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

Abstract

Recent hypotheses suggest that immunosuppression, resulting from altered environmental conditions, may contribute to the increased incidence of amphibian disease around the world. Antimicrobial peptides (AMPs) in amphibian skin are an important innate immune defense against fungal, viral and bacterial pathogens. Their release is tightly coupled with release of the stress hormone noradrenaline (norepinephrine). During metamorphosis, AMPs may constitute the primary immune response in the skin of some species because acquired immune functions are temporarily suppressed in order to prevent autoimmunity against new adult antigens. Suppression of AMPs during this transitional stage may impact disease rates. We exposed leopard frog tadpoles (Lithobates pipiens) to a factorial combination of competitor and caged-predator environments and measured their development, growth and production of hydrophobic skin peptides after metamorphosis. In the absence of predator cues, or if the exposure to predator cues was late in ontogeny, competition caused more than a 250% increase in mass-standardized hydrophobic skin peptides. Predator cues caused a decrease in mass-standardized hydrophobic skin peptides when the exposure was late in ontogeny under low competition, but otherwise had no effect. Liquid chromatography tandem mass spectrometry of the skin peptides showed that they include six AMPs in the brevinin and temporin families and at least three of these peptides are previously uncharacterized. Both of these peptide families have previously been shown to inhibit harmful microbes including Batrachochytrium dendrobatidis, the fungal pathogen associated with global amphibian declines. Our study shows that amphibians may be able to adjust their skin peptide defenses in response to stressors that are experienced early in ontogeny and that these effects extend through an important life-history transition.

The Frog Skin-Derived Antimicrobial Peptide Esculentin-1a(1-21)NH2 Promotes the Migration of Human HaCaT Keratinocytes in an EGF Receptor-Dependent Manner: A Novel Promoter of Human Skin Wound Healing?

“…In contrast, the estimated concentration of peptides in the skin mucus of resting (non-stressed) frogs is within the concentration range that shows antimicrobial activity in vitro [95], supporting the notion that AMPs produced in amphibian skin provide remarkable chemical weapons against skin pathogens [96]. This may be especially important for newly metamorphosed frogs in which the adaptive immune system is still immature [35,97]. Another advantageous feature of Esc(1-21) compared to classical mammalian AMPs is that, given its short sequence, it may be possible to produce this AMP more economically.…”

Synthetic predator cues impair immune function and make the biological pesticide Bti more lethal for vector mosquitoes

“…, Groner et al. ). In adults, this reduction in PO activity was also present when they had been exposed as larvae only to natural or synthetic kairomones (predation risk cues that did not evoke a faster development), suggesting that besides food re‐allocation toward an accelerated development, also a reduced food acquisition may have contributed to the immunosuppression.…”

“…, Groner et al. ) and may be an important factor negatively affecting prey population dynamics (Preisser and Bolnick ).…”

Life history linked to immune investment in developing amphibians

“…Locomotion ability at metamorphosis lags below that of both tadpoles and adults, leaving metamorphs at greater risk of predation (Wassersug and Sperry, 1977). The type of predation, competition and environmental conditions, in addition to infection status, influence size at metamorphosis (Alford, 1999; Parris and Cornelius, 2004; Vonesh and Warkentin, 2006; Groner et al ., 2014), and size at metamorphosis may influence subsequent survival (Pechenik, 2006; Scott et al ., 2007). The timing of metamorphosis and stress during early ontogeny may have a significant influence on disease risk (Rollins-Smith, 1998; Groner et al ., 2014).…”