Macrofungal conservation in Canada and target species for assessment: a starting point

The ability to make informed decisions about the conservation status of an organism is premised on a clear understanding of its life history. Occasionally, we are able to observe patterns because the prevalence of one fungal species is so striking. For example, the Death Cap mushroom (Amanita phalloides) could be tracked in its invasive spread through North America because of its prolific fruiting and human interest (Pringle et al. 2009). However, most of the time, the presence of fungi is not evident even though fungi are key ecosystem players and are everywhere. The reason is that most fungal growth happens out of sight, by the mycelium embedded in its substrate (e.g., soil, wood). Seasonal, unpredictable, and ephemeral macrofungal fruiting and cryptic lifestyles make devising conservation management and monitoring systems difficult. Additionally, when mushrooms or other macrofungi fruit, mycologists cannot readily distinguish different individuals of the same species because different fruiting bodies may be arising from the same embedded network of microscopic filamentous cells. It is therefore difficult to answer basic questions key to conservation action plans such as: What is a fungal individual? How big is a fungal population?

Data-deficient species are more likely to be at risk (Bland et al. 2015). There are not nearly as many high-quality data points for fungi as for birds or plants, although their decline has been shown at least for some groups (Arnolds 1991). For most macrofungi, fruiting bodies are evanescent, and their morphology can be confusing. As a result, the vast majority of macrofungi in Canada are only known from a few collections and are incompletely sampled throughout their range, making them difficult to assess for rarity and threatened status. For example, it becomes challenging to tease apart how much of the recorded geographical distribution of a species of fungus is due to mycologists’ territories (where they live, collect, or go on holiday) rather than the geographical distributions of the fungi collected, leading to the question: Which fungi are rare and which are poorly sampled?

The lack of data is especially alarming in light of changing climatic conditions. One of the more insidious consequences of global climate change is that remote environments may be irreversibly disrupted before their baseline levels of diversity have been assessed. Without predisruption assessments of diversity, managing the recovery of these ecosystems becomes challenging or impossible, as there is no standard with which to assess the effectiveness of recovery efforts. The impacts of global climate change and other anthropogenic activities on the structure and function of fungal communities in Canada is not currently known, making it difficult to predict their effects on future landscapes. Fungi are especially sensitive to climate change (Körner 2003; Giauque and Hawkes 2013; Kivlin et al. 2013; Fernandez et al. 2017; Andrew et al. 2018a, 2018b) and atmospheric pollution, including nitrogen deposition (Treseder 2004; Lilleskov et al. 2011; Allen and Allen 2017; van Strien et al. 2018); changing or extreme weather patterns due to global warming may lead to fruiting body declines and shifts in phenology (Gange et al. 2007; Kauserud et al. 2012; Boddy et al. 2014; Gange et al. 2018).

One of the recent triumphs towards fungal conservation in Canada was the production of Wild Species 2020, in which the known status of ∼7,000 species of macrofungi was assessed and listed (wildspecies.ca/reports, available 2022). Much of the data used in the assessment came from fungaria with digital records and local mushroom club surveys, highlighting the crucial importance of these institutions and organizations in fungal conservation. A second major advance in our knowledge was the recent release of over 200,000 digitized fungal specimens from Agriculture and Agri-Food Canada’s Canadian National Mycological Herbarium, Canada’s largest collection of nonlichenized fungi, now searchable in Mycoportal.org. In the light of these major advances, as well as updates in the Canadian Species at Risk Act (Mooers et al. 2010), the meaningful integration of Indigenous knowledge (Turner 2020; Turcotte et al. 2021), and the recent interest in global fungal conservation, we present an update of the state of fungal conservation in Canada.

Driven by passion and enthusiasm, members of mycological organizations have long made crucial contributions to advancing knowledge of fungi (Watling 1998; Perry 2008; Lemelin and Fine 2013). Mushroom club members and amateur mycologists have greatly improved our collective knowledge of fungal diversity and occurrence through many activities and projects. The role of the nonprofessional mycological community initiatives has been multifold, with the overarching goal to encourage enthusiasm for fungi. Such organizations have increased awareness of the need to document fungal diversity and have prioritized the training of community members to create high-quality, vouchered observations.

Gathering field data has been part of the regular activities of mushroom clubs and organizations through organizing forays and surveys (e.g., Foray Newfoundland and Labrador, Fédération québécoise des groupes de mycologues, Mycoquébec, Pacific NorthWest Key Council). These typically annual events have resulted in the development of robust data sets on fungal biodiversity for target regions in Canada that have been used for developing valuable reference material for fungal taxonomy and biogeography (e.g., Mycoquébec.org, including the app “La Fonge du Québec”, Mushroom Expert, Bolete Filter, MatchMaker/MycoMatch, Pictorial Key to Mushrooms of the Pacific Northwest). Reference books and magazines have also been an invaluable product of community activities in Canada, for example, the exceptionally thorough “Répertoire des cortinaires du Québec” (Landry et al. 2021) or the Foray Newfoundland and Labrador journal Omphalina. Many nonprofessionals have enthusiastically embraced the use of DNA sequence data paired with morphological investigation to aid in specimen identification, especially in North America, where many species await formal taxonomic description, for example, Mycoquébec, which has contributed ∼3000 sequences obtained from public or private Quebec fungaria or through surveys of undersampled areas since 2017, or the Puget Sound Mycological Society’s Danny’s DNA discoveries (alpental.com/psms/ddd/). Through these activities nonprofessionals—often in collaboration with professional mycologists—have described and published new species in official outlets (e.g., Xerocomellus diffractus N. Siegel, C.F. Schwarz & J.L. Frank, in Frank et al. 2020; Hygrophorus canadensis Lebeuf & P.-A. Moreau, in Bellanger et al. 2021; Cortinarius amabilis Bojantchev, Ammirati & Pastorino, in Bojantchev 2015). Seattle-based architect Benjamin Woo (1923–2008) is an example of an independent mycologist who made a large contribution to our understanding of a taxonomic group. Over 30 years (1974–2007), Woo developed an expertise in the genus Russula and his collection was used to describe several new species (Hyde et al. 2017), understand the local diversity of Russula (Bazzicalupo et al. 2017), develop keys for identification of Pacific Northwest Russula species (alpental.com/psms/PNWMushrooms/PictorialKey/Russula.htm, zoology.ubc.ca/∼biodiv/mushroom/) and inform a regional book, “Mushrooms of British Columbia” (MacKinnon and Luther 2021).

Recently, iNaturalist and MushroomObserver have emerged as tools for citizen scientists to upload geotagged biodiversity observations, allowing researchers to study fungal diversity and biogeography with an unprecedented level of resolution. In Canada alone, approximately 40,000 contributors have uploaded over half a million fungal observations. There are currently ongoing projects that leverage iNaturalist data to improve the knowledge of patterns of biodiversity for select taxa such as chanterelles (Cantharellus spp., Craterellus spp.) and hedgehog mushrooms (Hydnum spp.) in New Brunswick (inaturalist.org/projects/chanterelles-and-hedgehog-mushrooms-in-new-brunswick) and in Newfoundland (inaturalist.org/projects/foray-nl-hydnum-project). These genera have been widely foraged as edible for decades, and identified as similarly looking European species, but the actual species present in Canada have only been described in the past 5 years (Thorn et al. 2017; Niskanen et al. 2018; Swenie et al. 2018), and additional undescribed taxa very likely remain to be found. Similar conservation-focused efforts are underway, such as the Rare Fungi Challenge for Northeastern North America (inaturalist.org/projects/fundis-rare-fungi-challenge-northeast), which aims to generate new observations for 20 potentially rare species of macrofungi.

Amateur mycologists have contributed to our collective knowledge of fungal species and their efforts have been used in many forms from identification keys, to fungarium collections to species assessments for Wild Species 2020 (wildspecies.ca/reports, available 2022). Community science mycological organizations will be key in the service and advancement of fungal conservation.

The most complete assessment of fungal species in Canada is the Wild Species 2020 report, which includes ∼7,000 species of macrofungi. This milestone report was produced by compiling national data from across Canada through collaboration with every provincial and territorial government in an effort to assess the status of species at both the national and subnational level. To calculate a national rank for each species, provincial and local species occurrence data were used. The species were assessed based on a rank calculator that included range extent and occurrence. Species categories are based on a system used by NatureServe, a US-based conservation organization that provides conservation tools. Their categories are already used by the regional Conservation Data Centres in Canada, and these categories are similar (but not identical) to those used by the IUCN. In the past 5 years there was a sharp uptick in the number of species assessed from 87 in the Wild Species 2015 report (CESCC 2016) to ∼7,000 in the 2020 report, a hopeful and exciting result.

For conservation lists to be effective, baseline data (taxonomic, ecological, biogeographic) need to be generated and evaluated for fungal species occurring in Canada. Taxonomic expertise, in particular, is badly needed to be able to accurately reflect which species we should prioritize for fungal conservation. A representative example is the mushroom genus Pluteus, which has been the subject of much taxonomic work in the past 10 years (e.g., Justo et al. 2014). In the current version of the Canada Wild Species 2020, three species of Pluteus are included, but none of them are confirmed to occur in North America based on current taxonomic work. On the other hand, five other species of Pluteus present in Canada (P. elaphinus, P. eos, P. leucoborealis, P. oreibatus, and P. rangifer) should be included in the Natureserve list and highly prioritized in conservation actions because of their relative rarity and endemicity to Eastern North America or the circumboreal area. Conservation efforts for macrofungi have been hampered by the lack of basic taxonomic knowledge; research funds dedicated to taxonomic research are hard to obtain. Since 2010 the Natural Sciences and Engineering Research Council of Canada has awarded only 8 small grants (less than CAN$27,000) directly related to the taxonomy or diversity of macrofungi, and none were Canada-wide in scope (nserc-crsng.gc.ca/ase-oro/index_eng.asp).

Although species of fungi occur across governmental borders, governments have different laws and priorities for their protection. Two main approaches are used for conservation implementation. Firstly, assessments can target specific habitats (e.g., Carolinian forest in Ontario and the Okanagan valley in British Columbia). Some species are likely limited to threatened habitats, for example sand dunes or old growth forests (Ruokolainen et al. 2018; Yang et al. 2021), but data are limited for threatened habitats and the species inhabiting them. One drawback of this specific approach in Canada is that it is often restricted to species that are at the edge of their northern range, making their habitat very limited. As another approach, assessment can target species endemic only to Canada or species having a large proportion of their global geographic range in Canada. It is difficult to designate a species as endemic to Canada because detailed (or even approximate) distribution data are lacking for most macrofungal species in North America. The conservation directive is that Canada becomes responsible to maintain those species in the world. The practical consequences of the “conservation directive” depends on the case that can be presented to government agencies to act upon the conservation issue. By identifying priority targets we can make the case for the species that need more urgent action. While identifying targets does not imply that other conservation measures will happen, without first identifying targets nothing will happen because there is no case to be presented.

With the recent momentum of the Canadian Institute of Ecology and Evolution’s Virtual Working Group in Fungal Conservation as well as the Canadian Fungal Research Network (CanFunNet, fungalresearch.ca, Horianopoulos et al. 2020), we aim to unite those working with macrofungi in Canada towards establishing conservation goals. In Table 1, we provide a preliminary list of fungi to be considered for formal conservation assessment, with justification. As formal frameworks can aid actionable conservation recommendations, in Fig. 1 we outline a process for assessment of Canadian macrofungi for conservation. Representative fungi from our list of potential candidate species for assessment are illustrated in Fig. 2. While by no means exhaustive, our species list is a starting point to invite a broader conversation in the Canadian mycological community to determine macrofungal conservation priorities. For example, Phaeocollybia species found in western Canada also deserve our attention as they occur in threatened old growth forests (Redhead and Norvell 1993; Kroeger and Berch 2017).