Temperature, hydric environment, and prior pathogen exposure alter the experimental severity of chytridiomycosis in boreal toads

Abstract

Prevalence of the pathogen Batrachochytrium dendrobatidis (Bd), implicated in amphibian population declines worldwide, is associated with habitat moisture and temperature, but few studies have varied these factors and measured the response to infection in amphibian hosts. We evaluated how varying humidity, contact with water, and temperature affected the manifestation of chytridiomycosis in boreal toads Anaxyrus (Bufo) boreas boreas and how prior exposure to Bd affects the likelihood of survival after re-exposure, such as may occur seasonally in long-lived species. Humidity did not affect survival or the degree of Bd infection, but a longer time in contact with water increased the likelihood of mortality. After exposure to ~106 Bd zoospores, all toads in continuous contact with water died within 30 d. Moreover, Bd-exposed toads that were disease-free after 64 d under dry conditions, developed lethal chytridiomycosis within 70 d of transfer to wet conditions. Toads in unheated aquaria (mean = 15°C) survived less than 48 d, while those in moderately heated aquaria (mean = 18°C) survived 115 d post-exposure and exhibited behavioral fever, selecting warmer sites across a temperature gradient. We also found benefits of prior Bd infection: previously exposed toads survived 3 times longer than Bd-naïve toads after re-exposure to 10 6 zoospores (89 vs. 30 d), but only when dry microenvironments were available. This study illustrates how the outcome of Bd infection in boreal toads is environmentally dependent: when continuously wet, high reinfection rates may overwhelm defenses, but periodic drying, moderate warming, and previous infection may allow infected toads to extend their survival.KEY WORDS: Boreal toads · Disease severity · Chytridiomycosis · Temperature · Moisture · Acquired immunity Resale or republication not permitted without written consent of the publisherDis Aquat Org 95: 31-42, 2011 32 lethal chytridiomycosis, however, depends not only on Bd, but on the host's immune response. Resistance to Bd has been linked to antimicrobial skin peptides and other hydrophobic molecules (Woodhams et al. 2007, Rollins-Smith et al. 2009) and cutaneous bacteria (Harris et al. 2006), both of which may change in effectiveness depending on body temperature and hydric environment (Matutte et al. 2000, Rollins-Smith et al. 2002.Although the effects of varying temperature on chytridiomycosis have been studied experimentally, the outcomes in vivo have not always been consistent with the temperature optima of Bd in pure culture. For example, Carey et al. (2006) found no difference in survival time in infected boreal toads Anaxyrus boreas boreas housed at 12 and 23°C, although 12°C is well below the optimal growth range of Bd. Likewise, 2 studies have found that moderate changes in temperature within the optimal growth range of Bd (from 17 to 22-23°C) increased survival in exposed amphibians (Andre et al. 2008, Bustamante et al. 2010. Amphibians often modify their body temperature behaviorally, including in response t...

Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus

“…In this study, approximately 30% of golden frogs either cleared infection (14%) or were predicted to clear infection (16%). Susceptibility to Bd can differ among amphibian species and populations [47], probably due to variation in defence mechanisms of the host [18,48,49], the virulence of Bd [46] and properties of the environment where the host and pathogen interact [50]. The environment and Bd strain in this study were constant across all frogs and were therefore not factors in the variation in Bd susceptibility.…”

Behavioral fever in ectothermic vertebrates

“…Up to date, behavioral fever has been described in all groups of ectothermic vertebrates including reptiles (Bernheim and Kluger, 1976a,b;Burns et al, 1996;do Amaral et al, 2002;Hallman et al, 1990;Kluger et al, 1975;Merchant et al, 2007Merchant et al, , 2008Monagas and Gatten, 1983;Muchlinski et al, 1995;Ortega et al, 1991;Ramos et al, 1993;Vaughn et al, 1974), amphibians (Casterlin and Reynolds, 1977;Kluger, 1977;Murphy et al, 2011;Myhre et al, 1977;Richards-Zawacki, 2010;Sherman et al, 1991), fish (Boltaña et al, 2013;Cabanac and Laberge, 1998;Covert and Reynolds, 1977;Grans et al, 2012;Reynolds, 1977;Reynolds et al, 1976Reynolds et al, , 1978 but also in invertebrates (Campbell et al, 2010;Elliot et al, 2002) and newborn mammals, which in response to bacterial pyrogens are unable to develop fever physiologically but do so behaviorally (Satinoff et al, 1976). However, there have been some contrasting data showing that injection of pyrogens, killed bacteria or parasites in some species of lizards (Don et al, 1994;Hallman et al, 1990;Laburn et al, 1981;Muchlinski et al, 1995;Ortega et al, 1991;Schall, 1990), turtles (Zurovsky et al, 1987b), snakes (Burns et al, 1996;Zurovsky et al, 1987a) and fish …”

“…1b) including LPS (Cabanac and Laberge, 1998;do Amaral et al, 2002;Grans et al, 2012;Merchant et al, 2007Merchant et al, , 2008Reynolds et al, 1978;Sherman et al, 1991), various species of Gram-positive and Gram-negative bacteria, administrated as killed or live forms (Bernheim and Kluger, 1976a,b;Burns et al, 1996;Casterlin and Reynolds, 1977;Covert and Reynolds, 1977;Hallman et al, 1990;Kluger, 1977;Kluger et al, 1975;Monagas and Gatten, 1983;Muchlinski et al, 1995;Myhre et al, 1977;Ortega et al, 1991;Ramos et al, 1993;Reynolds, 1977;Reynolds et al, 1976Reynolds et al, , 1978Vaughn et al, 1974), fungi (Murphy et al, 2011;Richards-Zawacki, 2010), ectoparasite (Gyrodactylus turnbulli) (Mohammed et al, 2016), synthetic dsRNA (poly I:C) (Boltaña et al, 2013) or viruses (Boltaña et al, 2013). Because of the relatively low sensitivity of fish and toads to LPS, the dose used to induce behavioral fever in these animals (toad:…”

Condition-dependent reproductive effort in frogs infected by a widespread pathogen

“…Because calling requires substantial energy, reduced body condition can also lead to reduction of calling effort or temporal shifts in calling effort [20]. Frogs infected by B. dendrobatidis often have lower body condition than uninfected frogs [28][29][30]; when this occurs, they might reduce calling effort. On the other hand, infected hosts with relatively good body condition may have the plasticity to respond to the infection by investing more in present reproductive effort than uninfected individuals when their expectation of survival to the next reproductive bout is lower [13][14][15][16][17][18].…”