The cost of non-native aquatic species introductions in Spain : fact or fiction ?

The ecological and economic impact of non-native species introduction on local native biodiversity is often reported as undeniable scientific evidence on which to base management and sound policy. Here I used a combination of databases (Fishbase, FAO and IMPASSE) and an extensive review of existing literature to establish the proportion of non-native aquatic species introductions in Spain that are responsible for ecological and economic impacts. In Spain, aquaculture and angling are the two main ecosystem services responsible for introduction of non-native aquatic species. In total, forty two percent of all nonnative aquatic introductions are intentional. Very little ecological impact resulting from these non-native species introductions has been demonstrated with some representing a benefit to Spanish ecosystem services. In 2007, the economic benefits to Spanish aquaculture arising from non-native aquatic species (n=9) was close to €46.73 million (about U.S. $69 million) annually for an estimated average ecological risk for all introductions of 16.5% (SD= 26.85). These results must be seen in the context of other environmental factors such as habitat destruction, water abstraction and pollution from agricultural farming which represent major environmental pressures on Spanish aquatic fauna.


Introduction
Like many Mediterranean countries, in the last 30 years Spain has seen the demand and pressure on water rocketing (Anonymous 2005(Anonymous , 2006(Anonymous , 2007)).These water abstractions for irrigation of agricultural land, golf courses or supply of disproportionate urban development, underpin a rapid growth in the national and regional economy.According to the Spanish Ministry for the Environment, there are 510,000 illegal wells in Spain (Anonymous 2006).The main ecological impacts of such unregulated water abstraction have been the decline of wetland ecosystems, changes in land use, as well as the deterioration of water quality (Marchetti et al. 2006;Light and Marchetti 2007).In addition to deterioration of physical habitat and its direct consequences on native biotic fauna, increasingly, existing communities are modified by the introduction of non-native species (Elvira and Almodovar 2001;Rodriguez et al. 2005;Orizaola and Brana 2006).However, due to the magnitude of physical habitat changes, it remains difficult to determine if aquatic nonnative species are the driver of biodiversity changes or only passengers (Brown 2007;Didham et al. 2005;Sagoff 2005Sagoff , 2007)).For the same reasons, it is difficult to precisely characterise the non-native species contribution to both ecological and economic costs (Marchetti et al. 2004;Marchetti et al. 2006;Light and Marchetti 2007).
Worldwide, the ecological impacts arising from non-native fish species have rarely been demonstrated contrarily to an established idea that non-native fish are necessarily the cause of ecological disruptions if not of ecological impact (Gozlan 2008;Gozlan 2009;Gozlan and Newton 2009;Brown 2007;Didham et al. 2005;Sagoff 2005Sagoff , 2007)).However, it is worth noting that in some cases potential impacts of most non-native fish species are unknown due to geographical and taxonomic bias (Gherardi 2007).
Aquaculture and sport fishing, the main drivers for aquatic non-native species introduction (Gozlan et al. 2010a(Gozlan et al. , 2010b) ) are rapidly expanding worldwide and will continue to grow as a response to over-exploitation of wild fish stocks as currently major fisheries are commercially unsustainable and many others are on the verge of extinction (Pontecorvo and Schrank 2009).In order to grow, aquaculture will have to rely on market diversification and as such on the farming of new species likely to be non-native ones.Here the community of nonnative aquatic species introduced in Spain is analysed in terms of ecological impacts and economic benefits and perspectives are drawn on the future need/cost of non-native introductions in Spain.
The aim of this study is to 1) quantify the number and type of non-native aquatic species introduced in Spain, 2) to characterise the probability of ecological impacts associated with these species, 3) to evaluate the importance of these species for the Spanish economy in line with species potential for ecological impacts.

Datasets
Open access and independently collected databases were used to characterise the pattern of non-native aquatic species introductions in Spain.I used a combination of datasets on species introductions related to aquaculture and stock-enhancement activities (IMPASSE Database), Spanish aquaculture production (Food and Agriculture Organisation FAO; Here aquaculture production includes fish, crustaceans, shellfish and algae.Species names which could not confidently be linked to a Latin name were eliminated.For the remaining 16 species, family, introduction status and confirmed ecological impact were obtained from scientific peered reviewed publications. In this study, a non-native species was referred to as a single species introduction from outside national boundaries, not from translocations within Spain.No measure of propagule pressure at country level is provided (number/ volume of repeated introductions within the same country) but volumes of production for non-native farmed species are provided.Here I followed the European community definition of ecological impact derived from Gozlan (2008) where only negative impacts on native ecosystems are considered.It is measured through peer reviewed publication of ecological impact defined as a quantifiable impact resulting in habitat degradation, competition with native species for spawning ground, hybridisation threatening species integrity and/or predation on native species populations resulting in their decline.In this way, over at least a 57 year period, it is assumed that an undisputed ecological impact arising from aquatic species introduction would have been picked up in scientific literature.

Human pressure on Spanish aquatic ecosystems
In the last decades, the changes in land use and water demand that have affected Spanish society have resulted in a deep modification of aquatic ecosystems (Table 1).For example, according to a recent report (Anonymous 2006), there are 510,000 illegal wells in Spain accounting for about the average water consumption of 58 million people (i.e 3600 hm 3 ).Such drastic changes over a relatively limited period of time have clear consequences on the structure of aquatic community as well as the associated ecosystem function.In this context, other potential for additional ecological impacts, such as the introduction of non-native species, are difficult to measure (Light and Marchetti 2007).Most non-native aquatic species introduced (n=105) are fish species (36%) followed by algae (16%), crustaceans (14%), parasites of aquatic hosts (14%), gastropods (12%) bivalves (7%) and fungi (1%).Overall, forty two percent of all non-native aquatic introductions are intentional (n=60) with the majority of accidental non-target   (2006) species introductions illustrated by parasites and fungi (24%), gastropods (18%) and bivalves (7%) (Figure 1).In Spain, the trend in non-native aquatic species introduction shows that most introductions are intentional, mainly in support of existing aquatic ecosystem services such as aquaculture and sport fishing (Elvira and Almodovar 2001).This is particularly true for fish and crustacean introductions for which the majority are intentional and for which species are integral parts of the Spanish aquaculture portfolio (See Annex 1, Figure 1).

Ecological impact resulting from non-native species
Overall very little ecological impact resulting from these non-native species introductions has been demonstrated with some representing a benefit to Spanish ecosystem services (Figure 2).For example, the economic benefits to Spanish aquaculture arising from non-native aquatic species (n=9) is close to €46.73 million (about U.S. $69 million) annually for an estimated average ecological risk for all introductions of 16.5% (SD= 26.85).It is now apparent for nonnative species introduced to Spain that the more introductions occur, the greater the chance of associated ecological impacts (n=105, Pearson correlation 0.96, P<0.01).However, our capacity to quantify the true value of individual species likely ecological impact remains limited (Hermoso et al. 2009;Rincón et al. 1990Rincón et al. , 2002)).Out of the 37 fish species introduced to Spain, 31 are freshwater species with the greatest potential for ecological impact attributed to black bullhead Ameiurus melas (Rafinesque, 1820) (42 % of all introductions worldwide, n=21) followed by topmouth gudgeon Pseudorasbora parva (Temminck and Schlegel, 1846) (37% of all introductions worldwide, n=35).
Recently Williamson's rule of ten stating that ten percent of all introductions will become invasive and that ten percent of these invasive species will cause an ecological impact (Williamson 1996) has been reinforced for nonnative freshwater fish introduced worldwide (Gozlan 2008).This gives rise to the most common comment about the vast level of unknown (see Figure 2) and the associated risk of underestimating the true level of ecological impact resulting from non-native aquatic species introductions.This concern raises two key points: 1) there is an urgent effort to be made in the field of biological invasion to characterise the true impact of non-native species introduction (i.e.significant decline of native biodiversity, a loss of genetic integrity or/and a change in ecosystem function; see Gozlan 2008 for a full definition); 2) If after an extensive period of time (to be define by the various stakeholders) there is no obvious ecological impact associated with the introduction of nonnative species then one could argue that either there is no impact or if there is one, then it is very mild and should be assessed in a wider perspective of biodiversity conservation.

Perspectives
Other more serious ecological impacts resulting from other ecosystem services such as sea fisheries, may force European countries to put the risk of non-native introduction from aquaculture into perspective with stock decline of wild populations (Pontecorvo and Schrank 2009).The need to release the pressure on wild stocks may in the future also drive individual countries to rely on an enlarged portfolio of aquaculture with emphasis on herbivore species, at the same time increasing reliance on nonnative species.Rainbow trout Oncorhynchus mykiss (Walbaum, 1792) is a good example of a species which has been introduced worldwide for its farming potential and following an increased consumer demand despite a high risk of ecological impact on native salmonid populations (Bartholomew and Reno 2002;McDowall 2006;Buria et al. 2007;Fausch 2007).Other species such as A. melas, Procambarus clarkii (Girard, 1852) or P. parva have also been introduced via an aquaculture pathway and have been reported to cause ecological impacts on native fauna through disease introduction (Gozlan et al. 2005(Gozlan et al. , 2006(Gozlan et al. , 2010b) ) and/or direct competition (Rodriguez et al. 2005;Musil et al. 2008) but with not associated benefits to any ecosystem services.If policy makers were to put the cost of any ecological impact resulting from a non-native species introduction (Britton and Brazier, 2006) back to the entity responsible for that introduction, in a similar way as is done for chemical pollution, then sport fishing and the aquaculture industry would look closely at the ratio between financial benefit and risk of biological pollution (Gozlan and Newton 2009) (Figure 3).
Finally, the need for further science based evidence of the relationship between non-native species introduction and ecological impact are urgently needed in order to put in place sound and reliable risk assessments (Gozlan et al. 2010a;Copp et al. 2009).
Annex 1. List of non-native aquatic species (or aquatic hosts) introduced to Spain.Data extracted from IMPASSE data base and completed with literature review.* indicates species which were omitted from analysis.Abbreviations are as follow: A= aquaculture/farming/fisheries, S = sport fishing, At = Aquarium trade, B = biological control, N = natural dispersal and H = intentional human introduction.

Figure 1 .
Figure 1.Total number of non-native aquatic species (or aquatic hosts) introduced in Spain until 2010 per given group (black bars) and proportion of intentional introduction (white bars) is given.

Table 1 .
Estimates of illegal anthropogenic pressure on water abstraction in various Spanish River basins.