Interactions of environmental stressors impact survival and development of parasitized larval amphibians

Abstract

Infected hosts are exposed to many environmental stressors that must be taken into account in order to determine the importance of disease, as various combinations can interact in unpredictable ways. Here, northern leopard frog (Rana pipiens) tadpoles, a species in decline, were exposed to stressors singly or in combination. Stressors included infection by Echinostoma trivolvis (a trematode parasite), exposure to predator chemical cues (larval dragonflies), and exposure to varying concentrations of the herbicide atrazine. Parasitism decreased survival only in combination with exposure to 3 microg/L atrazine, with a negative interaction observed for mass as well. Similarly, a negative interaction of parasitism and predation on survival occurred. However, atrazine exposure alone negatively affected the survival, mass, and developmental stage of tadpoles. These results indicate that certain stressor combinations are particularly deleterious for young parasitized tadpoles. Notably, very common low-intensity parasite infection can be particularly harmful in certain situations. Such negative impacts on larval amphibians in certain scenarios may contribute to ongoing amphibian population declines, emphasizing that the combination of environmental stressors must be considered when evaluating the general role of disease in species extinctions.

Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality

“…However, this study is unique because it demonstrates that early-life exposure to atrazine can have enduring negative effects on tolerance to infections. Similar to our findings, short-term atrazine exposure reduced tadpole tolerance to trematode infections [26], but in other studies, atrazine altered resistance to infections [21,25]. Effects of early-life exposure to stressors are complex [50], and we suspect that the effects of atrazine on these two defence strategies are context-dependent.…”

“…In addition, the 6-day exposure to atrazine was associated with reduced amphibian size that was only apparent later in life (see [30] for similar effect), an effect that can reduce fitness by diminishing reproductive output [49]. These findings are consistent with several studies demonstrating that atrazine can affect physiology, behaviour, growth, immunity and survival of mammals, fish and amphibians [21][22][23][24][25][26][27][28][29][30], and with a recent study demonstrating that atrazine exposure causes negative effects on genes involved in early immunity [48]. However, this study is unique because it demonstrates that early-life exposure to atrazine can have enduring negative effects on tolerance to infections.…”

“…Thus, we also hypothesized that, even when controlling for size and developmental stage, atrazine exposure would have immediate and persistent effects on Bd-induced mortality mediated by changes to host physiology. Finally, atrazine has been shown to affect amphibian resistance and tolerance to macroparasites [21,25,26,33], and thus we hypothesized that it would affect both resistance and tolerance to Bd.…”

Helminth Parasites of the Wood Frog, Lithobates sylvaticus, in Prairie Pothole Wetlands of the Northern Great Plains

“…However, several laboratory experiments have found that echinostome infection can impair renal function, increase mortality, or decrease growth, at least in tadpoles (Martin and Conn 1990;Fried et al 1997;Holland et al 2007) and under some environmental conditions (Belden 2006;Holland 2010;Koprivnikar 2010). Echinoparyphium rubrum dominated the helminth community of wood frog metamorphs in our study, accounting for 90.8% of all worms in those frogs.…”

“…Most of what we know about amphibianhelminth interactions comes from a small but growing number of experimental studies involving a few parasite taxa and primarily larval amphibians (Szuroczki and Richardson 2009), although a few studies focused on recently metamorphosed amphibians (e.g., Goater 1994). These studies have demonstrated some effects of parasitic infection on some aspects of host fitness, with impacts often dependent on interactions with other environmental factors such as larval density and aspects of water quality (Goater 1994;Kiesecker and Skelly 2001;Belden 2006;Johnson et al 2007;Rohr et al 2008a;Holland 2010;Koprivnikar 2010). There is thus reason to think that parasites might play a role in amphibian population dynamics, at least under some conditions.…”