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Fungus-Chomping Micro Predators Could Protect Amphibians from Deadly Skin Disease

Microbes that thrive in lakes happily consume the pandemic fungus that has caused declines in more than half the planet’s amphibian species
tree frog


This tree frog Hylomantis lemur (recently named Agalychnis lemur), was photographed in Cerro Azul, Panama, in 2007, before the chytrid fungus arrived. The fungus appeared at the site in 2009 and this tree frog species has likely become locally extinct. First noted when the golden toad and about half of the frog species disappeared in Monteverde reserve in Costa Rica in 1987, the killer fungus has been spreading eastward through the Central American highlands and also through a large portion of the Andes Mountains (likely from a separate introduction) ever since.
Credit: Justin C. Touchon, Smithsonian Tropical Research

In 2012 a team of temperamental donkeys picked their way down the French Pyrenees carrying a payload of voracious protists. Donkeys wouldn't ordinarily be required to ferry single-celled microbes, but these tiny organisms happened to be inhabitants of the several hundred pounds of lake water that the donkeys were also carrying, whether they liked it or not. “It's kind of funny,” says Dirk Schmeller, the scientist whose team hired the donkeys, “because it shows donkeys can help save amphibians.”
 
What makes that unlikely scenario possible is the microorganisms’ appetite for an equally minute chytrid fungus—a group of fungi with a swimming stage that resemble the ancestors of all fungi—called Batrachochytrium dendrobatidis, or Bd, which is wiping out amphibians worldwide. It turns out that a diverse collection of single-celled protists and tiny multicellular animals naturally hunt down and eat Bd in lakes, preventing the killer fungus from infecting frogs and other amphibians. Although Bd is an introduced fungus, similar fungi are abundant in lakes and a natural part of these micro predators' diets, so their ability to prey on Bd is not unexpected. What was unexpected was the gusto with which they can eat the invasive fungus in the wild. Scientists had previously shown in experimental lab containers that a few micro predators would eat swimming Bd spores, but a new study indicates that the hunt happens in real-world mountain lakes, and seems to be taking place on a scale large enough to significantly reduce amphibian infections and deaths in those lakes. Schmeller, of the Helmholtz Center for Environmental Research in Germany, and colleagues published these conclusions in January in Current Biology.
 
The promising implication is that capitalizing on native microorganisms' Bd-feasting ability could cut down the pandemic fungus enough to boost amphibian survival, without relying on the iffy introduction of foreign bacteria or deployment of ecosystem-disrupting antifungal chemicals—two methods that have been proposed. Rather, protecting amphibians may be as simple as promoting the health and survival of the microbes that already live in a lake or introducing them where they've been lost or suppressed.
 
Bd was discovered killing amphibians globally in 1997. Theories abound regarding its origin and dissemination. One popular version is that the fungus was spread primarily via the international trade in frogs used for laboratory studies and early pregnancy testing (which makes it apparent how peeing on a stick was an Earth-shattering advance).
 
Schmeller had noticed that the lakes sampled in the high Pyrenees by colleague Matthew Fisher, of Imperial College London, were generally positive for Bd, whereas those closer to him were negative. He decided to see if he could find out what might be driving the difference. He first suspected water quality, but their initial water analysis revealed little. So Schmeller and his colleagues started counting the number of predatory microorganisms in their samples. These include both active predators that seek out prey as well as filter feeders who prefer to let their dinner come to them.
 
When the team counted the number of these microorganisms in water from lakes with high and low prevalence of Bd, a striking difference leapt out: the lakes with lots of Bd were impoverished in microbial predators.
 
This wasn't enough to prove that the microbes were responsible for the scarcity of disease, however. In a series of further experiments, Schmeller and a team of colleagues in Germany, France, Belgium and the U.K. showed that introduced Bd zoospores survived far longer in water brought back (by the donkeys) from high-prevalence lakes than in water from low-prevalence lakes. They also showed that filtering water from low Bd-prevalence lakes significantly reduced its ability to kill Bd zoospores—presumably because the microbial predators had been filtered out.
 
Furthermore, tadpoles housed in Bd-spiked water from low-prevalence lakes had lower rates of infection and less severe infections than those residing in similarly spiked water from high prevalence lakes or in heat-treated (and presumably sterilized) water from low-prevalence lakes. The same effect persisted when the tadpoles were housed with individual species of a microscopic predatory animal, one of which was isolated from a Pyrenean lake.
 
The striking ability of the microorganisms to eat fungal spores and protect amphibians—and the fact that this protection did not rely on a combination of environmental factors—was a great surprise to the scientists. “We expected a reduction but not to this level,” Schmeller says, “[but] every pattern we can see in the wild can be explained by the microorganisms.”
 
It's been long known that native micro predators will target prey in the size range of Bd. What has been lacking, however, is finding out whether enough of that predation is happening to matter, says Pieter Johnson, associate professor of ecology and evolutionary biology at the University of Colorado Boulder, who has studied the role that predators of parasites and parasite alternate hosts can play in disease dynamics, but who was not involved in this study. That was something this study directly addressed, he says, and the strength of the connection between the predators and patterns of infections surprised him.
 
In principle (although such a practice requires much further testing), these results point to a simple, relatively natural solution to ponds plagued with Bd: boost native micro predator populations. This could be accomplished by maintaining the natural state of pristine lakes and preventing invasive species from getting in. In other lakes it could take the form of removing introduced species such as fishes (often stocked for anglers in mountain lakes that were originally fishless) that eat micro predators. In lakes where Bd is a problem, once the conditions that suppress micro predators have been reversed or removed, ecologists could even try lake water microbial transfusions, similar to the way fecal bacterial transplants can help reestablish ecological balance to human guts ravaged by antibiotics or infection. Because a threshold of Bd density is needed to infect any particular frog, it is probably not necessary to wipe out the fungus to protect amphibians. “In most cases its either not possible or not even practical to really try to eradicate disease from a system,” Johnson says. “But if you can figure out ways to manage the system that actually keep disease levels at some desirably low level, then that could actually be a really cost-effective way to approach certain diseases.”
 
Andrew Blaustein, a professor of integrative biology at Oregon State University who has also studied micro predators’ effect on Bd and their possible use as a biocontrol agent (and was not involved in this study), agreed that the paper study was both well conducted and groundbreaking in its probing of complex, real-world lake communities.
 
In retrospect, Blaustein says, past difficulties with experimental ponds that were stocked with zooplankton (which include many micro predators) Bd and amphibians could have offered a clue to the tiny predators' surprising lethality. In these artificial environments it has traditionally been hard to build up sufficient quantities of Bd for experiments. The reason, he said, may be that the micro predators were so good at eating it.

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