A call to include fungi in wildlife trade research and policy

Abstract

Fungi, essential for ecosystem functions such as nutrient recycling and carbon sequestration, also play a crucial role in forest responses to climate change and provide medicines and food globally (Antonelli et al., 2019; Boa, 2004; Gonçalves et al., 2021; Pennisi & Cornwall, 2020). Moreover, fungi provide key livelihoods and are potentially a sustainable resource because they can be harvested in ways that align with conservation and development goals (Oyanedel et al., 2022). For the last 15 years, the importance of fungi has been recognized in policy, conservation, and research (Cao et al., 2021; Pérez-Moreno et al., 2021). For instance, the International Union for Conservation of Nature (IUCN) recently ramped up assessment of fungi to address the scarce number of fungal species that have been assessed for their red list (through the Global Fungal Red List initiative [https://redlist.info/en/iucn]). Moreover, calls have been made to add Funga to the ways macroscopic nature (flora and fauna) is referred to and thought of as biodiversity targets, a concept now embraced by the IUCN and others (Kuhar et al., 2018; Oyanedel et al., 2022).

Despite the essential role of fungi in ecosystems, the growing attention to this kingdom has not permeated wildlife trade research and policy. We refer to macroscopic fungi throughout because it is the target of wildlife trade. The trade in wild fungi has increased significantly in recent years. Over the last decade, annual growth in global markets has been 15%, making it one of the most rapidly expanding food commodities (de Frutos et al., 2019). Although estimates of participants in the trade in wild fungi are absent (in contrast to other trades, such as fishes), there is diverse evidence of the key livelihood role the trade plays for gatherers. For example, in areas of Tanzania and Mexico, trade in wild fungi is the seasonal primary livelihood for rural people and is key for women, who represent the majority of fungal gatherers and vendors (Pérez-Moreno et al., 2008; Tibuhwa, 2013)

The neglect of the trade in wild fungi is leaving species vulnerable to exploitation and depletion (Gonçalves et al., 2021; Oyanedel et al., 2022; ‘t Sas-Rolfes et al., 2019). Several fungi species are threatened by trade despite limited (to date) assessment efforts. For example, the caterpillar fungus (Ophiocordyceps sinensis) has declined 30% in the Himalayas over 15 years due to overharvesting for trade (Hopping et al., 2018). Another example is the matsutake in China (Tricholoma matsutake), classified as vulnerable by the IUCN, which has declined due to destructive collection practices and overharvesting (Chen, 2004). We argue for the inclusion of fungi in wildlife trade research and policy by highlighting key knowledge and capacity gaps in fungi trade research and policy and proposing a research agenda for more thoughtful inclusion of wild fungi in wildlife trade research. We discuss potential actions at the local and national levels that can improve the conservation status of traded species.

Comprehensive and detailed data on the scale of fungal trade remain scant, which prevents understanding of its value in the economy, ecology, and society (Boa, 2004; Oyanedel et al., 2022; Pérez-Moreno, 2021). Evidence of this data gap is the lack of research on the socioecological effects of fungal trade on local communities, in contrast to the many studies on animal and plant trade impacts (Arias et al., 2020; Esmail et al., 2020; Hinsley et al., 2018). Trade records for many fungi species are absent, and misidentification of similar species often occurs. Indeed, unidentified and possibly toxic mushrooms have been discovered in wild mushroom products at international grocery stores (Cutler et al., 2021). Overcoming misidentification is challenging given that the vast majority (∼95%) of fungal species (encompassing macro- and microfungi [e.g., yeasts and molds]) remain undocumented (Heilmann-Clausen et al., 2015).

The effects of fungal trade on species and ecosystems are difficult to assess, limiting insights into its sustainability and the risks it poses to biodiversity (Egli et al., 2006). Understanding of the ecological roles of fungi and the consequences of their decline is lacking. Although sustainability research on wild fungi trade is increasing, it remains geographically narrow, focusing on just a few species in select countries (e.g., Australia, New Zealand, Chile, Nepal, Croatia, Italy, Mexico) (He et al., 2022; Heilmann-Clausen et al., 2015; Niskanen et al., 2023; Román et al., 2006; Wei et al., 2021). It is crucial to expand research to a wider range of species and regions and to adopt practices that can inform policies for sustainable use in line with internationally adopted principles of sustainable use, such as those from the IUCN Sustainable Use and Livelihood (SULi) group (https://iucnsuli.org/).

The nuances of wild fungi trade elude clear policy development, unlike other wildlife trade regulations, because of the unique methods used to collect wild fungi, which can involve harvesting only the fruiting bodies, not the entire organism, akin to picking fruits or berries. This practice generally has a less significant impact on the fungus as a whole. However, other practices are also used. For instance, O. sinensis is extracted in its entirety, and even though for polypores, which have long-lived fruiting bodies, only their sporocarps are collected; this collection is concerning because new growth can take years to develop (Wei et al., 2021). Policy makers’ limited understanding of varied fungi harvesting methods leads to regulatory gaps in governance and food safety. Hence, the fungi trade typically faces significant uncertainties, data scarcity, and a tendency toward informality.

Incorporating fungi into wildlife trade research requires a research agenda that addresses specific knowledge gaps and unique challenges of the fungal trade. This agenda should be supported by a robust database on traded fungi and be aligned with the Kunming–Montreal Global Biodiversity Framework and Sustainable Development Goals to meet wider sustainability targets. We devised a research agenda organized around 4 areas: ecological impacts of fungi trade, potential for wild fungi to contribute to food security, socioeconomic dynamics of trade, and the impacts of illegal trade.

The first component of the research agenda deals with the ecological impacts of fungi harvesting (Egli et al., 2006). This should encompass studying the effects of harvesting on fungal sustainability and the wider ecosystem (Hopping et al., 2018). Fungi removal could have significant effects on nutrient cycling and symbiotic relationships with other species, aspects that must be understood to ensure sustainable practices (Heilmann-Clausen et al., 2015). Understanding the basic mechanism behind nutrient recycling is therefore necessary to be able to predict and react to the potential effects that species removal can have (Heilmann-Clausen et al., 2015). Moreover, fundamental research on fungal ecology, including life cycles, reproduction, and habitats, is essential for guiding conservation and sustainable harvesting (Gonçalves et al., 2021).

The second component of the research agenda addresses the potential of wild fungi for food security (Pérez-Moreno et al., 2021). Fungi are rich in nutrients and have the potential to contribute significantly to food supplies and thus food security (Román et al., 2006). Unanswered questions here relate to how to balance fungi use with conservation. Studies on the role of fungi in food security, through cultivation and exploration of new edible or medicinal species, should go beyond the 1100 species currently in use (Heilmann-Clausen et al., 2015; Román et al., 2006). Moreover, understanding the fungi market requires analyzing trade patterns and consumer demand to guide sustainable practices (de Frutos et al., 2019). Finally, the nutritional value and micronutrient profile of fungi requires detailed research to highlight their dietary importance, which would entail a cross-disciplinary approach, combining ecology, economy, and nutrition sciences (Boa, 2004).

Third, research must explore the socioeconomic aspects of wild fungi trade, its importance for livelihoods, and how regulations affect dependent communities, similar to the evaluation of fishery policies on coastal populations (Tibuhwa, 2013). Such research should aim to improve understanding of participants in the fungi trade and their reliance on it (e.g., Christensen & Larsen, 2005; Christensen et al., 2008; Pérez-Moreno et al., 2021). Research should also focus on enhancing the identification of wild fungi to better grasp the economic impact of their trade (Boa, 2004). Expanding the use of molecular, DNA-based techniques for identifying traded fungi can advance the monitoring and regulation efforts at various administrative levels (Dentinger & Suz, 2014). DNA-based methods, combined with artificial intelligence, can improve identification of traded fungi species, enhancing trade oversight and knowledge of fungal biodiversity (Niskanen et al., 2023). For instance, the Wildcheck initiative, which evaluates the trading of wild plant ingredients, offers a model for wild fungi trade. This initiative assesses biological, social, and trade risks and provides guidelines on responsible sourcing for policy makers (Schindler et al., 2022).

The fourth component of the agenda examines the potential impacts of illegal trade. Understanding the effects and extent of illicit trade, identifying the most trafficked species, and delineating supply chains can inform and strengthen compliance and the sustainability of the trade in wild fungi (Hopping et al., 2018). Illegal trade in wild fungi threatens key species with overexploitation and has social impacts (Hopping et al., 2018). Applying existing methods used to examine the endangered plant trade could enhance understanding of the scope and networks of potentially illegal wild fungi trade. For instance, FloraGuard, an initiative led by KEW, investigated the extent of internet-facilitated trade in endangered plant species (Lavorgna et al., 2022). To counter illegal trade, it recommended provision of AI tools to researchers and officials for species recognition and to differentiate between farmed and wild-harvested (ecologically detrimental) species. Examining case studies of illicit activities and charting global illegal trade patterns will deepen comprehension of wildlife trafficking. Evaluating case studies of illegal fungi trade and assessing its global spread can improve overall understanding of illegal wildlife trade.

Local collaboration between researchers, stakeholders, and policy makers is crucial. Engaging these groups can reveal traditional knowledge about fungi biology and trade, aid in capacity building, and inform better conservation strategies. Moreover, collaboration at the local level can help set specific regulations to control the level of harvesting, help set measures to protect the habitats of traded fungi, or provide education for improved identification of species. Such collaborative efforts should be established on the principles provided by groups such as IUCN SULi. Their recommendations, evidence, and rich policy experience can be leveraged to ensure sustainable use.

An example of an action at the local level comes from Italy, where fungi gatherers are required to obtain a license, known as tesserino, and sometimes to take a course on identification and regulations (Table 1). Harvesters face regulations such as designated harvest areas and size and species restrictions. Another example is in Chile, where there is a campaign to correct the false belief that forest burning promotes growth of the prized Morchella spp., a practice endangering Chilean forests (see https://www.ffungi.org/campaign/no-forest-no-morels).

Initiatives to reduce the pressures of wild harvesting through cultivation can provide a solid foundation for the conservation of traded endangered species (Cirlincione et al., 2022). However, such initiatives are often not applicable to ectomycorrhizal (ECM) fungi, which are valued as food but hard to cultivate due to their intricate environmental symbiosis (Dauphin & Peter, 2023). Thus, cultivating ECM fungi must be done cautiously with native trees to prevent adverse effects from non-native plant introductions.

Governments worldwide must integrate wild fungi trade into conservation policies, recognizing their significance for nutrition, food security, livelihoods, and health (Pérez-Moreno et al., 2008, 2021; Román et al., 2006). Efforts should focus on funding education about the importance of fungi, enhancing sustainable harvesting skills, supporting local conservation actions, and improving livelihoods related to wild fungi trade (Bonet et al., 2014; Kant Raut et al., 2019; Radomir et al., 2018). It is important to include harvesters in labor protection plans due to the unregulated and vulnerable nature of their work. Moreover, empowering those commonly involved in fungi harvesting, such as women in rural areas, through local cooperatives can bolster responsible use, value addition, and technology transfer, providing key livelihood options (Bonet et al., 2014; Tibuhwa, 2013).

Moreover, to improve management of fungal trade, incorporating fungi into customs regulations and documentation is key. Training customs officials to identify fungal species and to record their origin and destination can build on existing successful wildlife trade management models and their expansion to include fungi (Ogden, 2008).

As the critical role of fungi in ecosystems and economies continues to be unveiled, the urgency to integrate this kingdom into wildlife trade research and policy becomes evident. The challenge is to recognize the importance of fungi and to bolster scientific research to improve understanding of their biology and ecology, the effects of trade on their populations, and the socioeconomic impacts of the trade. Drawing from positive experiences and networks, such as IUCN SULi, it is possible to tap into established knowledge and frameworks that advocate for sustainable use. This can ensure efforts are informed by best practices and case studies and that researchers, policy makers, and other crucial stakeholders are involved, thereby fostering a robust interdisciplinary approach.

The inclusion of fungi is not merely a matter of adding a category to wildlife trade policy but a pressing necessity for the conservation of biodiversity. This inclusion requires addressing existing knowledge and capacity gaps to promote a sustainable and holistic approach to wildlife trade policy more generally. As societies journey toward this integrated future, it is paramount to maintain focus on the protection of these invaluable organisms. It is through recognition of their importance and investment in scientific research that the myriad benefits the trade of wild fungi provides can be protected, thereby protecting the ecosystems and communities they support and that, in turn, depend on them.