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Patterns of Spatial Overlap Between Non-Indigenous and Critically Endangered Freshwater Fishes from a Mediterranean Biodiversity Hotspot †

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Patterns of Spatial Overlap Between Non-Indigenous and Critically Endangered Freshwater Fishes from a Mediterranean Biodiversity Hotspot † diversity Article Patterns of Spatial Overlap between Non-Indigenous and Critically Endangered Freshwater Fishes from a Mediterranean Biodiversity Hotspot † Nicholas Koutsikos 1,2,*, Leonidas Vardakas 1,3, Olga-Ioanna Kalantzi 2 and Stamatis Zogaris 1 1 Hellenic Centre for Marine Research, Institute of Marine Biological Resources and Inland Waters, Anavissos, 19013 Attica, Greece; [email protected] (L.V.); [email protected] (S.Z.) 2 Department of Environment, University of the Aegean, 81100 Mytilene, Greece; [email protected] 3 Department of Forestry and Management of the Environment and Natural Resources, Democritus University of Thrace, 193 Pantazidou St., 68200 Orestiada, Greece * Correspondence: [email protected]; Tel.: +30-22910-76393 † Parts of this article have been presented at the 1st International Electronic Conference on Biological Diversity, Ecology and Evolution, 15–31 March 2021, as “Overlapping Areas of Non-Indigenous and Critically Endangered Freshwater Fishes: Setting Conservation Priorities in Greece”. Available online: https://bdee2021.sciforum.net/. Abstract: Non-indigenous fish species (NIFS) can cause severe ecological impacts on the invaded ecosystems and are considered as one of the leading factors of freshwater biodiversity loss. Unravel- ing the spatial overlap between NIFS and critically endangered (CR) fish species can contribute to targeted conservation actions to minimize the potential negative effects. In this study, we applied geostatistical analyses to investigate the spatial overlap of NIFS against fish species that are desig- nated under the CR status according to the IUCN and the Hellenic Zoological Society (HZS) Red Citation: Koutsikos, N.; Vardakas, L.; Lists. Distributional data (presence–absence) from 800 records of 52 NIFS were compiled for both Kalantzi, O.-I.; Zogaris, S. Patterns of lentic and lotic ecosystems of Greece. Our results indicate that freshwater ecosystems under high Spatial Overlap between NIFS richness were located mainly in lowland areas and often near large cities and ecosystems with Non-Indigenous and Critically well-developed commercial and recreational fisheries. On the contrary, low NIFS richness was ob- Endangered Freshwater Fishes from a served in mountainous regions and in relatively small river basins. Overlapping areas of CR species † Mediterranean Biodiversity Hotspot . with moderate to high NIFS richness (1.5–4.3 NIFS per 1 km2) were relatively high (~50%). A quarter Diversity 2021, 13, 233. https:// of the overlapping areas (24.8%) fall within NATURA 2000 network, where legal management bodies doi.org/10.3390/d13060233 could implement specialized programs to minimize the negative impacts. However, the majority of CR fish species’ distribution remains in unprotected areas indicating that protected areas should be Academic Editor: Michael Wink re-designed to include areas containing freshwater species under the highest threatened category. Received: 21 April 2021 Our findings demonstrate that whole assemblages of fishes are rapidly changing as NIFS spread into Accepted: 23 May 2021 Greece and many freshwater ecosystems of outstanding biodiversity conservation value are under Published: 26 May 2021 significant invasion pressure. Publisher’s Note: MDPI stays neutral Keywords: invasive species; alien; translocated; critically endangered; freshwater fishes; freshwater with regard to jurisdictional claims in ecosystems; conservation; biodiversity; red list published maps and institutional affil- iations. 1. Introduction Recent scientific studies have indicated that biodiversity is declining at an extremely Copyright: © 2021 by the authors. rapid rate, suggesting that the sixth mass extinction of species is already under way [1–3]. In- Licensee MDPI, Basel, Switzerland. deed, according to the International Union for the Conservation of Nature (IUCN), more than This article is an open access article 35,500 species (or 28% of all assessed species) are threatened with extinction worldwide, while distributed under the terms and at least 1677 species out of 15,060 assessed are threatened with extinction in Europe. Fresh- conditions of the Creative Commons water fishes are considered among the most threatened species worldwide [4,5]. The most Attribution (CC BY) license (https:// recent IUCN Red List includes 20,109 species belonging to the class of Actinopterygii, 51.8% creativecommons.org/licenses/by/ of which inhabit freshwater ecosystems (10,434 species), where 2234 species (i.e., 22%) of the 4.0/). Diversity 2021, 13, 233. https://doi.org/10.3390/d13060233 https://www.mdpi.com/journal/diversity Diversity 2021, 13, 233 2 of 13 freshwater species are at risk of global extinction as they are under a threatened category (CR: Critically Endangered (576 species; 5.5%), EN: Endangered (857 species; 8.2%), VU: Vulnerable (961 species; 9.2%)). In Europe, freshwater fishes display the third highest percentage of taxa which are at risk; that is, in order of extinction risk: freshwater mollusks (59%), endemic trees (58%), and freshwater fish (40%). Pollution is one of the major threats that significantly affects freshwater fish species in the European region [6]; however, currently it is not considered the leading factor for species extinctions. Other pressures such as over-abstraction, combined with the increasing frequency of drought events due to climate change [7], the disruption of river connectivity due to the construction of multiple barriers [8], and the introduction of invasive alien species severely affect the viability of the native freshwater fish fauna of Europe [9]. Freshwater fish species inhabiting Mediterranean inland water ecosystems are con- siderably more vulnerable compared to the species located in the northern temperate regions of Europe since they are forced to survive under diverse and unstable hydrological regimes [10]. In addition, a large number of the fish species occurring in Mediterranean countries display a range-restricted geographical distribution, as they may occur in a single river or lake [11], thus making them even more vulnerable to additive threats. Greece, located in the eastern Mediterranean region, holds a unique ichthyofaunal diversity within Europe and displays one of the highest levels of fish species endemism in the Mediter- ranean [10,12]. The complex geological processes of the wider area of the Balkans and the eastern Mediterranean has allowed multiple fish species colonizations, long-term survival of ancient taxa in aquatic refugia, and enhanced speciation due to long-term biogeograph- ical barriers that enhance hydrographic isolation among very different biogeographic areas [12,13]. These factors are mainly responsible for the increased diversity and high degree of endemicity in Greece’s freshwater fish fauna. As elsewhere in the Mediterranean basin, anthropogenic alterations such as habitat degradation and fragmentation are the main threats for freshwater fishes in Greece [13]. These anthropogenic stresses are also augmented by the introduction of alien and intra- country translocated fishes (i.e., species transferred out of their natural distributional range but within the country limits) [14]. Non-indigenous species can have severe ecological impacts on the recipient ecosystems they invade. Due to the possible absence of natural predators they are able to increase in numbers and disperse to new areas. In addition, they can hybridize with related native species, spread diseases, compete and displace native species, and alter the structure and function of ecosystems, even leading to local extinctions of native species [15,16]. The aim of this study was to identify the potential overlapping areas of non-indigenous fish species (hereafter NIFS) against fish species that are designated under critically endangered- CR status according to the IUCN and the Hellenic Zoological Society (HZS) Red Lists. This applied geographical analysis aims to support conservation planning and actions to minimize the potential negative effects that NIFS may pose to freshwater biodiversity. 2. Materials and Methods 2.1. Study Area and Species Pool According to the most recent checklist to date [17], 160 fish species have been recorded in freshwater ecosystems of Greece, where 137 are native. The country presents a substantial proportion of country-specific endemics, 47 in total (or 34% of the native fish fauna). Moreover, a further 10% of the freshwater fish species are “near endemic”; that is, occurring also in shared transboundary freshwater lake basins. By excluding aliens and species of marine origin, the percentage of endemic and near-endemic species rises to 57%. In Greece, 51 fish species are considered threatened at a global scale (i.e., CR, Critically Endangered (20); EN, Endangered (15); and VU, Vulnerable (16)) corresponding to 31.8% of all native inland water fish species in Greece based on the most recent IUCN Red List and distinctions made in Barbieri et al. [17]. Diversity 2021, 13, 233 3 of 13 2.2. Data Acquisition We obtained geographic range data for fish species designated as critically endangered (CR) based on the IUCN Red List integrated with the critically endangered fish species listed by the Hellenic Zoological Society (HZS) Red List (Table1). The distributional range of CR species have been developed during the conservation status assessment of EU species of conservation concern [18]. Furthermore, we included three additional fish species not yet evaluated since they display extremely restricted distributional ranges in Greece. Table 1. Freshwater
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