ChapterPDF Available

Herpetological History of the Balearic Islands: When Aliens Conquered These Islands and What to Do Next

Authors:

Abstract and Figures

Balearic herpetofauna represents a paradigmatic case of multiple biological invasions within the Mediterranean Basin, with a much higher number of alien amphibians (i.e. frogs and toads) and reptiles (i.e. lizards, snakes and turtles/tortoises) than native. The paleogeography of the Balearic Islands, located on Western Mediterranean between Spain and Sardinia, is complex, comprehending an ancient split from the continent during the late Miocene and Pleistocene climatic fluctuations connecting and disconnecting islands from one another (but not them to the continent) that eventually re-shaped the archipelago’s biota. The archipelago has been also influenced by humans since the Neolithic, being a cross-road for alien biota between North Africa and Southern Europe, which caused range regressions and extinctions in the native herpetofauna, nowadays restricted to one amphibian and two reptiles. During the last century, tourism development, the pet trade, and cargo transport of ornamental plants have produced a new wave of biological invasions. Recently introduced snakes are of particular concern, since the effect of predation may seriously threaten the remaining native reptiles in the main islands and endemic subspecies in surrounding islets. Balearic people have a negative social perception of such snakes, mainly due to the lack of familiarity with snakes among islanders but also to the herpetophobic attitude of many Mediterranean cultures. Here we review the herpetological invasions in the Balearic Archipelago and their impacts. We further discuss the on-going management actions on alien reptiles in this archipelago, namely the control of invasive snakes in Ibiza involving monitoring, trapping, environmental education and promotion of social participation.
Content may be subject to copyright.
A preview of the PDF is not available
... The Balearic Islands, like many other islands around the world, suffer the especially severe effects of one of the major threats to biodiversity: invasive species (Whittaker and Fernández-Palacios, 2007;Silva-Rocha et al., 2018). Located in the western Mediterranean Sea, these islands have been isolated from the continent for 5.33 millions of years, developing a specific biota which has suffered natural extinction processes during the Plio-Pleistocene, and anthropogenic extinctions from the end of the third millennium BCE, coinciding with human colonization of the islands (Bover, Quintana and Alcover, 2008). ...
... Located in the western Mediterranean Sea, these islands have been isolated from the continent for 5.33 millions of years, developing a specific biota which has suffered natural extinction processes during the Plio-Pleistocene, and anthropogenic extinctions from the end of the third millennium BCE, coinciding with human colonization of the islands (Bover, Quintana and Alcover, 2008). Snakes, particularly, have been historically introduced to the Balearic Islands, except for the two smallest islands of the archipelago, Ibiza and Formentera (the Pitiusic Islands; Silva-Rocha et al., 2018). However, since 2003, the horseshoe whip snake (Hemorrhois hippocrepis) has been introduced to Ibiza by cargo, within the holes of old olive trees coming from southern Iberian Peninsula and used for ornamental gardening (Silva-Rocha et al., 2018). ...
... Snakes, particularly, have been historically introduced to the Balearic Islands, except for the two smallest islands of the archipelago, Ibiza and Formentera (the Pitiusic Islands; Silva-Rocha et al., 2018). However, since 2003, the horseshoe whip snake (Hemorrhois hippocrepis) has been introduced to Ibiza by cargo, within the holes of old olive trees coming from southern Iberian Peninsula and used for ornamental gardening (Silva-Rocha et al., 2018). It has spread to more than half of the island area and is threatening the only endemic terrestrial vertebrate, the Ibiza wall lizard (Podarcis pityusensis; unpubl. ...
Article
The key to fighting a biological invasion may lie in understanding every variable that can explain its success. The Enemy Release Hypothesis (ERH) states that when an invader arrives to a new environment, the absence of its common enemies (predators, parasites and competitors) facilitates the invasion success. The Horseshoe whip snake ( Hemorrhois hippocrepis ) has been recently introduced from the Iberian Peninsula to the island of Ibiza, and it is currently threatening the only endemic vertebrate, the Ibiza wall lizard ( Podarcis pityusensis ). We hypothesized that the snake invasion success is caused by the absence of natural predators, and we checked the ERH by relating the tail breakage rate to predation pressure. The invasive population showed a much lower incidence of tail breakage than the source population, which is in agreement with the almost absence of snake predators among the Ibizan reduced and naïve native vertebrate community. These results confirm the ERH, and support the prolongation of invasive snake trapping campaigns.
... The Western Mediterranean area has been marked by intense human activities for the last three millennia, and human interventions have altered mammalian and herpetological communities in both continental and insular regions (Dobson, 1998;Corti et al., 1999;Silva-Rocha et al., 2018, 2019. In this context, the Mediterranean tree frog (Hyla meridionalis) nicely illustrates exchanges between human civilizations. ...
... The domination of Carthage along the Mediterranean coasts of Iberia and Morocco then intensified exchanges between Africa and Europe in the following centuries. This era could account for the arrival of tree frogs and other herpetofauna in the Balearic Islands (Pinya & Carretero, 2011;Silva-Rocha et al., 2018). Archaeozoological remains suggest the presence of Hylids on Menorca around the 3 rd -2 nd centuries BC (Alcover et al., 1984;Rivera & Arribas, 1993), and mitochondrial analyses indicated a Spanish ancestry (Silva-Rocha, 2012;Mateo, 2015). ...
... Although the Western Mediterranean is a famous hotspot for historical invasions, only a handful of amphibian taxa were involved. Apart from H. meridionalis, we can mention the Italian green toad Bufo viridis balearicus, supposedly introduced to the Balearic Islands during the Bronze Age by the Nuragics from Sardinia for religious purposes (Hemmer et al., 1981;Silva-Rocha et al., 2018). Perez's frog (Pelophylax perezi) was released from Spain to the Balearics for insect control according to Pinya & Carretero (2011). ...
Article
Full-text available
An illustration of the human footprint on biodiversity are the faunal movements that have accompanied commercial and cultural exchanges between civilizations throughout history. In this article, we provide an integrative review of biogeographical and archaeological knowledge to understand these processes for the Mediterranean tree frog (Hyla meridionalis), an African species that has reached several regions of south-western Europe and associated islands. By re-analysing molecular (multilocus mitochondrial and genome-wide markers) and bioclimatic (ecological niche modelling) data, we give a comprehensive picture of the genetic diversity, structure and environmental suitability of H. meridionalis across its natural and exotic ranges, which in turn offer specific clues to the putative routes of colonization and associated events. Long-term monitoring efforts suggest northwards shifts of local range margins, potentially due to global warming, and we further demonstrate that this species is the most frequent amphibian to travel via the food supply chain in Western Europe. High dispersal ability, ecological tolerance and proximity to human settlements have made H. meridionalis a recurrent witness to the complexity and diversity of the civilizations that ruled the Western Mediterranean.
... At the beginning of the 21st century, hundreds of large ornamental olive trees were imported from the southern Iberian Peninsula to the Balearic Islands to cater to a fad for Mediterranean landscaping. These trees brought with them to Ibiza three species of stowaway snakes: Malpolon monspessulanus, which appears to have disappeared; Zamenis scalaris, which maintains a small but stable population on the island; and Hemorrhois hippocrepis, which has rapidly expanded (Álvarez et al. 2010;Silva-Rocha et al. 2018). On Ibiza, H. hippocrepis has a diet mainly (56% in frequency) composed of the endemic Ibiza wall lizard (Podarcis pityusensis; Hinckley et al. 2017). ...
... Hemorrhois hippocrepis is a thermophilic snake that ranges across two-thirds of the Iberian Peninsula and from Morocco to Tunisia in northern Africa. It is present on the islands of Zembra, Pantellaria and Sardinia due to human introduction (Feriche 2017); in addition, it has been recently introduced to the Balearic Islands of Mallorca, Ibiza and Formentera, currently maintaining established populations on Mallorca and Ibiza (Silva-Rocha et al. 2018). It preys almost exclusively on vertebrates, is rupicolous, and anthropic structures on Ibiza form favorable habitats for this snake (Feriche 2017). ...
Article
Full-text available
The invasive snake Hemorrhois hippocrepis colonized the island of Ibiza (Balearic Islands) in 2003 as stowaways inside trunks of olive trees imported for gardening. It has quickly spread since 2010, posing a threat to the island’s only remaining endemic vertebrate, the Ibiza wall lizard Podarcis pityusensis. We map the yearly expansion rate of the snake and estimate via transect surveys how severely it affects the distribution and abundance of the endemic lizard. As well, we surveyed nine of 30 small lizard populations on islets surrounding Ibiza that have been isolated since the Last Glacial Maximum. Snakes had invaded 49% of Ibiza’s land area by 2018, and censuses show a critical contrast in lizard abundance between areas with and without snakes; almost all censuses in areas without snakes show lizard presence whereas nearly all censuses in areas with H. hippocrepis lack lizard sightings. Moreover, at least one subspecies previously thriving on one of the offshore islets has become extinct, and there have been several snakes recorded swimming between Ibiza and the surrounding islets. Therefore, lizard populations have been dramatically reduced or have vanished within the range of the snake, and our results quantitatively support upgrading this species’ threat level for extinction. This study can inform to programs to manage invasive snake populations and to conservation actions to recover the endemic lizard.
... This species has been introduced to some regions such as Argentina, Uruguay and California (USA) and islands as Tenerife, Madeira and Azores (Barreiros et al., 2010;Vogrin et al., 2017). It was introduced to the Balearic Islands (Spain) in ancient times (Mayol, 1985;Pinya and Carretero, 2011) and currently it is widely distributed in the main islands of the archipelago (Salvador and Pérez-Mellado, 1984;Hódar, 2002;Rato, 2015;Salvador, 2016;Silva-Rocha et al., 2018) and the islets (Mayol, 1981). It is a nocturnal predator (Hódar et al., 2006) that frequently inhabits humanized habitats as it uses human constructions as shelters (Martínez-Rica, 1974;Hódar, 2002). ...
Article
Stressful situations induce an increase in the production of reactive oxygen species (ROS) which can lead to molecular damage and alteration of cell function. The introduction of new potential predators induces physiological stress in native fauna. However, behavioral responses have been reported in preys, demonstrating an induction of the defenses against alien species. Behavioral and antioxidant enzyme responses in the moorish gecko, Tarentola mauritanica, against the invasive predator horseshoe whip snake (Hemorrhois hippocrepis) were assessed. Behavior was recorded and a tissue sample from the tail was collected after placing the gecko in a terrarium with previous absence or presence of the snake in ‘Control’ and ‘H. hippocrepis’ groups, respectively. Fifteen behavioral variables were examined, including tongue flick (TF) and locomotion patterns. Antioxidant enzyme activities -catalase (CAT), superoxide dismutase (SOD), glutathione peroxidase (GPx), glutathione reductase (GR)-, and the levels of reduced (GSH) and oxidized glutathione (GSSG), glutathione/glutathione disulfide ratio (GSH/GSSG) and malondialdehyde (MDA) concentrations were measured in the tissue sampled. Geckos exposed to the snake's odor showed a higher number of TF, longer amounts of time remaining motionless or moving in slow motion and they spent less time on the ground in comparison to the ‘Control’ group. The presence of the snake produced a significant increase in the activities of CAT, SOD and GR and a decrease in the GSH/GSSG ratio in T. mauritanica individuals exposed to the snake's scent. Thus, both behavioral responses and oxidative stress biomarkers clearly showed that T. mauritanica is able to recognize H. hippocrepis as a potential predator, despite being a recently introduced snake at the Balearic Islands.
... This species has been introduced to some regions such as Argentina, Uruguay and California (USA) and islands as Tenerife, Madeira and Azores (Barreiros et al., 2010;Vogrin et al., 2017). It was introduced to the Balearic Islands (Spain) in ancient times (Mayol, 1985;Pinya and Carretero, 2011) and currently it is widely distributed in the main islands of the archipelago (Salvador and Pérez-Mellado, 1984;Hódar, 2002;Rato, 2015;Salvador, 2016;Silva-Rocha et al., 2018) and the islets (Mayol, 1981). It is a nocturnal predator (Hódar et al., 2006) that frequently inhabits humanized habitats as it uses human constructions as shelters (Martínez-Rica, 1974;Hódar, 2002). ...
... The Italian wall lizard is native to the Italian Peninsula and Sicily but arrived as a hitchhiker on cargo and through the nursery trade on several Mediterranean islands, with similarities to Cyprus, and subsequently established (Silva-Rocha et al. 2014) with documented impacts through competitive exclusion of and hybridisation with native lizards (Nevo et al. 1972;Capula et al. 2002;Downes and Bauwens 2002 This generalist predator could establish on Cyprus and have major adverse effects on native species (including other snakes, turtles, small mammals and birds) (Roy et al. 2018a). Several studies have shown that introduced snakes can have devastating impacts on native (often endemic) herpetofauna of Mediterranean islands, and so impact upon the natural and cultural heritage of island ecosystems, whose inhabitants often consider native species as iconic (Cabrera-Pérez et al. 2012;Silva-Rocha et al. 2018). ...
... In 2003, the colubrid snake Hemorrhois hippocrepis ( Fig. 1C) was first reported as introduced to Ibiza via imported olive trees, and it rapidly expanded in numbers and range (Silva-Rocha et al. 2018). Although the exact date of introduction is unknown, it is presumed to be soon before 2003. ...
Article
Full-text available
Fifteen years have elapsed since the arrival of the invasive snake Hemorrhois hippocrepis to the island of Ibiza (Balearic Islands, Spain). In that time, the only endemic vertebrate, the Ibiza Wall Lizard (Podarcis pityusensis), has disappeared across half of the island, a subspecies restricted to an offshore islet has vanished, and its extinction in its native range is likely to happen in the next several years if managers do not implement conservation measures with alacrity and decisiveness. In light of these findings, our re-assessment of the IUCN extinction risk category for this lizard shows that its risk status has increased by two levels since its last assessment in 2008, from Near Threatened to Endangered. We also classify this snake as producing a Massive (MA) impact under the Environmental Impact Classification for Alien Taxa. Lastly, we suggest six management measures to prevent the extinction of the majority of genetic and taxonomic diversity of this lizard on Ibiza, Formentera, and the numerous surrounding islets.
... Thus, dispersal followed by fragmentation of the extended geographic range (i.e., peripatric speciation) associated with these tectonic/climatic events are suggested to have shaped the evolutionary patterns of several invertebrates (e.g., Bauz a-Ribot, Jaume, Forn os, Juan, & Pons, 2011;Chueca, Madeira, & G omez-Moliner, 2015;Delicado, Machordom, & Ramos, 2014;Guiller & Madec, 2010;L azaro et al., 2011;Sherpa et al., 2018) and vertebrates (e.g., Carranza & Wade, 2004;Marra, 2005;Mas et Speciation processes (vicariance vs. dispersal) on the Balearic Islands can be best inferred from fossil data. However, so far, fossil records are available only for Balearic vertebrates (Alcover, Moya-Sola, & Pons-Moy a, 1981;Silva-Rocha et al., 2018) and land snails (Cuerda, 1975;Paul & Altaba, 1992). Indirectly, molecular phylogenies can be used to estimate species' origins and divergence times to help unravel their biogeographic history. ...
Article
Until recently, the evolutionary origin of aquatic organisms in the Balearic archipelago (western Mediterranean) had been scarcely addressed. The freshwater gastropod genus Pseudamnicola Paulucci, 1878 (Hydrobiidae), consisting of $60 species in the Mediterranean area, is widely distributed across the major islands of Majorca and Minorca. From phylogenetic datasets of limited geographic coverage, a recent well-supported split has been inferred between the Minorca and Iberian Pseudamnicola species, but the phylogenetic position of the Majorca clade composed of three species remained uncertain. In this study, we extend published sequence data for the COI and 16S rRNA mitochondrial genes and the 28S rRNA nuclear gene in western Mediterranean populations of Pseudamnicola with homologous sequences from individuals of the non-surveyed region of Morocco to assess the origin of the Balearic species from a wider geographic perspective. Our maximum likelihood and Bayesian inference analyses recovered a strongly supported clade comprising the Majorcan species and four phylogenetic lineages in Morocco, two of which are new to science (described here as P. ramosae sp. nov. and P. ouarzazatensis sp. nov.). Dating the nodes using an external molecular clock rate, younger ages were estimated for the Majorcan species ($1 Mya) than for the Moroccan ones ($5 Mya), which were still younger than the formation of the Balearic Islands ($30 Mya). An independent well-supported clade grouped the Minorca and Iberian species diverging at $4 Mya. Thus, we found two independent evolutionary origins within the Balearic archipelago likely attributable to long-distance dispersal events from the African and Eurasian continents. http://zoobank.org:pub:24D17C1D-4A42-4722-9867-D8D84465F55A http://zoobank.org:act:85EC4DF1-9BFA-4B28-B3F2-C091212AFCF1 http://zoobank.org:act:C790EAC6-F22B-489A-93EB-CABF9EEAF282
... Thus, dispersal followed by fragmentation of the extended geographic range (i.e., peripatric speciation) associated with these tectonic/climatic events are suggested to have shaped the evolutionary patterns of several invertebrates (e.g., Bauz a-Ribot, Jaume, Forn os, Juan, & Pons, 2011;Chueca, Madeira, & G omez-Moliner, 2015;Delicado, Machordom, & Ramos, 2014;Guiller & Madec, 2010;L azaro et al., 2011;Sherpa et al., 2018) and vertebrates (e.g., Carranza & Wade, 2004;Marra, 2005;Mas et Speciation processes (vicariance vs. dispersal) on the Balearic Islands can be best inferred from fossil data. However, so far, fossil records are available only for Balearic vertebrates (Alcover, Moya-Sola, & Pons-Moy a, 1981;Silva-Rocha et al., 2018) and land snails (Cuerda, 1975;Paul & Altaba, 1992). Indirectly, molecular phylogenies can be used to estimate species' origins and divergence times to help unravel their biogeographic history. ...
Preprint
Until recently, the evolutionary origin of aquatic organisms in the Balearic archipelago (western Mediterranean) had been scarcely addressed. The freshwater gastropod genus Pseudamnicola Paulucci, 1878 (Hydrobiidae), consisting of ∼60 species in the Mediterranean area, is widely distributed across the major islands of Majorca and Minorca. From phylogenetic datasets of limited geographic coverage, a recent well-supported split has been inferred between the Minorca and Iberian Pseudamnicola species, but the phylogenetic position of the Majorca clade composed of three species remained uncertain. In this study, we extend published sequence data for the COI and 16S rRNA mitochondrial genes and the 28S rRNA nuclear gene in western Mediterranean populations of Pseudamnicola with homologous sequences from individuals of the non-surveyed region of Morocco to assess the origin of the Balearic species from a wider geographic perspective. Our maximum likelihood and Bayesian inference analyses recovered a strongly supported clade comprising the Majorcan species and four phylogenetic lineages in Morocco, two of which are new to science (described here as P. ramosae sp. nov. and P. ouarzazatensis sp. nov.). Dating the nodes using an external molecular clock rate, younger ages were estimated for the Majorcan species (∼1 Mya) than for the Moroccan ones (∼5 Mya), which were still younger than the formation of the Balearic Islands (∼30 Mya). An independent well-supported clade grouped the Minorca and Iberian species diverging at ∼4 Mya. Thus, we found two independent evolutionary origins within the Balearic archipelago likely attributable to long-distance dispersal events from the African and Eurasian continents. http://zoobank.org:pub:24D17C1D-4A42-4722-9867-D8D84465F55A http://zoobank.org:act:85EC4DF1-9BFA-4B28-B3F2-C091212AFCF1 http://zoobank.org:act:C790EAC6-F22B-489A-93EB-CABF9EEAF282
Article
Full-text available
The negative impacts of invasive alien species on native biota are common due to ecological interactions, such as competition, predation, hybridisation, or the introduction of new pathogens. Among them, some snake species are considered to have a dramatic impact on local biodiversity. Here, we focus on a large-sized colubrid species, the Green Whip Snake, Hierophis viridiflavus (Lacépède, 1789) with established populations outside of its natural distribution in western Switzerland as a result of multiple introductions during the second half of the 20th century. The aim of this study was to determine the subspecies and geographical origin of the populations at three locations using molecular methods. The subspecies assessment was based on morphological features and mitochondrial DNA (Cyt-b gene) sequencing. Specimens from the two introduced populations in the area of Onnens and Chamblon (North of the canton of Vaud) could be assigned to the subspecies H. v. viridiflavus, while those from a population near the river La Gryonne (southeast of the canton of Vaud) belong to the subspecies H. v. carbonarius. However, due to the low diversity in the mitochondrial gene (Cyt-b) in both subspecies, it was not possible to assess the geographical origin of the introduced populations. Nevertheless, based on historical faunistic data there is strong evidence the three examined populations were not the result of a natural colonisation process. To propose adequate management actions, future changes in the distribution of the species and its ecological impact on native species at the introduction sites need to be investigated.
Article
Full-text available
Research on the taxonomy of European amphibians and reptiles has increased noticeably over the last few decades, indicating the need for recognition of new species and the cancellation of others. This paper provides a critical review of recent changes and draws up a tentative species list.
Article
Full-text available
Invasive species currently account for a major threat to global biodiversity, and island ecosystems are among the most vulnerable, because of the frequency and success of spe- cies introductions on islands. Within Mediterranean islands, reptiles not only are frequently introduced species but are also among the most threatened because of these introductions. The Balearic archipelago is a good example of this, since only two of its current 16 species of reptiles are native. Thirteen years ago, the snake Hemorrhois hippocrepis was introduced by cargo in Ibiza island, and it is in expansion. Individuals obtain- ed from an early eradication campaign showed a fast expres- sion of phenotypic plasticity and acquired larger sizes than those of the source population, probably due to a high prey availability and predator scarcity. The species is thriving at the expense of a small variety of native and non-native prey, but the predation pressure on the endemic Podarcis pityusensis, the only native reptile in the island, is very high, as this lizard represents 56% of the prey in frequency, which might threaten its survival on the long term. Our results on the feeding ecol- ogy of the snake are of sufficient concern to justify the main- tenance of actions to eradicate this invader.
Article
Investigations carried out in the Aeolian Islands (off north-east Sicily) during 1989–99 gathered evidence strongly indicating that the endemic Aeolian wall lizard Podarcis raffonei is close to extinction. Competitive exclusion by the lizard Podarcis sicula, which has been introduced by man, habitat degradation, and possibly reduced genetic variability and inbreeding, were the main causes for the decline of the species. For the Aeolian wall lizard to recover from its threatened status and to prevent further decimation of populations, collection and trade in the species should be prohibited, and an education programme for local people should be promoted. An integrated project involving habitat protection and captive breeding is needed to secure the species in the wild for the future.
Book
How, when and why did inherited differences of wealth, status and power arise in human communities? At the heart of Emerging Complexity is the thesis that complex societies developed independently during the Copper and Bronze Ages in south-east Spain, and in the wider context of the Iberian peninsula and the west Mediterranean. Chapman rejects the concept of diffusion from the Aegean and east Mediterranean, until recently seen as the cradle of complex society in later prehistoric Europe. The unprecedented amount of new data on south-east Spain since the 1970s unavailable to many prehistorians. This detailed synthesis is therefore valuable as a general introduction to the area, as well as being important for prehistorians concerned with the emergence of complexity in the Aegean and throughout Europe.
Article
Among the different anthropogenic processes that affected the current distribution of the European pond turtle (Emys orbicularis), the timing of the human-mediated translocations is rarely known. Here we present data derived from an archaeological specimen of E. orbicularis obtained at the Roman site of Pollentia (Mallorca, Balearic Islands) using direct radiocarbon dating. These remains correspond to the early Roman period and represent the first reliable evidence for the ancient introduction of this turtle species in a Western Mediterranean Island.