An official website of the United States government
The amphibian chytrid fungus, Batrachochytrium salamandrivorans ( Bsal ) threatens salamander biodiversity. The factors underlying Bsal susceptibility may include glucocorticoid hormones (GCs). The effects of GCs on immunity and disease susceptibility are well studied in mammals, but less is known in other groups, including salamanders. We used Notophthalmus viridescens (eastern newts) to test the hypothesis that GCs modulate salamander immunity. We first determined the dose required to elevate corticosterone (CORT; primary GC in amphibians) to physiologically relevant levels. We then measured immunity (neutrophil lymphocyte ratios, plasma bacterial killing ability (BKA), skin microbiome, splenocytes, melanomacrophage centres (MMCs)) and overall health in newts following treatment with CORT or an oil vehicle control. Treatments were repeated for a short (two treatments over 5 days) or long (18 treatments over 26 days) time period. Contrary to our predictions, most immune and health parameters were similar for CORT and oil-treated newts. Surprisingly, differences in BKA, skin microbiome and MMCs were observed between newts subjected to short- and long-term treatments, regardless of treatment type (CORT, oil vehicle). Taken together, CORT does not appear to be a major factor contributing to immunity in eastern newts, although more studies examining additional immune factors are necessary. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.
more »
« less
Dermal glucocorticoids are uncoupled from stress physiology and infection
Abstract Ongoing amphibian population declines are caused by factors such as climate change, habitat destruction, pollution and infectious diseases not limited to chytridiomycosis. Unfortunately, action is taken against these factors once population collapses are underway. To avoid these post hoc responses, wildlife endocrinology aims to analyse physiological mediators that predict future population declines to inform wildlife management. Mediators typically investigated are stress hormones known as glucocorticoids, which are produced by the Hypothalamus—Pituitary—Interrenal axis (HPI axis). The HPI axis is the part of the endocrine system that helps amphibians cope with stress. Chronic increases in glucocorticoids due to stress can lead to immune dysfunction, which makes amphibians more susceptible to infectious diseases. Despite this predictive potential of glucocorticoids, interpretation of glucocorticoid data is confounded by sampling design and type. Glucocorticoid monitoring classically involves blood sampling, which is not widely applicable in amphibians as some are too small or delicate to sample, and repeated samples are often valued. To address this, we tried to validate skin swabbing via corticosterone (CORT) and adrenocorticotropin hormone (ACTH) injections in adults of two amphibian species: Eastern red-spotted newts, Notophthalmus viridescens viridescens, with natural skin infections with Batrachochytrium dendrobatidis (Bd) upon collection in the field, and Northern leopard frogs, Rana (Lithobates) pipiens, raised in captivity and naïve to Bd exposure. Further, we determined the predictive potential of skin glucocorticoids on Bd load in the field via correlations in Eastern red-spotted newts. We found that hormones present in the skin are not related to the HPI axis and poorly predict infection load; however, skin hormone levels strongly predicted survival in captivity. Although skin swabbing is not a valid method to monitor HPI axis function in these species, the hormones present in the skin still play important roles in organismal physiology under stressful conditions relevant to wildlife managers.
more »
« less
- PAR ID:
- 10572659
- Editor(s):
- Porteus, Cosima
- Publisher / Repository:
- Oxford Academic
- Date Published:
- Journal Name:
- Conservation Physiology
- Volume:
- 13
- Issue:
- 1
- ISSN:
- 2051-1434
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Invasive fish predators are an important factor causing amphibian declines and may have direct and indirect effects on amphibian survival. For example, early non-lethal exposure to these stressors may reduce survival in later life stages, especially in biphasic species. In amphibians, the glucocorticoid hormone corticosterone is released by the hypothalamo–pituitary–interrenal axis (HPI), as an adaptive physiological response to environmental stressors. The corticosterone response (baseline and response to acute stressors) is highly flexible and context dependent, and this variation can allow individuals to alter their phenotype and behavior with environmental changes, ultimately increasing survival. We sampled larvae of the spring salamander (Gyrinophilus porphyriticus) from two streams that each contained predatory brook trout (Slavelinus fontinalis) in the lower reaches and no predatory brook trout in the upper reaches. We measured baseline and stress-induced corticosterone release rates of larvae from the lower and upper reaches using a non-invasive water-borne hormone assay. We hypothesized that corticosterone release rates would differ between larvae from fish-present reaches and larvae from fish-free reaches. We found that baseline and stressor-induced corticosterone release rates were downregulated in larvae from reaches with fish predators. These results indicate that individuals from reaches with predatory trout are responding to fish predators by downregulating corticosterone while maintaining an active HPI axis. This may allow larvae more time to grow before metamorphosing, while also allowing them to physiologically respond to novel stressors. However, prolonged downregulation of corticosterone release rates can impact growth in post-metamorphic individuals.more » « less
-
Synopsis Emerging infectious diseases have been of particular interest as a major threat to global biodiversity. In amphibians, two fungal sister taxa, Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal), along with the viral pathogen ranavirus, have affected global populations. Factors such as host traits, abiotic and biotic environmental conditions, and pathogen prevalence contribute to species-specific disease susceptibility. The eastern United States is home to the Appalachian Mountain system, known as a “hotspot” for salamander biodiversity. Bd and ranavirus are present throughout the Appalachians, and a Bsal emergence could be imminent. Throughout the Appalachians are the spotted salamanders, Ambystoma maculatum, a mostly terrestrial salamander that participates in mass breeding migration to ponds and vernal pools in the late spring. Previous experimental studies have shown that spotted salamanders appear to be resistant to Bd and Bsal infection, but the mechanisms behind Bd defense remain unknown. Spotted salamanders emerging from their overwintering habitats were hypothesized to have potent anti-Bd function expressed in their mucus and in their skin microbiomes, as a countermeasure to annual Bd re-emergence. We used non-invasive sampling at two pools during the spotted salamander annual breeding event to (I) determine pathogen prevalence, (II) quantify the antifungal potential of salamander skin mucus, and (III) characterize the diversity and composition of the salamander skin microbiome and contrast it to that of the corresponding environmental microbiome. We did not detect any Bd, Bsal, or ranavirus in the salamanders. The salamander mucus did not inhibit Bd growth in vitro, and anti-Bd bacteria were at low relative abundance in the microbiome. The salamander microbiome sourced a proportion of bacteria from the environment and appeared to select rare taxa from their respective pools; however, their functional relevance in pathogen defense is unclear. Our results suggest that the spotted salamander mucosal secretions and skin microbiome are not the mechanisms of defense against Bd. Rather, elements not captured by the mucosome (e.g., immune cell gene expression) may confer resistance. This study contributes to the understanding of salamander intraspecies variation in disease susceptibility.more » « less
-
Reguera, Gemma (Ed.)ABSTRACT Mucosal defenses are crucial in animals for protection against pathogens and predators. Host defense peptides (antimicrobial peptides, AMPs) as well as skin-associated microbes are key components of mucosal immunity, particularly in amphibians. We integrate microbiology, molecular biology, network-thinking, and proteomics to understand how host and microbially derived products on amphibian skin (referred to as the mucosome) serve as pathogen defenses. We studied defense mechanisms against chytrid pathogens, Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal), in four salamander species with different Batrachochytrium susceptibilities. Bd infection was quantified using qPCR, mucosome function (i.e., ability to kill Bd or Bsal zoospores in vitro ), skin bacterial communities using 16S rRNA gene amplicon sequencing, and the role of Bd-inhibitory bacteria in microbial networks across all species. We explored the presence of candidate-AMPs in eastern newts and red-backed salamanders. Eastern newts had the highest Bd prevalence and mucosome function, while red-back salamanders had the lowest Bd prevalence and mucosome function, and two-lined salamanders and seal salamanders were intermediates. Salamanders with highest Bd infection intensity showed greater mucosome function. Bd infection prevalence significantly decreased as putative Bd-inhibitory bacterial richness and relative abundance increased on hosts. In co-occurrence networks, some putative Bd-inhibitory bacteria were found as hub-taxa, with red-backs having the highest proportion of protective hubs and positive associations related to putative Bd-inhibitory hub bacteria. We found more AMP candidates on salamanders with lower Bd susceptibility. These findings suggest that salamanders possess distinct innate mechanisms that affect chytrid fungi. IMPORTANCE How host mucosal defenses interact, and influence disease outcome is critical in understanding host defenses against pathogens. A more detailed understanding is needed of the interactions between the host and the functioning of its mucosal defenses in pathogen defense. This study investigates the variability of chytrid susceptibility in salamanders and the innate defenses each species possesses to mediate pathogens, thus advancing the knowledge toward a deeper understanding of the microbial ecology of skin-associated bacteria and contributing to the development of bioaugmentation strategies to mediate pathogen infection and disease. This study improves the understanding of complex immune defense mechanisms in salamanders and highlights the potential role of the mucosome to reduce the probability of Bd disease development and that putative protective bacteria may reduce likelihood of Bd infecting skin.more » « less
-
null (Ed.)Transmission is the fundamental process whereby pathogens infect their hosts and spread through populations, and can be characterized using mathematical functions. The functional form of transmission for emerging pathogens can determine pathogen impacts on host populations and can inform the efficacy of disease management strategies. By directly measuring transmission between infected and susceptible adult eastern newts (Notophthalmus viridescens) in aquatic mesocosms, we identified the most plausible transmission function for the emerging amphibian fungal pathogen Batrachochytrium salamandrivorans (Bsal). Although we considered a range of possible transmission functions, we found that Bsal transmission was best explained by pure frequency dependence. We observed that >90% of susceptible newts became infected within 17 days post-exposure to an infected newt across a range of host densities and initial infection prevalence treatments. Under these conditions, we estimated R_0 = 4.9 for Bsal in an eastern newt population. Our results suggest that Bsal has the capability of driving eastern newt populations to extinction and that managing host density may not be an effective management strategy. Intervention strategies that prevent Bsal introduction or increase host resistance or tolerance to infection may be more effective. Our results add to the growing empirical evidence that transmission of wildlife pathogens can saturate and be functionally frequency-dependent.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/conphys/coaf005
