List of the non-indigenous fish species of Indo-Pacific and Red Sea origin with references on quantitative information in abundance in the Mediterranean Sea
Geological history of life on earth tells that continents have been isolated for long periods. It also reveals that collisions of land masses as well as lower sea levels allowed the spread of fauna and flora (Stachowicz and Tilman, 2005). In today's seas, marine communities are being altered and remodelled at an unprecedented rate, when compared to natural changes which occured over geological times. While many marine species populations are dwindling due to overfishing and habitat destruction (Jackson et al., 2001), other species are invading new areas through anthropogenic vectors (Carlton 1985, Galil 2006, Galil et al. 2007). During the last centuries, human transport has increased the number of non-indigenous species (NIS) introductions. For example, half of the plant species of Hawaii are exotics (Sax et al., 2002) as are about 20% of plants in California bay (Sax, 2002) and about 18% of fish species in the eastern Mediterranean Sea (Golani et al. 2002, Golani et al. 2006, EastMed 2010, Golani 2010).
Understanding invasion ecology requires a good knowledge of ecological processes in the systems under study, prior to invasion. Diversity, structure, and function of natural communities would give insights into fundamental ecological processes which could in turn give a better understanding of potential effects following the introduction of NIS.
From a societal perspective, species invasions might pose serious threats to human economic interests and health (Yang et al., 1996; Sabrah et al., 2006; Katikou et al., 2009). Species invasions have also been considered to have negative impacts on native biodiversity (Reise et al., 2006; Streftaris and Zenetos, 2006; Galil, 2007; Lasram and Mouillot, 2008; Zenetos et al., 2009). Furthermore, invasions interacts with other disturbing factors to the marine ecosystem functioning such as habitat destruction, pollution and climate change (Rilov and Crooks, 2009). Disturbance caused by habitat destruction may open up space for invaders but space can also be released by the invaders themselves. Consider the example given by Rilov and Galil (2009) where two non-indigenous siganids might have modified the competition between algae and mussels through intensive grazing, thus providing space for the non-indigenous mussel
The increase of water temperature is also allowing the success of tropical exotic species in the Mediterranean Sea, a phenomenon that has been called ‘tropicalization’ (Bianchi and Morri, 2003). Conditions facilitating invasions are usually related to the physical and biological attributes of the new colonized habitats. Biological impact studies include mostly those species of economic interests (e.g. fisheries) (Streftaris and Zenetos, 2006), human health (e.g. toxic species) (Yang et al., 1996; Bentur et al., 2008; Katikou et al., 2009) and biodiversity (e.g. competition with indigenous species or habitat modifiers) (Golani, 1993a; Golani, 1994; Bariche et al., 2004; Azzurro et al., 2007a; Kalogirou et al., 2007; Wallentinus and Nyberg, 2007; Bariche et al., 2009). A lot of research has also focused on the factors controlling success or failure of invasive species by considering mechanisms of interactions between indigenous and NIS. There is no universal model explaining the mechanisms controlling the success or failure of an invading species (Stachowicz and Tilman, 2005). As far as the Mediterranean Sea is concerned, important mechanisms include competition for resources or space (Bariche et al., 2004; Kalogirou et al., 2007), top-down forces (Goldschimdt et al., 1993), herbivory (Lundberg and Golani, 1995; Galil, 2007), and parasites (Diamant, 2010).
A widely cited theory in invasion ecology is about the relationship between diversity and invasibility of an ecosystem (i.e. more diverse communities should be more resistant to invasion) (Leppäkoski and Olenin, 2000). The mechanism suggests that as species richness increases the competition intensifies and less food resources remain available for new colonizers (MacArthur, 1955; Levine and D' Antonio, 1999). Less diverse ecosystems possessing fewer species and simpler food-web interactions would therefore provide available niches for the establishment of NIS. This hypothesis is known as the "biotic resistance hypothesis" (Levine and Adler, 2004). As an aid to understand this mechanism, both observational and experimental approaches have been applied with conflicting results (Levine and D' Antonio, 1999). Studies that employ both observational and experimental approaches show that high diverse systems does reduce invasion success (Stachowicz and Tilman, 2005). There is a long history of theoretical discussions about the relationship between species richness and productivity or stability of a system. Threats to global species diversity caused by human activities have raised concern on the consequences of species losses to the functioning of ecosystems. In ecology, this concern has received a lot of attention. During the last 20 years, experimental tests of the relationship between species richness and ecosystem processes such as productivity, stability and invasibility have increased rapidly (Stachowicz and Whitlatch, 1999).
Other theories go back to the work of Darwin. Darwin’s “naturalization hypothesis” predicts that NIS are less prone to invade areas where closely related species are present. Those species would compete with their relatives and would encounter predators and pathogens. An opposing view is the “pre-adaptation” hypothesis predicting that NIS should succeed in areas where indigenous closely related species are present because they are more likely to share traits that pre-adapt them to their own environment. So far, these theories have been seldom tested on fish species and no clear pattern has emerged so far for these taxa (Ricciardi and Mottiar (2006). Ricciardi and Mottiar (2006) agreed with Moyle and Light (1996) that success is primarily determined by competitive interactions (e.g. “biotic resistance” hypothesis), propagulae pressure and environmental abiotic factors (i.e. the degree to which NIS physiological tolerances are compatible to local physical conditions). Rapid changes in environmental conditions, caused by human activities, have also been mentioned as to increase invasiveness (Occhipinti-Ambrogi and Savini, 2003). Habitats that lack predators are also suggested to be more prone to introductions of NIS (Moyle and Light, 1996). There is also a higher risk of further establishment of species in habitats that have already been invaded, referred as the "invasional meltdown" (Simberloff and Von Holle, 1999; Ricciardi, 2001). In a study from Great Lakes, Ricciardi (2001) found support for the "invasional meltdown" hypothesis by showing that positive interactions (mutualistic) among NIS are more common than negative (competitive). In further support of the "invasional meltdown" hypothesis, Ricciardi (2001) showed that exploitative interactions (e.g. predator-prey) among NIS are strongly asymmetrical to the benefit of one invading species at a negligible cost to another.
2. Current patterns of change of the Mediterranean biota
In the last century the Mediterranean Sea has been a receptacle of NIS, most of them arrived by mean of direct or indirect mediation of humans. Today, the Mediterranean Sea can be considered as one of the main hotspots of marine bio-invasions on earth (Quignard and Tomasini, 2000), and is by far the major recipient of NIS among European seas including macrophytes, invertebrates and fishes (Streftaris et al., 2005; Zenetos et al., 2010). The Mediterranean is unique because of its connection to the Indo-West Pacific realm via the Suez Canal (Fig. 1), allowing the so called Lessepsian migration (Por, 1978). The rate of this immigration has increased in recent decades and has ecological, social and economic impacts (Zenetos et al., 2008; Bilecenoglu, 2010; Zenetos et al., 2010). The Eastern Mediterranean basin is potentially more prone to introductions of subtropical and tropical NIS than the western basin. This has been mainly attributed to different physical and biological conditions between the two basins. It is to mention that the construction of the Aswan Dam on the Nile River in 1966 reduced significantly the freshwater flood into the Mediterranean Sea. This led to an increased salinity of 2-3% along the Mediterranean coast of Egypt and to a reduction of the most important sources of nutrients in the eastern Mediterranean Sea (Galil, 2006). The damming of the Nile might have positively favoured the westward dispersion of Lessepsian NIS along the Northern African shores (Ben-Tuvia, 1973).
New terms have been recently created to describe current changes of the Mediterranean biodiversity. Due to the tropical nature of most of the exotic species that enter the Mediterranean, various authors have defined the process of entrance and spread of these organisms as ‘tropicalization’ (Bianchi and Morri, 2004; Bianchi, 2007). Another definition that has been used is “demediterranization”(Quignard and Tomasini, 2000) that put the emphasis on the process of biotic homogenization of the Mediterranean Sea. Instead Massuti et al. (2010) used the term ‘meridianization’ to indicate the increasing divergence (in terms of composition of the biological communities) between the Eastern and Western sectors of the Mediterranean, due to the continuous influx of Lessepsian and Atlantic biota. This latter term, ‘meridianization’ should not be confused with ‘meridionalization’, which instead would indicate the northward expansion of southern (‘meridional’) species towards the northern sectors of the basin (Azzurro, 2008). Several indigenous species such as
More than 700 fish species inhabit the Mediterranean Sea with a general decrease in number moving eastwards (Quignard and Tomasini, 2000; Lasram et al., 2009). Among these, at least 80 are non-indigenous of Indo-West Pacific and Red Sea origin (Cicek and Bilecenoglu, 2009; Bariche, 2010b; EastMed, 2010; Golani, 2010; Bariche, 2011b; Sakinan and Örek, 2011; Salameh, 2011; Bariche and Heemstra, 2012). The abundance of these non-indigenous species is not well documented. The list of non-indigenous fish species with quantitative information from the Mediterranean Sea can be found in Table 1.
|Callionymidae||(Gucu and Bingel, 1994; Kalogirou|
|Carangidae||(Shakman and Kinzelbach, 2007)|
|Dussumieriidae||(Goren and Galil, 2005; Bariche|
|Fistulariidae||(Shakman and Kinzelbach, 2007; Carpentieri|
|Hemiramphidae||(Shakman and Kinzelbach, 2007; Carpentieri|
|Leiognathidae||(Gucu and Bingel, 1994)|
|Monacanthidae||(Gucu and Bingel, 1994; Harmelin-Vivien|
|Mullidae||(Gottlieb, 1960; Oren|
|Mullidae||(Gucu and Bingel, 1994; Golani and Ben-Tuvia, 1995; Goren and Galil, 2005; Shakman and Kinzelbach, 2007; Carpentieri|
|Scaridae||(Bariche and Saad, 2008; Carpentieri|
|Scombridae||(Shakman and Kinzelbach, 2007; Carpentieri|
|Siganidae||(Gucu and Bingel, 1994; Bariche|
|Siganidae||(George and Athanassiou, 1967; Bariche|
|Sphyraenidae||(Golani and Ben-Tuvia, 1995; Carpentieri|
The arrival of these invaders raises plain concern on the ecological and economic impact that such migrants have but the available information is still scarce (Rilov and Galil, 2009) and there is an obvious lack of knowledge. It is at the same time obvious that the ecological effect of some species is significant (Kalogirou et al., 2007; Bariche et al., 2009). Competitive exclusion and displacement of native species are often potential expectations in ecological studies (Bariche et al., 2004; Galil, 2007). A noteworthy example is the presence of the two Lessepsian herbivorous
3. The case of the invasive pufferfish
Lagocephalus sceleratus: Ecological consequences, economic impacts and risks for human health
Pufferfishes are marine fish species that are distributed in tropical and subtropical areas of the Atlantic, Indian and Pacific Ocean. Puffers include 121 species within the Tetraodontidae family among which nine (
Few dozens of tetrodotoxin poisoning cases occurred along the Levantine coast and in Cyprus (Bentur et al., 2008).
These efforts have included setting up posters warning the public about the lethal effects if consumed, but also that small individuals could easily be misidentified with other small commercial edible species such as
An invading species might sometimes go to a peak of density and then decline, a path often called boom and bust (Williamson and Fitter, 1996). This path followed the NIS bluespotted cornetfish
4. Do we need new methodologies to monitor current changes of Mediterranean fish diversity?
Concern has been expressed to the lack of monitoring, coordination, and study in relation to the changing diversity of the Mediterranean Sea. As a matter of fact, exotic fishes spreading in the Mediterranean Sea are usually found by chance as specific procedures for their detection are lacking (Azzurro, 2010). Consequently, the extent of these changes may be underestimated as usually happens in several other marine systems (Witenberg and Cock, 2001). Increasing efforts are being devoted to the survey of marine habitats but one of the major obstacles to research remains the lack of data at large geographical scales. This would be important to perceive temporal and spatial trends and to fill important existing information gaps. New methodologies involving local communities have recently proved to be successful in discovering trends of change in Mediterranean fish diversity (Azzurro et al., 2011). As a matter of fact, collaboration with local communities are increasingly used to approach the study of large scale changes in the natural world. As a matter of facts some countries, such as Australia and the USA (California; Hawaii) have already started monitoring projects which involve community-based actions for the detection of marine invasive species. People are basically asked to ‘monitor’ the marine environment around them, in the course of their daily activities and to provide reports of invasions and various tools and detection kits have been developed all around the world with the aim to widely disseminate information about potential invaders to target communities. In a pilot study called ‘alien fish alert’ fishermen and divers of the Sicily Strait were asked to provide reports of all “unusual occurrences” (Azzurro, 2010). Given the familiarity of fishermen with local species, no training on fish taxonomy was considered necessary and no black list was proposed, with the following slogan:
The collaboration with local fishery communities has several advantages when the species to monitor are fishes in respect to other groups of organisms. Fishery landings also provide quantitative data, samples and additional information. In addition, the identification of many fishes is relatively easy and this is an obvious advantage for their detection (Fig. 3). Therefore, members of local fishery communities, with broad geographical distributions and familiarity of natural environments could play a dynamic role for the early detection of environmental changes.
Another significant example of innovative ideas to monitor fish diversity changes in the Mediterranean Sea was ‘‘Local Ecological Knowledge’’ (LEK). In recent years, LEK has emerged as an alternative information source on species presence or qualitative and quantitative indices of species abundance (Rasalato et al., 2010). Local Ecological Knowledge can be defined as the information that a group of people have about local ecosystems. We usually rely on knowledge gained by individuals over their lifetimes, and not on what information has been handed through generations. To extract data and information from individuals’ memory, semi-structured or unstructured conversations between the researcher and the participant were used, a practice commonly called ‘‘oral history’’. In a recent study, Azzurro et al. (2011) provided evidence of a trend for thermophilic taxa to increase in the Central Mediterranean Sea on the basis of a set of interviews to local fishermen. The study was based on interviews to local fishermen and divers with more than ten years of experience. Species mentioned in each interview were used to build a presence-absence dataset that provided extremely coherent results about the northward expansion of families such as Carangidae and Sphyraenidae, whose expansion was only previously noted by occasional records in the scientific literature. These new methodologies give us the chance to get information that otherwise cannot be obtained from the efforts of single researchers. Hopefully in the next future their potential will be increasingly exploited for the monitoring and the understanding of the biodiversity changes in the Mediterranean Sea.