Amphibian Commerce as a Likely Source of Pathogen Pollution

Abstract

The commercial trade of wildlife occurs on a global scale. In addition to removing animals from their native populations, this trade may lead to the release and subsequent introduction of nonindigenous species and the pathogens they carry. Emerging infectious diseases, such as chytridiomycosis caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), and ranaviral disease have spread with global trade in amphibians and are linked to amphibian declines and die-offs worldwide, which suggests that the commercial trade in amphibians may be a source of pathogen pollution. We screened tiger salamanders involved in the bait trade in the western United States for both ranaviruses and Bd with polymerase chain reaction and used oral reports from bait shops and ranavirus DNA sequences from infected bait salamanders to determine how these animals and their pathogens are moved geographically by commerce. In addition, we conducted 2 surveys of anglers to determine how often tiger salamanders are used as bait and how often they are released into fishing waters by anglers, and organized bait-shop surveys to determine whether tiger salamanders are released back into the wild after being housed in bait shops. Ranaviruses were detected in the tiger salamander bait trade in Arizona, Colorado, and New Mexico, and Bd was detected in Arizona bait shops. Ranaviruses were spread geographically through the bait trade. All tiger salamanders in the bait trade were collected from the wild, and in general they moved east to west and north to south, bringing with them their multiple ranavirus strains. Finally, 26-73% of anglers used tiger salamanders as fishing bait, 26-67% of anglers released tiger salamanders bought as bait into fishing waters, and 4% of bait shops released tiger salamanders back into the wild after they were housed in shops with infected animals. The tiger salamander bait trade in the western United States is a useful model for understanding the consequences of the unregulated anthropogenic movement of amphibians and their pathogens through trade.

Ranavirus Ecology and Evolution: From Epidemiology to Extinction

“…Second, selection during the initial phases of a growing epidemic, when susceptible hosts are not limiting, should favor rapid transmission and virulence (Day and Proulx 2004 ;Bolker et al 2010 ). If new, susceptible animals are continually introduced into a population undergoing an epidemic, as appears to be the case in some bait shops selling tiger salamanders (Picco and Collins 2008 ), this could favor more proliferative, virulent viral strains over those that would be favored when hosts become limiting. Lastly, competition between pathogens within a host can favor increased virulence, even at the cost of reduced transmission (e.g., de Roode et al 2005 ).…”

Recent host-shifts in ranaviruses: signatures of positive selection in the viral genome

“…Direct contact and ingestion of contaminated water are known transmission modes, and infection leads to necrosis of the liver, spleen, skin and haematopoietic tissue (Lesbarrères et al, 2012). The bait, pet and food industries are major factors in the spread of these pathogens geographically to naïve localities and species (Jancovich et al, 2005;Picco & Collins, 2008). Although both pathogens pose a lethal threat to amphibians, ranaviruses tend to cause recurrent population dieoffs that target larval-stage amphibians (Chinchar, 2002).…”

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

“…Well-known examples of non-indigenous species that negatively affect California's native amphibians through competition and predation include bullfrogs (Rana catesbeiana ;Moyle 1973;Kupferberg 1997;Kiesecker and Blaustein 1998;Pearl et al 2004), crayfishes (Gamradt and Kats 1996) and fishes (Hayes and Jennings 1986;Bradford 1989;Gamradt and Kats 1996;Lawler et al 1999;Knapp and Matthews 2000). Additionally, tiger salamanders (Ambystoma tigrinum) have been widely introduced into California and throughout the western United States (Collins et al 1988), leading to hybridization with native populations (Riley et al 2003;Storfer et al 2004) and the widespread potential for the spread of disease (Picco and Collins 2008). 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.…”