Biodiversity and Conservation 14: 119–133, 2005.
# Springer 2005
Fern richness, tree species surrogacy, and fragment complementarity in a Mexican tropical montane cloud forest ´ NICA PALACIOS-RIOS GUADALUPE WILLIAMS-LINERA*, MO ´ ´ ´ and RENE HERNANDEZ-GOMEZ Instituto de Ecologı´a, A.C., Apartado Postal 63, 91000 Xalapa, Veracruz, Me´xico; *Author for correspondence (e-mail:
[email protected]; fax: þ52-228-8187809) Received 14 April 2003; accepted in revised form 30 September 2003
Key words: Cloud forest, Complementarity, Conservation, Fern richness, Fern species diversity, Fragments, Mexico, Surrogacy Abstract. We related pteridophytes versus tree species composition to identify surrogate measures of diversity, and complementarity of seven cloud forest fragments. Forest structure, and fern and tree composition were determined in 70 (2 50 m) transects. Fern density (10,150–25,080 individuals/ha) differed among sites. We recorded 83 fern species in the transects. Nonparametric richness estimators indicated that more sampling effort was needed to complete fern inventories (14 more species). However, ferns recorded outside of the transects increased richness to 103 species (six more species than predicted). Twenty-eight species were unique and rare due to special habitat requirements (Diplazium expansum, Hymenophyllum hirsutum, Melpomene leptostoma, Terpsichore asplenifolia), or were at a geographical distribution edge (Diplazium plantaginifolium, Lycopodium thyoides, Pecluma consimilis, Polypodium puberulum). Correlations between fern richness and tree richness and density were not significant, but were significant between fern richness and fern density, between epiphytic fern density and tree richness and density. Tree richness is not a good surrogate for fern diversity. Only three species were recorded in all fragments (Polypodium lepidotrichum, P. longepinnulatum, P. plebeium); thus fragments’ pteridophytes compositions are highly complementary, but more similar for ferns than for trees. A regional conservation approach which includes many small reserves needs to focus supplementarity on patterns of tree and fern species richness.
Introduction Regional biodiversity is represented by surrogates such as indicator groups and correlates. Also, complementary networks selected using cross-taxon congruence in complementarity are used as biodiversity surrogates (e.g., Gaston 1996; Howard et al. 1998; Pharo et al. 1999; Margules et al. 2002; Negi and Gadgil 2002). Numerous studies have tried to identify plants and several animal taxa as indicator groups in different regions. Correlation between two major groups of vascular plants, ferns and phanerogams, and also to other groups has important implications for monitoring diversity, and establishing conservation priorities for a region. Woody plants, moths, butterflies, birds and small mammals were evaluated as potential indicator groups for reserve selection in Uganda (Howard et al. 1998). Other studies have been designed to find whether density and diversity of vascular plants are overlapped to other taxonomic groups of organisms. In Australian forests, a study focused on the relationship between
120 vascular plant diversity and bryophyte and lichen diversity, showed that the ferns had potential as surrogate for bryophyte species richness (e.g., Dirkse and Martakis 1998; Pharo et al. 1999). In an Amazonian rain forest pteridophytes and Melastomataceae were studied as indicators of different soil conditions (Tuomisto and Ruokolainen 1993). There are few studies on montane cloud forest. In Honduras and El Salvador, Curculionidae and Staphylinidae were evaluated for completeness and surrogacy for general patterns of biodiversity (Anderson and Ashe 2000). In central Veracruz, Mexico, cloud forest fragments and coffee plantations, beetles, bats and frogs were studied to identify indicator groups of richness (E. Pineda and G. Halffter, personal communication). One outstanding feature of the tropical montane cloud forest (TMCF) is the topographic and microclimatic heterogeneity. In this sense, patterns of plant diversity change over short distances, showing high levels of beta diversity or species turnover from one site to another, due in part to habitat heterogeneity (Churchill et al. 1995). Also, high diversity at mid-altitude of some taxa, like ferns, has been described (Tryon 1989). Biodiversity conservation in these cloud forests requires a large number of sites to be protected. Therefore, the efficiency of priority sets of sites could be considerably improved, if those areas are chosen so as to account not just for their absolute biological richness but also for how well they complement one another biotically (Colwell and Coddington 1994; Howard et al. 1998; Anderson and Ashe 2000; Williams-Linera 2002). The TMCF is the most diverse type of vegetation in Mexico because it occurs in less than 1% of the territory but harbors 2500 plant species that grow preferentially or exclusively in this forest. Eighteen percent of the plant species are trees, more than 30% are epiphytes (the most diverse group in cloud forests) and around 20% are ferns (the last two categories overlap because several ferns are also epiphytes; Rzedowski 1996; Challenger 1998). Some taxa are particularly illustrative of the high endemicity in the cloud forest of Mexico; ferns are a good example. Thus, there are several reasons to choose ferns when studying the biodiversity of the cloud forest. First, with around 500 species it holds a higher number of fern species than any other vegetation type in Mexico. Given the high diversity of ferns in the cloud forest, they could be excellent indicator species and could be used as surrogate taxa to study the diversity in a site, and compare diversity among sites. Second, fern specificity for certain environments makes the presence (or absence) of this group a good indicator to define an area as pristine or disturbed forest. In general, pteridophytes are abundant in the understory because of the deep shadow and high humidity in this stratum (Challenger 1998; Hietz and Briones 1998). Third, most ferns are terrestrial, thus they are easier to sample than epiphytes such as orchids which also have a high endemicity. Fourth, ferns (and fern allies plants) is one of the oldest groups of plants, and their high species richness has been reduced due to habitat destruction. Fifth, the taxonomy of cloud forest ferns has been well studied, and we have first-hand taxonomic expertise (Palacios-Rios 1992). Forest fragmentation and habitat reduction due to urban expansion are major threats to the conservation of the diversity of the cloud forest in central Veracruz (Williams-Linera et al. 2002). It is imperative to make informed decisions on
121 Table 1. Characteristics of the seven forest fragments studied in central Veracruz, Mexico: geographical coordinates, altitude, total annual precipitation (pp), mean temperature (T), basal area (m2/ha) and density (individuals/ha) of trees 5 cm dbh. Study site
1 2 3 4 5 6 7
Ecological Park Las Can˜ adas Xolostla Rancho Viejo Banderilla Mesa Yerba Acatlan Volcano
Coordinates
0
19830 N, 198110 N, 198320 N, 198300 N, 198350 N, 198330 N, 198400 N,
Altitude (m)
0
96856 W 968590 W 968580 W 978000 W 968560 W 978010 W 968510 W
1250 1340 1450 1500 1470 1875 1840
pp (mm)
1517 2200 1650 1650 1451 1350 1806
T (8C)
18 17 16 14 16 12 14
Trees 5 cm dbh Basal area
Density
61.31 35.32 45.53 89.36 40.67 44.24 37.66
1120 1370 1170 1700 1320 810 360
conservation priority and to determine the correlation between major groups of plants to identify surrogate measures of biodiversity at several spatial scales. Thus, we addressed two hypotheses: (1) fern species richness in the forest fragments is correlated with tree species diversity, and with some abiotic and biotic environmental variables such as altitude, climate, and vegetation structure, and (2) fern species richness pooled over the study sites is complementary and representative of the regional fern diversity. The objectives were to determine the diversity and abundance of ferns and to relate woody species diversity and density, to assess the complementarity of the fern diversity in seven forest fragments, and to relate fern and woody species diversity to select the most diverse sites and the most complementary set of sites to be protected.
Methods The study area was located in the TMCF region of central Veracruz, Mexico (198300 N, 968540 W, 1250–1875 m altitude). The forest type corresponds to the lower montane rain forest sensu Grubb (1977) or bosque meso´ filo de montan˜ a sensu Rzedowski (1996). Total annual precipitation varies between 1300 and 2200 mm, while mean annual temperature is between 12 and 18 8C (Table 1). The soil in the region has been classified as Andosols (Rossignol 1987). In this area, seven forest fragments were selected (for a detailed description of vegetation structure, woody plant diversity, and disturbance of each site see Williams-Linera 2002). Along the same ten 2 50 m transects used to determine composition of trees 5 cm dbh in each site (Williams-Linera 2002), the fern species inventory was carried out. Ferns were identified and individuals were counted taking special care to count true individuals and not ramets. Ferns were grossly classified as terrestrial if they were found growing in the forest floor or epiphytic if they were rooted on a host (up to ca. 5–6 m height). Fern species were determined by Palacios-Rios and Herna´ ndez-Go´ mez, who previously developed the list of fern species of the cloud forest in Veracruz. Species that could not be consistently
122 identified in the field were always collected. Vouchers for all species are deposited at herbarium XAL of the Instituto de Ecologı´a, A.C. A complete list will be published separately (Palacios-Rios et al., unpublished). Nomenclature follows the Flora of Veracruz (Sosa and Go´ mez-Pompa 1994). Additionally, the central part of each study site was exhaustively surveyed for fern species that were not found in the transects, the species were recorded and identified. The importance value index (IVI) for each species was estimated as the sum of relative frequency (number of transects in which a species was recorded) and density (number of individuals per area) divided by two. Completeness of inventories was assessed using EstimateS version 5.0.1 (Colwell 1997). The non-parametric incidence-based coverage estimator of species richness (ICE) was used because it best satisfied the criteria established for an ideal species-richness estimator (Chazdon et al. 1998). The formulas to estimate ICE can be found in Colwell (1997). Uniques are species that occur in a single sample unit, and duplicates are species that occur in only two samples (rare species; Colwell and Coddington 1994; Colwell 1997). True richness can hardly be determined in highly diverse communities; thus we used a surrogate variable, Strue*, which is the total number of species found after searching the forest interior of each fragment. True richness (Strue*) is actually a surrogate of the richness in each site. Performance of the non-parametric richness estimator was evaluated following Brose (2002). The accuracy of richness estimators was estimated as percent of true richness (PRT), PRT ¼ ICE 100=Strue*. Complementarity refers to the degree to which an area contributes otherwise unrepresented species to a set of areas (Colwell and Coddington 1994). Complementarity varies from 0% when the lists are identical to 100% when the lists are completely distinct. The formulas to estimate species complementarity of two forest fragments can be found in Colwell and Coddington (1994). Canonical correspondence analysis (CCA) was used to assess the relative importance of some environmental factors in determining the observed fern species distribution. We used the program CANOCO version 4 (ter Braak and Smilauer 1998) with all default options setting and the forward selection of variables option to construct a model of significant variables. Importance values of ferns were used, and the environmental variables tested were altitude, precipitation, and basal area and density of trees. Significance of the canonical axes was determined using a Monte Carlo test. Density of ferns was analyzed using one-way ANOVA, and Pearson correlation coefficients were calculated to relate diversity and density of ferns to diversity and density of trees, and environmental variables. Data were analyzed using the statistical package JMP (SAS 1997).
Results A total of 83 fern species and 12,627 individuals were recorded in the 70 transects in the seven study sites: 46 terrestrial ferns and 37 epiphytic ferns. In the same
123 Table 2. Species of the 15 terrestrial and 15 epiphytic ferns with the highest importance value indexes, and very rare fern species only recorded in one site in the cloud forest region of central Veracruz, Mexico. Species
Family
Study sites 1
2
3
4
5
6
7
Selaginellaceae Blechnaceae Selaginellaceae Pteridaceae Dryopteridaceae Lophosoriaceae Lomariopsidaceae Aspleniaceae Lomariopsidaceae Cyatheaceae Dryopteridaceae Gleicheniaceae Cyatheaceae
22.0 20.2 12.7 13.3 – 1.3 – 9.4 – 3.7 – – –
21.7 4.1 44.4 10.5 – – – 5.8 – 2.9 – – 4.9
33.0 26.9 – 23.3 – – – 6.7 – – – 2.6 1.3
24.3 16.1 23.2 1.3 – 5.6 – – – 6.2 – 7.1 4.2
38.4 26.4 – 15.6 – – – – – 3.4 15.5 2.4 –
– – – – 1.0 16.1 – – 19.6 – – 3.1 4.0
– 0.8 – – 31.1 2.4 23.1 – – – – –
Dryopteridaceae Dryopteridaceae
– –
– –
– –
– –
– –
2.4 –
10.3 12.1
Epiphytic fern species Polypodium plebeium P. longepinnulatum Pecluma dispersa Pleopeltis crassinervata Hymenophyllum tunbrigense Polypodium conterminans Phlebodium pseudoaureum Vittaria graminifolia Polypodium rhodopleuron P. loriceum Hymenophyllum polyanthos Pleopeltis fallax Trichomanes reptans Polypodium lepidotrichum Elaphoglossum vestitum
Polypodiaceae Polypodiaceae Polypodiaceae Polypodiaceae Hymenophyllaceae Polypodiaceae Polypodiaceae Vittariaceae Polypodiaceae Polypodiaceae Hymenophyllaceae Polypodiaceae Hymenophyllaceae Polypodiaceae Lomariopsidaceae
9.7 5.1 8.1 8.4 – 18.5 3.3 7.2 10.4 – – – – 3.6 9.5
25.7 2.6 2.9 5.6 – 1.5 5.1 4.6 0.7 1.0 – 21.5 3.9 2.6 3.0
15.2 13.7 14.7 10.6 – 16.3 7.0 4.7 8.4 – – – – 1.1 –
13.8 12.9 10.1 10.5 0.6 – 8.2 3.4 3.0 7.0 1.3 – – 2.0 1.4
19.9 44.8 – 12.0 – 2.5 6.3 7.0 – – – – – 3.9 –
13.5 10.9 – – 30.0 – 7.1 – – 20.2 9.8 – – 1.2 –
11.7 8.5 12.3 – 9.3 – 9.6 6.7 – 13.6 – 12.8 – –
Rare terrestrial fern species Adiantopsis radiata Asplenium abscissum Blechnum schiedeanum B. stoloniferum Botrychium decompositum B. virginianum Ctenitis equestris Cyathea fulva Dennstaedtia distenta Diplazium franconis D. plantaginifolium
Pteridaceae Aspleniaceae Blechnaceae Blechnaceae Ophioglossaceae Ophioglossaceae Dryopteridaceae Cyatheaceae Dennstaedtiaceae Athyriaceae Athyriaceae
– * – – – – – – – – *
– – – – – – – – – – –
* – – – * * – – * – –
– – – – – – – – – – –
– – * – – – * * – – –
– – – * – – – – – – –
– – – – – – – – – * –
Terrestrial fern species Selaginella martensii Blechnum glandulosum Selaginella galeottii Pteris orizabae Ctenitis hemsleyana Lophosoria quadripinnata Elaphoglossum seminudum Asplenium miradorense Elaphoglossum muelleri Alsophila firma Arachniodes denticulata Sticherus palmatus Cyathea divergens var. tuerckheimii Polystichum distans Phanerophlebia nobilis var. nobilis
124 Table 2. (continued) Species
Elaphoglossum erinaceum Hypolepis nigrescens Lycopodium clavatum L. thyoides Mildella intramarginalis var. serratifolia Polystichum ordinatum Pteris quadriaurita Thelypteris scalaris Rare epiphytic fern species Asplenium cuspidatum Hymenophyllum hirsutum Melpomene leptostoma Pecluma consimilis Polypodium eatonii P. fraternum P. puberulum Trichomanes pyxidiferum
Family
Study sites 1
2
3
4
5
6
7
Lomariopsidaceae Dennstaedtiaceae Lycopodiaceae Lycopodiaceae Pteridaceae
– – – – –
– – – – –
– – – – –
– – – – –
– – – – –
– * * * –
* – – – *
Dryopteridaceae Pteridaceae Thelypteridaceae
– – –
* – *
– * –
– – –
– – –
– – –
– – –
Aspleniaceae Hymenophyllaceae Grammitidaceae Polypodiaceae Polypodiaceae Polypodiaceae Polypodiaceae Hymenophyllaceae
– – – – – – – –
– – – * – – – –
– – – – – * – –
– * * – – – – *
– – – – * – – –
– – – – – – – –
* – – – – – * –
Figure 1. Density of terrestrial and epiphytic ferns in 0.1 ha sampled in seven cloud forest fragments in central Veracruz, Mexico. The bar is one SE of the mean density of all ferns in each site.
samples we recorded only 69 species of trees 5 cm dbh and 785 individuals. The fern species in each site with the highest IVI are listed in Table 2. Density of pteridophytes varied between 1015 and 2508 individuals/0.1 ha. The highest number of individuals was recorded in sites 2 and 6, and the lowest density in sites 3, 5 and 7 (F ¼ 17.13, P < 0.0001, Figure 1). Terrestrial ferns followed the
125
Figure 2. Species accumulation curves (Sobs), the richness estimator (ICE), uniques and duplicates (rare species). (A) All fern species, (B) terrestrial fern species, and (C) epiphytic fern species recorded in seven fragments of the cloud forest in central Veracruz, Mexico.
126 Table 3. Performance of the non-parametric species richness estimators (ICE) for (A) all fern species, (B) terrestrial ferns, and (C) epiphytic ferns. Samples are the number of transects, Sobs is number of species in the samples, Strue* is an approximation to the real number of species in each site, PTR (percent of true richness) is the accuracy of the estimator. Forest fragments 1
4
5
Mean (SD)
2
3
(A) All fern species Samples 10 Sobs 29 Strue* 36 ICE 30 PTR (ICE) 83.3
10 34 39 42 107.7
10 21 31 24 77.4
10 34 37 36 97.3
10 22 31 30 96.8
10 28 32 30 93.8
10 26 32 30 93.8
70 83 103 97 94.2
92.9 (9.1)
(B) Terrestrial ferns Samples 10 15 Sobs 17 Strue* ICE 16 PTR (ICE) 94.1
10 11 13 12 92.3
10 10 17 15 88.2
10 12 13 12 92.3
10 13 18 23 127.8
10 20 24 20 83.3
10 14 15 17 113.3
70 46 63 55 87.3
98.8 (14.7)
(C) Epiphytic ferns Samples 10 14 Sobs Strue* 17 ICE 14 PTR (ICE) 82.4
10 23 25 30 120.0
10 11 12 11 91.7
10 22 24 25 104.2
10 9 10 10 100
6
ALL
10 8 8 8 100
7
10 12 15 13 86.7
70 37 40 42 105
97.8 (11.6)
same trend as all ferns (F ¼ 17.67, P < 0.0001, Figure 1). For epiphytic ferns the sites with the highest densities were 2, 4 and 5, and site 7 had the lowest density recorded in the transects (F ¼ 4.66, P ¼ 0.0006; Figure 1). Density of trees 5 cm dbh varied among study sites (Table 1). Both density and richness of all ferns and trees were not significantly correlated. Density of all ferns was positively correlated with richness of all fern species (r ¼ 0.76, P ¼ 0.04) and with density of terrestrial ferns (r ¼ 0.98, P ¼ 0.0001). Richness of epiphytic ferns was positively correlated with richness of all ferns (r ¼ 0.84, P ¼ 0.02). Also, density of epiphytic ferns showed a positive correlation with density of trees 5 cm dbh (r ¼ 0.83, P ¼ 0.02). The species-accumulation curves did not reach an asymptote in any case, indicating that the sampling effort was not sufficient (Figure 2). Of the 83 species of ferns, 17 were unique species. Five terrestrial uniques were relatively common species in the cloud forests of Veracruz (Asplenium abscissum, Blechnum schiedeanum, Dryopteris wallichiana, Polystichum ordinatum, and Pteris quadriaurita). Other unique species were not very common (Diplazium expansum, D. franconis), rare (Elaphoglossum mexicanum), or common only in higher elevation sites (Lycopodium thyoides). In contrast, most unique epiphytes were uncommon species in the regional forest: Hymenophyllum hirsutum, Melpomene leptostoma, Pecluma
127 Table 4. Complementarity between pairs of fragments of tropical montane cloud forest in central Veracruz, Mexico. (A) All fern species, (B) terrestrial ferns, and (C) epiphytic ferns. Complementarity varies from 0% (when the lists are identical) to 100% (when the lists are completely distinct). Sites
2
(A) All fern species 1 50 2 3 4 5 6
3
4
5
6
7
57 55
66 58 66
66 67 52 70
86 87 86 73 84
75 82 83 82 86 80
65 65 71
73 67 56 68
91 93 93 77 90
79 86 91 92 88 87
67 55 63
56 67 46 71
78 81 73 70 69
70 79 72 74 83 67
(B) Terrestrial fern species 1 56 75 2 50 3 4 5 6 (C) Epiphytic fern species 1 46 33 2 58 3 4 5 6
Figure 3. Biplot of canonical correspondence analysis (CCA) of seven fragments of cloud forest in central Veracruz, Mexico. The environmental variables are altitude, precipitation, basal area, and density of trees.
128 consimilis, Polypodium eatonii, P. puberulum, and Trichomanes pyxidiferum (Palacios-Rios 1992). The richness estimators indicated that 14 additional species of ferns should be found in the region: nine more terrestrial ferns and five additional epiphytic ferns (Figure 2, Table 3). The exhaustive search for Strue* in each fragment indicated that the number of fern species found in a forest fragment outside of the transects was higher than that predicted by ICE. Anyhow, the ratio ICE–Strue* indicated that the accuracy of ICE was high for all fern species (92.9%, Table 3). Richness increased to 103 species when we added the new records found surveying outside the transects. Eleven of the 20 species found searching exhaustively each of the fragments were actually common species, seven were uncommon (e.g., Diplazium plantaginifolium), one was subject to special protection (Cyathea fulva; under the Mexican Norm 059 for Protection of Mexican Native Species, SEMARNAT 2002) and one was rare in Veracruz (Adiantopsis radiata; Palacios-Rios 1992). Fern species complementarity of pairs of forest fragments varied between 50 and 89% (Table 4). Thus, fern species composition was more similar between fragment pairs than tree species composition, which even reached 100% between the site at the highest altitude and sites 1–4 (Williams-Linera 2002). Nevertheless, fern richness was highly complementary among the forest fragments (Table 4). There were only three species recorded in all the study sites (Polypodium lepidotrichum, P. longepinnulatum, P. plebeium). Direct gradient analysis of the 83 fern species and seven sites using CCA revealed that the first axis accounted for 36.2% of the explained variance and the second axis for 21.9%. Biplots indicated that sites 6 and 7, which were located at the higher elevations, were different from the other sites, and altitude was the only significant environmental variable in the model (F ¼ 2.53, P ¼ 0.02, Figure 3). The Monte Carlo test of significance of the first canonical axis was significant (F ¼ 1.14, P ¼ 0.03).
Discussion The regional richness and density of ferns were very high with 83 species sampled in 0.7 ha, and a total of 103 fern species recorded in the seven forest fragments (110 ha; Williams-Linera et al. 2002). Between 2 and 10 km from the study sites, Tryon et al. (1973) found 14 fern species/100 m2 with a density of 2.4 individuals/ m2. The cloud forest of Veracruz (123 km2) harbors 372 species of ferns (Veracruz state (72,417 km2) has 572 fern species; Palacios-Rios 1992); this richness is high when compared with other neotropical montane forest in Costa Rica (175 species above 1200 m of altitude in 58 km2 in Monteverde; Bigelow and Kukle 2000; Haber 2000; 129 species at 2000–3300 m altitude in Chirripo´ National Park; Kappelle and Go´ mez 1992) and Peru (12, 61 and 109 species in lower montane wet forest, montane wet, and montane rain forest, respectively, in Rio Abiseo National Park; Young and Leon 1991). In Mexican tropical lowland forests, fern diversity is far smaller than in montane forests. In Los Tuxtlas Reserve, Veracruz, Mexico, 80
129 species of ferns were recorded (Riba and Pe´ rez-Garcı´a 1997), representing 14% of the pteridophytes reported for the state of Veracruz (Palacios-Rios 1992). Apparently, density of ferns is higher in other neotropical forests. In La Selva, Costa Rica, there were 171 species of pteridophytes (Hartshorn and Hammel 1994), and fern density was reported as 21 species and 204 individuals/0.01 ha (Whitmore et al. 1985). Near Iquitos, Peru, 40 fern species and 7860 individuals in 0.7 ha (Tuomisto and Ruokolainen 1993), and at Cuyabeno, Ecuador, 50 pteridophyte species and 4637 rooted individuals/ha were recorded (Poulsen and Nielsen 1995). Our sampling program using ten 100 m2 transects per site was sufficient in most cases to estimate fern species richness of cloud forest, and the evaluation of the performance of the estimators of species richness indicated a mean accuracy of 92%. The non-parametric estimators may provide a tool to achieve reliable estimates of species richness in studies with minimal sampling programs (e.g., agricultural landscape research; Brose 2002). However, our results strongly suggest that it is important to use different sampling methods when a complete inventory is required. When a regional comparison is made, Tuomisto and Poulsen (2000) suggest sample of the local variation at each site as completely as possible. Otherwise regional differences can be identified when in fact there are none. Our sampling at the different sites captured different parts of the local variation. In the cloud forest sites, most of the common species were also uniques because they required specific microhabitat conditions (Hietz and Briones 1998). A study carried out in the highest study site indicated that fern distribution was significantly correlated with physiological traits associated with water relations. For instance, Asplenium cuspidatum with no evident adaptations to cope with drought, grew in the second most shaded zone within the tree crowns whereas Polypodium puberulum has some xeric adaptations (succulent rhizomes) and tends to grow in the most exposed locations (Hietz and Briones 1998), which may explain why some species were not easily targeted using transects. The rarity of some of the species found in the transects could be explained in terms of their special microhabitat requirement, like H. hirsutum which requires an extremely humid condition proper to the interior of an undisturbed forest (Hietz and Briones 1998). Also, it was a new record in the cloud forest of Veracruz (Palacios-Rios 1992). Some species are naturally rare in the cloud forest, like M. leptostoma, which is endemic to Mexico and Guatemala and it was thought to be extinct in Veracruz (Palacios-Rios 1992), and P. eatonii, which is endemic to Mexico (Palacios-Rios and Go´ mez-Pompa 1997). Complementarity of sites is very important in the cloud forest fragments of central Veracruz (Williams-Linera 2002). For instance, five fern species, endangered of extinction (Palacios-Rios 1992; SEMARNAT 2002), were not detected as rare species because they were abundant in just one study site. Cibotium schiedei (Dicksoniaceae) was found in site 6 only, but with 37 individuals. Other species were growing in several sites, like Trichomanes reptans (Hymenophyllaceae), and Marattia laxa (Marattiaceae), but with just a very few individuals. M. laxa is endemic to Mexico and has the status of protected species (Palacios-Rios and Go´ mez-Pompa 1997). Tree ferns were observed in several sites; however, Sphaeropteris horrida was not recorded in any of the study sites. Another study
130 carried out in this cloud forest region suggested that S. horrida is apparently a forest interior species whereas other tree ferns like Alsophila firma and Lophosoria quadripinnata can be found in more disturbed sites with some edge effect (Bernabe et al. 1999). Interestingly, sites 6 and 7 were different from other study sites with regard to both fern and tree species composition, and also in vegetation structure (WilliamsLinera 2002). Altitude was the only significant factor to separate sites above 1800 m; however, there is not a clear trend in abundance or composition of ferns with altitude. Sites 6 and 7 are characterized by the presence of Fagus grandifolia var. mexicana, a very rare Mexican tree species which was dominant in those sites (Williams-Linera 2002), and Ctenitis hemsleyana and Polystichum distans were only recorded there, but Selaginella spp. were not recorded, even when Selaginella is very abundant in all other cloud forests at lower elevations. Site 6 was special since Blechnum glandulosum was not found, although it is very successful in all sites, and it could be an indicator of disturbance (Tryon 1989; Bigelow and Kukle 2000). Nevertheless, six species were found and abundant only in this site (e.g., Arachniodes denticulata, Blechnum falciforme, Elaphoglossum muelleri) while two were scarce (Lycopodium clavatum and L. thyoides), and two rare (B. stoloniferum and Hypolepis nigrescens). The status for these species has not been evaluated, but apparently they are unthreatened species in the cloud forests of Veracruz (PalaciosRios 1992). Studies on epiphytic communities along an altitudinal gradient in central Veracruz, Mexico, showed that altitude was the factor determining the composition of the epiphytic vegetation of a tree, and that fern richness increased with altitude (Hietz and Hietz-Seifert 1995). The tropical mid-elevation diversity bulge has been documented for ferns (Tryon 1989). In the NE Iberian Peninsula, also, a significant relationship was found between pteridophyte richness and altitude (Pausas and Sa´ ez 2000). Richness of fern and tree species were not correlated in central Veracruz. Therefore, tree species may not be a good surrogate for fern richness. However, epiphytic fern density was positively correlated with tree density, indicating that the abundance and co-occurrence of epiphytes were the result of very large resource heterogeneity and the difficulty of establishing in all but the most suitable microhabitats (Hietz and Briones 1998). In Amazonian rain forests, species richness was affected by the density of individuals (Tuomisto and Poulsen 2000). Also, fern richness distribution has been related to edaphic conditions (Young and Leon 1989; Werff 1992), and the distributions of ferns and Melastomataceae were paralleled along transects, apparently reflecting edaphic conditions (Tuomisto and Ruokolainen 1993). In temperate areas, ferns correlated with bryophyte species richness and showed potential as surrogate for bryophytes in an Australian forest (Pharo et al. 1999). Some studies indicated that many other taxonomic groups show a correlation of species numbers with overall site specific species diversity, but other studies showed opposite results. In Dutch forests, the geographical patterns in species density of vascular plants and bryophytes have little in common, and diversity of hot spots for vascular plants and mosses seldom coincide (Dirkse and Martakis 1998). In tropical areas (Uganda), cross-taxon congruence in com-
131 plementarity may arise because the groups examined showed fundamentally similar biogeographical patterns (Howard et al. 1998). In TMCF in Central America, priority areas analyses based on richness, endemic species, complementarity and higher taxon diversity for Curculionidae and Staphylinidae did not provide a clear indication of either group as the better surrogate for general patterns of biodiversity (Anderson and Ashe 2000). We concluded that our hypothesis one is not supported since fern richness is not related to tree richness or vegetation structure, or any environmental variable. However, the sites at higher altitudes harbor a set of different fern composition. The potential value of an area to overall plant biodiversity conservation may depend on which plant species that area contains, not how many (Gaston 1996). Hypothesis two is supported, since fern species were highly abundant and fern composition was complementary in the cloud forest fragments that we studied. Fragments’ tree species compositions are highly complementary, but less similar for trees than for ferns. Ferns can be used as surrogate species to monitor other forest fragments with high regional biodiversity and relatively undisturbed forest interior conditions. But, a regional conservation approach which includes many small reserves needs to focus supplementarity on patterns of tree and fern species richness, and also consider the threatened species categories.
Acknowledgements This work formed part of the BIOCORES project funded by the EC under the INCO IV programme, contract no. ICA4-CT-2001-10095.
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