**3. Recent invasion of gobies: why?**

e.g., coot, *Fulica atra*, and swan, *Cygnus* sp. [56]. Nevertheless, it is important to mention that the use of grass carp has allowed in certain cases to effectively control macrophyte development while avoiding the use of more costly and environmentally unacceptable alternatives

These two examples illustrated what has occurred in the past in France (and more generally in Europe) to improve angling, aquaculture production, and management of ecosystems. Today, it would be a futile and potentially a controversial exercise to try to eradicate these two species and more generally already established alien fish species because of high expense, difficulty of success, and the likelihood of imposing substantial collateral damage [56, 64]. However, as the possible outcomes of introductions are still very poorly documented, the precautionary approach ("guilty until proven innocent") is most appropriate for dealing with new alien species introductions [3, 51]. Because, nowadays, aquaculture is the main pathway of initial introduction of new fish species in Europe [6], one possible way to decrease risks while increasing production [16] would be therefore to rely more on the production of local species with valuable qualities such as pikeperch (*Sander lucioperca*) or European perch (*Perca* 

The topmouth gudgeon is a small cyprinid originating from East Asia, including Japan, the Korean section of the Amur River Basin, China (basins of the rivers Yangtze and Hoanghe), and Taiwan [65]. It was accidentally released in Europe in early 1960s with stocking material of Asian herbivorous cyprinids [51, 56, 65–67]. Then, because of both stocking and natural range expansion, it has rapidly spread across Europe [51, 56, 67] and more generally in numerous countries in the world, being now classified as a worldwide pest [66]. It still continues today to expand its range, and represent one of the most common alien species in France [49]. Similarly, following its introduction into lakes in the UK in 1996, populations appear to establish rapidly and become dominant in the fish community (often >97% by number) [64]. The reason for its success is its very high reproductive rate, which gives rise to dense populations of fish that compete with fry of other species [65]. Besides, this species is opportunist and has a wider ecological and physiological tolerance than many European fish species and can survive to a moderate degree of pollution, elevated temperatures, and low water levels. The ability to spawn on any smooth-surfaced object, such as branches, leaves, and artificial substrata, is another important factor likely to have contributed to the rapid dispersal of this species [65]. The impact of the topmouth gudgeon is poorly documented in France [42]. Yet, in other countries, it has been shown that it can compete for food with other species such as *Aphanius anatolie* and *Orthrias* sp. [65]. It was also described that populations of *Leucapius delineatus* decreased when topmouth gudgeon increased, the latter being a vector of a lethal pathogen for the former [49, 64, 65]. More generally, their high abundance provokes concerns of detrimental ecological impacts through, for example, high competition for resources such as food and spawning habitat, and they become a pest species to anglers [64]. The topmouth gudgeon is included in the list of exotic species of concern in the framework of European Union legislation addressing the problem of invasive alien

such as insecticides or herbicides [16].

82 Biological Resources of Water

*fluviatilis*) ([54], Teletchea et al. 2009).

species (EU Regulation No. 1143/2014).

**2.2. One unwanted invasive species:** *Pseudorasbora parva*

The recent, spectacular invasion of French hydrosystems by gobies is a good medium to discuss about what makes the success of an invasion. Since 2007, four freshwater Gobiidae species have been introduced in French hydrosystems: the tubenose goby (*Proterorhinus semilunaris*) in 2007, the bighead goby (*Ponticola kessleri*) in 2010, the round goby (*Neogobius melanostomus*) in 2011, and the monkey goby (*Neogobius fluviatilis*) in 2015. All that Ponto-Caspian species have moved in Europe with a contiguous East to West range expansion, with a spread from the Black Sea to the Rhine Delta observed as early as in the 1960s for the tubenose goby. Here, we focused on the round goby that reach locally high densities in many locations of the Upper Rhine and the Moselle River [35, 68]. This species has begun to spread in the 1990s [69]. It was observed for the first time in a downstream section of the Upper Rhine in Germany (between Düsseldorf and Cologne) in 2008, upstream of the confluence with the Neckar in 2010, in the French Upper Rhine (the Gambsheim fishway) in 2011 and in Basel harbor, 143 km upstream the Gambsheim fishway, in 2012 [35, 70]. Five years after its first observation, the round goby represented in several locations along the Upper Rhine more than 80% of the total catch by electrofishing (100 fishing points). The relative density of the round goby never fall below 25% of the total catch 1 year after its first observation, with a maximum value reaching 90% in a location dominated by rip-rap embankment [68]. This population dynamic is an amazing success that we dissected considering first the species bio/ecological traits and secondly the characteristics of its recipient ecosystems.

#### **3.1. A profile of invader**

Potential reasons for the proliferation of the round goby include (1) its reproductive success, (2) its singular behavior by comparison with native species, and (3) its tolerance to a wide range of physicochemical conditions. The fecundity per round goby female during a reproductive season ranges between some hundreds and a maximum of 5200 eggs that are divided in up to six spawns per year (unpublished results and values reported in [71, 72]). This number of eggs is not important by comparison with native species but the round goby exhibits two characteristics that make them prolific: multiple spawning combined to a protracted reproductive season and some forms of parental cares [73, 74]. The male occupies and defends a nest an enclosed cavity—to which females are attracted to spawn adhesive eggs on the undersize of rocks [75–77]. In laboratory experiments conducted in Canada, up to three females were selected by a male and spawned sequentially in a nest [78], but field observations reported that up to 15 different females could enter a nest to spawn [76]. Inside the nest, eggs are regularly inspected by males and constantly ventilated using pectoral and caudal fins. In Europe, gobies are the most typical species of guarders—nest spawners according to the typology of parental investment recently used by [23] in a comparative study between exotic and native fish.

Gobies lack a swimbladder, which makes their positioning in the water column predominantly benthic. They stand at the bottom and are considered bad swimmers in that they cannot fight against an important current or make jumps. A consequence is that at any stage of their biological cycle the gobies need numerous shelter and hiding places in their environment. Mineral structures (pebble, stones, and blocks) or macrophytes are useful habitats but in a given environment they would be more frequent in hard substrates as typically rip-rap embankments [79–81]. Few other native species, such as the European bullhead (*Cottus gobio*), the freshwater blenny (*Salaria fluviatilis*) or the ruffe (*Gymnocephalus cernua*), have these characteristics [43, 82]. *Neogobius melanostomus* inhabits a wide range of temperate freshwater and brackish-water ecosystems [72]. It has also demonstrated its capacity to adapt to local conditions in terms of prey availability [72]. This species exhibits a wide thermal tolerance, ranging from −1 to 30°C, but its energetic optimum temperature is estimated to be 26°C [72]. They would also be fairly little sensitive to pollutions. The distinguishing ecological features of the round goby by comparison with native ones make them singular in the range of bio/ecological profiles of species in place, a distinctiveness that could promote its success [25].

can have a declining level of competition. The resulting consequence is that the remained native species in place is not efficient to compete with some euryecious and prolific species. Furthermore, the rule of biotic factors in the success of gobies can be explained from a theoretical point of view by the invasional meltdown [84] and the enemy release hypotheses [85, 86, 87]. To be explained, the invasional meltdown can be drawn schematically. The propagule pressure received by a navigated and highly modified hydrosystem, such as the Rhine, is so important that a first exotic species always finished successfully. This one became a factor favoring a second exotic species, for example, because it will decrease the pressure of a potential predator. The two exotic species can then pave the way for a third exotic species and so on. This concept could probably be applied to the round goby in that it was preceded by the invasion of crustaceans and molluscs fed massively by this fish [88]. The enemy release hypothesis assumes the advantage of the loss of the original parasite burden of an invader. A recent study [89] revealed that 3 years after its first observation, the round goby hosted only one macroparasite in the French Upper Rhine, whereas in all other locations along its invasive pathway or its native range a minimum of three macroparasites were reported. This is typically an example of the enemy release an introduced species can benefit at least at the

Alien Fish Species in France with Emphasis on the Recent Invasion of Gobies

http://dx.doi.org/10.5772/intechopen.73408

85

The main goal of the present chapter is to give an update picture of alien fish species in France and their fate in the past decades. We dissected how the fish introduction history in France switched from voluntary introduction in the nineteenth century to unintentional but humanaided introductions (aquarium trade and global ship transport). The 28 alien fish established represent one-third of the fish species in France and >25% of the European exotic fish. Four species of our list are included among the 100 worst invasive species of Europe (DAISIE) and three others among the 100 worst invasive species of the world (IUCN). The information gathered will allow discussing the possible reasons explaining whether an alien species is able or not to establish sustainable populations in France and thereafter became invasive, such as gobies. Now and in the near future, natural resource managers have no other choice than to deal with them because no invasive fish have spontaneously collapsed up to a local

beginning of the invasion process.

**4. Conclusions**

extinction in France.

**Author details**

Fabrice Teletchea<sup>1</sup>

and Jean-Nicolas Beisel<sup>2</sup>

\*Address all correspondence to: jn.beisel@engees.unistra.fr

\*

1 University of Lorraine, UR AFPA, USC INRA, Vandoeuvre-lès-Nancy, France

2 University of Strasbourg, CNRS, ENGEES, LIVE UMR, Strasbourg, France

#### **3.2. Hydrosystems prone to invasions**

There are multiple potential and non-exclusive hypotheses to explain the gobie's success from the hydrosystem point of view. Among these, we emphasize the ideas (1) that the environments are not saturated in species and (2) that the rivers were man-modified in a way favoring the installation of exotic species.

The environments invaded by exotic species are not saturated in species for two main reasons. First, they correspond to hydrosystems that were largely defaunated during the Würm glaciation (80,000–10,000 BP). At the end of this period, the Rhine basin was recolonized by fish species from refuge areas that were outside ice range extension [83]. This recolonization by natural process takes a long time in the Rhine River considering the isolation of this basin and its geographical orientation with the downstream part to the North. The process was artificially accelerated these last centuries by human-aided introduction and the opening of the hydrographic basin with canals. Nowadays, the Upper Rhine is the main navigating way in Europe with two-third of goods transported on that fluvial road (330 millions of tons per year). Man activities allowed species from refuge area during the last glaciation, in particular the Ponto-Caspian area, to reach this unsaturated ecosystem. The Rhine has hence become the main entrance point for the dispersal of many invasive aquatic animal species in France over recent decades [7]. Another reason why ecosystems are not saturated in species is that pollution and human activities have profoundly modified natural communities, leaving vacant ecological niches within the hydrosystem. The decline of the Atlantic salmon (*Salmo salar*) or the European eel (*Anguilla anguilla*) in French inland waters are for example well documented. In conclusion, the ecosystems are not saturated because the post-glaciation process of recolonization is not achieved and several native species in place have already declined.

Second, the river stretches that served as entrance point in French hydrosystems are highly modified in terms of structure, quality, and functioning. The alteration of their habitats has placed the native species in a situation of anachronism: they are un-adapted to their own natural environment. The changes of habitats were too fast since the nineteenth century to allow a real adaptive response from species in place. Most of them disappeared, and the others can have a declining level of competition. The resulting consequence is that the remained native species in place is not efficient to compete with some euryecious and prolific species. Furthermore, the rule of biotic factors in the success of gobies can be explained from a theoretical point of view by the invasional meltdown [84] and the enemy release hypotheses [85, 86, 87]. To be explained, the invasional meltdown can be drawn schematically. The propagule pressure received by a navigated and highly modified hydrosystem, such as the Rhine, is so important that a first exotic species always finished successfully. This one became a factor favoring a second exotic species, for example, because it will decrease the pressure of a potential predator. The two exotic species can then pave the way for a third exotic species and so on. This concept could probably be applied to the round goby in that it was preceded by the invasion of crustaceans and molluscs fed massively by this fish [88]. The enemy release hypothesis assumes the advantage of the loss of the original parasite burden of an invader. A recent study [89] revealed that 3 years after its first observation, the round goby hosted only one macroparasite in the French Upper Rhine, whereas in all other locations along its invasive pathway or its native range a minimum of three macroparasites were reported. This is typically an example of the enemy release an introduced species can benefit at least at the beginning of the invasion process.
