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Presence of cushion plants increases community diversity in the high equatorial Andes
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Flora 204 (2009) 270–277 www.elsevier.de/flora
Presence of cushion plants increases community diversity in the high equatorial Andes Petr Sklena´rˇ Department of Botany, Charles University, Bena´tska´ 2, 128 01 Prague 2, Czech Republic Received 10 December 2007; accepted 14 April 2008
Abstract Cushion plants are a common growth form in the equatorial pa´ramo vegetation and their surfaces are often colonized by other plants. This paper analyzes the effect of the cushion plants on the community diversity at 4650 m on the eastern slope of the Iliniza volcano in Ecuador. Ninety sample plots of 1 m2 size were located in the study area and were divided into 25 subplots in which presence and abundance of plant species was recorded. The community diversity was expressed as species richness, Simpson’s diversity index, and evenness. Correlation between the cushion species and the composition of the colonists was measured with the CCA ordination analysis, correlation between the cushion cover and community diversity was measured by means of correlation analysis. Randomized species–area curves were used to compare richness of plant communities with and without the cushions. A total of 32 species were found including five cushion plants. Most species preferred to grow on the cushion surface whereas only a few species were able to colonize open ground. Species richness and Simpson’s index were significantly correlated to the cushion area but no correlation was found for evenness. The cushions were usually composed of more than one species which hampered the examination of the cushion–colonist specific relationships. Nevertheless, cushions of Azorella and Arenaria seemed to provide more favorable habitat for colonization than the other cushion species. Comparison with an earlier study made on Iliniza indicates that the presence of the cushions significantly increases the richness of the plant community. r 2008 Elsevier GmbH. All rights reserved. Keywords: Ecuador; Nurse plant; Pa´ramo; Plant community diversity; Species richness; Tropical alpine
Introduction Cushion plants are a successful growth form in high altitude and high latitude ecosystems of the world (Ko¨rner, 2003). They are remarkably diverse in the southern hemisphere, including temperate and equatorial Andes of South America (Badano and Cavieres, 2006a; Cleef, 1978; Godley, 1978; Heilborn, 1925). The cushion growth form is known to ameliorate the E-mail address: [email protected]. 0367-2530/$ - see front matter r 2008 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2008.04.001
physical environment of the plant. Dead organic material which accumulates inside the cushion and provides nutrient storage in a form of slowly decomposing tissues (Halloy, 1983; Svoboda, 1977) may be the major advantage of this growth form in harsh and unproductive alpine environments (Ko¨rner, 2003). Beside the organic material, water is preserved inside and below the cushion which may reduce the risk of water shortage to the plant (Benoist, 1935; Cavieres et al., 1998; Heilborn, 1925). The temperature of the cushion surface is usually several degrees above that of
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the air, which may be beneficial to the developing tissues (Hedberg and Hedberg, 1979; Ko¨rner, 2003; Ramsay, 1992). Furthermore, the cushion growth form may reduce wind velocity (Hager and Faggi, 1990) and provide a protection from abrasion by wind-borne particles. The cushion growth form is favorable also to other plants which may use the cushion surface as a suitable habitat for establishment. Plants that are able to colonize the cushions are known from various alpine regions of the world (e.g., Alliende and Hoffmann, 1985; Griggs, 1956; Mangen, 1993; Pysˇ ek and Lisˇ ka, 1991) and have been sometimes called cushion-epiphytes (Alliende and Hoffmann, 1985; Heilborn, 1925). By providing a habitat for growth of other plants, the cushions affect the diversity and structure of the plant community (e.g., Alliende and Hoffmann, 1985; Arroyo et al., 2003; Badano and Cavieres, 2006b; Pysˇ ek and Lisˇ ka, 1991). The effect of the cushions on the plant community is species-specific, but it is well established that the occurrence of the cushions generally increases the community diversity. For instance, seedling survival and plant performance are higher in individuals growing inside the cushions than outside them (Cavieres et al., 2005, 2006), as a consequence of the ameliorated conditions provided by the cushion. The cushion plants are a distinct feature of the equatorial pa´ramo vegetation (Cleef, 1981; Harling, 1979; Ramsay and Oxley, 1997) and often host other species on their surfaces (Heilborn, 1925). Despite their importance in the pa´ramo vegetation the ecology of the cushions and their effect on the plant community have only scarcely been studied. Heilborn (1925) discussed the growth and development of the cushions and commented on their xerophytic characters, and Benoist (1935) analyzed the structure of the cushion plant Plantago rigida. Sklena´rˇ (1998) measured the rate of decomposition of organic material inside the Azorella cushions and Sklena´rˇ (2007) studied the thermal ambient of a Xenophyllum cushion. This paper analyzes the effect of the cushion plants on the community diversity in the high-altitude pa´ramo environment of Ecuador. Particularly, the study will: (i) examine the correlation between the cushion plants and the species composition of the community, (ii) examine the correlation between the cover of the cushions and the community diversity, and (iii) compare the species richness of pa´ramo habitats with and without presence of the cushions.
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facing lateral moraine at an altitude of 4650 m. Iliniza is an extinct, eroded volcano located in the western cordillera of Ecuador and hosts distinct pa´ramo vegetation (Sklena´rˇ , 2000, 2006; Sklena´rˇ and Balslev, 2007). Two upper superpa´ramo communities with a prominent occurrence of cushion plants have been found at this altitude, i.e., Xenophyllum humile– Baccharis caespitosa and Arenaria dicranoides–Senecio canescens. The former plant community is confined to more sandy soils (Fig. 1), whereas soils of the latter community contain more coarse material (Sklena´rˇ , 2000). Both communities are characterized by relatively low species richness (12–17 species) and low vegetation cover (10–40% cover). Short-term microclimatic measurements indicate that air temperatures barely reach 12 1C during the day, and night frosts may occur at any time of the year (Sklena´rˇ , 1999, 2007). The daily temperature oscillation of the soil surface is over 50 K, with the minimum close to 5 1C, whereas only a few cm below the soil surface the temperature does not drop below 0 1C. There are no precipitation measurements from the study area.
Data collection The field work was carried in October 2006. A rectangular sample area of 150 50 m with the longer side running parallel to the contour was delineated. Eighty-four square sample plots of 1 m2 were randomly placed within the sample area. In order to increase the number of samples with a high cover of cushions, six large cushions were selected semi-randomly nearby the sample area giving a total of 90 sample plots. The plots were delimited with a frame which was placed on the soil and cushion surfaces. Within the plots, 25 square subplots of the size 20 20 cm were delimited. All vascular plant species present in the subplots were recorded and their abundance was measured by a fivegrade cover scale, i.e., o5%, 5–25%, 25–50%, 50–75%,
Material and methods Study site The research was carried out in the pa´ramo of the Iliniza volcano (5263 m, 01400 S, 781420 W), on an east-
Fig. 1. Cushion-dominated plant community on the eastern slope of Iliniza at an altitude of ca. 4500 m.
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and 75–100%. The cover was estimated as the plant’s vertical projection over the ground and/or over the cushion. On the sides of the cushions the projection of the plant cover was made with regards to the cushion surface and so in those cases the total cover might have exceeded 100%. Species’ score in the 1 m2 plots was estimated by averaging their abundances obtained from the 20 20 cm subplots.
Ordination analysis The habitat preference of the species and their association to grow on the specific cushions in the 90 plots was analyzed by means of the canonical correspondence analysis (CCA), part of the statistical package CANOCO version 4.5 (ter Braak and Sˇmilauer, 1998). The cover estimates of the cushion plants were used as the explanatory environmental variables. Data were square-root transformed and rare species downweighted prior to the analysis, otherwise default options of the program were used. The significance of the resulting ordination was evaluated by 499 Monte Carlo permutations.
Community diversity The community diversity was expressed as: (i) species richness S, (ii) Simpson’s diversity index D, and (iii) evenness E. Species richness was the number of species found in the sample; cushion plants, if present, were excluded from the counts since it was their effect on the community diversity that was analyzed. Simpson’s diversity index was calculated as a reciprocal of the Simpson’s index for finite sample size: D¼P
1 ðni ðni 1Þ=NðN 1ÞÞ
where ni is the cover value of species i, and N is the total sample cover. Evenness was calculated as: E ¼ D/S (Peet, 1974). Correlation between the community diversity and the total cushion cover was analyzed in both the 1 m2 plots and the 20 20 cm subplots. The total cushion cover was obtained by summing up cover values of the individual cushions present in the sample. If the cushion was formed by a single rosette (Hypochaeris) and/or if it covered less than 5% of the subplot area, the plant was treated as a juvenile. Such cushions were arbitrarily considered too small to provide a habitat for colonization by other plant species and were excluded from the calculation of the total cushion cover. The package Resampling Stats for Excel 3.2 (Resampling Stats, Inc., Arlington, VA, USA) was used to obtain the random frequency distribution of the species’ occurrence outside and inside the cushions.
Given the total frequency count of the species in the subplots, expected frequency of occurrence outside and inside the cushions was estimated by 1000 randomizations. The observed frequency was compared to the frequency distribution obtained from the randomization procedure and the significance was estimated. The package EstimateS (Colwell, 2004) was used for the construction of cumulative species–area curves from the samples. A randomization procedure with replacement (100 randomizations) was employed in order to obtain estimates of variance for the entire curves. Correlation coefficients between variables and nonparametric Kruskal–Wallis ANOVA were calculated employing the statistical package NCSS 6.0 (NCSS Statistical Software, Kaysville, UT, USA). A parametric Pearson’s correlation coefficient was calculated if data was distributed normally, otherwise Spearman rank correlation coefficient was employed.
Results There were five species of cushion plants in the sample plots, i.e., A. dicranoides, Azorella corymbosa, Eudema nubigena, Hypochaeris sp., and X. humile. Xenophyllum and Azorella formed the largest cushions, whereas the cushions of Eudema were the smallest. Often, two or more cushion plant species grew together and formed variously tightly interconnected multi-species cushions (i.e., one species-cushion – 10 times, two species-cushion – 17 times, three species-cushion – 21 times, and four species-cushion – 12 times). Beside the cushion plants, 27 species were encountered inside the sample plots (Appendix A), but due to difficulties in distinguishing sterile Agrostis foliata from A. tolucensis and Hypochaeris sessiliflora from H. sonchoides, the two species pairs were pooled together prior to the analyses. The most frequent species were B. caespitosa and Senecio nivalis, whereas Chuquiraga jussieui, Luzula racemosa, and Valeriana alypifolia were the least frequent. Additionally eight species were found, at a very low abundance, within the sample area but outside the sample plots. Nineteen sample plots were empty and contained only rock or bare soil, 30 sample plots did not contain cushion plants. The CCA with the cushion plants used as environmental variables primarily divided the species according to their habitat preference. Most species, located at the right-hand side of the diagram (Fig. 2), were confined to the cushions (e.g., Lachemilla spp., Poa spp.) whereas only a few species tended to occur more often or at higher abundance in the open ground (e.g., Pentacalia microdon and Bromus lanatus). The second axis arranged the species according to their preference for a specific cushion plant, such as
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o0.2% of the total sample area were excluded (Fig. 3). On the contrary, the species richness did not correlate to the cover of bare ground; Spearman rank correlation coefficient r ¼ 0.164, p ¼ 0.394, n ¼ 30 sample plots without cushions. Simpson’s diversity index also correlated positively to the log of the cushion area (Pearson’s r ¼ 0.444, p ¼ 0.001, n ¼ 52 – plots with cushions o0.2% of the total cover and two plots with zero species richness excluded), but the correlation of the evenness was not significant (Pearson’s r ¼ 0.171, p ¼ 0.226, n ¼ 52). A positive correlation between the species richness and cushion cover was also found in
12 10
Species richness
14
Species richness
Calamagrostis spp. and Oritrophium peruvianum tended to prefer X. humile whereas Lachemilla spp. and Poa spp. occurred more frequently on Arenaria and Azorella. Nevertheless, since the cushions were usually formed by more than one species, the preference is not very distinct in most cases. In general, the ordination analysis captured only a small portion of the total variation among the data, the first axis accounted for 7.6% (F ¼ 5.135, p ¼ 0.002) and all canonical axes together accounted for about 10.8% (F ¼ 2.121, p ¼ 0.002) of the variance. The preference of species to inhabit either cushions or open ground was further tested at the level of the 20 20 cm subplots. More than a half of the species occurred significantly more frequently inside the cushions whereas only one species did so in the open ground (see Appendix A for frequency counts and probability estimates). The maximum richness (cushion species excluded) in the 1 m2 sample plots was 13 species encountered in one plot, whereas three sample plots contained only cushion(s) without any other species present. Species richness significantly correlated to the log of the cushion area; Pearson’s correlation coefficient was r ¼ 0.658, po0.001, n ¼ 54 – plots with cushions that covered
273
PoaSubs
6 4
0 0.1
1
LachMand SeneCane PentMicr
Agrostis
EudeNubi
ArenDicr AzorCory
CalaFibr
Simpson's Diversity index
3
100
10
100
10
100
1
0
2 1
1
0.9
Myrosmodes SeneNiva BromLana Festuca TrisSpic CastNubi BV DrabAret OritLimn GentSedi CeraFloc CalaJame XenoHumi OritPeru
4
10
0% cushion cover 2
0 0.1
LachHisp
PoaCucu
5
0.8
Evenness
0.7
LuzuRace
0.6 0.5 0.3 0.2 0.1 0 0.1
Hypochaeris
0% cushion cover 1
0.4 Evenness
ErigEcua
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ChuqJuss
1
8
6
1.0
0% cushion cover 2
0.5
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1 Cushion cover [%]
ValeAlyp -1.0 -0.6
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Fig. 2. CCA ordination diagram of 25 species indicates their correlation for growing in association with the cushions or open ground; eigenvalue of the first canonical axis ¼ 0.210 (p ¼ 0.002), eigenvalue of all canonical axes ¼ 0.401 (p ¼ 0.002), total inertia ¼ 2.744; cover of the cushion plants used as the environmental variables; for species abbreviations see Appendix A.
Fig. 3. Correlation between species richness (top), Simpson’s diversity index (middle), and evenness (bottom) and log cushion area in the 1 m2 sample plots; cushion species excluded from the calculation of the diversity measures; zero richness samples excluded from the calculation of Simpson’s index and evenness. Black points, which indicate the sample plots with the cover of cushions o0.2%, were not included in the correlation analysis. Variation in the sample plots which did not contain any cushions is shown in the inset box-plot diagrams.
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the 20 20 cm subplots; Pearson’s r ¼ 0.385; n ¼ 574 (richness categories 7 and 8 were excluded from the calculation since each of them contained only one observation).
Discussion Most of the species encountered in the study area prefer to grow inside the cushions and only a few of them favor the open ground. The latter group includes the prostrate subshrub P. microdon that grows outside the cushions, B. lanatus which is more frequent in the open ground than on the cushions, and S. canescens which is equally frequent in both types of habitat. A few other species, such as B. caespitosa, S. nivalis, and Draba aretioides, also inhabit the open ground but even then they occur often in the more stabilized soil near the cushions. The general preference of species for growing inside the cushions in the cushion-dominated plant community is also observed in the southern temperate Andes (Arroyo et al., 2003; Cavieres et al., 2002), although it is not always confirmed (Badano et al., 2002; Cavieres et al., 2005; see also Mark and Wilson, 2005). Species richness and Simpson’s index significantly increase with the cushion cover in the 1 m2 sample plots and a consistent trend for the richness is seen also in the 20 20 cm subplots. Similar findings are known from the southern Andes and central Asia (Arroyo et al., 2003; Badano and Cavieres, 2006b; Cavieres et al., 2006; Pysˇ ek and Lisˇ ka, 1991). On the contrary, evenness is not affected by the increasing cushion cover on Iliniza, consistent with central Asia but not with the southern Andes (Badano and Cavieres, 2006a, b). The positive correlation between Simpson’s index and cushion cover thus reflects increasing species richness. The pattern observed in evenness, however, may partly be an artifact due to the semi-quantitative abundance scale which was employed. On smaller cushions, the colonizing species would fall into one or two abundance categories whereas on larger cushions they could be ranked in up to five categories. Such scaling underscores the abundance variation and consequently inflates the evenness in smaller cushions. In the southern Andes, a positive species–area correlation was found for the bare ground (Arroyo et al., 2003; Cavieres et al., 2002). There is no such evidence for Iliniza, which may be due to the very limited pool of species that are able to colonize the open ground (see also Sklena´rˇ , 2006). Vegetation without a prominent occurrence of cushion plants was surveyed on this slope of Iliniza at comparable altitudes by Sklena´rˇ (2006) who used 75 regularly spaced sample plots of 1 m2 size. By comparing the two studies the effect of the cushions on the community diversity can be evaluated. The present
study found 30 species compared to 23 species recorded by Sklena´rˇ (2006) and 19 species were shared between the two studies. From the species found only here, Lachemilla mandoniana, L. hispidula, Poa subspicata, Festuca, Calamagrostis fibrovaginata, and Oritrophium limnophilum were significantly confined to the cushions, Trisetum spicatum, C. jussieui, B. lanatus, and Gentiana sedifolia did not show significant correlation to the habitat type (although only marginally in the latter two), and P. microdon significantly preferred open ground (Appendix A). From the species found only by Sklena´rˇ (2006), Cystopteris fragilis grows in crevices of rocks and boulders (habitats which were avoided in this study), Draba obovata and Werneria pumila colonize open ground, and Calamagrostis aurea has no evident habitat preference (the latter two species were found also here but only outside the sample plots). The cushions thus provide a suitable habitat for growth to those species that are not able to establish on the sloping, bare soil. For instance, L. mandoniana and O. limnophilum typically inhabit humid habitats along rivulets and in cushion mires and their occurrence on the study site is only conditioned by the presence of the cushions upon which surfaces they can establish. There is significantly higher species richness in the cushion-dominated community up to 8 m2 sample size (Fig. 4). At greater sample sizes, the local species pool is being approached and the richness does not differ any longer between the two communities. It should be noted, however, that five cushion species were excluded from the calculation of the curve for the cushion-dominated community whereas they were retained in the other. If the cushion species were excluded from the calculation of the curve for the community without the dominance of cushions, the significant difference between the two curves would remain until 430 m2 sample size. In spite of the limitations due to the different sampling designs between the two studies, it can be concluded that the
Species richness
274
10
1
0.1 1
10 5 Sample area [m2]
50
100
Fig. 4. Log–log cumulative species–area curves for 90 randomly located sample plots of this study (squares; cushion species excluded) and 75 systematically located sample plots from Sklena´rˇ (2006) (diamonds); bars are 1.96 SD resulting from 100 randomizations with replacement.
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plant community diversity increases due to the presence of the cushions on the slope of Iliniza. This supports findings from the southern Andes where a positive effect of cushions on plant community diversity in cushion-dominated environment was found (Badano and Cavieres, 2006a, b). The preference of plants for growth inside the cushions may be due to the higher and less variable moisture inside the cushions (Cavieres et al., 2006). Nevertheless in the sloping pa´ramo habitats the spatial distribution of plants is generally determined by the soil instability (Pe´rez, 1994; Sklena´rˇ , 2006). The high frequency of cushion colonists relative to the open ground thus may also reflect frequent solifluction on Iliniza. The positive effect of the cushions on the community diversity increases in more stressful conditions (Arroyo et al., 2003; Cavieres et al., 2002, 2006). If soil stability was indeed an important factor, habitats less exposed to soil disturbance, such as the flat ground, should have fewer plants colonizing the cushions. Unfortunately, exact data to test this hypothesis are not available from the pa´ramo. Mechanical properties of the cushions, such as compactness, determine the abundance of colonizing plants (Alliende and Hoffmann, 1985) and may explain differences in the colonization frequency among the five cushion species. Eudema forms small cushions of densely packed rosettes and was not observed to host colonizing plants. Hypochaeris has the largest leaves and forms tight cushions which provide little space for colonization. Moreover, Hypochaeris often seems to be the species that colonizes other cushions rather than being colonized. Among the remaining three species, Azorella and Arenaria appear to be more favorable for colonization than Xenophyllum. The smoother surfaces of the former two species may provide better conditions for seedling establishment than stiff leaves protruding from the surface of the Xenophyllum cushions. Since the cushions were usually composed of more than one species and exact recording of cushion preference by the colonizing species was not done, further examination of the cushion-specific relationship cannot be made.
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As the species colonizing the cushions on the slope of Iliniza can be found in other pa´ramo habitats as well, the cushions do not affect the overall pa´ramo species richness. Nevertheless, by providing favorable sites for the establishment of other species the cushions increase the local community diversity. Furthermore, the species inhabiting the cushions may serve as a potential source of colonizers of the surrounding soil once it has become more stabilized. The cushion plants are slow-growing and long-lived organisms (Kleiner and Rundel, 2004; Ko¨rner, 2003; Ralph, 1978), although exact age dating is lacking for the pa´ramo. Due to their longevity, one cushion may serve several generations of colonizing plants. Unfortunately, nothing is known about plant survival and species turnover on the pa´ramo cushions.
Acknowledgements The author is grateful to the Ministry of Education of the Czech Republic (Grant no. MSˇMT 0021620828) and Grant Agency of the Academy of Sciences of the Czech Republic (Grant no. IAA601110702) for the financial support of the research, and to Katya Romoleroux and Hugo Navarrete (PUCE, Quito) for providing research facilities in Ecuador. Two anonymous reviewers are thanked for valuable comments on an earlier draft of the paper, Maurice Jensen kindly revised the English text.
Appendix A A list of species with their abbreviations which were encountered in the 90 sample plots on the slope of Iliniza. Frequency of species’ occurrence outside (OUT) and inside (IN) the cushions in the 20 20 cm subplots, and probability (obtained by 1000 randomizations) that the observed frequencies depart from randomness are given in the last three columns (Table A1).
Table A1 Species
Abbreviation
OUT
IN
p
Arenaria dicranoides Kunth Azorella corymbosa Pers. Eudema nubigena Bonpl. Hypochaeris spp. (H. sessiliflora+H. sonchoides) Xenophyllum humile (Kunth) V.A. Funk Baccharis caespitosa (Ruiz & Pav.) Pers. Calamagrostis jamesoni Steudel. Draba aretioides Kunth Festuca spp. (F. andicola+F. glumosa) Myrosmodes sp.
ArenDicr AzorCory EudeNubi Hypochaeris XenoHumi BaccCaes CalaJame DrabAret Festuca Myrosmodes
– – – – – 168 4 34 9 3
– – – – – 273 52 72 101 75
– – – – – o0.001 o0.001 o0.001 o0.001 o0.001
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Table A1. (continued ) Species
Abbreviation
OUT
IN
p
Oritrophium limnophilum (Sch. Bip.) Cuatrec. Poa cucullata Hack. Lachemilla hispidula (L.M. Perry) Rothm. Calamagrostis fibrovaginata Laegaard Lachemilla paludicola Rothmaler Senecio nivalis (Kunth) Cuatrec. Poa subspicata (Presl) Kunth Oritrophium peruvianum (Lam.) Cuatr. Agrostis spp. (A. foliata+A. tolucensis) Gentiana sedifolia Kunth Castilleja nubigena Kunth Erigeron ecuadoriensis Hieron. Chuquiraga jussieui J.F. Gmelin Cerastium floccosum Benth. Trisetum spicatum (L.) K. Richt Luzula racemosa Desv. Valeriana alypifolia Kunth Senecio canescens (Bonpl.) Cuatrec. Bromus lanatus Kunth Pentacalia microdon (Wedd.) Cuatrec.
OritLimn PoaCucu LachHisp CalaFibr LachMand SeneNiva PoaSubs OritPeru Agrostis GentSedi CastNubi ErigEcua ChuqJuss CeraFloc TrisSpic LuzuRace ValeAlyp SeneCane BromLana PentMicr
1 10 0 3 3 108 0 6 19 0 0 4 0 4 2 0 0 9 25 36
41 57 8 18 16 157 5 15 33 4 4 8 2 7 3 1 1 9 15 5
o0.001 o0.001 0.001 0.002 0.002 0.003 0.030 0.043 0.045 0.062 0.068 0.183 0.257 0.297 0.498 0.507 0.513 0.587 0.081 o0.001
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Harling, G., 1979. The vegetation types of Ecuador – a brief survey. In: Larsen, K., Holm-Nielsen, L.B. (Eds.), Tropical Botany. Academic Press, London, pp. 165–174. Hedberg, I., Hedberg, O., 1979. Tropical-alpine life-forms of vascular plants. Oikos 33, 297–307. Heilborn, O., 1925. Contributions to the ecology of the Ecuadorian pa´ramos with special reference to cushionplants and osmotic pressure. Sven. Bot. Tidskr. 19, 153–170. Kleiner, C., Rundel, P.W., 2004. Microsite requirements, population structure and growth of the cushion plant Azorella compacta in the tropical Chilean Andes. Austral Ecol. 29, 461–470. Ko¨rner, C., 2003. Alpine Plant Life. Functional Plant Ecology of High Mountain Ecosystems, second ed. Springer, Berlin. Mangen, J.-M., 1993. Ecology and vegetation of Mt. Trikora, New Guinea (Irian Jaya/Indonesia). Trav. Sci. Mus. Natl. Hist. Nat. Luxembourg 21, 1–216. Mark, A.F., Wilson, J.B., 2005. Tempo and mode of vegetation dynamics over 50 years in a New Zealand alpine cushion/tussock community. J. Veg. Sci. 16, 227–236. Peet, R.K., 1974. The measurement of species diversity. Annu. Rev. Ecol. Syst. 5, 285–307. Pe´rez, F.L., 1994. Geobotanical influence of talus movement on the distribution of caulescent Andean rosettes. Flora 189, 353–371. Pysˇ ek, P., Lisˇ ka, J., 1991. Colonization of Sibbaldia tetrandra cushions on alpine scree in the Pamiro-Altai Mountains, Central Asia. Arctic Alpine Res. 23, 263–272. Ralph, C.P., 1978. Observations on Azorella compacta (Umbelliferae), a tropical Andean cushion plant. Biotropica 10, 62–67.
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Ramsay, P.M., 1992. The pa´ramo vegetation of Ecuador: the community ecology dynamics and productivity of tropical grasslands in the Andes. Ph.D. Thesis, University of Wales, Bangor. Ramsay, P.M., Oxley, E.R.B., 1997. The growth form composition of plant communities in the Ecuadorian pa´ramos. Plant Ecol. 131, 173–192. Sklena´rˇ , P., 1998. Decomposition of cellulose in the superpa´ramo environment of Ecuador. Preslia 70, 155–163. Sklena´rˇ , P., 1999. Nodding capitula in superparamo Asteraceae: an adaptation to unpredictable environment. Biotropica 31, 394–402. Sklena´rˇ , P., 2000. Vegetation ecology and phytogeography of Ecuadorian superpa´ramos. Ph.D. Thesis, Charles University, Prague. Sklena´rˇ , P., 2006. Searching for altitudinal zonation: species distribution and vegetation composition in the superpa´ramo of Volca´n Iliniza, Ecuador. Plant Ecol. 184, 337–350. Sklena´rˇ , P., 2007. Temperature environment of Xenophyllum humile (Kunth) V.A. Funk, a high Andean cushion plant. Arnaldoa 14, 97–104. Sklena´rˇ , P., Balslev, H., 2007. Geographic flora elements in the Ecuadorian superpa´ramo. Flora 202, 50–61. Svoboda, J., 1977. Ecology and primary production of raised beach communities, Truelove Lowland. In: Bliss, L.C. (Ed.), Truelove Lowland, Devon Island, Canada: A High Arctic Ecosystem. University of Alberta Press, Canada, pp. 185–216. ter Braak, C.J.F., Sˇmilauer, P., 1998. CANOCO Reference Manual and User’s Guide to Canoco for Windows. Centre of Biometry, Wageningen.
Flora 204 (2009) 270–277 www.elsevier.de/flora
Presence of cushion plants increases community diversity in the high equatorial Andes Petr Sklena´rˇ Department of Botany, Charles University, Bena´tska´ 2, 128 01 Prague 2, Czech Republic Received 10 December 2007; accepted 14 April 2008
Abstract Cushion plants are a common growth form in the equatorial pa´ramo vegetation and their surfaces are often colonized by other plants. This paper analyzes the effect of the cushion plants on the community diversity at 4650 m on the eastern slope of the Iliniza volcano in Ecuador. Ninety sample plots of 1 m2 size were located in the study area and were divided into 25 subplots in which presence and abundance of plant species was recorded. The community diversity was expressed as species richness, Simpson’s diversity index, and evenness. Correlation between the cushion species and the composition of the colonists was measured with the CCA ordination analysis, correlation between the cushion cover and community diversity was measured by means of correlation analysis. Randomized species–area curves were used to compare richness of plant communities with and without the cushions. A total of 32 species were found including five cushion plants. Most species preferred to grow on the cushion surface whereas only a few species were able to colonize open ground. Species richness and Simpson’s index were significantly correlated to the cushion area but no correlation was found for evenness. The cushions were usually composed of more than one species which hampered the examination of the cushion–colonist specific relationships. Nevertheless, cushions of Azorella and Arenaria seemed to provide more favorable habitat for colonization than the other cushion species. Comparison with an earlier study made on Iliniza indicates that the presence of the cushions significantly increases the richness of the plant community. r 2008 Elsevier GmbH. All rights reserved. Keywords: Ecuador; Nurse plant; Pa´ramo; Plant community diversity; Species richness; Tropical alpine
Introduction Cushion plants are a successful growth form in high altitude and high latitude ecosystems of the world (Ko¨rner, 2003). They are remarkably diverse in the southern hemisphere, including temperate and equatorial Andes of South America (Badano and Cavieres, 2006a; Cleef, 1978; Godley, 1978; Heilborn, 1925). The cushion growth form is known to ameliorate the E-mail address: [email protected]. 0367-2530/$ - see front matter r 2008 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2008.04.001
physical environment of the plant. Dead organic material which accumulates inside the cushion and provides nutrient storage in a form of slowly decomposing tissues (Halloy, 1983; Svoboda, 1977) may be the major advantage of this growth form in harsh and unproductive alpine environments (Ko¨rner, 2003). Beside the organic material, water is preserved inside and below the cushion which may reduce the risk of water shortage to the plant (Benoist, 1935; Cavieres et al., 1998; Heilborn, 1925). The temperature of the cushion surface is usually several degrees above that of
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the air, which may be beneficial to the developing tissues (Hedberg and Hedberg, 1979; Ko¨rner, 2003; Ramsay, 1992). Furthermore, the cushion growth form may reduce wind velocity (Hager and Faggi, 1990) and provide a protection from abrasion by wind-borne particles. The cushion growth form is favorable also to other plants which may use the cushion surface as a suitable habitat for establishment. Plants that are able to colonize the cushions are known from various alpine regions of the world (e.g., Alliende and Hoffmann, 1985; Griggs, 1956; Mangen, 1993; Pysˇ ek and Lisˇ ka, 1991) and have been sometimes called cushion-epiphytes (Alliende and Hoffmann, 1985; Heilborn, 1925). By providing a habitat for growth of other plants, the cushions affect the diversity and structure of the plant community (e.g., Alliende and Hoffmann, 1985; Arroyo et al., 2003; Badano and Cavieres, 2006b; Pysˇ ek and Lisˇ ka, 1991). The effect of the cushions on the plant community is species-specific, but it is well established that the occurrence of the cushions generally increases the community diversity. For instance, seedling survival and plant performance are higher in individuals growing inside the cushions than outside them (Cavieres et al., 2005, 2006), as a consequence of the ameliorated conditions provided by the cushion. The cushion plants are a distinct feature of the equatorial pa´ramo vegetation (Cleef, 1981; Harling, 1979; Ramsay and Oxley, 1997) and often host other species on their surfaces (Heilborn, 1925). Despite their importance in the pa´ramo vegetation the ecology of the cushions and their effect on the plant community have only scarcely been studied. Heilborn (1925) discussed the growth and development of the cushions and commented on their xerophytic characters, and Benoist (1935) analyzed the structure of the cushion plant Plantago rigida. Sklena´rˇ (1998) measured the rate of decomposition of organic material inside the Azorella cushions and Sklena´rˇ (2007) studied the thermal ambient of a Xenophyllum cushion. This paper analyzes the effect of the cushion plants on the community diversity in the high-altitude pa´ramo environment of Ecuador. Particularly, the study will: (i) examine the correlation between the cushion plants and the species composition of the community, (ii) examine the correlation between the cover of the cushions and the community diversity, and (iii) compare the species richness of pa´ramo habitats with and without presence of the cushions.
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facing lateral moraine at an altitude of 4650 m. Iliniza is an extinct, eroded volcano located in the western cordillera of Ecuador and hosts distinct pa´ramo vegetation (Sklena´rˇ , 2000, 2006; Sklena´rˇ and Balslev, 2007). Two upper superpa´ramo communities with a prominent occurrence of cushion plants have been found at this altitude, i.e., Xenophyllum humile– Baccharis caespitosa and Arenaria dicranoides–Senecio canescens. The former plant community is confined to more sandy soils (Fig. 1), whereas soils of the latter community contain more coarse material (Sklena´rˇ , 2000). Both communities are characterized by relatively low species richness (12–17 species) and low vegetation cover (10–40% cover). Short-term microclimatic measurements indicate that air temperatures barely reach 12 1C during the day, and night frosts may occur at any time of the year (Sklena´rˇ , 1999, 2007). The daily temperature oscillation of the soil surface is over 50 K, with the minimum close to 5 1C, whereas only a few cm below the soil surface the temperature does not drop below 0 1C. There are no precipitation measurements from the study area.
Data collection The field work was carried in October 2006. A rectangular sample area of 150 50 m with the longer side running parallel to the contour was delineated. Eighty-four square sample plots of 1 m2 were randomly placed within the sample area. In order to increase the number of samples with a high cover of cushions, six large cushions were selected semi-randomly nearby the sample area giving a total of 90 sample plots. The plots were delimited with a frame which was placed on the soil and cushion surfaces. Within the plots, 25 square subplots of the size 20 20 cm were delimited. All vascular plant species present in the subplots were recorded and their abundance was measured by a fivegrade cover scale, i.e., o5%, 5–25%, 25–50%, 50–75%,
Material and methods Study site The research was carried out in the pa´ramo of the Iliniza volcano (5263 m, 01400 S, 781420 W), on an east-
Fig. 1. Cushion-dominated plant community on the eastern slope of Iliniza at an altitude of ca. 4500 m.
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and 75–100%. The cover was estimated as the plant’s vertical projection over the ground and/or over the cushion. On the sides of the cushions the projection of the plant cover was made with regards to the cushion surface and so in those cases the total cover might have exceeded 100%. Species’ score in the 1 m2 plots was estimated by averaging their abundances obtained from the 20 20 cm subplots.
Ordination analysis The habitat preference of the species and their association to grow on the specific cushions in the 90 plots was analyzed by means of the canonical correspondence analysis (CCA), part of the statistical package CANOCO version 4.5 (ter Braak and Sˇmilauer, 1998). The cover estimates of the cushion plants were used as the explanatory environmental variables. Data were square-root transformed and rare species downweighted prior to the analysis, otherwise default options of the program were used. The significance of the resulting ordination was evaluated by 499 Monte Carlo permutations.
Community diversity The community diversity was expressed as: (i) species richness S, (ii) Simpson’s diversity index D, and (iii) evenness E. Species richness was the number of species found in the sample; cushion plants, if present, were excluded from the counts since it was their effect on the community diversity that was analyzed. Simpson’s diversity index was calculated as a reciprocal of the Simpson’s index for finite sample size: D¼P
1 ðni ðni 1Þ=NðN 1ÞÞ
where ni is the cover value of species i, and N is the total sample cover. Evenness was calculated as: E ¼ D/S (Peet, 1974). Correlation between the community diversity and the total cushion cover was analyzed in both the 1 m2 plots and the 20 20 cm subplots. The total cushion cover was obtained by summing up cover values of the individual cushions present in the sample. If the cushion was formed by a single rosette (Hypochaeris) and/or if it covered less than 5% of the subplot area, the plant was treated as a juvenile. Such cushions were arbitrarily considered too small to provide a habitat for colonization by other plant species and were excluded from the calculation of the total cushion cover. The package Resampling Stats for Excel 3.2 (Resampling Stats, Inc., Arlington, VA, USA) was used to obtain the random frequency distribution of the species’ occurrence outside and inside the cushions.
Given the total frequency count of the species in the subplots, expected frequency of occurrence outside and inside the cushions was estimated by 1000 randomizations. The observed frequency was compared to the frequency distribution obtained from the randomization procedure and the significance was estimated. The package EstimateS (Colwell, 2004) was used for the construction of cumulative species–area curves from the samples. A randomization procedure with replacement (100 randomizations) was employed in order to obtain estimates of variance for the entire curves. Correlation coefficients between variables and nonparametric Kruskal–Wallis ANOVA were calculated employing the statistical package NCSS 6.0 (NCSS Statistical Software, Kaysville, UT, USA). A parametric Pearson’s correlation coefficient was calculated if data was distributed normally, otherwise Spearman rank correlation coefficient was employed.
Results There were five species of cushion plants in the sample plots, i.e., A. dicranoides, Azorella corymbosa, Eudema nubigena, Hypochaeris sp., and X. humile. Xenophyllum and Azorella formed the largest cushions, whereas the cushions of Eudema were the smallest. Often, two or more cushion plant species grew together and formed variously tightly interconnected multi-species cushions (i.e., one species-cushion – 10 times, two species-cushion – 17 times, three species-cushion – 21 times, and four species-cushion – 12 times). Beside the cushion plants, 27 species were encountered inside the sample plots (Appendix A), but due to difficulties in distinguishing sterile Agrostis foliata from A. tolucensis and Hypochaeris sessiliflora from H. sonchoides, the two species pairs were pooled together prior to the analyses. The most frequent species were B. caespitosa and Senecio nivalis, whereas Chuquiraga jussieui, Luzula racemosa, and Valeriana alypifolia were the least frequent. Additionally eight species were found, at a very low abundance, within the sample area but outside the sample plots. Nineteen sample plots were empty and contained only rock or bare soil, 30 sample plots did not contain cushion plants. The CCA with the cushion plants used as environmental variables primarily divided the species according to their habitat preference. Most species, located at the right-hand side of the diagram (Fig. 2), were confined to the cushions (e.g., Lachemilla spp., Poa spp.) whereas only a few species tended to occur more often or at higher abundance in the open ground (e.g., Pentacalia microdon and Bromus lanatus). The second axis arranged the species according to their preference for a specific cushion plant, such as
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o0.2% of the total sample area were excluded (Fig. 3). On the contrary, the species richness did not correlate to the cover of bare ground; Spearman rank correlation coefficient r ¼ 0.164, p ¼ 0.394, n ¼ 30 sample plots without cushions. Simpson’s diversity index also correlated positively to the log of the cushion area (Pearson’s r ¼ 0.444, p ¼ 0.001, n ¼ 52 – plots with cushions o0.2% of the total cover and two plots with zero species richness excluded), but the correlation of the evenness was not significant (Pearson’s r ¼ 0.171, p ¼ 0.226, n ¼ 52). A positive correlation between the species richness and cushion cover was also found in
12 10
Species richness
14
Species richness
Calamagrostis spp. and Oritrophium peruvianum tended to prefer X. humile whereas Lachemilla spp. and Poa spp. occurred more frequently on Arenaria and Azorella. Nevertheless, since the cushions were usually formed by more than one species, the preference is not very distinct in most cases. In general, the ordination analysis captured only a small portion of the total variation among the data, the first axis accounted for 7.6% (F ¼ 5.135, p ¼ 0.002) and all canonical axes together accounted for about 10.8% (F ¼ 2.121, p ¼ 0.002) of the variance. The preference of species to inhabit either cushions or open ground was further tested at the level of the 20 20 cm subplots. More than a half of the species occurred significantly more frequently inside the cushions whereas only one species did so in the open ground (see Appendix A for frequency counts and probability estimates). The maximum richness (cushion species excluded) in the 1 m2 sample plots was 13 species encountered in one plot, whereas three sample plots contained only cushion(s) without any other species present. Species richness significantly correlated to the log of the cushion area; Pearson’s correlation coefficient was r ¼ 0.658, po0.001, n ¼ 54 – plots with cushions that covered
273
PoaSubs
6 4
0 0.1
1
LachMand SeneCane PentMicr
Agrostis
EudeNubi
ArenDicr AzorCory
CalaFibr
Simpson's Diversity index
3
100
10
100
10
100
1
0
2 1
1
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Myrosmodes SeneNiva BromLana Festuca TrisSpic CastNubi BV DrabAret OritLimn GentSedi CeraFloc CalaJame XenoHumi OritPeru
4
10
0% cushion cover 2
0 0.1
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ChuqJuss
1
8
6
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1 Cushion cover [%]
ValeAlyp -1.0 -0.6
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Fig. 2. CCA ordination diagram of 25 species indicates their correlation for growing in association with the cushions or open ground; eigenvalue of the first canonical axis ¼ 0.210 (p ¼ 0.002), eigenvalue of all canonical axes ¼ 0.401 (p ¼ 0.002), total inertia ¼ 2.744; cover of the cushion plants used as the environmental variables; for species abbreviations see Appendix A.
Fig. 3. Correlation between species richness (top), Simpson’s diversity index (middle), and evenness (bottom) and log cushion area in the 1 m2 sample plots; cushion species excluded from the calculation of the diversity measures; zero richness samples excluded from the calculation of Simpson’s index and evenness. Black points, which indicate the sample plots with the cover of cushions o0.2%, were not included in the correlation analysis. Variation in the sample plots which did not contain any cushions is shown in the inset box-plot diagrams.
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the 20 20 cm subplots; Pearson’s r ¼ 0.385; n ¼ 574 (richness categories 7 and 8 were excluded from the calculation since each of them contained only one observation).
Discussion Most of the species encountered in the study area prefer to grow inside the cushions and only a few of them favor the open ground. The latter group includes the prostrate subshrub P. microdon that grows outside the cushions, B. lanatus which is more frequent in the open ground than on the cushions, and S. canescens which is equally frequent in both types of habitat. A few other species, such as B. caespitosa, S. nivalis, and Draba aretioides, also inhabit the open ground but even then they occur often in the more stabilized soil near the cushions. The general preference of species for growing inside the cushions in the cushion-dominated plant community is also observed in the southern temperate Andes (Arroyo et al., 2003; Cavieres et al., 2002), although it is not always confirmed (Badano et al., 2002; Cavieres et al., 2005; see also Mark and Wilson, 2005). Species richness and Simpson’s index significantly increase with the cushion cover in the 1 m2 sample plots and a consistent trend for the richness is seen also in the 20 20 cm subplots. Similar findings are known from the southern Andes and central Asia (Arroyo et al., 2003; Badano and Cavieres, 2006b; Cavieres et al., 2006; Pysˇ ek and Lisˇ ka, 1991). On the contrary, evenness is not affected by the increasing cushion cover on Iliniza, consistent with central Asia but not with the southern Andes (Badano and Cavieres, 2006a, b). The positive correlation between Simpson’s index and cushion cover thus reflects increasing species richness. The pattern observed in evenness, however, may partly be an artifact due to the semi-quantitative abundance scale which was employed. On smaller cushions, the colonizing species would fall into one or two abundance categories whereas on larger cushions they could be ranked in up to five categories. Such scaling underscores the abundance variation and consequently inflates the evenness in smaller cushions. In the southern Andes, a positive species–area correlation was found for the bare ground (Arroyo et al., 2003; Cavieres et al., 2002). There is no such evidence for Iliniza, which may be due to the very limited pool of species that are able to colonize the open ground (see also Sklena´rˇ , 2006). Vegetation without a prominent occurrence of cushion plants was surveyed on this slope of Iliniza at comparable altitudes by Sklena´rˇ (2006) who used 75 regularly spaced sample plots of 1 m2 size. By comparing the two studies the effect of the cushions on the community diversity can be evaluated. The present
study found 30 species compared to 23 species recorded by Sklena´rˇ (2006) and 19 species were shared between the two studies. From the species found only here, Lachemilla mandoniana, L. hispidula, Poa subspicata, Festuca, Calamagrostis fibrovaginata, and Oritrophium limnophilum were significantly confined to the cushions, Trisetum spicatum, C. jussieui, B. lanatus, and Gentiana sedifolia did not show significant correlation to the habitat type (although only marginally in the latter two), and P. microdon significantly preferred open ground (Appendix A). From the species found only by Sklena´rˇ (2006), Cystopteris fragilis grows in crevices of rocks and boulders (habitats which were avoided in this study), Draba obovata and Werneria pumila colonize open ground, and Calamagrostis aurea has no evident habitat preference (the latter two species were found also here but only outside the sample plots). The cushions thus provide a suitable habitat for growth to those species that are not able to establish on the sloping, bare soil. For instance, L. mandoniana and O. limnophilum typically inhabit humid habitats along rivulets and in cushion mires and their occurrence on the study site is only conditioned by the presence of the cushions upon which surfaces they can establish. There is significantly higher species richness in the cushion-dominated community up to 8 m2 sample size (Fig. 4). At greater sample sizes, the local species pool is being approached and the richness does not differ any longer between the two communities. It should be noted, however, that five cushion species were excluded from the calculation of the curve for the cushion-dominated community whereas they were retained in the other. If the cushion species were excluded from the calculation of the curve for the community without the dominance of cushions, the significant difference between the two curves would remain until 430 m2 sample size. In spite of the limitations due to the different sampling designs between the two studies, it can be concluded that the
Species richness
274
10
1
0.1 1
10 5 Sample area [m2]
50
100
Fig. 4. Log–log cumulative species–area curves for 90 randomly located sample plots of this study (squares; cushion species excluded) and 75 systematically located sample plots from Sklena´rˇ (2006) (diamonds); bars are 1.96 SD resulting from 100 randomizations with replacement.
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plant community diversity increases due to the presence of the cushions on the slope of Iliniza. This supports findings from the southern Andes where a positive effect of cushions on plant community diversity in cushion-dominated environment was found (Badano and Cavieres, 2006a, b). The preference of plants for growth inside the cushions may be due to the higher and less variable moisture inside the cushions (Cavieres et al., 2006). Nevertheless in the sloping pa´ramo habitats the spatial distribution of plants is generally determined by the soil instability (Pe´rez, 1994; Sklena´rˇ , 2006). The high frequency of cushion colonists relative to the open ground thus may also reflect frequent solifluction on Iliniza. The positive effect of the cushions on the community diversity increases in more stressful conditions (Arroyo et al., 2003; Cavieres et al., 2002, 2006). If soil stability was indeed an important factor, habitats less exposed to soil disturbance, such as the flat ground, should have fewer plants colonizing the cushions. Unfortunately, exact data to test this hypothesis are not available from the pa´ramo. Mechanical properties of the cushions, such as compactness, determine the abundance of colonizing plants (Alliende and Hoffmann, 1985) and may explain differences in the colonization frequency among the five cushion species. Eudema forms small cushions of densely packed rosettes and was not observed to host colonizing plants. Hypochaeris has the largest leaves and forms tight cushions which provide little space for colonization. Moreover, Hypochaeris often seems to be the species that colonizes other cushions rather than being colonized. Among the remaining three species, Azorella and Arenaria appear to be more favorable for colonization than Xenophyllum. The smoother surfaces of the former two species may provide better conditions for seedling establishment than stiff leaves protruding from the surface of the Xenophyllum cushions. Since the cushions were usually composed of more than one species and exact recording of cushion preference by the colonizing species was not done, further examination of the cushion-specific relationship cannot be made.
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As the species colonizing the cushions on the slope of Iliniza can be found in other pa´ramo habitats as well, the cushions do not affect the overall pa´ramo species richness. Nevertheless, by providing favorable sites for the establishment of other species the cushions increase the local community diversity. Furthermore, the species inhabiting the cushions may serve as a potential source of colonizers of the surrounding soil once it has become more stabilized. The cushion plants are slow-growing and long-lived organisms (Kleiner and Rundel, 2004; Ko¨rner, 2003; Ralph, 1978), although exact age dating is lacking for the pa´ramo. Due to their longevity, one cushion may serve several generations of colonizing plants. Unfortunately, nothing is known about plant survival and species turnover on the pa´ramo cushions.
Acknowledgements The author is grateful to the Ministry of Education of the Czech Republic (Grant no. MSˇMT 0021620828) and Grant Agency of the Academy of Sciences of the Czech Republic (Grant no. IAA601110702) for the financial support of the research, and to Katya Romoleroux and Hugo Navarrete (PUCE, Quito) for providing research facilities in Ecuador. Two anonymous reviewers are thanked for valuable comments on an earlier draft of the paper, Maurice Jensen kindly revised the English text.
Appendix A A list of species with their abbreviations which were encountered in the 90 sample plots on the slope of Iliniza. Frequency of species’ occurrence outside (OUT) and inside (IN) the cushions in the 20 20 cm subplots, and probability (obtained by 1000 randomizations) that the observed frequencies depart from randomness are given in the last three columns (Table A1).
Table A1 Species
Abbreviation
OUT
IN
p
Arenaria dicranoides Kunth Azorella corymbosa Pers. Eudema nubigena Bonpl. Hypochaeris spp. (H. sessiliflora+H. sonchoides) Xenophyllum humile (Kunth) V.A. Funk Baccharis caespitosa (Ruiz & Pav.) Pers. Calamagrostis jamesoni Steudel. Draba aretioides Kunth Festuca spp. (F. andicola+F. glumosa) Myrosmodes sp.
ArenDicr AzorCory EudeNubi Hypochaeris XenoHumi BaccCaes CalaJame DrabAret Festuca Myrosmodes
– – – – – 168 4 34 9 3
– – – – – 273 52 72 101 75
– – – – – o0.001 o0.001 o0.001 o0.001 o0.001
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Table A1. (continued ) Species
Abbreviation
OUT
IN
p
Oritrophium limnophilum (Sch. Bip.) Cuatrec. Poa cucullata Hack. Lachemilla hispidula (L.M. Perry) Rothm. Calamagrostis fibrovaginata Laegaard Lachemilla paludicola Rothmaler Senecio nivalis (Kunth) Cuatrec. Poa subspicata (Presl) Kunth Oritrophium peruvianum (Lam.) Cuatr. Agrostis spp. (A. foliata+A. tolucensis) Gentiana sedifolia Kunth Castilleja nubigena Kunth Erigeron ecuadoriensis Hieron. Chuquiraga jussieui J.F. Gmelin Cerastium floccosum Benth. Trisetum spicatum (L.) K. Richt Luzula racemosa Desv. Valeriana alypifolia Kunth Senecio canescens (Bonpl.) Cuatrec. Bromus lanatus Kunth Pentacalia microdon (Wedd.) Cuatrec.
OritLimn PoaCucu LachHisp CalaFibr LachMand SeneNiva PoaSubs OritPeru Agrostis GentSedi CastNubi ErigEcua ChuqJuss CeraFloc TrisSpic LuzuRace ValeAlyp SeneCane BromLana PentMicr
1 10 0 3 3 108 0 6 19 0 0 4 0 4 2 0 0 9 25 36
41 57 8 18 16 157 5 15 33 4 4 8 2 7 3 1 1 9 15 5
o0.001 o0.001 0.001 0.002 0.002 0.003 0.030 0.043 0.045 0.062 0.068 0.183 0.257 0.297 0.498 0.507 0.513 0.587 0.081 o0.001
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