Endocrine and immune responses of larval amphibians to trematode exposure

Koprivnikar, Janet; Hoye, Bethany J.; Urichuk, Theresa M. Y.; Johnson, Pieter T. J.

doi:10.1007/s00436-018-6154-6

Cited by 14 publications

(7 citation statements)

References 85 publications

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“…Larvae of various amphibian species also show variation in their GC alterations stemming from infection by various parasites or pathogens. While infection with ranavirus or the chytrid fungus Batrachochytrium dendrobatidis seems to elevate GCs in tadpoles (Gabor, Fisher, & Bosch, ; Warne, Crespi, & Brunner, ), infection with trematode helminths has no effect or even results in decreased GCs (Koprivnikar, Hoye, Urichuk, & Johnson, ; Marino, Holland, & Middlemis Maher, ).…”

Section: Introductionmentioning

confidence: 99%

Parasite infection leads to widespread glucocorticoid hormone increases in vertebrate hosts: A meta‐analysis

O’Dwyer

Dargent

Forbes

et al. 2019

Journal of Animal Ecology

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Parasites and pathogens (hereafter parasites) commonly challenge organisms, but the extent to which their infections are physiologically stressful to hosts remains unclear. Importantly, vertebrate hormones, glucocorticoids (GCs), have been reported to increase, decrease or show no alterations stemming from infections, challenging the generality of parasite‐associated GC responses and motivating a search for important moderator variables. We undertook the first meta‐analysis of changes in vertebrate GCs following experimental infection with parasites, extracting 146 effect sizes from 42 studies involving 32 host and 32 parasite species to test for general patterns of GC following infection, as well as the influence of moderators. Overall, infection increased GCs relative to preliminary or control levels when the single largest effect sizes from repeated measures studies were examined, suggesting that parasites of vertebrate hosts can be thought of generally as physiological stressors by elevating GCs. When all effect sizes were included along with the moderator of sampling time post‐infection (tPI), parasite infection still had a positive effect on host GCs. However, the strength of that effect did not relate consistently to tPI, illustrating temporal differences in GC changes during the course of infection among parasite taxa (e.g. arthropod vs. bacterial infections). Other moderator variables examined did not influence GC responses. Studies broadening the range of host and parasite taxa, and sampling during critical time windows, would aid in our understanding of variation in the host stress response and its consequences for fitness of both vertebrate hosts and their parasites.

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Section: Introductionmentioning

confidence: 99%

Parasite infection leads to widespread glucocorticoid hormone increases in vertebrate hosts: A meta‐analysis

O’Dwyer

Dargent

Forbes

et al. 2019

Journal of Animal Ecology

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“…Although our study did not directly assess the causal mechanism underlying this increased susceptibility to infection after exposure to 10 ppb PFHxS, PFOS exposure is negatively associated with eosinophil levels (i.e., white blood cells) in dolphins (Fair et al 2013). Given the critical role of white blood cells in regulating trematode infection (LaFonte and Johnson 2013; Koprivnikar et al 2019), future work quantifying immunological parameters and behavioral responses to PFAS exposure would provide mechanistic insights. These results add to the growing literature documenting negative effects of PFAS on immune function (Yang et al 2000; Dewitt et al 2009; Qazi et al 2009; Rockwell et al 2017).…”

Section: Discussionmentioning

confidence: 99%

Perfluoroalkyl Substances Increase Susceptibility of Northern Leopard Frog Tadpoles to Trematode Infection

Brown

Flynn

Hoverman

2020

Enviro Toxic and Chemistry

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Per/polyfluoroalkyl substances (PFAS) are contaminants of emerging concern that can impair immune function, yet few studies have tested whether exposure increases infection risk. Using laboratory experiments, we found that exposure to 10 ppb of perfluorohexanesulfonic acid increased trematode (Echinoparyphium lineage 3) infections in larval northern leopard frogs (Lithobates pipiens). However, there was no effect of perfluorooctanesulfonic acid. Our results demonstrate that PFAS can potentially enhance infection risk in natural systems.

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“…Helminth-induced immunosuppression is a well-documented strategy used by trematodes to increase their survival in the host (Maizels et al ., 2009; Taylor et al ., 2012), but it is unclear if this occurs in the metacercarial stage that infects amphibians. There is, however, evidence to suggest that early exposure to trematode cercariae can heighten resistance to a later challenge by a functionally different parasite (Hoverman et al ., 2013; Wuerthner et al ., 2017; Koprivnikar et al ., 2019). The fact that mean infection load of individuals exposed to Echinoparyphium on day 0 and Echinostoma on day 3 was significantly lower than the expected value supports the cross-immunity hypothesis and suggests that the E. trivolvis on day 3 had an infection success lower than what would be expected if the infection was additive (i.e.…”

Section: Discussionmentioning

confidence: 99%

“…A limitation of this study is that in coinfected tadpoles, we were unable to differentiate between the cysts of two echinostome species. Several studies of amphibian trematode infections have used fluorescing dye to label cercariae used for exposures on different days, a potentially useful method for future studies of infection dynamics with morphologically similar parasites (Leung and Poulin, 2011; Hoverman et al ., 2013; LaFonte and Johnson, 2013; Johnson et al ., 2014; LaFonte et al ., 2015; Koprivnikar et al ., 2019). Another limitation is that because our field surveys were limited in scope, we can draw few conclusions about how the prevalence of each species changes through the year in natural systems.…”

Section: Discussionmentioning

confidence: 99%

Timing and order of exposure to two echinostome species affect patterns of infection in larval amphibians

Billet¹,

Wuerthner²,

Hua³

et al. 2020

Parasitology

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The study of priority effects with respect to coinfections is still in its infancy. Moreover, existing coinfection studies typically focus on infection outcomes associated with exposure to distinct sets of parasite species, despite that functionally and morphologically similar parasite species commonly coexist in nature. Therefore, it is important to understand how interactions between similar parasites influence infection outcomes. Surveys at seven ponds in northwest Pennsylvania found that multiple species of echinostomes commonly co-occur. Using a larval anuran host (Rana pipiens) and the two most commonly identified echinostome species from our field surveys (Echinostoma trivolvis and Echinoparyphium lineage 3), we examined how species composition and timing of exposure affect patterns of infection. When tadpoles were exposed to both parasites simultaneously, infection loads were higher than when exposed to Echinoparyphium alone but similar to being exposed to Echinostoma alone. When tadpoles were sequentially exposed to the parasite species, tadpoles first exposed to Echinoparyphium had 23% lower infection loads than tadpoles first exposed to Echinostoma. These findings demonstrate that exposure timing and order, even with similar parasites, can influence coinfection outcomes, and emphasize the importance of using molecular methods to identify parasites for ecological studies.

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Endocrine and immune responses of larval amphibians to trematode exposure

Cited by 14 publications

References 85 publications

Parasite infection leads to widespread glucocorticoid hormone increases in vertebrate hosts: A meta‐analysis

Parasite infection leads to widespread glucocorticoid hormone increases in vertebrate hosts: A meta‐analysis

Perfluoroalkyl Substances Increase Susceptibility of Northern Leopard Frog Tadpoles to Trematode Infection

Timing and order of exposure to two echinostome species affect patterns of infection in larval amphibians

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