Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis

Abstract

Mounting evidence implicates the disease chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis, in global amphibian declines and extinctions. While the virulence of this disease has been clearly demonstrated, there is, as yet, no mechanistic explanation for how B. dendrobatidis kills amphibians. To investigate the pathology of chytridiomycosis, blood samples were collected from uninfected, aclinically infected and clinically diseased amphibians and analyzed for a wide range of biochemical and hematological parameters. Here, we show that green tree frogs Litoria caerulea with severe chytridiomycosis had reduced plasma osmolality, sodium, potassium, magnesium and chloride concentrations. Stable plasma albumin, hematocrit and urea levels indicated that hydration status was unaffected, signifying depletion of electrolytes from circulation rather than dilution due to increased water uptake. We suggest that B. dendrobatidis kills amphibians by disrupting normal epidermal functioning, leading to osmotic imbalance through loss of electrolytes. Determining how B. dendrobatidis kills amphibians is fundamental to understanding the hostpathogen relationship and thus the population declines attributed to B. dendrobatidis. Understanding the mechanisms of mortality may also explain interspecific variation in susceptibility to chytridiomycosis. KEY WORDS:Amphibian declines · Chytridiomycosis · Batrachochytrium dendrobatidis · Pathogenesis · Mortality · Osmoregulation Resale or republication not permitted without written consent of the publisherDis Aquat Org 77: [113][114][115][116][117][118] 2007 Amphibian skin is well studied due to its unique functions (Deyrup 1964, Heatwole & Barthalmus 1994, Jorgensen 1997. The integument is a site of regulated transport for water, ions (electrolytes) and respiratory gases (Deyrup 1964, Heatwole & Barthalmus 1994, Jorgensen 1997. Permeability of frog skin varies over the body surface of an individual and also among species (Deyrup 1964, Heatwole & Barthalmus 1994. In some species osmotic permeability is greatest in an area of ventral integument commonly referred to as the pelvic patch (Czopek 1965, Baldwin 1974, Word & Hillman 2005, where there is dense cutaneous vasculature (Czopek 1965). Concomitantly, Batrachochytrium dendrobatidis occurs more commonly and at higher density in the ventral integument of infected frogs (Berger et al. 2005b, Puschendorf & Bolaños 2006. B. dendrobatidis grows within the keratinized cells of the superficial epidermis and causes irregular skin sloughing, hyperplasia and hyperkeratosis (Berger et al. 1998, 2005b, 2007. Other pathological changes including cytoplasmic degeneration and vacuolation in scattered cells have been observed by light and electron microscopy, but these changes are not usually severe (Berger et al. 2007). Thus, it is unclear how a superficial skin infection kills frogs.The aim of this research was to investigate pathogenesis in amphibians with chytridiomycosis. We evaluated changes in physiological parameters...

SUSCEPTIBILITY TO THE AMPHIBIAN CHYTRID FUNGUS VARIES WITH ONTOGENY IN THE DIRECT-DEVELOPING FROG,ELEUTHERODACTYLUS COQUI

“…The aquatic fungus that causes chytridiomycosis, Batrachochytrium dentrobatidis (Bd), is known to infect over 500 amphibian species (Olson et al 2013). The fungus colonizes the keratinized tissue of amphibian skin (Longcore et al 1999) and, in at least one species, causes death through osmotic and electrolyte imbalance (Voyles et al 2007). Species vary in susceptibility (e.g., Searle et al 2011), with responses ranging from mass mortality (Lips et al 2006), to tolerance of subclinical infection (Garner et al 2006), and to resistance (Marquez et al 2010).…”

Dynamics of an emerging disease drive large-scale amphibian population extinctions

“…Effects of chytridiomycosis on frogs are highly variable, with frogs of some species dying from the disease within weeks and others experiencing few negative effects (4). Chytridiomycosis likely causes frog mortality by severely disrupting epidermal functions and causing osmotic imbalance (14,15). However, it remains unknown how chytridiomycosis is able to cause the extinction of its amphibian hosts, an outcome that would require that Bd not be severely limited by density-dependent factors.…”

Reduced Itraconazole Concentration and Durations Are Successful in Treating <em>Batrachochytrium dendrobatidis</em> Infection in Amphibians

“…The amphibian chytrid fungus is not host specific and it is unclear what qualities of the host allow for Bd infection to progress causing severe disease. Chytridiomycosis causes death by disrupting ion channels in the skin, resulting in electrolyte loss and heart failure 4 . Also, Bd supernatant (containing no Bd zoospores) causes an immune response in tadpoles 5 leading researchers to believe Bd produces a toxic by-product 6 .…”