Loss of a single tree species will lead to an overall decline in plant diversity: Effect of Dracaena cinnabari Balf. f. on the vegetation of Socotra Island

Biological Conservation 196 (2016) 165–172

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Biological Conservation journal homepage: www.elsevier.com/locate/bioc

Loss of a single tree species will lead to an overall decline in plant diversity: Effect of Dracaena cinnabari Balf. f. on the vegetation of Socotra Island Martin Rejžek a,⁎, Martin Svátek a, Jan Šebesta a, Radim Adolt b, Petr Maděra a, Radim Matula a a b

Department of Forest Botany, Dendrology and Geobiocoenology, Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemědělská 3, 613 00 Brno, Czech Republic NFI Methodology and Analysis, Forest Management Institute Brandýs nad Labem, Náměstí Míru 497, 767 01 Kroměříž, Czech Republic

a r t i c l e

i n f o

Article history: Received 21 August 2015 Received in revised form 2 February 2016 Accepted 11 February 2016 Available online xxxx Keywords: Diversity decline Dracaena cinnabari Endemics Facilitation Socotra Understorey

a b s t r a c t Dracaena cinnabari, the dominant endemic tree of Socotra Island (Yemen), is in serious decline. The effect this will have on the island's plant diversity remains unknown. We aimed to identify plants associated with Dracaena understorey and assess the importance of Dracaena for maintaining plant diversity. A total of 272 relevés were sampled in Dracaena understorey and in open sites to record the number of individuals of vascular plants. Species richness and composition were compared between understorey and open sites, and species associated with each of these habitats were identified. Additionally, the effect of canopy closure on species richness and abundance was analysed. We also recorded woody species composition of Dracaena stands and investigated spatial relations between Dracaena and other mature woody plants. Understorey plant species composition differed from open site composition. The former habitat showed higher β-diversity and species richness. Among recorded plants, 15 species were classified as understorey specialists, 6 as open-site specialists, and 23 as generalists. Rare species, especially endemics, were more common in the understorey. Canopy closure had differential effect on species abundances among the species classes. Species richness and total abundance were found to be highest in the understorey, particularly in the case of low-to-intermediate canopy closure where understorey and open-site specialists may co-occur. For mature woody plant species, Dracaena was spatially independent from other woody species at most distances. Our results suggest that the decline of Dracaena may negatively affect plant diversity, reduce abundance of rare endemic plants and lead to homogenization of vegetation. As no other tree species exists in the study area which could replace the Dracaena, our findings underline the importance of conservation efforts to preserve Dracaena stands on Socotra. © 2016 Elsevier Ltd. All rights reserved.

1. Introduction In recent decades, there has been increasing evidence that positive non-trophic plant interactions (facilitation) play a role in shaping structure, dynamics, and productivity of plant communities (e.g., Hunter and Aarssen, 1988; Callaway, 1995; Bruno et al., 2003; Brooker et al., 2008; Pugnaire et al., 2011). Facilitation contributes to biodiversity of arid and semi-arid ecosystems (Callaway, 1995; Flores and Jurado, 2003) through so-called ‘nurse plants’ (Callaway, 1995; Tielbörger and Kadmon, 2000) which facilitate the establishment and growth of seedlings under and in the vicinity of canopies. Nurse plants are key for maintaining plant diversity in these ecologically harsh environments as they mitigate environmental stress (Callaway, 1995) and provide protection against mechanical damage and herbivory (McAuliffe,

⁎ Corresponding author. E-mail address: [email protected] (M. Rejžek).

http://dx.doi.org/10.1016/j.biocon.2016.02.016 0006-3207/© 2016 Elsevier Ltd. All rights reserved.

1986; García et al., 2000). Their disappearance could have a highly negative impact on species they facilitate. The Socotra Archipelago forms part of the Horn of Africa, an internationally recognized biodiversity hotspot (Mittermeier et al., 2004). Out of 842 species of vascular plants found on Socotra Archipelago, 37% are endemic (Brown and Mies, 2012), which ranks the archipelago as having the fourth highest density of endemic plants among the world's islands (Banfield et al., 2011). The archipelago has an arid climate with limited water availability (Scholte and De Geest, 2010), which indicates that facilitation may play a fundamental role in maintaining Socotra's plant diversity as previously suggested by several authors (Beyhl, 1995; Mies and Beyhl, 1996; Mies, 2001; Miller and Morris, 2004; Brown and Mies, 2012). Empirical proof for this phenomenon, however, is still lacking. The most striking endemic species of Socotra, Dracaena cinnabari Balf. f., known as the Dragon's Blood Tree, currently has only a fragmented distribution in Socotra (Miller and Morris, 2004), but the study by Attorre et al. (2007) suggests that the original distribution of Dracaena has been substantially reduced in the past and that it occupies only 5%

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of its current potential habitat. In its current distribution areas, Dracaena is dominant and often the only tree-size species present, which suggests its possible key facilitative effect on its understorey vegetation which may harbour high plant diversity, including many endemic species. However, the remaining Dracaena stands are currently experiencing severe decline (Mies, 2001; Adolt and Pavliš, 2004; Miller and Morris, 2004; Attorre et al., 2007; Habrová et al., 2009; Hubálková, 2011; Adolt et al., 2012, 2013) and almost completely lack any regeneration due to the effects of long-term aridification and overgrazing (Brown and Mies, 2012). Density of some Dracaena stands decreased by 44% during the 20th century (Habrová et al., 2009) while it has been estimated that the most extensive remaining Dracaena woodland in Socotra will reach the stage of intensive disintegration within 30–77 years (Adolt and Pavliš, 2004). D. cinnabari is an evergreen tree exceeding in height other cooccurring woody species. Its umbrella-shaped dense crowns collect water from air humidity (Beyhl, 1996) through moisture condensation on the large leaf area and through interception of droplets of water from fog. This water then drips and flows down the tree, enriching the soil with moisture, and benefitting the understorey vegetation. It may additionally facilitate understorey vegetation by reducing soil evaporation by shading as well as by enriching the soil through leaf litter. As no other tree species exists in Socotra that would possibly replace the declining Dracaena population, its loss may have negative impacts on overall plant diversity on Socotra Island and could potentially lead to significant negative changes in species composition. While several authors have described Dracaena decline on Socotra (Mies, 2001; Adolt and Pavliš, 2004; Miller and Morris, 2004; Attorre et al., 2007; Habrová et al., 2009; Hubálková, 2011; Adolt et al., 2012, 2013), all of these studies focused exclusively on the Dracaena itself. The effect of its disappearance on other plants has never been explored. In order to assess the consequences of Dracaena absence on overall plant diversity and composition, we compared vegetation under and outside Dracaena canopies by testing the following hypotheses: a) Dracaena absence may have a negative effect on overall plant diversity and abundance. b) Absence of Dracaena may lead to changes in overall plant species composition. c) Dracaena loss could have a negative effect on the occurrence and abundance of endemic plant species.

Furthermore, as all the abovementioned potential facilitative mechanisms of Dracaena are likely to be connected with the density of crowns, we used Dracaena canopy closure as a surrogate environmental variable for understorey resource conditions and hypothesized that all of the effects (hypotheses a, b, c) would be driven by decrease in canopy closure resulting from the disappearance of the Dracaena. In addition to studying understorey vegetation, we also explored higher strata by recording woody species composition of Dracaena stands and investigating spatial associations between Dracaena trees and other mature woody species. While Dracaena is known to be the dominant woody species on Socotra Island, no previous study has focused on investigating the species composition of its stands or has determined any positive or negative relationships between Dracaena and other shrub and tree species. 2. Methods 2.1. Study area The study was carried out on the limestone plateau Rokeb di Firmihin (hereinafter referred to as Firmihin) located in the central eastern part of Socotra Island (12°29′18.33″N 54°00′56.49″E; Fig. 1) where the largest stand of Dracaena in Socotra has been preserved. The altitude of the plateau ranges between 390 and 760 m a. s. l. Soils in the area are

not well developed, with deeper soils usually occurring on flat surfaces below sloping surfaces where soil material accumulates, or in hollows and crevices of rocks which are common in the area. The mean annual temperature is 23.4 °C, with January being the coldest month (mean monthly temperature 21.8 °C) and April the warmest (26.4 °C) (Habrová et al., 2007). The mean total annual precipitation is 344 mm, with rains occurring predominantly during the southwesterly summer monsoon, especially in May and September, while the northeasterly winter monsoon brings rain mainly in November (Habrová et al., 2007). The transition periods between monsoons are dry, with little or no rain. The important feature of the Firmihin summer monsoon is its fog formation which brings additional moisture into the environment (Scholte and De Geest, 2010). The main vegetation type is Buxanthus pedicellatus–D. cinnabari woodland (Brown and Mies, 2012) in which Dracaena is predominant. Whole plateau is subjected to livestock grazing, mainly by goats and sheep, and to a lesser extent, donkeys and camels. 2.2. Data collection 34 sampling points were randomly established throughout Firmihin using spatially stratified sampling with a regular tessellation by congruent squares (for further details of the sampling design, see Adolt et al., 2013) to select sites for studying understorey vegetation as well as composition and spatial patterns of mature woody plants. Fine-scale spatial relations between Dracaena trees and other mature woody plants were investigated in 34 circular plots with a radius of 25 m from each centre point of the samplings. In each plot, all woody plants with DBH (diameter at breast height, i.e., 1.3 m above ground) ≥ 5 cm were identified into species and their DBH and positions were measured to the nearest mm and cm, respectively, using the FieldMap laser technology (the Institute of Forest Ecosystem Research (IFER), Ltd., Jílové u Prahy, Czech Republic; for details of the technology, see Hédl et al., 2009). To collect data on understorey vegetation, we selected the nearest solitary mature Dracaena tree to each sampling point, under and around which 8 rectangular relevés were placed, measuring 0.5 m × 1.0 m (longer side along each cardinal direction). Dracaena trees located on slopes and near potential nurse objects such as other trees, rocks and large stones (Haussmann et al., 2010) were avoided. Four of the eight relevés were placed below the canopy of each selected Dracaena tree (understorey relevés), the longer side placed along the crown radius. Another four relevés of the same size and orientation were placed in the open ground, at distances equal to the crown radius (of a given Dracaena tree) away from the crown edge (open-site relevés; see Fig. A1). Inside each relevé, all rooted individual herbs, shrubs, subshrubs, and tree seedlings were counted and identified into species. We did not include grasses in our study because most of them had heavily browsed above-ground biomass and traits for identifying them could not be well developed. In the case of plants with clonal growth, a plant was considered an individual if it had developed its own independent roots. The taxonomy and nomenclature of species followed Miller and Morris (2004). Among 34 trees, 20 and 14 trees were sampled in September 2010 and January/February 2011, respectively (272 relevés in total). The vegetation in September 2010 was very well developed for both perennial and annual species present, because it was also the end of moisture-laden summer monsoon. At the time of second data collection (January/February 2011), the weather was markedly drier, however the vegetation was still well developed, with the exception of 4 annual species which we therefore excluded from the analyses (see below). To measure Dracaena canopy closure which we expected to affect studied plant assemblages, a hemispherical photograph was taken at the centre of each relevé from a height of 0.5 m above the ground, using a Canon EOS 550D digital SLR camera with Sigma 4.5 mm f/2.8 EX DC HSM Circular Fisheye lens. Images were analysed using the software WinScanopy v. 2008a Reg (Regent Instruments Canada Inc.).

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Fig. 1. Location of Socotra Island and the Rokeb di Firmihin.

Canopy closure for each site was calculated as averages (in %) for 4 relevés under, and 4 relevés outside each Dracaena. 2.3. Data analysis To test whether mature woody plants were spatially associated with Dracaena trees and if so, to what extent, we computed the pair correlation function which is the second-order statistic of spatial point patterns (Diggle, 2003; Illian et al., 2008; Wiegand and Moloney, 2013). The bivariate pair correlation function g12(r) expresses the relationship between patterns 1 (Dracaena) and 2 (other woody species), and gives the expected number of points (i.e., plants) of pattern 2 at distance r from an arbitrary point of pattern 1 (Wiegand and Moloney, 2004). Values of g12(r) greater, equal to, or less than 1 suggest attraction, independence, or repulsion between the two patterns at the distance r, respectively. The g12(r) function was computed four times to investigate separate bivariate relationships between Dracaena and three most abundant woody species (B. pedicellatus, Croton socotranus and Jatropha unicostata), as well as between Dracaena and all woody species (which additionally included with the three species mentioned above, all other rare woody plants). For each bivariate relationship, we summarized the results from all replicate plots by combining the resulting g functions of individual plots into weighted average statistics (Diggle, 2003; Wiegand and Moloney, 2013), where the weight equals the number of points in a given plot divided by the total number of points. Our aim was to increase the sample size and determine general summary characteristics for respective bivariate relationships (Wiegand and Moloney, 2013). Out of all 34 plots, we used only those that contained ≥ 15 woody plants (24 plots in total). The functions were computed with grid-based Programita software (Wiegand and Moloney, 2004) using a cell size of 0.05 m × 0.05 m. A ring width of 0.1 m was used for all functions. The fifth lowest and highest of 199 Monte Carlo simulations of a null model of complete spatial randomness were computed to construct simulation envelopes for g functions. Details on the functions used,

null model and edge correction, are provided by Wiegand and Moloney (2004). The understorey data from four relevés beneath each Dracaena tree were pooled and were treated as data for a given Dracaena tree. Analogously, data from four open-site relevés around each Dracaena were pooled to get data outside the given tree. These tree level data were then used in all following analyses and indices. To test for differences in species composition between understorey and open site plots, we employed non-metric multidimensional scaling ordination (NMDS) with Bray–Curtis index as the measure of dissimilarity using the vegan package (Oksanen et al., 2013) in R 3.1.0 (R Core Team, 2014). Because the data were collected in two sampling periods, we excluded four annual or short-lived perennial species (Acalypha indica, Exacum affine, Oldenlandia balfourii and Oldenlandia bicornuta) from the analysis, because these species were already nearly absent at the time of the second data collection. The significance of differences in community composition of understorey and open-site plots was tested using the “adonis” function in vegan, which performs an analysis of variance using the Bray–Curtis distance matrix. Homogeneities of understorey and open-site composition (i.e., beta diversity) were compared using the “betadisper” function in vegan using the same Bray–Curtis dissimilarity index. This function calculates multivariate homogeneity of group dispersion between plots based on species abundance and is a multivariate analogue of Levene's test for homogeneity of variances (Oksanen et al., 2013). To test for differences in group dispersions, analysis of variance (ANOVA) was performed for the distances of group members to the group centroid. To compare the number of observed species in understorey and open site plots as a function of the sampling effort, we constructed species accumulation curves (SACs) relating species richness to the number of sampled trees using the “specaccum” function in the vegan package with the method “random” and 100 permutations of the data. To analyse the evenness in distribution of species abundance within each habitat, rank abundance plots displaying logarithmic species

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abundances against species rank order were created and models (broken stick, geometric series, log normal, Zipf, and Zipf–Mandelbrot) with a Poisson error distribution were fitted to the plots with the “radfit” function in the vegan package. The difference between rank abundance plots was tested with the Kolmogorov–Smirnov test. The best model for each habitat was selected by Akaike information criterion (AIC). To identify Dracaena understorey specialists, open-site specialists, and species indifferent to Dracaena presence, i.e., generalists, we used the multinomial species classification method (CLAM) by Chazdon et al. (2011). This method classifies species as either generalist, habitat A specialist, habitat B specialist or as too rare for confirmed classification. It uses a multinomial model based on estimated species relative abundance in two habitats and permits robust statistical classification, without a priori exclusion of rare species (Chazdon et al., 2011). The analysis was performed in R, using the “clamtest” function in the vegan package. We used a conservative approach with the supermajority specialization threshold (two-third) and performed the classification at p = 0.005 (for details on this method, see Chazdon et al., 2011). To determine whether the canopy closure affected abundances of most common species (present under and around at least 10 Dracaena trees) and all species together (total abundance), as well as species richness under and outside Dracaena trees, we used generalised linear models (GLM) with a Poisson error distribution. The analyses were performed in R 3.1.0 (R Core Team, 2014) and results were visualised using package ggplot2 (Wickham, 2009). 3. Results 3.1. Woody plant vegetation The plots were dominated by D. cinnabari with an admixture of C. socotranus, J. unicostata and B. pedicellatus, the only other species that represented more than 0.1% of the measured woody plants (Table 1). Dracaena was the only abundant tree-sized species and was dominant in both density and basal area, while the other three species rarely exceeded shrub stature. Patterns of Dracaena and the other three woody species tested were spatially independent at most scales, apart from a weak tendency of Buxanthus and Jatropha to cluster at 1 m from Dracaena (Fig. 2A, B), and a weak repulsion of Croton at 1.5 m from Dracaena (Fig. 2C). Similarly, except for a tendency to small-scale attraction at about 1 m, Dracaena trees and all other woody plants were independent at all other scales (Fig. 2D). 3.2. Understorey vs. open-site vegetation The plant species composition and its homogeneity under Dracaena trees significantly differed from those for open sites (adonis: R2 = 0.175, p b 0.01; betadisper: F = 10.552, p b 0.01), with the understorey being more heterogeneous (average distance to group median 0.4683) than the open site (average distance to median 0.4072). In accordance with the aforementioned, the visualization of NMDS clearly showed two distinct groups of plots (Fig. 3) with understorey plots being

much more scattered due to greater heterogeneity of the species composition. The species accumulation curves (SACs) revealed no difference in species richness up to accumulation of species around two Dracaena trees but revealed higher species richness in the understorey than in open site plots after following species accumulation of three and more trees. The average difference in species richness between understorey and open site plots became consistent (with constant curve slopes and distance) after pooling species from 10 trees (Fig. 4). The initial steep slope of understorey curve points to the higher beta diversity in the understorey and is concordant with the findings of the NMDS. SACs also revealed that the sampling effort was sufficient for characterizing the studied vegetation, as species richness neared an asymptote with increased sampling both in understorey and open sites (Fig. 4). There was no significant difference between the species abundance distributions in understorey and open site plots (D = 0.096, p = 0.905) (Fig. A2).

3.3. Understorey/open-site specialists and generalists In total, 92 species of vascular plants were recorded, 83 under and 60 outside Dracaena canopies. Among these species, 32 (34.8%) were found exclusively in the understorey, 9 (9.8%) exclusively in open sites, and 51 (55.4%) were common to both habitats. The multinomial species classification ranked 15 species (16.3%) as understorey specialists, 6 (6.5%) as open-site specialists, and 23 (25.0%) as generalists; 48 species (52.2%) were too rare to be classified (Table 2; Fig. A3). Among endemics, 7, 3 and 11 species were understorey specialists, open-site specialists and generalists, respectively. Both species richness and abundance of rare species, especially those that were endemics, was substantially higher in understorey than in open sites (Table 2).

3.4. The effect of canopy closure on species abundances, species richness and total abundance Canopy closure was higher in the understorey (mean value and standard deviation 48.2% ± 14.5%) than in open sites (13.2% ± 9.4%). It had significant effect on abundances of several species (Table A1) but its prevalent direction varied among species classes (Table 3, Fig. A4). The prevalent effect of canopy closure was positive on understorey specialists, only negative on open-site specialists and mostly neutral on generalists. The analysis of the effect of canopy closure on species richness and total abundance (all species without distinguishing between species classes) indicated the unimodal relationships (Fig. 5), as the second order polynomial models were both significant (p b 0.001). The highest species richness occurred with canopy closure value of 34%. Total abundance was highest with canopy closure at 29% (Fig. 5). These values of canopy closure supporting the highest levels of both species richness and total abundance were found exclusively in understorey, but on the lower end of the range of canopy closure, where understorey and open-site specialists can co-occur. At the higher end of the aforementioned range, few species and individuals were recorded (Fig. 5).

Table 1 The composition of woody species in Firmihin.

DBH ≥ 50 mm DBH ≥ 100 mm

Number of individuals Basal area (m2) Number of individuals Basal area (m2)

Dracaena cinnabari

Croton socotranus

Jatropha unicostata

Buxanthus pedicellatus

Other species

Total

125.9 (60.3%) 13.191 (97.3%) 125.9 (95.8%) 13.191 (99.0%)

48.5 (23.3%) 0.139 (1.0%) 0.7 (0.6%) 0.007 (0.1%)

16.7 (8.0%) 0.071 (0.5%) 1.7 (1.3%) 0.019 (0.1%)

12.0 (5.8%) 0.041 (0.3%) 0.5 (0.4%) 0.005 (0.0%)

5.5 (2.6%) 0.110 (0.8%) 2.5 (1.9%) 0.100 (0.8%)

208.6 (100%) 13.553 (100%) 131.3 (100%) 13.321 (100%)

Data given for 1 ha. Based on the examination of 34 circular sampling plots with 25 m radius (total area 6.68 ha).

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Fig. 2. Bivariate analyses of spatial associations between Dracaena cinnabari and A) Buxanthus pedicellatus, B) Jatropha unicostata, C) Croton socotranus, and D) all woody species. The x-axis shows a distance from an arbitrary Dracaena tree. Solid lines show joined pair correlation functions, i.e., weighted average statistics calculated from the functions of individual plots. The area between the simulation envelopes, representing the fifth smallest and largest values of the 199 simulations of the null model, is shown in grey. Values above and below the simulation envelopes indicate significant attraction and repulsion, respectively. Complete spatial randomness was used as a null model. The subscripts 1 and 2 refer to Dracaenas and the species stated above, respectively. The horizontal lines give the expected g12(r) function for independent patterns (g12(r) = 1).

4. Discussion Our results indicated that continuing Dracaena decline may impact not only the Dracaena itself but could also have an important negative effect on unique vascular plant diversity of Socotra Island and is likely to cause significant homogenization of vegetation. The decline will likely have particularly negative effects on understorey specialists, including endemic species, whose abundances may be substantially reduced to numbers now found in open sites (Table 2). We found not only the number of specialist species to be greater in understorey than in open sites, but also overall species richness (including a number of endemic and rare species) to be significantly higher in the understorey. Although the rare species could not be classified, their almost two times higher species richness and much greater abundance under Dracaena crowns (Table 2) indicate that Dracaena decline may have severe impact on them. In addition, it is likely that for some species occurring both

Fig. 3. NMDS ordination of open-site and understorey plots. Dashed lines denote boundaries of understorey and open-site plot clusters.

under and outside the Dracaena canopy, their understorey populations may be the principal seed sources that maintain their populations outside Dracaena understorey. Therefore, disappearance of the understorey populations could possibly lead to an overall decline of these species, particularly the rare and endemic ones, making them eventually even more vulnerable to extinction. Moreover, rare species may play an important role in maintaining ecosystem processes (Lyons et al., 2005; Mouillot et al., 2013), further emphasizing the importance of maintaining high proportions of rare plant species by conservation of Dracaena populations. The greater heterogeneity of species composition in understorey plots (greater beta diversity) could be explained by the wider range of

Fig. 4. Species accumulation curves for understorey and open site plots. The curves represent the mean value of species richness based on 100 permutations of the samples. Vertical bars show the standard deviation (SD).

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Table 2 The classification of species as habitat specialists or generalists, based on a multinomial model using estimated species relative abundance in two habitats. Number of individuals Species

Class

Understorey

Open site

Endemic

Acalypha indica Ageratum conyzoides Allophylus rubifoliusc Asystasia gangetica Blepharis maderaspatensis Dracaena cinnabaric Erucastrum rostratum Euryops arabicusb Hypoestes pubescens Oldenlandia balfourii Oxalis corniculata Pulicaria diversifolia Ruellia patula Trichodesma laxiflorum Withania adunensisb Convolvulus hildebrandtii Corchorus erodioides Endostemon tenuiflorus Euphorbia kischenensis Melhania muricataa Portulaca quadrifida Buxanthus pedicellatusb Commelina albescens Convolvulus sarmentosus Crotalaria leptocarpa Croton socotranusb Evolvulus alsinoides Exacum affine Glossonema revoili Helichrysum balfourii Hybanthus enneaspermusa Indigofera nephrocarpa Launaea crepoides Launaea socotrana Lavandula nimmoi Nanorrhinum hastatum Oldenlandia bicornuta Orthosiphon pallidus Phyllanthus maderaspatensis Polygala erioptera Rhinacanthus scoparius Sida ovataa Tephrosia odorata Trichocalyx orbiculatusb Rare endemics Rare non-endemics Rare unidentified Total endemics Total non-endemics Total unidentified All species

UND UND UND UND UND UND UND UND UND UND UND UND UND UND UND OPE OPE OPE OPE OPE OPE GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN GEN TR TR TR

159 66 28 72 22 30 53 72 701 104 67 561 102 44 18 62 289 78 89 129 1 223 36 42 54 40 13 532 5 1390 566 268 115 142 18 6 813 25 9 27 27 28 33 17 86 (18 species) 56 (15 species) 8 (6 species) 5206 2112 8 7326

33 0 2 0 0 2 4 0 34 23 0 49 22 4 1 311 657 648 214 443 24 83 10 102 111 15 6 187 13 1251 210 445 220 79 9 18 621 49 22 65 11 58 62 6 11 (6 species) 18 (10 species) 8 (5 species) 3873 2280 8 6161

No No No No No Yes Yes No Yes Yes No Yes No Yes Yes Yes Yes No Yes No No No No Yes No Yes No Yes No Yes No No Yes Yes Yes No Yes No No No Yes No Yes Yes

UND — understorey specialist, OPE — open-site specialist, GEN — generalist, TR — too rare to classify. a Subshrubs. b Shrubs (including shrub seedlings). c Tree seedlings.

Table 3 Frequency of positive, negative, and neutral relationships between canopy closure and species abundance within each species class and in total. Only species present in data for at least 10 Dracaena trees (under and around relevés pooled) were analysed, using generalised linear models (GLM) with a Poisson error distribution. Values represent the number of species with a given relationship in each species class (percentage of the relationship within each class is shown in parentheses). Canopy closure × abundance relationship Species class

Positive

Negative

Neutral

Understorey specialists Open-site specialists Generalists Total

4 (50%) 0 (0%) 3 (17%) 7 (23%)

1 (13%) 5 (100%) 3 (17%) 9 (29%)

3 (38%) 0 (0%) 12 (67%) 15 (48%)

environmental factors under the canopy, as we found the span of canopy closure above the understorey to be two times larger than in open sites. Our results showed how such a high degree of environmental heterogeneity provided by a single tree species may be utilized by other vascular plants. However, this important microscale environmental heterogeneity would be almost completely lost with the disappearance of Dracaena, as its replacement by other tree species is highly unlikely. We did not find any other abundant tree-sized species in the Socotra's largest Dracaena stand; the three most frequent woody species were sparse shrub-like individuals randomly distributed in understorey and open sites. The improbability of Dracaena being replaced by other tree species is also evident in Dracaena stands adjacent to Firmihin, where already widely scattered Dracaena trees (Attorre et al., 2007) have not been replaced by any species. The present study also confirms the lack of active regeneration of Dracaena in its most extensive stand in Firmihin (Adolt and Pavliš, 2004; Miller and Morris, 2004; Attorre et al., 2007; Hubálková, 2011; Adolt et al., 2012, 2013). In a total of 272 relevés, we captured only 32 seedlings of Dracaena (mostly below the canopy), all under several months in age. Furthermore, in sampling woody vegetation in a total area of almost 7 ha, not a single young Dracaena tree with DBH b 100 mm was found. This shows that while Dracaena is still capable of germination, though weakly, regeneration is not viable due to rapid mortality of newly emerged seedlings, likely due to either grazing or drought (Miller and Morris, 2004; Habrová and Pavliš, 2015). Thus, Dracaena's nursing effect, facilitating other plant species, is not sufficient for its own seedlings to thrive. Hypothetically, mature Dracaenas may have even a negative distance-dependent effect on mortality of conspecific seedlings as we found a significant negative relationship between canopy closure and the abundance of Dracaena seedlings. Due to the lack of available seedlings, we were not able to verify such effects. Further experimental research specifically designed to test for distance-dependent survival of seedlings while controlling for grazing and other factors will be necessary to explore this hypothesis. Grazing pressure is an important factor shaping plant communities (Milchunas and Lauenroth, 1993; Adler et al., 2001). Heavy grazing may override beneficial effects of trees on understorey vegetation and subsequently leads to the homogenization of vegetation (Belsky et al., 1993; Abule et al., 2005; Abdallah et al., 2012). Because the entirety of our study area has been subjected to long-term overgrazing (by goats, sheep and, to a lesser extent, by donkeys and camels), we assume that differences in species composition and richness between Dracaena understorey and open sites could be even greater under grazing exclusion. It is highly unlikely that grazing would have little or no effect on Socotra vegetation, because all but a few plant species found in our survey are livestock forage (Miller and Morris, 2004) and almost all individuals in our plots showed visible signs of heavy grazing. Furthermore, heavy grazing (combined with aridification) has also been identified as the most probable explanation for the lack of Dracaena regeneration (Brown and Mies, 2012; Habrová and Pavliš, 2015). While long-term drought is impossible to prevent, we see grazing exclusion as the most effective way to ensure survival of Dracaena seedlings and consequently, of the facilitated vegetation. We used Dracaena's canopy closure as readily measurable explanatory proxy variable and we expect it to show a positive correlation with other environmental variables directly affecting vegetation. The influence of Dracaena on the environment is most likely realized through its dense umbrella-shaped crown which provides shade and collects atmospheric humidity (Beyhl, 1996). D. cinnabari occurs mainly in areas with a south-western aspect (Attorre et al., 2007) affected by southwesterly summer monsoon which brings moisture resulting in fog formation (Scholte and De Geest, 2010). Measurements of fog-derived moisture on the Dixam plateau adjacent to Firmihin suggested that it may constitute up to two-thirds of total moisture (Scholte and De Geest, 2010) similar to values taken from seasonal cloud forests of the Dhofar mountains in Oman (Hildebrandt and Eltahir, 2006;

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Fig. 5. The effect of canopy closure on species richness and total abundance. Generalized linear models (GLM) with a Poisson error distribution were used. Both models were significant (p b 0.001).

Abdul-Wahab et al., 2009). Another process which might possibly contribute to providing moisture in Dracaena habitats, is hydraulic lift (Richards and Caldwell, 1987) through which water is drawn up by roots from moist deep soil layers and then exuded into the dry surface. Several previous studies on positive and negative plant interactions stressed the role of facilitation in resource-limited communities in which established plants mitigate environmental stress of their neighbours (Brooker and Callaghan, 1998; Lortie and Callaway, 2006; Brooker et al., 2008; Gómez-Aparicio, 2009; Martorell and Freckleton, 2014). In our study of a water-limited ecosystem with undeveloped soils, the prevalent effect of Dracaena was indeed positive, as a significantly greater proportion of vascular plant species found in Dracaena stands favoured the Dracaena understorey. Conversely, a smaller proportion of species tended to avoid the canopy and were more prolific in open sites. This indicates the species-specific role of Dracaena, as it facilitates most of the species present but supresses others, and thus further contributes to differences in plant species composition between habitats. Dracaena's impact on overall plant diversity is even more crucial as it is the only abundant tree in the studied area making it impossible for facilitated plants to find an alternate benefactor. Further reduction of Dracaena population will most probably lead to pronounced decline of these associated plants which will then be able to grow only in benign microhabitats such as rock cavities and clefts or in shaded areas among rocks and their populations will be substantially reduced. Our findings indicate that Dracaena acts on Socotra Island as an ecosystem engineer (Jones et al., 1997; Gilad et al., 2007), i.e., a key species that alters the abiotic environment, controls the availability of resources and facilitates the growth of other species. The loss of such a keystone species may result in the disappearance of entire communities (Jones et al., 1997; Stachowicz, 2001), which, unfortunately, may be the case on Socotra Island. 5. Conclusions Understanding biodiversity patterns and their fundamental processes is an essential part of nature conservation in that it allows us to focus conservation efforts, ultimately rendering them more effective. Our study showed that the possible extinction of D. cinnabari on Socotra Island (Adolt and Pavliš, 2004; Attorre et al., 2007; Habrová et al., 2009; Hubálková, 2011; Adolt et al., 2012, 2013) could have far reaching impacts beyond the mere disappearance of this unique tree species and could lead to the disappearance of habitats for a vast array of other herbaceous and woody plants. These findings highlight the importance of

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