Correction: Hibernating Little Brown Myotis (Myotis lucifugus) Show Variable Immunological Responses to White-Nose Syndrome

Abstract

White-nose syndrome (WNS) is an emerging infectious disease devastating hibernating North American bat populations that is caused by the psychrophilic fungus Geomyces destructans. Previous histopathological analysis demonstrated little evidence of inflammatory responses in infected bats, however few studies have compared other aspects of immune function between WNS-affected and unaffected bats. We collected bats from confirmed WNS-affected and unaffected sites during the winter of 2008-2009 and compared estimates of their circulating levels of total leukocytes, total immunoglobulins, cytokines and total antioxidants. Bats from affected and unaffected sites did not differ in their total circulating immunoglobulin levels, but significantly higher leukocyte counts were observed in bats from affected sites and particularly in affected bats with elevated body temperatures (above 20uC). Bats from WNS-affected sites exhibited significantly lower antioxidant activity and levels of interleukin-4 (IL-4), a cytokine that induces T cell differentiation. Within affected sites only, bats exhibiting visible fungal infections had significantly lower antioxidant activity and levels of IL-4 compared to bats without visible fungal infections. Overall, bats hibernating in WNS-affected sites showed immunological changes that may be evident of attempted defense against G. destructans. Observed changes, specifically elevated circulating leukocytes, may also be related to the documented changes in thermoregulatory behaviors of affected bats (i.e. increased frequencies in arousal from torpor). Alterations in immune function may reflect expensive energetic costs associated with these processes and intrinsic qualities of the immunocapability of hibernating bats to clear fungal infections. Additionally, lowered antioxidant activity indicates a possible imbalance in the pro-versus antioxidant system, may reflect oxidative tissue damage, and should be investigated as a contributor to WNS-associated morbidity and mortality.

Biomarker Metabolites Discriminate between Physiological States of Field, Cave and White-nose Syndrome Diseased Bats

“…Alkanes and methylated alkanes also have been associated with oxidative stress and lipid peroxidation [ 54 , 55 , 56 ]. Moore et al [ 57 ] provided evidence that oxidative stress was a significant factor contributing to WNS-associated mortality. Lawal et al [ 52 ] found several alkanes including decane, hexane, octane and cyclohexane that were elevated when epithelial cells were exposed to oxidative stress.…”

“…The CA-biomarkers do not appear to be related to physiological activities associated with vigorous physical activities (such as flying), but are more associated with sedentary awake activities such as cleaning or grooming off activities which are conscious activities more commonly practiced by active field bats or bats that have recently entered a cave (and have not yet initiated torpor), and less common in torpid cave bats that engage in grooming activities only for brief intermittent periods during infrequent prolonged arousals. The release of CA-biomarkers in cave bats also may possibly be correlated with activation of major histocompatibility complex (MHC) immune responses when bats are awake, involving cytokine production, that have been indicated as adaptive immunity to WNS in certain European bat species developing long-term resistance, but may not yet be fully or effectively operating in North American bat species due to only recent occurrence of this disease [ 57 , 73 , 74 ].…”