Introduction
Human action influence natural environments in many ways, often with unintended consequences. One of the most significant phenomena that substantially increased with globalization is the invasion of alien species. Together with habitat loss, it is the main reason for native species’ populations decrease and extinction (Lowe et al., 2000; Scheele et al., 2019). Invasive species control efforts are expensive and commonly ineffective (Ficetola & Scali, 2010; Hulme, 2006), resulting in the necessity to understand invasion pathways to avoid the colonization of new species or the release of new propagules that might increase genetic variability and fitness of already established populations (Kolbe et al., 2004).
Alien species are sometimes intentionally spread for economic reasons, such as agriculture, biological control, and pet trade (Chiaverano et al., 2014; Ng & Lim, 2010). In these cases, human history can be a useful tool to help identifying and explaining translocation events. It is also common to find information in the lay literature that can help elucidate the origin and pathways of introduction. However, gathering and interpreting information from such literature around the globe can be difficult due to access limitations, language differences, contradicting and misleading information. In this case, population genetics can be a useful tool for reconstructing and understanding the history behind the events of invasions (Ficetola et al., 2008; Bai et al., 2012; Kamath et al., 2016).
The world’s most widespread invasive amphibian species is the North American bullfrog (hereafter bullfrog for short), Lithobates catesbeianus , which is native from eastern North America but currently can be found in many countries in the Americas, Europe, and Asia, where the species was introduced for frog farming and subsequently became established (Kraus, 2009). Despite recognized impacts on native populations (Both & Grant, 2012; Schloegel et al., 2010; Li et al., 2011; Borzée et al., 2017; O’Hanlon et al., 2018), there is a small number of eradication attempts (Adams & Pearl, 2007; Snow & Witmer, 2010, Groffen et al., 2019), possibly as a reflection of the high cost and low rate of success of these attempts (Adams & Pearl, 2007). The lack of information on history and paths of invasion, connectivity and dispersal among populations and their genetic structure, is one of the main reasons why management strategies tend to fail (Rollins et al., 2009).
The first country in the world to be colonized by the American bullfrog was Japan. The first importation consisted of only a few breeding pairs from New Orleans, under the initiative of the biologist Shozaburo Watase in 1918 (Maeda & Matsui, 1999; Yanai, 2003; Hirai, 2004). New events occurred in the 1920s (Minowa et al., 2008), 1952 (Goris, 1967; Ota, 2002; Kraus, 2009), 1953, 1954 and late 1950s (Ota, 1983; Kraus, 2009) from undocumented sources.
Japan exported bullfrogs to Taiwan in 1924 and 1951 (Kraus, 2009; Santos-Barrera et al., 2009). During the same period, Japan also exported bullfrogs to Korea, first in 1959 when all individuals died, and once again in the 1970’s when farming took hold, allegedly supplemented by bullfrogs originating from the USA (Groffen et al., 2019). Until recently, Taiwan province was one of the greatest bullfrog producers and exporters of the world, being the source of many introductions in Southeast Asia. Some of these introductions happened in Singapore (from the 1980s to present) (Ng & Lim, 2010); Indonesia (1984, Indo Prima Bullfrogs’ owner, personal communication); and Malaysia (Hardouin, 1997), which was one of the sources for the Cambodian population (Neang, 2010).
China reconnected with Japan in the late 1950s, after getting isolated by the split with the USSR due to political disagreements. China received bullfrogs from Japan, but these animals died without producing offspring (Li & Xie, 2002; Bai et al., 2012; Liu & Li, 2009; Xuan et al., 2010). Political links at that period resulted in Cuba exporting bullfrogs to China during this period (Li & Xie, 2002; Bai et al., 2012; Liu & Li, 2009; Xuan et al., 2010).
Cuba was one of the first countries to receive bullfrog specimens. The first known introduction happened in 1915-1916 (Kraus, 2009; Santos-barrera et al., 2009), with other two events of introduction in 1927 and 1946. All animals were exported from the USA (Borroto-Páez et al., 2015) and adapted well to the island.
In South America, bullfrogs have been introduced into 10 countries (Akmentins & Cardozo, 2009; Kraus, 2009; Urbina-Cardona & Nori, 2011), although no evidence of persistent populations exists in Chile and Paraguay (F. Bauer, personal communication). Brazil was the first country to be invaded, with two legal importations reported. The first happened in 1935, while Brazil was facing a turbulent political period known as the “1930s revolution”. There was a pressure from some segments of society for the diversification of the economy (Fonseca, 2012). The government started a breeding program with 300 couples introduced by a Canadian technician named Tom Cyrril Harrison (Ferreira et al., 2002). Apart from speculation about the Canadian origin of these animals, Rueda-Almonacid (1999) reported the United States as the native source population, although he did not state the basis for that assertion. As noted by other authors ((Measey et al., 2017), the study by Rueda-Almonacid (1999) contains mistakes; thus, we prefer to disregard it
The second importation to Brazil happened in mid-1980s (Kraus, 2009) with 20 pairs from Michigan (Schloegel et al. 2010). This population is widespread in the country, especially in the state of Minas Gerais (Jorgewich-Cohen et al., in press). Later, all other South American countries received founders exclusively from Brazil (G. Laufer, ump. data; Gallardo, 2004; Kraus, 2009; Pereyra et al., 2006) during the 1980s and 1990s, as part of a general effort to improve the economy after the “lost decade” of the 1980s (Ghirardi et al., 2011; Laufer et al., 2008).
Using population genetics data from within the native range (Austin et al., 2004), some efforts were made to determine the source of alien populations and the genetic structure in Europe (Ficetola et al., 2008), western USA (Funk et al., 2011; Kamath et al., 2016), China (Bai et al., 2012), and Brazil (Prim et al., 2003; Jorgewich-Cohen et al., in press), but none of these studies aimed to reconstruct global pathways of introduction. In order to reveal the paths of invasion of the main bullfrog alien populations around the globe, combining our findings with information from previous works and historical data, we focused on the following questions: How many different lineages are there among alien clusters around the world? Through what paths did these lineages get to different countries? What is the native source of these introduced populations?