Research Article |
Corresponding author: Luís Reino ( luis.reino@cibio.up.pt ) Academic editor: Franz Essl
© 2023 Miguel Monteiro, César Capinha, Maria Teresa Ferreira, Martin A. Nuñez, Luís Reino.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Monteiro M, Capinha C, Ferreira MT, Nuñez MA, Reino L (2023) Negative and positive impacts of alien macrofungi: a global scale database. NeoBiota 85: 23-42. https://doi.org/10.3897/neobiota.85.101770
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Advances in ecological research during the last decades have led to an improved understanding of the impacts of alien species. Despite that, the effects of alien macrofungi have often received little attention and are still poorly understood. With the aim of reducing this knowledge gap, we compiled a database of the recorded socio-economic and environmental impacts of alien macrofungi. This database was compiled from all relevant sources we could identify, through an exhaustive literature review, considering the identity of known alien taxa and explicit indications of impacts of any kind. In total, 1440 records of both negative and positive impacts were collected for 374 distinct species in different regions of all continents, except Antarctica. The most frequently recorded impacts are related to the mutualistic interactions that these fungi can form with their host plants. In total 47.8% of all records refer to the indirect negative effect of these interactions, by facilitating the colonization of invasive plants, while 38.5% refer to their positive contribution to the growth of forestry species. Less frequently recorded negative impacts included ectomycorrhizal interactions with native plants, plant pathogenicity and human poisoning after ingestion. Additional positive impacts include the use as a food source by native species and human populations and commercial exploitation. Alien macrofungi are an increasingly prevalent component of human-dominated ecosystems, having a diverse array of negative and positive impacts on native biota and human population. Our database provided a first step towards the quantification and mapping of these impacts.
Biogeography, biological invasions, fungi, impact assessment, non-native species
The introduction and naturalization of alien species are recognized as important threats to native biodiversity (
In recent years, fungi as alien species have received some attention, through a higher availability of distribution data and information about their impacts in introduced ecosystems (
Despite being comparatively less represented in invasion studies than other groups, macrofungi comprise a large number of species that have been introduced widely across the globe over recent centuries (
In this context, we compiled a database of the socio-economic and environmental impacts of macrofungi reported in all relevant sources we could identify, namely scientific publications, reports, citizen science websites and databases on alien species. We reviewed sources in multiple languages and considered not only information on negative impacts but also impacts perceived as positive. We applied the precautionary principle and categorized impacts as ‘negative’ if they were known to have detrimental effects on native communities and human populations, or if they had no known beneficial effects (i.e., causing ecological change without any apparent gain to humans or native biota). In contrast, we categorized impacts as ‘positive’ if they were documented to have beneficial effects according to values associated with nature conservation or human interests (
We used as a starting point the recently published Global Database of Alien Macrofungi (
To classify species impacts, we first divided them into either positive or negative. Negative impacts – referring to detrimental effects on native communities and human populations, or ecological changes without any apparent gain to humans or native communities – were divided into the following subcategories: human health problems, competition with native fungi, ectomycorrhizal interactions with native plants, plant disease agents, ectomycorrhizal interaction with alien invasive species and other ecosystem changes. Positive impacts, referring to recorded beneficial effects on nature conservation or human interests, were categorized into benefits for forestry plantations, as food source for local human populations, food source for other species, and commercial use (Table
Percentage of each category of impacts on the total of records (n=1440). Environmental impacts are signaled by one asterisk (*) while socio-economic impacts are represented by two (**).
Impact categories | Description | Percentage |
---|---|---|
Negative Impacts | ||
Competition with native fungi species (*) | Competition between alien macrofungi and native macrofungi. | 0.1 |
Ecosystems (*) | Changes to biochemical properties of soil without any apparent ecological or human-related benefit. | 0.1 |
Human health (**) | Negative consequences on human health through ingestion. | 0.9 |
Plant disease agents (*) | Negative consequences of alien macrofungi as plant disease agents. | 3.6 |
Ectomycorrizhal interactions with native plant species (*) | Ectomycorrhizal interactions with native plants without confirmed benefits for these and potentially weakening ectomycorrhizal interactions with native fungi. | 7.9 |
Ectomycorrizhal interactions with alien plant species (*) | Negative ecological impacts owing to promotion of alien plant invasions. | 47.8 |
Positive Impacts | ||
Food source for other species (*) | Alien macrofungi used as food source for some animal groups, hence directly contributing to the sustaining of its population. | 0.1 |
Human food source (**) | Alien macrofungi used as a human food source. | 0.2 |
Commercial purposes (**) | Alien macrofungi used as a product in food industries. | 0.8 |
Forestry (**) | Establishment of ectomycorrhizal interactions with important forestry trees. | 38.5 |
Finally, in order to evaluate if the number of negative and positive impacts was directly related to the wealth of each included region, we performed for both impact categories (negative vs positive impacts) a Spearman’s rank correlation (r) between the number of impacts per region and their respective per capita GDP (gross domestic product). The GDP variable represents the mean income (in US$) in 2019 (or closest year available) and can be considered a proxy of wealth of the different introduced locations. Our hypothesis is that wealthier regions will have a higher number of recorded impacts (both negative and positive) owing to more introduction opportunities (
We collected a total of 1440 records of impacts from 246 data sources. Of these, 869 were identified in the sources as negative impacts and 571 as positive. Regarding negative impacts, most were related to mutualistic interactions that alien fungi form with alien plants (47.8% of the records; Table
In terms of the taxonomy, a total of 374 species belonging to 2 phyla, 5 classes, 15 orders, 50 families and 85 genera respectively were reported as having impacts. The families with the highest proportion of negative impacts were Suillaceae (110 records), Amanitaceae (96 records) and Russulaceae (65 records) (Fig.
Number of the records per taxonomic family for negative (A) and positive impacts (B). Only the 15 families with most records are represented. Taxonomic orders are represented by distinct colors.
Macrofungi species with the greatest diversity of impact types from both negative and positive categories. In the table ‘X’ represents the type of impacts that the species was recorded to cause in alien regions.
Species | Negative impacts | Positive impacts | Total number of different impacts | ||||||
---|---|---|---|---|---|---|---|---|---|
Human health | Ecosystems | Ectomycorrhizal interactions with native species | Ectomycorrhizal interactions with non-native species | Human food source | Forestry | Food source for other species | Commercial purposes | ||
Suillus luteus (L.) Roussel | X | X | X | X | X | X | 6 | ||
Amanita pantherina (DC.) Krombh. | X | X | X | X | 4 | ||||
Amanita phalloides (Vaill. ex Fr.) Link | X | X | X | X | 4 | ||||
Amanita muscaria (L.) Lam. | X | X | X | X | 4 | ||||
Boletus edulis Bull. | X | X | X | X | 4 | ||||
Suillus bovinus (L.) Roussel | X | X | X | X | 4 | ||||
Suillus granulatus (L.) Roussel | X | X | X | X | 4 | ||||
Amanita gemmata (Fr.) Bertill. | X | X | X | 3 | |||||
Chalciporus piperatus (Bull.) Bataille | X | X | X | 3 | |||||
Descolea alba (Klotzsch) Kuhar, Nouhra & M.E.Sm. | X | X | 3 | ||||||
Hydnangium carneum Wallr. | X | X | X | 3 | |||||
Hysterangium inflatum Rodway | X | X | X | 3 | |||||
Laccaria fraterna (Sacc.) Pegler | X | X | X | 3 | |||||
Russula sardonia Fr. | X | X | X | 3 | |||||
Scleroderma flavidum Ellis & Everh. | X | X | X | 3 | |||||
Scleroderma verrucosum (Bull.) Pers. | X | X | X | 3 | |||||
Suillus brevipes (Peck) Kuntze | X | X | X | 3 | |||||
Suillus spraguei (Berk. & M.A.Curtis) Kuntze | X | X | X | 3 | |||||
Tricholoma saponaceum (Fr.) P.Kumm. | X | X | X | 3 |
The global distribution of recorded impacts is uneven between regions (Fig.
Global distribution of negative (A) and positive (B) impacts of alien macrofungi. The colors gradient represents the total number of number of species with recorded impacts.
Additionally, the results of the Spearman’s rank correlation between the number of impacts per country and the per capita GDP were rs = 0.14 for the negative impacts and rs = 0.04 for the positive impacts.
This study allowed identifying a high number and diversity of impacts of alien macrofungi in many regions of the world, including negative and positive effects on humans, native and alien plant taxa, other fungi and animal species and soil biochemistry.
Notwithstanding this variety, interactions of EM macrofungi with alien plants were the most common impacts recorded. EM species are important mutualists for plants, by providing nutrients from the soil in return for photosynthetically derived carbon (
The direct impacts of fungal introductions on native plant communities are also important to consider. Several studies have shown that alien EM fungi are highly persistent in their novel environments and can form novel associations with native host plants (
Some species of macrofungi could also cause negative effects on native plants by causing diseases. The main pathogens in our database were root rotting fungi such as Pyrrhoderma noxium (Corner) L.W.Zhou & Y.C.Dai and Heterobasidion annosum (Fr.) Bref. The former species (P. noxium) is responsible for causing the brown root rot disease on more than 200 plant species (
In terms of human health, most reported impacts were related to the consumption of some species. The most reported of these impacts is the poisoning caused by the ingestion, by mistake, of the dead cap (Amanita phalloides (Vaill. ex Fr.) Link) (
Other less known negative impacts, with just a few records, refer to the introduction of alien radiata pines (Pinus radiata) and accompanying EM fungi Amanita phalloides, leading to observed changes in soil, including the release of recalcitrant nutrients, a loss of up to 30% of soil carbon and increased bacterial dominance (
Despite the overall availability of impact records and some recent advances regarding the identification of alien fungi (
Finally, there are now well-defined frameworks for classifying and ranking the impacts of non-native species. For example, IUCN EICAT (
By compiling and analyzing recorded impacts of alien macrofungi, we demonstrated the highly frequent and diverse types of effects that these taxa have on recipient ecosystems, economic activities and human well-being. Besides identifying mutualistic interactions with plant species as the most frequent (either negative or positive) impact recorded, we also showed that these and other impacts have a wide taxonomic and geographical distribution, underscoring the need for transnational cooperation strategies in managing the spread of alien species beyond single-species prevention efforts (
This work was funded by the FEDER Funds through the Operational Competitiveness Factors Programme – COMPETE and by National Funds through FCT, I.P. – Foundation for Science and Technology in the scope of the project PTDC/BIA-ECO/0207/2020. Miguel Monteiro was funded by a PhD fellowship SFRH/BD/119170/2016. César Capinha was supported by Portuguese national funds to the CEG/IGOT Research Unit (UIDB/00295/2020 and UIDP/00295/2020), through FCT—Fundação para a Ciência e a Tecnologia, I.P. Luís Reino was funded by National Funds through FCT, I.P., under the programme of ‘Stimulus of Scientific Employment – Individual Support’ within contract ‘CEECIND/00445/2017’. Martin A. Nuñez was funded through Agencia Nacional de Promócion de la Investigácion, el Desarollo Tecnólogico y la Innovácion within contract PICT SU 2018-329.
File format: Microsoft Comma Separated Values File (.csv).
Explanation note: File containing the records of negative impacts of alien macrofungi worldwide.
File format: Microsoft Comma Separated Values File (.csv).
Explanation notes: File containing the records of positive impacts of alien macrofungi worldwide.
Negative impacts of alien macrofungi
Data type: Ocurrences
Explanation note: File containing the records of negative impacts of alien macrofungi worldwide.
Positive impacts of alien macrofungi
Data type: Ocurrences
Explanation note: File containing the records of positive impacts of alien macrofungi worldwide.