Advance of the Fungi/
Decline of the Animals

© Peter G. Werner
Original publication: Mycena News, December 2010

Biodiversity loss, and in particular the precipitous decline of several groups of animals, has been a subject that has received a great deal of attention over the last several years. Forty percent of all amphibian species worldwide are in serious decline. Many bat species in the northeastern US and perhaps elsewhere may be extinct within 20 years. Beekeeping and crop pollination is devastated in several parts of the US due to the decline of honeybees.

The role of fungi in these epidemics is also making news. It was established several years ago that a fungal pathogen played a key role in amphibian decline, but more recently, the role of fungal pathogens in the decline of bats and honeybees is being established.

Brown Bat

Little brown bat, New York. Close-up of nose with fungus.
From Ryan von Linden, NYDEC

Over the last several years, populations of the domesticated European honey bee (Apis mellifera) in North America have been devastated by colony collapse disorder (CCD). This disease manifests itself most visibly in the complete abandonment of hives by the entire population of worker bees, leaving behind the hive’s entire honeycomb food supply and an abandoned queen. This has not only had a devastating effect on commercial beekeeping in many regions, but agriculture in crops dependent on honeybees for pollination. It also has a ripple effect through the larger biological community, as honeybees in many cases have displaced native bee species, leaving many wild plants dependent on them for pollination.

So far, the known major pathogens of A. mellifera, such as Varroa mites, do not seem to play a major role in CCD. A recent investigation using proteomics, that is, mass screening of proteins found in the hives and on the bees, reveals the characteristic protein signatures of two infectious agent in all of the sampled colonies affected by CCD. One is Nosema ceranae, a pathogen in the microsporidia, a poorly-understood fungal group with an extremely reduced unicellular morphology. N. ceranae is already a known pathogen endemic infection among Asian honeybees (Apis cerana), but not seriously pathogenic. It is also not typically a serious pathogen in A. mellifera, hence unlikely to be the sole cause of CCD. However, the other pathogen that has been detected is a virus, IIV-6, and it is hypothesized that the N. ceranae and IIV-6 in combination, perhaps alongside other factors, is what is driving CCD. Further investigation is now taking place to test this hypothesis.

Bat species in the northeastern US have been similarly devastated by a mysterious epidemic, causing them to break hibernation in midwinter and then to starve to death, as their energy needs cannot be met by stored fat and the available food at that time of year. Investigation of infected colonies of bats revealed them to be infected en masse by a fungal hair and skin pathogen, know as “white-nose syndrome” (WNS), that penetrates into the living layers of skin and even muscle tissue. The WNS pathogen apparently favors the relatively low body temperatures of bats during hibernation, leading to its easy spread while they are massed together in this state.

Section

Histological section of wing membrane a bat (Myotis lucifugus) showing extensive fungal infection by G. destructans. Fungal hyphae replace muscle bundles (arrows); invasion through the skin (arrowhead). From: Cryan et al, 2010

In 2008, a group of mycologists that included Andrea Gargas and Tom Volk identified the fungus as Geomyces destructans, an asexual (“imperfect”) ascomycete species new to science. Other species of Geomyces, are known keratinophiles that break down dead skin, hair, and feathers, and several other species are widespread soil fungi.

It has been known for several years that a major cause of the decline of amphibians is a disease called chytridiomycosis, caused by a chytrid, Batrachochytrium dendrobatidis (also known as “Bd”). Chytrids are a group of relatively primitive aquatic fungi representing the form that fungi likely took at the time of their divergence from other unicellular eukaryotes. They largely exist as alternating generations of several types of free-swimming zoospores and simple microscopic fruiting bodies, often also having a mycelial phase as well. In the case of Bd, part of the life cycle takes the form of a cystlike sporangium that grows within the skin of the amphibian. A heavy infestation with these cysts can be devastating on an infected amphibian, leading to bleeding ulcers on the skin, and eventual loss of the ability to osmoregulate or even breathe. The Sierra Nevada yellow-legged frog (Rana sierrae) and a number of other frog species in the High Sierra (already threatened by the introduction of trout) have been driven down to critical levels by this disease.

These diseases are in addition to a number of plant pathogen epidemics that are ongoing or recently established, such as the spread of fusarium pitch canker in pines (including Monterey and Bishop pine), the loss of California’s tanoak and coast live oak trees to the oomycete disease sudden oak death, and more recently, the threat to ancient Rocky Mountain and Great Basin bristlecone pine forests from white pine rust.

What is driving the emergence of these devastating diseases that threaten so many species? Several factors encourage their spread. The largest factor is the sheer mobility of organisms deliberately or accidentally carried from one part of the world to another, and into host populations that lack evolved resistance. Pathogens are quite often invasive species in much the same way that more visible plant and animal invaders are. There is evidence now that Bd originated as a stable endemic organism in Southern Africa and was spread by the widespread breeding of the African clawed frog (Xenopus laevis) in new areas as a research animal and exotic pet. Similarly, a stable endemic infestation of WNS has been found in some European bat populations.

Another factor is global climate change, which opens up new regions to habitability by these invaders. There is strong evidence that this is what is taking place with Bd; in many parts of the world, water temperatures are rising to a optimal level for its growth and infectivity. Another key factor is that pathogens typically have a much greater capacity to migrate into new, more hospitable regions and away from less favorable ones than their animal and plant hosts.

The role of environmental stresses from climate change, pollution, and other factors cannot be underestimated, and it is thought that in several of these epidemics, notably in amphibian decline and in CCD in bees, that the fungal and viral pathogens are merely the coup de grace after a series of environmental blows. In the case of amphibians, there is evidence that pesticide exposure and increased UV-B levels associated with ozone depletion compromises their immune system and makes them more vulnerable to a range of pathogens. Carlos Davidson, an SFSU conservation biologists, has carried out a study correlating lower population counts of several Sierra Nevada frog and toad species in years in which increased levels of cholinesterase-inhibiting pesticides were released upwind in the San Joaquin Valley. There have also been several cases of amphibian population die-offs where chytridiomycosis has not been seen.

In the case of bees, colony malnutrition, brought about by feeding from poor food sources between pollination releases, is present in the majority of hives affected by CCD. There is also a concern that bees are being negatively affected by increased use of long-lasting neonicotinoid pesticides in areas that they pollinate.

Frog

Histological section of skin of frog (Litoria caerulea) severely infected with chytridiomycosis, from Queensland, Australia. S = sporangium. D = zoospore discharge tubes. From: Berger, et al, 1998

The loss of species and larger effects on habitat are an ongoing environmental tragedy, but not one that is utterly without hope. WNS in bats, for example, may be treatable by existing antifungal drugs. In amphibians, a group of scientists led by Reid Harris of James Madison University in Virginia has discovered a symbiotic bacterial species, Janthinobacterium lividum (“Jliv”), on the skin of resistant populations of amphibians. This bacterium produces a compound called violacein, an antifungal compound endemic to some amphibian species, but greatly enhanced when Jliv is present. One of the scientists in the group that discovered Jliv and who is now at SFSU, Vance Vredenburg, has been treating frogs from a High Sierra population of R. sierrae in a Jliv solution. So far, the treated group show a much higher survival rate than the control group.

Research is also being carried out on the population structure and dynamics of pathogens like sudden oak death and Bd. A better understanding of how they enter and spread through populations, and what makes them such effective pathogens, is critical in both controlling existing diseases and spotting potential new disease organisms before they’re spread to begin with.

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