Marine alien species as an aspect of global change

Advances in Oceanography and Limnology ISSN: 1947-5721 (Print) 1947-573X (Online) Journal homepage: https://www.tandfonline.com/loi/taol20 Marine alien species as an aspect of global change Anna Occhipinti-Ambrogi & Bella Galil To cite this article: Anna Occhipinti-Ambrogi & Bella Galil (2010) Marine alien species as an aspect of global change, Advances in Oceanography and Limnology, 1:1, 199-218, DOI: 10.1080/19475721003743876 To link to this article: https://doi.org/10.1080/19475721003743876 Published online: 05 Jul 2010. Submit your article to this journal Article views: 2575 View related articles Citing articles: 12 View citing articles Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=taol20 Advances in Oceanography and Limnology Vol. 1, No. 1, June 2010, 199–218 Marine alien species as an aspect of global change Anna Occhipinti-Ambrogia* and Bella Galilb a Department of ‘Ecologia del Territorio’, University of Pavia, Pavia, Italy; bNational Institute of Oceanography, Israel Oceanographic & Limnological Research, Haifa, Israel (Received 6 December 2009; final version received 22 February 2010) The transport of organisms across oceans is an anthropogenic agent of global change that has profoundly affected the natural distribution of littoral biota and altered the makeup of biogeographic regions. The homogenization of marine biotas is a phenomenon especially affecting coastal regions and is spearheaded by a suite of opportunistic species at the expense of native species. Climate change may exacerbate the trend: sea surface temperatures, hydrodynamics, pH and carbonate cycles, already show marked fluctuations compared to the past. Alien invasive species are impacted by the change of marine climate in a variety of ways, which are we have just begun to notice, observe and interpret. A conceptual framework has yet to be conceived that links theories on biological introductions and invasions with the physical aspects of global change. Therefore predicting the scale of invasions or their impact on biodiversity is a daunting task. Integration of biological and environmental information systems, niche models, and climate projections would improve management of aquatic ecosystems under the dual threats of biotic invasions and climate change. The recorded spread of alien species and analysis of patterns of invasions may serve as the starting point for searching connections with climate change descriptors. The Mediterranean Sea is home to an exceptionally large number of alien species, resulting from its exceptional history and multiple vectors. For much of the twentieth century alien thermophilic species, which had entered the Mediterranean through the Suez Canal, have been confined to the Levantine Basin. In recent years climate driven hydrographic changes have coincided with a pronounced expansion of alien thermophilic biota to the central and western basins of the Mediterranean. We discuss some changes in emergent functions and services in Mediterranean ecosystems under the combined effect of invasive species and climate changes. Keywords: bioinvasions; alien species; climate change; Mediterranean Sea 1. Introduction Biological invasions in world’s oceans are not only an academic subject for marine biology specialists, but a growing concern for both nature conservation and economic activities; while the awareness of the general public is being raised by national governments and international agencies. Alien taxa (synonyms: exotic, non-native, non-indigenous, allochthonous) are species, subspecies or lower taxa introduced outside of their natural range (past or present) and outside of their natural dispersal potential. Their presence in the given region is due to intentional or unintentional introduction or care by humans, or they have arrived there without the help of people from an area in which they are alien. *Corresponding author. Email: [email protected] ISSN 1947–5721 print/ISSN 1947–573X online ß 2010 Taylor & Francis DOI: 10.1080/19475721003743876 http://www.informaworld.com 200 A. Occhipinti-Ambrogi and B. Galil This includes any part, gamete or propagule of such species that might survive and subsequently reproduce [1–4]. Invasive species are those alien taxa that have established large populations, significantly expanding their range, and/or exert substantial negative impact on native biota, economic values, or human health [5]. This paper encompasses different scientific approaches that have been proposed to deal with changes caused by alien species introductions and issues of ‘global change’. This latter is mainly perceived as change in the earth’s climate, but in fact it is closely interlinked with the evolution of biodiversity of our planet [6,7]. The interactions between the global change in distribution of biota and the global change of habitat conditions, mainly caused by climate warming, are highly complex and will be outlined in the next section of the paper. Bio-invasions processes are very dynamic and their outcome depends not only on human mediated transport, but also on the physical chemical and biological conditions of the receiving environment and hence (in a global perspective) on climate change and its related consequences. Ecological equilibria will evolve and predictions are still rather rough. In Section 3 some approaches are outlined and some of the changes that are already beginning to emerge are quoted. The Mediterranean Sea, for historical, physical and biological reasons, is an area where signals of early alert are visible, and examples from the literature in Section 4 will be used to further document the changes that are rapidly taking place under the combined pressure of alien species and climate change. 2. Climate change and alien species: a framework of possible interactions Climatic variables are primary drivers of distributions and dynamics of marine communities ([8–10] and References therein). Climate change is affecting the marine systems through warmer temperatures, hydrographical changes, carbon cycle and acidiphication. In the same time human activities, such as shipping, aquaculture, and canal construction, are affecting species distribution worldwide. These changes are expected to have a profound effect on the structure and productivity of marine ecosystems. Though often considered independent of each other, there is a strong likelihood that these two primary drivers of global environmental change interact. Climate change may enhance the ability of certain alien species to invade new regions, while simultaneously eroding the resistance to invasion of native communities by disturbing the dynamic equilibrium maintaining them. Climate change facilitates overcoming historic geographic barriers (e.g. through the opening of new polar routes for navigation due to ice melting). Eventually this will increase the societal and environmental impacts of alien species [11,12]. 2.1. Global warming and shift in distribution of species To the extent that dispersal and resource availability allow, species are expected to track the warming climate and shift their distributions towards higher latitudes. Polewards range shifts have been observed in many regions and across different taxa [13]. Records show significant shifts of phytoplankton and zooplankton communities in concert with regional oceanic climate regime shifts [14]. Shifts in marine fish and invertebrate communities have been well documented off western North America and the United Kingdom [10,15]. The distributions of 90 demersal species of exploited and non-exploited North Sea fishes responded to recent increases in sea temperature (þ1.05 C), with two-thirds of the species shifting in mean latitude, depth, or both, over 25 years. The shift was marked in particular Advances in Oceanography and Limnology 201 in short-lived and small sized species [16]. Such shifts augur profound impacts on commercial fisheries. These observations of climate driven range shifts may lead, over time, to alteration of latitudinal distribution and when these are checked by impassable barriers, to species extinctions. The consequences on local species richness are often foreseen as negative, but some recent observations are at variance with this paradigm: so far temperature increase has not led to biodiversity loss in North Sea fish fauna and even has a positive effect on species richness, with the advent of southern species [17]. The introduction of alien species by human-mediated transport is concomitant with range expansion caused by climate change; both agents result on the introduction of species in new habitats and regions, however some important differences have been underlined by Lonhart [18]: vectors and rates of movement are very different, so that man-mediated introductions are local and frequent while climate related expansions occur at large scale and slow rate; alien species often come from geographically disjoint areas, whereas range expansion implies contiguous areas; matching of habitat conditions and ecological characters of species in the latter is by far more difficult and coevolution is less probable. In spite of differences, the response of established invasive species to recent global warming mirrors native species: on the Pacific coast of North America, all nine of the invasive species that have apparently responded to recent global warming moved poleward [19]. The benthic fauna of the Antarctic region has been influenced by the effects of warming climate and ship-mediated introductions on species composition [20]. In particular, the Antarctic fauna is characterised, since late Eocene, by the absence of skeleton-crushing (durophagous) predators. This absence has been interpreted as a consequence of physiological barriers due to cold temperatures established in geological time following studies on palaeontology, biogeography, oceanography, physiology, molecular ecology, and community ecology [21]. Some alien species of predators, such as Hyas araneus (L.), and large king crabs, are now re-invading the Antarctica, owing to a warmer climate [19]. They have been probably introduced to Antarctica via the transport of adults on ships’ hulls or larvae in ballast water [22,23]. 2.2. Climatic conditions and the success of alien species in their new environment Climate change may impact the process of invasion by affecting the sources of alien species, pathways of dispersal, and their establishment in host ecosystems. Of these the last is the most important and relevant constraint, since the influence of climate change can be considered less decisive in generating additional propagule pressure, or to modify patterns and pathways of dispersal as they are defined primarily by human economic and trade activity [24]. After the introduction a given species may remain geographically confined for a period ranging from years to a century, followed by a phase of active population growth and expansion, or it may pass an asymptotic growth phase and disperse very quickly over a large geographic region. Numerous factors may trigger the rapid growth phase, notably natural or human-induced disturbances. Climate change, creating disturbance events, may favour previously quiescent alien species providing more chances to survive, reproduce and compete with native species [25]. Occhipinti-Ambrogi [26], on the basis of the model by Colautti et al. [27], has discussed climate change impact on the transition between different temporal stages of an alien species invasion, pointing out that modified climatic conditions affect the environmental filters between successive stages. In the following points we list five potential consequences of climate change on invasive 202 A. Occhipinti-Ambrogi and B. Galil species development and summarise the relevant key hypotheses, as reviewed by Hellmann et al. [12]. (1) Altered mechanisms of transport and introduction: propagule pressure may be altered by climate-dependent changes in maritime transportation routes [28,29], and in intentional introductions for mariculture, recreation or conservation objectives. (2) Altered climatic constraints on invasive species: warm stenothermal alien species will be able to spread further if conditions become more similar to their native range, and they will be able to establish persistent populations [30]. (3) Altered distribution of existing alien species: cold-temperature constraints on alien species will be reduced at their higher-latitude or depth range limits. Warmtemperature constraints on alien species will increase at their lower-latitude or depth range limits. Hydrologic constraints on alien species will be altered by changing current patterns and termohaline gradients [31,32]. Many invasive species are fast-growing and responsive to resources and will be favoured by environmental changes that increase disturbance and/or resource availability, which will facilitate their spread. (4) Altered impact of alien invasive species: the population densities of some invasive species already present in a given area, and thus their impact on native species, will be altered. Per capita or per biomass impacts of some invasive species will be altered through effects on their competitive interactions with native species [33]. Relative impact of some invasive species will increase when the abundance of native species or resources decrease in response to the invader [34]. (5) Altered effectiveness of management strategies for invasive species: since management practices such as eradication and biocontrol are seldom used at sea [35], potential alterations at his stage are less likely to occur than in inland waters. 2.3. Driving forces act synergetically Distribution shifts and range expansion of alien species can be favoured by climate change, but very often rely on continuous or even increasing propagule pressure by human transportation. Interactions among species introductions, global warming, storm frequency and sea level rise, combining with regional factors such as declining nutrient have been described as the main determinants of drastic changes in the ecosystem of the Wadden Sea. Spartina anglica C.E. Hubbard, introduced in 1920 is now expanding after a long time lag, due to earlier warming springs. Crassostrea gigas (Thunberg, 1793) was introduced for aquaculture in the belief that it will not reproduce in the wild due to low temperature but is now building extensive reefs. Crepidula fornicata (Linnaeus, 1758) had been previously limited by severe winters but is now thriving, as are some ascidians and Ensis (directus) americanus (Conrad, 1843). Consequences are seen in food web interactions (less pelagic food web, more macrophytes and algae, more filtration, less predators) and habitat modifications: oysters have replaced mussels as reef builders, Spartina has trapped sediments and reinforced banks [36,37]. A notable example from the US regards the European green crab (Carcinus maenas) (L., 1758), which was introduced to the mid-Atlantic coast in the early 1800s, and has subsequently spread 1000 km upstream, where the invasion seemingly stalled in the 1960s Advances in Oceanography and Limnology 203 around Halifax, Nova Scotia, presumably owing to the increased time needed for larval development as water temperature decreases. However, in the 1990s, C. maenas populations suddenly expanded farther north into the Canadian Maritimes. Roman [38] demonstrated that the new expansion was driven by a new introduction of C. maenas to northern Canada from Europe that possessed distinct haplotypes from the older established population in North America. The actual poleward range extension observed is attributable to numerous factors, among which global warming, increased propagule pressure, and, according to Byers and Pringle [32], the presence of upstream retention zones in tidal environments. The latter authors contend that, once inoculated farther north of Halifax by humans, C. maenas could be retained and even expand because of the presence of upstream retention zones throughout the Canadian Maritimes, e.g. the Straight of Canso and the Bras d’Or Lakes. Moreover, once anchored there, these upstream C. maenas populations should then flood downstream areas with their propagules and have a great competitive advantage over downstream populations, which they will eventually displace. 3. Are predictions possible? We face the possibilities that biological invasions will be favoured by climate change and that local assemblages will be altered by global change (bioinvasions þ climate). Even without the complexity introduced by changing climatic conditions, forecasting the dynamics of invasions has been considered a daunting task [39]. The high level of uncertainty concerning determinants of invasiveness of species and invasibility of habitats engendered different approaches, including assessment of the biological characters of the most ‘invasive’ species, the probability of transport (if vectors are known) [40], and the susceptibility of habitats to invasions [41]. Predictions as to how climate change will influence aquatic invasive species are hampered by uncertainty in climate-change scenarios and by inadequate knowledge of how factors, such as temperature and hydrography, influence the distribution and abundance of aquatic organisms. Even if one considers temperature models, that are used for broad-scale predictions of species invasions, predictions for local scale, in which multiple factors likely interact, are scarcely useful [42]. 3.1. Niche theory and predictions While invasion has been regarded as an enormously complex process, some phases of the process are considered predictable; for example, modelling the ecological niche characteristics of a species can predict its potential geographic distribution at a level sufficient for management [40,43]. The conditions for a successful invasion involve the intersection of a species, its vector, and an appropriate receiving environment. This climate matching approach relies on the assumption that invasive species conserve their climatic niche in the invaded ranges. Climate matching is thus a useful approach to identify areas at risk of introduction and establishment of newly or not-yet-introduced neophytes, but may not predict the full extent of invasions [44]. Locke [45] developed a screening tool for potential tunicate invaders of Atlantic Canada by using species distribution (biogeography) and vector traffic patterns. 204 A. Occhipinti-Ambrogi and B. Galil He derived a ‘watch list’ for early detection of species to be monitored examining Tunicates with a known history of introductions and comparing donor regions and maritime routes. Should the climatic conditions be perturbed significantly, the differences of temperature regimes between Canada and some potential donor regions could not justify the exclusion of some species from the list of candidates. Many modelling exercises can be quoted, even if a common drawback is the lack of detailed information on the actual occurrence of species over large areas. For instance, Reusser and Lee [46] used a new modelling technique (Non-Parametric Multiplicative Regression – NPMR) to predict species distribution over different spatial scales for estuaries and their habitats over the entire west coast of the United States, where they could make use of a large data set of species with associated landscape and watershed characteristics. Lee et al. [47] suggest that combining the outputs from biological information systems with environmental data would allow the development of ecological niche models that predict the potential distribution or abundance of native and non-native species. Environmental projections from climate models can be used in these niche models to project changes in species distributions or abundances under altered climatic conditions and to identify potential high-risk invaders. 3.2. The special case of pest prediction An interesting case of possible interactions between climate change and effects of the altered distribution of organisms is that of pathogens. Pathogens have been seen as the main cause for the loss of biodiversity in some areas, their spread having caused unprecedented declines in host populations due to changes in their mutual relations. This is a particular case of concern for predictions, due to the health and economic consequences, besides those concerning biodiversity, and also a subject where traditionally climate linked predictions are used in order to forecast epidemic outbreaks. However, given the paucity of baseline disease data, the multivariate nature of climate change, and nonlinear thresholds in both disease and climate processes only a few attempts have been made. The hypothesis that climate warming will affect host-pathogen interactions was made by Harvell et al. [48] through the following processes: (i) increasing pathogen development rates, transmission, and number of generations per year; (ii) relaxing overwintering restrictions on pathogen life cycles; and (iii) modifying host susceptibility to infection. Changes in these mechanisms could cause pathogen range expansions and host declines, or could release hosts from disease control by interfering with the precise conditions required by many parasites. Links between pathogens and changing ocean temperatures have been observed for human diseases, such as cholera and emerging coral pathogens associated with coral bleaching [49]. For instance, in the temperate north-western Mediterranean Sea, large-scale disease outbreaks in benthic invertebrate species have recently occurred during climatic anomalies characterized by elevated seawater temperatures; in 1999, gorgonians, scleractinian corals, zoanthids, and sponges in the Ligurian Sea were affected by a temperature-linked epizootic, where mortality likely resulted from the effects of environmental stress and an Advances in Oceanography and Limnology 205 unidentified opportunistic pathogen [50,51]. From experimental inoculations of four bacterial isolates onto healthy Paramuricea clava (Risso, 1826,) a Vibrio coralliilyticus strain (a thermodependent pathogen of a tropical coral species), was recognized as the probable causative agent [52]. The recent increase of oyster disease outbreaks may be related to climate change. Parasites have been introduced into new areas through increased shipment of host oysters for fisheries and aquaculture, and changing environmental conditions may have triggered host-pathogen dynamics [53]. A notable example is the mid-1980s northward expansion of oyster diseases. The agent of Eastern oyster disease (Perkinsus marinus) extended its range from Long Island to Maine during a winter warming trend. El Niño events are known to influence Perkinsus marinus infection intensity and prevalence in the Gulf of Mexico, where it is endemic [54]. Although there is evidence for temperature and climate-related links in some marine diseases, lack of reliable baselines and incomplete disease time series complicate the partitioning of climate effects and other anthropogenic disturbances, such as the high densities under which animals are grown and the high temperatures sustained in hatcheries favour the proliferation and transmission of opportunistic pathogens. 3.3. Observation of what is happening is a good start Climate change is no more a fancy prediction derived from complicate models of the ocean-atmospheric coupling: observational evidences accumulate on the rapid, albeit not uniform, rate of temperature increase and related phenomena (see for instance [55]). Plants and animals can survive only within certain climatic zones, so with the warming of recent decades many of them are seen to migrate poleward. The study of Parmesan and Yohe [9] found that 1700 plant, animal and insect species moved poleward at an average rate of 6 km (about 4 miles) per decade in the last half of the twentieth century. The invasion success of Ponto-Caspian crustacean onychopods (cladocerans) in inland and coastal waters outside their native range has been attributed to increased temperatures in receiving water bodies, where these euryhaline species have found optimal conditions. For instance Cercopages pengoi (Ostroumov 1891) has been introduced to the Baltic Sea and North American Great Lakes, by resting eggs accumulated in the sediments of ballast tanks [56]. There are many examples of geographic range shifts or phenological shifts consistent with climate change predictions for terrestrial, inland and marine species [9,10,16,57,58]. It is commonly assumed that more northerly species will contract their ranges in response to climate warming [59], but just the opposite has been seen during recent decades in at least one part of the northwest Atlantic. In shelf ecosystems upstream of the tail of the Grand Banks, the predominantly positive NAO conditions since the 1970s have led to colder bottom waters that are physiologically favourable for boreal species like the northern shrimp Pandalus borealis Krøyer, 1838 [60]. 4. The Mediterranean Sea as a miner’s Canary The recent evolution of biodiversity in the Mediterranean Sea serves us with an example of changes occurring under the pressure of both climate forcing and species introductions. The present Mediterranean biota contains an exceptionally large number of alien species, resulting from a long history of introductions and presence of exceptional pathways of introduction. The recent warming trend in sea surface temperatures [61] and other 206 A. Occhipinti-Ambrogi and B. Galil hydrological changes, enumerated below, may have facilitated the spread of thermophilic species [62]. The consequences of these changes, and the concomitant effects of pollution, coastal eutrophication, habitat destruction, fisheries overexploitation etc., are raising a growing concern [63]. The recognition that marine organisms had been introduced into the Mediterranean from other parts of the world came gradually. Naturalists noted the many fouling species on vessels reporting from distant regions of the world: ‘it should not be overlooked, that those species, as Balanus tintinnabulum, amphitrite, improvisus, and, in a lesser degree, B. trigonus and Tetraclita radiata, which seem to range over nearly the whole world (excepting the colder seas), are species which are habitually attached to ships, and which could hardly fail to be widely transported’ ([64], p. 163). In 1873 the tri-masted Karikal arrived at the port of Marseille from India carrying on its flanks a ‘. . .petite forêt d’êtres vivants était peuplée de Crustacés’ ([65], p. 4) including Planes minutus, Pachygrapsus transversus (reported as P. advena) and Plagusia squamosa, the latter numbering in the hundreds of specimens. But it was the opening of the Suez Canal that focused scientific attention on the movement of marine species. Even before the Suez Canal was fully excavated it was argued that ‘Le percement de l’isthme de Suez . . . offrira . . . une occasion précieuse de constater les phénomènes que doivent amener l’émigration des espèces et le mélange des faunes’ ([66], p. 97). Indeed, Keller, who traveled to Egypt in 1882 and 1886 to seek evidence for the presence of Red Sea and Mediterranean species in the Canal, considered it ‘. . . auch als Karawanenstrasse für die thierischen Bewohner beider Meere benutzt’ ([67], p. 3). While Erythrean aliens were pouring through the Suez Canal into the Levantine Basin, along the European coast of the Mediterranean alien shellfish and their ‘associates’ were introduced via shipping and mariculture. Though records of alien species introduced into the Western Mediterranean kept appearing in the scientific literature, their number and impact were considered negligible and thus they ‘. . . have not been the subject of inventories as representative as those of lessepsian migrants’ ([68], p. 45). The rapid spread and conspicuous impacts of a pair of invasive chlorophytes [69,70], have helped raise awareness of the raging problem of alien species in the Mediterranean. The European Commission Environmental Programme and the Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée (CIESM) have organized a workshop on ‘Introduced species in European coastal waters’ [71], that was followed by CIESM research workshops on ‘Ship-transported alien species in the Mediterranean and Black Sea’ [72] and on the ‘Impact of mariculture on Mediterranean coastal ecosystems’ [73] (www.ciesm.org). The first comprehensive inventory of alien decapod and stomatopod crustaceans in the Mediterranean was published in 2002 (www.ciesm.org/atlas), followed by a project funded by the European Commission under the Sixth Framework Programme, that created an inventory of alien species in the European marine environment, including a Mediterranean-wide dataset and collated data on invasive and potentially invasive species in particular habitats (DAISIE European Invasive Alien Species Gateway, http://www.europe-aliens.org/). Drawing on the latter database, another EU project, IMPASSE (http://ec.europa.eu/research/fp6/ssp/impasse_en.htm), has studied aquaculture related introductions in European waters, including the Mediterranean Sea. Over 620 metazoan species have been listed as alien in the Mediterranean Sea (compared with 10,000–11,000 native metzoan species) (Galil, in preparation). All are littoral and sublittoral and most are benthic or demersal species (or their parasites). Since the shallow coastal zone, and especially the benthos, has been extensively studied, and is Advances in Oceanography and Limnology 207 more accessible, the chances that new arrivals will be encountered and identified are higher. Also, the species most likely to be introduced by the predominant means of introduction (Suez Canal, vessels, mariculture) are shallow water species. There is no doubt that the location of the opening of the Suez Canal at the southeastern Levantine Sea directly influenced the outcome of the Erythrean Invasion. The higher sea surface temperature (SST) [61], the prevailing counter clockwise coasthugging currents and the wide shallow shelf influenced establishment success. Already in the 1950s it was suggested that the establishment of Erythrean aliens was related to a rise in SST: the sudden escalation in the populations of certain Erythrean aliens had been attributed to a rise of 1–1.5 C during the winter of 1955 [74–76]. Ben Tuvia ([77], p. 254) contended that the thermophilic aliens require ‘temperatures high enough for the reproductive processes and development of eggs, and minimum winter temperatures above their lethal limits’ to establish populations in the Mediterranean. 4.1. The speeding spread of alien species For much of the twentieth century Erythrean aliens were confined within the Levantine Sea, but the 1990s saw the breaching of the barrier. The sudden spread of Erythrean species westwards and northwards coincided with significant hydrographic changes which include a shift in the source of the Eastern Mediterranean Deep Water from the Adriatic to the southern Aegean Sea [78]. The increased outflow of the newly formed, denser water through the Cretan Arc Straits into the eastern Mediterranean has been compensated by inflowing Levantine surface and intermediate water [79,80]. The more extensive inflow of the warm-water Asia Minor Current along the Anatolian coastline, carrying westwards warm, salty water from the Levant, was positively correlated with the initiation of a significant increase in the number of Erythrean aliens along the southwestern Anatolian and the southern Aegean coasts: only one of the 13 Erythrean decapod and stomatopod species now known in the Aegean Sea, the swimming crab Thalamita poissonii (Audouin, 1826), was collected before 1991 [81]. But Erythrean aliens are found much further westwards – among the marine alien species recorded from the coast of Italy are 46 Erythrean species. The bivalves, Brachidontes pharaonis (Fischer P., 1870), Pinctada radiata (Leach, 1814), Fulvia fragilis (Forsskål in Niehbur, 1775), and the gastropod Cerithium scabridum (Philippi, 1848), are likely to have been vessel transported, either from established Levantine populations or from their native range. Both B. pharaonis, P. radiata and C. scabridum were initially recorded in the late 1960s and early 1970s, but spread only in the past decade, whereas F. fragilis was first sighted as recently as 2003 in Livorno, but has since been recorded from the Gulf of Pozzuoli (Naples), Castellaneta Marina (Taranto), Calabria, Messina Strait (Reggio Calabria Airport) and Syracuse, Sicily [82]. Indeed, in past decade witnessed a rapid expansion of alien species: the bluespotted cornetfish, Fistularia commersonii Rüppell, 1835, was first recorded in Italy in 2002 from the straits of Sicily [83,84]. In the following year it was recorded from the Gulf of Castellammare in the southern Tyrrhenian Sea [85], and seems to have established populations along the central Tyrrhenian coasts soon after [86–88]. In 2005, a specimen was collected off the east coast of Sardinia [89]. In 2007 a single adult fish was caught near Sanremo [90] and in 2008 a school was sighted near Laigueglia, Savona [91], both localities on the northwestern Tyrrhenian coast of Italy. In 2007 a specimen was collected in Montenegro, on the east coast of the Adriatic Sea [92]. 208 A. Occhipinti-Ambrogi and B. Galil The fact that a fish described as ‘tropical, reef-associated’ (www.fishbase.org) thrives in the Mediterranean is cause for alert. The last decades of the twentieth century saw pronounced thermal fluctuations and a significant increase in the average SST in the Mediterranean, and a growing concern over the ‘tropicalization’ of its biota by the marked rise in the number, abundance and geographic expansion of thermophilic alien species, with the Levantine Sea acting as a reservoir [81,93]. Persistence of the warming trend would likely have a significant influence on the establishment and distribution of thermophilic species and, consequently, on the biodiversity of the Mediterranean [94,95]. Rising seawater temperature may change the pool of species which could establish themselves in the Mediterranean, enable the warm stenothermal species (native and alien) to expand beyond their present distributions, and may impact on a suite of population characteristics (reproduction, survival) that determines interspecific interactions, and, therefore, the dominance and prevalence patterns of both native and alien species, and provide the thermophilic aliens with a distinct advantage over the native Mediterranean biota. To date, aquaculture- introduced warm water species have not been recorded as invasive in the Mediterranean, with the exception of Penaeus japonicus (Bate, 1888), an Erythrean species that has turned invasive in the eastern basin, at variance with inland water bodies that have been invaded by Tilapia spp. introduced through aquaculture facilities. Nevertheless, the concern for species associated with aquaculture transfer of stocks is high, bearing in mind the spread of alien algae in western Mediterranean lagoons [96]. Though no extinction of a native species is known, sudden decline in abundance concurrent with proliferation of aliens had been recorded. Examination of the profound ecological impacts of some of the most conspicuous invasive alien species underscores their role, among multiple anthropogenic stressors, in altering the infralittoral communities [97]. Local population losses and niche contraction of native species may not induce immediate extirpation, but they augur reduction of genetic diversity, loss of functions, processes, and habitat structure, increase the risk of decline and extinction, and lead to biotic homogenization. A handful of Mediterranean invasive aliens have drawn the attention of scientists, management, and media, for the conspicuous impacts on the native biota attributed to them. Perhaps the most notorious and the best studied invasive species in the Mediterranean are a pair of coenocytic chlorophytes: Caulerpa taxifolia [69] and Caulerpa racemosa var. cylindracea [70]. Other studies traced the impacts of invasive aliens that entered the Mediterranean through the Suez Canal and displaced native species [98]. The Mediterranean Sea is highly susceptible to ship-transported bioinvasions: one-fifth of the alien species recorded in the Mediterranean have been primarily introduced by vessels [97]. And no wonder – in 2006, 13,000 merchant vessels made 252,000 calls at Mediterranean ports and an additional 10,000 vessels transited through the sea [99]. The increase in shipping-related invasions was noted in recent publications, and may be attributed to the increase in shipping volume throughout the region, changing trade patterns that result in new shipping routes, improved water quality in port environments, augmented opportunities for overlap with other introduction vectors, and rising awareness and research effort [72,100]. The swarms of the vessel-transported American comb jelly, Mnemiopsis leidyi, that have spread across the Mediterranean, from Israel to Spain, in 2009, raise great concern because its notorious impacts on the ecosystem and the fisheries (www.ansamed.info). Advances in Oceanography and Limnology 209 4.2. Changes in emergent functions and services in Mediterranean ecosystems In-depth in-situ or experimental studies of changes in ecosystem functions and services in the Mediterranean Sea due to the introduction of alien invasive species are rare. The aliens’ impacts have been inferred on the basis of observations, rather than rigorous experimentation. The combined effect of invasive species, some of which are ecosystem engineers, and climate change has profoundly modified the functioning of Mediterranean ecosystems. The extremely invasive Caulerpa racemosa var. cylindracea (Sonder) Verlaque, Huisman and Boudouresque, 2003, endemic to southwestern Australia, was discovered in the Mediterranean in 1990, and has since spread from Cyprus to Spain and even unto the Canary Islands [70,101]. The species is considered an habitat modifier and ecosystem engineer [102]. Its compact multilayered mats forming ‘web-like green meadow’ contribute to large-scale landscape modification, even in highly diverse, native macroalagal assemblages with dense coverage [103,104]. Invaded assemblages have been characterized by lower alpha diversity, but the difference between assemblages at 5 and 25 m depth were smaller than in non-invaded assemblages, due to proliferation of few opportunistic species [105]. Its invasion may modify water movement, sediment deposition, substrate characteristics and landscape, as well as benthic assemblages. An invasive strain of a tropical green alga, Caulerpa taxifolia (Vahl) C. Agardh, widely available through the aquarium trade, was unintentionally introduced into the Mediterranean in 1984 [106]. The species’ rapid spread, high growth rate, and its ability to form dense meadows (up to 14,000 blades per m2) on various infralittoral bottom types, especially in areas plagued by higher nutrient loads, led to formation of homogenized microhabitats and replacement of native algal species [107–109]. Caulerpa taxifolia is associated with reduction of species richness of native hard substrate algae [107] and, under certain conditions, outcompetes Cymodocea nodosa (Ucria) Ascherson and Posidonia oceanica L. Delile [110,111]. Moreover, the most potent of its repellent endotoxins caulerpenyne, is toxic for molluscs, sea urchins, herbivorous fish, at least during summer and autumn when metabolite-production peaks, and capable of decimating microscopic organisms [112–114]. The diminution in the structural complexity of the invaded habitat, together with the replacement of the rich native biota with the C. taxifolia species-poor community, result in a dramatic reduction in the richness and diversity of the affected littoral, and constitutes ‘a real threat for the balance of the marine coastal biodiversity’ [115]. The two species of siganid fish, Siganus rivulatus (Forsskål, 1775) and S. luridus (Rüppell, 1828), entered the Mediterranean from the Red Sea through the Suez Canal. Both species are found as far west as the southern Adriatic Sea, Sicily, Tunisia, and recently – west of Marseille, France [100,116]. The schooling, herbivorous fishes form thriving populations in the Levant Sea where they comprise 80% of the herbivorous fish in some shallow coastal sites and replaced native herbivorous Sarpa [117]. Prior to the arrival of the siganids in the Mediterranean, there were few herbivorous fish and invertebrates and their role in the food web off the Levantine rocky habitats had been negligible. The siganids increased the recycling of algal material accelerating the transfer of energy from the producer to the consumer levels, and by serving as major item of prey (up to 70%) for larger infralittoral predators such as groupers [118,119]. Their grazing pressure on intertidal rocky algae may have benefited the proliferation of an alien Erythrean mussel by providing suitable substrate for its settlement (see below). An analysis of the siganids’ gut 210 A. Occhipinti-Ambrogi and B. Galil contents, in conjunction with the spatial and seasonal composition of the local algal community, showed that their diet has a significant impact on the structure of the local algal community: it seems that by feeding selectively they have nearly eradicated some of their favorite algae locally [120]. A small Erythrean mytilid mussel, Brachidontes pharaonis (Fischer P., 1870), spread as far west as Sicily, probably in ship fouling, where it is found in high-salinity, high temperature environments [121]. In the early 1970s B. pharaonis was many times rarer than the native mytilid Mytilaster minimus (Poli, 1795), along the Levantine intertidal rocky ledges [122]. A recent survey has shown a rapid shift in dominance [123]. The establishment of massive beds of Brachidontes has had significant effects on the biota of the hard substrate intertidal. The displacement of the native mussel by the larger, thickershelled Erythrean alien appears to have changed predation patterns so that the population of the native whelk, Stramonita haemastoma (Linnaeus, 1758), that was found to preferentially prey on Brachidontes, increased greatly [124]. The lack of publications is misleading and gravely understates the grievous state of the Mediterranean biota. Of the nearly 30,000 specimens collected by commercial benthic trawler off the central Israeli coast at depths between 15 and 30 m, on October 2008, only 9% were native Mediterranean species, the rest of the sample consisted of Erythrean aliens, such as the highly venomous striped catfish, Plotosus lineatus (Thunberg, 1787) (11,437 specimens), the blotchfin dragonet, Callionymus filamentosus Valenciennes, 1837 (5745), the silver sillago, Sillago sihama (Forsskål, 1775) (1423), the kuruma prawn, Marsupenaeus japonicus (Bate, 1888) (1154) and the velvet shrimp Metapenaeopsis consobrina (Nobili, 1904) (1138). In front of our very eyes the native macrobenthic biota of the soft sediments of the upper shelf in the southeastern Levantine Sea has been substituted by Erythrean aliens and constitute today an assemblage dominated by thermophilic invasive alien species. 5. Conclusions Alien species introductions can lead to biological invasions concomitantly with climate change at a global scale in all planet’s oceans. These two concurrent phenomena can interact between themselves and with others in a variety of ways. Man’s role and responsibility is clearly involved in influencing the evolution of biological communities and ecosystem and the management and adaption strategies are clearly influenced by our understanding of how these changes occur. In our analysis we have tried to distinguish three interacting mechanisms influencing the distribution of species in marine environments: (i) the ‘natural’ range shift induced by climate change; (ii) the long distance transport of species by ships and aquaculture; and (iii) the secondary spread of species, after being introduced in a new location. The second one is characterized by being essentially discrete, i.e. man is bringing a species from a remote region of the sea to another region. The other two mechanisms involve the establishment of new climatic conditions, facilitating the spread in contiguous locations. The literature examples shown often describe how the local biodiversity is affected during the process of change, especially when native species are negatively impacted and alien species take their place: there is a strong correlation between the demise of native species and the success of alien species, but seldom a causation can be demonstrated. In other words, there is no evident answer to the following question: did the native ones became less abundant because of the aliens, or did the aliens become more abundant because the local Advances in Oceanography and Limnology 211 species decreased in number for some other reason? In the Mediterranean Sea the physical conditions have probably enhanced the aliens, as in the case of Erythrean species, and maybe they have discouraged the natives, as in the case of Posidonia. So the changes in dominance between natives and aliens might be mediated by physical change. Evidently, the Mediterranean Sea is a warning example of the consequences of a very high propagule pressure of alien species (especially through the Suez Canal), coupled with the influence of changing climate and hydrographic conditions at a wider basin scale, leading to a revolution in much shorter times than the geological scale. We have limited knowledge concerning extinction of marine species caused by invasive aliens, though observations of extirpation and displacement of native species by aliens have been amply recorded. It is yet unresolved whether the deterioration of coastal habitats and their native assemblages permitted the establishment of opportunistic aliens, or the influx of aliens synergetically with the physical disturbance of the environment brought on the decimation of native communities. Still, the more common outcome at present is that species richness is locally increased when alien species are added to native ones. At some specific coastal regions, mostly heavily polluted or physically altered, like lagoons, estuaries, ports and marine farms, we witness the progressive homogenization of biotas, as only stress resistant opportunistic species, both native and ‘cosmopolitan’ invasive species dominate [125]. Homogenization is best documented for inland fish faunas, where a small set of species introduced for sport fishing, aquaculture, or ornamental purposes, has become widespread throughout the world [13], but it is known for marine faunas as well [126]. Studies on the ecology of alien species and changing climate should aim at disentangling cause/effect relationships, taking into account aspects, such as the influence of regime shifts on species interactions and phenology [127–129] microevolution and genetic aspects leading eventually to speciation [130]. Longterm data yield important insights on the impacts of anthropogenic disturbances and should be continued or resumed as in the case of the English Channel [30,131]. In the ongoing debates in the scientific community, priorities are shifting already. The sort of problems stakeholders increasingly face will be much less predictable than those associated with ‘classic’ pollution of the marine environment faced in the late twentieth century. Pressure from demography, economy and climate change builds up for a long time – and then triggers abrupt shifts – as the one we witness in the Mediterranean today. The current international system is ill-designed for such a world. The Copenhagen 2009 meeting demonstrated that the way governments deal with new threats is inappropriate to the task – it frequently takes decades just for them sign on already negotiated agreements, i.e. the International Convention for the Control and Management of Ships’ Ballast Water and Sediments. Merely tinkering with reducing risk is insufficient. We call for a closer interlinking of regional (& international) scientific expertise to induce governments to recognize their mutual obligations and interests, and to consider the consequences of failure to act now on the biotic safety of the sea. Acknowledgements ICES (International Council for the Exploration of the Sea) sponsored the participation of one of us in the sixth International Conference on Marine Bioinvasions, held in Portland (Oregon) on August 24–27, 2009; most of the ideas developed in this paper were presented at the opening lecture by AOA. Research leading to the publication was funded by the E.U. Integrated Project SESAME [BG] and by the Porter School of Environmental Studies at Tel Aviv University with funding from the Italian Ministry of the Environment, Land and Sea [BG]. Two anonymous referees have raised constructive criticism on the manuscript. 212 A. Occhipinti-Ambrogi and B. Galil References [1] IUCN The World Conservation Union, 2000. Species Survival Commission (SSC). Guidelines for the prevention of biodiversity loss caused by alien invasive species prepared by the SSC Invasive Species Specialist Group. Approved by the 51st Meeting of the IUCN Council, Gland Switzerland, February 2000. http://iucn.org/themes/ssc/pubs/policy/invasivesEng.htm [2] IUCN The World Conservation Union, 2002. Policy Recommendations Papers for Sixth meeting of the Conference of the Parties to the Convention on Biological Diversity (COP6). The Hague, Netherlands, 7–19 April 2002. http://www.iucn.org/themes/pbia/wl/docs/biodiversity/ cop6/invasives.doc [3] P. Pyšek, P.H. Hulme, and N. Wolfang, Glossary of the main technical terms used in the handbook. DAISIE Handbook of Alien Species in Europe. Invading nature: Springer series in invasion ecology 3 Chapter 14 (2009), pp. 375–379. [4] A. Occhipinti-Ambrogi and B.S. Galil, A uniform terminology on bioinvasions: a chimera or an operative tool?, Mar. Poll. Bull. 49 (2004), pp. 688–694. [5] D.M. Lodge, S. Williams, H.J. MacIsaac, K.R. Hayes, B. Leung, S. Reichard, R.N. Mack, P.B. Moyle, M. Smith, D.A. Andow, J.T. Carlton, and A. McMichael, Biological invasions: recommendations for US policy and management, Ecol. Appl. 16 (2006), pp. 2035–2054. [6] A. Occhipinti-Ambrogi, Transfer of marine organisms: a challenge to the conservation of coastal biocoenoses, Aquatic Conserv: Mar. Freshw. Ecosyst. 11 (2001), pp. 243–251. [7] D.B. Botkin, H. Saxe, M.B. Araujo, R. Betts, R.H.W. Bradshaw, T. Cedhagen, P. Chesson, T.P. Dawson, J.R. Etterson, D.P. Faith, S. Ferrier, A. Guisan, A.S. Hansen, D.W. Hilbert, C. Loehle, C. Margules, M. New, M.J. Sobel, and D.R.B. Stockwell, Forecasting the effects of global warming on biodiversity, Bioscience 57 (2007), pp. 227–236. [8] G.-R. Walther, E. Post, P. Convey, A. Menzel, C. Parmesan, T.J.C. Beebee, J.-M. Fromentin, O. Hoegh-Guldberg, and F. Bairlein, Ecological responses to recent climate change, Nature 416 (2002), pp. 389–395. [9] C. Parmesan and G. Yohe, A globally coherent fingerprint of climate change impacts across natural systems, Nature 421 (2003), pp. 37–42. [10] C. Parmesan, Ecological and evolutionary responses to recent climate change, Annu. Rev. Ecol. Evol. Syst. 37 (2006), pp. 637–669. [11] C.R. Pyke, R. Thomas, R.D. Porter, J.J. Hellmann, J.S. Dukes, D.M. Lodge, and G. Chavarria, Current practices and future opportunities for policy on climate change and invasive species, Conservation Biol. 22 (2008), pp. 585–592. [12] J.J. Hellmann, J.E. Byers, B.G. Bierwagen, and J.S. Dukes, Five potential consequences of climate change for invasive species, Conservation Biol. 22 (2008), pp. 534–543. [13] F.J. Rahel, Biogeographic barriers, connectivity, and biotic homogenization: it’s a small world after all, Freshwater Biol. 52 (2007), pp. 696–710. [14] A.J. Richardson and D.S. Schoeman, Climate impact on plankton ecosystems in the Northeast Atlantic, Science 305 (2004), pp. 1609–1612. [15] J.P. Barry, C.H. Baxter, R.D. Sagarin, and S.E. Gilman, Climate-related, long-term faunal changes in a California Rocky Intertidal Community, Science 267 (1995), pp. 672–675. [16] A.L. Perry, P.J. Low, J.R. Ellis, and J.D. Reynolds, Climate change and distribution shifts in marine fishes, Science 308 (2005), pp. 1912–1915. [17] J.G. Hiddink and R. Ter Hofstede, Climate induced increases in species richness of marine fishes, Glob. Change Biol. 14 (2008), pp. 453–460. [18] S.I. Lonhart, Natural and climate change mediated invasions, in Biological Invasions in Marine Ecosystems, G. Rilov and J.A. Crooks, eds., Springer-Verlag, Berlin Heidelberg, 2009, Ecological Studies 204, pp. 57–69. [19] J.T. Carlton, Global change and biological invasions in the oceans, in Invasive Species in a Changing World, H.A. Mooney and R.J. Hobbs, eds., Island Press, Washington, DC, 2000, pp. 31–53. Advances in Oceanography and Limnology 213 [20] Y. Frenot, S.L. Chown, J. Whinam, P.M. Selkirk, P. Convey, M. Skotnicki, and D.M. Bergstrom, Biological invasions in the Antarctic: extent, impacts and implications, Biol. Rev. 80 (2005), pp. 45–72. [21] R.B. Aronson, S. Thatje, A. Clarke, L.S. Peck, D.B. Blake, C. Wilga, and B.A. Seibel, Climate change and invasibility of the Antarctic benthos, Annu. Rev. Ecol. Evol. Syst. 38 (2007), pp. 129–154. [22] D.K.A. Barnes, D.A. Hodgson, P. Convey, C.S. Allen, and A. Clarke, Incursion and excursion of Antarctic biota: past, present and future, Glob. Ecol. Biogeogr. 15 (2006), pp. 121–142. [23] M. Tavares and G.A.S. De Melo, Discovery of the first known benthic invasive species in the Southern Ocean: the North Atlantic spider crab Hyas araneus found in the Antarctic Peninsula, Antarct. Sci. 16 (2004), pp. 129–131. [24] W. Thuiller, Climate change and the ecologist, Nature 448 (2007), pp. 550–552. [25] W. Thuiller, D.M. Richardson, and G.F. Midgley, Will climate change promote alien plant invasions?, W. Nentwig, ed., Springer-Verlag, Berlin Heidelberg, 2007, Ecological Studies 193, Biological Invasions, pp. 197–211. [26] A. Occhipinti-Ambrogi, Global change and marine communities: alien species and climate change, Mar. Poll. Bull. 55 (2007), pp. 342–352. [27] A.D.M. Colautti, I.A. Grigorovich, and H.J. MacIsaac, Propagule pressure: a null model for biological invasions, Biol. Invasions 8 (2006), pp. 1023–1037. [28] R.A. Kerr, A warmer Arctic means changes for all, Science 297 (2002), pp. 1491–1492. [29] P. Kaluza, A. Kölzsch, M.T. Gastner, and B. Blasius, The complex network of global cargo ship movements, J.R. Soc. Interface (2010) published online doi: 10.1098/rsif.2009.0495R.A. [30] J.R. Lewis, Coastal zone conservation and management: a biological indicator of climatic influences, Aquatic Conser: Mar. Freshw. Ecosyst. 9 (1999), pp. 401–405. [31] C.A. Oviatt, The changing ecology of temperate coastal waters during a warming trend, Estuaries 27 (2004), pp. 895–904. [32] J.E Byers and J.M. Pringle, Going against the flow: retention, range limits, and invasions in advective environments, Mar. Ecol. Prog. Ser. 313 (2006), pp. 27–41. [33] I.M. Parke, D. Simberloff, W.M. Lonsdale, K. Goodell, M. Wonham, P.M. Kareiva, M.H. Williamson, B. Von Holle, P.B. Moyle, J.E. Byers, and L. Goldwasser, Impact: toward a framework for understanding the ecological effects of invaders, Biol Invasions 1 (1999), pp. 3–19. [34] J.J. Stachowicz, J.R. Terwin, R.B. Whitlatch, and R.W. Osman, Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions, PNAS 99 (24) (2002), pp. 15497–15500. [35] D. Secord, Biological control of marine invasive species: cautionary tales and land-based lessons, Biol. Invasions 5 (2003), pp. 117–131. [36] K. Reise and J.E.E. van Beusekom, Interactive effects of global and regional change on a coastal ecosystem, Helgol. Mar. Res. 62 (2008), pp. 85–91. [37] J. Kochmann, C. Buschbaum, N. Volkenborn, and K. Reise, Shift from native mussels to alien oysters: differential effects of ecosystems engineers, J. Exp. Mar. Biol. Ecol. 364 (2008), pp. 1–10. [38] J. Roman, Diluting the founder effect: cryptic invasions expand a marine invader’s range, Proc. R. Soc. B 273 (2006), pp. 2453–2459. [39] J.T. Carlton, Pattern, process and prediction in marine invasion ecology, Biol. Conserv. 78 (1996), pp. 97–106. [40] L.H. Herborg, C.L. Jerde, D.M. Lodge, G.M. Ruiz, and H.J. MacIsaac, Predicting invasion risk using measures of introduction effort and environmental niche models, Ecol. Appl. 17 (2007), pp. 663–674. [41] E.O. Wiley, K.M. McNyset, A.T. Peterson, C.R. Robins, and A.M. Stewart, Niche modeling and geographic range predictions in the marine environment using a machine-learning algorithm, Oceanogr. Soc. 16 (2003), pp. 120–127. 214 A. Occhipinti-Ambrogi and B. Galil [42] F.J. Rahel and J.D. Olden, Assessing the effects of climate change on aquatic invasive species, Conservation Biol. 22 (2008), pp. 521–533. [43] A.T. Peterson, Predicting the geography of species’ invasions via ecological niche modelling, Q. Rev. Biol. 78 (2003), pp. 419–434. [44] O. Broennimann, U.A. Treier, H. Müller-Schärer, W. Thuiller, A.T. Peterson, and A. Guisan, Evidence of climatic niche shift during biological invasion, Ecol. Lett. 110 (2007), pp. 701–709. [45] A. Locke, A screening procedure for potential tunicate invaders of Atlantic Canada, Aquatic Invasions 4 (2009), pp. 71–79. [46] D.A. Reusser and H. Lee II, Predictions for an invaded world: a strategy to predict the distribution of native and non-indigenous species at multiple scales, ICES J. Mar. Sci. 65 (2008), pp. 742–745. [47] H. Lee II, D.A. Reusser, J.D. Olden, S.S. Smith, J. Graham, V. Burkett, J.S. Dukes, R.J. Piorkowski, and J. McPhedran, Integrated monitoring and information systems for managing aquatic invasive species in a changing climate, Conserv. Biol. 22 (2008), pp. 575–584. [48] C.D. Harvell, C.E. Mitchell, J.R. Ward, S. Altizer, A.P. Dobson, R.S. Ostfeld, and M.D. Samuel, Climate warming and disease risks for terrestrial and marine biota, Science 296 (2002), pp. 2158–2162. [49] O. Hoegh-Guldberg, Climate change, coral bleaching and the future of the world’s coral reefs, Mar. Freshwat. Res. 50 (1999), pp. 839–866. [50] C. Cerrano, G. Bavestrello, C.N. Bianchi., R. Cattaneo-Vietti, S. Bava, C. Morganti, C. Morri, P. Picco, G. Sarà, S. Schiaparelli, A. Siccardi, and F. Sponga, A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (North-western Mediterranean), summer 1999, Ecol. Lett. 3 (2000), pp. 284–293. [51] C. Cerrano, C. Totti, F. Sponga, and G. Bavestrello, Summer disease in Parazoanthus axinellae (Schmidt, 1862 (Cnidaria, Zoanthidea), Italian J. Zool. 73 (2006), pp. 355–361. [52] M. Bally and J. Garrabou, Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change, Global Change Biol. 13 (2007), pp. 2078–2088. [53] K.D. Lafferty, J.W. Porter, and S.E. Ford, Are diseases increasing in the ocean?, Annu. Rev. Ecol. Evol. Syst. 35 (2004), pp. 31–54. [54] E. Hofmann, S. Ford, E. Powell, and J. Klinck, Modeling studies of the effect of climate variability on MSX disease in eastern oyster (Crassostrea virginica) populations, Hydrobiol. 460 (2001), pp. 195–212. [55] J. Hansen, M. Sato, R. Ruedy, K. Lo, D.W. Lea, and M. Medina-Elizade, Global temperature change, Proc. Natl. Acad. Sci. 103 (2006), pp. 14288–14293. [56] V.E. Panov, N.V. Rodionova, P.V. Bolshagin, and A.E. Bychek, Invasion biology of PontoCaspian onychopod cladocerans (Crustacea: Cladocera: Onychopoda), Hydrobiol. 590 (2007), pp. 3–14. [57] K. Hiscock, A. Southward, I. Itittley, and S. Hawkins, Effects of changing temperature on benthic marine life in Britain and Ireland, Aquatic Conserv: Mar. Freshw. Ecosyst. 14 (2004), pp. 333–362. [58] R. Hickling, D.B. Roy, J.K. Hill, R. Fox, and C.D. Thomas, The distributions of a wide range of taxonomic groups are expanding polewards, Glob. Change Biol. 12 (2006), pp. 450–455. [59] CIESM, Climate warming and related changes in Mediterranean marine biota, F. Briand, Ed., CIESM Workshop Monographs 35 (2008) Monaco, pp. 1–152. http://www.ciesm.org/online/ monographs/Helgoland.html [60] H.C. Greene, B.C. Monger, and L.P. McGarry, Some like it cold, Science 324 (2009), pp. 733–734. [61] L. Nykjaer, Mediterranean Sea surface warming 1985–2006, Climate Res. 39 (2009), pp. 11–17. [62] S. Puce, G. Bavestrello, C.G. Di Camillo, and F. Boero, Long-term changes in hydroid (Cnidaria Hydrozoa) assemblages: effect of Mediterranean warming?, Mar. Ecol. 30 (2009), pp. 313–326. Advances in Oceanography and Limnology 215 [63] C.N. Bianchi, Biodiversity issues for the forthcoming tropical Mediterranean Sea, Hydrobiologia 580 (2007), pp. 7–21. [64] C.R. Darwin, A monograph on the sub-class Cirripedia, with figures of all the species. The Balanidæ, (or sessile cirripedes); the Verrucidæ, etc. etc. etc., The Ray Society, London, Volume 2 (1854). [65] J.D. Catta, Note sur quelques crustace´s erratiques, Ann. Sci. Nat. Zool. 3 (1876), pp. 1–33. [66] L. Vaillant, Recherches sur la faune malacologique de la baie de Suez, J. Conchyliol. 13 (1865), pp. 97–127. [67] C. Keller, Die Fauna im Suez-Kanal und die Diffusion der Mediterranean und Erythräischen Tierwelt, Neue Denkschr. Allg. Schweiz. Ges. Gesammten Naturwiss. ser. 3 28 (1883), pp. 1–39. [68] H. Zibrowius, Introduced invertebrates: examples of success and nuisance in the European Atlantic and in the Mediterranean, in Introduced Species in European Coastal Waters, C.F. Boudouresque, C. Briand, and C. Nolan, eds., European Commission publications, Luxembourg, 1994, pp. 44–49. [69] A. Meinesz, D. Simberloff, and D. Quammen, Killer Algae, University of Chicago Press, Chicago, IL, 2002, 360 pp. [70] M. Verlaque, J. Afonso-Carrillo, M.C. Gil-Rodrı́guez, C. Durand, C.F. Boudouresque, and Y. Le Parco, Blitzkrieg in a Marine Invasion: Caulerpa racemosa var. cylindracea (Bryopsidales Chlorophyta) Reaches the Canary Islands (North-East Atlantic), Biol. Invasions 6 (2004), pp. 269–281. [71] C.F. Boudouresque, F. Briand, and C. Nolan, Introduced Species in European Coastal Waters, Ecosystems Research Reports No. 8, (1994) European Commission, Luxembourg. [72] CIESM, Alien marine organisms introduced by ships in the Mediterranean and Black seas, CIESM Workshop Monographs, Monaco 20 (2002), pp. 1–136. http://www.ciesm.org/online/ monographs/Istanbul.html [73] CIESM, Impact of mariculture on coastal ecosystems, CIESM Workshop Monographs, Monaco 32 (2007), pp. 1–118. http://www.ciesm.org/online/monographs/Lisboa.html [74] M. Ben Yami, 1954 – 1955: over-fishing or bad season?, Fisher. Bull. Haifa 6 (1955), pp. 10–14 [Hebrew]. [75] J. Chervinsky, A systematic and biological comparison between the lizardfish (Saurida grandisquamis) from the Mediterranean and the Red Sea, Fisher. Bull. Haifa 19 (1959), pp. 10–14 [English Abstract]. [76] M. Ben Yami and T. Glaser, The invasion of Saurida undosquamis (Richardson) into the Levant Basin – an example of biological effect of interoceanic canals, Fish. Bull. 72 (1974), pp. 359–373. [77] A. Ben Tuvia, Red Sea fishes recently found in the Mediterranean, Copeia 2 (1966), pp. 254–275. [78] A. Theocharis, P. Georgopoulos, A. Karagevrekis, L. Iona, I. Perivoliotis, and N. Charalambidis, Aegean influence in the deep layers of the eastern Ionian Sea, Rapp. P.-V. Reun. Comm. Int. Exp. Sci. Mer. Médit. 3 (1992), p. 235. [79] P. Wu, K. Haines, and N. Pinardi, Toward an understanding of deep-water renewal in the eastern Mediterranean, J. Phys. Ocean. 30 (2000), pp. 443–458. [80] W. Roether, B. Klein, B.B. Manca, A. Theocharis, and S. Kioroglouet, Transient Eastern Mediterranean deep waters in response to the massive dense-water output of the Aegean Sea in the 1990s, Progr. Oceanogr. 74 (2007), pp. 540–571. [81] B.S. Galil, Taking stock: inventory of alien species in the Mediterranean Sea, Biol. Invasions 11 (2009), pp. 359–372. [82] F. Crocetta, W. Renda, and A. Vazzana, Alien Mollusca along the Calabrian shores of the Messina Strait area and a review of their distribution in the Italian seas, Bollettino Malacologico 45 (2009), pp. 15–30. [83] F. Fiorentino, G.B. Giusto, G. Sinacori, and G. Norrito, First record of Fistularia commersonii (Fistulariidae, Pisces) in the Strait of Sicily (Mediterranean), Biol. Mar. Medit. 11 (2004), pp. 583–585. 216 A. Occhipinti-Ambrogi and B. Galil [84] E. Azzurro, F. Pizzicori, and F. Andaloro, First record of Fistularia commersonii (Fistulariidae) from the Central Mediterranean, Cybium 28 (2004), pp. 72–77. [85] C. Pipitone, G. D’Anna, M. Coppola, G. Di Stefano, and F. Badalamenti, First record of the lessepsian fish Fistularia commersonii in the Western Mediterranean, Biol. Mar. Medit. 13 (2004), p. 327. [86] P. Micarelli, M. Barlettani, and R. Ceccarelli, First record of Fistularia commersonii (Rüppel, 1838) (Fistulariidae, Pisces) in the North Tyrrhenian Sea, Biol. Mar. Medit. 13 (2006), pp. 887–889. [87] A. Ligas, P. Sartor, M. Sbrana, R. Sirna, and S. De Ranieri, New findings of Fistularia commersonii Rüppell, 1835 and Sphoeroides pachygaster (Müller and Troschel, 1848) in the northern Tyrrhenian Sea, Atti Soc. Toscana Sci. nat. Mem. Ser. B 114 (2007), pp. 131–133. [88] P.N. Psomadakis, U. Scacco, I. Consalvo, M. Bottaro, F. Leone, and M. Vacchi, New records of the lessepsian fish Fistularia commersonii (Osteichthyes: Fistulariidae) from the central Tyrrhenian Sea: signs of an incoming colonization? JMBA 2, Biodiversity Records (2008). www.mba.ac.uk/jmba/pdf/6123.pdf [89] A. Pais, P. Merella, M.C. Follesa, and G. Garippa, Westward range expansion of the Lessepsian migrant Fistularia commersonii (Fistulariidae) in the Mediterranean Sea, with notes on its parasites, J. Fish Biol. 70 (2007), pp. 269–277. [90] F. Garibaldi and L. Orsi Relini, Record of the bluespotted cornetfish Fistularia commersonii Rüppell, 1838 in the Ligurian Sea (NW Mediterranean), Aquatic Invasions 3 (2008), pp. 471–474. [91] A. Occhipinti-Ambrogi and B.S. Galil, The northernmost record of the blue-spotted cornetfish from the Mediterranean Sea, Med. Mar. Sci. 9 (2008), pp. 127–129. [92] A. Joksimović, B. Dragičević, and J. Dulčić, Additional record of Fistularia commersonii from the Adriatic Sea (Montenegrin coast), JMBA2 – Biodiversity Records Published on-line. doi:10.1017/S1755267208000328. [93] C.N. Bianchi and C. Morri, Global sea warming and ‘tropicalization’ in the Mediterranean Sea: biogeographic and ecological aspects, Biogeographia 24 (2003), pp. 319–327. [94] UNEP-MAP-RAC/SPA, Impact of climate change on biodiversity in the Mediterranean Sea, T. Perez, ed., RAC/SPA Edit., Tunis, 2008, pp. 1–61. [95] D.D. Gambaiani, P. Mayol, S.J. Isaac, and M.P. Simmonds, Potential impacts of climate change and greenhouse gas emissions on Mediterranean marine ecosystems and cetaceans, J. Mar. Biol. Assoc. UK 89 (2009), pp. 179–201. [96] M. Verlaque, Checklist of the macroalgae of Thau lagoon (He´rault, France), a hot spot of marine species introduction in Europe, Oceanol. Acta 24 (2001), pp. 29–49. [97] B.S. Galil, Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea, Mar. Poll. Bull. 55 (2007), pp. 314–322. [98] B.S. Galil, Seeing red – marine alien species along the Mediterranean coast of Israel, Aquatic Invasions 2 (2007), pp. 281–312. [99] REMPEC The Regional Marine Pollution Emergency Response Centre for the Mediterranean Sea. Study of maritime traffic flows in the Mediterranean sea. First GloBallast Regional Task Force Meeting Dubrovnik, Croatia, 11–12 September 2008. http://www.maritime-connector.com/Administration/_Upload/Documents/ Study%20of%20Maritime%20Traffic%20Flows.pdf [100] B.S. Galil, Shipwrecked: shipping impacts on the biota of the Mediterranean Sea, in The ecology of transportation: managing mobility for the environment, J.L. Davenport and J. Davenport, eds., Springer, Dordrecht, 2006, pp. 39–69. [101] M. Verlaque, C. Durand, J.M. Huisman, C.F. Boudouresque, and Y. Le Parco, On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta), Eur. J. Phycol. 38 (2003), pp. 325–339. [102] J. Klein and M. Verlaque, The Caulerpa racemosa invasion: a critical review, Mar. Poll. Bull. 56 (2008), pp. 205–225. Advances in Oceanography and Limnology 217 [103] L. Piazzi, G. Ceccherelli, and F. Cinelli, Threat to macroalgal diversity: effects of the introduced alga Caulerpa racemosa in the Mediterranean, Mar. Ecol. Prog. Ser. 210 (2001), pp. 149–159. [104] L. Piazzi, D. Balata, E. Cecchi, and F. Cinelli, Co-occurrence of Caulerpa taxifolia and C. racemosa in the Mediterranean Sea: interspecific interactions and influence on native macroalgal assemblages, Crypt. Alg. 24 (2003), pp. 233–243. [105] L. Piazzi and D. Balata, The spread of Caulerpa racemosa var. cylindracea in the Mediterranean Sea: an example of how biological invasions can influence beta diversity, Mar. Env. Res. 65 (2008), pp. 50–61. [106] O. Jousson, J. Pawlowski, L. Zaninetti, A. Meinesz, and C.F. Boudouresque, Molecular evidence for the aquarium origin of the green alga Caulerpa taxifolia introduced to the Mediterranean Sea, Mar. Ecol. Prog. Ser., 172 (1998), pp. 275–280. [107] M. Verlaque and P. Fritayre, Modification des communaute´s algales me´diterrane´ennes en presence de l’algue envahissante Caulerpa taxifolia (Vahl) C. Agardh, Oceanol. Acta 17 (1994), pp. 659–672. [108] C.F. Boudouresque, A. Meinesz, M.A. Ribera, and E. Ballesteros, Spread of the green alga Caulerpa taxifolia (Caulerpales, Chlorophyta) in the Mediterranean: possible consequences of a major ecological event, Sci. Mar. 59 (1995), pp. 21–29. [109] M. Harmelin-Vivien, P. Francour, and J.G. Harmelin, Impact of Caulerpa taxifolia on Mediterranean fish assemblages: a six year study, in Proceedings of the workshop on invasive Caulerpa in the Mediterranean, MAP Tech. Rep. Athens, UNEP 125 (1999), pp. 127–138. [110] X. Villèle de and M. Verlaque, Changes and degradation in a Posidonia oceanica bed invaded by the introduced tropical alga Caulerpa taxifolia in the north Western Mediterranean, Bot. Mar. 38 (1995), pp. 79–87. [111] G. Ceccherelli and F. Cinelli, Effects of Posidonia oceanica canopy on Caulerpa taxifolia size in a north-western Mediterranean bay, J. Exp. Mar. Biol. Ecol. 240 (1999), pp. 19–36. [112] S. Ruitton, and C.F. Boudouresque, Impact de Caulerpa taxifolia sur une population de l’oursin Paracentrotus lividus à Roquebrune-Cap Martin (Alpes Maritimes, France), in First International Workshop on Caulerpa Taxifolia. C.F. Boudouresque, A. Meinesz, and V. Gravez, eds., GIS Posidonie, Marseille, 1994, pp. 371–378. [113] R. Lemée, C.F. Boudouresque, J. Gobert, P. Malestroit, X. Mari, A. Meinesz, V. Menager, and S. Ruitton, Feeding behaviour of Paracentrotus lividus in the presence of Caulerpa taxifolia introduced in the Mediterranean Sea., Oceanol. Acta 19 (1996), pp. 245–253. [114] P. Amade and R. Lemée, Chemical defence of the Mediterranean alga Caulerpa taxifolia variations in caulerpenyne production, Aquat. Toxicol. 43 (1998), pp. 287–300. [115] S. Longpierre, A. Robert, F. Levi, and P. Francour, How an invasive alga species (Caulerpa taxifolia) induces changes in foraging strategies of the benthivorous fish Mullus surmuletus in coastal Mediterranean ecosystems, Biodivers. Conserv. 14 (2005), pp. 365–376. [116] B. Daniel, S. Piro, E. Charbonnel, P. Francour, and Y. Letourneur, Lessepsian rabbitfish Siganus luridus reached the French Mediterranean coasts, Cybium 33 (2009), pp. 163–164. [117] M. Bariche, Y. Letourneur, and M. Harmelin-Vivien, Temporal fluctuations and settlement patterns of native and Lessepsian herbivorous fishes on the Lebanese coast (Eastern Mediterranean), Environ. Biol. Fishes 70 (2004), pp. 81–90. [118] A. Aronov, Comparative study of the ecology of three groupers (Epinephelidae, Serranidae) at the shallow rocky habitats of the Israeli Mediterranean coast, M.Sc. Thesis, Tel Aviv University, Tel Aviv, Israel, 90 pp. (2002) [Hebrew]. [119] M. Goren and B.S. Galil, A review of changes in the fish assemblages of Levantine Inland and marine ecosystems following the introduction of non-native fishes, J. Appl. Ichthyol. 21 (2005), pp. 364–370. [120] B. Lundberg, R. Ogorek, B.S. Galil, and M. Goren, Dietary choices of siganid fish at Shiqmona reef, Israel, Isr. J. Zool. 50 (2004), pp. 39–53. [121] M. De Pirro, G. Sarà, A. Mazzola, and G Chelazzi, Metabolic response of a new Lessepsian Brachidontes pharaonis (Bivalvia, Mytilidae) in the Mediterranean: effect of water temperature 218 [122] [123] [124] [125] [126] [127] [128] [129] [130] [131] A. Occhipinti-Ambrogi and B. Galil and salinity, in R. Casagrandi and P. Melià, eds., Ecologia. Atti del XIII Congresso della Società Italiana di Ecologia, 2004, pp. 70–71. http://www.ecologia.it/congressi/XIII/atti/ index.htm U.N. Safriel, A. Gilboa, and T. Felsenburg, Distribution of rocky intertidal mussels in the Red Sea coasts of Sinai, the Suez Canal, and the Mediterranean coast of Israel, with special reference to recent colonizer, J. Biogeogr. 7 (1980), pp. 39–62. H. Mienis, Native marine molluscs replaced by Lessepsian migrants, Tentacle 11 (2003), pp. 15–16. G. Rilov, A. Gasith, and Y. Benayahu, Effect of an exotic prey on the feeding pattern of a predatory snail, Mar. Environ. Res. 54 (2002), pp. 85–98. J.D. Olden and T.P. Rooney, On defining and quantifying biotic homogenization, Global Ecol. Biogeogr. 15 (2006), pp. 113–120. J.L. Ruesink, H.S. Lenihan, A.C. Trimble, K.W. Heiman, F. Micheli, J.E. Byers, and M.C. Kay, Introduction of non-native oysters: ecosystem effects and restoration implications, Annu. Rev. Ecol. Evol. Syst. 36 (2005), pp. 643–689. M. Edwards and A.J. Richardson, Impact of climate change on marine pelagic phenology and trophic mismatch, Nature 430 (2004), pp. 881–884. P. Koeller, C. Fuentes-Yaco, T. Platt, S. Sathyendranath, A. Richards, P. Ouellet, D. Orr, U. Skúladóttir, K. Wieland, L. Savard, and M. Aschan, Basin-scale coherence in phenology of shrimps and phytoplankton in the North Atlantic Ocean, Science 324 (2009), pp. 791–793. L.H. Yang and V.H.W. Rudolf, Phenology, ontogeny and the effects of climate change on the timing of species interactions, Ecol. Lett. 13 (2010), pp. 1–103. L.H. Yang and V.H.W. Rudolf, Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities?, Ecol. Lett. 9 (2006), pp. 357–374. A.J. Southward, O. Langmead, N.J. Hardman-Mountford, J. Aiken, G.T. Boalch, P.R Dando, M.J Genner, I. Joint, M.A. Kendall, N.C. Halliday, R.P.H. Harris, R. Leaper, N. Mieszokowska, R.D. Pingree, A.J. Richardson, D.W. Sims, T. Smith, A.W. Walne, and S.J. Hawkins, Long-term oceanographic and ecological research in the western English Channel, Adv. Mar. Biol. 47 (2005), pp. 1–105.