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Over the past century, conservationists have become more effective in sounding the alarm about species at risk of extinction. However, some groups, such as fungi, remain understudied, and the level of risk they face is unknown.

This isn’t because fungi are insignificant; according to the , fungi are important contributors to soil health and soil carbon sequestration, or the process of removing carbon dioxide from the atmosphere and storing it in soil. However, because so many fungi are poorly studied, the full extent of their contributions to global ecosystems remains unknown.

���񱦵� scientist Alisha Quandt and her research colleagues argue for the importance of closing taxonomical knowledge gaps related to fungi.

The importance of closing these gaps in taxonomical knowledge, or knowledge from the field of science concerned with the classification of organisms, are by C. Alisha Quandt and Danny Haelewaters of the ���񱦵� Department of Ecology and Evolutionary Biology, as well as colleagues from several European institutions.

In the study, Laboulbeniomycetes, a taxonomic class of fungi that either parasitize arthropods or use them for dispersal, represent fungi and understudied taxa generally.

Knowing what we don’t know

While there will always be some things that scientists don’t know, taking stock of knowledge gaps, or “shortfalls,” is necessary to correct these blind spots and avoid unjustified certainty. To this end, Quandt and her co-researchers created a list of gaps in ecological knowledge, specifically those that can hinder conservation efforts. These four types of gaps are the Linnean, Wallacean, Latimerian, and Scottian shortfalls.

The Linnean shortfall, named after Carl Linnaeus, father of modern taxonomy, is the difference between the number of species that exist and those that scientists have described, Quandt says. While many species of macro-organisms, and some groups in particular (such as birds) have been discovered and described, this is not true of micro-organisms and groups like fungi. As to the shortfall’s significance for conservation, Quandt continues, species that are unknown cannot be conserved.

The Wallacean shortfall, named after Alfred Russel Wallace, a biologist who was an early proponent of the theory of evolution, has to do with incomplete information on species’ geographical distribution, according to Quandt. “The example from our paper is a species of Herpomyces [a genus of fungi] that we know from the Northeast, Panama and an area in eastern Africa.” Since these places are distant and apparently unrelated, it is unlikely that this species occurs only in those places.

The Latimerian shortfall, named after Marjorie Courtenay-Latimer, a naturalist who rediscovered a supposedly long-extinct fish, is expressed as the number of species in a taxonomic group that may or may not be extinct, “because they haven't been seen or recorded officially, or even unofficially in some cases, for 50 or more years,” Quandt says. Fifty years may seem like a long time for an existing species to go unobserved, but the fish Latimer documented was thought to have been extinct since the discovery of its fossils in the prior century.

Finally, the Scottian shortfall, named after Sir Peter Markham Scott, founder of the International Union for Conservation of Nature (IUCN)  of Threatened Species, is the difference between the number of described species in higher taxonomic groups (e.g., kingdom, phylum, class) and the number that have been assigned an IUCN classification. The IUCN is a global authority on the conservation status of various species, particularly via its Red List.

Why are some taxa understudied?

Laboulbeniales parasitic fungi growing on a Harmonia axyridis, or Asian ladybug. (Photo: ) 

There are several characteristics that make members of particular taxonomic groups difficult to study—they are often relatively uncommon, microscopic, lack distinctive form or do not grow in culture.

“There is a bias for scientists in general to describe things that are really common,” Quandt says. “So, things that many people are encountering on a regular basis get described sooner than rare taxa that you don't encounter that often.”

Of course, size plays into this, as does the lack of morphological traits: organisms the size of Laboulbeniomycetes will tend to go unnoticed even when they are encountered. For example, a fly agaric mushroom can be easily identified by its distinctive red-and-white cap, but the same is not true for the microscopic Laboulbeniomycetes.

The ability to grow cells in a cell culture—an artificial environment outside of a living organism—is similarly important, as it allows researchers to both manipulate and define the environment in which cells develop. This makes things that grow in culture easier to describe, Quandt says.

Another potential issue in poorly described taxa that Laboulbeniomycetes exemplifies is cryptic speciation. Cryptic speciation is when a new species forms without any traits that are clearly different from other species’.

Quandt gives an example: “The (study’s) first author, my former postdoc Danny Haelewaters, worked on one ladybug-associated taxon that people thought was one species because, morphologically, it looked like one thing; but when he was able to get samples from all over the globe, he used genetic data to separate them into separate clades, which he is now describing formally as individual species.”

There were morphological differences between the species, including size variation in some of their cells, but that sort of thing can be easily missed.

Knowledge shortfalls in Laboulbeniomycetes

In looking for the Linnean shortfall for Laboulbeniomycetes, the researchers first tried to use the class’ discovery curve data. Ideally, a discovery curve  represents the gradually increasing number of discovered species within a group. However, this approach produced unrealistic results, likely because the species discovery curve data for Laboulbeniomycetes is flawed, as is typical in poorly studied taxa.

Laboulbeniales parasitic fungi growing on a Scaphidium quadrimaculatum, or shining fungus beetle. (Photo: )

“One of the reasons that it's misleading for poorly studied taxa is because there are different rates of study for these groups,” Quandt says. For instance, certain specialist taxonomists may contribute significantly to the known number of species in a short time, creating a rapid increase in discoveries after several decades of little progress.

This “skewed specialist effect” isn’t the only problem with discovery curves of understudied taxa though, Quandt continues, since a species can become popular and receive a lot of study from different labs around the world. “This is like something my lab is working on: describing some new species related to the fungus that causes White Nose Syndrome of bats. Because that was just discovered in 2009, there has just been this exponential rise in the number of people studying it.”

So, while the lack of solid discovery curve data prevents a certain estimate of the Linnean shortfall, this proves the difficulty of creating conservation strategies for members of understudied taxa, as such strategies cannot be effectively applied to species that have not been found.

To examine the Wallacean shortfall, the researchers created a heatmap of reports of Laboulbeniomycetes species. This heatmap showed that the highest reported diversity existed in the United States, with several other unconnected hotspots around the world. Quandt says that this is likely the result of the geographical bias in field work and taxonomy toward North America and the northern hemisphere generally.

For example, many countries that have been characterized as megadiverse, such as Colombia and the Democratic Republic of the Congo, report very few species, and many in the southern hemisphere report zero. However, the presence of a single species in distant places without reports from intervening countries (e.g., Guatemala, Spain and Ukraine, but not in between) suggests a significant Wallacean shortfall.

This shortfall makes it hard to estimate a species’ range size, which is a major consideration in conservation assessments such as the Red List. It also interferes with the use of species distribution models, which are similarly important for conservation efforts targeting rare species.

The Latimerian shortfall for Laboulbeniomycetes was determined using species description dates and published records of species sightings. The researchers found that at least 71% of Laboulbeniomycetes species were not reliably observed after their initial description, and the last reliable observation was 50 or more years ago for 51% of species, compared to 1.7–3% for land-dwelling vertebrates.

The number of species that have not been seen for a long time is an issue for conservationists because it means that it is unknown whether these species are in danger of extinction or have already gone extinct.

As to the Scottian shortfall, not a single species of Laboulbeniomycetes has been assessed for the Red List. While less than 100%, the Scottian shortfall for all fungi is pronounced too, Quandt says, as “at the time we wrote this paper, there were only 625 Red List assessments for all fungi,” compared to 150,000 described fungal species, which is likely a vast underrepresentation .

Stigmatomyces scaptomyzae fungi, a species of Laboulbeniomycetes, on a vinegar fly. (Photo: )

This is important because the Red List is a significant tool for conservationists and, Quandt says, it is difficult to act to conserve a species if it hasn’t been assessed for its Red List status.

Addressing knowledge shortfalls

All of this raises the question of how gaps in scientists’ knowledge of microscopic and otherwise difficult-to-study species like Laboulbeniomycetes can be filled. Quandt and her research colleagues say that emerging technologies and trends in scientific data collection may help, and list several examples: DNA metabarcoding, environmental DNA analysis and citizen science.

“DNA metabarcoding is a way to use a barcode, which is a section of the DNA that is unique to a specific species, and sequence those regions of the DNA for all the organisms in that DNA sample,” Quandt explains. “So, if I took a gram of soil, and I extracted all the DNA from that soil, I could use the barcode to see which species of fungi are in that one gram of soil.”

Environmental DNA analysis is very similar, she continues, as it is also DNA that is sequenced from the environment. That “could be a gram of soil, it could be a leaf; but it's DNA that is not from a pure culture that we have in the lab, or from a fruiting body like a mushroom. It's a whole community of DNA from some environment.”

Both technologies could be useful for surveying understudied taxa, as their presence may not be immediately apparent but would show up in DNA analysis of soil or other places where they live.

Citizen science is a movement in which regular people help scientists by contributing data, Quandt says. One example of a citizen science platform is , whose website says that every user observation “can contribute to biodiversity science,” and that findings will be shared with a data infrastructure organization “to help scientists find and use your data.”

The data provided by citizen scientists are generally useful, but in particular might help correct the Wallacean and Latimerian shortfalls—at least in more easily observable species—as more people looking will yield more sightings, and these can be used to fill out information about a species’ geographical distribution and/or reduce uncertainty about whether it has gone extinct.

Most importantly, Quandt continues, “we're at an important moment in the fungal conservation movement. There's a lot of momentum right now, among my colleagues, to start pushing fungal conservation forward, and that's really different than when I started in the field 15 or more years ago.

“The big take home from this paper that we wrote is that we need to be mindful, as we have all this momentum towards trying to help push fungal conservation, that we don't leave behind some of these groups that are already understudied, and that we try to bring them in and help conserve them, and think about their conservation status, and also keep them in mind when we're talking about fungal conservation as a whole.”

Researchers Thomas Matthews, Joseph Wayman, Jonathan Cazabonne, Felix Heyman and Thomas Martin also contributed to this study.

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