The Adaptiveness of Parental Care in Desmognathus ochrophaeus (Urodela: Plethodontidae)

Forester, Don C.

doi:10.2307/1443421

Cited by 76 publications

(57 citation statements)

References 12 publications

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“…Amphibians periodically shed their skins, so it is reasonable to expect that some proportion of the population lacks violacein on the skin at any given time. Species that attend their embryos in nests, such as P. cinereus, minimize the effects of pathogenic fungi on their embryos (1,6,14). We have shown that in another species of salamander, H. scutatum, females with culturable antifungal skin bacteria can minimize embryonic mortality due to fungi (1).…”

Section: Discussionmentioning

confidence: 99%

The Bacterially Produced Metabolite Violacein Is Associated with Survival of Amphibians Infected with a Lethal Fungus

Becker

Brucker

Schwantes

et al. 2009

Appl Environ Microbiol

185

161

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The disease chytridiomycosis, which is caused by the chytrid fungus Batrachochytrium dendrobatidis, is associated with recent declines in amphibian populations. Susceptibility to this disease varies among amphibian populations and species, and resistance appears to be attributable in part to the presence of antifungal microbial species associated with the skin of amphibians. The betaproteobacterium Janthinobacterium lividum has been isolated from the skins of several amphibian species and produces the antifungal metabolite violacein, which inhibits B. dendrobatidis. In this study, we added J. lividum to red-backed salamanders (Plethodon cinereus) to obtain an increased range of violacein concentrations on the skin. Adding J. lividum to the skin of the salamander increased the concentration of violacein on the skin, which was strongly associated with survival after experimental exposure to B. dendrobatidis. As expected from previous work, some individuals that did not receive J. lividum and were exposed to B. dendrobatidis survived. These individuals had concentrations of bacterially produced violacein on their skins that were predicted to kill B. dendrobatidis. Our study suggests that a threshold violacein concentration of about 18 M on a salamander's skin prevents mortality and morbidity caused by B. dendrobatidis. In addition, we show that over one-half of individuals in nature support antifungal bacteria that produce violacein, which suggests that there is a mutualism between violaceinproducing bacteria and P. cinereus and that adding J. lividum is effective for protecting individuals that lack violacein-producing skin bacteria.The amphibian fungal pathogen Batrachochytrium dendrobatidis causes a lethal skin disease that has caused substantial declines in amphibian populations (18). However, some species, such as the bullfrog (Rana catesbeiana) and the tiger salamander (Ambystoma tigrinum), are relatively asymptomatic when they are infected with this pathogen (4, 5). Variation in survival among species has been attributed to differences in innate immune factors, such as antimicrobial peptides (20) and skin-associated microbial species (8-11), as well as behavior (16). The presence of antifungal microbes is of particular interest because it suggests that these organisms are mutualistic associates of amphibian species. In addition, augmentation of the cutaneous microbial community by adding species of bacteria that inhibit B. dendrobatidis has the potential to provide resistance to chytridiomycosis (9).We have identified a number of bacteria associated with the skin of amphibians that inhibit B. dendrobatidis in vitro via secretion of antifungal metabolites (2,3,10,11). The bacterial species used in this study, Janthinobacterium lividum, produces the anti-B. dendrobatidis metabolites violacein and indole-3-carboxaldehyde (MIC, 1.82 M and 69 M, respectively) (3). We have shown that violacein inhibits B. dendrobatidis in laboratory assays (3) and is strongly correlated with survival in vivo of the frog species Ra...

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Section: Discussionmentioning

confidence: 99%

The Bacterially Produced Metabolite Violacein Is Associated with Survival of Amphibians Infected with a Lethal Fungus

Becker

Brucker

Schwantes

et al. 2009

Appl Environ Microbiol

185

161

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“…Females frequently desert their eggs in joint nests, leaving only one female to brood the eggs (Blanchard, 1934;Harris et al, 1995). Females that stay at the nest provide parental care, such as aeration, moistening and cleaning of the embryos and weave among them (Forester, 1979). The female lays her eggs in spring, in a clump of moss, leaf litter or rotting wood overhanging a pond or seepage and attends them for 30-60 days.…”

Section: Methodsmentioning

confidence: 99%

“…When amphibian embryos of species that attend their nests are deserted, embryos often succumb to fungal infections (Forester, 1979;Harris et al, 1995). Fungi may develop preferentially on nonviable or spoiled eggs (Villa, 1979), but in some cases fungi are pathogenic and kill healthy eggs (Villa, 1979;Warkentin et al, 2001;JL Banning et al, unpublished data).…”

Section: Introductionmentioning

confidence: 99%

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Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders

et al. 2007

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Among the microbiota of amphibian skin are bacteria that produce antifungal compounds. We isolated cutaneous bacteria from the skins of three populations of the nest-attending plethodontid salamander Hemidactylium scutatum and subsequently tested the bacterial isolates against two different fungi (related to Mariannaea elegans and Rhizomucor variabilis) that were obtained from dead salamander eggs. The culturable antifungal bacteria were phylogenetically characterized based on 16S rRNA phylogeny, and belonged to four phyla, comprising 14 bacterial families, 16 genera and 48 species. We found that about half of the antifungal bacterial genera and families were shared with a related salamander species, but there was virtually no overlap at the species level. The proportion of culturable antifungal bacterial taxa shared between two large populations of H. scutatum was the same as the proportion of taxa shared between H. scutatum and Plethodon cinereus, suggesting that populations within a species have unique antifungal bacterial species. Approximately 30% of individuals from both salamander species carried anti-M. elegans cutaneous bacteria and almost 90% of P. cinereus and 100% of H. scutatum salamanders carried anti-R. variabilis cutaneous bacteria. A culture independent method (PCR/DGGE) revealed a shared resident bacterial community of about 25% of the entire resident bacterial community within and among populations of H. scutatum. Thus, the culturable antifungal microbiota was far more variable on salamander skins than was the bacterial microbiota detected by PCR/DGGE. The resident cutaneous antifungal bacteria may play an important role in amphibians' innate defense against pathogens, including the lethal chytrid fungus Batrachochytrium dendrobatidis.

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“…In many natural amphibian populations, fungal infections of eggs impose moderate levels of mortality (e.g., Forester 1979, Simon 1983, Kam et al 1996. Fungi and water molds pathogenic to eggs can impose selection on oviposition site choice, egg distribution (degree of clumping), and parental care behavior (Forester 1979, Kiesecker and Blaustein 1997, Green 1999. These pathogens are also implicated as a cause of amphibian population declines, in combination with environmental stresses such as low temperature and pH and high UV-B radiation that magnify the lethal effects of pathogen infections (Banks and Beebee 1988, Bellemakers and van Dam 1992, Kiesecker and Blaustein 1995.…”

Section: Introductionmentioning

confidence: 99%

Egg-Killing Fungus Induces Early Hatching of Red-Eyed Treefrog Eggs

Warkentin¹,

Currie²,

Rehner³

2001

Ecology

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Abstract. Pathogens can cause substantial mortality of amphibian eggs. If the timing of hatching is phenotypically plastic, embryos could escape from otherwise lethal infections by hatching early. We tested this with the arboreal eggs of red-eyed treefrogs, Agalychnis callidryas. A filamentous ascomycete (Dothideales: Phaeosphaeriaceae) was present on ϳ7% of egg clutches collected from a pond in the rain forest in Panama and, when present, killed 40% of the eggs, on average. Inoculation experiments confirmed that the fungus attacked and killed healthy embryos, establishing that this fungus is a pathogen of A. callidryas eggs. As predicted from life history theory, embryos hatched earlier from both naturally infected and inoculated clutches than from fungus-free control clutches. Within infected clutches, live embryos in contact with fungal hyphae hatched before those embryos not in contact with the fungus. Accelerated hatching allowed embryos to survive that otherwise would have been killed, and tadpoles hatched from infected clutches were themselves uninfected. Red-eyed treefrog embryos also hatch early if attacked by predators, apparently in response to vibratory cues. Because fungal infection provides no vibratory stimuli, embryos must respond to different cues in fungus-induced hatching than in predatorinduced hatching. The behavioral decision of when to hatch is complex and merits further investigation. Our study indicates that pathogens can influence the timing of life history transitions, as do other stage-specific risks.

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The Adaptiveness of Parental Care in Desmognathus ochrophaeus (Urodela: Plethodontidae)

Cited by 76 publications

References 12 publications

The Bacterially Produced Metabolite Violacein Is Associated with Survival of Amphibians Infected with a Lethal Fungus

The Bacterially Produced Metabolite Violacein Is Associated with Survival of Amphibians Infected with a Lethal Fungus

Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders

Egg-Killing Fungus Induces Early Hatching of Red-Eyed Treefrog Eggs

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