Abstract
The relationship between amphibian immune function and disease susceptibility is of primary concern given current worldwide declines linked to the pathogenic fungus Batrachochytrium dendrobatidis (Bd). We experimentally infected lowland leopard frogs (Lithobates yavapaiensis) with Bd to test the hypothesis that infection causes physiological stress and stimulates humoral and cell-mediated immune function in the blood. We measured body mass, the ratio of circulating neutrophils to lymphocytes (a known indicator of physiological stress) and plasma bacterial killing ability (BKA; a measure of innate immune function). In early exposure (1-15 days post-infection), stress was elevated in Bd-positive vs. Bd-negative frogs, whereas other metrics were similar between the groups. At later stages (29-55 days post-infection), stress was increased in Bd-positive frogs with signs of chytridiomycosis compared with both Bd-positive frogs without disease signs and uninfected control frogs, which were similar to each other. Infection decreased growth during the same period, demonstrating that sustained resistance to Bd is energetically costly. Importantly, BKA was lower in Bd-positive frogs with disease than in those without signs of chytridiomycosis. However, neither group differed from Bd-negative control frogs. The low BKA values in dying frogs compared with infected individuals without disease signs suggests that complement activity might signify different immunogenetic backgrounds or gene-by-environment interactions between the host, Bd and abiotic factors. We conclude that protein complement activity might be a useful predictor of Bd susceptibility and might help to explain differential disease outcomes in natural amphibian populations.
Highlights
The pathogenic fungus Batrachochytrium dendrobatidis (Bd) was first identified as the causative agent of chytridiomycosis and definitively linked to declines and extinctions of natural amphibian populations in 1998 (Berger et al, 1998)
Eleven of the remaining 12 infected frogs developed all signs of chytridiomycosis and were euthanized immediately to collect fresh samples before they died; the 12th frog died before euthanasia could take place (31 days post-infection (DPI)), and we were unable to collect any viable samples
Given that the 12 dying frogs manifested all signs of chytridiomycosis over a 21 day period, some of the ‘surviving’ group of frogs that were euthanized between 29 and 55 DPI may have been Bd susceptible but not yet manifesting signs
Summary
The pathogenic fungus Batrachochytrium dendrobatidis (Bd) was first identified as the causative agent of chytridiomycosis and definitively linked to declines and extinctions of natural amphibian populations in 1998 (Berger et al, 1998). Only recently has it been demonstrated that host immune function plays a role in Bd susceptibility (Ribas et al, 2009; Savage and Zamudio, 2011; Rosenblum et al, 2012) and that the pathogen actively suppresses host immunity by inducing lymphocyte apoptosis (Fites et al, 2013). These findings highlight the need to gain a better understanding of amphibian immune responses, in the context of Bd infections. Vertebrates share a complex network of serum proteins, known as the complement system, that plays a key role in both innate (Koppenheffer, 1987) and acquired immunity (Nielsen and Leslie, 2002). Through a coordinated cascade of reactions, these proteins trigger local inflammatory responses, promote the uptake and destruction of pathogens by phagocytes, and form membrane-attack complexes that destroy certain pathogens directly (Janeway et al, 2001)
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