Co-Infection by Chytrid Fungus and Ranaviruses in Wild and Harvested Frogs in the Tropical Andes.

Robin W Warne,Vance T Vredenburg,Brandon Labumbard,Alessandro Catenazzi,Seth Lagrange

doi:10.1371/journal.pone.0145864

Abstract

While global amphibian declines are associated with the spread of Batrachochytrium dendrobatidis (Bd), undetected concurrent co-infection by other pathogens may be little recognized threats to amphibians. Emerging viruses in the genus Ranavirus (Rv) also cause die-offs of amphibians and other ectotherms, but the extent of their distribution globally, or how co-infections with Bd impact amphibians are poorly understood. We provide the first report of Bd and Rv co-infection in South America, and the first report of Rv infections in the amphibian biodiversity hotspot of the Peruvian Andes, where Bd is associated with extinctions. Using these data, we tested the hypothesis that Bd or Rv parasites facilitate co-infection, as assessed by parasite abundance or infection intensity within individual adult frogs. Co-infection occurred in 30% of stream-dwelling frogs; 65% were infected by Bd and 40% by Rv. Among terrestrial, direct-developing Pristimantis frogs 40% were infected by Bd, 35% by Rv, and 20% co-infected. In Telmatobius frogs harvested for the live-trade 49% were co-infected, 92% were infected by Bd, and 53% by Rv. Median Bd and Rv loads were similar in both wild (Bd = 101.2 Ze, Rv = 102.3 viral copies) and harvested frogs (Bd = 103.1 Ze, Rv = 102.7 viral copies). While neither parasite abundance nor infection intensity were associated with co-infection patterns in adults, these data did not include the most susceptible larval and metamorphic life stages. These findings suggest Rv distribution is global and that co-infection among these parasites may be common. These results raise conservation concerns, but greater testing is necessary to determine if parasite interactions increase amphibian vulnerability to secondary infections across differing life stages, and constitute a previously undetected threat to declining populations. Greater surveillance of parasite interactions may increase our capacity to contain and mitigate the impacts of these and other wildlife diseases.

Highlights

Emerging infectious diseases are threatening biodiversity [1]
Batrachochytrium dendrobatidis (Bd) infection intensity ranged from 101 to 106 zoospore equivalents. 58% of individuals had Bd infection intensity values above 1,000 zoospore equivalents and 24% were above the 10,000 zoospore threshold that is often associated with a high likelihood of mortality [6, 54] (Fig 2A)
There was no association between Bd and Rv infection intensity among co-infected Telmatobius frogs (r = 0.22, P = 0.17, n = 39)

Summary

Introduction

The recent emergence of the chytrid fungus Batrachochytrium dendrobatidis (Bd) is linked to extirpations and even extinctions of amphibians globally; especially in Central America [2, 3], the tropical Andes [4, 5], the western US [6] and Australia [7]. Bd and Rv have been reported to co-occur in varied habitats [15, 16], and to co-infect individual hosts [13]. Beyond these reports, little is known about the prevalence of ranaviruses in other regions of high amphibian biodiversity, the extent to which Bd and Rv coinfect amphibians, modes of disease spread, or the threat that any such co-infections present for amphibians.

Methods

Results

Conclusion