Understanding patterns of invasions on Mediterranean coastal dunes : from environmental filtering to biotic interactions across scales

(1)

(2)

(3)

DOCTORAL SCHOOL IN BIOLOGY

Section: Biodiversity and Ecosystem Analysis

XXIII CYCLE

Understanding patterns of invasions

on Mediterranean coastal dunes:

From

environmental filtering to biotic interactions

across scales

Analisi multiscalare delle invasioni di piante esotiche

in ambienti di duna costiera:

dal filtraggio ambientale alle

interazioni biotiche

Marta Carboni

A.A. 2010/2011

(4)

Thesis Defense on the 16th December 2010 in front of the following jury:

Luigi Boitani (National evaluator) Alessandro Chiarucci (National evaluator) Maike Isermann (European reviewer) Peter B. Pearmann (European evaluator) Wilfried Thuiller (European reviewer) Marzio Zapparoli (National evaluator)

(5)

Abstract

As a consequence of the human mediated blurring of biogeographical barriers to species dispersal, many plant communities are becoming increasingly dominated by introduced species (“aliens”). Mediterranean sandy shores are threatened conservation targets at the European level, for which plant invasions are a recognized prime agent of alteration. This thesis takes advantage of the value of coastal dunes as model systems to understand features that make plant communities more invasible and to determine the implications of the spatial resolution used for the analysis. I examine alien distribution patterns on holocenic dunes of several central Italian regions both within large grid cells (ca. 35 km2) and within small random plots (4 m2 and 64 m2). At the coarse resolution I analyze broad latitudinal gradients building a data set of environmental drivers (climate and coastline movements) and of human drivers (land cover, urbanization and tourism). For the small resolution I built a dataset of environmental field measurements along the sea-inland gradient: soil features related to level of environmental stress (e.g. content in organic matter, soil moisture and salinity, etc.) and wind factors related to natural disturbance (sand burial, wind abrasion, etc.). I found that presence and abundance of alien species on Mediterranean coastal dunes is driven in different measure by environmental filtering, biotic interactions and human impact depending on the spatial scale and on the sampling resolution examined. With respect to extrinsic abiotic factors there are several main differences between regional and local scales. Along a regional latitudinal gradient a rich alien plant species pool is promoted mostly by mild climatic conditions and broad heterogeneous dune systems. Instead, large scale modifications brought about by humans impact Mediterranean littorals mostly directly by reducing native biodiversity, rather than indirectly by favoring alien species abundance. The situation is turned around when focusing on fine scale patterns. Propagule pressure mediated by human recreational structures explains most of the variability in the fine resolution alien distribution data. Nonetheless, clear directional gradients of environmental stress and natural disturbance can be quantified along the dune profile. This small scale spatial variation in abiotic conditions also explains differences in invasibility. Specifically, intermediate levels of environmental stress

(8)

offer the best conditions for spread of alien species locally. Turning to intrinsic biotic factors, the sampling resolution influences two main aspects. First, the relationship between native diversity and invasion success turns from positive at large sampling resolutions to negative at fine resolutions supporting a recently proposed conceptual model. The positive relationship can be explained with comparable responses to broad scale extrinsic factors and to varying heterogeneity while the small scale negative relationship can be ascribed to competitive interactions. Second, by addressing a long lasting debate in invasion ecology (Darwin’s naturalization conundrum), this thesis demonstrates that the measure of the phylogenetic distance from successful invaders to the recipient community is also sensitive to sampling resolution. At the smallest spatial scale existing members of invaded plant communities are less related to most invaders than expected by chance (phylogenetic overdispersion). Yet with increasing scale, since species can co-occur while avoiding direct competition, native assemblages become more invasible for closely related species because of habitat filtering (phylogenetic clustering). In conclusion these findings suggest that many apparently contrasting patterns in the study of invasibility of communities can actually be reconciled by recognizing the implications of different sampling resolutions.

(9)

Riassunto

A seguito del crollo delle barriere biogeografiche alla dispersione delle specie causato dall’uomo, numerose comunità vegetali risultano sempre più frequentemente invase da specie aliene. In particolare, le invasioni biologiche sono una delle principali cause di alterazione per gli ambienti dunali costieri mediterranei, habitat target di conservazione a livello europeo. In questa tesi, gli ambienti dunali costieri sono presi come sistemi modello per indagare i fattori che rendono le comunità vegetali più facilmente invadibili e per determinare le implicazioni della risoluzione spaziale utilizzata nell’ analisi dei pattern di invasione. Le analisi condotte si concentrano sui pattern di distribuzione delle specie aliene sulle dune oloceniche di diverse regioni dell’Italia centrale, sia utilizzando una griglia ad

ampia maglia (ca. 35 km2), sia all’interno di plot random di piccole

dimensioni (4 m2 and 64 m2). Alla risoluzione più grossolana ho

analizzato ampi gradienti latitudinali mentre a risoluzione fine ho costruito una banca dati di misure ambientali (legate al suolo e all’azione del vento) lungo il gradiente mare-terra. I miei risultati mostrano che la presenza e l’abbondanza delle specie aliene sulle dune costiere mediterranee è determinata in diversa misura dal filtraggio ambientale, dalle interazioni biotiche e dall’impatto antropico a seconda della scala spaziale e della risoluzione di campionamento considerata. Rispetto ai fattori abiotici estrinseci sono emerse numerose differenze tra la scala regionale e quella locale. Lungo il gradiente latitudinale un ricco pool di specie aliene è favorito soprattutto da condizioni climatiche miti e da ampi sistemi dunali con maggiore eterogeneità. Le modificazioni antropogeniche su ampia scala invece hanno un impatto negativo sui litorali mediterranei soprattutto direttamente riducendo la biodiversità nativa, piuttosto che indirettamente attraverso l’introduzione di specie aliene. La situazione è invece capovolta quando ci si concentra sui pattern a scala fine. Mentre il filtraggio ambientale è maggiormente importante per l’abbondanza di specie aliene ad una scala ampia, a risoluzione fine è la pressione del propagulo attraverso strutture umane ricreative che spiega la maggior parte della variabilità nei dati di distribuzione delle specie aliene. Tuttavia è possibile quantificare chiari gradienti di stress ambientale e di disturbo naturale lungo il profilo dunale. Anche questa variazione spaziale nelle condizioni abiotiche è in grado di spiegare differenze

(10)

nel grado di invadibilità delle comunità. Specificamente, livelli intermedi di stress ambientale offrono le migliori condizioni per l’espansione locale delle specie aliene. Per quanto riguarda invece i fattori biotici intrinseci, la risoluzione di campionamento influenza due principali aspetti. In primo luogo la relazione tra diversità di specie native e successo di invasione cambia da positiva con risoluzione di campionamento grossolana a negativa con risoluzione fine. Ciò rispecchia le previsioni di un modello concettuale proposto di recente. La relazione positiva può essere spiegata come derivante da risposte paragonabili a fattori estrinseci su ampia scala mentre la relazione negativa a scala fine può essere ricondotta a interazioni competitive tra le specie. In secondo luogo, affrontando un dibattito da lungo aperto nel campo dell’ecologia dell’invasione (l’enigma della naturalizzazione di Darwin), questa tesi dimostra che anche la distanza filogenetica tra invasori e comunità nativa è variabile a seconda della risoluzione di campionamento. Alla scala spaziale più fine i membri residenti delle comunità vegetali invase sono meno affini con le specie invadenti rispetto ad una situazione casuale (sovradispersione filogenetica). Tuttavia con l’aumentare della scala, poiché le specie possono coesistere ma allo stesso tempo evitare la competizione diretta, le comunità native in seguito al filtraggio ambientale diventano più facilmente invadibili per specie strettamente affini (aggregazione filogenetica). In conclusione, questi risultati suggeriscono che molti pattern apparentemente contrastanti nello studio dell’invadibilità delle comunità possono essere riconciliati riconoscendo le implicazioni di risoluzioni di campionamento diverse.

(11)

Papers published or prepared in the course of the PhD

Paper 1

Carboni M., Carranza M.L. & Acosta A. 2009. Assessing conservation status on coastal dunes: A multiscale approach.

Landscape and Urban Planning 91: 17-25. Paper 2

Carranza M.L., Carboni M., Feola S. & Acosta A. 2010. Landscape-scale patterns of alien plant species on coastal dunes. The case of iceplant in central Italy. Applied Vegetation Science 13: 135–145 (DOI: 10.1111/j.1654-109X.2009.01065.x).

Paper 3

Carboni M., Santoro R. & Acosta, A. 2010. Are some communities of the coastal dune zonation more susceptible to alien plant invasion?

Journal of Plant Ecology 3: 139-147 (DOI: 10.1093/jpe/rtp037). Paper 4

Carboni, M., Thuiller, W., Izzi, F. & Acosta, A. 2010. Disentangling the relative effects of environmental versus human factors on the abundance of native and alien plant species in Mediterranean sandy shores. Diversity and Distributions 16: 537– 546 (DOI: 10.1111/j.1472-4642.2010.00677.x).

Paper 5

Carranza M.L., Ricotta C., Carboni M. & Acosta A. Habitat selection by invasive alien plants. A bootstrap approach. Ecological

Indicators (Submitted). Paper 6

Santoro R., Prisco I., Carboni M., Battisti C. & Acosta A. Effects of

trampling limitation on coastal dune plant communities.

Environmental Management (Submitted). Paper 7

Carboni M., Santoro R. & Acosta A.T.R. Sea-inland gradient or propagule pressure: what drives small scale alien distribution patterns on Mediterranean coastal dunes? Journal of Vegetation

(12)

Paper 8

Santoro, R, Carboni, M., Carranza, M.L. & Acosta, A.T.R. Finding effects of plant invasions on diversity. Focusing on conservation interest species may affect conclusions. Ecological Indicators (Submitted).

Paper 9

Fenu G., Carboni M., Acosta A.T.R. & Bacchetta G. Which environmental factors influence dune vegetation zonation on Mediterranean sandy coasts? (In prep.).

Paper 10

Carboni M., Münkemüller T., Gallien L., Lavergne S., Acosta A. & Thuiller W. Darwin’s naturalization hypothesis: scale matters in coastal plant communities. (In prep.).

(13)

Preface

This thesis represents a multiscale analysis of alien plant species distribution patterns on Mediterranean coastal dunes.

In the introduction I briefly address the issues related to alien plant species introductions and naturalizations, to the peculiar model system of coastal dunes, to environmental and human drivers of vegetation and species patterns and finally to the crucial aspect of spatial scale.

In the first chapter I pinpoint the main factors that drive diversity patterns of native and alien plants on coastal dunes of central Italy at a large scale of analysis (paper 4).

In the second chapter I focus on small scale sea-inland environmental and vegetation gradients of Mediterranean sandy shores and analyze their importance next to propagule pressure for the invasibility of coastal plant communities (paper 7).

Finally the third chapter demonstrates the importance of the spatial scale for the investigation of invasion patterns, by addressing for the first time with field data a long lasting debate in invasion ecology: Darwin’s naturalization conundrum (paper 10).

The conclusions section synthesizes and links the findings of the thesis in the contexts of ecology and conservation, and suggests directions for future research.

For brevity, the Material and Methods sections of Chapters 1, 2 and 3 are reported as appendices in the electronic supplementary materials, along with the two other papers (3 and 9) directly linked with the research presented in Chapter 2.

(14)

(15)

General introduction

Plant invasions and invasibility of plant communities

As a consequence of the human mediated blurring of biogeographical barriers to species dispersal (D'Antonio & Vitousek 1992; Sala et al. 2000) many plant communities are becoming increasingly dominated by introduced plant species, leading to a sort of globalization of the Earth’s biota (Levine & D'Antonio 2003; Sax & Gaines 2003). Unlike natives (taxa that evolved in the region or reached it from another area where they are native without help from humans), aliens (‘non-native’ or ‘exotic’) owe their presence to direct or indirect activities of humans. Invasion ecology is the exploding field of research addressing this intentional or accidental movement of organisms to areas outside their natural dispersal range and of the consequences of such transfers.

An important first step for focusing research effort in invasion ecology is to define a framework of definitions to label alien taxa. According to their ‘invasion status’ (Richardson et al., 2000; Pyšek et al. 2004) alien plants can be classified in three main categories: casual alien plants occur only temporarily and are not able to persist for a long time without human-assisted input of diaspores because they do not form self-replacing populations; naturalized aliens sustain self-replacing populations by recruitment from seed or other propagules without continuous intervention by humans; invasive aliens are a subset of naturalized plants that not only reproduce but are also able to spread fast over a large natural or semi-natural area. Further, from the point of view of their residence time, alien species are traditionally classified as archaeophytes if introduced before the year 1500, and neophytes if introduced after that date (Pyšek et al. 2004). Finally, not all naturalized plant taxa, and not even all invaders, are necessarily dangerous. However some harmful invaders (“weeds”) can cause severe environmental changes by altering native species composition and the functioning of ecosystems (Vitousek et al. 1997; Mack et al. 2000) and at times even affect human economic wealth directly by impacting on agriculture, forestry and health (Pimentel et al. 2001). Recent naturalizations and invasions are therefore a significant component of human-mediated global environmental change (Vitousek et al. 1997) and pose significant challenges to managing and maintaining

(16)

indigenous biodiversity in natural systems. Considering that most studies have found a strong correlation between the number of successful naturalizations and the number of harmful invaders (tens rule - Richardson & Pyšek 2006) and that the separation between archeophytes and natives is especially difficult in the Mediterranean basin, in this thesis I will focus exclusively on patterns of naturalized neophytes. For simplicity, by viewing aliens on a ‘naturalization– invasion’ continuum, in the following I refer to alien distribution patterns as “invasion patterns” and to naturalized species as “invaders” in a general sense.

A part from analyzing the impact and consequences of plant invasions on natural ecosystems, the main focus of invasion ecology has been to investigate how, why and where human-introduced species transported far from their original range manage to establish, survive and maintain viable populations into native communities. Specifically there are two main questions that have been traditionally addressed to understand the mechanisms of invasion. First, the question of “why are some communities more prone to invasion than others?” attempts to define community characteristics and environmental situations that facilitate invasions (i.e. the community invasibility). Second the question “do invaders have particular characteristics conveying a competitive advantage over other species?” is focused on the search for traits that separate successful from less successful invaders (i.e. the species invasiveness). These two sets of questions have been historically investigated separately although they are intrinsically linked (Richardson & Pyšek 2006). Most authors have concluded that traits contributing to the success of

taxa as invasive aliens are not universal (Williamson 1999) and need

to be related to the characteristics of the invaded community. In this sense, concentrating on the invaded communities my thesis highlights the influence in first place of extrinsic abiotic features such as geographical setting, environmental conditions and human influence but also of intrinsic biotic features such as diversity and community structure.

Our understanding of the extrinsic abiotic factors controlling the presence, diversity and spread of alien species in an ecosystem (i.e. influencing community invasibility) is still limited (Rejmánek et al. 2005; Thuiller et al. 2010). In general, environmental factors that have been found to influence patterns of alien species richness at a

(17)

regional scale include climate, landscape heterogeneity, spatial patterns, geomorphologic processes and level of protection (van Rensburg et al. 2002; Hawkins et al. 2003; Davies et al. 2005; Moser et al. 2005; Thuiller et al. 2006a). Moreover human influence is a constant agent of change for regional alien species richness and diversity patterns (Maestre 2004; Gaston 2005). At more local scales features promoting alien plant naturalizations include availability of unexploited resources, natural disturbance and environmental stress (Alpert et al. 2000; Davis et al. 2000; Hobbs & Huenneke 1992; Lortie & Cushman 2007; Sher & Hyatt 1999; Cushman et al. 2004) as well as human mediated propagule pressure. The expression “propagule pressure” refers to the number of individuals (or viable propagules) released into a region where they are not native (Lockwood et al. 2005; Wilson et al. 2007; Britton-Simmons & Abbott 2008). Uncontrolled urbanization, suburban gardens and other human activities have been related to higher levels of propagule pressure for alien plant species. Consequently most proxies of human presence and activity tend to be particularly important determinants for the level of invasion of communities (O'Shea & Kirkpatrick 2000; McKinney 2002; Pyšek et al. 2002; Liu et al. 2005; Thuiller et al. 2006b). A highly invaded community or site (that is a community or site with a high level of invasion) may thus result either from strong human mediated propagule pressure or from environmental characteristics that make it more invasible or from a combination of both (Richardson & Pyšek 2006). In this thesis I attempt to disentangle the relative contribution of these two aspects (Fig. 1).

The role played by biotic interactions for successful plant invasions is one of the most intriguing and controversial issues which has occupied invasion ecologists. Two main aspects (diversity and the structure of invaded communities) have been at the center of debates. One first long lasting debate has revolved on the diversity of recipient communities. Some among the earliest studies addressing plant invasions (e.g. Elton 1958) found that more diverse communities better resisted invasion by alien species than communities with few native residents. Many studies have later shown, on the lines of Elton’s findings, a negative relationship between invasive and native species richness mostly in small plots (Levine et al. 2004), implying that highly diverse communities are characterized by some kind of ‘biotic resistance’ because of limited

(18)

available space and resources for newly introduced species. However a number of global, regional and landscape scale studies have instead demonstrated a positive relationship between invasive/alien and native species richness, pinpointing as reasons both species interactions and habitat filtering or comparable responses to the same or covarying external factors (Stohlgren et al., 1999; 2003; Sax, 2002; Fridley et al., 2004; Davies et al., 2005; Richardson et al., 2005). These contrasting patterns can however be theoretically reconciled by recognizing that the relationship between native richness and invasion success changes with sampling scale: at a large scale a series of negative relationships is enclosed in a general positive relationship (Shea and Chesson 2002). A second much debated and unresolved conundrum has regarded the structure of invaded communities (i.e. functional and phylogenetic composition). Phylogenetic relatedness combines multiple functional trait information and is a good proxy for niche similarity, provided that traits and thus niches are conserved along evolutionary history. Two opposing hypotheses were originally proposed by Darwin (1859) about the influence of evolutionary history on naturalizations. Relatedness of invaders to native communities on the one hand is predicted to hamper naturalization due to niche overlap and

competition with native species (Darwin’s naturalization

hypothesis). On the other hand appropriate niche-adaptations may instead favor the naturalization of closely related introduced species (Habitat filtering) (Duncan & Williams 2002). Previous studies have found support alternatively for either one of these hypotheses leading to a strong controversy in the literature (Daehler 2001; Diez et al. 2009; Lambdon & Hulme 2006; Ricotta et al. 2010). Among the reasons to explain this apparent discrepancy, appropriate scales, metrics and analytical tests are likely to play a major role (Thuiller et al. 2010). Both crucial questions highlighted in this paragraph are addressed and discussed in the following thesis.

A useful theoretical framework to address biotic interactions in the context of invasions and to express the link between invaders and native communities is provided by the α niche concept (Silvertown et al. 2006). The α niche expresses the resources exploited by a species in comparison to the resources exploited by co-existing species (Pickett & Bazzaz 1978). It is therefore a community-scale measurement indicating the niche differentiation between a species and the community and can be quantified by relying on functional or

(19)

phylogenetic distances (Thuiller et al. 2010). In the functional trait space, the α trait niche could be measured by the distance from the invader's trait value to the community average trait value (Ackerly & Cornwell 2007), while in the phylogenetic space, it could be defined as the mean phylogenetic distance of the invader to the rest of the community. This conceptual background is at the base of the last part of this thesis.

Drivers of plant diversity across spatial scales: from environmental filters to biotic interactions

As the previous section has highlighted, scale is a central issue in invasion ecology, and is often the key for theoretically reconciling apparently contrasting patterns in this field (Catford & Downes 2010; Jones et al. 2010; Stohlgren et al. 1997; Stohlgren et al. 2002). Nevertheless, scale is often ignored in empirical studies of invasions and there has not been much specific research. However a lot can be learned from what has been done in the general field of community ecology.

Ecological phenomena in general are scale dependent and the resolution at which communities are sampled is known to affect results in plant community ecology (Hanan & Ross 2010; Huston 1999; Qian & Kissling 2010; Rocchini et al. 2010; Willis & Whittaker 2002). A local plant assemblage can be viewed as the result of a process of deletion by which the environment acts as a filter for the regional species pool removing those species (or, more realistically, increasing their probability of being removed) lacking the adequate trait attributes for persisting under that given set of conditions (Keddy 1992; Díaz et al. 1998). Chance biogeographical events (e.g. dispersal), climatic conditions, environmental productivity, disturbances and biotic interactions (e.g. competition, facilitation and predation) are examples of such filters which tend to operate at increasingly finer spatial scales (Grime 1998; Lortie et al. 2004; Michalet et al. 2006; Forey et al. 2008). Following Pickett & White (1985), community patterns may be analyzed at four spatial scales, the patch scale (or neighborhood scale, Naeem et al. 2000), the local scale (Mittelbach et al. 2001), the regional scale (Pärtel et al. 1996; Loreau et al. 2001; Mittelbach et al. 2001) and the continental scale (MacArthur & Wilson 1967). Chance biogeographical events are believed to be most influencing at the largest (continental) scale (Zobel 1992; Mittelbach et al. 2001).

(20)

Climate is probably the major driver of species distributions and of biodiversity at regional scales of analysis (Thuiller et al., 2003; Thuiller et al., 2004), followed by present and historical land use (Lavergne et al. 2005; Von Holle & Motzkin 2006). Natural disturbance and environmental stress regimes are often most important at more local scales (Hobbs & Huenneke 1992; Sher & Hyatt 1999). Further, there is a large consensus on the idea that biotic interactions are prevalent at the smallest scale (i.e. the patch scale). At any particular site only those species or in general traits/functions which are viable under the prevailing climatic conditions, and then under the predominant disturbance regime at landscape level, have the opportunity to be “filtered out” (or not) by the interactions with other organisms at the local level (Díaz et al. 1998).

The relative importance of environmental filtering and biotic interactions in community assembly across scales is increasingly being addressed using phylogenetic relatedness as a proxy for trait and niche similarity. For example it has been reported that related species co-occurred in the same environmental unit at broader scales because of shared environmental preferences (clustering), while still avoiding interspecific competition and predation by occurring in mutually exclusive patterns at finer scales (overdispersion) (Cavender-Bares et al. 2006). Therefore both phylogenetic clustering indicating habitat filtering and overdispersion indicating biotic interactions of native species within communities can be found in the same system, but across different spatial scales.

All these aspects need to be taken into consideration for the study of invasions. Cross-scale field-based approaches are still needed in order to tackle many important issues, including both the relative importance of different “filters” and the extent to which successful invaders are related to native communities (Thuiller et al. 2010; Proches et al. 2008). In this thesis I will first analyze patterns at multiple scales and then merge the results (fig. 1).

Mediterranean coastal dunes: a perfect model system

Together with sandy beaches, dunes form a buffer zone and link between the marine system and the stabilized terrestrial land surfaces (Packham & Willis 1997). While the economic and social value of sandy shores is generally acknowledged, these characteristic

(21)

ecotones also contain a distinctive biodiversity and have special ecological features that are often not recognized. They are highly constrained by environmental filters, subject to natural stress and disturbance, characterized by sea-inland gradients and vegetation zonation, threatened by human impact and finally highly invaded by alien species. Here I briefly address one by one all these features. Given that coastal sand dunes occur at almost all latitudes, climatic conditions and ecological habitats developing on coastal dunes are very diverse, covering biomes which range from polar to tropical latitudes (van der Maarel 1993; Martínez et al. 2004). However all over the world, the vegetation found in such ecosystems must be able to tolerate a wide range of environmental features that vary in space and time making of sandy shores a typical example of a severely constrained ecosystem in which environmental filters are particularly intense. On Mediterranean shores the total local species pool is filtered by harsh environmental conditions acting at the broad scale including summer droughts, high air temperatures, large temperature fluctuations, intense solar radiation (incident and reflected), erosion and coastline movements (Forey et al., 2008; Rubio-Casal et al. 2010). At a finer resolution, these regional limiting factors are likely to be overridden by local ones. Extreme physical stress and disturbance factors caused by low levels of soil nutrients and soil moisture, soil salinity and pH, highly permeable and abrasive substrate, strong winds, substrate mobility, sand accumulation, episodic over-wash and immersion, and salt spray all come into play in coastal ecosystems (Oosting & Billings 1942; Salisbury 1952; van der Valk 1974; Barbour et al. 1985; Clark 1986). However, how they influence the vegetation and which factor is most determinant are still controversial questions.

Coastal dune habitats are often described as being “stressful” and frequently “disturbed”. Extreme soil conditions cause abiotic stress on dune vegetation by limiting the rate of dry matter production. Grime (1979) defined stress as: “the external constraints which limit the rate of dry matter production of all or part of the vegetation”. According to this definition, stress causes a predictable and rather continuous deviation from the optimum conditions (usually a reduction) in variables such as photosynthetic productivity, biomass production and reproduction. However, dune environments are also frequently subject to natural disturbances, which are stochastic

(22)

events that directly cause the physical destruction of species. Grime (1979) defined disturbance as “the mechanisms, which limit the plant biomass by causing its partial or total destruction”. Disturbance can be particularly high in coastal foredunes and includes wind action during storms, salt spray, occasional flooding by sea waves and sand movement. The latter can lead to burial, exposure, or physical damage from sand-blasting. Consequently, disturbance induced by sand burial (Wilson & Sykes 1999; Moreno-Casasola 1986; Maun 1998) and stress caused by salt (Barbour & De Jong 1977; Debez et al. 2004 ; Franks & Peterson 2003; Oosting & Billings 1942; Sykes & Wilson 1991) are the two main abiotic factors believed to drive community zonation on coastal dunes. In fact, sandy shores are characterized by the presence of gradients of soil mobility (sandy sediments) and salinity (sea spray). Characteristics of the substrate and wind-sea action vary along the dune profile giving rise to a steep sea-inland environmental gradient, which determines the progressively increasing intensity of natural stress and disturbance on coastal dune vegetation (Wilson & Sykes 1999; Forey et al. 2008). This allows the coexistence of different plant communities in relatively small spaces (Frederiksen et al. 2006), leading to complex mosaics and a long known zonation phenomenon in coastal dunes worldwide (Doing 1985). It consists in the formation of zones or belt-like plant communities in which the species show a fairly distinct range of tolerance. Worldwide similar coastal dune sequences have been described along the beach-inland gradient. Usually, the full sequence of vegetation from pioneer to mature types includes upper beach, foredune, mobile dune, transition dunes and fixed dune plant communities. This “standard zonation” is optimally developed in warm-temperate, humid climates and shores, exposed to ocean tides and winds (Doing 1985). The environmental requirements of coastal phytocoenoses are very specific, so their position in the phyto-toposequence tends to be fixed. For example, the backdune vegetation is theoretically progressively less exposed to the rigid conditions of the foredunes and, gradually, less tolerant to salt spray, winds, and sand burial, while upper beach species are generally pioneer and stress tolerant (Wiedemann & Pickart 2004; Acosta et al. 2009). As a consequence, one of the main characteristics of coastal dunes is their high ecological diversity due to environmental heterogeneity and the spatial variability of the plant communities (Van der Maarel 1993; Acosta et al. 2000; Acosta et al.

(23)

2005). Ever since the early studies performed by Cowles, more than a century ago (1899), zonation on coastal dunes along this gradient has been the focus of much research. Importantly, the studies by Cowles were seminal for Clements who, almost 20 years later (1916), proposed the successional theory of plant communities, which became a key concept in ecological theory (Martínez et al. 2004). In synthesis, because of their dynamic nature and of the strong zonation patterns exhibited by the vegetation sandy coastal habitats have long been typical model systems for the study of abiotic factors driving community change (Oosting & Billings 1942; Olson 1958).

The relationships between coastal communities and environmental determinants have been mainly studied in oceanic environments. In New Zealand both sand burial and salt were important in determining zonation (Sykes and Wilson, 1991; Wilson and Sykes, 1999), and in South African coastal dunes the interaction between sand burial and nutrient limitation was very important to understand the zonation (Gilbert et al. 2008). On French Atlantic coasts sand burial was most important for community composition on a local level, while salinity had lower importance (Forey et al. 2008). Similar studies have been conducted on other northern European coasts focusing on different parameters including soil characteristics (Frederiksen et al. 2006), pH (Isermann 2005) and wind dynamics (Jungerius & van der Meulen 1997). Conversely, to owr knowledge, no studies have concentrated on the role of environmental factors on coastal communities in the Mediterranean basin. This thesis is a first attempt to do so.

Coastal sandy ecosystems in Europe have been largely altered by human activities, and many dune systems have already been extensively degraded (Acosta et al. 2006; Carter 1991; Grootjans et al. 1997; Martínez et al. 2004). Human activities in littoral areas, including suburban development and touristic exploitation, have historically been widespread and are ever increasing (Brown & McLachlan 2002; Defeo et al. 2009). Nowadays, approximately one third of the European population lives less than 50 km away from the coast. The degradation and loss of the littoral landscape has concerned all coastal countries of the European Union, and is particularly striking on the coasts of the Mediterranean sea. Consequently, several coastal sandy habitats were included in the

(24)

European Council Habitat Directive 92/43/EEC, the most important legal tool for nature conservation in the European Union. The latest national report on the implementation of the Habitat Directive concludes that “1. Coastal and halophytic habitats” and “2. Coastal sand dunes and inland dunes” are the typologies with the worst conservation state in Italy with only ca. 20% and 10% of their extent in a favorable state respectively (La Posta et al. 2008). Alas, in spite of national and international conservation measures, Mediterranean coastal dunes remain among the most fragile and threatened ecosystems in Europe.

Significant changes are predicted to take place in Mediterranean biodiversity in the near future, and the invasion by exotic species is considered one of the main factors responsible for these changes (Sala et al. 2000). Sandy shores have been affected by the establishment and spread of numerous alien plant species worldwide (Bruno et al. 2004; Dark 2004; Von Holle & Motzkin 2007; Chytrý et al. 2008a), in the Mediterranean basin (Badano & Pugnaire 2004; Campos et al. 2004, Sobrino et al. 2002) and specifically in Italy (Brundu et al. 2003; Acosta et al. 2008; Izzi et al. 2007; Paper 2). Further, as we have seen, sandy coasts are nowadays subjected to uncontrolled suburbanization and tourism development, both of which support the introduction of propagules in the neighboring natural landscape (Alston & Richardson 2006). Focusing on how alien invasion patterns vary along directional natural gradients in the presence of strong human driven propagule pressure is a promising research lane in the field of invasion ecology. In this sense, coastal dune habitats provide a unique opportunity to shed further light on what drives the invasibility of communities. Nevertheless, up to date very few studies have taken full advantage of these features (partially Lortie & Cushman 2007).

Aims

In synthesis Mediterranean coastal dunes are simultaneously classical model systems for the study of environment/plant relations, strongly altered by humans and highly invaded: they are thus ideal to understand features that make plant communities more invasible. Furthermore they are conservation targets at the European level, for which plant invasions are a recognized prime agent of alteration. Given this, the general goal of this thesis is to analyze plant invasion

(25)

patterns on coastal dunes of Central Italy. This is achieved by pursuing two main aims, subdivided in four specific objectives. 1) The first aim is to pinpoint the filtering factors that drive plant invasion patterns per scale (Fig. 1). Two specific objectives are addressed:

a) to compare and contrast regional scale filters that act on native and on naturalized alien plant species in dune systems of the region Lazio using a coarse sampling resolution (Fig. 1). The study in chapter 1 explores the relative importance of the main environmental drivers of large scale diversity patterns (climate and land cover) and of proxies of human mediated modifications (population density and tourism pressure).

b) to explore local scale environmental filters (stress and

disturbance) and local human activities on invaded

Mediterranean coastal dunes using a fine sampling resolution. Chapter 2 analyzes the importance of small scale sea-inland stress and disturbance gradients next to propagule pressure for alien species presence and spread along the vegetation zonation. This chapter builds upon two works which are reported in the appendix (Fig. 1). The study in appendix E quantifies the main sea-inland environmental gradients and explores how they influence native vegetation zonation in the Mediterranean basin (Lazio and Sardinia). The study in appendix D describes differences in level of invasion among the typical plant communities of the Tyrrhenian vegetation zonation (Province of Rome).

2) The second aim is to demonstrate the importance of the spatial resolution for the investigation of alien invasion patterns:

c) by addressing for the first time with field data a long lasting conundrum in invasion ecology (Darwin’s naturalization hypotheses). Chapter 3 relies on phylogenetic relationships to uncover the varying importance of habitat filtering and biotic interactions with sampling resolution on shores of central Italy (Lazio, Abruzzi and Molise – Fig.1).

d) by merging results obtained at different scales to highlight the main differences between local and regional patterns for both extrinsic abiotic factors and biotic factors (General conclusions).

(26)

Figure 1. Outline of the thesis summarizing the different aspects addressed in each chapter. For each chapter the main gradient analyzed is reported, the sampling resolutions used, the regions or provinces where sampling took place (region Lazio, province of Rome, or other regions – Sardinia, Molise and Abruzzi), whether alien or native species patterns or both are considered, and finally whether environmental filtering, human impact or biotic relations are analyzed.

Latitudinal Sea-inland ca. 35 km2 64 m2 4 m2 Native Alien Human Environment Biotic CHAP. 3 CHAP. 1 M a in g ra d ie n

t CHAP. 2 APP. D APP. E

R e s o lu ti o n E x te n t S C A L E S p e c ie s P a tt e rn F ilt e ri n g

(27)

CHAPTER 1 Disentangling the relative effects of environmental versus

human factors on the abundance of native and alien plant

species in Mediterranean sandy shores

1

INTRODUCTION

Many factors govern plant community assembly and invasibility (Richardson & Pyšek 2006). Understanding which specific features affect native plant assemblages is ever more important in light of the increasing global loss of biodiversity. In general, environmental factors that have been found to influence patterns of species richness at a regional scale include climate, landscape heterogeneity, spatial patterns, geomorphologic processes and level of protection (van Rensburg et al. 2002; Hawkins et al. 2003; Davies et al. 2005; Moser et al. 2005; Thuiller et al. 2006a). Moreover human influence is nowadays one further important agent of change for species richness and diversity patterns (Maestre 2004; Gaston 2005). Human population density and proxies thereof have often been shown to correlate positively with species richness in response to similar factors, such as productivity, (Balmford et al. 2001; Araújo 2003; Chown et al. 2003), a congruence that suggests a marked conflict between conservation and development. However, depending on spatial scale and overall level of urbanization, intense human disturbance can finally lead to an inversion of this tendency with troubling effects on native biodiversity (e.g. Koh et al. 2006). At the same time, the abundance of alien species is also strongly affected by features of the recipient environment influencing community invasibility (Rejmánek et al. 2005; Thuiller et al. 2010). Pinpointing abiotic and socio-economic factors associated with greater abundances of neophytes and with higher levels of invasion can thus help elucidate the threat of biotic exchange (Dark 2004; Richardson et al. 2005). Human related factors tend to be particularly important (O'Shea & Kirkpatrick 2000; McKinney 2002; Pyšek et al.

1_{This chapter corresponds to Paper 4, published in Diversity and Distributions}

(28)

2002; Liu et al. 2005; Thuiller et al. 2006b). This is consistent with theories that relate urbanization and other human activities to higher levels of propagule pressure (a measure of the number of individuals released into a region to which they are not native; Lockwood et al. 2005; Wilson et al. 2007; Britton-Simmons & Abbott 2008) which increase chances of alien species establishment (Alston & Richardson 2006). Studies considering both introduced and native species have also generally found a greater importance of factors associated with human disturbance for alien species (Deutschewitz et al. 2003; Arévalo et al. 2005).

Regional-scale observational studies consistently find a positive native-alien species richness correlation. Such emergent patterns have been partially explained in terms of ecological processes including species interactions and comparable responses to the same or covarying external factors (Stohlgren et al. 1999, 2003; Sax 2002; Fridley et al. 2004; Davies et al. 2005; Richardson et al. 2005). However, how environmental and human determinants differentially influence alien species distribution patterns in contrast with native ones has not yet been convincingly clarified, particularly in very stressful ecosystems. Extrinsic factors that favour high numbers of native species may also directly increase niche opportunity for invaders or different specific determinants may facilitate the establishment of alien species (Davis et al. 2000, Thuiller et al. 2010).

We use Mediterranean coastal sand dunes as target ecosystems to tease apart environmental determinants from human-related parameters underlying patterns of richness for native and alien species. Sandy shores are a typical example of a severely constrained ecotone in which both kinds of determinants are particularly intense. Extreme physical stress and disturbance factors (e.g. sand burial, wind or salinity) act at very small spatial scales shaping community zonation along the dune profile in a gradient from pioneer communities on the beach to shrublands and macchias on fixed dunes (Wilson & Sykes 1999; Acosta et al. 2008). The total local species pool is moreover filtered by severe environmental conditions acting at the broad scale including summer droughts and coastline movements (Forey et al. 2008). At the same time, human activities in littoral areas, including suburban development and touristic exploitation, have been historically widespread (Brown & McLachlan 2002; Defeo et al. 2009).

(29)

The aim of this work is therefore to explore how the interplay of environmental and human factors determines native-alien patterns of plant richness at a regional scale but focusing specifically on coastal dune habitats. Considering the level of transformation of Mediterranean coasts we hypothesize a strong influence of human activity on both the native and alien flora. In particular, for alien species we may expect to find a strong role of human-mediated introduction and propagule pressure as the main drivers of invasions,

whereas environmental factors, generally more important

determinants of patterns of native species richness, should play a secondary role.

SYNTHETIC DESCRIPTION OF METHODS

To achieve these objectives we analyzed the alien and native plant richness of coastal holocenic dunes on 250 km of the Italian

Tyrrhenian coast (Region Lazio) using a 3’ by 5’ (ca. 35 km2) grid

(figure 1.4). We studied the effect of environmental and human drivers selecting a total of 25 predictors (see table SA.2 in Supplementary Material). We fit separate generalized additive models (GAMs) for native richness, for alien richness and for alien richness after controlling for the influence of native richness. Specifically we fit GAMs in a multimodel-inference framework after an explicit treatment of multicolinearity and accounting for spatial structures in the data using an autocovariate term (SAC). The weight of evidence in favour of a given variable was calculated using

Akaike weights (wi). Comprehensive randomisation procedures were

carried out to estimate the absolute contribution (∆p) of

environmental and human correlates in explaining the observed patterns.

RESULTS

We found a total of 550 species on the entire Tyrrhenian coast. Alien species make up 8% of the total plant species richness in the study area (see table SA.1 in Supplementary Material). Moreover, alien and native richness are positively related (r=0.50, p<0.001; figure 1.1), but different external correlates determine their spatial pattern.

(30)

Figure 1.1. Positive relationship between alien and native species richness (Pearson correlation r=0.50, p<0.001).

For natives, three variables had absolute weights greater than zero (figure 1.2a; Adj. R-square: 0.464, p<0.001). Human population density (correlated with degree of urbanization) was the most important factor and was negatively related to richness (figure 1.3a). The negative effect of human impact on native species richness seems to level off at population densities greater than 40 residents per ha. Numbers of natives were also decreased by high proportions of natural land cover and, to a lesser degree, affected by the progress of the coastline (higher percentages of advancing coastline favour greater numbers of native dune species) (figure 1.3a; figure SA.1). No spatial autocorrelation of native richness was detected by examining Moran Is (st. deviate = 0.937, p-value = 0.1744). However we highlighted a certain degree of spatial clustering for alien richness (Moran I st. deviate = 1.608, p-value = 0.05), especially after controlling for native richness (Moran I st. deviate = 3.653, p-value < 0.001).

(31)

Figure 1.2. Absolute weights of evidence (∆p) of independent variables for explaining

from left to right patterns of native and alien richness, and of residuals of alien richness after simple linear regression on native richness.

The model for alien richness included five variables with positive absolute weights, with precipitation and natural surfaces as most important variables, followed by progress of the coastline, recent development and the spatial autocovariate (figure 1.

square = 0.373, p<0.001). More aliens are found in sectors that receive greater precipitation and have lower winter temperatures (as they were negatively correlated) (figure 1.3b).

After controlling for natives, the spatial autocovariate term (SAC) was the most important variable for alien patterns (figure

) of independent variables for explaining from left to right patterns of native and alien richness, and of residuals of alien

The model for alien richness included five variables with positive absolute weights, with precipitation and natural surfaces as most important variables, followed by progress of the coastline, recent 1.2b; Adj. R-square = 0.373, p<0.001). More aliens are found in sectors that receive greater precipitation and have lower winter temperatures (as iate term (SAC) was the most important variable for alien patterns (figure 1.2c; Adj.

(32)

R-square = 0.587, p<0.001). As for the influence of human factors, alien introduction appears to be related not to overall degree of urbanization but only to recent urban development after the 70’s (figure 1.2c). Alien richness tends to increase with density of recent buildings, but evens out at higher densities (figure 1.3c). Annual precipitation and advancing coast were again important variables for alien richness also after removing variability explained by native richness.

Figure 1.3. Response curves for the three most important independent variables of GAMs for native (a) and alien (b) richness, and for residuals of alien richness variability after simple linear regression on native richness (c). Additional response curves for the other independent variables in Supplementary Material.

(a)

(b)

(c)

square = 0.587, p<0.001). As for the influence of human factors, alien introduction appears to be related not to overall degree of development after the 70’s 2c). Alien richness tends to increase with density of recent 3c). Annual precipitation and advancing coast were again important variables for fter removing variability explained by native

3. Response curves for the three most important independent variables of GAMs for native (a) and alien (b) richness, and for residuals of alien richness variability after simple linear regression on native richness (c). Additional response

(33)

Figure 1.4. Map of residuals of alien richness after simple linear regression on native richness along the coast of the Region Lazio (42°23’N, 11°39’E to 41°11’N, 13°20’E).

DISCUSSION

Tyrrhenian sandy shores sectors richer in native plant species harbour more introduced species, as has been previously reported at comparable scales of analysis in other areas. Bruno et al. (2004) in particular observed this relationship even on coastal en

North America. Several authors have observed that the same external factors were independently driving a similar response of both alien and indigenous species (Richardson et al. 2005; Kumar et al. 2006; Stohlgren et al. 2006). In particular, Deutschewitz et al. (2003) found at a regional scale of analysis comparable to our study that similar factors were influencing both alien and native species

different order of importance. The situation appears to be more complex in the coastal environment, where for a large part

and uncorrelated drivers regulate richness of native plants and abundance of alien species.

4. Map of residuals of alien richness after simple linear regression on native richness along the coast of the Region Lazio (42°23’N, 11°39’E to 41°11’N,

Tyrrhenian sandy shores sectors richer in native plant species harbour more introduced species, as has been previously reported at comparable scales of analysis in other areas. Bruno et al. (2004) in particular observed this relationship even on coastal environments in Several authors have observed that the same external factors were independently driving a similar response of both alien and indigenous species (Richardson et al. 2005; Kumar et al. 2006; Deutschewitz et al. (2003) found at a regional scale of analysis comparable to our study that similar influencing both alien and native species, even if in different order of importance. The situation appears to be more for a large part different and uncorrelated drivers regulate richness of native plants and

(34)

While we assumed that physical environmental factors would be important determinants of the distribution of native plant species, we were only able to show a strong response to human pressure. Human population density (positively related to overall level of urbanization) negatively impacts native plant richness, and is the predictor variable with the highest weight of evidence. This result is in contrast with the theory of coincidence of biodiversity with human population (Araújo 2003). However, studies supporting this theory have generally been conducted at rather coarse scales, while it has been noted that at finer spatial resolutions the relationship between species richness and human density may turn negative (Gaston 2005; Pautasso 2007). Nevertheless, Deutschewitz et al. (2003) still found a positive correlation with urbanization with the same grain used in our study. However, human pressure on Mediterranean shores is often quite extreme (Acosta et al. 2006) and other authors have suggested that very intense human disturbance may also cause an inversion of the correlation with human population density (Koh et al. 2006). Moreover, coastal environments are particularly sensitive to anthropogenic changes (Defeo et al. 2009). In fact there are a number of ways in which human disturbances can affect sandy shore habitats. A direct impact on the vegetation is related to exploitation for tourism (which in our study is correlated to population density; e.g. for bathing establishments r>0.5), leading to trampling and destructive beach management practices. Intensive management typical of many touristic beaches of Lazio includes mechanical cleaning and dune flattening and affects primarily mature stands of the mobile dune but eventually also pioneer communities of the beach which is the most heavily exploited zone. Such a simplification of the community gradient in dunes inevitably leads to lower overall species richness at the grain examined in this study. Moreover, human disturbances can also have other more indirect effects (coastal erosion, infrastructural barriers landwards blocking the retreat of the vegetation, pollution) on diversity by altering the overall dynamic equilibrium of the coastal ecotone and the successional processes of the vegetation.

Richness of native plants was also inversely related to the percentage of natural land cover in the surrounding landscape, a fact which may appear somewhat surprising at first sight. However, natural cover is negatively correlated with agricultural land use, which may support the introduction of native weeds and ruderal species directly

(35)

favoured by farming activities (Prach et al. 2001). Moreover, private farmed lands represent quite effective barriers for touristic exploitation since they offer few public accesses to the beach. Conversely, Tyrrhenian natural areas are very fragmented and have often been inappropriately reforested (Bellarosa et al. 1996) representing in this way rather an incentive for summer tourists frequentation and consequently channels of disturbance with negative effects on native diversity.

Physical environmental factors appear to influence patterns of native species only moderately. In fact only an effect of the movement of the coastline is supported by a small positive absolute weight of evidence. The advancing coastline, which is inversely related to coastal erosion, appears to favour native richness, probably by influencing the overall community zonation. The continuous deposition of sand is fundamental for the formation and conservation of a wide beach area, embryo dunes and mobile dunes (Packham & Willis 1997). Several seaward plant communities (on the beach, embryo dunes and mobile dunes) are therefore more common on progressing coasts with more complex dune profiles leading to a more complete vegetation zonation and greater habitat heterogeneity. For example progressing coastlines offer greater availability of beach habitat which is colonized by typical pioneer communities of specialized halophylous and psammophylous native species such as

Cakile maritima and Salsola kali (e.g. Packham & Willis 1997; Debez et al. 2004). Moreover, many typical species of the mobile dune, Ammophila arenaria (L) Link being the prime example, are very specialized and have particular adaptations for sand burial and accumulation (Maun 1998) and are thus less frequent or declining in those coastal sectors where sand build up is not important.

In contrast with patterns observed for native species, the key driver of alien plant richness was not anthropogenic but climatic. We found more introduced species in more mesic and cooler sectors of Tyrrhenian sandy shores. A strong positive effect of precipitation on the number of naturalized aliens has been reported even at the European level (Lambdon et al. 2008). Even though the opposite trend has been reported as well, with more non-native species in warmer and drier sectors (Gasso et al. 2009), it is a widely shared idea that alien species are more successful invaders where environmental conditions are not excessively harsh and resources are not limiting (e.g., light, nutrients, and water). This is in relation to

(36)

theories that suggest that competition intensity and thus biotic resistance are inversely correlated with the amount of resources available (Alpert et al. 2000; Davis et al. 2000; Richardson & Pyšek 2006). From this point of view, in xeric environments such as coastal dune systems, the increase in water availability due to higher precipitation may play an important role on alien plant abundance. Indeed in other physically challenging semiarid environments, for example of North America, observational (Hobbs & Mooney 1991; Hunter 1991) as well as experimental (Milchunas & Lauenroth 1995) studies have also found a positive influence of higher annual precipitation or water availability on invasion by aliens (Dukes & Mooney 1999).

Two factors with influence on alien abundance (natural cover and advancing coastline) show similar relationships as with native species, a fact which may partially help explain the positive correlation among the two groups of species. Firstly, more neophytes are associated with fewer natural areas, probably again rather in relation to agricultural lands which may represent introduction sources for some species. However other factors are also probably at play here, since farming does not seem to be a likely invasion pathway for many non-native species we recorded (table SA.1). Secondly, progressing coastlines as highlighted for natives increase habitat heterogeneity, and thus provide more opportunities for alien species as well as for natives (Deutschewitz et al. 2003; Kumar et al. 2006).

On the other hand population density, although strongly correlated with several urbanization, tourism and beach exploitation indicators (all sources of propagule pressure in coastal environments) does not have a positive effect on numbers of aliens. Chytrý et al. (2008b) focusing on many different habitats and multispecies assemblages also found that the effect of propagule pressure (human-related proxy variables) on the abundance of alien species was very small relative to the effect of local habitat properties. Indeed the relative contribution of propagule pressure to abundances of alien species may vary widely depending on the habitat examined. Under the extreme conditions typical of coastal habitats, propagule pressure appears to play a less important role for the abundance of non-native species, in contrast to trends observed in other environments for several alien species (Lockwood et al. 2005; Rouget & Richardson 2003). In our study the only strong exception is recent coastal

(37)

suburbanization after controlling for native richness, which appears to be the most effective source of propagules for aliens in the study area (besides perhaps a minor role of farming). Garden areas associated with urban sprawl and with summer structures built after the 70s, often without clear urban plans and with gardens directly facing the beach, support the continuous introduction of alien plants on the neighbouring sand dune system. In fact for a noticeable proportion of the alien flora found on natural dunes, including the invasives Carpobrotus acinaciformis and Agave americana, gardening is the most likely invasion pathway. Alien richness thus increases with coastal urban sprawl up to a certain point, levelling off only when extreme suburbanization removes out a number of propagule sources for alien species, like gardens and intensive crops, leading to a decrease of the exotic flora.

While no spatial autocorrelation could be detected for native richness, we highlighted the spatial clustering of alien richness, in particular after removing variability explained by natives (in which case spatial patterning was the most important explanatory variable). Autocorrelation is especially interesting in the case of alien plants because it suggests a spreading trend related to one or few specific source sites that account for the majority of introductions (Pino et al. 2005). For instance, hotspots of alien richness may be related to larger urban nuclei in the inland (e.g. Rome; figure 1.4).

CONCLUSIONS

On Tyrrhenian Italian sandy coasts, while native and alien richness are positively correlated, by and large different variables influence their spatial patterns. Contrary to what we might have expected, native plants are more affected by human factors than alien species, which at this resolution are strongly influenced by environmental conditions. The physical harshness of the coastal environment may play an important role in explaining this apparent paradox on multiple grounds. Specialized and well adapted native species in a fragile equilibrium with their natural environment are extremely sensitive to environmental modifications brought about by humans. On the other hand, for more generalist alien species known to naturalize across a wide range of niches in Mediterranean systems, the availability of the limited resources plays a predominant role. In this context, quite surprisingly, overall human development appears

(38)

to be less important for the abundance of introduced species than may have been anticipated.

From a conservation perspective these findings can offer important guidance for regional level managers of coastal sandy systems in the Mediterranean. First of all, there appears to be a strong conflict between human activities close to the coastal landscape (residential and related to tourism, which is highly important for the local economy of many Mediterranean areas) and the preservation of native plant biodiversity on dunes. The importance of more sustainable beach management practices on Mediterranean coastal dunes cannot be overemphasized. On the other hand, exotic species control measures in these physically challenging semiarid environments need to be carried out keeping in mind that sectors with greater availability of limiting resources (e.g. water) may be more exposed to alien species establishment. On the introduction front, urban sprawl and garden areas should be closely monitored, as they appear to be the key sources of propagules in these environments.

SUPPLEMENTARY MATERIAL

Additional Supplementary Material may be found in the electronic Appendix A.