Changes in selected aspects of immune function in the leopard frog, Rana pipiens , associated with exposure to cold

Maniero, Gregory D.; Carey, Cynthia

doi:10.1007/s003600050072

Cited by 176 publications

(156 citation statements)

References 29 publications

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“…Many components of amphibian innate and adaptive immune systems depend on external temperature, but it takes time for amphibians to adjust these systems to temperature changes. Thus, changes in immune responses tend to lag behind short-term (daily to weekly) temperature changes, with increases in temperature generating suboptimal immunity (32,34). Drops in temperature on a monthly or seasonal time scale might also be particularly important, because ectotherms seem to take longer to acclimate to a temperature decrease than to a temperature increase (35).…”

Section: Resultsmentioning

confidence: 99%

“…Drops in temperature on a monthly or seasonal time scale might also be particularly important, because ectotherms seem to take longer to acclimate to a temperature decrease than to a temperature increase (35). For a variety of immune cells and proteins, low temperatures can dramatically reduce their production and/or activity levels, including (but probably not limited to) peripheral leukocyte levels (32,34), T and B cell proliferation (35), macrophage endocytosis (36), and abundance of antimicrobial skin peptides (37), the latter of which are known to be important for defending against Bd (22). Potential increases in host susceptibility with drops in temperature are of particular concern for Bd epidemics because decreases in temperature might benefit this relatively cold-tolerant pathogen (22,32,38).…”

Section: Resultsmentioning

confidence: 99%

“…Although increases in temperature induced by global warming are expected to be small in tropical relative to temperate regions, recent evidence suggests that the greatest extinction risk from global warming might be for ectotherms in the hyperdiverse tropics because of their adaptations to relatively narrow and stable temperature ranges (46,47). Effects of temporal variation in temperature might also be generalizable across ectotherm classes, given many conserved components of ectotherm innate and adaptive immune responses (32)(33)(34). If so, elevated temperature variability caused by climate change could diminish the defenses of ectothermic hosts generally, potentially representing a common, but underappreciated, link between climate change and both disease and the loss of biodiversity.…”

Section: Discussionmentioning

confidence: 99%

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Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease

Rohr

Raffel

2010

Proc. Natl. Acad. Sci. U.S.A.

305

282

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The role of global climate change in the decline of biodiversity and the emergence of infectious diseases remains controversial, and the effect of climatic variability, in particular, has largely been ignored. For instance, it was recently revealed that the proposed link between climate change and widespread amphibian declines, putatively caused by the chytrid fungus Batrachochytrium dendrobatidis ( Bd ), was tenuous because it was based on a temporally confounded correlation. Here we provide temporally unconfounded evidence that global El Niño climatic events drive widespread amphibian losses in genus Atelopus via increased regional temperature variability, which can reduce amphibian defenses against pathogens. Of 26 climate variables tested, only factors associated with temperature variability could account for the spatiotemporal patterns of declines thought to be associated with Bd . Climatic predictors of declines became significant only after controlling for a pattern consistent with epidemic spread (by temporally detrending the data). This presumed spread accounted for 59% of the temporal variation in amphibian losses, whereas El Niño accounted for 59% of the remaining variation. Hence, we could account for 83% of the variation in declines with these two variables alone. Given that global climate change seems to increase temperature variability, extreme climatic events, and the strength of Central Pacific El Niño episodes, climate change might exacerbate worldwide enigmatic declines of amphibians, presumably by increasing susceptibility to disease. These results suggest that changes to temperature variability associated with climate change might be as significant to biodiversity losses and disease emergence as changes to mean temperature.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease

Rohr

Raffel

2010

Proc. Natl. Acad. Sci. U.S.A.

305

282

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“…dIndicates only weak positivity in PCR test for ranavirus DNA. (Maniero & Carey, 1997). Although we conducted the experimental inoculation in early spring, a time when wood frogs are most likely to come in contact with infected carriers as they go to the ponds for mating (Brunner et al, 2004), the temperature maintained during the experiment (average 21 u C) was higher than the environmental temperature would have been in the wild.…”

Section: Discussionmentioning

confidence: 99%

Clinical signs, pathology and dose-dependent survival of adult wood frogs, Rana sylvatica, inoculated orally with frog virus 3 Ranavirus sp., Iridoviridae

Forzán

Jones

Vanderstichel

et al. 2015

Journal of General Virology

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School of Veterinary and Biomedical Sciences, James Cook University, Townsville, Australia Amphibian populations suffer massive mortalities from infection with frog virus 3 (FV3, genus Ranavirus, family Iridoviridae), a pathogen also involved in mortalities of fish and reptiles. Experimental oral infection with FV3 in captive-raised adult wood frogs, Rana sylvatica (Lithobates sylvaticus), was performed as the first step in establishing a native North American animal model of ranaviral disease to study pathogenesis and host response. Oral dosing was successful; LD 50 was 10 2.93 (2.42-3.44) p.f.u. for frogs averaging 35 mm in length. Onset of clinical signs occurred 6-14 days post-infection (p.i.) (median 11 days p.i.) and time to death was 10-14 days p.i. (median 12 days p.i.). Each tenfold increase in virus dose increased the odds of dying by 23-fold and accelerated onset of clinical signs and death by approximately 15 %. Ranavirus DNA was demonstrated in skin and liver of all frogs that died or were euthanized because of severe clinical signs. Shedding of virus occurred in faeces (7-10 days p.i.; 3-4.5 days before death) and skin sheds (10 days p.i.; 0-1.5 days before death) of some frogs dead from infection. Most common lesions were dermal erosion and haemorrhages; haematopoietic necrosis in bone marrow, kidney, spleen and liver; and necrosis in renal glomeruli, tongue, gastrointestinal tract and urinary bladder mucosa. Presence of ranavirus in lesions was confirmed by immunohistochemistry. Intracytoplasmic inclusion bodies (probably viral) were present in the bone marrow and the epithelia of the oral cavity, gastrointestinal tract, renal tubules and urinary bladder. Our work describes a ranavirus-wood frog model and provides estimates that can be incorporated into ranavirus disease ecology models.

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“…shtml); thus the average temperature is still within the range of temperatures that support the existence of B. dendrobatidis. The wide fluctuation of temperature in early spring here may disturb the immune systems of amphibians and may increase the probability of disease occurrence (Clem et al 1991, Maniero & Carey 1997.…”

Section: Discussionmentioning

confidence: 99%

Early-spring survey for Batrachochytrium dendrobatidis in wild Rana dybowskii in Heilongjiang Province, China

Wei¹,

Xu²,

Zhu³

et al. 2010

Dis. Aquat. Org.

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Batrachochytrium dendrobatidis has been investigated worldwide because of its importance in population declines in multiple species of amphibians; however, little is known regarding the disease status of all native amphibian species in China. The present study is the first survey of chytridiomycosis in free-ranging amphibian populations in China, and it examined the possible presence of B. dendrobatidis in Rana dybowskii in northeastern China (Heilongjiang Province). R. dybowskii is mainly distributed in the northeast part of China and is intensively hunted for human consumption, making populations vulnerable to extirpation in the event of additional stresses from disease epidemics. The survey was performed in early spring of 2008, using a PCR assay, histological examination of skin samples, and zoospore culture. In total, 191 frogs were examined; thus, a 95% confidence limit for prevalence of 1.57% was selected. Our results demonstrate that R. dybowskii is currently free from chytridiomycosis in Heilongjiang, even though the natural conditions of the sampling sites are suitable for the occurrence of B. dendrobatidis. Central and local governments should implement strict management measures to prevent the escape of non-native commercial amphibian species into this area, which might endanger local populations of native species.

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Changes in selected aspects of immune function in the leopard frog, Rana pipiens , associated with exposure to cold

Cited by 176 publications

References 29 publications

Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease

Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease

Clinical signs, pathology and dose-dependent survival of adult wood frogs, Rana sylvatica, inoculated orally with frog virus 3 Ranavirus sp., Iridoviridae

Early-spring survey for Batrachochytrium dendrobatidis in wild Rana dybowskii in Heilongjiang Province, China

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