Recovery of the Critically Endangered Bracket Fungus Amylocystis Lapponica in the Estonian Network of Strictly Protected Forests

Recovery of the Critically Endangered bracket fungus Amylocystis lapponica in the Estonian network of strictly protected forests

K ADRI R UNNEL,INDREK S ELL and A SKO L ÕHMUS

Abstract In regions where primeval forests have vanished it Targets (Convention on Biological Diversity, ) provide is unclear whether forest protection can sustain specialized political support to improve this situation by further ex- old-forest biota, and over what time scale. We report on panding reserve networks, restoring degraded ecosystems, population expansion of an old-growth specific fungus of and preventing species extinctions. However, the targets do European conservation concern, Amylocystis lapponica,in not specify how to combine conservation options in practice the forest reserve network of Estonia. This conspicuous (e.g. Jørgensen, ; Venter et al., ). species was known for  years from only single records A central management problem in historically degraded, in one old-growth forest and was categorized nationally as but now protected forests is that old-growth qualities de- Critically Endangered. During the last  years A. lapponica velop slowly, and the prospects for old-forest biota depend has expanded over the eastern half of the country, with nine on unpredictable colonization and extirpation processes. In subpopulations, in  localities, now known, all in long- most countries protected forest networks have existed for protected old-growth forests and several .  km apart. only a few decades and thus have limited structural recovery In most of the new localities historical absence of the (e.g. Meyer & Schmidt, ; Paillet et al., ; Bujoczek species can be reliably assessed based on earlier surveys. et al., ). There is some evidence of broad-scale recovery The historical remnant subpopulation has also increased. of species with moderate old-forest associations within The population size (c.  mature individuals) in Estonia a few decades of the protection of secondary forests (e.g. indicates the species should be recategorized nationally as Vandekerkhove et al., ; Deinet et al., ; Romero Endangered. This success story suggests that more than et al., ), but such recoveries depend on species’ life his-  years of non-intervention may be needed even in large tory traits,locationofsourcepopulations, and dispersal capa- old-forest reserves for old-growth specialist species to bilities (Sverdrup-Thygeson et al., ). Non-intervention recover. management has also enabled a disturbance-phase specialist fungus to spread across large naturally disturbed areas Keywords Amylocystis lapponica, bracket fungus, forest, (Bässler & Müller, ). However, for the most demanding fungal conservation, old growth, Picea abies, refuge popula- old-forest species broad-scale recoveries attributable to tion, succession reserve network initiatives have not been described. Supplementary material for this article is available at Here, we report on population expansion of an old- https://doi.org/./S growth specific fungus Amylocystis lapponica (Agarico- mycetes, Polyporales, Polyporaceae) in the forest reserve network of Estonia. Although its preliminary global Red n many developed countries a major conservation List status is Least Concern (IUCN, ), in Europe it is Ichallenge is to sustain old-forest biota despite historical one of the  threatened fungi recommended for listing in loss of natural forests. Most European countries retain , % the Bern Convention (Dahlberg & Croneborg, ). In of their primary forest (Sabatini et al., ) and reserves the last  years this species has been recorded in eight already cover . % of current forest area (Forest Europe, European countries, with the majority of the population ). In degraded forests many old-forest specialist species in the boreal zone. Outside the boreal zone, this species is may not be viable and will be extirpated unless their habitat only present in a few refugia in the best-preserved Central is restored (Hanski, ). The global Aichi Biodiversity European primeval forests (Holec & Kučera, ). In Estonia (the hemiboreal zone) A. lapponica was known for  years from a single old-growth patch (Parmasto, ), KADRI RUNNEL (Corresponding author, orcid.org/0000-0002-7308-3623) has been categorized as Critically Endangered since , Department of Zoology, Institute of Ecology and Earth Sciences, University of   Tartu, Vanemuise 46, EE-51014 Tartu, Estonia. E-mail [email protected] when first assessed (Lilleleht, ; Lõhmus et al., b), and is legally protected. INDREK SELL MTÜ Puuseen, Tartu, Estonia  Forests currently cover % of Estonia’s , km land ASKO LÕHMUS Department of Zoology, Institute of Ecology and Earth Sciences,  ,   University of Tartu, Tartu, Estonia area but old natural stands cover only %( km ), over half of which is in reserves (Raudsaar et al., ). Before sig- Received  January . Revision requested  February . Accepted  April . First published online  September . nificant spread of agriculture, c.  BCE, forest cover was

Oryx, 2020, 54(4), 478–482 © 2019 Fauna & Flora International doi:10.1017/S0030605319000334 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.219, on 29 Sep 2021 at 03:06:44, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605319000334 Critically endangered bracket fungus 479

probably at least %; spruce forests are a major ecosystem potential localities have been monitored by IS during of the east and south (Laasimer, ). At least % of land –. The fruit bodies of A. lapponica are easily detect- has remained long-term forest (although repeatedly logged), able when mature and fresh (Lõhmus, ), but parts and other forests are either th century reforestations (vari- of juvenile or old fruit bodies that could not be reliably ous types of agricultural lands) or new forests on drained identified have been collected for microscopy. Substrate wetlands. descriptions of the records were made on-site, but stand In the second half of the th century most Estonian characteristics are reported according to the National forests were managed with a medium-intensity semi-natural Forest Registry (based on geographical coordinates of the approach, which maintained tree species diversity and records). relatively high volumes of dead wood. As a consequence, The synthesis of these datasets reveals a recent expansion many generalist old-forest species could inhabit production of A. lapponica from a single forest reserve to other long- forests (e.g. Lõhmus et al., ; Runnel & Lõhmus, ). protected parts of the national network of protected forests. Nevertheless, several highly specialized species, including Its fruit bodies were first discovered in eastern Estonia in A. lapponica and other fungi of spruce-dominated forests, ,ina-ha old-growth patch, protected since  remain highly threatened in protected old-forests or have (the first Estonian forest reserve) and surveyed by mycolo- already become regionally extinct (Runnel & Lõhmus, ; gists since the s. Despite frequent visits to this reserve, Lõhmus et al., b). the species was re-recorded on a single trunk only in , The Estonian network of strictly protected forests devel- ,  and . The findings became annual from oped slowly from  until the s, without central plan-  (three records), and with  records in , the ning (Tuvi et al., ). Later focused developments include species had spread over most of the reserve. designation of Natura  sites of European importance During – there were a total of  additional re- and, nationally, targeting minimum areas for old-growth cords. The number of known subpopulations (here defined forest species in each forest type (Lõhmus et al., ). as localities separated by .  km) expanded to nine (Fig. ); The area of strictly protected forests increased from c. % these include  separate localities (contiguous forest areas of forest land in the early sto%in and %by with records typically ,  km and no more than  km  (Lõhmus et al., ; Raudsaar et al., ). However, apart). In  two records were made in Muraka nature re- reflecting general forest history, few of the strictly protected serve (north-eastern Estonia), which is probably the largest sites include any primeval forest and . % of their total surviving primeval spruce forest in the country (officially area will still be ,  years old by  (Lõhmus, ). protected since ; surveyed by mycologists since the Recently intensified timber harvesting has fragmented the s). In  another locality . km away and another landscapes and isolated the strictly protected sites (Forest subpopulation  km away were discovered. In , two Europe, ; Lõhmus, ). new subpopulations were found elsewhere in Estonia: in The A. lapponica material we analysed is based on fruit- Alam-Pedja Nature Reserve in east-central Estonia (de facto body records from three main sources, and survey histo- protected since  when it became a Soviet military ries in these localities to evaluate historical absences area) and in old-growth stands in Karula National Park, (Supplementary Material ). () All casual collections of southern Estonia (officially protected since ). There Estonian polypores are documented in public database were a total of  records in , all in long-protected for- Plutof (Abarenkov et al., ). Polypores have been well ests and most in previously surveyed areas (Supplementary surveyed since the s in Estonian forests, with emphasis Material ). These records included four additional subpo- on old forests and rare species. Parmasto () published pulations, all to the west of previously known records, and all material up to  (. , records), mostly collected thus the species’ known western range in Estonia has shifted by professional mycologists. Later data include increasing from °E in  to °E in . contributions from amateur mycologists, national moni- All fruit bodies were found on medium to well-decayed toring activities, and results of fungal surveys in several downed Norway spruce Picea abies trunks (diameter at protected forest areas. () Over , polypore records breast height – cm). The  forest stands inhabited originate from c.  systematic stand-scale surveys during were either mesic to eutrophic highly productive stands –, representing the main forest types and stages of on mineral soil ( stands; site types ranging from Oxalis– forest age and naturalness. The survey method detects local Rhodococcum to Aegopodium) or old drained peatland species pools and also documents species absences (Lõhmus forests ( stands). Their common feature was a developed et al., a). This dataset has been instrumental in assessing old-growth structure, with variable coverage of spruce the national conservation status of polypores (Runnel & in the overstorey (–%). Six stands had a dominant tree Lõhmus, ; Lõhmus et al., b). () A. lapponica is layer ,  years old; this was a result of natural succession the most strictly protected (Category I) species under the after historical disturbance or natural replacement of old- national Nature Conservation Act, and its confirmed and growth spruce forest with nemoral broad-leaved trees.

FIG. 1 Distribution of Amylocystis lapponica subpopulations in Estonia (discovery year/total no. of records). Light grey indicates forests, dark grey indicates strictly protected forests. The graph shows the annual number of records and cumulative no. of known localities, –.

Based on annual maximum numbers of recent records, likely to attractive habitats (in this case old-growth forests); we estimate that A. lapponica currently inhabits .  spruce to confirm that such visiting bias (cf. Lõhmus & Lõhmus, trunks in the  known Estonian localities, with c.  ma- ) did not undermine documentation of the actual dis- ture individuals (Dahlberg & Mueller, ). It should thus tribution of A. lapponica, we used a separate sampling be categorized nationally as Endangered under criterion D, scheme representing less attractive habitats (e.g. younger based on population size (IUCN, ). Given the adequate forests; Runnel & Lõhmus, ). Despite careful synthesis protection of existing localities and the population increase of multiple data sources, only one location was known for observed, the species has potential to improve nationally to the first  years of the survey history and the expansion Vulnerable (in terms of population size). However, the re- of records was not related to parallel expansion of site visits. cords also confirm the species’ strict requirements for long- The qualities of the Estonian strictly protected forest developed natural forest (Dahlberg & Croneborg, ; network that have supported A. lapponica require study. Holec & Kučera, ; Nordén et al., ). Such habitats The network’s extent facilitated the species’ range expansion have almost vanished outside strictly protected forests and (Fig. ) and the presence of old-growth forest was needed for the improving status of A. lapponica depends on a network formation of local populations that could act as future of such forests. Given the long history of spruce-dominated sources, but we cannot yet explain the historical absences old-growth ecosystems in Estonia (Reitalu et al., ), it is of A. lapponica in those patches and the species’ relatively thus plausible that A. lapponica passed a population bottle- rapid spread. We suggest, however, that the explanation neck in Estonia during the unprecedented forest loss of the lies in the dramatic socio-economic changes in forest man- first half of the th century (e.g. Meikar & Etverk, ). agement in the s, which reversed forest loss (increasing However, there are no mycological records available to attest landscape connectivity; cf. Penttilä et al., ), and reduced to its status in preceding centuries. timber harvesting and local forest use (e.g. Tomson et al., We highlight the data quality of our assessment, which ). Several localities appear to have become de facto pro- includes long-term monitoring in key locations, systematic tected during this time, even if forest reserves and the net- surveys, and the availability of all historical data. Specifically, works for strictly protected forests were only established we used the significance of the species to assess absences later. Thus, habitat development for A. lapponica may re- based on site visits: iconic species are likely to be reported quire .  years of non-intervention even in old stands. whenever specialists visit the sites (see also Halme et al., The exact reasons for such long time delay, opportunities ), and documentation of all records of this species is le- for active habitat restoration, and the role of dispersal gally required in Estonia. Frequent visits are, however, more sources are unknown. At least in north-east Estonia,

there may have been eastern cross-border colonization, but International and the European Bird Census Council. Zoological the recent accelerated spread of the species (Fig. ) indicates Society of London, London, UK.  ’  an increasing role of local dispersal. Our findings indicate FOREST EUROPE ( ) State of Europe s Forests . Ministerial Conference on the Protection of Forests in Europe, Madrid, Spain. that, for fungi, the merits of non-intervention management HALME, P., HEILMANN-CLAUSEN, J., RÄMÄ, T., KOSONEN,T.& regimes and large strictly protected forest networks may KUNTTU,P.() Monitoring fungal biodiversity–towards an become evident only in the long term, and therefore research integrated approach. Fungal Ecology, , –. on such species requires a combination of species indicators, HANSKI,I.() Extinction debt and species credit in boreal forests: monitoring schemes and historical data. modelling the consequences of different approaches to biodiversity conservation. Annales Zoologici Fennici, , –. HOLEC,J.&KUČERA,T.() Remarks to the ecology of the Acknowledgements Long-term data on Estonian forest fungi have boreo-montane polypore Amylocystis lapponica based on data from been collected by many local and visiting mycologists. We specifically the Czech Republic and Poland. Acta Mycologica, , –. thank Urmas Ojango for his records from north-east Estonia. Financial IUCN () IUCN Red List Categories and Criteria: Version .. support to KR and AL was provided by the Estonian Research Council IUCN Species Survival Commission, IUCN, Gland, Switzerland. (grant IUT 34-7). IS has been financed by the Estonian Environmental IUCN () List of Preliminary Assessed Fungal Species. IUCN Global Agency and Environmental Board (national programme for moni- Fungal Red List Initiative. http://iucn.ekoo.se/iucn/species_list/ toring biodiversity and landscapes, during 2008–2018) and the #tab-species-list-thumbs-assessment-prel [accessed  November Environmental Investment Centre (mycological surveys in various ]. conservation areas during 2015–2018). We thank Agu Leivits for JØRGENSEN,D.() Ecological restoration in the Convention commenting on the text, and two anonymous reviewers for their on Biological Diversity targets. Biodiversity and Conservation, constructive comments. Collecting was permitted by the Estonian , –. Environmental Board (permit no. 1-1/16/354 for sampling protected LAASIMER,L.() Vegetation of the Estonian SSR. Valgus, Tallinn, species); all collected material is stored in the fungal collections Estonia. TAAM and TU. 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