A cryptic invasion within an invasion and widespread introgression in the European water frog complex: consequences of uncontrolled commercial trade and weak international legislation

Abstract

In Western Europe, many pond owners introduce amphibians for ornamental purposes. Although indigenous amphibians are legally protected in most European countries, retailers are circumventing national and international legislation by selling exotic nonprotected sibling species. We investigated to what extent non-native species of the European water frog complex (genus Pelophylax) have become established in Belgium, using morphological, mitochondrial and nuclear genetic markers. A survey of 87 sampling sites showed the presence of non-native water frogs at 47 locations, mostly Marsh frogs (Pelophylax ridibundus). Surprisingly, at least 19% of all these locations also harboured individuals with mitochondrial haplotypes characteristic of Anatolian water frogs (Pelophylax cf. bedriagae). Nuclear genotyping indicated widespread hybridization and introgression between P. ridibundus and P. cf. bedriagae. In addition, water frogs of Turkish origin obtained through a licensed retailer, also contained P. ridibundus and P. cf. bedriagae, with identical haplotypes to the wild Belgian populations. Although P. ridibundus might have invaded Belgium by natural range expansion from neighbouring countries, our results suggest that its invasion was at least partly enhanced by commercial trade, with origins as far as the Middle East. Also the invasion and rapid spread of Anatolian lineages, masked by their high morphological similarity to P. ridibundus, is likely the result of unregulated commercial trade. We expect that Anatolian frogs will further invade the exotic as well as the native range of P. ridibundus and other Pelophylax species elsewhere in Western and Central Europe, with risks of large-scale hybridization and introgression.

Impact assessment with different scoring tools: How well do alien amphibian assessments match?

“…For example, species only impacting communities through hybridisation (e.g. Pelophylax ridibundus and P. bedriagae in our study; Arano et al 1995, Pagano et al 1997, Holsbeek et al 2008 are less likely to cause such impacts in other areas where these native species are not present than species like A. tigrinum which also affect native communities through predation (Ryan et al 2009). Furthermore, we show that high confidence for an assessed impact score might come from a single, well executed study, while many studies which are poor with respect to defining impact will not result in a higher level of confidence (but see Evans et al 2016).…”

Cryptic invasion drives phenotypic changes in central European threespine stickleback

“…The potential for phenotypic shifts in native populations as a result of a cryptic invasion is rarely assessed (Wandeler et al 2007;Crispo et al 2011; but see Holsbeek et al 2008;Mackie et al 2012), which may also reflect the paucity of historic samples and data available to document such shifts. Comparing historical and contemporary stickleback, I show a phenotypic shift in lateral plate characteristics, a trait which is associated with a major effect gene (Fig.…”

“…The occurrence and impact of such invasions may however be underestimated in cases of cryptic invasions, i.e., when a native species becomes admixed or even genetically replaced by one or multiple distinct genetic lineages of the same species (Saltonstall 2002;Mabuchi et al 2008;Holsbeek et al 2008). Cryptic invasions are commonly unrecognized because the invaders are in many cases mistaken for native species (Saltonstall 2002;Mabuchi et al 2008), yet the invading lineage may differ from their native counterparts in their phenotype (Holsbeek et al 2008;Mackie et al 2012) and/ or physiology (McIvor et al 2001). Such phenotypic changes are however less often reported because relatively few cases exist where historical records are available to document phenotypic changes following a cryptic invasion (Wandeler et al 2007;Crispo et al 2011).…”

The origin of tiger salamander (Ambystoma tigrinum) populations in California, Oregon, and Nevada: introductions or relicts?

“…Hybridization is an often-overlooked consequence of biological invasions because it occurs more rarely and is more difficult to detect than the effects of competition and predation. But the effects of genetic invasions can be great (Allendorf et al 2001), and there are now several examples of the negative effects of hybridization with non-indigenous amphibian taxa (Arntzen and Thorpe 1999;Storfer et al 2004;Holsbeek et al 2008;Ryan et al 2009;Fitzpatrick et al 2010).…”