Biological Conservation 122: 71–79. Wolf, J. H. D. 1993. Ecology of Epiphytes and Epiphyte Communities in Montane Rain Forest, Colombia. Dissertation, University of Amsterdam, Netherlands. ms. received February 23, 2009; accepted July 30, 2009. Appendix. Family and species list of liverworts and mosses found in Piedras Blancas, Colombia. The ocurrence of species in each forest type is indicated within parenthesis. Forest types were abbreviated as follows: C 5 cypress plantations, SMF 5 secondary montane forests and P 5 pine plantations. 20 The Bryologist 113(1): 2010 LIVERWORTS. ACROBOLBACEAE: Lethocolea glossophylla (C/SMF/-); ANEURACEAE: Riccardia smaragdina (C/SMF/-); BALANTIOPSACEAE: Isotachis sp.1 (C/-/-); CALYPOGEIACEAE: Calypogeia peruviana (C/SMF/-), Calypogeia rhombifolia (C/SMF/P), Mnioloma fissistipulum (-/SMF/-); CEPHALOZIACEAE: Odontoschisma denudatum (C/SMF/-); CEPHALOZIELLACEAE: Cylindrocolea sp. 1 (C/-/-); FRULLANIACEAE: Frullania apiculata (-/SMF/-), Frullania bicornistipula (C/-/-), Frullania brasiliensis (C/-/P), Frullania caulisequa (-/SMF/-), Frullania mirabilis (C/-/-), Frullania setigera (-/SMF/-), Frullania sp. 1 (C/-/-), Frullania sp. 2 (C/SMF/P), Frullania subgen. Chonantelia (C/-/-); HERBERTACEAE: Herbertus acanthelius (C/-/-), Herbertus divergens (C/-/-); JUNGERMANNIACEAE: Anastrophyllum nigrescens (C/-/-), Jamesoniella rubricaulis (C/-/-); LEJEUNEACEAE: Aphanolejeunea sp. 1 (C/-/P), Ceratolejeunea cornuta (C/-/-), Ceratolejeunea cubensis (C/-/-), Ceratolejeunea desciscens (C/-/-), Ceratolejeunea fallax (C/-/-), Ceratolejeunea filaria (C/-/-), Cheilolejeunea comans (C/-/P), Cheilolejeunea discoidea (C/-/-), Cheilolejeunea inflexa (C/-/-), Cheilolejeunea rigidula (C/SMF/P), Cheilolejeunea trifaria (C/SMF/-), Cyclolejeunea peruviana (C/SMF/-), Dicranolejeunea axillaris (C/-/-), Drepanolejeunea bidens (C/-/-), Drepanolejeunea campanulata (C/-/-), Drepanolejeunea inchoata var. inchoata (C/SMF/P), Drepanolejeunea lichenicola (C/-/-), Frullanoides densifolia (C/SMF/-), Harpalejeunea sp. 1 (C/-/-), Lejeunea flava (C/SMF/P), Lejeunea monimiae (C/-/-), Leptolejeunea sp. 1 (C/-/-), Leucolejeunea xanthocarpa (-/-/P), Lopholejeunea subfusca (C/SMF/P), Marchesinia brachiata (C/SMF/-), Mastigolejeunea auriculata (C/-/P), Microlejeunea bullata (C/SMF/P), Omphalanthus filiformis (C/SMF/-), Schiffneriolejeunea polycarpa (C/SMF/P), Symbiezidium barbiflorum (C/SMF/P), Taxilejeunea pterigonia (C/-/-), Taxilejeunea sp. 1 (C/SMF/-), Taxilejeunea sp. 2 (C/-/-), Trachylejeunea decurviloba (C/-/-); LEPIDOZIACEAE: Bazzania falcata (C/-/-), Bazzania gracilis (-/SMF/-), Bazzania hookeri (C/SMF/-), Bazzania longistipula (C/SMF/-), Bazzania stolonifera (-/SMF/-), Kurzia capillaris (C/SMF/-), Lepidozia cupressina (C/-/-), Telaranea nematodes (C/SMF/P); LOPHOCOLEACEAE: Heteroscyphus sp.1 (-/SMF/-), Leptoscyphus porphyrius (C/-/-), Lophocolea bidentata (C/SMF/-), Lophocolea connata (C/SMF/-), Lophocolea muricata (C/SMF/-), Lophocolea pycnophylla (C/-/-); METZGERIACEAE: Metzgeria albinea (C/SMF/P), Metzgeria decipiens (C/SMF/P), Metzgeria sp. 1 (C/SMF/-); MONOCLEACEAE: Monoclea gottschei (-/SMF/-); PALLAVICINIACEAE: Symphyogyna aspera (C/-/-), Symphyogyna brasiliensis (-/SMF/-); PLAGIOCHILACEAE: Plagiochila aerea (C/SMF/-), Plagiochila bifaria (C/SMF/-), Plagiochila heterophylla (C/SMF/-), Plagiochila sp. 1 (C/SMF/-), Plagiochila sp. 2 (C/SMF/-), Plagiochila sp. 3 (C/SMF/-), Plagiochila sp. 4 (C/-/-), Plagiochila sp. 5 (C/SMF/-), Plagiochila sp. 6 (C/-/-); RADULACEAE: Radula nudicaulis (-/SMF/-), Radula sp.1 (C/-/-). MOSSES. AMBLYSTEGIACEAE: Calliergonella cuspidata (C/-/-); BARTRAMIACEAE: Breutelia chrysea (C/SMF/P), Philonotis hastata (C/-/-); BRACHYTHECIACEAE: Brachythecium stereopoma (C/-/-); BRYACEAE: Bryum andicola (C/-/-), Rhodobryum grandifolium (C/SMF/P); CALYMPERACEAE: Syrrhopodon gaudichaudii (C/SMF/-), Syrrhopodon incompletus var. incompletus (C/SMF/P), Syrrhopodon prolifer (-/SMF/-), Syrrhopodon prolifer var. prolifer (C/SMF/-), Syrrhopodon prolifer var. scaber (C/-/-), Syrrhopodon sp.1 (-/SMF/-); DALTONIACEAE: Adelothecium bogotense (C/SMF/-), Daltonia longifolia (-/SMF/-); DICRANACEAE: Atractylocarpus longisetus (C/SMF/P), Bryohumbertia filifolia (C/SMF/P), Campylopus anderssonii (C/-/-), Campylopus arctocarpus (C/-/-), Campylopus cuspidatus (C/-/-), Campylopus flexuosusvar. incacorralis (C/-/-), Campylopus luteus (C/SMF/P), Campylopus pauper (C/-/-), Campylopus pilifer (C/-/P), Campylopus richardii (C/-/-), Campylopus subcuspidatus (C/SMF/P), Dicranum frigidum (C/SMF/P), Dicranum peruvianum (C/-/-); FISSIDENTACEAE: Fissidens asplenioides (-/SMF/-), Fissidens elegans (C/SMF/-); HYPNACEAE: Ctenidium malacodes (C/-/P), Hypnum amabile (C/SMF/P), Mittenothamnium reptans (C/SMF/P); HYPOPTERYGIACEAE: Hypopterygium tamarisci (C/SMF/-); LEUCOBRYACEAE: Leucobryum antillarum (C/SMF/P), Leucobryum giganteum (C/-/-); METEORIACEAE: Meteorium nigrescens (C/-/-), Pilotrichella flexilis (C/SMF/P), Squamidium livens Corrales et al.: Terrestrial bryophytes in Colombian forests (C/SMF/-), Squamidium nigricans (C/-/-); MNIACEAE: Plagiomnium rhynchophorum (C/SMF/-); ORTHOTRICHACEAE: Macromitrium podocarpi (C/-/-); PILOTRICHACEAE: Cyclodictyon albicans (C/SMF/P), Lepidopilum scabrisetum (C/SMF/-), Trachyxiphium glanduliferum (C/-/-), Trachyxiphium subfalcatum (C/SMF/-), POLYTRICHACEAE: Polytrichum juniperinum (C/-/-); POTTIACEAE: Leptodontium luteum (C/-/P); RHIZOGONIACEAE: 21 Pyrrhobryum spiniforme (C/-/-); SEMATOPHYLLACEAE: Acroporium estrellae (C/SMF/P), Acroporium pungens (C/SMF/-), Aptychella proligera (-/SMF/-), Heterophyllium affine (C/-/-), Sematophyllum cuspidiferum (C/SMF/P), Sematophyllum subpinnatum (C/SMF/P), Sematophyllum sp. 1 (C/SMF/P); SPHAGNACEAE: Sphagnum sp. 1 (C/SMF/P); THUIDIACEAE: Thuidium peruvianum (C/SMF/P).