Distribution of alien tetrapods in the Iberian Peninsula

Distribution of alien tetrapods in the Iberian Peninsula Fernando Ascensão1, Marcello D’Amico1, Ricardo C. Martins1, Rui Rebelo2, A. Márcia Barbosa3, Joana Bencatel1, Rafael Barrientos4, Pedro Abellán5, José L. Tella6, Laura Cardador7, José D. Anadón8, Martina Carrete9, Enrique Murgui10, Pedro Fernandes11, Sara M. Santos12, António Mira12, Maria da Luz Mathias13, Patrícia Tiago2, Eduardo Casabella14, Luís Reino1, Octávio S. Paulo2, Henrique M. Pereira15, César Capinha16 1CIBIO/InBio, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Vairão, Portugal 2cE3c – Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal 3CICGE – Universidade do Porto, Porto, Portugal 4Road Ecology Lab, Department of Biodiversity, Ecology and Evolution, Complutense University of Madrid, E-28040, Madrid, Spain 5Departamento de Zoología, Universidad de Sevilla, Seville, Spain 6Department of Conservation Biology, Estación Biológica de Doñana (CSIC), Avda. Américo Vespucio 26, 41092 Sevilla, Spain 7CREAF – Centre de Recerca Ecològica i Aplicacions Forestals. Campus de Bellaterra (UAB) Edifici C, 08193 Cerdanyola del Vallès, Spain 8Department of Agricultural Sciences and the Environment, University of Zaragoza, Zaragoza, Spain 9Department Physical, Chemical and Natural Systems, University Pablo de Olavide, Sevilla, Spain 10Grupo para el estudio de las aves, CV marques del Turia 28, 46010 Valencia, Spain 11Sociedade Portuguesa para o Estudo das Aves, Lisboa, Portugal 12MED – Mediterranean Institute for Agriculture, Environment and Development; University of Évora, Évora, Portugal 13ACESAM (Centro de Estudos do Ambiente e Mar) Faculdade de Ciências da Universidade de Lisboa, Lisboa, Portugal 14Proyecto AVIS – Birdwatching registry system of the Iberian Peninsula Team, Madrid, Spain 15iDIV – German Centre for Integrative Biodiversity Research, Martin Luther University Halle-Wittenberg, Deutscher Platz 5E, 04103 Leipzig, Germany, Leipzig, Germany 16IGOT – Centro de Estudos Geográficos, Instituto de Geografia e Ordenamento do Território, Universidade de Lisboa, Rua Branca Edmée Marques, 1600-276 Lisboa, Portugal Corresponding author: Fernando Ascensão ([email protected]) Academic editor: S. Bertolino|Received 18 June 2020|Accepted 27 November 2020|Published 11 January 2021 Citation: Ascensão F, D’Amico M, Martins RC, Rebelo R, Barbosa AM, Bencatel J, Barrientos R, Abellán P, Tella JL, Cardador L, Anadón JD, Carrete M, Murgui E, Fernandes P, Santos SM, Mira A, da Luz Mathias M, Tiago P, Casabella E, Reino L, Paulo OS, Pereira HM, Capinha C (2021) Distribution of alien tetrapods in the Iberian Peninsula. NeoBiota 64: 1–21. https://doi.org/10.3897/neobiota.64.55597 NeoBiota 64: 1–21 (2021) doi: 10.3897/neobiota.64.55597 https://neobiota.pensoft.net Copyright Fernando Ascensão et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. DATA PAPER Advancing research on alien species and biological invasions A peer-reviewed open-access journal NeoBiota Fernando Ascensão et al. / NeoBiota 64: 1–21 (2021) 2 Abstract We present a dataset that assembles occurrence records of alien tetrapods (amphibians, reptiles, birds and mammals) in the Iberian Peninsula, a coherent biogeographically unit where introductions of alien species have occurred for millennia. These data have important potential applications for ecological research and management, including the assessment of invasion risks, formulation of preventive and management plans, and research at the biological community level on alien species. This dataset summarizes inventories and data sources on the taxonomy and distribution of alien tetrapods in the Iberia Peninsula, comprising known locations from published literature, expert knowledge and citizen science platforms. An expertbased assessment process allowed the identification of unreliable records (misclassification or natural dispersion from native range), and the classification of species according to their status of reproduction in the wild. Distributional data was harmonized into a common area unit, the 10 × 10 km Universal Transverse Mercator (UTM) system (n = 6,152 cells). The year of observation and/or year of publication were also assigned to the records. In total, we assembled 35,940 unique distribution records (UTM × species × Year) for 253 species (6 amphibians, 16 reptiles, 218 birds and 13 mammals), spanning between 1912 and 2020. The species with highest number of distribution records were the Mediterranean painted frog Discoglossus pictus (n = 59 UTM), the pond slider Trachemys scripta (n = 471), the common waxbill Estrilda astrild (n = 1,275) and the house mouse Mus musculus (n = 4,043), for amphibians, reptiles, birds and mammals, respectively. Most alien species recorded are native to Africa (33%), followed by South America (21%), Asia (19%), North America (12%) and Oceania (10%). Thirty-six species are classified by IUCN as threatened in their native range, namely 2 Critically Endangered (CR), 6 Endangered (EN), 8 Vulnerable (VU), and 20 species Near Threatened (NT). Species maps are provided in DataSet1, as well R code and GIS layers to update them as new records are obtained. Keywords Alien terrestrial vertebrates, biological invasions, Iberian Peninsula, invasive species, Portugal, Spain Introduction The human-mediated introduction of species into regions outside their native range is an important component of global change. Alien species (sensu Essl et al. 2018) are responsible for the decline and extinction of native species, economic losses and human health problems (Clavero and García-Berthou 2005; Tatem et al. 2006; Hulme 2009; Simberloff et al. 2013) and are leading to irreversible changes to the diversity and distribution of life on Earth (Simberloff et al. 2013; Capinha et al. 2015). Alien species can impact receiving ecosystems, even if simply through competition with native species for space, food, water or other resources. Although impacts perceived as ‘significant’ are generally recorded for only a subset of alien species, i.e. the ‘alien invasive species’ (sensu IUCN 2000), many ongoing invasions may have simply not yet spread to the point when impacts become noticeable. Furthermore, several invasions may have already been set in motion, leading to impacts in the near future (Essl et al. 2011). Some alien species may be currently in a lag-phase, during which little or no increase in distributional ranges is observed; that may be followed by an increase-phase in which their occurrence and invasiveness rises rapidly (Aikio et al. 2010; Essl et al. 2011; Russell and Blackburn Alien terrestrial vertebrates in the Iberian Peninsula 3 2017). Hence, data on alien species occurrence is crucial and a first step to understand the main drivers shaping their distribution (Abellán et al. 2017; Ascensão et al. 2020) and delineate effective management actions and policies accordingly (Abellán et al. 2017; Hattab et al. 2017; Carboneras et al. 2018; Ascensão et al. 2020). In natural environments, alien tetrapods (amphibians, reptiles, birds and mammals) can compete with, and predate, native species. The American mink (Neovison vison), for example, led to significant population declines of ground nesting birds (e.g. the black-headed gull Chroicocephalus ridibundus or the common tern Sterna hirundo), and small mammals (e.g. the European water vole Arvicola amphibius and the Pyrenean desman Galemys pyrenaicus) in its introduced range (Craik 1997; Aars et al. 2001). Also, the rose-ringed Parakeet (Psittacula krameri), invasive in Iberia, is highly aggressive toward the tree-dwelling greater noctule bat (Nyctalus lasiopterus) when trying to occupy their tree cavities. Rose-ringed parakeet aggressions often result in noctule death, causing population declines and disruption of the complex social behavior of this bat species (Hernández-Brito et al. 2018). Likewise, the pond slider (Trachemys scripta) feeds on several native species of plants and animals, and it potentially competes with native turtles, such as the endangered European pond turtle (Emys orbicularis), for food, basking and nesting sites (Cadi and Joly 2003, 2004; Balzani et al. 2016). On the other hand, the economic impacts of tetrapods can be striking. For example, in Italy the coypu (Myocastor coypus) caused over 11 Mio € in damages during 1995–2000 and similar developments have been suggested for Spain (Panzacchi et al. 2007). Likewise, the monk parakeet (Myiopsitta monachus) or the rose-ringed Parakeet are considered important avian pests (Kumschick and Nentwig 2010; Senar et al. 2016; Reyns et al. 2018). Here, we provide a first compilation of the distribution of the alien tetrapods in Iberian Peninsula. This region integrates the Mediterranean biodiversity hotspot, harboring about half of the European plant and terrestrial vertebrate species (Myers et al. 2000). It is also a region where many alien species are becoming common and spreading, but no cross-taxonomic assessment on distribution patterns has been performed to date, except for birds (Abellán et al. 2016, 2017; Ascensão et al. 2020). The dataset here described contains information on the known occurrences of alien amphibians, reptiles, birds and mammals in this region. We considered all known species with individuals occurring freely in cities and in the countryside (not in captivity), but we discarded domestic species. For each species, we have also included information on current status of establishment in the Iberian Peninsula, classifying each species as ‘established’, ‘not established’, or ‘uncertain’. The applications of these data range from supporting the development of measures for the prevention and management of biological invasions to undertaking speciesand community-level ecological research. Specifically, the assembled data allows more detailed research on the distribution of single alien species and of the spatial patterns of richness and composition of alien species assemblages at the regional scale (Ascensão et al. 2020). These potential applications are of specific relevance for a number of species currently being targeted by national and EU-level legislation. Fernando Ascensão et al. / NeoBiota 64: 1–21 (2021) 4 Metadata Data set descriptors A. Data set identity Registry of alien tetrapods (terrestrial and freshwater vertebrates) in the Iberian Peninsula. B. Data set description This dataset summarizes inventories and data sources on the distribution of alien tetrapods in the Iberian Peninsula, from 1912 onwards, comprising known locations from published literature, expert knowledge and citizen science platforms. An expert-based filtering process allowed the identification of unreliable records (e.g., misclassification or natural dispersion from native range). Distributional data was harmonized into a common area unit, the Universal Transverse Mercator (UTM) system (n = 6,152 10×10 km cells). The dataset consists of one file, containing a 15 × 159,677 matrix of values, including information on species, location, time, current establishment status and source. In total, we assembled 35,940 unique distribution records (UTM × species × Year) for 253 species (6 amphibians, 16 reptiles, 218 birds and 13 mammals) (Fig.1), spanning between 1912 and 2020 (Fig. 2). Fifty-six species (22%) are known to reFigure 1. Richness of alien tetrapods in Iberian Peninsula, by taxonomic Class. Alien terrestrial vertebrates in the Iberian Peninsula 5 produce in the wild (established in Iberia), whereas for 98 species (39%) there is no evidence for being established, and for 99 species (39%) the establishment status is uncertain. The species with the highest number of distribution records were the Mediterranean painted frog Discoglossus pictus (n = 59 UTM), the pond slider Trachemys scripta (n = 471), the common waxbill Estrilda astrild (n = 1,275) and the house mouse Mus musculus (n = 4,043). Most alien species recorded are native to Africa (33%), followed by South America (21%), Asia (19%), North America (12%) and Oceania (10%). Thirty-six species are classified by IUCN as threatened in their native range, namely 2 Critically Endangered (CR), 6 Endangered (EN), 8 Vulnerable (VU), and 20 species Near Threatened (NT). The file is labelled as “Data_AscensãoEtAl_Neobiota.csv”. 1. Principal investigators Fernando Ascensão – CIBIO/InBio, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto. Current address: cE3c – Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências da Universidade de Lisboa. César Capinha – CIBIO/InBio, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto. Current address: IGOT – Centro de Estudos Geográficos, Instituto de Geografia e Ordenamento do Território, Universidade de Lisboa, Rua Branca Edmée Marques, 1600-276 Lisboa, Portugal. Figure 2. Yearly distribution of records on non-native tetrapods in the Iberian Peninsula. Year in x-axis refers to the most accurate timeframe information available and may indicate the time of publication (e.g., Spanish Atlas of Mammals in 2007), or the actual time of observation for the data (e.g., from citizen science platforms). Between 1912 and 1980 there are 138 records (<0.1% of total), not shown. Fernando Ascensão et al. / NeoBiota 64: 1–21 (2021) 6 Research origin descriptors A. Overall project description 1. Identity This dataset assembles and harmonizes all known locations of alien terrestrial and freshwater vertebrates (tetrapods) in the Iberian Peninsula by UTM cell (ca. 10 × 10km). The taxonomy and origin are also provided for each species. 2. Originators The data was collected under the project “The role of transportation in Biological Invasions” funded by Infraestruturas de Portugal Biodiversity Chair (ref02035004). Methodology was developed by Fernando Ascensão and César Capinha. All authors participated in data collection and validation process. 3. Period of study Data was collected from 01/01/2017 to 10/08/2020. Collected data included records from 1912 to 2020. 4. Objectives The primary objective of the present work was to compile a registry of non-native vertebrates (tetrapods) present in the Iberian Peninsula. The applications of these data range from supporting the development of measures for the prevention and management of biological invasions to undertaking speciesand community-level ecological research. Specifically, the assembled data allows more detailed research on the distribution of single alien species and of the spatial patterns of richness and composition of alien species assemblages at the regional scale. These potential applications are of specific relevance for a number of species currently being targeted by national and EU-level legislation. 5. Source of funding Infraestruturas de Portugal Biodiversity Chair (ref02035004) funded the project “The role of transportation in Biological Invasions”. F. Ascensão was also funded by Fundação para a Ciência e Tecnologia – grant SFRH/BPD/115968/2016. Summary of “The role of transportation in Biological Invasions” project The naturalization of non-native species is now one of the main mechanisms responsible for altering the biosphere, causing profound changes in the structure and functioning of ecosystems. Given the increasing mobility of people and goods, concomitant with the increase in road and rail networks, and consequent increase in the number of introductions Alien terrestrial vertebrates in the Iberian Peninsula 7 (intentional or not) of non-native species in new locations, it is expected that these changes will continue worsening sharply in the future. The main objective of this project was to deepen the knowledge about the biogeographic patterns that are emerging as a result of this growing mix of species. Part of the data has been published in Ascensão et al. (2020). B. “Specific” subproject description 1. Site description: a. Site type Data was collected for all of the Iberian Peninsula, namely continental areas of Portugal and Spain, together with Gibraltar (a British Overseas Territory located at the southern tip of the Iberian Peninsula). b. Geography Continental areas of Portugal and Spain, together with Gibraltar (a British Overseas Territory located at the southern tip of the Iberian Peninsula). c. Habitat The region includes terrestrial and freshwater habitats. d. Geology, landform The region includes various geological types, ranging from Ediacaran to the Quaternary. e. Watersheds, hydrology All river systems in the Iberian Peninsula. f. Climate Climatic conditions in the study area range from Mediterranean (most part) to Atlantic (northern region). 2. Experimental or sampling design a. Design characteristics Data was obtained following the framework depicted in Fig. 3, through extensive data source search, from scientific literature to online databases, museum collections and by requesting unpublished data to experts on alien species and from citizen science Fernando Ascensão et al. / NeoBiota 64: 1–21 (2021) 8 platforms. Data was then validated through an expert-based procedure to ensure the accuracy and validity of the occurrence records. b. Data collection period, frequency, etc. Basic data collection period was 01/01/2017 to 10/08/2020. 3. Research methods The first step was to identify all tetrapod species occurring in the Iberian Peninsula. We first listed these species by searching in key publications, including national atlases from Portugal (Matias 2002; Equipa Atlas 2008; Loureiro et al. 2008; Catry et al. 2010; Bencatel et al. 2017) and Spain (Barbadillo et al. 1999; Pleguezuelos et al. 2002; Martí and del Moral 2003), and from the recent assessments dedicated to alien birds in the Iberian Peninsula by Abellán et al. (2016). The listing was updated whenever the indication of additional alien species was found during the occurrence data search. All names were standardized according to the IUCN (www.iucnredlist.org), but we retained the alternative names to perform subsequent data searches. A collection of experts was gathered (all authors of this study) to discuss the cryptogenic status of some species. This resulted in a list of 406 species potentially occurring in the Iberian Peninsula. After debate among the authors, a few species listed as alien in some data sources were not considered because there was substantial uncertainty about their nativity in the region (Table 1). Occurrence data was searched in multiple types of sources, including published literature (atlases, research articles, databases), from citizen science data portals and through requests of unpublished data to institutions and experts. Published literature: The ISI Web of Science (https://apps.webofknowledge.com) was searched using the search term: “TS = ((list of species names including alternative ones Figure 3. Framework of collection of occurrence records of alien tetrapod species in the Iberian Peninsula. Alien terrestrial vertebrates in the Iberian Peninsula 9 separated by “OR”) AND CU = (Portugal OR Spain)) AND DOCUMENT TYPES: (Article OR Book OR Book Chapter OR Data Paper OR Proceedings Paper OR Review)”. The search was then refined by using the filters RESEARCH AREAS: (ZOOLOGY OR ENVIRONMENTAL SCIENCES ECOLOGY) AND WEB OF SCIENCE CATEGORIES: (ZOOLOGY OR ECOLOGY OR BIODIVERSITY CONSERVATION). The timespan was 2002 (inclusive) onward. We restricted the search to 2002 because previous records are expected to be compiled in the Atlases (see below). The searches were last updated on August 10th, 2020. This resulted in a collection of 767 references, of which 199 articles were identified from their abstracts as potentially containing useable location data. Finally, occurrences of alien species were retrieved from 65 publications (Table 2). For Portugal, occurrence data further included information from atlases (Bencatel et al. 2017; Catry et al. 2010; Equipa Atlas 2008; Loureiro et al. 2008; Matias 2002); and for Spain information was also obtained from the online database ‘Inventario Español de Especies Terrestres’ (IEET 2014). This database compiles information from several sources, including atlases and other databases (Table 3). Additional information for Spain was obtained from Barbadillo et al. (1999), Martí and del Moral (2003) and Pleguezuelos et al. (2002). Citizen science: We further collected information from four different citizen science platforms, including ‘Biodiversity4all’ (Biodiversity4All 2020), ‘Proyecto Avis’ (Varela et al. 2014; URL: proyectoavis.com), ‘Colectivo Ornitologico Cigüeña Negra’ (COCN; URL: http://bd.cocn.eu), eBird (eBird 2020; Sullivan et al. 2009), and iNaturalist (iNaturalist 2020). The records from Proyecto Avis, COCN and Biodiversity4all were provided directly by their administrators, P. Tiago and E. Casabella, in August 2020. The records from eBIRD were downloaded from its site (full dataset) in August 2020. iNaturalist, records were downloaded using the R packages ‘rgbif’ (Chamberlain et al. 2016) in R environment (R Core Team 2020) in August 2020. Table 1. Species for which there was debate among the authors about whether or not they should be considered native, and for which it was finally decided not to consider as such. Species Support Edible frog Highly difficult to distinguish from Rana perezi, requires genetic data. Pelophylax kl. Esculentus Spur-thighed tortoise Unclear origin (Graciá et al. 2013) Testudo graeca False smooth Snake Unclear origin (Loureiro et al. 2008) Macroprotodon cucullatus Egyptian mongoose Unclear origin (Gaubert et al. 2011) Herpestes ichneumon European mink Unclear origin (Clavero 2014; Maran et al. 2016) Mustela lutreola Fernando Ascensão et al. / NeoBiota 64: 1–21 (2021) 16 to FCT/MCTES for the financial support to CESAM (UID/AMB/50017/2019), through national funds. Work supported by National Funds through FCT-Fundação para a Ciência e a Tecnologia in the scope of the project UIDB/50027/2020. 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Santos, António Mira, Maria da Luz Mathias, Patrícia Tiago, Eduardo Casabella, Luís Reino, Octávio S. Paulo, Henrique M. Pereira, César Capinha Data type: table Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/neobiota.64.55597.suppl1 Fernando Ascensão et al. / NeoBiota 64: 1–21 (2021) 20 Supplementary material 2 Maps Authors: Fernando Ascensão, Marcello D’Amico, Ricardo C. Martins, Rui Rebelo, A. Márcia Barbosa, Joana Bencatel, Rafael Barrientos, Pedro Abellán, José L. Tella, Laura Cardador, José D Anadón, Martina Carrete, Enrique Murgui, Pedro Fernandes, Sara M. Santos, António Mira, Maria da Luz Mathias, Patrícia Tiago, Eduardo Casabella, Luís Reino, Octávio S. Paulo, Henrique M. Pereira, César Capinha Data type: Maps Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/neobiota.64.55597.suppl2 Supplementary material 3 GIS Authors: Fernando Ascensão, Marcello D’Amico, Ricardo C. Martins, Rui Rebelo, A. Márcia Barbosa, Joana Bencatel, Rafael Barrientos, Pedro Abellán, José L. Tella, Laura Cardador, José D Anadón, Martina Carrete, Enrique Murgui, Pedro Fernandes, Sara M. Santos, António Mira, Maria da Luz Mathias, Patrícia Tiago, Eduardo Casabella, Luís Reino, Octávio S. Paulo, Henrique M. Pereira, César Capinha Data type: GIS data Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/neobiota.64.55597.suppl3 Alien terrestrial vertebrates in the Iberian Peninsula 21 Supplementary material 4 R code Authors: Fernando Ascensão, Marcello D’Amico, Ricardo C. Martins, Rui Rebelo, A. Márcia Barbosa, Joana Bencatel, Rafael Barrientos, Pedro Abellán, José L. Tella, Laura Cardador, José D Anadón, Martina Carrete, Enrique Murgui, Pedro Fernandes, Sara M. Santos, António Mira, Maria da Luz Mathias, Patrícia Tiago, Eduardo Casabella, Luís Reino, Octávio S. Paulo, Henrique M. Pereira, César Capinha Data type: R code Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/neobiota.64.55597.suppl4