Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs

Abstract

Many species of amphibians in the wet tropics of Australia have experienced population declines linked with the emergence of a skin-invasive chytrid fungus, Batrachochytrium dendrobatidis. An innate defense, antimicrobial peptides produced by granular glands in the skin, may protect some species from disease. Here we present evidence that supports this hypothesis. We tested ten synthesized peptides produced by Australian species, and natural peptide mixtures from five Queensland rainforest species. Natural mixtures and most peptides tested in isolation inhibited growth of B. dendrobatidis in vitro. The three most active peptides (caerin 1.9, maculatin 1.1, and caerin 1.1) were found in the secretions of non-declining species (Litoria chloris, L. caerulea, and L. genimaculata). Although the possession of a potent isolated antimicrobial peptide does not guarantee protection from infection, non-declining species (L. lesueuri and L. genimaculata) inhabiting the rainforest of Queensland possess mixtures of peptides that may be more protective than those of the species occurring in the same habitat that have recently experienced population declines associated with chytridiomycosis (L. nannotis, L. rheocola, and Nyctimystes dayi). This study demonstrates that in vitro effectiveness of skin peptides correlates with the degree of decline in the face of an emerging pathogen. Further research is needed to assess whether this non-specific immune defense may be useful in predicting disease susceptibility in other species.

Predicted Disease Susceptibility in a Panamanian Amphibian Assemblage Based on Skin Peptide Defenses

“…For example, species with potentially weak predicted defenses may be targeted for captive husbandry. However, the link between in vitro peptide effectiveness and protection in the wild is tentative (Woodhams et al, 2006).…”

“…Chytridiomycosis is an emerging infectious disease of amphibians caused by Batrachochytrium dendrobatidis that affects some species more than others within an assemblage (Berger et al, 1998;Lips et al, 2003b;Retallick et al, 2004;Woodhams and Alford, 2005). For example, chytridiomycosis-associated population declines in Queensland, Australia, may have contributed to the extirpation of some species from high elevations, whereas other species persisted in the same habitat (Richards et al, 1993;Berger et al, 1998).…”

“…In vitro studies showed that many isolated antimicrobial peptides of frogs had potent activity against the fungal pathogen (Rollins-Smith and Conlon, 2005). Natural mixtures of skin peptides are also active (Rollins-Smith et al, 2002b;Woodhams et al, 2006), and this may be more relevant to the natural immune defense of amphibians given that some peptides may act in synergy to inhibit pathogen growth (Westerhoff et al, 1995;Rollins-Smith et al, 2002a). Anuran species show significant variation in the number, structure, and antimicrobial activity of skin peptides (Vanhoye et al, 2003;Apponyi et al, 2004;Conlon et al, 2004).…”

Antimicrobial Peptide Defenses in the Salamander, Ambystoma Tigrinum, Against Emerging Amphibian Pathogens

“…For example, Woodhams et al (2005), using collection procedures similar to those in this study, examined five species of Australian frogs and found total peptide levels ranging from 10.5 to 29.6 mg/gram body weight. This is in contrast to the 325-400 mg/gram body weight collected from tiger salamanders (Table 1).…”

“…The relative amounts of active peptides produced by each acclimation treatment were compared using MIC equivalent measures per gram of body weight and per cm 2 of surface area. MIC equivalents are defined as the total amount of peptides recovered (mg) per gram weight or per cm 2 surface area divided by the experimentally determined MIC (mg/ml) for each treatment (Woodhams et al, 2005). Surface area of the salamanders in cm 2 was calculated using the following allometric equation: surface area58.42 3 (weight in grams) 0.694 (Whitford and Hutchinson, 1967).…”