Pets becoming established in the wild : free – living Vietnamese potbellied pigs in Spain

Pets becoming established in the wild: free–living Vietnamese potbellied pigs in Spain.— Vietnamese potbellied (VPB) pigs (Sus scrofa) are a common pet in North America and Europe, but their recent decrease in popularity has increased their abandonment. Our main aim was to identify potential cases of free–living VPB pigs in Spain through an in–depth Google search. We identified 42 cases of free–living VPB pigs distributed throughout the country. The number of free–living VPB pigs reported increased by year but the species abundance still seems to be low. Signs of VPB pig reproduction and possible hybrids between VPB pigs and wild boar or feral pigs have been also reported. Free–living VPB pigs could erode the gene pool of the Spanish wild boar population and exacerbate the damage (e.g. crop damage or spread of diseases) already caused by wild board. Urgent evaluation and adequate management of wild VPB pig sightings is needed to prevent their establishment in natural habitats.


Introduction
The deliberate or accidental release of pets has frequently resulted in the successful establishment of new wild populations (e.g.Bertolino & Lurz, 2013).Over the last years, Vietnamese potbellied pigs (Sus scrofa; hereafter VPB pigs; fig. 1) have become a popular pet species in many regions of the world (Braun & Casteel, 1993), including Spain (Jarandilla, 2011).However, their popularity has recently declined, leading to their frequent abandonment (Tynes, 1997).Given that this is a very opportunistic species, it could be expected that released or abandoned VPB pigs eventually establish free-living populations.Nevertheless, to our knowledge this has not yet been demonstrated.In this paper our main objective was to report, for the first time, the existence of free-living VPB pigs in Spain.In addition, we aimed to gather complementary information regarding these potential introductions, concerning the year, locality and habitat type in which they were observed (table 1).We also investigated whether pregnant VPB female pigs, piglets and/or hybrids between VPB pigs and wild boar (or feral pigs) were reported, as such sightings could indicate that VPB pigs are successfully establishing wild populations (see an example in Magalhaes & Jacobi, 2013).Finally, we briefly discuss the potential risks associated with the successful establishment of free-living VPB pigs.

Material and methods
We identified cases of free-living VPB pigs by means of a thorough Google search.We searched for terms that stemmed from the following words (in Spanish) in the following combinations: Vietnamese pig or Vietnamese boar, combined with wild boar or hybrid or wild or hunting or stalking or harvested or escaped or abandoned or abandonment (i.e. 9 * 2 = 18 combinations).We identified all the cases in which VPB pigs (or their reported hybrids with wild boar or feral pigs; see below) were unequivocally reported as roaming freely.We stopped the search for a word combination when 100 consecutive results did not identify any additional valid record, i.e., when we retrieved only repeated cases, results that did not exactly relate to free-living VPB pigs (e.g.web pages offering VPB pigs for sale), and/or cases in which it was impossible to unequivocally identify free-living VPB pigs (e.g.unclear observations, inconsistent rumours, etc.).Most valid cases were reported through searches in Internet forums (mainly in hunting websites) and in online newspapers and television channels.In total, more than 1,800 records were checked (18 word combinations and at least 100 records per search).All the searches were conducted between mid-February and mid-March 2013.
When possible, we recorded the year, locality (and province), and number of individuals for each reported case (table 1).We differentiated between cases in urban and rural areas because the former would correspond to momentary VPB pig escapes or abandonments, whereas the latter would be more closely associated with individuals potentially becoming established in the wild.All the records from cities/towns, urban parks, highways close to the city/town, and so on were included in the urban area category, and those from natural environments (scrublands, woodlands, crops interspersed with natural vegetation, etc.) in the rural area category (table 1).We also recorded the presence of pregnant VPB pig females, piglets and/or potential VPB pig hybrids with wild boar or feral pig (table 1), as such sightings could indicate the establishment of viable free-living populations.Reported hybrids were described as individuals showing mixed morphological characteristics between VPB pigs and wild boar or feral pigs (fig.1B).Furthermore, we differentiated between killed, captured or observed individuals, and we recorded the source of information: reported by hunters, reports in the news (online newspapers or televisions), and reports provided by forest rangers, hikers, bikers, and similar (table 1).

Results
We identified 42 cases of free-living VPB pigs (table 1, fig. 2).A very low percentage (< 1%) of the total records obtained through a Google search reported valid cases of free-living VPB pigs.Cases of free-living VPB pigs were relatively well distributed throughout Spain (fig.2).Many occurred close to main cities, especially those identified near the coast (fig.2).Free-living VPB pigs were firstly reported in Spain in 2007, and since then the number of cases has increased considerably.VPB pigs were recorded slightly more frequently in rural than in urban areas (57.15% vs 42.85%, n = 42).The first hybrid between VPB pig and wild board (or feral pig) was reported in 2010, and since then, the proportion of records of potential hybrids has increased substantially (table 1).Hybrids were reported in > 25% of the total cases (table 1).In addition, pregnant females or females taking care of piglets were also sporadically observed, captured or killed (table 1).
Table 1 also shows that: 1) on most occasions, only one individual was observed, captured or killed (70%, n = 34), although some pairs and larger groups were also reported; 2) the number of records of observed, captured and killed individuals was similar; captured and killed animals were better sources for the identification of VBP pigs and hybrids (fig.1); 3) most cases were reported either by hunters or in newspapers; and 4) nearly all the cases recorded in urban areas were reported in newspapers, and all the records provided by hunters came from rural landscapes.

Discussion
In this study we provide the first evidences of freeliving VPB pigs in Spain, and, to the best of our knowledge, elsewhere in Europe, although they are also common pets in other countries.According to our findings, free-living VPB pigs have been reported throughout the country.Although the number of cases identified was not high, it has increased in recent years.Importantly, our results indicate that VPB pigs might have successfully established wild populations because signs of VPB pig reproduction (i.e.pregnant females and females taking care of piglets, and/or hybrids of VPB pigs and wild boar or feral pigs) have been frequently observed in the wild.Reasons for the successful establishment, spread and adaptation of VPB pigs to wild habitats are probably related to their highly adaptive and opportunistic behaviour, the scarcity of natural predators, and the favourable climatic conditions in Spain.
Internet search engines are increasingly used in ecological studies (e.g.Maccallum & Bury, 2013), and in particular to monitor the escapes/releases of non-native pets into the wild (see Kikillus et al., 2012).From this perspective, Google searching could be an appropriate tool to monitor the presence of free-liv-Fig.1. A. A docile Vietnamese potbellied pig captured by a hunter in a wild environment within northern Spain (ID 3 in table 1 and fig.2); B. Four potential hybrids between Vietnamese potbellied pigs and wild boar (on the left of the picture) killed during a hunting day in northern Spain (ID 1 in table 1 and fig.2).The morphological aspect of reported hybrids differs notably to that of young wild boar (on the right of the picture).

Fig. 1. A. Un cerdo vietnamita dócil capturado por un cazador en un entorno natural del norte de España (ID 3 en la tabla 1 y en la fig. 2); B. Cuatro posibles híbridos entre cerdos vietnamitas y jabalíes (a la izquierda de la imagen) cazados en el norte de España (ID 1 en la tabla 1 y en la fig. 2). El aspecto morfológico de los híbridos observados difiere notablemente del de los jabalíes jóvenes (a la derecha de la imagen).
A B   ing VPB pigs in Spain.However, the use of Internet searches in scientific studies presents several limitations that must be taken into account.For example, in our study it was almost impossible to check the reliability of most of the observations of free-living VPB pigs; nevertheless, pictures of killed or captured VPB pigs were frequently shown on the websites returned from our searches.Similarly, identification of hybrids between VPB pigs and wild boar (or feral pigs) was not unequivocal through Google searching, and therefore genetic studies are needed to accurately confirm their presence in the wild.In addition, Google searching excludes communities that use Internet less frequently (Maccallum & Bury, 2013), such as older people, or residents in small villages (Proulx et al., in press).Such communities may be closer to wildlife, as these people frequently work in the field (e.g.farmers and gamekeepers); it could therefore be expected that their knowledge about the presence of free-living VPB pigs would be higher than that of other people.Taking this into consideration, we could have underestimated the number and distribution of wild VPB pigs.In contrast, given that striking news is especially highlighted in websites, the presence of free-living VPB pigs could also have been overestimated in our study.In any case, Internet search engines offer some advantages over conventional field-monitoring programs.For example, they permit cost-effective and rapid assessments to detect the recent introduction of invasive animals (Proulx et al., in press), such as the case addressed in the present manuscript.
The introduction of VPB pigs into the wild is a result of their deliberate or accidental release, and seems to have been favoured by the huge development of the online pet-trade (Magalhaes & Jacobi, 2010).Thus, the number of Spanish websites advertising VPB pigs for sale estimated through a Google search increased from less than 10 in 2006 to more than 1,300 in 2012.As a result, the prize paid for VPB pigs in Spain has decreased drastically, dropping from several hundred euros to as little as 20 euros, a fact that facilitates their abandonment (Lord & Wittum, 1998).According to our results, VPB pigs observed were mostly solitary, suggesting that the number of individuals released per event was low.Nevertheless, as observed with other introduced pets (e.g.Alda et al., 2013), only a few founders may have been sufficient to establish free-living populations of VPB pigs across Spain.Furthermore, free-living VPB pigs were frequently documented in parks and gardens in urban areas, indicating these areas could play a key role in the establishment of free-living populations.This closely resembles the manner in which racoons were introduced (Procyon lotor) in central Spain (García et al., 2012).
As VPB pigs have become established in wild ecosystems in Spain only recently, we can only speculate about the risk they may pose.Given the notable genetic divergence between European and Asian S. scrofa (Fernández et al., 2010), free-living VPB pigs could cause erosion of the gene pool of Spanish wild boar populations.In addition, they could create problems similar to those already caused by the wild boar in large areas of Spain (e.g.negative effects on crops and/or natural vegetation, Herrero et al., 2006;Gómez & Hódar, 2008).
The fact that we found only a few cases of apparently successful establishment of VPB pigs in the wild suggests they are not yet abundant in our setting.However, previous experiences suggest that calls for early management action are required, because by the time released exotic animals are publicly recognised as a problem, it is often too late for effective action, due to logistic, economic, or scale factors (Bertolino & Genovesi, 2003).We therefore recommend the situation should be suitably managed before it runs out of control.An in-depth monitoring plan is needed to determine the current distribution and abundance of free-living VPB pigs in Spain, and to accurately assess the risk they may cause.To prevent further releases of exotic pets in the wild, we urgently need stricter trade regulations in Spain (see for a wider explanation on this topic Bertolino & Lurz, 2013).At the same time, we need to increase public awareness about the risks of free-living pets and the benefits of their prevention and mitigation for native biodiversity.

Table 1 .
Cases of free-living Vietnamese potbellied pigs in Spain identified through an in-depth Google search (see Methods for details): ID.Locality numbers plotted in fig.2; N. Number of pigs observed, captured or killed in each case; A. Area (R. Rural, U. Urban); H. Hybrid; P/N.Pregnant/nursing (* females that were taking care of piglets); T. Type (K.Killed, C. Captured, O. Observed); S. Source (H.Hunters, N. Newspaper, O. Others: O 1 Forest rangers, O 2 Conservationists).