Larval exposure to predator cues alters immune function and response to a fungal pathogen in post‐metamorphic wood frogs

Abstract

For the past several decades, amphibian populations have been decreasing around the globe at an unprecedented rate. Batrachochytrium dendrobatidis (Bd), the fungal pathogen that causes chytridiomycosis in amphibians, is contributing to amphibian declines. Natural and anthropogenic environmental factors are hypothesized to contribute to these declines by reducing the immunocompetence of amphibian hosts, making them more susceptible to infection. Antimicrobial peptides (AMPs) produced in the granular glands of a frog's skin are thought to be a key defense against Bd infection. These peptides may be a critical immune defense during metamorphosis because many acquired immune functions are suppressed during this time. To test if stressors alter AMP production and survival of frogs exposed to Bd, we exposed wood frog (Lithobates sylvaticus) tadpoles to the presence or absence of dragonfly predator cues crossed with a single exposure to three nominal concentrations of the insecticide malathion (0, 10, or 100 parts per billion [ppb]). We then exposed a subset of post-metamorphic frogs to the presence or absence of Bd zoospores and measured frog survival. Although predator cues and malathion had no effect on survival or size at metamorphosis, predator cues increased the time to metamorphosis by 1.5 days and caused a trend of a 20% decrease in hydrophobic skin peptides. Despite this decrease in peptides determined shortly after metamorphosis, previous exposure to predator cues increased survival in both Bd-exposed and unexposed frogs several weeks after metamorphosis. These results suggest that exposing tadpoles to predator cues confers fitness benefits later in life.

Interactive effects of competition and predator cues on immune responses of leopard frogs at metamorphosis

“…The negative effect of late exposure to predator cues on mass-standardized skin peptides is consistent with a previous study on the effects of predator cues on mass-standardized skin peptides in wood frogs, which showed a trend of reduced skin peptides in the presence of predators (Groner et al, 2013). While the exposure of wood frogs was not late in their development, this species develops more rapidly than leopard frogs.…”

“…However, inhibition of desorption/ionization was suspected and confirmed when addition of our samples to known standards prevented detection of a signal. This has been previously observed (Groner et al, 2013), suggesting that metamorphic frogs release the inhibiting compound. Ultimately, determination of peptide sequences was done using capillary liquid chromatography (Michrom BioResourses Corporation, Auburn, CA, USA) electrospray ionization (ESI) MS/MS.…”

Toxic and genotoxic effects of the imazethapyr-based herbicide formulation Pivot H® on montevideo tree frog Hypsiboas pulchellus tadpoles (Anura, Hylidae)

“…It is well known that pesticide effects on predator-prey interactions are often complex and have the potential to alter aquatic community composition (Hanlon and Relyea, 2013). It has been claimed that pesticides may have positive, negative, or no impact on the outcome of predator-prey interactions, depending upon the sensitivity of the species to contaminant exposure (Boone and Semlitsch, 2003;Bridges, 1999;Groner et al, 2013;Junges et al, 2010). We observed that sublethal levels of IMZT induced ethological disturbances, i.e., IS and IM, as well as morphological alterations, i.e., decreased frequency of keratodonts, in exposed tadpoles.…”

Evidence for carry-over effects of predator exposure on pathogen transmission potential

“…In the wood frogs (Lithobates sylvaticus), for example, Groner et al [15] showed that larval exposure to predation alters adult immune response to a fungal pathogen. However, to the best of our knowledge, no study to date has examined possible carry-over effects of predation exposure on pathogen transmission.…”