A fungal disease that has killed amphibians worldwide may be spreading by making the mating calls of infected males more attractive to females. The finding—one of the first—to show that the pathogen can alter a species’s reproductive behavior could explain why frogs and related animals continue to disappear across the globe.
“If true—that the fungus is manipulating individuals’ behaviors to facilitate its spread—then this is extraordinary,” says Michael Ryan, a herpetologist at the University of Texas, Austin, who was not involved in the study.
The pathogenic fungus, Batrachochytrium dendrobatidis (Bd), causes chytridiomycosis (also known as chytrid fungus disease, which kills amphibians by destroying their skin, disrupting their immune systems, and causing heart failure). Scientists first recognized its lethal effects in the 1990s when numerous species of frogs in Australia and Central and South America experienced massive die-offs; a related fungus attacks salamanders. Bd has been blamed for the extinction of hundreds of amphibian species, and poses a threat to up to one-third of the world’s frogs, salamanders, and other amphibians. There is no cure, but some frog species infected with the fungus are able to survive for years, indicating that they’ve adapted to the disease. Indeed, a recent study showed that Bd has been evolving with amphibians for some 40,000 years, although some species have only recently encountered it.
But even amphibian populations adapted to Bd continue to suffer and decline from its effects, says Bruce Waldman, a behavioral ecologist at Seoul National University and one of the authors of the new paper. “Some people think that amphibian populations are declining primarily due to catastrophic die-offs caused by Bd,” he says. “But the story is much more complicated than that.”
To find out how Bd affects a frog species that appears to be tolerant of the pathogen, Waldman and his student Deuknam An (the study’s lead author, who died shortly after completing the study), studied Japanese tree frogs (Hyla japonica) in the wild. This species, which is found in eastern and central Asia, the Koreas, and Japan, has not been reported dying en mass from Bd even though individuals get infected.
An and Waldman studied the mating calls of 42 male Japanese tree frogs. They recorded the animals during their breeding season from June to mid-August 2011 in rice paddies in South Korea. The calls are composed of a train of pulsing notes. (Listen to a normal call, below.)
The scientists analyzed the calls for such things as the number of pulses per note, the repetition rate of the pulses, the number of notes, and the call’s duration.
Only nine of the frogs tested positive for Bd. These males were slightly larger than uninfected males (40.17 versus 39.24 mm), the team reports today in Biology Letters, and they exerted more effort when calling than their healthy counterparts, producing faster and longer calls—traits female frogs are known to prefer. (Listen to the call of a Bd-infected male, below.)
Curiously, frogs infected with Bd become lethargic, Ryan notes. “Therefore one would expect the amount of calling to be lower in infected males. But this is not what the study found—and that’s very surprising.” It suggests, he adds, that Bd can act like a parasite and turn its host into a zombie.
Those zombie males may be spreading Bd in the population by attracting more females that in turn become infected and then pass on to their offspring the males’ susceptibility to the disease, the study’s authors say. (They do not yet know the mechanism Bd uses to change the host’s behavior.) Or, the scientists point out, selection may be acting on the infected males, which because of their shortened lifespans, may be increasing their calls in order to reproduce earlier. Either way, the disease ends up enhancing an individual’s reproductive success while harming the population.
And that means that “Bd has an impact on frog populations even when we don’t see outbreaks of chytridiomycosis,” says Cori Richards-Zawacki, a behavioral ecologist at the University of Pittsburgh in Pennsylvania, who recently found that the disease causes male leopard frogs in the lab to up their reproductive efforts. Although it might seem that a species has adapted to Bd and shows no clinical signs of the disease, she says, “in reality it’s still stressed by the infection, which is likely to take a less dramatic but still important toll on the population over time.”
Indeed, Waldman says that even if a species survives an initial die-off from the pathogen, it could still end up going extinct due to the disease’s “sublethal” effects. “Some of these populations that were hard hit are coming back, but slowly. Their populations are small, and that leaves them vulnerable to other random catastrophic events that might lead to extinction.” In which case, Bd would still have killed them off, just indirectly.
The scientists looked at only one frog species—and only one of its life history stages, Waldman also notes. “It shows that Bd continues to be an enigma.” And a far greater challenge to understand and control.