Proceedings of the Fourteenth International MEDCOAST Congress on Coastal and }vfarine Sciences, Engineering, Management and Conservation

MEDCOAST 2019, 22-26 October 2019, Marmaris, Turkey, E. Dzhan (Editor)

Impact of Climate Change on Non-native Species

Patrice Francour(1), Virginie Raybaud(1

), Christine Pergent­Martini(2) and Joseph Donini(3)

OJ ECOSEAS (UMR 7035), University Côte d'Azur- CNRS, Nice, France Tel: +33 6 7717 63 36 Email: Patrice.FRANCOUR@univ-cotedazur.fr

(2) Coastal Ecosystem Team, FRES 3041 1 UMR 6134

University of Corsica, Corte, France Tel: +33 495 45 00 55 Email: pmartini@univ-corse.fr

(J) Office de l'Environnement de la Corse, Corte, France Tel: +33 495 450 426 E-mail: donini@oec.fr

Abstract

Non-indigenous species (NIS) represent one of the major causes of the loss of biodiversity. The Mediterranean is one of the most severely invaded seas, with to date more than 800 NIS recorded. The majority are thermophilous species which arrived via the Suez canal, but certain NIS have also extended their natural range of distribution by passing through the strait of Gibraltar. Maritime transport, aquaculture and aquariology are other vectors of introduction ofNIS. Iftoday the western basin of the Mediterranean is less affected by the arrivai of NIS than the eastern basin, climate warming may well aggravate this problem in the coming decades. Recently, a few individuals, of several Lessepsian species, have been observed in the western basin, and it is expected that the future increase in temperatures will facilitate their installation. The NIS are the cause of numerous forms of impact affecting native species, the functioning of ecosystems and the goods and services that they provide. Furthermore, many NIS are toxic and their presence may constitute a real health risk.

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In the face of the increase of the risks related to these NIS, it must be admitted that the resources for managing them remain limited, but that early detection constitutes an asset for preventing or at least delaying the acclimatation of new NIS and controlling those that are already established. The contribution of modelling, for the purpose of identifying the priority regions for surveillance (by means of mapping of the risk of installation of NIS), or the development of observation networks, such as the 'Alien Corse' network, which provides ongoing surveillance and information for all the stakeholders (through the involvement of the Office de l'Environnement de la Corse (Corsica environmental authority), scientists and fishery professionals and representatives of the Fédération Française d 'Etudes et de Sports Sous-Marins (French federation for underwater sports and studies)) consitute essential measures for ensuring the success of eradication operations.

Introduction

Non indigenous species (NIS) are considered to be one of the most important cause of biodiversity loss and a major pressure on several ecosystems (Katsanevakis et al., 2014). In the same way, actual knowledge on climate change allows to suppose that climate change could be responsible of major impacts on the functioning of Mediterranean ecosystems in the next future. The aim of this approach is to evaluate the present situation conceming NIS at the regional level and to evaluate potential relationships between these both phenomenons, which alter biodiversity, and if it is possible to reduce their negative effects.

Status of Knowledge Concerning Arrivai of the Non-indigenous Species

What is a non indigenous species?

NIS, sometimes also referred to as non-native, introduced or exotic species, are plants or animals which have been introduced, intentionally or not, which have established populations and which have propagated in the wild state within the new host region (Otero et al., 2013). In their original range of distribution, these species live in equilibrium with their local natural environment and the populations are controlled by interactions such as predation, parasitism and disease. However, once they penetrate into a new environment, there is a risk that these species may be out of control and, if they become established, may then become invasive.

The NIS are introduced outside their natural range of distribution by human means, either directly or indirectly, and may cause damage to the biodiversity and to the ecosystem services by being in competition with and sometimes replacing the native species, giving rise to complex alterations in the structure and functioning of the new host ecosystem. Because of certain characteristics that make them more difficult to control and contain, the invasive species often succeed in colonising new ecosystems. These characteristics include their ability to prosper in different environments and to tolerate a wide diversity of environmental conditions, high rates of growth and reproduction, the absence of natural predators and the ability to exploit different types of food sources.

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In the Mediterranean, more than 800 NIS have been recorded to date (Zenetos et al., 2017). They are essentially pluricellular organisms; the unicellular organisms are still very poorly known.

The vectors of arrivai in the Mediterranean

The majority ofNIS observed in the Eastern Mediterranean came in through the Suez Canal (Lessepsian species); in the western basin, they are rather species which have come through the Strait of Gibraltar (Herculean species). Consistently with the above defmition, the passage of a species through the Suez Canal is the result of an indirect action by man; it is therefore truly a non-native species. Passage via Gibraltar corresponds to an extension of the species' range of distribution, even if it may have been favoured by climate change of human origin. Besicles entry via straits, whether natural or excavated by man, transport by ships represent one of the major vectors of introduction. Other activities such as aquaculture or aquariology may also be vectors of introduction ofNIS '(Katsanevakis et al., 2014).

Transportation by ship over long distances may occur in different ways for these species: attached to the hull of a ship, carried in the ballast waters or trapped in the sea­chests. Attachment to the hull of ships (or fouling) concerns plants and sessile invertebrates. The use of old anti-fouling paint may favour this type of transportation. Transportation in ballast water can on1y be envisaged for small-sized pelagie or planktonic organisms or larvae, capable of passing through the uptake filters and able to survive in darkness (Bailey, 20 15). Although there is no scientific evidence for it, it is possible that certain species may also be carried onto ships by the anchors and survive in the anchor locker before being released into the water in a new environment when the anchor is lowered. This means of transport was suggested as an explanation for the dissemination of Caulerpa taxifolia (Sant et al., 1996). Until recently, the transportation of fishes of a certain size by ships seemed difficult or impossible. In certain ships, there are sea-chests, fairly large cavities (as big as a man or bigger), open to the exterior and from which the water for the ballast is pumped (Coutts and Dodgshun, 2007). Fishes of a certain size may take refuge there. While the ship is on the move, the speed of the ship will trap the fishes inside the sea-chest. They can only escape when the ship stops. This form of transportation was suggested for Oplegnathus fasciatus, a fish from the Indian Ocean found at Malta (Schembri et al., 2010).

Aquariology constitutes a professional activity (public aquariums) and a private hobby (personal aquariums) which represents a potential vector of introduction if NIS kept in the aquarium are released, intentionally or not, into the sea. The strains of Caulerpa taxifolia occurring in the Mediterranean come from a public aquarium (Jousson et al., 1998). Several species of tropical fish, frequently used in aquariology, have recently been observed in the Mediterranean (Zenetos et al., 20 16).

What is happening in the North-Western Mediterranean?

The North-Western Mediterranean is not under the direct influence of the Suez Canal. The Lessepsian species are therefore rare in the western basin and mainly occur in the eastern basin of the Mediterranean (Katsanevakis et al., 2014). The non-native

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species of the western basin are mainly of Atlantic origin. Since entry via the Strait of Gibraltar may correspond to a natural extension of a species, their arrivai is not necessarily related to hurnan activities. For exarnple, the gradua! spread of Parablennius pilicornis from the tropical Atlantic to the Mediterranean is probably not due to man (Pastor and Francour, 2010). The same is the case for other tropical Atlantic species (Ben Rais Lasrarn et al., 2008). Nevertheless, the intensity of commercial and private traffic makes likely the arrivai of a non-native species in the Western Mediterranean by another route. For example, among the invertebrates, numerous exotic species have recently been observed in harbours following their introduction by ships (see for exarnple L6pez-Legentil et al., 20 15). Sirnilarly, the intensity of trade related to aquariology and aquaculture means that severa! species have been introduced, deliberately or not, into the Western Mediterranean, such as, for exarnple, Caulerpa taxifolia (Jousson et al., 1998), Scatophagus argus (Zarnmit and Schembri, 2011). The Thau Lagoon certainly represents the place where the specifie richness in non-native macrophytes and invertebrates is the highest in the North-Western Mediterranean because of aquaculture (Katsanevakis et al., 2014 ). Although none of these species has yet been identified along the coasts of Corsica, at least 49 NNS have already been reported there (Monnier et al., 2017).

Over the past 10 years, severa! Lessepsian species, already established for severa! years in the Eastern Mediterranean, have been observed in the western basin (Siganus luridus, Daniel et al., 2009; Fistularia commersonii, Bodilis et al., 2011; Lagocephalus sceleratus, Kara et al., 20 15). If certain of these species (Fistularia commersonii, Si gan us rivulatus) frequent the coasts of Corsica, sightings of them remain rare (Monnier et al., 20 17). These recent arrivais may have resulted from an alteration in the exchanges between the two basins (Francour et al., 2010; Otero et al., 2013), related to climate change (e.g. Lascaratos et al., 1999). The various scenarios proposed by the IPCC for the coming decades give grounds for fears that the passage of Lessepsian species from the eastern basin to the western basin is bound to intensify. A model of the changes to come is thus much to be desired in order to anticipate the arriva! of new non-native species in the western basin (see last section).

Impact of Climate Change on the Spread of Exotic Species

Alterations of the native biodiversity and of existing ecosystems

The establishment of non-native species, whether invasive or not, generally has an impact on the host ecosystem, but the aquatic environrnents have still been very sparsely studied. In the Mediterranean, the main impacts have been reported from the eastern basin, with for exarnple alterations in the trophic chains (Goren et al., 2016). In the western basin, the main references con cern impacts linked to the spread of Caulerpa taxifolia : decline in abundance for fishes (Franco ur et al., 1995) or invertebrates (Francour et al., 2009), changes in the behaviour patterns (Longepierre et al., 2005) or col our of fishes (Arigoni et al., 2002).

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Alterations at landscape scale have also been reported. In the Eastern Mediterranean, for exarnple, the arrivai of non-native herbivorous fishes (Siganus spp.) led to a regime shift with the disappearance of forests of erect macrophytes (Sala et al., 2011 ). In the western basin, the homogenisation of the bottoms during colonisation by C. taxifolia resulted in the loss of the structual complexity of the habitat and an impact on the recruitment offishes (Cheminée et al., 2016).

Alterations in human activities related to the marine environment

Direct (decline of abundance) or indirect (alteration of the landscape) alterations of the existing ecosystems through invasions may result in the disturbance of extractive activities such as fishing if the native species become less abundant or iftheir biological cycle is disturbed (Katsanevakis et al., 2014a). These consequences may be negative, or positive when an ecosystem service is provided or improved by a non-native species. For exarnple, the presence of fish species of tropical origin may enhance the attraction of divers to a Mediterranean sit~. Nevertheless in the Mediterranean, knowledge is still very patch y, and does not provide an adequate basis for assessment of this impact.

The health risks associated with the arrivai of exotic species

The presence of toxins is more frequent in tropical species than in those of temperate zones. Consequently, the arrivai of non-native species of tropical origin increases the risk of seeing toxic species arrive. This reduces the possibility of there being a natural process of control by a native predator, but it represents above all a potential health risk. The presence of highly toxic species in the Mediterranean is already a reality, with the stonefish Synanceia verrucosa and the lionfish Pterois miles (Edelist et al., 2011). A fish close to the Japanese fugu, Lagocephalus sceleratus, also occurs in the Eastern Mediterranean and has recently reached the western basin (Kara et al., 2015). The consumption of this species has caused human health problems in the Eastern Mediterranean since 2005 (Bentur et al., 2008).

Similarly, with climate change, we may note an increase in the frequency and intensity of algal blooms, sorne of which are associated with organisms that produce toxins and are known under the term Harmful Algal Blooms (Smayda, 1997). Thus, numerous episodes of harmful blooms of the genus Ostreopsis have been reported in the Mediterranean, for exarnple in Corsica (Blanfuné et al., 20 15). This benthic dinoflagellate, which develops in shallow waters on hard substrate or on macrophytes, may cause the death of benthic organisms and have adverse effects on human health such as respiratory difficulties, conjunctivitis and skin irritation, which can occur either by direct contact with cells and by inhalation or by indirect contact through ingestion of seafood (Blanfuné et al., 2015). In urbanized areas, blooms of Ostreopsis spp. can induce beach closures or evacuation of the shore, resulting in economie loss for the tourism industry (see Blanfune et al., 2015). Furthermore, in the case ofbloom events in mussel culture areas, the closure of aquaculture facilities can be ordered, also resulting in economie loss. Finally, it should be borne in mind that ballast water can transport pathogen organisms and is thus likely to cause public health problems (Takahashi et al., 2008).

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The Future: Alterations are a Certainty, Which We will have to Learn to Manage

Improved early detection of exotic species

There is generally a time-lag between the entry of a non-native species into the Mediterranean and its detection. This time-lag, depending on its duration, may limit the effectiveness of any subsequent control measures. Networks of observers can be organised with the aim of improving the potential for early detection of NIS. The current climate change will probably result in the arrivai of non-native species in the Mediterranean in the coming years (see below). It would thus seem to be a necessity to develop networks of observers (Azzurro and Bariche, 2017) orto enhance the means for early detection by issuing specially designed information sheets or brochures (Otero et al., 2013). For this purpose, Corsica has since 2015 maintained a purpose-designed monitoring system -the Réseau Alien Corse - for the early detection ofNNS (Barralon et al., 2019). This network, through the participation of the French diving and educational federation FFESSM and scientists, enables the deployment along much of the coast of regularly-informed observers (provision and updating of information by team leaders, distribution of submersible information sheets, identification cards for NIS already reported in the western basin).

Use of ecological niche models to predict the risk of establishment of exotic species

Ecological niche models are currently one of the most widely used tools for studying the spatial distribution of organisms in relation with the environmental conditions. Their purpose is to predict the geographical distribution of a species on the basis of a mathematical representation of its ecological niche, and thus to map the probability of its occurrence according to the environmental conditions. In the case of NNS, these techniques enable maps of risk establishment to be produced, illustrating the probability that a species will find favourable conditions and become established in a new environment (Raybaud et al., 2015). These ecological niche models thus provide a basis for prioritising the first zones to be placed under surveillance for early detection monitoring. The models focus on identifying statistical associations between the geographical distribution of a species and environmental conditions recorded at this site. The modelled niche is first projected in the geographical area of the native region in order to validate the model by comparing it with the observed distribution pattern. Then, in the case of NIS, the modelled niche is projected in one or several non-native regions in order to map the risk of establishment (Fig. 1).

Coupled with the IPCC climate scenarios, the ecological niche models also offer a basis for predicting the future distribution of high risk zones, at all stages up until the end of the century and according to various socio-economic scenarios (Beaugrand et al., 2015; Bellard et al., 2013; Raybaud et al., 2015; Fig. 1).

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Probability of presence

0.5

0

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Present time

Projection for 2090-2099 with the RCP8.5 scenario

Fig. 1: Top: map of the current probability of presence of the lionfish Pterois miles in the Mediterranean Sea and occurrence records (black dots). Bottom: projection of the probability of presence for the period 2090-2099 according to the scenario RCP8.5. (Adapted from Fontaine 2017).

Although much progress has been made over recent years in refming the predictions of these models, there is still ample room for improvement. For example, the ecologica1 niche models have been established species by species and do not take into account the biotic relationships which operate between organisms, such as predation or competition (Mellin et al., 20 16). Taking into account all the processes that might alter the defmed niche of an exotic species is the next stage to be achieved in order to refine future projections ofhigh risk zones.

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Can management measures be envisaged?

The current means for the management and control of non-native species are still fairly basic and involve simply destroying the new individuals (Otero et al., 2013). The recourse to biological methods of control is difficult and is very rarely used in the aquatic medium (Giakoumis et al., 2019a). The success of these campaigns of destruction will only be ensured on condition that they are started as far upstream as possible, irnmediately after the frrst sightings. Eradication is then possible. Otherwise, it will only be a matter of controls that will have to be repeated over time. In the Western Mediterranean, for example, regular uprooting after prospection surveys limited the spread of C. taxifolia, but did not eradicate it (Barcelo et al., 2013).

The degree of invasibility of an environment by non-native species is based on severa! factors. Often, it is shown that the invasibilty decreases when the specifie richness of the host environment is high. It may thus be assumed that well protected environments in which the biomass of predators of high trophic level is high (integral reserves, for example) are environments where the probability of establishment of a species will be low because of the potential control exercised (Francour et al., 2010). This hypothesis has not yet been properly tested in the Mediterranean, in particular because such environments are to be found in the Western Mediterranean, whereas the majority of non-native species occur in the eastern basin (Giakoumi et al., 2019b). The maintenance of communities in good condition nevertheless represents an additional argument in favour of limiting the expected proliferation non-native species in the Mediterranean as a result of the current climate changes.

Conclusion

Climate change already favours the arrivai of new non-native thermophilous species and their acclimatation in the Mediterranean, and it is highly likely that we will see an increase in the frequency of these arrivais and the success of acclimation over the coming decades. Severa! of the NNS reported in the Mediterranean (Ostreopsis sp, Lagocephalus sceleratus, Mnemiopsis leydii, Pterois miles) present an invasive character and have an impact on certain socio-economic activities. The naturalisation of new NNS might alter the functioning of ecosystems and the economie activities which are dependent on them, and clearly it is therefore necessary to improve the methods of detection of NNS, to assess their future patterns of distribution, and above all to anticipate and integrate the changes resulting from their presence in the management of economie activities such as fisheries or tourism, as well as with regard to public health issues.

Acknowledgements

This study could not have been carried out without the fmancial support of the Fondation Prince Albert II de Monaco and of the IUCN.

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