Unlikely Remedy: Fungicide Clears Infection from Pathogenic Fungus in Larval Southern Leopard Frogs (Lithobates sphenocephalus)

Hanlon, Shane M.; Kerby, Jacob L.; Parris, Matthew J.

doi:10.1371/journal.pone.0043573

Cited by 37 publications

(38 citation statements)

References 73 publications

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“…Tadpoles were placed in 50 ml water baths (3 individuals per 50 ml in 500 ml containers) and zoospores (2.88 × 10 6 zoospores) was added to each bath for 48 h. The non-exposed group (N = 12) followed the same protocol but the water was added to plates with TGhL alone. This design simulates transmission by water, a possible mode of Bd transmission in natural environments (Johnson & Speare 2005), and has resulted in successful infections in previous studies (Venesky et al 2009, Hanlon et al 2012. After 48 h, tadpoles were removed from their exposure treatment, individually placed into containers containing clean water, and infection was allowed to develop over 7 d.…”

Section: Batrachochytrium Dendrobatidis Inoculationmentioning

confidence: 99%

Section: Batrachochytrium Dendrobatidis Inoculationmentioning

confidence: 99%

“…As keratin occurs in the mouthparts of tadpoles in most species (McDiarmid & Altig 1999), Bd also infects tadpole mouthparts; however it is not usually a direct cause of mortality (but see Searle et al 2013, Hanlon & Parris 2014. While non-lethal, Bd-induced damage to tadpole mouthparts has been shown to reduce foraging efficiencies (Venesky et al 2009) and reduce tadpole growth (Venesky et al 2009(Venesky et al , 2013; but see Hanlon et al 2012, Kleinhenz et al 2012. Recently, Venesky et al (2013) showed that Bd exposure reduced tadpole size, and mouthpart damage reduced the size of tadpole guts relative to body size.…”

Section: Introductionmentioning

confidence: 99%

“…Stock cultures were transferred monthly, plated to TGhL plates, and all Bd inoculates were taken from these plates. This strain has resulted in successful infections in both laboratory and field experiments (Venesky et al 2009, Hanlon et al 2012.We harvested Bd zoospores by flooding the plates with sterile water and collecting the zoospores that emerged from the zoosporangia after 45 min. All water from the flooded plates was combined, and we estimated the density of zoospores using a 0.100 mm deep hemocytometer (Fisher Scientific).…”

mentioning

confidence: 99%

“…This extraction technique is known to be reliable for extracting Bd DNA and the same exposure protocols have resulted in successful infections in previous experiments (e.g. Cheng et al 2011, Hanlon et al 2012, Prunier et al 2012.For qPCR analysis, standards were obtained from Commonwealth Scientific and Industrial Research Organisation (CSIRO) labs in Australia and were the same as those used in Boyle et al (2004). The standards used in the qPCR reaction served as the positive controls on each plate and each plate contained a negative control; all samples were run in triplicate.…”

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confidence: 99%

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Batrachochytrium dendrobatidis exposure effects on foraging efficiencies and body size in anuran tadpoles

Hanlon¹,

Lynch²,

Kerby³

et al. 2015

Dis. Aquat. Org.

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Chytridiomycosis, the amphibian disease caused by the pathogenic fungus Batrachochytrium dendrobatidis (Bd), is fatal to adults of many species. Bd is largely sublethal to amphibian larvae; however, it is known to reduce larval (i.e. tadpole) growth rates, with possible long-term effects on population dynamics and fitness. We conducted an experiment to test how Bd altered southern leopard frog Lithobates sphenocephalus tadpole mouthpart damage, percentage of food ingested, and subsequent body size. We examined our results using path analyses. We hypothesized that Bd would increase mouthpart damage, causing less food to be ingested, and ultimately reduce body size. In our model, both Bd exposure and increased mouthpart damage significantly reduced food ingested and subsequent body size. However, our study provides evidence against the long-standing hypothesis of mouthpart damage as a pathway for Bd-induced reductions in larval group. Here we provide evidence for reduced foraging efficiency (percentage of food ingested) as a mechanism for Bd-induced reductions in body size. This work highlights the importance of studying the sublethal effects of Bd on larval amphibians. KEY WORDS: Chytrid fungus · Feeding · Larvae · Life history traits · Path analysisResale or republication not permitted without written consent of the publisher © Inter-Research 2015 · www.int-res.com Dis Aquat Org 112: [237][238][239][240][241][242] 2015 al. (2013) showed that Bd exposure reduced tadpole size, and mouthpart damage reduced the size of tadpole guts relative to body size. In other words, studies have shown that Bd causes mouthpart damage, damage reduces foraging efficiency, and reduced efficiency reduces growth. So it can be inferred that Bd-induced mouthpart damage potentially reduces growth. However, this pathway has never been proven. While previous studies have provided evidence for possible pathways by which Bd-induced reductions in tadpole growth may occur, a direct pathway from Bd-induced mouthpart damage to reduced growth has yet to be confirmed.Much work has focused on the direct, lethal effects of Bd on host populations. While such research is imperative to our understanding of the disease, the sublethal effects of Bd, especially on larval amphibians, could have lasting carry-over effects that negatively alter natural populations. To address the sublethal impact(s) of Bd on tadpoles and identify a pathway whereby Bd reduces growth and development, we tested the hypothesis that Bd would cause mouthpart damage, food intake, and subsequent growth. We conducted a laboratory study using southern leopard frog Lithobates sphenocephalus tadpoles. Using path analyses, we tested how Bd, mouthpart damage, and percentage of food in the gut (hereafter gut content), directly or indirectly influenced body size (growth measure). We predicted that Bd would increase mouthpart damage, in turn reducing gut content and subsequent body size. Also, independent of Bd exposure, we predicted that increased mouthpart damage would negati...

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Section: Batrachochytrium Dendrobatidis Inoculationmentioning

confidence: 99%

Section: Batrachochytrium Dendrobatidis Inoculationmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Batrachochytrium dendrobatidis exposure effects on foraging efficiencies and body size in anuran tadpoles

Hanlon¹,

Lynch²,

Kerby³

et al. 2015

Dis. Aquat. Org.

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A pesticide paradox: fungicides indirectly increase fungal infections

Rohr

Brown

Battaglin

et al. 2017

Ecological Applications

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There are many examples where the use of chemicals have had profound unintended consequences, such as fertilizers reducing crop yields (paradox of enrichment) and insecticides increasing insect pests (by reducing natural biocontrol). Recently, the application of agrochemicals, such as agricultural disinfectants and fungicides, has been explored as an approach to curb the pathogenic fungus, Batrachochytrium dendrobatidis (Bd), which is associated with worldwide amphibian declines. However, the long-term, net effects of early-life exposure to these chemicals on amphibian disease risk have not been thoroughly investigated. Using a combination of laboratory experiments and analysis of data from the literature, we explored the effects of fungicide exposure on Bd infections in two frog species. Extremely low concentrations of the fungicides azoxystrobin, chlorothalonil, and mancozeb were directly toxic to Bd in culture. However, estimated environmental concentrations of the fungicides did not reduce Bd on Cuban tree frog (Osteopilus septentrionalis) tadpoles exposed simultaneously to any of these fungicides and Bd, and fungicide exposure actually increased Bd-induced mortality. Additionally, exposure to any of these fungicides as tadpoles resulted in higher Bd abundance and greater Bd-induced mortality when challenged with Bd post-metamorphosis, an average of 71 days after their last fungicide exposure. Analysis of data from the literature revealed that previous exposure to the fungicide itraconazole, which is commonly used to clear Bd infections, made the critically endangered booroolong frog (Litoria booroolongensis) more susceptible to Bd. Finally, a field survey revealed that Bd prevalence was positively associated with concentrations of fungicides in ponds. Although fungicides show promise for controlling Bd, these results suggest that, if fungicides do not completely eliminate Bd or if Bd re-colonizes, exposure to fungicides has the potential to do more harm than good. To ensure that fungicide applications have the intended consequence of curbing amphibian declines, researchers must identify which fungicides do not compromise the pathogen resistance mechanisms of amphibians.

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The interactive effects of chytrid fungus, pesticides, and exposure timing on gray treefrog (Hyla versicolor) larvae

Hanlon

Parris

2013

Environmental Toxicology and Chemistry

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Aquatic organisms are often exposed to a wide variety of perturbations in nature, including pathogens and chemical contaminants. Despite the co-occurrence of these 2 stressors, few studies have examined the effects of chemical contaminants on host-pathogen dynamics. The authors tested the individual and combined effects on gray treefrog (Hyla versicolor) tadpoles of 2 commonly used pesticides (Roundup® and Sevin®) and the pathogenic fungus Batrachochytrium dendrobatidis (Bd). A fully factorial design was used, and tadpoles were exposed to Bd, Roundup, or Sevin alone, or a combination of Bd and either pesticide at 3 points during larval development (early, mid, late). It was predicted that pesticides would mediate the effect of Bd on tadpoles and reduce the likelihood of negative consequences of infection and that timing of exposure would influence these effects. Tadpoles exposed to Bd at the mid point experienced higher survival through metamorphosis than those exposed to Bd at the early or late points, while tadpoles exposed to Sevin at the early point experienced reduced survival compared with those exposed to Roundup or no-pesticide control at the same exposure point. Roundup ameliorated the effects of Bd on survival compared with tadpoles exposed to Bd alone, while there was no interactive effect of Sevin on survival. In addition, Sevin reduced mass of new metamorphs compared with Roundup and reduced snout-vent length compared with all other treatments. The present study supports the hypothesis that pesticides can mitigate the effects of Bd on amphibian hosts and that such effects may depend on the timing of exposure.

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Unlikely Remedy: Fungicide Clears Infection from Pathogenic Fungus in Larval Southern Leopard Frogs (Lithobates sphenocephalus)

Cited by 37 publications

References 73 publications

Batrachochytrium dendrobatidis exposure effects on foraging efficiencies and body size in anuran tadpoles

Batrachochytrium dendrobatidis exposure effects on foraging efficiencies and body size in anuran tadpoles

A pesticide paradox: fungicides indirectly increase fungal infections

The interactive effects of chytrid fungus, pesticides, and exposure timing on gray treefrog (Hyla versicolor) larvae

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