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Science of the Total Environment 703 (2020) 134505 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Alien animal introductions in Iberian inland waters: An update and analysis ⇑ Rafael Muñoz-Mas , Emili García-Berthou GRECO, Institute of Aquatic Ecology, University of Girona, 17003 Girona, Spain graphical abstract article info abstract Article history: Inland waters provide innumerable ecosystem services and for this reason are among the most negatively Received 31 July 2019 impacted ecosystems worldwide. This is also the case with invasive alien species, which have enormous Received in revised form 15 September economic and ecological impacts in freshwater ecosystems. The pace of alien introductions has not 2019 decreased in recent years and the first step to their management is to update checklists and to determine Accepted 15 September 2019 introduction pathways and origins of species. This study updates the list of alien animal species intro- Available online 31 October 2019 duced and naturalised in inland waters of the Iberian Peninsula. Additionally, the most relevant charac- Editor: Dr. Damia Barcelo teristics and association patterns of these species (region of origin, taxonomic group, introduction pathway and main habitat) and introduction trends in the Iberian Peninsula, mainland Portugal and Keywords: Galicia are analysed. We identified 125 alien animal species introduced in Iberian inland waters (increase Freshwater ecosystems of 30% compared to previous reviews) whereas 24 additional species have uncertain establishment or Habitat native status. We found marked associations among taxonomic groups and their region of origin, intro- Iberian Peninsula duction pathway and main habitat used but less relationship between these three latter features. Introduction pathway Considering the whole territory of the Iberian Peninsula, the introduction rates seem to be experiencing Invasive alien species a decrease or to have achieved stabilization. However, this is not applicable to mainland Portugal and Species origin Galicia for which the historical delay in the first record dates for alien species is fading-out, suggesting increasing spread rates. Our results should facilitate early detections and the design of prevention protocols and taxon-specific management plans. Ó 2019 Elsevier B.V. All rights reserved. 1. Introduction ⇑ Corresponding author. Inland waters provide fundamental ecosystem services, which E-mail address: [email protected] (R. Muñoz-Mas). has prompted an increasing number of environmental pressures https://doi.org/10.1016/j.scitotenv.2019.134505 0048-9697/Ó 2019 Elsevier B.V. All rights reserved. 2 R. Muñoz-Mas, E. García-Berthou / Science of the Total Environment 703 (2020) 134505 (Borgwardt et al., 2019; Culhane et al., 2019). Thus, they are cur- the impact of real changes in commodity trade routes should not rently among the most impacted biomes in the world (Gozlan be neglected (Seebens, 2019). et al., 2019). Despite worldwide efforts for environmental protec- Another relevant characteristic of invasive alien species is its tion (Cazzolla Gatti, 2016), these threats are rather expected to diversity, in terms of taxonomy and biological traits, which allow increase in line with the requirements related to the foreseen them to thrive in a number of different ecosystems and regions expansion of agriculture and urban areas (Jordà-Capdevila et al., (McKnight et al., 2017). The Iberian Peninsula is very heteroge- 2019). A consequence of human activities in inland water ecosys- neous in terms of climate, geology and ecology (Benito-Calvo tems is the introduction and thriving of alien species (Westphal et al., 2009). Thus, this heterogeneity has favoured a great freshwa- et al., 2008). Alien species are those whose presence in a region ter biodiversity and the existence of isolated regions (e.g. Galicia, is attributable to human actions that enabled them to overcome Spain) with a set of particular geographic and climatologic charac- fundamental biogeographical barriers (i.e. human-mediated teristics that formerly permitted them to avoid or delay most of the extra-range dispersal) (Richardson et al., 2010). Moreover, based introductions occurred in other regions of the Peninsula (Cobo on the observed trends on international trading, the pace of intro- et al., 2010). However, the introduction and establishment of alien ductions may be accelerated in the near future as it is an acknowl- species typically occurs from neighbouring catchments (Marr et al., edged pathway that facilitates their spread (Seebens, 2019). 2010) and it is, in addition, favoured by enhanced communication Depending on their status within the naturalization-invasion networks (Dawson et al., 2017) and river basin developments (e.g. continuum (sensu Richardson et al., 2000), alien species may be river regulation by dams) (Cobo et al., 2010). Therefore, although objectively classified as casual/introduced, naturalized/established some parts of the territory have been considered the gateway of or invasive. Invasive species correspond to the last stage when spe- species introductions (Clavero and García-Berthou, 2006) and cies sustain self-replacing populations over several life cycles, pro- other redoubts for native species (Cobo et al., 2010), it can be duce reproductive offspring (often in very large numbers at hypothesised that the existent avoidance or delay of few regions considerable distances from the parent and/or site of introduction) towards species introductions may have currently faded-out. In and have the potential to spread over long distances. Alternatively, addition, the heterogeneity of the Iberian Peninsula has, regret- invasive species can be defined as these species that additionally tably, facilitated the naturalisation of a large number of alien spe- harm the recipient ecosystem (Blackburn et al., 2014). Although cies, with representatives occupying almost every different habitat the former definition, followed in this study, does not imply any within the Iberian inland waters (García-Berthou et al., 2007). negative impact in the recipient ecosystem it is, nevertheless, In accordance with the importance of this base knowledge, broadly recognised that alien species often have a number of ongoing changes and urgent management, three publications have adverse economic and ecologic impacts, such as predation, hybridi- revised the checklist of alien naturalised animals in the fresh sation, vectoring diseases, food web alteration and interspecific waters of the whole Iberian Peninsula and two Iberian sub- competition (Blackburn et al., 2014; Almeida et al., 2013; regions: Galicia (Spain) and Portugal. In particular, the entire Ibe- Perrings et al., 2000), which makes necessary to undertake actions rian Peninsula was considered in García-Berthou et al. (2007) addressed to maintain them under governance (McGeoch et al., whereas Cobo et al. (2010) reviewed the list of species introduced 2010). to Galicia and Anastácio et al. (2019) that to Portugal. However, as Although pest control and/or eradication has proven to be fea- with the rest of the world (Thomaz et al., 2015), the deliberated or sible in several cases (Rytwinski et al., 2018; Hussner et al., unintended introduction of new species is the main cause of the 2017; Kiernan et al., 2012), once an invasive species is established, increasing trend in the number of alien species found in the Iberian coexisting with the invasive species is, unfortunately, the most Peninsula (Anastácio et al., 2019) but it is not the sole cause. Cur- habitual outcome (Muñoz-Mas et al., 2019; Strayer, 2010). There- rently, genetic tools and increased taxonomic understanding often fore, updating checklists of species that have been already estab- reveal the existence of unnoticed long-lasting introductions lished in a given territory, as well as other information such as (Ribeiro et al., 2015; Aguilar-Alberola and Mesquita-Joanes, 2011) year of introduction and region of origin, taxonomic group or intro- and sometimes questions the introduced status of a few species duction pathway, is fundamental to design proficient prevention (Clavero et al., 2016; Martín-Torrijos et al., 2016). Therefore, updat- protocols, to adjust current legislation or to promote unequivocal ing checklists of alien species and analysing regions of origin, intro- prompt detections. duction pathways and main habitats are crucial for evaluating Within the Mediterranean basin, the Iberian Peninsula is a conservation statuses and improving environmental management. paradigmatic example of the impact that ecosystem degradation The main objective of the study was to update previous studies and the presence of alien species have on native organisms (e.g. on the topic by systematically listing the alien animal species Olaya-Marín et al., 2016). Owing to the isolation provided by the already naturalised (sensu Richardson et al., 2000) in the inland Pyrenean mountain range, the Iberian inland waters currently har- waters of the Iberian Peninsula while those that do not form self- bour a large proportion of endemic species, with half the freshwa- replacing populations (i.e. casual/introduced sensu Richardson ter fishes, amphibians and reptiles assessed as threatened of et al., 2000) are listed apart as uncertain (Objective 1). The second extinction (Hermoso et al., 2016). In this region, the introduction list also includes dubious introductions (i.e. cryptogenic

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