Richard Speare

Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs

The global emergence and spread of the pathogenic, virulent, and highly transmissible fungus Batrachochytrium dendrobatidis, resulting in the disease chytridiomycosis, has caused the decline or extinction of up to about 200 species of frogs. Key postulates for this theory have been completely or partially fulfilled. In the absence of supportive evidence for alternative theories despite decades of research, it is important for the scientific community and conservation agencies to recognize and manage the threat of chytridiomycosis to remaining species of frogs, especially those that are naive to the pathogen. The impact of chytridiomycosis on frogs is the most spectacular loss of vertebrate biodiversity due to disease in recorded history.

Emerging infectious diseases and amphibian population declines.

We review recent research on the pathology, ecology, and biogeography of two emerging infectious wildlife diseases, chytridiomycosis and ranaviral disease, in the context of host-parasite population biology. We examine the role of these diseases in the global decline of amphibian populations and propose hypotheses for the origins and impact of these panzootics. Finally, we discuss emerging infectious diseases as a global threat to wildlife populations.

Origin of the Amphibian Chytrid Fungus

Histologic evidence indicates southern Africa as the origin of the amphibian chytrid fungus.

Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines.

Croaking Frogs The global amphibian decline has been attributed, among other causes, to an amphibian skin disease chytridiomycosis caused by the fungus Batrachochytrium dendrobatidis. However, how this pathogen causes mortality has been unclear. Voyles et al. (p. 582) show that this superficial skin infection may lead to cardiac failure owing to changes caused by lowered ion transport through the skin and consequent electrolyte reduction in the blood. A fungal disease that is associated with frog mortality causes changes in electrolyte transport across the skin. The pathogen Batrachochytrium dendrobatidis (Bd), which causes the skin disease chytridiomycosis, is one of the few highly virulent fungi in vertebrates and has been implicated in worldwide amphibian declines. However, the mechanism by which Bd causes death has not been determined. We show that Bd infection is associated with pathophysiological changes that lead to mortality in green tree frogs (Litoria caerulea). In diseased individuals, electrolyte transport across the epidermis was inhibited by >50%, plasma sodium and potassium concentrations were respectively reduced by ~20% and ~50%, and asystolic cardiac arrest resulted in death. Because the skin is critical in maintaining amphibian homeostasis, disruption to cutaneous function may be the mechanism by which Bd produces morbidity and mortality across a wide range of phylogenetically distant amphibian taxa.

Endemic infection of the amphibian chytrid fungus in a frog community post-decline

The chytrid fungus Batrachochytrium dendrobatidis has been implicated in the decline and extinction of numerous frog species worldwide. In Queensland, Australia, it has been proposed as the cause of the decline or apparent extinction of at least 14 high-elevation rainforest frog species. One of these, Taudactylus eungellensis, disappeared from rainforest streams in Eungella National Park in 1985–1986, but a few remnant populations were subsequently discovered. Here, we report the analysis of B. dendrobatidis infections in toe tips of T. eungellensis and sympatric species collected in a mark-recapture study between 1994 and 1998. This longitudinal study of the fungus in individually marked frogs sheds new light on the effect of this threatening infectious process in field, as distinct from laboratory, conditions. We found a seasonal peak of infection in the cooler months, with no evidence of interannual variation. The overall prevalence of infection was 18% in T. eungellensis and 28% in Litoria wilcoxii/jungguy, a sympatric frog that appeared not to decline in 1985–1986. No infection was found in any of the other sympatric species. Most importantly, we found no consistent evidence of lower survival in T. eungellensis that were infected at the time of first capture, compared with uninfected individuals. These results refute the hypothesis that remnant populations of T. eungellensis recovered after a B. dendrobatidis epidemic because the pathogen had disappeared. They show that populations of T. eungellensis now persist with stable, endemic infections of B. dendrobatidis.

Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications.

Amphibian chytridiomycosis is an emerging infectious disease of amphibians thought to be moved between countries by trade in infected amphibians. The causative fungus, Batrachochytrium dendrobatidis, produces aquatic, motile zoospores; infections have been achieved in experiments by exposing amphibians to water containing zoospores. However, the ability of this fungus to survive in the environment in the absence of an amphibian host is unknown. We show that B. dendrobatidis will survive in tap water and in deionized water for 3 and 4 weeks, respectively. In lake water, infectivity was observed for 7 weeks after introduction. The knowledge that water can remain infective for up to 7 weeks is important for the formulation of disease control and quarantine strategies for the management of water that has been in contact with amphibians.

A proof of concept study establishing Necator americanus in Crohn’s patients and reservoir donors

The emergence of autoimmunity, including Crohn’s disease (CD) where the immune relationship with commensal bacteria is corrupted, has been linked to hygiene.1,2 A gradual decline in endoparasites is but one argument that might explain this phenomenon.3 Weinstock and colleagues have successfully tested the pig whipworm, Trichuris suis , in patients with inflammatory bowel disease (IBD).4,5 However, repeated inoculation was required and concern has been raised that aberrant migration could occur.6 The haematophagous hookworm, Necator americanus (NA), is proposed as an alternative. We have tested if CD patients tolerate hookworm infection, and the practical issues associated with establishing reservoir donors (RDs). Over 700 million people remain infected with hookworms. Infective larvae (L3i) are acquired through skin contact with contaminated soil.7 Auto-reinfection, direct person to person infection, aberrant migration, and hypobiosis do not occur. Adult worms live …

Sun exposure and melanocytic naevi in young Australian children

Queensland, Australia, has the highest rates of melanoma in the world and Queensland children have the greatest numbers of melanocytic naevi, the strongest risk factor for melanoma. Although both melanoma and naevi are broadly related to sun exposure in childhood, the relation to individual exposure early in life is difficult to study retrospectively in adults. We surveyed 506 children aged 1-6 years who had been born in Townsville, North Queensland. Sun exposure was assessed by questionnaire and melanocytic naevi were counted using a standard international protocol. Very high counts (upper quarter) of melanocytic naevi were significantly associated with sun exposure of more than 4 hours per day (adjusted relative risk ratio 3.29; 95% Cl 1.12-9.69), and with a history of sunburn (1.89; 1.11-3.21). Melanocytic naevus counts increased with age, light skin reflectance, and freckling. With exposure to intense ultraviolet light in Townsville, children develop melanocytic naevi early in life and in large numbers. We found that both acute and chronic exposure to sun are associated with their development.

The Decline of the Sharp-Snouted Day Frog (Taudactylus acutirostris): The First Documented Case of Extinction by Infection in a Free-Ranging Wildlife Species?

Infectious diseases are increasingly recognized as the cause of mass mortality events, population declines, and the local extirpation of wildlife species. In a number of cases, it has been hypothesized that pathogens have caused species extinctions in wildlife. However, there is only one definitively proven case of extinction by infection, and this was in a remnant captive population of a Polynesian tree snail. In this article, we review the potential involvement of infectious disease in the recent extinction of the sharp-snouted day frog Taudactylus acutirostris. Our review of available evidence suggests that a virulent pathogen of amphibians, Batrachochytrium dendrobatidis, caused a rapid, catastrophic decline of this species, from which it did not recover. We propose that this is the first case of extinction by infection of a free-ranging wildlife species where disease acted as both the proximate and ultimate cause of extinction. This highlights a probable underreporting of infectious disease as a cause of biodiversity loss historically and currently.

Effect of Hookworm Infection on Wheat Challenge in Celiac Disease – A Randomised Double-Blinded Placebo Controlled Trial

Background and Aims The association between hygiene and prevalence of autoimmune disease has been attributed in part to enteric helminth infection. A pilot study of experimental infection with the hookworm Necator americanus was undertaken among a group of otherwise healthy people with celiac disease to test the potential of the helminth to suppress the immunopathology induced by gluten. Methods In a 21-week, double-blinded, placebo-controlled study, we explored the effects of N. americanus infection in 20 healthy, helminth-naïve adults with celiac disease well controlled by diet. Staged cutaneous inoculations with 10 and 5 infective 3rd stage hookworm larvae or placebo were performed at week-0 and -12 respectively. At week-20, a five day oral wheat challenge equivalent to 16 grams of gluten per day was undertaken. Primary outcomes included duodenal Marsh score and quantification of the immunodominant α-gliadin peptide (QE65)-specific systemic interferon-γ-producing cells by ELISpot pre- and post-wheat challenge. Results Enteric colonisation with hookworm established in all 10 cases, resulting in transiently painful enteritis in 5. Chronic infection was asymptomatic, with no effect on hemoglobin levels. Although some duodenal eosinophilia was apparent, hookworm-infected mucosa retained a healthy appearance. In both groups, wheat challenge caused deterioration in both primary and several secondary outcomes. Conclusions Experimental N. americanus infection proved to be safe and enabled testing its effect on a range of measures of the human autoimmune response. Infection imposed no obvious benefit on pathology. Trial Registration ClinicalTrials.gov NCT00671138