Steep increase in red-listed lichens of Estonia

Abstract

National Red Lists are useful tools in establishing local conservation priorities. The threat status of Estonian lichens based on the IUCN system has been assessed twice, in 2008 and 2023. In the latest Red List, the proportion of species of elevated conservation concern, that is taxa belonging to the Near Threatened and threatened categories or having become regionally extinct in Estonia, was high (58%) while Least Concern (LC) species represented one-third (36%) of all taxa. Macrolichens were more threatened than microlichens. The Red List Index (RLI), illustrating the trends of species in their projected extinction risk, was calculated. The values were low (< 0.7 in 2023), thus indicating a heightened risk both for the set of all species and for macrolichens. More than half of all Estonian lichens are associated with woodlands and 54% of these species are of elevated conservation concern. Lichens preferring broad-leaved deciduous trees included more threatened than LC species, while among lichens preferring other deciduous or coniferous trees the proportion of LC species was higher than that of threatened taxa. Lichens inhabiting calcareous grasslands had the highest share (69%) of taxa of elevated conservation concern. Comparisons of national red-listed data with four selected countries (Czech Republic, Denmark, Finland and Sweden) revealed that the biggest overlaps of Estonian taxa of elevated conservation concern were with the Czech Republic and Finland.

Introduction

Biodiversity loss, including extinction of species, has exceeded the recently proposed planetary ‘safe’ boundary (Newbold et al. 2016) and was described as ‘biological annihilation’ in the ongoing sixth mass extinction on Earth (Ceballos et al. 2017). The International Union for the Conservation of Nature (hereafter IUCN) has provided the standard for classifying the status of species according to their extinction risk on a global scale (Brito et al. 2010; IUCN Standards and Petitions Committee 2022). Quantitative criteria based on population size, rate of decline, and area of distribution are applied to assign species to the categories of relative extinction risk (IUCN Standards and Petitions Committee 2022). Evaluation of species threat status using this standard procedure results in creating the IUCN Red List of Threatened Species which is the most comprehensive resource detailing the global threat status of species (Rodrigues et al. 2006; Mueller et al. 2022).

As most conservation efforts are conducted at national levels, there is a great demand for national scale Red Lists (Gärdenfors et al. 2001). National Red Lists can be useful tools in establishing conservation priorities within specific geographically defined areas. Therefore, the IUCN supports national Red List undertakings by presenting guidelines for the regional application of the IUCN Red List Categories and Criteria (IUCN 2012). By 2014, 36 European countries had already produced national or subnational Red Lists (Azam et al. 2016). Some of these countries, such as Germany (https://www.rote-liste-zentrum.de), use original criteria and categories to assess the occurrence and population trends of native species, while in other countries the criteria proposed by the IUCN have been fully adapted for different organism groups. For example, the latest Red Lists in Finland from 2019 (Hyvärinen et al. 2019) and Sweden from 2020 (SLU Artdatabanken 2020) contain c. 22 000 assessed taxa each; the Finnish list is the third and the Swedish is the fifth national assessment based on the IUCN system in their countries.

To interpret and generalize the outcome of the red-listing process either on a global or national level, the Red List Index (RLI) was developed (Butchart et al. 2005, 2007; Bubb et al. 2009). The RLI illustrates the relative rate at which species in a particular group change in their projected extinction risk as they move through the IUCN Red List categories, thus allowing the threat status of different groups of biodiversity to be compared (Butchart et al. 2005; Bubb et al. 2009). The RLI can be calculated for any set of species that has been assessed for the IUCN Red List at least twice (Bubb et al. 2009; Raimondo et al. 2022). For calculating its value, ranging from 0 to 1, the numbers of species in each red-list category and the category weight are used. The lower the value is, the faster the set of species is likely to become extinct (Bubb et al. 2009). It is possible to produce RLIs at the national level in two ways: firstly, by applying existing IUCN Red List assessments for global extinction risk of those species that are recorded in the country (the so-called ‘disaggregated global RLI’), or, secondly, by applying the national Red List categories, assuming that assessments of national extinction risk are in accordance with the IUCN guidelines (‘national RLI’) (Raimondo et al. 2022). An additional condition for calculating the RLI is that only genuine category changes should be considered, that is category changes that result from genuine improvement or deterioration in the status of species (Butchart et al. 2007; Bubb et al. 2009). Although the use of national RLIs is considered to be a valuable tool for presenting compact information on trends in species-level biodiversity (Juslén et al. 2013), these indexes are infrequently calculated. For example, out of 36 European countries that have produced national or subnational Red Lists, only nine have also compiled the national RLIs (Azam et al. 2016, Supplement 4).

In Estonia, five national Red Lists have been compiled: in 1979, 1988, 1998, 2008 and during 2018–2023. In the three early Red Lists, the system of threat categories used was conventional and applied criteria were not strictly defined but appeared to be mainly intuitive (Lilleleht 1998). Lichens were included in the national Red List for the first time in 1988, when 40 species were declared to be threatened (Anonymous 1993). Ten years later, 110 lichen species were already included in the Red Data Book (Randlane 1998). Internationally accepted IUCN threat categories and criteria (IUCN Standards and Petitions Working Group 2006) were applied for the first time in Estonia in 2008 (Tartes 2010). A total of 446 lichenized species were evaluated out of the 788 known lichens recorded nationally at that time (considering current taxonomy: Randlane et al. 2023). Among the evaluated species, 203 were then assigned to one of the IUCN categories of Regionally Extinct, Critically Endangered, Endangered, Vulnerable, Near Threatened or Data Deficient, while 243 species were assessed as Least Concern (Randlane et al. 2008).

The second round of threat status assessments of Estonian lichens based on the IUCN system was started in 2019 (Lõhmus et al. 2019). This process was carried out over the course of five different projects and ended in 2023. Some of the results of those projects have been published (Lõhmus et al. 2019; Randlane et al. 2021; Jüriado et al. 2022), while a comprehensive overview revealing the current condition of Estonian lichens has not yet been compiled. In this study we aim to: 1) give a general overview of the threat status of the Estonian lichen biota according to the recent national Red List assessments; 2) evaluate the changes in threat status of Estonian lichens during the last 15 years; 3) analyze the vulnerability of lichens of different ecological preferences in a national context; 4) broaden information regarding threatened lichens in Estonia by comparing the categories of these taxa in the national Red Lists of selected European countries.

Material and Methods

Study area

Estonia is located in Northern Europe on the eastern shores of the Baltic Sea. The bedrock in northern, western and central Estonia consists mainly of Ordovician and Silurian carbonate limestones, marls and dolomites, while southern Estonia is a region of Devonian sandstones and locally of carbonate rocks (Raukas 1995). Estonia has a flat topography with an absolute altitude c. 300 m above the sea level. It lies in the temperate climate zone with a mean annual temperature of c. 6 °C (monthly mean varies from –5 °C to 18 °C) and a mean annual precipitation varying between 500–750 mm per year (Estonian Weather Service 2024).

Around half of the territory of Estonia constitutes forest land, which includes forested areas as well as clear-cut and reforested patches. Forest stands are represented by a mosaic of smaller and larger areas of deciduous, mixed and coniferous forests (Sirkas & Valgepea 2023). Estonian forests belong to the hemiboreal subzone of the boreal forest zone, lying in the transitional area where the southern taiga forest subzone changes into the spruce-hardwood subzone (Ahti et al. 1968). Pinus sylvestris, Picea abies and Betula pendula together with B. pubescens are the most abundant tree species in the area (Sirkas & Valgepea 2023). Alnus incana, A. glutinosa and Populus tremula occur less frequently. The proportion of temperate broad-leaved species (i.e. Acer platanoides, Fraxinus excelsior, Quercus robur, Tilia cordata and Ulmus glabra) is nearly insignificant (Sirkas & Valgepea 2023). Many other habitats which are suitable for lichens, such as semi-natural grasslands (calcareous grasslands and wooded meadows), mires, sandy dunes, siliceous erratic boulders and carbonate rocks, are also found in the country (Raukas 1995).

Data collection (red-listing assessments)

The second evaluation of the threat status of Estonian lichens using the IUCN system was performed over five years, 2019–2023, in the course of five different projects (Supplementary Material Table S1, available online). The assessments in all five projects were carried out with a similar methodology following the IUCN guidelines (IUCN 2012; IUCN Standards and Petitions Committee 2017, 2019) and guidelines for applying IUCN criteria for fungi (Dahlberg & Mueller 2011), although a few methodological details differed (Supplementary Material Table S1). The following IUCN categories were used: Regionally Extinct (RE), Critically Endangered (CR), Endangered (EN), Vulnerable (VU), Near Threatened (NT), Least Concern (LC), Data Deficient (DD), Not Applicable (NA) and Not Evaluated (NE). Of these, CR, EN and VU are ‘threatened categories’ according to the IUCN guidelines; to refer to threatened plus RE and NT species collectively, the phrase ‘species of elevated conservation concern’ was used (IUCN Standards and Petitions Committee 2022). The species that have not been reliably reported from Estonia since 1950 were considered to be RE. For the category NT, quantitative threshold levels provided in Dahlberg & Mueller (2011) were used. The species for which herbarium material from Estonia is not available, and which are included in the list based on literature data only, were considered doubtful and placed into the category NA. The remaining taxa were treated as ʻreliably found’ in Estonia and were evaluated against the Red List criteria; two species (Cladonia monomorpha Aptroot et al. and Usnea substerilis Motyka) constituted an exception among the reliably found taxa because of their unclear distribution and frequency data, and they were left in the category NE. Applying IUCN standards, criteria A (Population Size Reduction), B (Geographic Range), C (Small Population Size and Decline) and D (Very Small or Restricted Population) were assessed for each species and the most threatened category of all assessments was assigned to the species. Criterion E (Quantitative Analysis) was not used due to the insufficiency of data.

Both the assessments and the reviews of assessments were performed by local experts; Polina Degtjarenko, Inga Jüriado, Piret Lõhmus, Liis Marmor-Ohtla, Ede Oja, Tiina Randlane and Ave Suija participated in several projects while Asko Lõhmus and Andres Saag were involved in one project.

The main data source for species occurrence records was the PlutoF biodiversity platform (https://plutof.ut.ee/; Abarenkov et al. 2010) that incorporates the data of specimens from all main Estonian herbaria (TUF, TALL and TAM). In addition, some datasets of lichen research projects or inventories in Estonia were uploaded onto the PlutoF database and made available to the experts. The assessment process was performed using the Estonian Nature Information System EELIS (https://www.eelis.ee); the species assessment sheets (including the distribution map files) are kept in this information system and are available to the registered users. For further details of the red-listing process, see Lõhmus et al. (2019), Randlane et al. (2021) and Jüriado et al. (2022). The full dataset of all 942 assessed species with added data is presented in Supplementary Material Table S2 (available online). Nomenclature follows Randlane et al. (2023) with some exceptions (indicated in Supplementary Material Table S2).

Calculation of RLI

The RLI value is calculated by multiplying the number of species in each red-list category by the category weight (0 for LC, 1 for NT, 2 for VU, 3 for EN, 4 for CR and 5 for EX). These products are summed, divided by the maximum possible value (i.e. number of species multiplied by the maximum weight 5), and subtracted from one (Bubb et al. 2009). Thus, an index value that ranges from 0 to 1 is produced. If the value is 1, all species in the set are LC, and if the value is 0, all species are (regionally) extinct (Bubb et al. 2009). We calculated the RLIs using the assessments of national Red Lists in 2008 and 2019–2023 following the revised method by Bubb et al. (2009), with one exception. This method excludes species categorized as EX in the first assessment. In our national Red List, globally extinct species are absent but several species have been assessed as RE. As suggested in a Finnish study using RLI at a national level, it is reasonable to include RE species in calculations because regional extinction is not necessarily irreversible and populations of RE species can be re-established; the category weight for RE was equal to the category weight for EX (i.e. 5) (Juslén et al. 2013). To separate genuine category changes from non-genuine changes, we carefully examined all species for which the category in 2019–23 was different from the category in 2008, excluding the taxa that were assigned to the categories NE or DD in either assessment round. The category changes were considered not genuine if the change was due to one of the following causes: revised taxonomy, improved knowledge or methodological issues (Bubb et al. 2009) (Supplementary Material Table S2). Among methodological issues were, for example, the cases where usage of the criterion D (very small or restricted population) resulted in different categories in 2008 (when D2 was used) and 2019–23 (when mainly D1 was used), although new distributional data were not recorded after 2008 (Lõhmus et al. 2019). We therefore used back-casting for all species with non-genuine changes, meaning that earlier Red List categorizations were retrospectively adjusted using current information (Butchart et al. 2007; Bubb et al. 2009).

We calculated the RLI for two datasets of species that have been assessed for the national Red List twice (in 2008 and 2019–2023): 1) dataset including all 445 species; 2) subset of the first dataset, containing 270 species of macrolichens. It has been noted that the RLI should not be calculated using only a subset of species in a particular taxonomic group since this could produce a biased result (Bubb et al. 2009). Lichens do not form a taxonomic entity but are accepted as a unique ecological-physiological group of self-sustaining symbiotic associations (Hawksworth & Grube 2020) and are often included as a separate group in Red Lists. We aimed to test whether the RLI for dataset 1, containing around half (56.6%) of all lichenized taxa, is very different from dataset 2 containing the majority (84.4%) of macrolichens recorded in Estonia.

A Sankey diagram for the visualization of changes in the categories of lichens based on the assessments in 2008 and during 2019–2023 was built with the SankeyMATIC web tool (https://sankeymatic.com/build/).

Grouping of red-listed species by ecological preferences

All 942 species included in the study were divided into groups according to their ecological preference for substratum and habitat (Supplementary Material Table S2). Two different substratum and habitat categorizations, general and specific, were used (Table 1). Each species was categorized into only one general and one specific substratum and habitat group. Primary substratum and habitat groups were assigned based on the label data of herbaria specimens and observations registered on the PlutoF biodiversity platform (Abarenkov et al. 2010).

Table 1. Categorization of lichens into ecological groups according to their preferences for substratum and habitat.

Five general and eleven specific substrata groups were applied (Table 1). In the case of epiphytic species, an initial check showed whether the species had more records from coniferous or deciduous trees; if there were more for deciduous trees, then the substratum group was chosen between temperate broad-leaved and all other deciduous trees. For species habitat preferences, three general and eight specific habitat groups were used (Table 1).

Red List assessments of Estonian lichens in selected European countries

For comparing how the threat status of lichenized species listed in the Estonian Red List is assessed in some other European countries, we collected the category data from recent Red Lists of the Czech Republic (Liška & Palice 2010), Denmark (Søchting 2019), Finland (Hyvärinen et al. 2019) and Sweden (SLU Artdatabanken 2020). All these countries adhere to the IUCN guidelines for applying the Red List categories and criteria at regional and national levels (IUCN 2003, 2012), and their Red Lists have been compiled or revised recently. We used the nVenn tool (Pérez-Silva et al. 2018; https://degradome.uniovi.es/cgi-bin/nVenn/nvenn.cgi) to build quasi-proportional Euler diagrams and visually depict the overlaps of lichenized species in the different Red List categories of Estonia and the four compared countries. Figures were edited in Affinity Designer 2. Source data for diagrams are provided in Supplementary Material Table S2.

Results

Distribution of lichenized species between the Red List categories in Estonia

According to the latest update of the checklist of lichenized, lichenicolous and closely allied fungi in Estonia (Randlane et al. 2023), 978 lichen-forming species have been nationally recorded. Of all listed taxa, the presence of 34 species in Estonia is doubtful and these species were placed into the category NA. The remaining taxa (944 species) are reliably found in Estonia, and the threat status for almost all of them (942) was assessed recently. Of these, 544 species are of elevated conservation concern, 415 of which are threatened; 334 lichenized taxa belong to the category LC (Table 2).

Table 2. Distribution of Estonian lichens between the Red List categories according to the assessments in 2008 and 2019–2023, together with the numbers of assessed and reliably found taxa. For the abbreviations of Red List categories, see Fig. 1; NE = Not evaluated.

The distribution of macro- and microlichens between the Red List categories according to the latest assessments in 2019–2023 was surveyed separately. Of all assessed macrolichen species, 67% were of elevated conservation concern; 53% of microlichens were in this category. The proportions of LC and DD categories were larger among microlichens (Fig. 1).

Figure 1. Distribution of macro- and microlichens amongst the Red List categories in Estonia according to the latest assessments during 2019–2023. Abbreviations of IUCN categories: RE = Regionally Extinct, threatened categories (CR = Critically Endangered, EN = Endangered and VU = Vulnerable), NT = Near Threatened, LC = Least Concern, DD = Data Deficient. In colour online.

Comparison of the two latest Estonian Red Lists of lichens

The two latest red-listings of lichen-forming fungi, both applying the IUCN threat categories and criteria, were completed in 2008 and in 2023. During 2019–2023, almost all recorded taxa (99.8%) were assessed against the established criteria, while in 2008 44% of lichen species remained in the category NE (Fig. 2; Table 2). In the last Red List, the proportion of species of elevated conservation concern (except the category RE) had increased by c. 6–14%, compared to the proportions of the same categories in 2008. The shares of species belonging to the categories LC and DD had both increased by c. 4% (Fig. 2) during this time.

Figure 2. Proportions of Red List categories of assessed lichens in Estonia in 2008 and 2019–2023. For the abbreviations of Red List categories, see Fig. 1; NE = Not Evaluated. In colour online.

A total of 445 lichen species have been assessed against the IUCN Red List criteria twice. Of these, 270 remained in the same category and 175 species were assigned to a different category during the latest assessment, including 30 cases that involved the change in category DD. For 133 species, their Red List category deteriorated during the second assessment, while only 12 species were assigned to a category of lower extinction risk (Supplementary Material Table S2, available online). Seven RE species (Diplotomma lutosum (Ach.) Arnold, Lecanora epibryon (Ach.) Ach., Peltigera elisabethae Gyeln., Ramalina elegans (Bagl. & Carestia) Jatta, Rostania occultata (Bagl.) Otálora et al., Thelidium pyrenophorum (Ach.) Mudd and Verrucaria maculiformis Kremp.) were found again for the first time since 1950; four of these were assigned to one of the threat categories (Fig. 3), while three remained DD in 2023. Of the 243 species that were evaluated as LC in 2008, 40 taxa have now been assigned to one of the categories of elevated conservation concern (Fig. 3).

Figure 3. Changes in the categories of lichens in the Red List of Estonia based on the assessments of lichenized taxa in 2008 and during 2019–2023. For the abbreviations of Red List categories, see Fig. 1. Values indicate the number of species within each category and changes of category; lines are coloured by the status in 2008. In colour online.

To evaluate the relative projected extinction risk, we calculated the RLI using the national Red List categories from the two latest evaluation periods, separately for all species (445) and for just macrolichens (270) that have been assessed twice (Fig. 4). Of all category changes, 101 changes were identified as genuine, a primary reason for the change of Red List category, and 44 changes were considered not genuine in the full dataset. The RLI value for Estonian lichens in 2008 was 0.742 and it decreased by 7.8% (to 0.684) from 2008 to 2019–2023. The RLI values for macrolichens were still lower, 0.701 and 0.634 respectively, and the decrease during the last 15 years was also steeper (9.6%).

Figure 4. Red List Index (RLI) values of Estonian lichens in 2008 and 2019–2023 for all species (n = 445) and for macrolichens (n = 270) that have been assessed twice using the IUCN criteria. In colour online.

Threat status of lichens with different ecological preferences in Estonia

The majority of lichens recorded in Estonia were epiphytic and epilithic (366 and 320 species, respectively), while the number of epigeic and epixylic species was considerably lower (153 and 73 species, respectively; see Supplementary Material Fig. S1, available online). The share of species of elevated conservation concern was highest among the epigeic lichens (67%), and was generally high (53–59%) in other general substratum groups (Supplementary Material Fig. S1). In the specific substratum grouping, the share of such species was highest among the lichens growing mainly on calcareous soil (85%), followed by the groups ‘lignum’ (70%) and ‘sandy soil’ (67%; Fig. 5). In other substratum groups, the share of species with elevated conservation concern varied between 41–62%. Among the epiphytic lichens, this value was 57% for lichens growing mainly on broad-leaved trees while it was 50–51% in the groups ‘coniferous trees’ and ‘other deciduous trees’ (Fig. 5). Among the epilithic lichens, 62% of the species growing mainly on siliceous rocks and 54% of those growing mainly on calcareous rocks belonged to the elevated conservation concern category (Fig. 5).

Figure 5. The number and share of Estonian lichen species assigned to IUCN categories in the specific substratum groups. The x-axis is ordered according to the summed proportions of the categories of elevated conservation concern (RE, CR, EN, VU, NT). For the abbreviations of Red List categories, see Fig. 1. In colour online.

Grouping Estonian lichens into habitat types according to their main preference revealed that the majority of species were associated with woodlands (485 species), while the number of species growing mainly in different open habitats was smaller (402 species; see Supplementary Material Fig. S2, available online). The share of lichens with elevated conservation concern was slightly higher in the open habitats compared to the woodlands (63% and 54%, respectively) (Supplementary Material Fig. S3, available online). Among the specific habitat groups, the proportion of such species was highest in the groups of lichens growing mainly in alvar grasslands (69%) and sandy dunes and heaths (68%; Fig. 6), while it varied between 54–63% in other open habitats, aquatic habitats and woodlands. The species included in the group ‘various habitats’ were in a better situation since those of higher conservation concern constituted 45% (Fig. 6).

Figure 6. The number and share of Estonian lichen species assigned to IUCN categories in the specific habitat type groups. The x-axis is ordered according to the summed proportions of the categories of elevated conservation concern (RE, CR, EN, VU, NT). For the abbreviations of Red List categories, see Fig. 1. In colour online.

Red List assessments of Estonian lichens compared to selected European countries

First, we calculated the overlap of the Estonian lichen checklist with the assessed lichens of the four compared countries (Czech Republic, Denmark, Finland and Sweden) separately; for this the full Estonian dataset of 942 assessed species was used. The highest number of shared species was found with the Swedish species list (922 species out of 942), and the lowest with the Danish list (637 species), whereas Finland (841 species) and the Czech Republic (756 species) showed an intermediate overlap (Fig. 7).

Figure 7. Distribution of Estonian lichenized species between the Red List categories from the 2019–2023 assessment, and the numbers of Estonian species in the checklists of the four compared countries (Czech Republic, Denmark, Finland and Sweden).

We then compared the species listed under the RE, CR, EN, VU and NT categories (combined as elevated conservation concern) from each of the four countries with the Estonian assessed species. The overlap of elevated conservation concern categories between the other four countries and the Estonian species showed the highest absolute value with the Czech Republic Red List assessments (305 species) and the lowest with Sweden (100 species) (Fig. 8). The comparison of taxa evaluated as LC in all four countries revealed that only some of these species were assigned to the threatened or NT categories in Estonia, seven and four species respectively (Fig. 9). Of these, Cladonia coccifera (L.) Willd. and Rusavskia elegans (Link) S. Y. Kondr. & Kärnefelt were assigned to EN, and Baeomyces rufus (Huds.) Rebent., Circinaria caesiocinerea (Nyl. ex Malbr.) A. Nordin et al., Porpidia soredizodes (Lamy ex Nyl.) J. R. Laundon, Pseudosagedia chlorotica (Ach.) Hafellner & Kalb and Rhizocarpon geographicum (L.) DC. were assigned to VU in Estonia. The latest Estonian Red List includes 544 lichenized species of elevated conservation concern, of which 429 were also classified as species of elevated conservation concern in any of the compared countries and 115 species were either not recorded, NE, DD or LC in the compared countries (Supplementary Material Fig. S4, available online). In addition, 205 species listed as LC in Estonia are considered to be species of elevated conservation concern in at least one of the compared countries (Supplementary Material Fig. S4) while 20 taxa are included in the elevated conservation concern categories in all five countries (Table 3).

Figure 8. The overlap of species listed under EX, CR, EN, VU and NT (combined as elevated conservation concern) categories from each of the four countries (Czech Republic, Denmark, Finland and Sweden) with Estonian species assessments.

Figure 9. The overlap of species listed under the LC category in the four compared countries (Czech Republic, Denmark, Finland and Sweden) with Estonian species listed under CR, EN, VU (combined as threatened), NT, LC and RE categories.

Table 3. Species of elevated conservation concern (categories RE, CR, EN, VU and NT) in all of the four compared countries and in Estonia, their Red List category in each country, and their main habitat in Estonia. For the abbreviations of Red List categories, see Fig. 1. Red List categories of compared countries were retrieved from: Hyvärinen et al. (2019) for Finland, SLU Artdatabanken (2020) for Sweden, Søchting (2019) for Denmark, and Liška & Palice (2010) for Czech Republic.

Discussion

Estonian lichen biota and its threat status

At present, 978 species of lichenized fungi have been recorded in Estonia (Randlane et al. 2023); such lichen diversity is noteworthy, considering that the area of the country is small (45 000 km²) and there is no vertical or latitudinal vegetational zonation in the country (Raukas 1995). Among neighbouring countries with comparable areas, Denmark (42 000 km²) has 1002 recorded lichen-forming species (Søchting 2019) while in Latvia and Lithuania (both c. 65 000 km²) less than 800 lichens have been listed (Motiejunaite 2017; Moisejevs 2022). The proportion of species of elevated conservation concern in Estonia is high (57.7%) while LC species form only one-third (35.5%) of all assessed taxa (Table 2). This alarming result may have different causes. First, lichens are characterized by a high habitat specificity and although they are highly tolerant to environmental stresses, they appear sensitive to environmental disturbances or habitat changes (Nimis et al. 2002). As poikilohydric organisms, they are vulnerable to combined changes in air humidity and temperature in the habitat, being among the most climate-change sensitive organisms (Matos et al. 2015; Nascimbene & Marini 2015). Second, two decades ago, the Estonian lichen biota had already been reported to include a high proportion (64%) of rare species (with fewer than 10 localities known) (Randlane et al. 2002). Although many taxa which belonged to the rare group 20 years ago have now been recorded repeatedly, 188 nationally new lichenized species have been reported during this period (Randlane & Saag 1999; Randlane et al. 2023) and the majority of these taxa are rare. Species with very small or restricted populations must be assigned, using the criterion D, to threatened or NT categories even without any indication of population decline (IUCN Standards and Petitions Committee 2019). Applying the IUCN criteria only to the portion of a population present within a particular region (here: a country) artificially divides the biological population into more restricted subpopulations. Because small, isolated populations face a higher threat of extinction than large, widespread populations (O'Grady et al. 2004), the artificially divided subpopulations may be assessed individually as having a higher risk of extinction than they actually face. Nevertheless, national threat assessments are useful tools in promoting conservation activities within defined areas and can be treated as early warning signs of local decline (Miller et al. 2007). Similar situations (high proportion of species of elevated conservation concern and low proportion of LC species in the biota of lichen-forming fungi nationally) have also been reported in some other countries. For example, in Finland the share of LC species among lichens is 38.9% (Pykälä et al. 2019).

According to our data, macrolichens form a more threatened segment of lichenized taxa compared to microlichens (Figs 1 & 4). This result is consistent with earlier studies indicating that macrolichen species are less tolerant to air pollution and disturbances than microlichens (Leppik et al. 2015; Guttová et al. 2017; Degtjarenko et al. 2018) and are vulnerable to climate change, either because they are more sensitive to decreasing water supply (Boch et al. 2019) or due to their higher dispersal limitations (Dettki et al. 2000). Macrolichen richness has been shown to be positively related to the total richness of microlichens; however, the number of threatened macrolichens was not an important predictor for threatened microlichens (Bergamini et al. 2007). Nevertheless, it has been proposed that in biodiversity assessments with scarce resources, lichen sampling could be focused on the better known macrolichens (Bergamini et al. 2007). A similar strategy could be useful in areas where available data are not yet sufficient for evaluating IUCN Red List categories for the full set of lichenized taxa. This strategy has been recently applied, for example, in Latvia, where out of 86 species assessed for the IUCN Red List, 52 were macrolichens (Degtjarenko et al. 2024). Another approach to broadening species representation in national Red Lists is adopting standard taxonomic groups for comprehensive assessment at national (and global) levels. The family Parmeliaceae, containing foliose and fruticose lichenized fungi, has been proposed as one of the suitable standard groups (Mueller et al. 2022; Raimondo et al. 2022).

Threat situation of lichens with different ecological preferences in Estonia

The Estonian lichen biota consists of species with variable ecological preferences, but more than half of the recorded lichenized taxa (485 species) are associated with woodlands (Supplementary Material Figs S2 & S3, available online). This is in accordance with earlier studies, where c. 530 lichenized, lichenicolous and allied saprophytic species have been shown to form a regional species pool in Estonian forests (Lõhmus & Lõhmus 2019) (we did not include lichenicolous and saprophytic species in the current study). The prevalence of forest lichens in Estonia is caused by local environmental conditions, with the forest lands covering more than 50% of the country (Sirkas & Valgepea 2023). Of the lichens which prefer woodlands as the main habitat, more than half of the taxa (54%) belong to the group of elevated conservation concern (Supplementary Material Fig. S3). The main threat to forest lichens relates to forest management activities, most devastatingly clear-cutting that destroys the habitat and causes breaks in stand continuity. Among the various effects of forest management, the changes in tree species composition, decreasing numbers of large and old trees and decreasing amounts of decaying wood should be emphasized. It is now well established that lichen richness, including lichens of elevated conservation concern, increases with stand age in both old-growth and managed forests (Marmor et al. 2011; Tullus et al. 2022; Nirhamo et al. 2023). The proportion of old-growth forests is low in Estonia, owing to a long history of clear-cutting, with the average age of forest stands being only 55 years. The vulnerability of forest lichens on a wider scale is demonstrated in Table 3: of 20 lichen species assessed as being of elevated conservation concern in all five compared countries, 16 species prefer woodlands as their main habitat.

In our study, the group of lichens preferring temperate broad-leaved deciduous trees included more threatened (73) than LC (65) species, while among lichens preferring other deciduous or coniferous trees the proportion of LC species was higher than that of threatened taxa (Fig. 5). Similar results have been reported in Sweden, where Fraxinus excelsior, Quercus robur and Ulmus spp. appeared among the most species-rich host trees for threatened lichens (Thor et al. 2010). In Estonia, many epiphytes that prefer temperate broad-leaved trees as the primary substratum are threatened or near threatened, as these phorophytes make up only 2.4% of tree volume in local forests (Sirkas & Valgepea 2023) and are close to their northern distribution limits in Estonia (Paal 1998). Recent outbreaks of tree-specific fungal diseases, such as Dutch elm disease and ash dieback (Watson et al. 1988; Lõhmus & Runnel 2014), probably also contribute to the local extinction risk of epiphytic lichens inhabiting broad-leaved deciduous trees.

Of other deciduous trees, Populus tremula has been pointed out as the phorophyte with the highest number of lichen species in Estonian forests (Jüriado et al. 2003) and as a good alternative substratum tree species for most threatened lichens dwelling on temperate broad-leaved trees (Marmor et al. 2017). In our study, the species-rich group of lichens preferring other deciduous trees (including Populus tremula) contained 50% of lichens of elevated conservation concern. Epiphytic lichens preferring coniferous trees demonstrated similar results (Fig. 5). In this group, besides species that inhabit Picea abies and Pinus sylvestris, the most common coniferous phorophytes in Estonia, epiphytic lichens preferring Juniperus communis are also listed. Juniperus communis is the main phorophyte in overgrown alvar grasslands (juniper-woodlands); in more open situations, it is known to be a species-rich host for epiphytic lichens with 140 recorded species (Jüriado et al. 2015) including several threatened or NT taxa (e.g. Blastenia ferruginea (Huds.) A. Massal., B. herbidella (Hue) Servít, B. hungarica (H. Magn.) Arup et al. and Protoparmelia oleagina (Harm.) Coppins).

Open habitats were divided into five specific habitats in our classification: calcareous grasslands (alvars), sandy dunes and heaths, mires and bogs, seashore, and other open habitats (Table 1). Of these, alvars were the main habitat for the highest number of lichens (171; Supplementary Material Fig. S2) and with the highest percentage of taxa of elevated conservation concern (69%; Fig. 6). These semi-natural grasslands with shallow soil on monolithic calcareous rock have been formed historically as a consequence of livestock grazing over centuries (Rosén 1982). On alvars with the thinnest soil layer, environmental stress (extreme droughts in summer, frost-induced soil movements in winter and small-scale flooding in spring) and grazing disturbances have created a species-rich community where lichens prosper (Rosén 1995; Leppik et al. 2013, 2015). The characteristic members of the alvar soil crust community, for example Gyalolechia bracteata (Hoffm.) A. Massal., Megaspora verrucosa (Ach.) Hafellner & V. Wirth, Psora decipiens (Hedw.) Hoffm. and Squamarina lentigera (Weber) Poelt, are all threatened or NT in Estonia because of threats to their specific habitat. Due to the cessation of traditional management on calcareous grasslands, these habitats have been largely overgrown with Juniperus communis and Pinus sylvestris and their area has diminished dramatically: over the last century, 80% of the former alvar territory has been devastated and currently only c. 17 000 ha of calcareous grasslands has remained in Estonia (Helm 2019). At the same time, lichen communities growing on shallow soil are highly susceptible to overgrazing and trampling impacts, highlighting the necessity for a careful balance in management practices (Eriksson & Rosén 2008).

Sandy dunes and heaths form another open habitat with a high percentage of taxa of elevated conservation concern (68%; Fig. 6); however, in our dataset, the number of species (28) preferring dunes and heaths as a primary habitat is quite small. These species are mainly threatened, like alvar-dwelling lichens, due to overgrowing of their open habitat by Juniperus and Pinus, but also by excessive trampling in recreation areas (Jüriado et al. 2016). Seashore lichens (48) are all epilithic, inhabiting mainly siliceous and sometimes calcareous rocks (with the exception of Xylographa opegraphella Nyl. ex Rothr. growing on lignum). The seashore taxa of elevated conservation concern (63%; Fig. 6) include several species which have been recorded in Estonia in fewer than five locations (e.g. Anaptychia runcinata (With.) J. R. Laundon, Protoparmeliopsis achariana (A. L. Sm.) Moberg & R. Sant., Ramalina siliquosa (Huds.) A. L. Sm., Umbilicaria decussata (Vill.) Zahlbr., U. nylanderiana (Zahlbr.) H. Magn. etc.) and therefore have been classified in a threat category due to the very low number of individuals in Estonian populations.

The group of lichens in other open habitats is species rich (143 species) and heterogenous, containing epigeic lichens inhabiting sandy or other acidic soils, epilithic taxa on calcareous or siliceous rocks and a small number of taxa growing on lignum. The main threat for the species of elevated conservation concern (57%; Fig. 6) in this group is a changing environment, from sparsely vegetated and well-lit habitats in grasslands and roadsides into densely vegetated shady and more humid habitats with trees and bushes. For some epixylic species, such as Adelolecia kolaënsis (Nyl.) Hertel & Rambold and Calicium notarisii (Tul.) M. Prieto & Wedin, the loss of old wooden buildings and fences was also highlighted as a threat factor. In fewer cases, anthropogenic activities such as limestone and sand mining, building, overgrazing and trampling might constitute a threat (Jüriado et al. 2022).

Mires and bogs, and freshwater aquatic habitats, are preferred only by a limited number of lichens (12 and 15, respectively). In the first group, three species (Cladonia cyanipes (Sommerf.) Nyl., C. incrassata Flörke and Ochrolechia frigida (Sw.) Lynge) are classified as VU and three others (Cladonia grayi G. Merr. ex Sandst., C. portentosa (Dufour) Coem. and Icmadophila ericetorum (L.) Zahlbr.) as NT. The majority of aquatic lichens are epilithic on siliceous rock and some on calcareous rock. From this small and poorly examined group, a small number of species are of elevated conservation concern (e.g. macrolichens Dermatocarpon luridum (With.) J. R. Laundon and Leptogium rivulare (Ach.) Mont., and microlichens Hydropunctaria rheitrophila (Zschacke) C. Keller et al., Verrucaria aethiobola Wahlenb. and V. submersella Servít). The major threats facing lichens in both of these groups are the construction of drainage systems, dredging and other structural changes for water-level regulation.

The group ‘various habitats’ contained 40 species that grew in a wide range of habitats, for example in woodlands and open areas, or in several different specific habitats. Many of these were common also in locations with heavy human influence, for example Phaeophyscia orbicularis (Neck.) Moberg, Physcia dubia (Hoffm.) Lettau and Xanthoria parietina (L.) Th. Fr. Thus, the share of LC species was the highest (53%) and of threatened species was the second lowest (30%; Fig. 6) in this group. Threatened species of this habitat group were mainly epilithic and epigeic lichens, for example Peltigera lepidophora (Nyl. ex Vain.) Bitter that can grow on endangered alvars but also in habitats with moderate human influence (e.g. roadside banks or old limestone quarries), or P. leucophlebia (Nyl.) Gyeln. that is recorded both in alvars and woodlands.

Possible processes behind the numbers

Comparison of the two latest national Red Lists of lichens revealed a severe deterioration of species towards their higher potential extinction risk (Figs 2 & 3). During 2019–2023, almost the full set of lichenized species (99.8% of recorded taxa) was assessed against the IUCN criteria, while in 2008 only 56% of the taxa were evaluated (Fig. 2, Table 2); therefore, our results are based on incomplete information.

Positive changes during the period 2008–2023 included a small number of species being assigned to a category of lower extinction risk, and re-finding seven species that had been evaluated as RE in 2008 (Supplementary Material Table S2, available online). In such cases, two possibilities can be considered: 1) the species was continuously present in Estonia but was not recorded, or 2) the species has re-dispersed recently. Of these taxa, two species (Lecanora epibryon and Ramalina elegans) were newly recorded quite close to their original locality, while Diplotomma lutosum, Peltigera elisabethae and Verrucaria maculiformis were re-found in the same region as earlier; new records of the remaining two species, Rostania occultata and Thelidium pyrenophorum, were from different regions of the country. In the cases of Lecanora epibryon and Ramalina elegans, the first alternative seems more probable, while in other cases both are equally possible.

Negative changes were overwhelming, with a category of greater extinction risk being assigned to 133 lichen species (Supplementary Material Table S2). The main factor underlying these negative changes is related to the deterioration of the environment, while the influence of the decrease in suitable habitats on lichenized taxa may vary between different species and habitats. The theory of extinction debt explains why local extinction of species can occur with a substantial delay following habitat loss or degradation (Kuussaari et al. 2009). Estonian forests suffer at the present time from severe management activities; for example, the annual clear-cut area has increased nearly three times between 2008–2018 (Sirkas & Valgepea 2023). Although a quarter of our forest land is currently protected (Sirkas & Valgepea 2023), a strict protection regime does not apply to the whole area and partial logging has increased in protected forest areas (Kiis et al. 2021). Forest felling (especially clear-cuts) has become easy to see in the landscape over the last decade (Kiisel & Remm 2022). The effect of extinction debt has been demonstrated for epiphytic and epixylic lichens in European forests (Berglund & Jonsson 2005; Johansson et al. 2018; Ellis & Coppins 2019; Larsson Ekström et al. 2023). It is possible that forest lichens are facing an extinction debt in Estonia just now, and although the threat status of many forest lichens has increased during the last decade because of the drastic management activities in Estonian forests in this period, even more negative changes related to extinction debt can be expected if forest management strategies are not changed in the near future.

Thus, the proportion of taxa belonging to the group of elevated conservation concern is smaller among lichens preferring woodlands than among lichens preferring open habitats (Supplementary Material Fig. S3). Open habitats, especially calcareous grasslands which are extremely valuable habitats for rare lichens, have lost the majority of their area not during the last decades but during the last century (Helm 2019). The lichens inhabiting calcareous grasslands had the highest percentage of taxa of elevated conservation concern (69%; Fig. 6) among all habitat groups. The long-term decline is consistent with the effect of habitat loss, resulting in small and isolated populations that are now paying their extinction debt.

Air pollution, which has been considered a classic threat to many lichens (Nimis et al. 2002), is probably not responsible for the general negative changes in the current threat status of lichens. The levels of air pollution have not increased in Estonia over recent decades, whereas the emissions of SO₂, one of the main pollutants known to affect lichens in the previous century, have decreased considerably (Kohv et al. 2024). Other possible factors, such as indirect effects of eutrophication on oligotrophic sites (Provoost et al. 2011) and calcareous grasslands or effects of climate change on lichen communities (Ellis et al. 2007), have not been investigated in our region.

The RLI values, which were calculated to measure trends in the overall extinction risk for sets of species (Bubb et al. 2009), were low for both the set of all species and for just macrolichens, reaching values lower than 0.7 in 2023 (Fig. 4). For comparison, the national RLI values in Finland for different organism groups in 2019 varied from 0.981 (dragonflies and damselflies) to 0.774 (birds), with lichens having the lowest value (0.766) (Hyvärinen et al. 2019). The general trends, namely the vulnerability of lichens and decline in lichen species survival during the last decade, are similar in Estonia and Finland, while the decrease is steeper in Estonia (Fig. 4). This may partly be related to how the factors causing category changes were analyzed. In Finland, 83 genuine category changes were recorded for 1545 assessed lichen species (Hyvärinen et al. 2019), whereas we identified 101 genuine changes for 445 assessed species. We accepted the assessments of local experts and considered category changes non genuine only if there was a clear indication that the change was caused either by revised taxonomy, improved knowledge or methodological refinements. Such a strategy is more conservative as possible misinterpretations might cause the extinction risk of the studied group to be overrated, which seems less harmful than it being underrated. Furthermore, guidance for RLI national use suggests that a sample of c. 1500 species should be assessed both at a global and national scale in order to provide sufficiently robust trends (Bubb et al. 2009). Our data sets were considerably smaller and therefore may not be representative for calculating RLI. Although the conclusions based on the changes in RLI values may sometimes appear premature because these changes could be explained by alternative factors (Moreno Saiz et al. 2015), it is still useful to analyze the causes of category change and differentiate between genuine and non genuine changes during the red-listing process, as has been done, for example, in the latest Finnish Red List (Hyvärinen et al. 2019).

Correspondence of lichens’ Red List assessments between Estonian and selected European countries

Four European countries with updated national Red Lists, two north (Finland and Sweden) and two south (Denmark and the Czech Republic) of Estonia, were selected to investigate overlaps of Red List categories in their lichen biota, compared to the most recent Estonian data. Although the Swedish species list covered the highest number of lichenized taxa recorded in Estonia (922 species out of 942; Fig. 7), the overlap of species of elevated conservation concern in Estonia and Sweden was the smallest (100 species; Fig. 8). At the same time, only a small number of lichens which were assigned to LC categories in Estonia were assessed as RE, threatened or NT in Sweden (Fig. 8). The Swedish lichen biota is the richest of the five compared countries, with 2211 lichenized taxa recorded (Westberg et al. 2021), while c. 50% of the species are classified in the national Red List as NE due to insufficient knowledge of the taxa (G. Thor, personal communication). The comparison of species’ categories in the two Red Lists (Supplementary Material Table S2) demonstrates that many Estonian threatened species belong to the category NE in Sweden. In a small country like Estonia, without great climatic and vegetational zonation, the threat status of taxa can be more easily assessed.

Finland is another Nordic country with a rich lichen biota, consisting of 1713 lichenized species at the time of the latest red-listing (Pykälä et al. 2019). Around 100 species recorded in Estonia have not been reported from Finland (Fig. 7), but the overlap of elevated conservation concern lichens between Finland and Estonia is rather large (229 species) and the number of taxa assessed as RE, threatened or NT in Finland but LC in Estonia is moderate (48 species; Fig. 8). Unlike in Sweden, all recorded taxa were assessed against the IUCN criteria, meaning that no one species belonged to the category NE in Finland, which, however, caused a high number of DD taxa (Pykälä et al. 2019). We have followed the practice in Estonia where almost all recorded lichen taxa were evaluated using available data, considering only species with such uncertain data that both CR and LC could be plausible categories, were assigned to DD (IUCN Standards and Petitions Committee 2022).

The species checklists of the two countries located south of Estonia, Denmark and the Czech Republic, shared smaller numbers of lichenized taxa recorded in Estonia (637 and 756 species out of 942, respectively) than checklists of the compared northern countries (Fig. 7). Although Denmark and Estonia are of comparable size and are similarly flat countries, the overlap of the Estonian lichen checklist with assessed lichens in Denmark was the smallest (Fig. 7). This may be due to the denser population and more widely spread agricultural landscapes in Denmark, while Estonia is scarcely populated and has a higher proportion of forestland (Sirkas & Valgepea 2023). Natural conditions are considerably different in the Czech Republic as it is the most southern of the five countries, with a mountainous landscape. The Estonian and Czech Red Lists had the highest number of common lichens of elevated conservation concern, but also the highest number of species that were assessed as RE, threatened or NT in the Czech Republic but assigned to the LC category in Estonia (Fig. 8).

Some variation in applying IUCN categories and criteria in national listings may confuse direct international comparisons of Red Lists in different countries; nevertheless, closer examination of these lists can provide valuable information about the biodiversity threat levels in different countries. The comparison of categories assigned to individual species in different national Red Lists is often highly informative. For example, 20 taxa from the latest Estonian Red List belonged to the group of elevated conservation concern in all five compared countries (Table 3). These taxa are evidently threatened at least in the northern and north-western part of Europe and may be good candidates for the planned European Red List of Fungi. Furthermore, 11 species (Fig. 9) that were assessed as LC in all four compared countries but were assigned to a threatened or NT category in Estonia, deserve our reconsideration. The category determined on the basis of the criteria in national Red Lists can be downlisted if the national population is breeding or connected to a more viable population outside the country (IUCN 2012). Such downlisting has been used in the latest Finnish Red List (Hyvärinen et al. 2019) but not in Estonia so far (Lõhmus et al. 2019).