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Plant Biosystems - An International Journal Dealingwith all Aspects of Plant Biology: Official Journal of theSocieta Botanica ItalianaPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/tplb20

Human trampling effects on Mediterranean coastaldune plantsE. Farrisa, S. Pisanua, G. Ceccherellia & R. Filigheddua

a Dipartimento di Scienze della Natura e del Territorio, Università di Sassari, Sassari, ItalyAccepted author version posted online: 04 Nov 2013.Published online: 27 Nov 2013.

To cite this article: E. Farris, S. Pisanu, G. Ceccherelli & R. Filigheddu (2013) Human trampling effects on Mediterraneancoastal dune plants, Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology: Official Journal ofthe Societa Botanica Italiana, 147:4, 1043-1051, DOI: 10.1080/11263504.2013.861540

To link to this article: http://dx.doi.org/10.1080/11263504.2013.861540

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Plant Biosystems, 2013 Vol. 147, No. 4, 1043–1051, http://dx.doi.org/10.1080/11263504.2013.861540

ORIGINAL ARTICLE

Human trampling effects on Mediterranean coastal dune plants

E. FARRIS, S. PISANU, G. CECCHERELLI & R. FILIGHEDDU

Dipartimento di Scienze della Natura e del Territorio, Universita di Sassari, Sassari, Italy

Abstract Coastal habitats are particularly vulnerable to recreational impacts because these environments are highly dynamic and continually change in response to biotic and abiotic factors. Sand dune communities are worldwide characterized by high levels of biodiversity, but are often affected by human-induced impacts as those caused by tourist trampling. To understand the effects of human frequentation, trampling, and other human-induced impacts, fencing experiments have been traditionally carried out on coastal dunes. Since in touristic areas dune systems are subjected to different intensities of human frequentations rather than to opening or fencing, in this study we explore the effects of accessibility on vascular plants cover. This study tests the hypothesis that human frequentation on beaches affects spatio-temporal variability of vascular plant abundance on dunes by comparing the plant assemblages of high and low accessible sites in North-East Sardinia (Italy). Our results show that accessibility plays a crucial role in conditioning the percentage of vegetation cover in Mediterranean dunes. In fact, not only we found a perennial vegetation cover that was significantly higher in the sites with low accessibility (and consequently low frequentation), but we also showed that at the sites with high accessibility there were significant differences in vegetation cover between times of sampling (cover was higher before than after summer): on the contrary, differences in perennial vegetation cover among times were not significant at the low frequentation sites. After summer, the difference among low and high frequentation sites in species composition and cover was .90%. Multivariate analysis identified those species that play a pivotal role in differentiating the low and the high frequentation sites. Among them, Crucianella maritima and Sporobolus virginicus can be considered as differential species. Overall, our data show vegetation and plant species responses to human-induced impacts, and are therefore important to support conservation actions in Mediterranean coastal areas interested by mass tourism.

Keywords: Biodiversity conservation, Habitats Directive, Mediterranean dune vegetation, Sardinia, trampling

Introduction et al. 2011; Mijovic et al. 2012; Selbmann et al. 2013). Adaptations in the biological form and life

Coastal habitats are particularly vulnerable to cycle of many species are frequent (Cogoni et al. recreational impacts because these environments 2012). These communities are often affected by are highly dynamic and continually change in mechanical disturbance, due to either human response to interactions between wind, waves, and activities or natural causes, and consequently bare sediments (Brown & McLachlan 2002; Fenu et al. ground areas are generated (Maun 2009). Particu­2012; Mijovic et al. 2012). For example, the larly, sand dunes plant removal is due to human mechanical disturbance is an important stressor for trampling, wild animals grazing, and sand burial/ a wide variety of systems. Abiotic (e.g., fire, wind, scouring (Brown & McLachlan 2002; Davenport & wave action, and temperature) and biotic factors Davenport 2006). Therefore, the occurrence of (e.g., grazing, predation, and trampling) may act as unvegetated free space has become common, agents of disturbance, depending on the specific especially in the fore- and middle-dune zones where properties of the particular ecological system. wind action can scour bare sand down to the water

Among coastal systems, sand dune communities table or burying other plants. The size of the areas are worldwide characterized by high levels of disturbed and the rate of disturbance vary consider-complexity and originality at both the species and ably depending on the disturbing source. Trampling the community levels (Costa et al. 2011; Peinado by beach visitors is a disturbance that affects dune

Correspondence: E. Farris, Dipartimento di Scienze della Natura e del Territorio, Universita degli Studi di Sassari, via Piandanna, 4, I-07100 Sassari, Italy. Tel.: þ39 079 228675. Fax: þ39 079 233600. Email: emfa@uniss.it

q 2013 Societa Botanica Italiana

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1044 E. Farris et al.

vegetation at both the species and the community levels. In general, plant communities subjected to trampling tend to be poorer in species and less structured with respect to undisturbed communities, because only dominant and tolerant species persist (Santoro et al. 2012). Several authors have high­lighted that dune plant species are pre-adapted to strong natural stress and disturbances such as wind and sea erosion, salt spray, and sand burial (Wilson & Sykes 1999; Perumal & Maun 2006). This pre­adaptation to natural disturbances is likely to be an effective mechanism against human-induced dis­turbances, allowing a fast improvement in general conditions of coastal dune communities once disturbance ceases or has been limited.

Several habitats contribute to high biodiversity of costal ecosystems (Costa et al. 2011; Onofri et al. 2011; Puglisi et al. 2012; Pulina et al. 2012), which are therefore considered worth of conservation at continental (Basset & Los 2012), national (Capotorti et al. 2012), and regional level (Mattana et al. 2012). In Sardinia even if the habitat categories that are most rich in endemic plants are rocky habitats, and coastal/halophytic habitats, the most endangered habitat is coastal sand dunes (Bacchetta et al. 2012) on the basis of the threat level of the vascular plants living on beaches (Fenu et al. 2013).

This study tests the hypothesis that human frequentation on beaches affects spatio-temporal variability of vascular plant abundance on dunes by comparing the plant assemblages of high and low accessible sites. Specifically, here we test if beach accessibility has a significant effect on the cover of perennial plants. To test the hypothesis, we assessed temporal (seasonal) and spatial changes in vegetation cover throughout different accessibilities of touristic beaches. Also, we identify the most vulnerable species to human frequentation.

An understanding of how the intensity and type of recreational use may affect biodiversity helps to implement appropriate future management plans to control adverse visitor impacts (Buerger et al. 2003).

Materials and methods

Study area

The study area is located on the eastern coast of northern Sardinia (Italy) at Tavolara-Punta Coda Cavallo Marine Protected Area (Figure 1). As many other Mediterranean dune systems (Fenu et al. 2012), in this area coastal beaches and dunes are also characterized by a 10–20m wide band of vegetation that includes some habitats of conservation concern, as those identified by the EU Habitats Directive (European Commission 2013) and by the Italian

Ministry for the Environment (Biondi et al. 2009): Habitat 1210 – Annual vegetation of drift lines (community dominated by Salsola kali and Cakile maritima); Habitat 2010 – Embryonic shifting dunes (characterized by the dominance of Sporobolus virginicus and Elymus farctus); Habitat 2120 – Shifting dunes along the shoreline with Ammophila arenaria (white dunes, dominated by Ammophila arenaria and the endemic Silene corsica); Habitat 2210 – Crucianellion maritimae fixed beach dunes (grey dunes dominated by Helichrysum italicum subsp. microphyllum, Scrophularia ramosissima, Thy­melaea tartonraira, Crucianella maritima, and Ephedra distachya); Habitat 2230 – Malcolmietalia dune grasslands (ephemeral communities with annual vegetation). Because of both dune morphology and anthropogenic disturbance, the classic zonation of the vegetation of the dunes is rarely, if not ever, present.

In the study area four sites were selected: two were considered as high frequentation sites at Porto Taverna (PT) and Cala Brandinchi (CB), 68 and 60 m long, respectively, both easily accessible from a parking place and a main entrance and two as low frequentation sites

Figure 1. Study area along the eastern coast of Sardinia (Italy). Porto Taverna (PT), Cala Brandinchi (CB), Cala Spalmatore (CS), and La Cinta (LC) are the four beaches where sampling was done.

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at Cala Spalmatore di Tavolara (CS) and La Cinta di San Teodoro (LC), 87 and 250 m long, respectively, the former located in a protected island and the latter with a fenced vegetation. The selected beaches are 5– 15 m wide. At the study sites, we studied all the above-mentioned habitats except Habitat 1210, because it is very discontinuous and ephemeral.

Sampling design

Sampling was done in the inner band of the dunes during spring (April–May, time 1) and summer 2006 (August–September, time 2), this is before and after summer frequentation. At each site, four areas were randomly selected and in each of them 10 quadrats, 50 £ 50 cm in size, were considered (320 quadrats in total). In each quadrat, the plant species cover was estimated in the field: to take accurate estimates, a grid of 25 sub-quadrats was used for each plot and a score from 0 to 4% was given in each sub-quadrat, so that the percentage cover was obtained by summing over the entire set of sub-quadrats (Dethier et al. 1993). In each sample plot, the number of the species and species cover were recorded. Variability in cover (percentage) of each species in spring (time 1. before human trampling) and in the late summer (time 2. after human trampling) was measured. For rhizoma­

tous perennial species (Sporobolus, Ammophila, and Elymus) only emerging stems were counted. Species’ names follow Conti et al. (2005). Each species was assessed as annual or perennial, according to Pignatti (1982): (therophytes ¼ annuals; geophytes þchamaephytes þ hemicryptophytes ¼ perennials).

Data analyses

To avoid the eventual overestimation of the effect of human frequentation, annual species (i.e. species Cakile maritima, Cutandia maritima, etc., in Table I) were not considered in the data analysis. The total cover of perennial plant species was analysed by means of a four-way analysis of variance (ANOVA): it included the factors “time” (before and after summer, fixed and orthogonal), “frequentation” (high and low, fixed and orthogonal), “site” (two levels, random and nested in the frequentation), and “area” (four levels, random and nested in the site) with n ¼ 10. Cochran’s test was conducted to check for homogeneity of variances, while the Student Newman-Keuls test was conducted to make a posteriori comparisons of mean values (Underwood 1997).

A non-metric multi-dimensional scaling (nMDS) ordination was done on the basis of a Bray–Curtis dissimilarity matrix calculated from fourth root transformed data. Ordination was obtained by plotting area centroids as the mean cover values of each taxon in the 10 replicate quadrats of each site x

Trampling effects on dune plants 1045

time combination. Stress values were shown in the nMDS plot to indicate the goodness of represen­tation of differences among samples (Clarke 1993). Similarity Percentages analysis (SIMPER) (Clarke 1993) was used to identify the taxa mostly contributing to differences between high and low frequentation sites for each time, highlighted by ANOVA. For each comparison, taxa that cumulat­

ively contributed to 90% of dissimilarities were shown. The spatial pattern of these important and most abundant taxa was examined using three-way ANOVAs using the model described above (Under­

wood 1997). The homogeneity of variances was tested by Cochran’s test.

Results

Species

At the four studied sites, we recorded a total of 55 vascular plants, of which 41.82% were annuals (therophytes, Table I).

Cover

A higher average vegetation cover at the low frequentation sites was highlighted with respect to high frequentation sites. Most importantly, there were significant differences in perennial vegetation cover between time 1 and time 2 at the high frequentation sites, but not at the low frequentation sites (Figure 2). At all sites, annual plants were present only at time 1 (before summer), but not at time 2 (after summer). ANOVA on perennial species cover highlighted a significant effect of time and frequentation (Table II). In fact, at time 2 vegetation cover was significantly lower (T2 ¼ 20.91 ^ 1.11%) than at time 1 (T1 ¼ 36.02 ^ 1.20%); the low frequentation sites showed a vegetation cover higher (low ¼ 35.96 ^ 1.12%) than that of high frequenta­tion sites (high ¼ 20.95 ^ 1.20%).

SIMPER for high and low frequentation groups

We performed an SIMPER to identify the species contributing mostly to dissimilarities between high and low frequentation sites at the two sampling times (Table III). Higher differences among sites were detected at time 2 (91.02%); the higher contribution to this difference was given by Crucianella maritima (17.59%), Sporobolus pungens (13.84%), and Scabiosa maritima (10.91%). Crucianella maritima can be considered a differential species because it is absent at the high frequentation sites. In an opposite way, Sporobolus pungens can also be considered a differen­tial species because its cover is significantly higher at the high frequentation sites (T1 ¼ 4.93 ^ 0.41%,

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Table 1. Species recorded on the four sampling beaches at two sampling times (time 1 and time 2) before and after summer season 2006.

Time 1 Time 2

High Low High Low

BF Species PT CB CS LC PT CB CS LC

Perennial Aetheorrhiza bulbosa (L.) Cass. þ þ þ þ 2 2 2 2Perennial Ammophila arenaria Link. þ þ þ þ 2 2 þ þPerennial Anthemis maritima L. þ þ 2 þ 2 þ þ þAnnual Avena sp. þ 2 2 2 2 2 2 2Annual Cakile maritima Scop. þ 2 2 2 2 2 2 2Perennial Calystegia soldanella (L.) R. Br. 2 2 þ þ 2 2 þ þPerennial Carpobrotus sp. 2 2 þ 2 2 2 2 2Annual Catapodium rigidum L. þ þ þ þ 2 2 2 2Annual Cerastium glomeratum Thuill. 2 þ 2 2 2 2 2 2Perennial Clematis flammula L. 2 2 2 2 2 2 2 þPerennial Crucianella maritima L. 2 2 þ þ 2 2 þ þAnnual Cutandia maritima (L.) Barbey 2 2 2 2 2 2 2 þPerennial Echinophora spinosa L. 2 2 2 2 2 2 þ 2Perennial Elymus farctus (Viv.) Runemark ex Melderis 2 2 2 2 2 2 þ 2Perennial Eryngium maritimum L. þ 2 2 þ 2 þ þ 2Annual Euphorbia terracina L. 2 2 2 2 2 2 2 þPerennial Galactites tomentosa Moench 2 2 2 2 þ 2 2 2Annual Helichrysum italicum (Roth) Don ssp. microphyllum (Willd.) Nyman 2 þ þ 2 2 þ þ 2Perennial Holoschoenus romanus (L.) Fritsch 2 2 2 2 2 þ 2 2Perennial Hyoseris radiata L. 2 2 þ 2 2 2 2 2Annual Hypecoum procumbens L. 2 þ 2 2 2 2 2 2Perennial Iris sisyrinchium L. 2 2 2 2 2 2 þ 2Perennial Juniperus turbinata Guss. 2 2 þ 2 2 2 þ 2Annual Lagurus ovatus L. 2 þ 2 þ 2 þ 2 2Annual Linaria flava (Poiret) Desf. ssp. sardoa (Sommier) Arrigoni þ þ 2 2 2 2 2 2Perennial Lobularia maritima (L.) Des. 2 2 2 2 2 2 2 2Perennial Lotus cytisoides L. þ þ 2 þ 2 þ þ þAnnual Lotus edulis L. 2 2 þ 2 2 2 2 2Annual Malcolmia ramosissima (Desf.) Gennari 2 þ þ 2 2 2 2 2Perennial Matthiola sinuata (L.) R. Br. 2 2 2 2 2 2 þ 2Ajinual Matthiola tricuspidata (L.) R. Br. 2 2 2 2 2 2 þ 2Annual Medicago littoralis Loisel þ þ þ þ 2 2 2 2Perennial Medicago marina L. þ 2 þ þ 2 2 þ 2Perennial Ononis minutissima L. 2 2 2 þ 2 2 2 2Perennial Otanthus maritimus (L.) Hoffmgg. et Link þ 2 þ þ 2 2 þ þPerennial Pancratium maritimum L. þ þ þ þ þ þ þ þAnnual Paronychia echinulata Chater 2 þ 2 2 2 þ 2 2Annual Plantago coronopus L. 2 2 þ 2 2 2 2 2Perennial Plantago macrorrhiza Poiret 2 2 þ 2 2 2 þ 2Annual Polycarpon tetraphyllum L. þ þ þ þ 2 2 2 2Perennial Romulea requienii Parl. 2 þ 2 2 2 2 2 2Perennial Romulea rollii Parl. 2 2 2 þ 2 2 2 2Perennial Rovya polygama (Desf.) Coincy 2 2 þ 2 2 2 2 2Perennial Rubiaperegrina L. 2 2 2 þ 2 2 2 2Annual Rumex bucephalophorus L. þ þ þ 2 2 2 2 2Annual Salsola kali L. 2 2 2 2 2 þ 2 2Perennial Scabiosa maritima L. 2 þ 2 þ 2 þ 2 þPerennial Scrophularia ramosissima Loisel. þ þ 2 2 2 þ 2 2Annual Senecio vulgaris L. 2 2 2 þ 2 2 2 2Perennial Silene corsica DC. þ þ þ þ 2 2 þ þAnnual Silene nicaeensis All. 2 þ 2 þ 2 þ 2 þAnnual Silene nummica Vals. þ þ þ þ 2 2 2 þPerennial Sporobolus virginicus Kunth þ þ þ þ þ þ þ þAnnual Valerianella eriocarpa Desv 2 þ 2 2 2 2 2 2Annual Vulpia fasciculata (Forssk.) Fritsch þ 2 2 2 2 2 2 2

Total perennial species 12 11 15 18 4 9 18 13 Total annual species 9 14 9 7 0 5 2 4

Notes: Beaches were divided into high intensity of frequentation (High: PT ¼ Porto Taverna; CB ¼ Cala Brandinchi) and low intensity of frequentation (CS ¼ Cala Spalmatore; LC ¼ La Cinta). Presence or absence of species is indicated as þ and 2, respectively. BF, biological form.

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Trampling effects on dune plants 1047

Figure 2. Species cover (%) in the four beaches (PT, CB, CS, and CB) at time 1 and time 2. High, high intensity of frequentation (PT ¼ Porto Taverna; CB ¼ Cala Brandinchi); Low, low intensity of frequentation (CS ¼ Cala Spalmatore; LC ¼ La Cinta).

T2 ¼ 5.21 ^ 2.20%) than at the low frequentation sites (T1 ¼ 1.58 ^ 0.39%, T2 ¼ 2.19 ^ 0.57%).

ANOVA on cover values for the species highlighted by SIMPER

ANOVA on cover values of those species highlighted by SIMPER showed the different effects of time, frequentation, and site on single species cover (Table IV, Figure 3).

Specifically, (a) time had a significant effect on the cover of Crucianella maritima (T1 ¼ 2.98 ^ 0.57%; T2 ¼ 3.28 ^ 0.55%) and Silene corsica (T1 ¼ 2.21 ^ 0.27%; T2 ¼ 0.21 ^ 0.11%); (b) frequenta­tion had a significant effect only on the cover of Crucianella maritima (high ¼ 0.00 ^ 0.00%: low ¼ 6.25 ^ 0.56%); (c) site had a significant effect on the cover of Aetheorrhiza bulbosa (only in the low frequentation sites CS ¼ 3.43 ^ 0.67%; LC ¼ 0.77 ^ 0.37%), Ammophila arenaria (at high frequen­tation sites were PT ¼ 5.18 ^ 0.75%, CB ¼ 0.49 ^ 0.25%; at low frequentation sites were

Table 2. ANOVA on species cover.

COVER

Factors Df MS F P

Fr 1 17955.0 20.88 0.0447 Ti 1 18255.9 73.33 0.0134 Si (Fr) 2 860.1 2.21 0.1529 Ar (Fr £ Si) 12 390.0 3.31 0.0002 Ti £ Fr 1 2327.4 9.35 0.0924 Ti £ Si (Fr) 2 248.9 0.42 0.6678 Ti £ Ar (Fr £ Si) 12 596.1 5.07 0.0000 RES 288 117.7 Cochran’s test C ¼ 0.1161 (P , 0.01)

Note: Factors are: frequentation (Fr: high and low), time (Ti: two levels), site (Si: two levels), and areas (Ar: four levels). Data were pffiffiffiffiffiffiffiffiffiffiffiffiffi transformed as X þ 1. Bold values mean significant P , 0.05.

CS ¼ 3.06 ^ 0.65%, LC ¼ 6.34 ^ 0.80%); Lotus cytisoides (at high frequentation sites were PT ¼ 0.36 ^ 0.16%, CB ¼ 2.88 ^ 0.40%; at low frequen­tation sites were CS ¼ 0.01 ^ 0.01%, LC ¼ 7.71 ^ 0.82%), Plantago macrorrhiza (only at low frequenta­tion sites were CS ¼ 2.90 ^ 0.40%, LC ¼ 0.00 ^ 0.00%), Scabiosa maritima (at high frequentation sites were PT ¼ 0.00 ^ 0.00%, CB ¼ 5.20 ^ 0.52%; at low frequentation sites were CS ¼ 0.00 ^ 0.00%; LC ¼ 4.05 ^ 0.73%), and Sporobolus virginicus (only at high frequentation sites were PT ¼ 8.16 ^ 0.85%; CB ¼ 1.98 ^ 0.32%).

Discussion and conclusions

In the last 65 years, the dunes located on the northern edge of the Mediterranean Basin experi­mented high levels of land consumption and degradation due to mass tourism development, urban sprawl, and invasive alien species propa­

gation. Because of these threats, during the last century, a loss of about 70% of dune systems for European coasts has been calculated as a result of increasing urbanization (Feola et al. 2011). In Italy, the process of dune degradation seems to be even more intense than the European average: up to 80%, from 45,000 ha in 1900 to a remaining 9000 ha at the end of the twentieth century (Feola et al. 2011).

The rapid growth of mass tourism in Mediterra­

nean areas in the last decades had as a consequence the increase in human impacts on plant populations and communities, driven by direct trampling, mechanical beach cleaning, infrastructure develop­ment, and invasive species introduction (Davenport & Davenport 2006). In fact, 63% of European holidaymakers prefer the coasts, and coastal environ­ments are also preferred by tourists. Worldwide the number of international arrivals (i.e. arrivals from

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Table 3. SIMPER analyses between high and low groups in species cover at time 1 and time 2.

High Low Species Av. Abund Av. Abund Av. Diss Diss/SD Contrib% Cum.%

Groups H and L (time 1) Average dissimilarity ¼ 76.97 Ammophila arenaria 5.66 5.73 10.19 1.08 13.24 13.24 Pancratium maritimum 6.61 6.39 9.64 1.22 12.52 25.77 Lotus cytisoides 2.59 6.05 9.04 0.97 11.75 37.51 Crucianella maritima 0.00 5.95 8.51 0.81 11.06 48.57 Aetheorrhiza bulbosa 1.86 4.20 6.89 0.80 8.96 57.53 Sporobolus pungens 4.93 1.58 6.69 0.94 8.69 66.21 Scabiosa maritima 3.41 0.73 5.41 0.70 7.03 73.25 Silene corsica 1.40 3.04 4.86 0.90 6.31 79.56 Medicago marina 1.48 2.41 4.48 0.52 5.82 85.38 Anthemis maritima 1.13 1.09 2.90 0.60 3.77 89.15 Otanthus maritimus 0.26 0.63 1.36 0.26 1.77 90.92

Groups H and L (time 2) Average dissimilarity ¼ 91.02 Crucianella maritima 0.00 6.55 16.02 0.91 17.59 17.59 Sporobolus pungens 5.21 2.18 12.60 0.93 13.84 31.43 Scabiosa maritima 1.79 3.33 9.93 0.75 10.91 42.34 Ammophila arenaria 0.00 3.68 8.21 0.66 9.02 51.36 Otanthus maritimus 0.00 2.64 6.28 0.42 6.90 58.26 Plantago macrorhiza 0.00 2.11 5.97 0.62 6.56 64.82 Pancratium maritimum 0.46 1.54 4.96 0.58 5.45 70.27 Helichrysum italicum ssp. microphyllum 0.46 1.63 4.66 0.45 5.12 75.39 Lotus cytisoides 0.65 1.68 4.47 0.65 4.91 80.30 Elymus farctus 0.59 1.35 4.12 0.47 4.53 84.82 Anthemis maritima 0.39 1.34 3.95 0.49 4.34 89.16

outside the country) has shown an increase from 25 million in 1950 to over 700 million in 2002, corresponding to an average annual growth rate of 6.6% and it is estimated that by 2020 there will be 350 million tourists visiting the Mediterranean coastal region alone (Davenport & Davenport 2006). In 2009, in Italy 54,375,079 Italian and 41,124,722 foreign tourists travelled, whereas in the same year there were 1,564,217 Italians and 883,130

Table 4. ANOVAs on cover for SIMPER species.

foreign people visiting Sardinia (data from http:// www.sardegnastatistiche.it/index.html).

In Sardinia, 260 out of 2407 vascular plants are exclusive of the Corsican–Sardinian biogeographical province: among them many are naturally rare (also called narrow endemics) but not threatened (par­ticularly those living in rocky habitats), whereas others have declined dramatically over the last decades (Bacchetta et al. 2012). Even if the habitat

Factors Ti Fr Si (Fr) Ar (Fr £ Si) Ti £ Fr Ti £ Si (Fr) Ti £ Ar (Fr £ Si) RES DF 1 1 2 12 1 2 12 288

Species MS

Crucianella maritima 7.20 3125.00 6.05 294.46 7.20 0.20 66.85 12.49 Silene corsica 324.01 84.05 12.06 22.61 30.01 3.93 19.34 5.39 Aetheorrhiza bulbosa 735.08 109.28 174.90 17.09 109.28 174.90 17.09 12.05 Ammophila arenaria 1189.65 279.38 653.97 60.98 261.00 489.07 38.14 24.57 Lotus cytisoides 796.95 402.75 1312.05 30.56 118.83 416.60 40.86 9.93 Medicago littoralis 2226.05 632.81 512.83 79.87 632.81 512.83 79.87 14.13 Plantago macrorrhiza 35.11 168.20 168.20 15.16 35.11 35.11 16.47 1.75 Scabiosa maritima 19.01 26.45 868.85 16.14 357.01 188.01 40.19 12.75 Sporobolus virginicus 15.75 816.00 767.82 65.01 1.95 5.09 109.76 17.00 Pancratium maritimum 2420.00 14.45 203.63 56.31 33.80 160.40 33.13 16.20 Helichrysum microphyllum 25.31 9.11 97.58 27.95 54.45 39.88 15.73 4.78 Medicago marina 285.01 22.05 149.31 78.42 13.61 129.63 72.17 7.25 Otanthus maritimus 61.25 180.00 113.01 60.43 103.51 28.41 28.56 9.88 Elymus farctus 75.08 11.63 21.35 6.19 11.63 21.35 6.19 4.19

Note: Factors are: time (Ti: two levels), frequentation (Fr: high and low), site (Si: two levels), and areas (Ar: four levels). Bold values mean significant MS for p , 0.05.

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Trampling effects on dune plants 1049

Figure 3. Species cover (%). Reported only for SIMPER species (see Table 3).

types that are most rich in endemic plants are rocky habitats and coastal/halophytic habitats, the most endangered habitat is coastal sand dunes because of the high number of vascular plants under threat (Bacchetta et al. 2012).

To understand the effects of human frequentation, trampling, and other human-induced impacts, fen­cing experiments have been traditionally carried out on coastal dunes (Nordstrom et al. 2000; Nordstrom et al. 2002; Farketic et al. 2010; Damgaard et al. 2013). However, it is not possible to fence all the thousands kilometres of dunes that are under threat, and in touristic areas dune systems are subjected to different intensities of human impact rather than to opening or fencing: in this study, we therefore

explored the effects of accessibility on vascular plants. Our results show how accessibility plays a crucial role in conditioning the percentage of vegetation cover in Mediterranean dunes. In fact, not only we found a perennial vegetation cover that was significantly higher in the sites with low accessibility (and consequently low frequentation), but we also showed that at the sites with high accessibility there were significant differences in vegetation cover between times of sampling (cover was higher before than after summer): on the contrary, differences in perennial vegetation cover among times were not significant at the low frequentation sites. At time 2 (after summer), the difference among low and high frequentation sites in species composition and cover was .90%.

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1050 E. Farris et al.

Furthermore, in this study, we not only deal with general effects on the vegetation as a whole, but we also go in deep exploring particular effects on single species. Multivariate analysis identified those species that play a pivotal role in differentiating the low and the high frequentation sites. Among them, Crucia­nella maritima can be considered a differential species that is negatively affected by human frequentation, whereas Sporobolus virginicus is positively affected. It is noteworthy that C. maritima is the only species of which the cover was significantly influenced by time and frequentation.

Overall, our data show vegetation and plant species responses to human-induced impacts, and are therefore important to support conservation actions in Mediterranean coastal areas interested by mass tourism. Direct actions such as biodiversity conservation (Guillet et al. 2012), protection and reintroduction of vascular plants (Cogoni et al. 2013), and related taxa (Minter 2011; Onofri et al. 2011; Venturella et al. 2011) should consider the different effects of human-induced impacts on dune vegetation cover at low and high accessible sites that were shown in this study. Unfortunately, in touristic areas, it is not always possible to fence dunes to prevent people entering, so conservation actions should include people information and motivation to reduce frequentation impacts. A challenge for future years is therefore not only the protection of dune environments itself, but also the reshaping of the so-called “sun and sand tourism” (Aguilo et al. 2005) through the promotion of nature-aware tourism (Nimis et al. 2012), public information (Martellos et al. 2011), involvement of local populations (Nordstrom et al. 2002), and development of citizen science programmes for monitoring and conserving biodiversity (Dickinson et al. 2012; Newman et al. 2012; Tulloch et al. 2013), also in the ambit of biodiversity databases (Basset & Los 2012; Hole­

tschek et al. 2012; Guntsch et al. 2012; Landucci et al. 2012). This study contributes to make the vast public more responsible, showing quantitative measures of the effects of human disturbance on dune perennial vegetation.

Acknowledgements

The authors are grateful to the staff of the Protected Marine Area of Tavolara-Capo Coda Cavallo for providing a logistic base and for the help offered throughout the research project. Part of the data were taken from the master thesis of Laura Bassanetti, which is acknowledged for her help on the field.

Funding

Financial support was obtained by project FAR 2011 for RF and project “Monitoraggio della vegetazione

dunale” from Comune di Olbia (Rep. 5 of 2.07.2012) for RF.

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