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BioInvasions Records (2021) Volume 10, Issue 1: 210–219

CORRECTED PROOF

Rapid Communication Invasion of Montpellier monspessulanus (Hermann, 1809) on : new threat to insular ecosystems in an internationally protected area

Maria Febrer-Serra1, Nil Lassnig1, Esperança Perelló1, Víctor Colomar2, Gabriela Picó2, Aina Aguiló-Zuzama1, Antoni Sureda1,3 and Samuel Pinya1,* 1Interdisciplinary Ecology Group, University of the , Ctra km 7.5, Balearic Islands, 2Department of Health Consortium for the Recovery of Fauna of the Balearic Islands (COFIB), Government of the Balearic Islands, Spain 3Research Group on Community Nutrition and Oxidative Stress (NUCOX), Department of Fundamental Biology, IdisBa and Health Sciences and CIBEROBN (Physiopathology of Obesity and Nutrition CB12/03/30038), University of the Balearic Islands, Ctra Valldemossa km 7.5, Balearic Islands, Spain Author e-mails: [email protected] (MF), [email protected] (NL), [email protected] (EP), [email protected] (VC), [email protected] (GP), [email protected] (AA), [email protected] (AS), [email protected] (SP) *Corresponding author

Citation: Febrer-Serra M, Lassnig N, Perelló E, Colomar V, Picó G, Aguiló- Abstract Zuzama A, Sureda A, Pinya S (2021) Invasion of Montpellier snake Malpolon Over the last decade, three alien snake have been reported in three of the monspessulanus (Hermann, 1809) on main islands of the Balearic Archipelago (Spain): Mallorca, and . Mallorca: new threat to insular ecosystems These introductions are considered a threat to the native biota and are associated in an internationally protected area. with the nursery trade from the . The Montpellier snake Malpolon BioInvasions Records 10(1): 210–219, https://doi.org/10.3391/bir.2021.10.1.22 monspessulanus (Hermann, 1809) was first reported in Mallorca in 2006. Since then, a significant number of observations and captures of this species have been Received: 26 April 2020 reported around the natural park of s’Albufera de Mallorca. Most of these captures Accepted: 7 July 2020 correspond to adult specimens, and the snout-vent length (SVL) values of the entire Published: 15 December 2020 population ranged from 31.5 to 137.0 cm (n = 69). The observed operative sex ratio was Handling editor: Tim Adriaens 1.00:1.56 (males:females) and adult males reached larger sizes than adult females. Thematic editor: Angeliki Martinou In terms of reproductive biology, five adult females presented oviductal eggs. Finally, Copyright: © Febrer-Serra et al. skeletal growth marks in the ectopterygoid bone were analyzed, giving results of This is an open access article distributed under terms age from 1 to 20 years old. The significant number of observations, the great sizes of the Creative Commons Attribution License and ages reached by some individuals and the detection of gravid females could (Attribution 4.0 International - CC BY 4.0). indicate that the population is well established, fully naturalized and threatening OPEN ACCESS. insular ecosystems. This naturalized population is the only insular population of M. monspessulanus located in the western Mediterranean. The proximity of the invasion event to sites of environmental relevance such as those included at Natura 2000 network and Ramsar wetland promotes the idea of assessing the impact of this alien species on native biodiversity. There is an urgent need of carrying out future control actions and implementing biosecurity measures in order to prevent new arrivals of this and other alien species into the Balearic Islands.

Key words: invasive snake species, Balearic Islands, invasion episode, insular ecosystem, Nature 2000 network, RAMSAR wetland

Introduction Alien species are the second cause of extinction of species after the habitat loss or fragmentation (Walker and Steffen 1997). The frequency of these biological invasions and, therefore, the rate of native biodiversity loss have

Febrer-Serra et al. (2021), BioInvasions Records 10(1): 210–219, https://doi.org/10.3391/bir.2021.10.1.22 210 Invasion of on Mallorca

progressively increased throughout the last century, mainly due to the growth of human population and globalization (Reaser et al. 2007; Meyerson and Mooney 2007). Island ecosystems are highly exposed to alien species compared to mainland territories (Reaser et al. 2007). Geographic isolation leads to native species evolving in isolation, in some cases originating endemism which lack the ability to survive against alien species (Mueller-Dombois 1981). The main effects of introduced species that threaten the native biota are mainly predation, competition and the transmission of parasites or pathogens (Sodhi et al. 2009). These processes can finally lead to the extinction of native species populations (Sodhi et al. 2009). The introduction of the brown tree snake Boiga irregularis (Merrem, 1802) to the island of Guam in the tropical western Pacific Ocean is a clear example of the harmful effects that an alien predator produces on an insular ecosystem previously free of (Rodda et al. 1992; Fritts and Rodda 1998). Since the introduction of B. irregularis in Guam in the 1950s, the island has lost many of its native vertebrates, including birds, mammals and (Rodda et al. 1992; Fritts and Rodda 1998). This phenomenon is not uncommon, with several examples of alien snake species which have been introduced to insular ecosystems worldwide (Kraus 2008). Some of the affected islands are located in the : Corsica (), which suffered from two different events of introduction of Natrix maura (Linnaeus, 1758) (Fons et al. 1991); Sardinia (), where Hemorrhois hippocrepis (Linnaeus, 1758) was introduced successfully (Bruno and Hotz 1976); and Malta, where Hemorrhois algirus (Jan, 1863) was introduced by cargo stowaway in the 1910s (Lanfranco 1955). Indotyphlops braminus (Daudin, 1803) introduction in Hawaii (USA) (Slevin 1930) and Izu Islands (Japan) (Ota et al. 1995) and Pantherophis guttatus (Linnaeus, 1766) introduction in Bahamas (Buckner and Franz 1994) and Cayman Islands (Franz et al. 1987) was conducted by nursery trade. In some other cases the pathway of introduction was pet trade, such as Boa constrictor Linnaeus, 1758 introduction in Aruba island (Quick et al. 2005). The Balearic Islands (Spain, Western Mediterranean) constitute an archipelago located in the Western Mediterranean Sea. In the last decade, the number of alien species introduction events has increased due to the merchandise trade in the archipelago, similarly to many other islands around the world (Perrings et al. 2005). Arthropods like the Asian hornet (Vespa velutina Lepeletier, 1836) (Leza et al. 2018) and the blue crab (Callinectes sapidus Rathbun, 1896) (Garcia et al. 2018) or mammals such as the common raccoon (Procyon lotor Linnaeus, 1758) (Pinya et al. 2009) and the coati (Nasua nasua (Linnaeus, 1766)) (Álvarez and Mayol 2007) are examples of species introduced to the Balearic Archipelago in the last 20 years.

Febrer-Serra et al. (2021), BioInvasions Records 10(1): 210–219, https://doi.org/10.3391/bir.2021.10.1.22 211 Invasion of Malpolon monspessulanus on Mallorca

Figure 1. Spatial distribution of M. monspessulanus in Mallorca (Balearic Islands, Spain). Records prior to 2015 are indicated in 1 × 1 km UTM purple squares, 2018 and 2019 records are displayed as circles. The size of the circle indicates the number of records in each location.

Despite the presence of many other alien taxa, reptiles deserve special attention for being an unusual case in the Balearic Islands, with more alien (19) than native (2) species (Pinya and Carretero 2011). Among the alien reptiles, five ophidians have been introduced at different times to the four main islands of the archipelago (Pinya and Carretero 2011; Silva-Rocha et al. 2015). Three of them date back to historical times: Macroprotodon mauritanicus (Guichenot, 1850) and Natrix maura in Mallorca and , and scalaris (Schinz, 1822) in Menorca (Alcover and Mayol 1981). However, two other species, H. hippocrepis and Malpolon monspessulanus (Hermann, 1809), have been reported for the first time in the Balearic Archipelago in the last two decades. Additionally, Z. scalaris was also recently recorded from Mallorca, Ibiza and Formentera (Pinya and Carretero 2011; Silva-Rocha et al. 2015). These introductions seem to be associated with the nursery trade from the Iberian Peninsula, mainly with olive trees (Álvarez et al. 2010). Hemorrhois hippocrepis and Z. scalaris were reported in Mallorca (both in 2004), Ibiza (both in 2003) and Formentera (2006 and 2011, respectively) and M. monspessulanus was only reported in Mallorca (2006) and Ibiza (2003). The first evidence of the arrival of M. monspessulanus to Mallorca was registered in municipality in 2006 (Mateo et al. 2011; Mateo 2015). Since then, only seven isolated observations of M. monspessulanus were reported in Mallorca island until 2015 (Species Protection Service database) in the municipalities of , Muro and (Northern Mallorca). All these remaining observations were recorded on the surroundings of Sant Martí hill (Alcúdia), near the s’Albufera natural park (Mateo et al. 2011; Mateo 2015) (Figure 1). S’Albufera natural park is the

Febrer-Serra et al. (2021), BioInvasions Records 10(1): 210–219, https://doi.org/10.3391/bir.2021.10.1.22 212 Invasion of Malpolon monspessulanus on Mallorca

largest wetland of the Balearic Islands, and it is located in the municipalities of Muro and Sa Pobla. It was declared Natural Park in 1988 and Wetland of International Importance, included in the Ramsar Convention, in 1989 (Riddiford and Serra 1996). This area is included into the European Natura 2000 net with two sites: the special protection area for birds (ES0000038) and the site of community interest (ES5310125). Furthermore, it is considered one of the hotspots of greatest biological diversity in the Balearic Archipelago (Pinya et al. 2008). With such a small number of observations, it was not possible to evidence the establishment of a naturalized population in the studied area. Therefore, the aims of the present study were: (a) to report for the first-time solid evidences of M. monspessulanus naturalization in Mallorca island and (b) to describe the main demographic parameters of the analyzed population.

Materials and methods Capture and processing of specimens Snake specimens were captured within the framework of the Snake Control Campaign carried out by the Consortium for the Recovery of Fauna of the Balearic Islands (COFIB) from the Government of the Balearic Islands. Snakes were captured with live traps designed by the COFIB, with dimensions of 50.0 × 35.5 × 17.0 cm. Traps were baited with a live mouse and they were divided into two rooms separated by a galvanized steel meshed in order to separate captured snakes and the bait. The front side of the trap was also made of a galvanized steel meshed and it had only one entrance for snakes with a one-way flap door which fell closed after the snake entered the trap (see Picó et al. 2019 for details; Figure 2) All traps were checked every nine days on average. Each trap was coded and georeferenced. Once captured, the specimens were euthanized by the veterinary service of COFIB and preserved frozen at −20 °C for further analysis. All specimens were measured its snout-vent length (SVL), sexed and dissected to check the occurrence of eggs in adult females. After the study, all animal remains were incinerated by COFIB in accordance with national regulations on animal by-products non-intended for human consumption (SANDACH).

Age determination The ectopterygoid bone was extracted from the head of 37 individuals captured during 2018, in order to analyze the age by skeletochronology techniques (Castanet 1994). Bones were cleaned with sodium hypochlorite 10% prior to their observation, in order to enhance the contrast between growth layers. Then, bones were observed with a binocular microscope LEICA DM 2500P 40x under transmitted light (Fornasiero et al. 2016).

Febrer-Serra et al. (2021), BioInvasions Records 10(1): 210–219, https://doi.org/10.3391/bir.2021.10.1.22 213 Invasion of Malpolon monspessulanus on Mallorca

Figure 2. Type of live trap designed by the COFIB used in the present work.

Databases, map production and statistical analysis Previous information of records of M. monspessulanus in Mallorca were taken from the Species Protection Service database from the Government of the Balearic Islands. They were included in a single database of records of this species (see Supplementary material Table S1). This database will be linked to Biodibal platform (https://biodibal.uib.cat/ca/#/) which is linked to GBIF. All previous and current records were plotted onto a map using ArcMap 10.5 software. Normality of SVL values was checked through Barlett’s test and differences in SVL between sexes were tested with a Student’s t test using R version 3.5.3 (R Core Team 2019).

Results and discussion A total of 69 individuals of M. monspessulanus (1 individual in 2017, 29 individuals in 2018 and 39 specimens in 2019) were analyzed from the municipalities of Alcúdia and Sa Pobla, in areas very close to s’Albufera de Mallorca natural park (Figure 1). The specimens were mainly captured from May to October 2018 and 2019, matching with the breeding activity period according to Feriche et al. (2008). All but four juvenile females, were classified as adults. The operational sex ratio was 1.00:1.56 (males:females) and SVL values of the entire population ranged from 31.5 to 137.0 cm (n = 69). Average SVL values for males and females from M. monspessulanus native range, the southeast of the Iberian Peninsula, were 934,6 mm (n = 160) and 750,3 mm (n = 80), respectively, according to Feriche et al. (2008). These data were slightly lower than SVL values recorded in the present study (Table 1). In the present work, adult males also reached larger sizes than adult

Febrer-Serra et al. (2021), BioInvasions Records 10(1): 210–219, https://doi.org/10.3391/bir.2021.10.1.22 214 Invasion of Malpolon monspessulanus on Mallorca

Table 1. Sample size (n), mean (x), standard deviation (SD) and range (minimum–maximum) of snout-vent length (SVL, cm) and weight (g) of adult males and females of the population sampled. n x ± SD Range Males 25 107.1 ± 18.7 72.6–137.0 SVL (mm) Females 39 87.9 ± 13.2 53.4–123.3 Total 64 95.4 ± 18.1 53.4–137.0 Males 25 540.2 ± 296.5 132.0–1134.0 Weight (g) Females 39 262.7 ± 148.4 46.0–822.0 Total 64 371.1 ± 255.7 46.0–1134.0

Figure 3. Size-frequency distribution presented as violin plots for adult males and females of the population sampled. Dashed lines indicate mean of SVL of both sexes.

females (Table 1, Figure 3), showing significant differences of SVL (t = −4.80, P = 1.03 × 10-5). This is in line with what is known about the species since it is believed that this sexual dimorphism is due to a greater male longevity (Pleguezuelos and Moreno 1988). Regarding reproductive biology, it should be noted that 39 of the 43 females analyzed had reached sexual maturity. Furthermore, five of the studied females presented oviductal eggs of different size and state of calcification in their oviducts. Three of these females only presented non- calcified oviductal eggs (all captured in June 2018 and 2019), while the remaining two females showed nine and ten calcified oviductal eggs (captured in June 2018 and 2019, respectively). The results obtained match with the study carried out by Feriche et al. (2008) in mainland Spain, where females with oviductal eggs were found in June and early July. Skeletal growth marks were analyzed, giving results of age from 1 to 20 years old. Males had a mean age (± standard deviation, SD) higher than females (males = 14.46 ± 3.84 years, n = 13; females = 11.45 ± 2.57 years old, n = 24), in line with the findings of Pleguezuelos and Moreno (1988). According to López-Calderón et al. (2017), males also reached older ages than females at the southeast of the Iberian Peninsula, reaching 14 years in case of males and eight years in females.

Febrer-Serra et al. (2021), BioInvasions Records 10(1): 210–219, https://doi.org/10.3391/bir.2021.10.1.22 215 Invasion of Malpolon monspessulanus on Mallorca

The proximity of the collected specimens to records prior to 2015 (Figure 1; additional data are given in Table S1), together with their age, suggest that these specimens could be descendants of the founders from the introduction of 2006. However, although this hypothesis is quite plausible, multiple introduction events over time through the harbour could also contribute to population growth. A mix of both hypotheses would be supported by the fact that the vast majority of the individuals captured were large and old snakes, but juvenile individuals were also captured. It could mean that the number of adult individuals increases year by year, suggesting a continuous introduction of adults through nursery trade. The reproduction of the adults would explain the presence of juveniles in the area. Nevertheless, further research including a genetic analysis would be appropriate to confirm the origin of the individuals and to discern between the suggested hypotheses. The closeness of all the observations made until 2019 to the Alcúdia harbor (except the one made in Capdepera in 2006) (Figure 1) could mean that the snakes entered the island through here, since Alcúdia harbor is one of the most relevant commercial harbors of Mallorca. Moreover, the proximity of an olive tree nursery located on Palma-Alcúdia highway, quite near to Alcúdia city, could also explain the presence of the M. monspessulanus population in the sorroudings of Alcúdia and the natural park of s’Albufera. In terms of demographic parameters, the large size of some individuals should be highlighted, as well as the detection of gravid females found in the present study, which appear to be in line with the native range (Pleguezuelos and Moreno 1988; Feriche et al. 2008). The collective evidence presented here demonstrates that the population found around the s’Albufera de Mallorca natural park is fully naturalized and well-established. The proximity of the invaded area to these sites of environmental relevance supports the idea of promoting future control actions such as management and containing of the populations, as well as assessing the impact of this alien species on native biodiversity. M. monspessulanus is known to feed on mainly vertebrates such as reptiles, birds and mammals. It preys upon some geckos such as Tarentola mauritanica Linnaeus, 1758 and some passerines as Luscinia megarhynchos (Brehm, 1831), Chloris chloris Linnaeus, 1758 and Parus major Linnaeus, 1758, among others, all of them inhabiting the Balearic Islands (Díaz-Paniagua 1976; Monrós 1997). Furthermore, the diet of M. monspessulanus is known to be composed of some hunting birds and mammals present in Mallorca, such as Alectoris rufa (Linnaeus, 1758) and Oryctolagus cuniculus (Linnaeus, 1758) (Díaz-Paniagua 1976). So, the wide diet of M. monspessulanus could be a threat for a great number of species of different taxa. Accordingly, it becomes necessary to record the colonization process of the species, since very few studies of this species have been conducted so far in insular ecosystems (Corti et al. 2001). Future research in the invaded area is needed, including genetic analyses, potential routes of introduction and dispersion of the snakes as well as potential impacts of M. monspessulanus on native species.

Febrer-Serra et al. (2021), BioInvasions Records 10(1): 210–219, https://doi.org/10.3391/bir.2021.10.1.22 216 Invasion of Malpolon monspessulanus on Mallorca

As far as we are concerned, any other M. monspessulanus insular population occur in the Mediterranean, since no previous information supported a naturalization evidence of a population until the present study. Therefore, the island of Mallorca could probably be the first case of M. monspessulanus naturalization in the Mediterranean basin. It could be due to the fact that this species had never reached the island before or that some climatic or habitat-related characteristics of the island showed a limited suitability for snakes (Silva-Rocha et al. 2015). Silva-Rocha et al. (2015) aimed that this scenario could change in the near future due to climate change. According to these authors, the Balearic Islands would become more suitable for alien snake populations, especially for M. monspessulanus, so this species could end up occupying almost all the extension of the all the archipelago. However, their predictions for 2020 are currently not occurring, since the presence of M. monspessulanus has only been reported in the studied area of the present work (Figure 1). Except Mallorca, M. monspessulanus insular populations have been only reported in Ibiza island (Balearic Islands, Spain, Western Mediterranean), where only seven individuals were observed between 2003 and 2010 (Mateo and Ayllón 2012; Mateo 2015). No specimen has been reported since 2010, which could indicate the extinction of this species in Ibiza (Montes et al. 2015), contrary to the colubrid H. hippocrepis, which seems to be well-established in the island. All in all, the presence of a naturalized population of M. monspessulanus in Mallorca enhances the need for implementing control and biosecurity measures in order to prevent new arrivals of snakes and to avoid the invasion of the rest of island. For this reason, biosecurity measures should not only be implemented close to the commercial harbor of Alcúdia but also in the rest of the island and the archipelago. By applying these control measures, the main pathways of entry of alien snakes and potential routes for dispersal throughout the island would be blocked. In this context, control actions and management of the population would contribute to avoiding the dispersal of the population throughout Mallorca island and, if possible, to eradicate it.

Acknowledgements

We want to thank the reviewers for the kindly suggestions and contributions to improve the manuscript.

Funding Declaration

This research has been done as part of a M.F.S. thesis at the University of the Balearic Islands under an FPU contract with the Ministry of Science, Innovation and Universities from the Spanish Government (FPU17/03484). AAZ is beneficiary of the Programa SOIB JOVE Qualificats del Sector Públic 2019 at the University of the Balearic Islands. This study has been partially funded by the AAEE002/17 Acció Especial de Recerca de la Direcció General d’Innovació i Recerca del Govern de les Illes Balears and by the Institute of Health Carlos III (CIBEROBN CB12/03/30038). This work has also been partially financed by the Biodibal project within the framework of the Collaboration Agreement between the University of the Balearic Islands and Red Eléctrica de España.

Febrer-Serra et al. (2021), BioInvasions Records 10(1): 210–219, https://doi.org/10.3391/bir.2021.10.1.22 217 Invasion of Malpolon monspessulanus on Mallorca

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Supplementary material The following supplementary material is available for this article: Table S1. Records of specimens of M. monspessulanus captured during the period 2006–2019 at the island of Mallorca. This material is available as part of online article from: http://www.reabic.net/journals/bir/2021/Supplements/BIR_2021_Febrer-Serra_etal_SupplementaryMaterial.xlsx

Febrer-Serra et al. (2021), BioInvasions Records 10(1): 210–219, https://doi.org/10.3391/bir.2021.10.1.22 219