- Email: [email protected]
Composition and diversity of herbaceous patches in woody vegetation: The effects of grazing, soil seed bank, patch spatial properties and scale
Flora 207 (2012) 310–317
Contents lists available at SciVerse ScienceDirect
Flora journal homepage: www.elsevier.de/flora
Composition and diversity of herbaceous patches in woody vegetation: The effects of grazing, soil seed bank, patch spatial properties and scale Har’el Agra a,∗ , Gidi Ne’eman b a b
Department of Evolutionary and Environmental Biology, Faculty of Natural Sciences, University of Haifa, Haifa 31905, Israel Department of Biology and Environment, Faculty of Natural Sciences, University of Haifa-Oranim, Tivon 36006, Israel
a r t i c l e
i n f o
Article history: Received 19 July 2011 Accepted 24 October 2011 Keywords: Canopy gaps Cattle grazing Israel Mediterranean maquis Plant diversity Shannon’s entropy
a b s t r a c t Herbaceous plants contribute much to plant diversity in Mediterranean-type ecosystems though mostly occupying relatively small patches within the dense woody vegetation. While studying species diversity in the herbaceous patches, we hypothesized that grazing, soil seed bank, and spatial properties of the patch affect plant diversity and composition at different spatial scales. The study site was in an LTER site located in the Mediterranean region in north Israel. We determined herbaceous species composition in: (1) randomly sampled quadrats in herbaceous patches in grazed and un-grazed plots; (2) soil seed bank samples taken from the same patches and germinated under optimal greenhouse conditions; (3) quadrats in the same patches sown with a homogenous mixture of local soil samples. Using GIS methods, we determined small-scale spatial characteristics of the herbaceous patches. Alpha and beta diversities were calculated at the patch and plot scales using Shannon’s entropy H. Grazing increased alpha diversity of local untreated seed bank samples but decreased alpha diversity of the artificial homogenous soil seed bank mixture at both patch and plot scales. Positive relation between alpha diversity and patch area was detected only under grazing. Grazing increased beta diversity in all three treatments at the patch scale. Grazing decreased the similarity in species composition between above-ground vegetation and soil seed bank. The results indicate that moderate cattle-grazing affects species diversity in the herbaceous patches within the dense maquis. This effect is scale-dependent, and interacts with the effects of soil seed bank and patch spatial-properties: without grazing soil seed bank plays a more important role than patch spatial properties, but under grazing the size and the accessibility of the patch are more important in the determination of herbaceous species composition. © 2012 Elsevier GmbH. All rights reserved.
Introduction Herbaceous plants typically occupy small, distinct patches within the dense woody maquis in Mediterranean-type ecosystems (diCastri et al., 1981). Herbaceous species are the main constituents of plant diversity in the Israeli flora (Naveh and Whittaker, 1979; Sternberg et al., 2000), where species richness and endemism are high (Médail and Quézel, 1999; Shmida, 1984). Under traditional agricultural practices, such as cutting and grazing, the Mediterranean maquis has evolved into a resilient biome with high plant and animal species richness (Naveh and Whittaker, 1979). In the absence of human intervention, natural succession turns this open and species-rich landscape into a close, dense, shady woody and species-poor landscape (Perevolotsky, 2005). Therefore, studying the responses of herbaceous plant diversity to cattle grazing, soil
∗ Corresponding author. E-mail addresses: [email protected] (H. Agra), [email protected] (G. Ne’eman). 0367-2530/$ – see front matter © 2012 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2011.10.009
seed bank composition and spatial characteristics of the patches at different spatial scales is crucial for the understanding of the mechanisms that determine this richness, and is important for planning and using sustainable grazing as a management tool for conservation of high biodiversity. In recent decades cattle-grazing has replaced traditional goat and sheep grazing in the woody Mediterranean region of Israel. Cattle grazing and its effect on plant species composition was studied mainly in grasslands of various biomes, including Mediterranean ecosystems (Dumont et al., 2011; Lavorel et al., 1999). However, its specific impact on the herbaceous component of the dense Mediterranean maquis got much less attention. In the absence, or under low grazing pressure, natural succession causes increase in tree cover on the expenses of open herbaceous patches (Carmel and Kadmon, 1999). In such systems cattle-grazing concentrates mainly in the open herbaceous patches (Gutman et al., 2000). Because of their high palatability, cattle grazing has a predominantly negative effect mainly on tall grasses that are generally dominant and highly competitive species (Sternberg et al., 2000), thus increasing the abundance of less competitive and rare plants. This process is
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317
accompanied by changes in the spatial distribution of plant species and their richness (Kohyani et al., 2011). The relative abundance and competition rate among the herbaceous plant species probably affects seed production and seed bank richness, which in interaction with biotic (e.g. grazing, granivory) and abiotic (e.g. water, light) factors determine species composition and richness in the open herbaceous gaps in the Mediterranean maquis (Sternberg et al., 2003). Soil seed bank, the pool of viable seeds, has been documented for many different types of plant communities; seed bank literature has recently increased considerably (Ma et al., 2010; Plue et al., 2010). Ecologists and evolutionary biologists have become increasingly aware of the role that seed banks can play in maintaining biodiversity in populations and communities, mainly under various disturbance regimes (Gross, 1990). Similarity between soil seed bank and standing vegetation has been studied frequently in different plant communities, aiming to improve understanding of the role of seed banks in succession and regeneration after disturbances as well as for rehabilitation programs. The similarity between seed bank and above-ground vegetation differs across habitats and environmental conditions (Egan and Unger, 2000; Esmailzadeh et al., 2011). Grazing was found to increase (Unger and Woodell, 1996), decrease (Chaideftou et al., 2009; Jutila, 1998) or have no effect (Peco et al., 1998) on the similarity between soil seed bank and above-ground vegetation. These contrasting patterns are probably due to differences in grazing regimes, environmental conditions and vegetation characteristics (Osem et al., 2006). In general, plant size, growth form, palatability and regeneration traits such as seed dormancy, seed and seedling size, play an important role in determining vegetation structure under different grazing regimes, thus contributing to the high plant species diversity of Mediterranean grasslands (Jacquemyn et al., 2011). Understanding the mechanisms controlling plant growth and diversity in canopy gaps is of major importance for sustainable biodiversity management programs. Species composition and richness of the herbaceous vegetation layer in near to natural beech forest in Germany, was determined by gap size, light availability and herbivory; generalist species use a persistent seed bank as well as transportation by ungulates, to colonize new gaps (Naaf and Wulf, 2007). Different environmental factors may act as major driving forces of diversity at different spatial scales, and the effect of any given factor may change at different scales. Kallimanis et al. (2008) found that the spatial pattern of diversity changed with observation scale or analysis, and that species richness (alpha diversity) was negatively correlated with the pattern of species turnover (beta diversity). Beta diversity in species-rich areas is lower as they have more species in common with their neighboring areas than speciespoor areas (Kallimanis et al., 2008). Alpha, beta, and gamma diversities are among the fundamental descriptive variables used in ecology and conservation biology (Jost, 2007; Whittaker, 1972; Wilson and Shmida, 1984). While alpha (local species richness) and gamma (regional species richness) are well defined, beta diversity, which reflects the turnover of species among samples, has several definitions and calculation modes. According to Jost (2007) Shannon measures are shown to be the only standard diversity measures that can be decomposed into meaningful independent alpha and beta components when community weights are unequal (Jost, 2007). Our aim was to study the determinants of herbaceous plant diversity in the open patches within the woody dense, evergreen sclerophyllous Mediterranean vegetation. To do so, we conducted a field experiment to determine herbaceous species composition in: (1) randomly sampled quadrats in small homogenous herbaceous patches in grazed and un-grazed plots; (2) soil seed bank samples taken from the same patches and germinated under
311
optimal greenhouse conditions; (3) quadrats in the same patches sown with a homogenous mixture of local soil seed bank samples, and examined the effects of cattle grazing, soil seed bank, and patch spatial properties on herbaceous plant diversity at the patch and plot scales. Our research questions were: (1) what is the effect of cattle grazing on alpha and beta diversities? (2) Is the effect scale dependent? (3) Which of the two factors, soil seed bank or patch spatial properties, is more important as determinants of plant diversity in the herbaceous patches? Our specific hypotheses were: (H1) A. Due to the selective feeding of the cows and consequent oppression of dominant palatable species grazing will positively affect species evenness which will increase alpha diversity both at the patch and plot scales. Grazing effects on local untreated seed banks that were determined under a long period of grazing in the patches is expected to be weaker than on a non-local soil seed bank sown in the patches. B. Patch area will have a positive effect on alpha diversity with no effect of grazing. (H2) A. Beta diversity will be negatively affected by cattle grazing both at the patch and plot scales due to selective feeding (which approximates similarity in species composition among patches). This effect is expected to be higher at the patch than the plot scale. Soil seed banks will have a stronger effect on beta diversity then patch spatial properties. B. Distance between patches will affect beta diversity with no effect of grazing. (H3) Grazing will have differential effects on the similarity in species composition inside the patches between our three treatments: natural above-ground vegetation, homogenous soil seed bank mixture growing in the natural patches, and natural soil seed bank from the patches growing in optimal greenhouse conditions. Materials and methods Study site Our research site was located on Mt. Tziv’on (35.25◦ E, 33.15◦ N), at the Mt. Meron Long-Term Ecological Research site, which was established as part of the Israeli LTER network, to study the effect of woody species as landscape modulators along the rainfall gradient in Israel (Agra and Ne’eman, 2009; Shachak et al., 2008). The site is located in northern Israel (35.25◦ E, 33.15◦ N), 850 m a.s.l., with mean annual precipitation of 900 mm, falling mainly during the short winter (December to February). The bedrock is limestone covered with terra-rossa soil. The vegetation forms a dense woody maquis, with small isolated herbaceous patches, most of which are annual plants that are green during winter and spring and dry in summer. Total vegetation cover at the site is ca. 95%, of which 60% are trees, mainly Quercus calliprinos (80% of tree cover) accompanied by Quercus boissieri, Pistacia palaestina, Crataegus aronia, and several other deciduous trees (Agra and Ne’eman, 2011). 15% of the cover is shrubs (e.g. Calicotome villosa, Rhamnus punctatus) 10% dwarf-shrubs (e.g. Sarcopoterium spinosum, Cistus creticus, Cistus salviifolius) and 10% herbaceous plants with the dominant grasses being Brachypodium distachyon, Bromus sterilis and Catapodium rigidum, and the dominant forbs Anagallis arvensis, Geranium robertianum, Sherardia arvensis, Hymenocarpos circinnatus, Trifolium campestre and Trifolium resupinatum. Since 1960 the area has been subjected to moderate cattle grazing with 0.3 cow ha−1 year−1 , a typical grazing intensity in such areas. Experimental design and procedure Five blocks of 2000 m2 were marked (November–December 2005) at the study site within an area of about 10 km2 ; each block was divided into two equal size plots, one plot was exposed to
312
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317
grazing livestock while one was wire-fenced and un-grazed. In summer 2009, three herbaceous patches in each plot, total of 30 herbaceous patches varying in their area from 0.5 to 15 m2 were selected for the experiment. Patches were selected to be homogenous so that the sampled quadrat will best represent the patch. Patches were well separated (distance of 5–15 m) from each other. Patches were marked on an aerial photo that was analyzed with GIS methods using ArcGIS® software, version 9 (2006) by Esri. We determined patches’ area and the distance between patches inside plots. To examine the effects of soil seed bank and grazing on the composition of the herbaceous vegetation, we applied three treatments: (1) we used an artificially homogenized mixture of soil samples containing the natural soil seed bank and germinated and grown under natural conditions (hereafter “HSB”) to examine the net effect of grazing and patch spatial-properties, neutralizing the natural variability in soil seed bank among patches. To create the HSB mixture we took soil seed bank samples (20 cm × 20 cm and 5 cm depth) from all 30 patches and mixed them together. In each patch, in grazed and un-grazed plots, we marked one quadrat of 400 cm2 with metal sticks, removed the top five centimeters of soil into a separate paper bag and filled up the empty space with an equal volume (2000 cm3 ) of the HSB mixture. To prevent arrival of naturally dispersed seeds, all HSB quadrats were covered with transparent plastic tape that was removed at the beginning of the growing season (November). (2) To examine the combined effects of grazing, patch spatial-properties, and the natural soil seed bank, we marked an additional 400 cm2 control quadrat (hereafter “CTL”) adjacent to the HSB quadrat in each of the 30 patches. (3) To examine the net effect of the natural variability in soil seed bank among patches, neutralizing the effect of patch spatial-properties and natural growing conditions, we germinated the original 2000 cm3 soil seed bank samples taken from each patch in 30 separate trays (30 cm × 20 cm × 5 cm) under optimal growing conditions (hereafter “OGC”) in the greenhouse at Oranim campus, with daily controlled irrigation and mild temperatures (18–28 ◦ C). In spring 2010 we determined the herbaceous species composition that germinated in all treatments. Plants were identified at peak season following Zohary and Feinbrun-Dothan (1966–1986), Feinbrun-Dothan and Danin (1991) and Danin (1998). The used nomenclature follows these floras.
model (SPSS 19: Mixed Models, Linear) using the block as our independent subject, and treatment and grazing as repeated factors (N = 5). Following our hypothesis (H1B) that alpha diversity at the patch scale will be positively related to patch area, we analyzed the relations between H of each patch and its area using one-tailed Pearson correlation tests (N = 15) for each treatment (HSB, OGC and CTL) and separately for grazed and for un-grazed patches. In cases where Pearson correlation was significant, we applied linear regression to test the dependence of H on patch area. To test our hypothesis (H2A) on the effects of grazing, treatment (CTL, OGC, and HSB) and their interactions on beta diversity at the patch and plot scales, we applied a repeated two-way ANOVA model (SPSS 19: Mixed Models, Linear) using the block as our independent subject, and treatment and grazing as repeated factors (N = 5). Following our hypothesis (H2B) that beta diversity at the patch scale (between-patches species turnover) will be positively related to the average distance between patches, to test the relation of beta diversity at the patch scale to distance between patches we applied one-tailed Pearson correlation tests between H beta and the average distance between the patches in the plot (N = 5) for each treatment (HSB, OGC and CTL) and separately for grazed and for un-grazed plots. We used Bray–Curtis distance index (BC) (Bray and Curtis, 1957) to determine dissimilarity in herbaceous species composition in patches among treatments (BCHSB–OGC , BCCTL–OGC and BCCTL–HSB ) in each plot. Following our hypothesis (H3) we examined the effects of grazing, treatment-couple (CTL–OGC, CTL–HSB and HSB–OGC), and their interactions on BC with a repeated two-way ANOVA model (SPSS 19: Mixed Models, Linear) using the block as our independent subject, and grazing and treatment-couple as repeated factors. To examine the different responses of grasses compared with forbs we applied repeated two-way ANOVA model (SPSS 19: Mixed Models, Linear) for the effects of grazing, treatment (CTL, OGC, and HSB) and their interactions on the abundance of grasses and forbs at the different treatments using the block as our independent subject, and treatment and grazing as repeated factors (N = 5). We used the block as the independent subject to compare the pooled data of the three patches in the un-grazed plot with the adjacent grazed plot.
Results Data analyses Following Jost (2007), we used Shannon entropy s
H=−
pi ln pi
i=1
where p is the proportion of a species i in the sample and s the number of species present in the sample, to determined alpha, and beta diversities (H alpha and H beta, respectively) for the patch and for the plot scales. At the patch scale, H alpha was determined as the average H (patch per plot) calculated for each single patch. At the plot scale, H alpha was calculated from the pooled data of all patches in the correspondent plot. H gamma at the patch scale equals H alpha of the correspondent plot scale. H gamma at the plot scale was calculated from the pooled data of all plots. At each scale we determined H beta as Hˇ = H − H˛
(Jost,2007)
Because treatments applied in the same block are not independent, to test our hypothesis (H1A) on the effects of grazing, treatment (CTL, OGC, and HSB) and their interactions on alpha diversity at the patch and plot scales, we applied a repeated two-way ANOVA
At both patch and plot scales alpha diversity was the highest in the homogenous seed bank (HSB) in un-grazed plots (Fig. 1A and B). ANOVA models showed significant effects of treatment (CTL, OGC or HSB) and of the interaction between treatment and grazing on alpha diversity at both the patch and plot scales (Table 1). The significant interaction is the result of higher alpha diversity in grazed than in un-grazed plots in the CTL and OGC treatments but the opposite in the HSB treatment. Alpha diversity was significantly and positively correlated with patch area, but only in the grazed CTL plots (r = 0.643, p(one-tailed) = 0.005). Patch area explained 37% of the variability in alpha diversity values of CTL in grazed plots (Fig. 1C). No differences between treatments were evident for beta diversity at the patch scale, while at the plot scale H beta was the lowest in HSB treatment (Fig. 2). ANOVA models showed a significant effect of grazing on H alpha at the patch but not at the plot scale, and a significant effect of treatment on H beta at the plot but not at the patch scale (Fig. 2, Table 2). No significant correlation was found between H beta and the average distance between patches in the plot for any of the treatments. The largest BC distance among treatments was between HSB and OGC. Because of the effect of grazing, decreasing BC distance between CTL and HSB and increasing BC between CTL and
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317
313
Fig. 1. (A) Alpha diversity (means ± SE) described by Shannon’s entropy (H alpha) in grazed and in ungrazed plots in three treatments: homogenous seed bank (HSB), optimal growing conditions (OGC) and control (CTL) at the patch scale (1–15 m2 ) (N = 5 for each column). (B) H alpha (means ± SE) in grazed and in un-grazed plots in HSB, OGC and CTL at the plot scale (1000 m2 ); N = 5 for each column. (C) Linear regression between H alpha at the patch scale and patch area for CTL in grazed plots (N = 15).
Table 1 Two-way ANOVA (SPSS 19: Mixed Models, Linear) testing the effects of treatment (CTL, HGC and HSB), cattle grazing and their interactions on alpha diversity described by Shannon’s entropy H (H alpha) at each of the two scales (patch and plot). Model’s covariance structure is listed for each variable. Significant effects are presented in bold. Covariance structure
Source
Numerator df
Denominator df
F
P
Treatment Grazing Treatment × grazing
2 1 2
10.02 11.74 10.02
18.800 1.349 6.307
<0.001 0.268 0.017
Treatment Grazing Treatment × grazing
2 1 2
8.00 8.00 8.00
14.261 0.727 5.075
0.002 0.419 0.038
H alpha patch Factor analytic – first order H alpha plot Unstructured
OGC, it is hard to tell which one is smaller (Fig. 3). The ANOVA model (first-order autoregressive covariance structure) showed a significant effect of treatment-couple (CTL–OGC, CTL–HSB and HSB–OGC) (F2,17.6 = 17.09, p < 0.001) and of the interaction between treatment-couple and grazing (F2,17.8 = 8.08, p = 0.003) on BC.
The abundance of grasses as well as forbs was higher at OGC treatment than at CTL and HSB. Without grazing at CTL and at OGC treatments the abundance of grasses was higher than the abundance of forbs. The abundance of grasses at CTL and at OGC was markedly lower under grazing (Fig. 4). The abundance of grasses
Fig. 2. (A) Beta diversity (means ± SE) described by Shannon’s entropy (H beta) in grazed and in un-grazed plots in three treatments: homogenous seed bank (HSB), optimal growing conditions (OGC) and control (CTL) at the patch scale (1–15 m2 ); N = 5 for each column. (B) H beta (means ± SE) in grazed and in un-grazed plots in HSB, OGC and CTL at the plot scale (1000 m2 ); N = 5 for each column.
314
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317
Table 2 Two-way ANOVA (SPSS 19: Mixed Models, Linear) testing the effects of treatment (CTL, HGC and HSB), cattle grazing and their interactions on beta diversity described by Shannon’s entropy H (H beta) at each of the two scales (patch and plot). Model’s covariance structure is listed for each variable. Significant effects are presented in bold. Covariance structure
Source
Numerator df
Denominator df
F
P
Treatment Grazing Treatment × grazing
2 1 2
13.62 17.80 13.62
0.226 4.489 0.005
0.800 0.048 0.995
Treatment Grazing Treatment × grazing
2 1 2
8.00 8.00 8.00
4.497 0.014 0.255
0.049 0.908 0.781
H beta patch Diagonal H beta plot Unstructured
Table 3 Two-way ANOVA (SPSS 19: Mixed Models, Linear) testing the effects of treatment (CTL, HGC and HSB), cattle grazing and their interactions on the abundance of (A) grasses and (B) forbs. Model’s covariance structure is listed for each variable. Significant effects are presented in bold. Covariance structure
Source
Numerator df
Denominator df
F
P
Treatment Grazing Treatment × grazing
2 1 2
5.59 7.10 5.99
14.807 21.075 8.966
0.006 0.002 0.018
Treatment Grazing Treatment × grazing
2 1 2
7.21 9.18 7.21
51.352 1.038 1.659
<0.001 0.334 0.255
(A) Grasses Diagonal (B) Forbs Diagonal
was affected by treatment and grazing as well as by their interactions while the abundance of forbs was only affected by the treatment (Table 3). Discussion Alpha diversity Grazing had an opposite effect on alpha diversity at the natural soil seed bank germinated in the field (CTL) and under optimal conditions in the greenhouse (OGC) compared with the homogenous seed bank (HSB) at both the patch and the plot scales. Alpha diversity was positively affected by grazing at CTL and OGC at both the patch and the plot scales, which agrees with studies that demonstrated a positive effect of grazing on diversity (Arevalo et al., 2011; Jacquemyn et al., 2011). At the OGC and CTL, grazing increases species evenness by decreasing the abundance of the palatable tall grasses that are sufficiently more abundant then the less palatable forbs (Fig. 4), and possibly increases diversity by facilitating import
of new species. In contrary, alpha diversity in the HSB treatment that was higher than at the OGC and CTL treatments, was negatively affected by grazing at the patch and the plot scales. It is because at HSB the palatable grasses were not pre-dominant (Fig. 4) and their elimination decreased the high alpha diversity (Fig. 1A and B), unlike at OGC and CTL where grasses were markedly more abundant. The results at the HSB treatment that were opposite to the similar results at the CTL and at the OGC treatments demonstrate the importance of the soil seed bank. The common convention, based on island biogeography theory (MacArthur and Wilson, 1967), holds that diversity is expected to be positively correlated with patch area regardless of grazing influence. Unlike our prediction (H1A), four years after cattle exclusion alpha diversity in the patches was positively correlated with patch area only in CTL treatment under grazing. A possible explanation is differential grazing pressure between small and large patches. According to optimal foraging theory, a cow grazing in a small patch is expected to spend less time (per unit area) before leaving for another patch, than when grazing in a large patch (Charnov, 1976). Low grazing pressure in the small patches is probably enough to eliminate the palatable species but not enough to affect the less palatable plants; but under higher grazing pressure in the large patches, the less palatable species are also consumed. This may also enable establishment of new species. In the absence of grazing, other characteristics of the patches (light intensity, soil depth, aspect, local water regime) probably play a more important role, so diversity is not dependent only on patch size as expected by the niche theory (Hutchinson, 1957).
Beta diversity
Fig. 3. Mean (±SE) Bray–Cutis (BC) distance in herbaceous species composition between treatments: homogenous seed bank (HSB), optimal growing conditions (OGC) and control (CTL) within patches for the three combinations of treatments: CTL–OGC, CTL–HSB and HSB–OGC. N = 5 for each column.
Contrary to our hypothesis (H2A) we found a positive effect of grazing on beta diversity at the patch scale that was similar in all treatments (HSB, OGC, and CTL). This was probably because of differences in grazing pressures among patches caused by accessibility differences due to distance from main walking routes, connectivity of open patches, or density of surrounding woody vegetation. As a result, grazing within the plots was heterogeneous, inducing a
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317
315
Fig. 4. Mean (±SE) abundance in 0.04 m2 squares of grasses and forbs in grazed and in un-grazed plots in three treatments: homogenous seed bank (HSB), optimal growing conditions (OGC) and control (CTL). N = 5 for each column.
consequent increase in the heterogeneity of the herbaceous vegetation (Adler et al., 2001). Grazing had no effect on beta diversity at the plot scale. Grazing pressure was not different among plots and our artificial HSB was similar and richer in species than the natural one. As result, beta diversity in HSB was lower than in OGC and CTL, whose soil seed banks were differently affected by local conditions at the different plots through the years, which partially supported our prediction (H2B). As oppose to our hypothesis (H2B) and to studies that found geographical distance a major determinant of beta diversity at large-scale (Chust et al., 2006), we found no relation between beta diversity and the average distance between patches at the small scale. Probably at our scale the size and the accessibility of the patches plays more important role than the absolute distance between patches. Soil seed bank vs. patch spatial properties Grazing decreased BC distance in species composition between CTL, representing above-ground vegetation, and HSB, representing a rich homogenous soil seed bank; grazing eliminates the more palatable species, making the HSB treatment more similar to the CTL, which is long affected by grazing. On the other hand, grazing increased BC distance between CTL and OGC. This result agrees with that of Chaideftou et al. (2009), who found that similarity between above-ground vegetation and seed bank in the grazed areas was lower than in the non-grazed areas. In support to our hypothesis (H3), without grazing species composition in CTL was more similar to OGC than to HSB while under grazing the situation was reversed (Fig. 3). Without grazing the local soil seed bank is the main factor determining species composition in the patch. Cattle grazing homogenized species composition inside the patches and decreased the effect of the soil seed bank, due to selective choice of patches, patch spatial properties became more important factors in determination of herbaceous species composition. Conclusions Moderate cattle grazing proved to have a significant effect on herbaceous plant diversity in the dense Mediterranean maquis. This effect was scale-dependent and interacted with the effects of soil seed bank and patch spatial properties. Grazing increased alpha diversity of actual local seed bank samples but decreased alpha diversity on homogenous soil seed bank at both patch and plot scales. This demonstrates the importance of the combined effect of
grazing and soil seed bank on herbaceous species diversity. On the other hand grazing increased beta diversity at the patch scale at all treatments but had no effect at the plot scale. We suggest that grazing may induce a positive relation between alpha diversity and the size of herbaceous patches. Our results show that without grazing soil seed bank plays a more important role than the spatial properties of the patch, but under grazing the size and the accessibility of the patch are more important in the determination of herbaceous species composition. Acknowledgments We thank the Israel Science Foundation and the Eshkol Fund, Israel Ministry of Science, for their financial support, the Nature and Park Authority for their permission to establish the LTER plots, A. Amitay for his help in establishing the research plots, M. Gross and the greenhouse staff at the botanical garden of Oranim, the University of Haifa for awarding a Ph.D. fellowship to H.A. and two anonymous reviewers for their comments. Appendix A. Alphabetic lists of herbaceous species Grasses (family Poaceae) Annuals Aegilops geniculata Aegilops peregrina Avena sterilis Brachypodium distachyon Briza maxima Bromus alopecuros Bromus brachystachys Bromus madritensis Bromus sterilis Catapodium rigidum Echinaria capitata Lolium rigidum Rostraria cristata Stipa capensis Vulpia muralis Vulpia myuros Perennials Brachypodium pinnatum Bromus syriacus Dactylis glomerata Hordeum bulbosum Piptatherum blancheanum Poa bulbosa
316
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317 Forbs
Forbs Species Annuals Alyssum simplex Anagallis arvensis Anthemis hebronica Anthemis palestina Aphanes arvensis Arabis verna Asperula arvensis Asterolinum linum-stellatum Astragalus epiglottis Biscutella didyma Bupleurum nodiflorum Capsella bursa-pastoris Carduus argentatus Carthamus tenuis Centaurea iberica Cerastium dubium Cerastium glomeratum Ceratocapnos turbinata Chaetosciadium trichospermum Coronilla cretica Coronilla repanda Coronilla scorpioides Crepis aspera Crepis sancta Crucianella macrostachya Crupina crupinastrum Erodium cicutarium Erodium malacoides Euphorbia aleppica Filago pyramidata Galium aparine Galium divaricatum Geranium molle Geranium robertianum Geropogon hybridus Hedypnois rhagadioloides Hippocrepis unisiliquosa Hirschfeldia incana Hymenocarpos circinnatus Inula viscosa Lactuca serriola Lathyrus aphaca Lathyrus marmoratus Lathyrus nissolia Lathyrus pseudocicera Legousia falcata Lens orientalis Linum corymbulosum Linum pubescens Linum strictum Lotus peregrinus Medicago coronata Medicago minima Medicago orbicularis Medicago polymorpha Medicago rotata Medicago rugosa Melilotus sulcatus Micropus supinus Minuartia hybrida Nonea obtusifolia Ochthodium aegyptiacum Onobrychis squarrosa Pimpinella cretica Pisum fulvum Plantago cretica Ranunculus chius Rapistrum rugosum Rhagadiolus edulis Salvia viridis Scandix pecten-veneris Scorpiurus muricatus Securigera securidaca Senecio vernalis Sherardia arvensis Silene aegyptiaca
Family Brassicaceae Primulaceae Asteraceae Asteraceae Rosaceae Brassicaceae Rubiaceae Primulaceae Fabaceae Brassicaceae Apiaceae Brassicaceae Asteraceae Asteraceae Asteraceae Caryophyllaceae Caryophyllaceae Fumariaceae Apiaceae Fabaceae Fabaceae Fabaceae Asteraceae Asteraceae Rubiaceae Asteraceae Geraniaceae Geraniaceae Euphorbiaceae Asteraceae Rubiaceae Rubiaceae Geraniaceae Geraniaceae Asteraceae Asteraceae Fabaceae Brassicaceae Fabaceae Asteraceae Asteraceae Fabaceae Fabaceae Fabaceae Fabaceae Campanulaceae Fabaceae Linaceae Linaceae Linaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Asteraceae Caryophyllaceae Boraginaceae Brassicaceae Fabaceae Apiaceae Fabaceae Plantaginaceae Ranunculaceae Brassicaceae Asteraceae Lamiaceae Apiaceae Fabaceae Fabaceae Asteraceae Rubiaceae Caryophyllaceae
Species
Family
Silene italica Silybum marianum Theligonum cynocrambe Thlaspi perfoliatum Torilis arvensis Torilis leptophylla Torilis tenella Trifolium campestre Trifolium cherleri Trifolium clypeatum Trifolium dasyurum Trifolium erubescens Trifolium glanduliferum Trifolium lappaceum Trifolium pilulare Trifolium plebeium Trifolium purpureum Trifolium resupinatum Trifolium scabrum Trifolium stellatum Urospermum picroides Valerianella coronata Valerianella muricata Veronica cymbalaria Veronica syriaca Vicia palaestina Vicia sativa Perennials Ajuga chamaepitys Allium neapolitanum Allium paniculatum Allium trifoliatum Asperula libanotica Bellevalia flexuosa Bituminaria bituminosa Cirsium phyllocephalum Colchicum hierosolymitanum Colchicum troodi Crepisreuteriana Cyclamen persicum Delphinium ithaburense Echinops adenocaulos Eryngium creticum Eryngium falcatum Feinbrunia speciosa Fibigia clypeata Gynandriris sisyrinchium Helichrysum sanguineum Lotus collinus Orchis anatolica Orchis galilaea Orchis papilionacea Ornithogalum narbonense Pimpinella peregrina Plantago lanceolata Ranunculus paludosus Salvia hierosolymitana Serratula cerinthifolia Symphytum brachycalyx Thrincia tuberosa Tragopogon coelesyriacus Veronica leiocarpa
Caryophyllaceae Asteraceae Theligonaceae Brassicaceae Apiaceae Apiaceae Apiaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Asteraceae Valerianaceae Valerianaceae Scrophulariaceae Scrophulariaceae Fabaceae Fabaceae Lamiaceae Liliaceae Liliaceae Liliaceae Rubiaceae Liliaceae Fabaceae Asteraceae Liliaceae Liliaceae Asteraceae Primulaceae Ranunculaceae Asteraceae Apiaceae Apiaceae Asteraceae Brassicaceae Iridaceae Asteraceae Fabaceae Orchidaceae Orchidaceae Orchidaceae Liliaceae Apiaceae Plantaginaceae Ranunculaceae Lamiaceae Asteraceae Boraginaceae Asteraceae Asteraceae Scrophulariaceae
References Agra, H., Ne’eman, G., 2009. Woody species as landscape modulators: their effect on the herbaceous plants in a Mediterranean maquis. Plant Ecol. 205, 165–177. Agra, H., Ne’eman, G., 2011. Quercus calliprinos regrowth advantage under grazing in Mediterranean maquis and its management implications. For. Ecol. Manage. 261, 143–147. Adler, P.B., Raff, D.A., Lauenroth, W.K., 2001. The effect of grazing on the spatial heterogeneity of vegetation. Oecologia 128, 465–479. Arevalo, J.R., de Nascimento, L., Fernandez-Lugo, S., Mata, J., Bermejo, L., 2011. Grazing effects on species composition in different vegetation types (La Palma, Canary Islands). Acta Oecol. 37, 230–238. Bray, J.R., Curtis, J.T., 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27, 325–349.
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317 Carmel, Y., Kadmon, R., 1999. Effects of grazing and topography on long-term vegetation changes in a Mediterranean ecosystem in Israel. Plant Ecol. 145, 243–254. Chaideftou, E., Thanos, C.A., Bergmeier, E., Kallimanis, A., Dimopoulus, P., 2009. Seed bank composition and above-ground vegetation in response to grazing in subMediterranean oak forests (NW Greece). Plant Ecol. 201, 255–265. Charnov, E.L., 1976. Optimal foraging, the marginal value theorem. Theor. Popul. Biol. 9, 129–137. Chust, G., Pérez-Haase, A., Chave, J., Pretus, J.L., 2006. Floristic patterns and plant traits of Mediterranean communities in fragmented habitats. J. Biogeogr 33, 1235–1245. Danin, A., 1998. Wild Plants of Eretz-Israel and Their Distribution. Carta, Jerusalem (in Hebrew). diCastri, F., Goodall, D.W., Specht, R. (Eds.), 1981. Mediterranean-type Shrublands. Elsevier, Amsterdam. Dumont, B., et al., 2011. Plant–herbivore interactions affect the initial direction of community changes in an ecosystem manipulation experiment. Basic Appl. Ecol. 12, 187–194. Egan, T.P., Unger, I.A., 2000. Similarity between seed bank and aboveground vegetation along a salinity gradient. J. Veg. Sci. 11, 189–194. Esmailzadeh, O., Hosseini, S.M., Tabari, M., Baskin, C.C., Asadi, H., 2011. Persistent soil seed banks and floristic diversity in Fagus orientalis forest communities in the Hyrcanian vegetation region of Iran. Flora 206, 365–372. Feinbrun-Dothan, N., Danin, A., 1991. Analytical Flora of Eretz-Israel. Cana, Jerusalem (in Hebrew). Gross, K.L., 1990. A comparison of methods for estimating seed numbers in the soil. J. Ecol. 78, 1079–1093. Gutman, M., Henkin, Z., Holzer, Z., Noy-Meir, I., Seligman, N.G., 2000. A case study of beef-cattle grazing in a Mediterranean-type woodland. Agroforest. Syst. 48, 119–140. Hutchinson, G.E., 1957. Concluding remarks. In: Cold Spring Harbor Symposium on Quant. Biol., vol. 22, pp. 415–427. Jacquemyn, H., Van Mechelen, C., Brys, R., Honnay, O., 2011. Management effects on the vegetation and soil seed bank of calcareous grasslands: an 11-year experiment. Biol. Conserv. 144, 416–422. Jost, L., 2007. Partitioning diversity into independent alpha and beta components. Ecology 88, 2427–2439. Jutila, H.M., 1998. Seed banks of grazed and ungrazed Baltic seashore meadows. J. Veg. Sci. 9, 395–408. Kallimanis, A.S., Halley, J.M., Vokou, D., Sgardelis, S.P., 2008. The scale of analysis determines the spatial pattern of woody species diversity in the Mediterranean environment. Plant Ecol. 196, 143–151. Kohyani, P.T., Bossuyt, B., Bonte, D., Hoffmann, M., 2011. Grazing impact on plant spatial distribution and community composition. Plant Ecol. Evol. 144, 19–28.
317
Lavorel, S., McIntyre, S., Grigulis, K., 1999. Plant response to disturbance in a Mediterranean grassland: how many functional groups? J. Veg. Sci. 10, 661–672. Ma, M., Zhou, X., Du, G., 2010. Role of soil seed bank along a disturbance gradient in an alpine meadow on the Tibet plateau. Flora 205, 128–134. MacArthur, R.H., Wilson, E.O., 1967. The Theory of Island Biogeography. Princeton University Press, Princeton. Médail, F., Quézel, P., 1999. Biodiversity hotspots in the Mediterranean basin: setting global conservation priorities. Conserv. Biol. 13, 1510–1513. Naaf, T., Wulf, M., 2007. Effects of gap size, light and herbivory on the herb layer vegetation in European beech forest gaps. For. Ecol. Manage. 244, 141–149. Naveh, Z., Whittaker, R.H., 1979. Structural and floristic diversity of shrublands and woodlands in northern Israel and other Mediterranean areas. Plant Ecol. 41, 171–190. Osem, Y., Perevolotsky, A., Kigel, J., 2006. Similarity between seed bank and vegetation in a semi-arid annual community: the role of productivity and grazing. J. Veg. Sci. 17, 29–36. Peco, B., Ortega, M., Levassor, C., 1998. Similarity between seed bank and vegetation in Mediterranean grassland: a predictive model. J. Veg. Sci. 9, 815–828. Perevolotsky, A., 2005. Integrating landscape ecology in the conservation of Mediterranean ecosystems: the Israeli experience. Israel J. Plant Sci. 53, 203–213. Plue, J., et al., 2010. Seed banks of temperate deciduous forests during secondary succession. J. Veg. Sci. 21, 965–978. Shachak, M., et al., 2008. Woody species as landscape modulators and their effect on biodiversity patterns. Bioscience 58, 209–221. Shmida, A., 1984. Endemism in the flora of Israel. Bot. Jahrb. Syst. Pflanzengesch. Pflanzengeogr. 104, 537–567. Sternberg, M., Gutman, M., Perevolotsky, A., Ungar, E.D., Kigel, J., 2000. Vegetation response to grazing management in a Mediterranean herbaceous community: a functional group approach. J. Appl. Ecol. 37, 224–237. Sternberg, M., Gutman, M., Perevolotsky, A., Kigel, J., 2003. Effects of grazing on soil seed bank dynamics: an approach with functional groups. J. Veg. Sci. 14, 375–386. Unger, I.A., Woodell, S.R.J., 1996. Similarity of seed bank to above ground vegetation in grazed and ungrazed salt marsh communities on the Gower Peninsula, South Wales. Int. J. Plant Sci. 157, 746–749. Whittaker, R.H., 1972. Evolution and measurement of species diversity. Taxon 21, 213–251. Wilson, M.V., Shmida, A., 1984. Measuring beta diversity with presence–absence data. J. Ecol. 72, 1055–1062. Zohary, M., Feinbrun-Dothan, N., 1966–1986. Flora Palaestina. The Israel Academy of Sciences and Humanities, Jerusalem.
Contents lists available at SciVerse ScienceDirect
Flora journal homepage: www.elsevier.de/flora
Composition and diversity of herbaceous patches in woody vegetation: The effects of grazing, soil seed bank, patch spatial properties and scale Har’el Agra a,∗ , Gidi Ne’eman b a b
Department of Evolutionary and Environmental Biology, Faculty of Natural Sciences, University of Haifa, Haifa 31905, Israel Department of Biology and Environment, Faculty of Natural Sciences, University of Haifa-Oranim, Tivon 36006, Israel
a r t i c l e
i n f o
Article history: Received 19 July 2011 Accepted 24 October 2011 Keywords: Canopy gaps Cattle grazing Israel Mediterranean maquis Plant diversity Shannon’s entropy
a b s t r a c t Herbaceous plants contribute much to plant diversity in Mediterranean-type ecosystems though mostly occupying relatively small patches within the dense woody vegetation. While studying species diversity in the herbaceous patches, we hypothesized that grazing, soil seed bank, and spatial properties of the patch affect plant diversity and composition at different spatial scales. The study site was in an LTER site located in the Mediterranean region in north Israel. We determined herbaceous species composition in: (1) randomly sampled quadrats in herbaceous patches in grazed and un-grazed plots; (2) soil seed bank samples taken from the same patches and germinated under optimal greenhouse conditions; (3) quadrats in the same patches sown with a homogenous mixture of local soil samples. Using GIS methods, we determined small-scale spatial characteristics of the herbaceous patches. Alpha and beta diversities were calculated at the patch and plot scales using Shannon’s entropy H. Grazing increased alpha diversity of local untreated seed bank samples but decreased alpha diversity of the artificial homogenous soil seed bank mixture at both patch and plot scales. Positive relation between alpha diversity and patch area was detected only under grazing. Grazing increased beta diversity in all three treatments at the patch scale. Grazing decreased the similarity in species composition between above-ground vegetation and soil seed bank. The results indicate that moderate cattle-grazing affects species diversity in the herbaceous patches within the dense maquis. This effect is scale-dependent, and interacts with the effects of soil seed bank and patch spatial-properties: without grazing soil seed bank plays a more important role than patch spatial properties, but under grazing the size and the accessibility of the patch are more important in the determination of herbaceous species composition. © 2012 Elsevier GmbH. All rights reserved.
Introduction Herbaceous plants typically occupy small, distinct patches within the dense woody maquis in Mediterranean-type ecosystems (diCastri et al., 1981). Herbaceous species are the main constituents of plant diversity in the Israeli flora (Naveh and Whittaker, 1979; Sternberg et al., 2000), where species richness and endemism are high (Médail and Quézel, 1999; Shmida, 1984). Under traditional agricultural practices, such as cutting and grazing, the Mediterranean maquis has evolved into a resilient biome with high plant and animal species richness (Naveh and Whittaker, 1979). In the absence of human intervention, natural succession turns this open and species-rich landscape into a close, dense, shady woody and species-poor landscape (Perevolotsky, 2005). Therefore, studying the responses of herbaceous plant diversity to cattle grazing, soil
∗ Corresponding author. E-mail addresses: [email protected] (H. Agra), [email protected] (G. Ne’eman). 0367-2530/$ – see front matter © 2012 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2011.10.009
seed bank composition and spatial characteristics of the patches at different spatial scales is crucial for the understanding of the mechanisms that determine this richness, and is important for planning and using sustainable grazing as a management tool for conservation of high biodiversity. In recent decades cattle-grazing has replaced traditional goat and sheep grazing in the woody Mediterranean region of Israel. Cattle grazing and its effect on plant species composition was studied mainly in grasslands of various biomes, including Mediterranean ecosystems (Dumont et al., 2011; Lavorel et al., 1999). However, its specific impact on the herbaceous component of the dense Mediterranean maquis got much less attention. In the absence, or under low grazing pressure, natural succession causes increase in tree cover on the expenses of open herbaceous patches (Carmel and Kadmon, 1999). In such systems cattle-grazing concentrates mainly in the open herbaceous patches (Gutman et al., 2000). Because of their high palatability, cattle grazing has a predominantly negative effect mainly on tall grasses that are generally dominant and highly competitive species (Sternberg et al., 2000), thus increasing the abundance of less competitive and rare plants. This process is
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317
accompanied by changes in the spatial distribution of plant species and their richness (Kohyani et al., 2011). The relative abundance and competition rate among the herbaceous plant species probably affects seed production and seed bank richness, which in interaction with biotic (e.g. grazing, granivory) and abiotic (e.g. water, light) factors determine species composition and richness in the open herbaceous gaps in the Mediterranean maquis (Sternberg et al., 2003). Soil seed bank, the pool of viable seeds, has been documented for many different types of plant communities; seed bank literature has recently increased considerably (Ma et al., 2010; Plue et al., 2010). Ecologists and evolutionary biologists have become increasingly aware of the role that seed banks can play in maintaining biodiversity in populations and communities, mainly under various disturbance regimes (Gross, 1990). Similarity between soil seed bank and standing vegetation has been studied frequently in different plant communities, aiming to improve understanding of the role of seed banks in succession and regeneration after disturbances as well as for rehabilitation programs. The similarity between seed bank and above-ground vegetation differs across habitats and environmental conditions (Egan and Unger, 2000; Esmailzadeh et al., 2011). Grazing was found to increase (Unger and Woodell, 1996), decrease (Chaideftou et al., 2009; Jutila, 1998) or have no effect (Peco et al., 1998) on the similarity between soil seed bank and above-ground vegetation. These contrasting patterns are probably due to differences in grazing regimes, environmental conditions and vegetation characteristics (Osem et al., 2006). In general, plant size, growth form, palatability and regeneration traits such as seed dormancy, seed and seedling size, play an important role in determining vegetation structure under different grazing regimes, thus contributing to the high plant species diversity of Mediterranean grasslands (Jacquemyn et al., 2011). Understanding the mechanisms controlling plant growth and diversity in canopy gaps is of major importance for sustainable biodiversity management programs. Species composition and richness of the herbaceous vegetation layer in near to natural beech forest in Germany, was determined by gap size, light availability and herbivory; generalist species use a persistent seed bank as well as transportation by ungulates, to colonize new gaps (Naaf and Wulf, 2007). Different environmental factors may act as major driving forces of diversity at different spatial scales, and the effect of any given factor may change at different scales. Kallimanis et al. (2008) found that the spatial pattern of diversity changed with observation scale or analysis, and that species richness (alpha diversity) was negatively correlated with the pattern of species turnover (beta diversity). Beta diversity in species-rich areas is lower as they have more species in common with their neighboring areas than speciespoor areas (Kallimanis et al., 2008). Alpha, beta, and gamma diversities are among the fundamental descriptive variables used in ecology and conservation biology (Jost, 2007; Whittaker, 1972; Wilson and Shmida, 1984). While alpha (local species richness) and gamma (regional species richness) are well defined, beta diversity, which reflects the turnover of species among samples, has several definitions and calculation modes. According to Jost (2007) Shannon measures are shown to be the only standard diversity measures that can be decomposed into meaningful independent alpha and beta components when community weights are unequal (Jost, 2007). Our aim was to study the determinants of herbaceous plant diversity in the open patches within the woody dense, evergreen sclerophyllous Mediterranean vegetation. To do so, we conducted a field experiment to determine herbaceous species composition in: (1) randomly sampled quadrats in small homogenous herbaceous patches in grazed and un-grazed plots; (2) soil seed bank samples taken from the same patches and germinated under
311
optimal greenhouse conditions; (3) quadrats in the same patches sown with a homogenous mixture of local soil seed bank samples, and examined the effects of cattle grazing, soil seed bank, and patch spatial properties on herbaceous plant diversity at the patch and plot scales. Our research questions were: (1) what is the effect of cattle grazing on alpha and beta diversities? (2) Is the effect scale dependent? (3) Which of the two factors, soil seed bank or patch spatial properties, is more important as determinants of plant diversity in the herbaceous patches? Our specific hypotheses were: (H1) A. Due to the selective feeding of the cows and consequent oppression of dominant palatable species grazing will positively affect species evenness which will increase alpha diversity both at the patch and plot scales. Grazing effects on local untreated seed banks that were determined under a long period of grazing in the patches is expected to be weaker than on a non-local soil seed bank sown in the patches. B. Patch area will have a positive effect on alpha diversity with no effect of grazing. (H2) A. Beta diversity will be negatively affected by cattle grazing both at the patch and plot scales due to selective feeding (which approximates similarity in species composition among patches). This effect is expected to be higher at the patch than the plot scale. Soil seed banks will have a stronger effect on beta diversity then patch spatial properties. B. Distance between patches will affect beta diversity with no effect of grazing. (H3) Grazing will have differential effects on the similarity in species composition inside the patches between our three treatments: natural above-ground vegetation, homogenous soil seed bank mixture growing in the natural patches, and natural soil seed bank from the patches growing in optimal greenhouse conditions. Materials and methods Study site Our research site was located on Mt. Tziv’on (35.25◦ E, 33.15◦ N), at the Mt. Meron Long-Term Ecological Research site, which was established as part of the Israeli LTER network, to study the effect of woody species as landscape modulators along the rainfall gradient in Israel (Agra and Ne’eman, 2009; Shachak et al., 2008). The site is located in northern Israel (35.25◦ E, 33.15◦ N), 850 m a.s.l., with mean annual precipitation of 900 mm, falling mainly during the short winter (December to February). The bedrock is limestone covered with terra-rossa soil. The vegetation forms a dense woody maquis, with small isolated herbaceous patches, most of which are annual plants that are green during winter and spring and dry in summer. Total vegetation cover at the site is ca. 95%, of which 60% are trees, mainly Quercus calliprinos (80% of tree cover) accompanied by Quercus boissieri, Pistacia palaestina, Crataegus aronia, and several other deciduous trees (Agra and Ne’eman, 2011). 15% of the cover is shrubs (e.g. Calicotome villosa, Rhamnus punctatus) 10% dwarf-shrubs (e.g. Sarcopoterium spinosum, Cistus creticus, Cistus salviifolius) and 10% herbaceous plants with the dominant grasses being Brachypodium distachyon, Bromus sterilis and Catapodium rigidum, and the dominant forbs Anagallis arvensis, Geranium robertianum, Sherardia arvensis, Hymenocarpos circinnatus, Trifolium campestre and Trifolium resupinatum. Since 1960 the area has been subjected to moderate cattle grazing with 0.3 cow ha−1 year−1 , a typical grazing intensity in such areas. Experimental design and procedure Five blocks of 2000 m2 were marked (November–December 2005) at the study site within an area of about 10 km2 ; each block was divided into two equal size plots, one plot was exposed to
312
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317
grazing livestock while one was wire-fenced and un-grazed. In summer 2009, three herbaceous patches in each plot, total of 30 herbaceous patches varying in their area from 0.5 to 15 m2 were selected for the experiment. Patches were selected to be homogenous so that the sampled quadrat will best represent the patch. Patches were well separated (distance of 5–15 m) from each other. Patches were marked on an aerial photo that was analyzed with GIS methods using ArcGIS® software, version 9 (2006) by Esri. We determined patches’ area and the distance between patches inside plots. To examine the effects of soil seed bank and grazing on the composition of the herbaceous vegetation, we applied three treatments: (1) we used an artificially homogenized mixture of soil samples containing the natural soil seed bank and germinated and grown under natural conditions (hereafter “HSB”) to examine the net effect of grazing and patch spatial-properties, neutralizing the natural variability in soil seed bank among patches. To create the HSB mixture we took soil seed bank samples (20 cm × 20 cm and 5 cm depth) from all 30 patches and mixed them together. In each patch, in grazed and un-grazed plots, we marked one quadrat of 400 cm2 with metal sticks, removed the top five centimeters of soil into a separate paper bag and filled up the empty space with an equal volume (2000 cm3 ) of the HSB mixture. To prevent arrival of naturally dispersed seeds, all HSB quadrats were covered with transparent plastic tape that was removed at the beginning of the growing season (November). (2) To examine the combined effects of grazing, patch spatial-properties, and the natural soil seed bank, we marked an additional 400 cm2 control quadrat (hereafter “CTL”) adjacent to the HSB quadrat in each of the 30 patches. (3) To examine the net effect of the natural variability in soil seed bank among patches, neutralizing the effect of patch spatial-properties and natural growing conditions, we germinated the original 2000 cm3 soil seed bank samples taken from each patch in 30 separate trays (30 cm × 20 cm × 5 cm) under optimal growing conditions (hereafter “OGC”) in the greenhouse at Oranim campus, with daily controlled irrigation and mild temperatures (18–28 ◦ C). In spring 2010 we determined the herbaceous species composition that germinated in all treatments. Plants were identified at peak season following Zohary and Feinbrun-Dothan (1966–1986), Feinbrun-Dothan and Danin (1991) and Danin (1998). The used nomenclature follows these floras.
model (SPSS 19: Mixed Models, Linear) using the block as our independent subject, and treatment and grazing as repeated factors (N = 5). Following our hypothesis (H1B) that alpha diversity at the patch scale will be positively related to patch area, we analyzed the relations between H of each patch and its area using one-tailed Pearson correlation tests (N = 15) for each treatment (HSB, OGC and CTL) and separately for grazed and for un-grazed patches. In cases where Pearson correlation was significant, we applied linear regression to test the dependence of H on patch area. To test our hypothesis (H2A) on the effects of grazing, treatment (CTL, OGC, and HSB) and their interactions on beta diversity at the patch and plot scales, we applied a repeated two-way ANOVA model (SPSS 19: Mixed Models, Linear) using the block as our independent subject, and treatment and grazing as repeated factors (N = 5). Following our hypothesis (H2B) that beta diversity at the patch scale (between-patches species turnover) will be positively related to the average distance between patches, to test the relation of beta diversity at the patch scale to distance between patches we applied one-tailed Pearson correlation tests between H beta and the average distance between the patches in the plot (N = 5) for each treatment (HSB, OGC and CTL) and separately for grazed and for un-grazed plots. We used Bray–Curtis distance index (BC) (Bray and Curtis, 1957) to determine dissimilarity in herbaceous species composition in patches among treatments (BCHSB–OGC , BCCTL–OGC and BCCTL–HSB ) in each plot. Following our hypothesis (H3) we examined the effects of grazing, treatment-couple (CTL–OGC, CTL–HSB and HSB–OGC), and their interactions on BC with a repeated two-way ANOVA model (SPSS 19: Mixed Models, Linear) using the block as our independent subject, and grazing and treatment-couple as repeated factors. To examine the different responses of grasses compared with forbs we applied repeated two-way ANOVA model (SPSS 19: Mixed Models, Linear) for the effects of grazing, treatment (CTL, OGC, and HSB) and their interactions on the abundance of grasses and forbs at the different treatments using the block as our independent subject, and treatment and grazing as repeated factors (N = 5). We used the block as the independent subject to compare the pooled data of the three patches in the un-grazed plot with the adjacent grazed plot.
Results Data analyses Following Jost (2007), we used Shannon entropy s
H=−
pi ln pi
i=1
where p is the proportion of a species i in the sample and s the number of species present in the sample, to determined alpha, and beta diversities (H alpha and H beta, respectively) for the patch and for the plot scales. At the patch scale, H alpha was determined as the average H (patch per plot) calculated for each single patch. At the plot scale, H alpha was calculated from the pooled data of all patches in the correspondent plot. H gamma at the patch scale equals H alpha of the correspondent plot scale. H gamma at the plot scale was calculated from the pooled data of all plots. At each scale we determined H beta as Hˇ = H − H˛
(Jost,2007)
Because treatments applied in the same block are not independent, to test our hypothesis (H1A) on the effects of grazing, treatment (CTL, OGC, and HSB) and their interactions on alpha diversity at the patch and plot scales, we applied a repeated two-way ANOVA
At both patch and plot scales alpha diversity was the highest in the homogenous seed bank (HSB) in un-grazed plots (Fig. 1A and B). ANOVA models showed significant effects of treatment (CTL, OGC or HSB) and of the interaction between treatment and grazing on alpha diversity at both the patch and plot scales (Table 1). The significant interaction is the result of higher alpha diversity in grazed than in un-grazed plots in the CTL and OGC treatments but the opposite in the HSB treatment. Alpha diversity was significantly and positively correlated with patch area, but only in the grazed CTL plots (r = 0.643, p(one-tailed) = 0.005). Patch area explained 37% of the variability in alpha diversity values of CTL in grazed plots (Fig. 1C). No differences between treatments were evident for beta diversity at the patch scale, while at the plot scale H beta was the lowest in HSB treatment (Fig. 2). ANOVA models showed a significant effect of grazing on H alpha at the patch but not at the plot scale, and a significant effect of treatment on H beta at the plot but not at the patch scale (Fig. 2, Table 2). No significant correlation was found between H beta and the average distance between patches in the plot for any of the treatments. The largest BC distance among treatments was between HSB and OGC. Because of the effect of grazing, decreasing BC distance between CTL and HSB and increasing BC between CTL and
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317
313
Fig. 1. (A) Alpha diversity (means ± SE) described by Shannon’s entropy (H alpha) in grazed and in ungrazed plots in three treatments: homogenous seed bank (HSB), optimal growing conditions (OGC) and control (CTL) at the patch scale (1–15 m2 ) (N = 5 for each column). (B) H alpha (means ± SE) in grazed and in un-grazed plots in HSB, OGC and CTL at the plot scale (1000 m2 ); N = 5 for each column. (C) Linear regression between H alpha at the patch scale and patch area for CTL in grazed plots (N = 15).
Table 1 Two-way ANOVA (SPSS 19: Mixed Models, Linear) testing the effects of treatment (CTL, HGC and HSB), cattle grazing and their interactions on alpha diversity described by Shannon’s entropy H (H alpha) at each of the two scales (patch and plot). Model’s covariance structure is listed for each variable. Significant effects are presented in bold. Covariance structure
Source
Numerator df
Denominator df
F
P
Treatment Grazing Treatment × grazing
2 1 2
10.02 11.74 10.02
18.800 1.349 6.307
<0.001 0.268 0.017
Treatment Grazing Treatment × grazing
2 1 2
8.00 8.00 8.00
14.261 0.727 5.075
0.002 0.419 0.038
H alpha patch Factor analytic – first order H alpha plot Unstructured
OGC, it is hard to tell which one is smaller (Fig. 3). The ANOVA model (first-order autoregressive covariance structure) showed a significant effect of treatment-couple (CTL–OGC, CTL–HSB and HSB–OGC) (F2,17.6 = 17.09, p < 0.001) and of the interaction between treatment-couple and grazing (F2,17.8 = 8.08, p = 0.003) on BC.
The abundance of grasses as well as forbs was higher at OGC treatment than at CTL and HSB. Without grazing at CTL and at OGC treatments the abundance of grasses was higher than the abundance of forbs. The abundance of grasses at CTL and at OGC was markedly lower under grazing (Fig. 4). The abundance of grasses
Fig. 2. (A) Beta diversity (means ± SE) described by Shannon’s entropy (H beta) in grazed and in un-grazed plots in three treatments: homogenous seed bank (HSB), optimal growing conditions (OGC) and control (CTL) at the patch scale (1–15 m2 ); N = 5 for each column. (B) H beta (means ± SE) in grazed and in un-grazed plots in HSB, OGC and CTL at the plot scale (1000 m2 ); N = 5 for each column.
314
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317
Table 2 Two-way ANOVA (SPSS 19: Mixed Models, Linear) testing the effects of treatment (CTL, HGC and HSB), cattle grazing and their interactions on beta diversity described by Shannon’s entropy H (H beta) at each of the two scales (patch and plot). Model’s covariance structure is listed for each variable. Significant effects are presented in bold. Covariance structure
Source
Numerator df
Denominator df
F
P
Treatment Grazing Treatment × grazing
2 1 2
13.62 17.80 13.62
0.226 4.489 0.005
0.800 0.048 0.995
Treatment Grazing Treatment × grazing
2 1 2
8.00 8.00 8.00
4.497 0.014 0.255
0.049 0.908 0.781
H beta patch Diagonal H beta plot Unstructured
Table 3 Two-way ANOVA (SPSS 19: Mixed Models, Linear) testing the effects of treatment (CTL, HGC and HSB), cattle grazing and their interactions on the abundance of (A) grasses and (B) forbs. Model’s covariance structure is listed for each variable. Significant effects are presented in bold. Covariance structure
Source
Numerator df
Denominator df
F
P
Treatment Grazing Treatment × grazing
2 1 2
5.59 7.10 5.99
14.807 21.075 8.966
0.006 0.002 0.018
Treatment Grazing Treatment × grazing
2 1 2
7.21 9.18 7.21
51.352 1.038 1.659
<0.001 0.334 0.255
(A) Grasses Diagonal (B) Forbs Diagonal
was affected by treatment and grazing as well as by their interactions while the abundance of forbs was only affected by the treatment (Table 3). Discussion Alpha diversity Grazing had an opposite effect on alpha diversity at the natural soil seed bank germinated in the field (CTL) and under optimal conditions in the greenhouse (OGC) compared with the homogenous seed bank (HSB) at both the patch and the plot scales. Alpha diversity was positively affected by grazing at CTL and OGC at both the patch and the plot scales, which agrees with studies that demonstrated a positive effect of grazing on diversity (Arevalo et al., 2011; Jacquemyn et al., 2011). At the OGC and CTL, grazing increases species evenness by decreasing the abundance of the palatable tall grasses that are sufficiently more abundant then the less palatable forbs (Fig. 4), and possibly increases diversity by facilitating import
of new species. In contrary, alpha diversity in the HSB treatment that was higher than at the OGC and CTL treatments, was negatively affected by grazing at the patch and the plot scales. It is because at HSB the palatable grasses were not pre-dominant (Fig. 4) and their elimination decreased the high alpha diversity (Fig. 1A and B), unlike at OGC and CTL where grasses were markedly more abundant. The results at the HSB treatment that were opposite to the similar results at the CTL and at the OGC treatments demonstrate the importance of the soil seed bank. The common convention, based on island biogeography theory (MacArthur and Wilson, 1967), holds that diversity is expected to be positively correlated with patch area regardless of grazing influence. Unlike our prediction (H1A), four years after cattle exclusion alpha diversity in the patches was positively correlated with patch area only in CTL treatment under grazing. A possible explanation is differential grazing pressure between small and large patches. According to optimal foraging theory, a cow grazing in a small patch is expected to spend less time (per unit area) before leaving for another patch, than when grazing in a large patch (Charnov, 1976). Low grazing pressure in the small patches is probably enough to eliminate the palatable species but not enough to affect the less palatable plants; but under higher grazing pressure in the large patches, the less palatable species are also consumed. This may also enable establishment of new species. In the absence of grazing, other characteristics of the patches (light intensity, soil depth, aspect, local water regime) probably play a more important role, so diversity is not dependent only on patch size as expected by the niche theory (Hutchinson, 1957).
Beta diversity
Fig. 3. Mean (±SE) Bray–Cutis (BC) distance in herbaceous species composition between treatments: homogenous seed bank (HSB), optimal growing conditions (OGC) and control (CTL) within patches for the three combinations of treatments: CTL–OGC, CTL–HSB and HSB–OGC. N = 5 for each column.
Contrary to our hypothesis (H2A) we found a positive effect of grazing on beta diversity at the patch scale that was similar in all treatments (HSB, OGC, and CTL). This was probably because of differences in grazing pressures among patches caused by accessibility differences due to distance from main walking routes, connectivity of open patches, or density of surrounding woody vegetation. As a result, grazing within the plots was heterogeneous, inducing a
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317
315
Fig. 4. Mean (±SE) abundance in 0.04 m2 squares of grasses and forbs in grazed and in un-grazed plots in three treatments: homogenous seed bank (HSB), optimal growing conditions (OGC) and control (CTL). N = 5 for each column.
consequent increase in the heterogeneity of the herbaceous vegetation (Adler et al., 2001). Grazing had no effect on beta diversity at the plot scale. Grazing pressure was not different among plots and our artificial HSB was similar and richer in species than the natural one. As result, beta diversity in HSB was lower than in OGC and CTL, whose soil seed banks were differently affected by local conditions at the different plots through the years, which partially supported our prediction (H2B). As oppose to our hypothesis (H2B) and to studies that found geographical distance a major determinant of beta diversity at large-scale (Chust et al., 2006), we found no relation between beta diversity and the average distance between patches at the small scale. Probably at our scale the size and the accessibility of the patches plays more important role than the absolute distance between patches. Soil seed bank vs. patch spatial properties Grazing decreased BC distance in species composition between CTL, representing above-ground vegetation, and HSB, representing a rich homogenous soil seed bank; grazing eliminates the more palatable species, making the HSB treatment more similar to the CTL, which is long affected by grazing. On the other hand, grazing increased BC distance between CTL and OGC. This result agrees with that of Chaideftou et al. (2009), who found that similarity between above-ground vegetation and seed bank in the grazed areas was lower than in the non-grazed areas. In support to our hypothesis (H3), without grazing species composition in CTL was more similar to OGC than to HSB while under grazing the situation was reversed (Fig. 3). Without grazing the local soil seed bank is the main factor determining species composition in the patch. Cattle grazing homogenized species composition inside the patches and decreased the effect of the soil seed bank, due to selective choice of patches, patch spatial properties became more important factors in determination of herbaceous species composition. Conclusions Moderate cattle grazing proved to have a significant effect on herbaceous plant diversity in the dense Mediterranean maquis. This effect was scale-dependent and interacted with the effects of soil seed bank and patch spatial properties. Grazing increased alpha diversity of actual local seed bank samples but decreased alpha diversity on homogenous soil seed bank at both patch and plot scales. This demonstrates the importance of the combined effect of
grazing and soil seed bank on herbaceous species diversity. On the other hand grazing increased beta diversity at the patch scale at all treatments but had no effect at the plot scale. We suggest that grazing may induce a positive relation between alpha diversity and the size of herbaceous patches. Our results show that without grazing soil seed bank plays a more important role than the spatial properties of the patch, but under grazing the size and the accessibility of the patch are more important in the determination of herbaceous species composition. Acknowledgments We thank the Israel Science Foundation and the Eshkol Fund, Israel Ministry of Science, for their financial support, the Nature and Park Authority for their permission to establish the LTER plots, A. Amitay for his help in establishing the research plots, M. Gross and the greenhouse staff at the botanical garden of Oranim, the University of Haifa for awarding a Ph.D. fellowship to H.A. and two anonymous reviewers for their comments. Appendix A. Alphabetic lists of herbaceous species Grasses (family Poaceae) Annuals Aegilops geniculata Aegilops peregrina Avena sterilis Brachypodium distachyon Briza maxima Bromus alopecuros Bromus brachystachys Bromus madritensis Bromus sterilis Catapodium rigidum Echinaria capitata Lolium rigidum Rostraria cristata Stipa capensis Vulpia muralis Vulpia myuros Perennials Brachypodium pinnatum Bromus syriacus Dactylis glomerata Hordeum bulbosum Piptatherum blancheanum Poa bulbosa
316
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317 Forbs
Forbs Species Annuals Alyssum simplex Anagallis arvensis Anthemis hebronica Anthemis palestina Aphanes arvensis Arabis verna Asperula arvensis Asterolinum linum-stellatum Astragalus epiglottis Biscutella didyma Bupleurum nodiflorum Capsella bursa-pastoris Carduus argentatus Carthamus tenuis Centaurea iberica Cerastium dubium Cerastium glomeratum Ceratocapnos turbinata Chaetosciadium trichospermum Coronilla cretica Coronilla repanda Coronilla scorpioides Crepis aspera Crepis sancta Crucianella macrostachya Crupina crupinastrum Erodium cicutarium Erodium malacoides Euphorbia aleppica Filago pyramidata Galium aparine Galium divaricatum Geranium molle Geranium robertianum Geropogon hybridus Hedypnois rhagadioloides Hippocrepis unisiliquosa Hirschfeldia incana Hymenocarpos circinnatus Inula viscosa Lactuca serriola Lathyrus aphaca Lathyrus marmoratus Lathyrus nissolia Lathyrus pseudocicera Legousia falcata Lens orientalis Linum corymbulosum Linum pubescens Linum strictum Lotus peregrinus Medicago coronata Medicago minima Medicago orbicularis Medicago polymorpha Medicago rotata Medicago rugosa Melilotus sulcatus Micropus supinus Minuartia hybrida Nonea obtusifolia Ochthodium aegyptiacum Onobrychis squarrosa Pimpinella cretica Pisum fulvum Plantago cretica Ranunculus chius Rapistrum rugosum Rhagadiolus edulis Salvia viridis Scandix pecten-veneris Scorpiurus muricatus Securigera securidaca Senecio vernalis Sherardia arvensis Silene aegyptiaca
Family Brassicaceae Primulaceae Asteraceae Asteraceae Rosaceae Brassicaceae Rubiaceae Primulaceae Fabaceae Brassicaceae Apiaceae Brassicaceae Asteraceae Asteraceae Asteraceae Caryophyllaceae Caryophyllaceae Fumariaceae Apiaceae Fabaceae Fabaceae Fabaceae Asteraceae Asteraceae Rubiaceae Asteraceae Geraniaceae Geraniaceae Euphorbiaceae Asteraceae Rubiaceae Rubiaceae Geraniaceae Geraniaceae Asteraceae Asteraceae Fabaceae Brassicaceae Fabaceae Asteraceae Asteraceae Fabaceae Fabaceae Fabaceae Fabaceae Campanulaceae Fabaceae Linaceae Linaceae Linaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Asteraceae Caryophyllaceae Boraginaceae Brassicaceae Fabaceae Apiaceae Fabaceae Plantaginaceae Ranunculaceae Brassicaceae Asteraceae Lamiaceae Apiaceae Fabaceae Fabaceae Asteraceae Rubiaceae Caryophyllaceae
Species
Family
Silene italica Silybum marianum Theligonum cynocrambe Thlaspi perfoliatum Torilis arvensis Torilis leptophylla Torilis tenella Trifolium campestre Trifolium cherleri Trifolium clypeatum Trifolium dasyurum Trifolium erubescens Trifolium glanduliferum Trifolium lappaceum Trifolium pilulare Trifolium plebeium Trifolium purpureum Trifolium resupinatum Trifolium scabrum Trifolium stellatum Urospermum picroides Valerianella coronata Valerianella muricata Veronica cymbalaria Veronica syriaca Vicia palaestina Vicia sativa Perennials Ajuga chamaepitys Allium neapolitanum Allium paniculatum Allium trifoliatum Asperula libanotica Bellevalia flexuosa Bituminaria bituminosa Cirsium phyllocephalum Colchicum hierosolymitanum Colchicum troodi Crepisreuteriana Cyclamen persicum Delphinium ithaburense Echinops adenocaulos Eryngium creticum Eryngium falcatum Feinbrunia speciosa Fibigia clypeata Gynandriris sisyrinchium Helichrysum sanguineum Lotus collinus Orchis anatolica Orchis galilaea Orchis papilionacea Ornithogalum narbonense Pimpinella peregrina Plantago lanceolata Ranunculus paludosus Salvia hierosolymitana Serratula cerinthifolia Symphytum brachycalyx Thrincia tuberosa Tragopogon coelesyriacus Veronica leiocarpa
Caryophyllaceae Asteraceae Theligonaceae Brassicaceae Apiaceae Apiaceae Apiaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Asteraceae Valerianaceae Valerianaceae Scrophulariaceae Scrophulariaceae Fabaceae Fabaceae Lamiaceae Liliaceae Liliaceae Liliaceae Rubiaceae Liliaceae Fabaceae Asteraceae Liliaceae Liliaceae Asteraceae Primulaceae Ranunculaceae Asteraceae Apiaceae Apiaceae Asteraceae Brassicaceae Iridaceae Asteraceae Fabaceae Orchidaceae Orchidaceae Orchidaceae Liliaceae Apiaceae Plantaginaceae Ranunculaceae Lamiaceae Asteraceae Boraginaceae Asteraceae Asteraceae Scrophulariaceae
References Agra, H., Ne’eman, G., 2009. Woody species as landscape modulators: their effect on the herbaceous plants in a Mediterranean maquis. Plant Ecol. 205, 165–177. Agra, H., Ne’eman, G., 2011. Quercus calliprinos regrowth advantage under grazing in Mediterranean maquis and its management implications. For. Ecol. Manage. 261, 143–147. Adler, P.B., Raff, D.A., Lauenroth, W.K., 2001. The effect of grazing on the spatial heterogeneity of vegetation. Oecologia 128, 465–479. Arevalo, J.R., de Nascimento, L., Fernandez-Lugo, S., Mata, J., Bermejo, L., 2011. Grazing effects on species composition in different vegetation types (La Palma, Canary Islands). Acta Oecol. 37, 230–238. Bray, J.R., Curtis, J.T., 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27, 325–349.
H. Agra, G. Ne’eman / Flora 207 (2012) 310–317 Carmel, Y., Kadmon, R., 1999. Effects of grazing and topography on long-term vegetation changes in a Mediterranean ecosystem in Israel. Plant Ecol. 145, 243–254. Chaideftou, E., Thanos, C.A., Bergmeier, E., Kallimanis, A., Dimopoulus, P., 2009. Seed bank composition and above-ground vegetation in response to grazing in subMediterranean oak forests (NW Greece). Plant Ecol. 201, 255–265. Charnov, E.L., 1976. Optimal foraging, the marginal value theorem. Theor. Popul. Biol. 9, 129–137. Chust, G., Pérez-Haase, A., Chave, J., Pretus, J.L., 2006. Floristic patterns and plant traits of Mediterranean communities in fragmented habitats. J. Biogeogr 33, 1235–1245. Danin, A., 1998. Wild Plants of Eretz-Israel and Their Distribution. Carta, Jerusalem (in Hebrew). diCastri, F., Goodall, D.W., Specht, R. (Eds.), 1981. Mediterranean-type Shrublands. Elsevier, Amsterdam. Dumont, B., et al., 2011. Plant–herbivore interactions affect the initial direction of community changes in an ecosystem manipulation experiment. Basic Appl. Ecol. 12, 187–194. Egan, T.P., Unger, I.A., 2000. Similarity between seed bank and aboveground vegetation along a salinity gradient. J. Veg. Sci. 11, 189–194. Esmailzadeh, O., Hosseini, S.M., Tabari, M., Baskin, C.C., Asadi, H., 2011. Persistent soil seed banks and floristic diversity in Fagus orientalis forest communities in the Hyrcanian vegetation region of Iran. Flora 206, 365–372. Feinbrun-Dothan, N., Danin, A., 1991. Analytical Flora of Eretz-Israel. Cana, Jerusalem (in Hebrew). Gross, K.L., 1990. A comparison of methods for estimating seed numbers in the soil. J. Ecol. 78, 1079–1093. Gutman, M., Henkin, Z., Holzer, Z., Noy-Meir, I., Seligman, N.G., 2000. A case study of beef-cattle grazing in a Mediterranean-type woodland. Agroforest. Syst. 48, 119–140. Hutchinson, G.E., 1957. Concluding remarks. In: Cold Spring Harbor Symposium on Quant. Biol., vol. 22, pp. 415–427. Jacquemyn, H., Van Mechelen, C., Brys, R., Honnay, O., 2011. Management effects on the vegetation and soil seed bank of calcareous grasslands: an 11-year experiment. Biol. Conserv. 144, 416–422. Jost, L., 2007. Partitioning diversity into independent alpha and beta components. Ecology 88, 2427–2439. Jutila, H.M., 1998. Seed banks of grazed and ungrazed Baltic seashore meadows. J. Veg. Sci. 9, 395–408. Kallimanis, A.S., Halley, J.M., Vokou, D., Sgardelis, S.P., 2008. The scale of analysis determines the spatial pattern of woody species diversity in the Mediterranean environment. Plant Ecol. 196, 143–151. Kohyani, P.T., Bossuyt, B., Bonte, D., Hoffmann, M., 2011. Grazing impact on plant spatial distribution and community composition. Plant Ecol. Evol. 144, 19–28.
317
Lavorel, S., McIntyre, S., Grigulis, K., 1999. Plant response to disturbance in a Mediterranean grassland: how many functional groups? J. Veg. Sci. 10, 661–672. Ma, M., Zhou, X., Du, G., 2010. Role of soil seed bank along a disturbance gradient in an alpine meadow on the Tibet plateau. Flora 205, 128–134. MacArthur, R.H., Wilson, E.O., 1967. The Theory of Island Biogeography. Princeton University Press, Princeton. Médail, F., Quézel, P., 1999. Biodiversity hotspots in the Mediterranean basin: setting global conservation priorities. Conserv. Biol. 13, 1510–1513. Naaf, T., Wulf, M., 2007. Effects of gap size, light and herbivory on the herb layer vegetation in European beech forest gaps. For. Ecol. Manage. 244, 141–149. Naveh, Z., Whittaker, R.H., 1979. Structural and floristic diversity of shrublands and woodlands in northern Israel and other Mediterranean areas. Plant Ecol. 41, 171–190. Osem, Y., Perevolotsky, A., Kigel, J., 2006. Similarity between seed bank and vegetation in a semi-arid annual community: the role of productivity and grazing. J. Veg. Sci. 17, 29–36. Peco, B., Ortega, M., Levassor, C., 1998. Similarity between seed bank and vegetation in Mediterranean grassland: a predictive model. J. Veg. Sci. 9, 815–828. Perevolotsky, A., 2005. Integrating landscape ecology in the conservation of Mediterranean ecosystems: the Israeli experience. Israel J. Plant Sci. 53, 203–213. Plue, J., et al., 2010. Seed banks of temperate deciduous forests during secondary succession. J. Veg. Sci. 21, 965–978. Shachak, M., et al., 2008. Woody species as landscape modulators and their effect on biodiversity patterns. Bioscience 58, 209–221. Shmida, A., 1984. Endemism in the flora of Israel. Bot. Jahrb. Syst. Pflanzengesch. Pflanzengeogr. 104, 537–567. Sternberg, M., Gutman, M., Perevolotsky, A., Ungar, E.D., Kigel, J., 2000. Vegetation response to grazing management in a Mediterranean herbaceous community: a functional group approach. J. Appl. Ecol. 37, 224–237. Sternberg, M., Gutman, M., Perevolotsky, A., Kigel, J., 2003. Effects of grazing on soil seed bank dynamics: an approach with functional groups. J. Veg. Sci. 14, 375–386. Unger, I.A., Woodell, S.R.J., 1996. Similarity of seed bank to above ground vegetation in grazed and ungrazed salt marsh communities on the Gower Peninsula, South Wales. Int. J. Plant Sci. 157, 746–749. Whittaker, R.H., 1972. Evolution and measurement of species diversity. Taxon 21, 213–251. Wilson, M.V., Shmida, A., 1984. Measuring beta diversity with presence–absence data. J. Ecol. 72, 1055–1062. Zohary, M., Feinbrun-Dothan, N., 1966–1986. Flora Palaestina. The Israel Academy of Sciences and Humanities, Jerusalem.