Status and distribution of stipitate hydnoid fungi in Scottish coniferous forests

Biological Conservation 107 (2002) 181–192 www.elsevier.com/locate/biocon

Status and distribution of stipitate hydnoid fungi in Scottish coniferous forests A.C. Newtona,*, E. Holdenb, L.M. Davyc, S.D. Wardd, L.V. Flemingd,1, R. Watlinge a

Institute of Ecology and Resource Management, University of Edinburgh, Kings Buildings, Mayfield Rd., Edinburgh EH9 3JU, UK b Allanaquoich, Mar Lodge Estate, Braemar, Ballater, Aberdeenshire AB35 5YJ, UK c 16 Pepys Way, Girton, Cambridge CB3 OPA, UK d Scottish Natural Heritage, 2 Anderson Place, Edinburgh EH6 5NP, UK e Caledonian Mycological Enterprises, 26 Blinkbonny Avenue, Edinburgh EH4 3HU, UK Received 28 August 2001; received in revised form 9 January 2002; accepted 15 January 2002

Abstract Stipitate hydnoid fungi (specifically members of the genera Bankera, Hydnellum, Phellodon, Sarcodon) have become the focus of increasing conservation concern, particularly following the detection of widespread declines in abundance. To assess their status in Scotland, 103 field surveys were undertaken, including searches of 50 of the 77 native pinewood sites, traversing a total of 902 km. Hydnoid fungi were encountered on 30 of the searches (29%), primarily in eastern regions of Scotland. A maximum of 8 species was recorded on a single search, 11 species being encountered in total. Of 22 plantation sites surveyed, 11 were found to contain populations of hydnoid fungi. Four species were relatively widespread, both in native woodlands and plantations: Bankera fuligineoalba, Hydnellum peckii, Phellodon tomentosum, and Sarcodon imbricatus. All species tended to be associated with particular microsites, especially riverbanks, tracksides or areas of exposed mineral soil; median values for percentage bare ground cover surrounding each sporome were generally above 50%. Median values for diameter at breast height (dbh) of associated trees were in the range 20–50 cm for all species. Data from the field surveys were pooled with previous records to assess the number of hydnoid species recorded for each native pine woodland. When examined by regression, a positive relationship was recorded between the number of species and woodland area (r2=0.69, P< 0.001, n=50). To assess the occurrence of declines, the number of 10 km gridsquares for each species was compared using records made pre- and post-1970. These data provided evidence for declines in only four of the 17 species considered. However, 12 species are threatened with extinction according to the IUCN Red List criteria, owing to their restricted patterns of distribution. The implications of these results for the conservation of hydnoid fungi in Scotland are discussed. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: Biodiversity Action Plan; Conservation; IUCN Red List; Ectomycorrhiza; Pinewood

1. Introduction Ectomycorrhizal fungi have become the focus of increasing conservation concern in recent years (Arnolds and de Vries, 1993), particularly after substantial declines were detected in the abundance of many taxa in western and central Europe (Feliner, 1989; Arnolds, 1991; Jansen and van Dobben, 1987; Lizon,

* Corresponding author. Present address: UNEP-World Conservation Monitoring Centre, 219 Huntingdon Road, Cambridge CB3 ODL, UK. E-mail address: [email protected] (A.C. Newton). 1 Present address: JNCC, Monkstone House, City Road, Peterborough PE1 1JY, UK

1993). The causes of these declines remain unclear, although both habitat loss and aerial pollution appear to have been contributory factors (Jansen and van Dobben, 1987). Particular concern has been directed towards stipitate hydnoid fungi, a taxonomically heterogeneous group of taxa [including the genera Bankera, Phellodon (Bankeraceae), Hydnellum and Sarcodon (Thelephoraceae)] which share the common characteristic of a toothed hymenophore (the origin of their common epithet, ‘tooth fungi’; Marren and Dickson, 2000). Evidence suggests that declines of hydnoid fungi have been particularly pronounced compared with other groups of fungi. For example in the Netherlands, Arnolds (1989) reported that since the early 1970s eight species have

0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(02)00060-5

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become extinct, the ranges of six species have declined by 90% or more, and the remaining seven species have suffered declines of between 58 and 87%. Similarly, in the Czech Republic, a considerable decline in occurrence has been reported for virtually all the species of this group over the past few decades (Hrouda, 1999). Stipitate hydnoid fungi are included on the Red Lists of a number of European countries, including the Netherlands, Poland, Germany and the UK (Lizon, 1993, 1995). In response to this concern, a Priority Species Action Plan was developed for 14 species of hydnoid fungi considered to be threatened (Anon, 1999), as part of the Biodiversity Action Plan developed by the UK (Anon, 1994) towards implementing the Convention on Biological Diversity (UNEP, 1992). The Plan highlighted the fact that the distribution and status of these fungi in the UK are still poorly understood (Anon, 1999). Such information is required for providing a baseline for assessing future changes in pattern of distribution or abundance, and for defining appropriate approaches to habitat management to ensure their effective conservation. The Plan also identified the need to evaluate the ability of these fungi to colonise newly available habitat, a critical issue given the current efforts to expand areas of native woodland in areas of the UK such as Scotland (Newton and Humphrey, 1997). At present, no evidence is available to assess whether hydnoid fungi are declining in the UK, and very little information is available concerning their ecological requirements. The aims of the current investigation were to assess the current distribution of stipitate hydnoid fungi in Scottish coniferous forests, and to define the principal characteristics of the habitat in which they occur. The native pine forests of Scotland are considered to be the most important stronghold for many of the species in this group within the UK, some taxa apparently being restricted to this habitat (Anon, 1999; Watling, 1997). However, no systematic survey of fungi in native pinewoods has ever been undertaken. In fact, no mention is made of ectomycorrhizal fungi in any of the key ecological accounts of native Scottish pinewoods which have been published (Aldhous, 1995; Steven and Carlisle, 1959; Bunce and Jeffers, 1977), despite their international conservation importance (Watling, 1997). In particular, this investigation was designed to test the following hypotheses: that hydnoid fungi in Scotland are: (1) restricted to forest stands that are relatively mature (> 40 years old), as recorded in the Netherlands (Arnolds, 1989); (2) restricted to long-established native pine woodland, displaying limited capacity to colonise plantations; (3) undergoing a decline in abundance; (4) threatened with extinction. To test these hypotheses, a field survey was undertaken of coniferous forests throughout Scotland, supported by analysis of herbarium accessions and previous records of these fungi.

2. Methods 2.1. Collation of existing records An attempt was made to collate Scottish records of hydnoid fungi from a comprehensive list of sources identified at the outset of the project, including: 1. The British Mycological Society (BMS) Foray Records Database. This database respresents the main national repository of fungal records, and mostly includes records made on official BMS forays, some personal records of individuals and data from published BMS foray lists collated by the Joint Nature Conservation Committee (JNCC; Cannon, 1998). 2. The Scottish Natural Heritage (SNH) Cairngorm fungal database. The database is largely based on the personal records of Professor Roy Watling, together with published lists, mostly from the Cryptogamic Society (now Botanical Society) of Scotland (Watling et al., 1995, 1996). 3. Foray lists of the Cryptogamic Society of Scotland published in the Annual Reports of that organization, and those of its successor the Botanical Society of Edinburgh published in the Transactions of the Society (see Watling, 1983a, b for full listing). 4. The national mycological herbaria at the Royal Botanic Gardens of Kew and Edinburgh. Both herbaria were visited (by RW), and details obtained of all accessions from Scottish locations. 5. Records of individual mycologists with experience of recording fungi in Scottish coniferous forests, who were contacted and records requested. 6. All local SNH offices and Biological Records Centres (BRC) in Scotland, who were contacted and asked for any records of hydnoid fungi on file. 7. Other published accounts of Scottish fungi, including: Silverside (1991; Clyde Valley), Dennis (1986; Hebrides), Henderson and Watling (1978; Mull), Watling (1970; Rum), Watling (1983c; Hebrides), Watling (1985; Mull), Watling (1992; Shetland), Watling et al. (1999; Orkney). All records obtained were cross-checked and incorporated into a database written in Microsoft Access v. 2.0 following the BMS standard recording format. 2.2. Field survey To assess the pattern of distribution of hydnoid fungi at the scale of individual forest stands, four survey plots were established in native pinewood stands where hydnoid fungi were located during a pilot survey, at sites distributed throughout the known range of the species

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in Scotland. Survey plots of 2040 m, 6060 m, 2020 m and 20120 m were marked out in Sites 1–4, respectively, using measuring tapes. Plot dimensions varied according to the characteristics of individual sites. Within each plot, all individual hydnoid sporomes visible on a single visit were mapped to the nearest 5 cm, together with major features such as streamsides and tracks. Results from this preliminary survey indicated that sporomes of hydnoid fungi tend to be associated with particular microsites, characterised by exposed mineral soil relatively free from organic material, and sandy, gravelly or shingle substrates in particular. These microsites were particularly associated with streamsides, tracksides, gravel pits or quarries, shingle banks and road cuts. To assess the current pattern of distribution of hydnoid fungi in Scottish coniferous forests, a survey was then undertaken of sites distributed throughout Scotland. Collation of previous records indicated that most existing records had been derived from a limited number of pinewood sites. The majority of Scottish native pinewoods appear never to have been surveyed for fungi. An attempt was therefore made to visit as many pinewood sites as possible, to assess the occurrence of hydnoid fungi. Woodlands were selected using the Caledonian Pinewood Inventory produced by the Forestry Commission in the UK (Forestry Commission, 1994), and all sites for which access permission was granted were visited. These sites were supplemented by surveys undertaken in a limited number of plantation forests, particularly focusing on those established on former pinewood sites or on sites for which hydnoid fungi had been recorded previously. The locations of older records were explicitly targeted to provide an indication of whether hydnoid species are declining in these areas. As the objective was to ascertain whether hydnoid fungi were present at each site, and given that these species are patchily distributed, a non-systematic approach to sampling was adopted. The surveys involved a timed, haphazard search, following the intuition of the searchers, all of whom were experienced field mycologists. Each site was searched as thoroughly as possible, but areas of disturbed or exposed soil (such as soil pits, riverbanks, roadcuts, vehicle tracks, gravel banks, etc.) were explicitly targeted. Sporomes of hydnoid fungi tend to occur in discrete groups or clusters, and therefore the number of sporome groups of each species encountered during a search was recorded. Such sporome groups are henceforth referred to as ‘colonies’, although it is recognised that this term strictly applies to the mycelium, which was not assessed directly. The route taken during each search was mapped, and the total length of the search estimated directly from the map.

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Searches were undertaken annually over 3-year period (1998–2000) and were timed to coincide with the main period of sporome production (September–October) as indicated by the appearance of sporomes at a reference site that was visited at least twice a month. To assess the characteristics of sites with populations of hydnoid fungi, when colonies were encountered, 1010 m survey plots were marked out centred on the sporomes located. The tree species present within each plot were identified and the diameter at breast height (1.3 m) of each individual tree measured using measuring tapes. To assess microsite characteristics, survey plots of 11 m were marked out, again centred on the sporomes, and the percentage cover of different vascular plant species in the ground vegetation, and the percentage cover of bare ground, were estimated visually. Records made during the field survey were entered into the database created by the project. Distribution maps were then generated on a 10 km grid using DMAP software (v. 7.0, Dr Alan Morton, Berkshire, UK) using the combined data. Using pooled data, the number of 10 km gridsquares for which records were made both pre- and post-1970 was calculated for each individual species, to provide an indication of trends in abundance. The number of 10 km squares for which species were recorded post-1970 was used to assess the status of the species according to the IUCN Red List categories of threat (IUCN, 1994). Voucher speciments were deposited in the herbarium of the Royal Botanic Garden, Edinburgh, UK. Statistical analyses included the use of t-tests (to examine the difference between species in microsite characteristics) and regression (to examine the relationship between woodland area and number of species), undertaken using SigmaPlot v. 5.0 (SPSS Inc.).

3. Results 3.1. Collation of existing data The database constructed for this project incorporated 782 records of 17 species. Relatively few records were obtained from published lists or from written requests to local SNH offices and BRCs, although the response rate was high ( > 90%). Most of the BRCs hold very few fungal data. Although a substantial number of records (540) were included in the BMS database at the outset of the project, at least 15% of records were found to be duplicates, and in addition at least 10% contained errors (e.g. in placename or grid reference). Records were therefore systematically cross-checked, and those which were duplicates or with missing or uncertain locality information were deleted. Collation of previous records raised a number of taxonomic issues. Hydnoid fungi are a critical group

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and have been associated with a high degree of taxonomic confusion (Pegler et al., 1997). Records bearing the names Hydnellum, mirabile, H. velutinum, H. gracilipes and H. cumulatum were either ignored or, where possible, synonymised, as these names are either no longer current or refer to species which are no longer considered to be native to Britain (Pegler et al., 1997; Newton et al., 2002). Synonymisation was only possible for those records supported by a voucher specimen; all the specimens in the national herbaria (RBGE and RBGK) were re-examined for this purpose (by RW). Any records bearing these names which were not supported by voucher specimens in the national herbaria were ignored for the purposes of this project. Records of H. compactum and H. diabolum not supported by voucher specimens were referred to H. caeruleum and H. peckii, respectively, following Pegler et al. (1997). Nomenclature throughout follows Pegler et al. (1997). 3.2. Field survey The intensive surveys of sporome distribution within individual forest stands indicated that sporomes of hydnoid fungi tend to be associated with areas of exposed mineral soil, particularly riverbanks or tracks (Fig. 1). In three of the four sites surveyed, all of the sporomes encountered were located within 3 m of either a pathside or a riverbank. On the fourth site (data not illustrated), those sporomes not within 3 m of a path were associated with a steep, unvegetated bank located in an abandoned gravel pit. These data also indicate that species of hydnoid fungi often occur together. Three and four species were recorded in the plots established on Sites 1 and 2, respectively (Fig. 1a, b); in the plots established on Sites 3 and 4, five and seven species were recorded respectively (data not illustrated). Over the 3 years of the project, 103 field surveys were undertaken, including searches of 50 of the 77 native pinewood sites (i.e. 65%) listed on the Caledonian Pinewood Inventory (Forestry Commission, 1994). The total duration of the searches was approximately 602 person-hours, and a total of 902 km was traversed. The survey sites were distributed over sixty-two 10 km gridsquares, 23 of which yielded records of hydnoid fungi (Fig. 2). Those 10 km squares which yielded records of hydnoid fungi tended to be distributed primarily in eastern regions of Scotland (Fig. 2). A maximum of eight species was recorded on a single search, 11 species being encountered in total. On 73 of the searches (7 1%), no sporomes of hydnoid fungi were encountered. Of the 22 plantation sites surveyed, none of which were located on sites listed in the Caledonian Pinewood Inventory, 11 were found to contain populations of hydnoid fungi. In total, seven species were found in association with plantations (Fig. 3); a maximum of five

species was recorded on a single visit to an individual plantation site. Comparison of the relative abundance of the different species, as indicated by the number of sites in which a species was encountered, indicates that four species were relatively widespread: Bankera fuligineoalba, Hydnellum peckii, Phellodon tomentosum and Sarcodon imbricatus. Each of these species was present on at least 13 sites; none of the other species were encountered on more than six sites (Fig. 3). On sites which hydnoid fungi were recorded, the number of colonies encountered was most commonly either one or two. However, some species were more abundant on particular sites; for example a maximum of 16 colonies of Phellodon tornentosum were recorded on an individual site. Corresponding maxima for B. fuligineoalba and Hydnellum peckii were 11 and eight respectively; none of the other species ever numbered more than five colonies per site on one visit. As some species were only rarely encountered (e.g. Hydnellum aurantiacum, H. caeruleum, Phellodon niger, Sarcodon glaucopus), the available data were too limited to define site characteristics with precision for all species. However, an overall comparison of the different species suggested that they do not differ substantially in their microsite preferences. For example, median values for dbh were in the range 20–50 cm for all species (Fig. 4a). Although both B. fuligineoalba and S. imbricatum were both recorded in very mature pine stands one on occasion (mean dbh > 80 cm), all species were most commonly associated with much smaller trees. Mean dbh values ( 95% confidence limit) ranged from 24.1 (  6.5) in H. peckii to 43.1 (  17.3) in H. ferrugineum. No significant differences (at P=0.05) were recorded between species when mean dbh values were compared using t-tests. Similarly, median values for percentage bare ground cover surrounding each sporome were generally above 50%, although values for some species (H. ferrugineum, H. aurantiacum, H. caeruleum and S. glaucopus) were below this threshold (Fig. 4b). The cluster of values around 50% was a consequence of the tendency of sporomes to occur precisely on the margin of a path or track. Even in situations where sporomes were not situated in areas of bare ground, the cover of vascular plants tended to be relatively low; often such sites were dominated by bryophytes or (less often) lichens. The most abundant vascular plant species in the ground flora present near to sporomes of hydnoid fungi were Calluna vulgaris and Vaccinium myrtillus (data not illustrated). Data from the field surveys were pooled with previous records to assess the number of hydnoid species recorded for each native pine woodland listed on the Caledonian Pinewood Inventory (Forestry Commission, 1994) for which data were available. When examined by regression, a positive relationship was recorded between the

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Fig. 1. Spatial pattern of distribution of sporomes of hydnoid fungi within two individual native pinewood stands, located in (a) Strathglass area (Site 1) and (b) Speyside, Scotland (Site 2). Key to symbols: (a) small filled circle, Hydnellum ferrugineum; open circle, Phellodon niger; large filled circle, Sarcodon glaucopus; (b) oval, Bankera fuligineoalba; star, Hydnellum peckii; rectangle, Phellodon tomentosus; filled circle, Sarcodon imbricatus.

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Fig. 3. The relative abundance of different species of hydnoid fungi recorded on the field surveys, as indicated by the number of sites for which each species was recorded. Black bars: number of semi-natural woodland sites; hatched bars: number of plantation sites.

4. Discussion Fig. 2. Distribution of field sites surveyed, plotted on a 10 km grid (Ordnance Survey). Filled circles indicate sites for which hydnaceous species were recorded; empty circles indicate sites for which no hydnoid fungi were encountered.

number of species and woodland area (r2=0.69, P < 0.001, n=50; Fig. 5). When only those sites in which hydnoid fungi had been recorded were included in the analysis, a slightly lower value of r2 was obtained (0.48), although the regression was still highly significant (P < 0.001, n=12). Although all species (with the exception of Bankera violascens) were recorded in native woodland, on the basis of the pooled data, 13 of the 17 species considered here were also found to have been recorded from a plantation site on at least one occasion (Table 1). Comparing the number of 10 km gridsquares pre- and post-1970, based on pooled data, four species registered a decline, whereas 11 species registered an increase, two species remaining unchanged (Table 1). On the basis of current (post-1970) distribution, according to the IUCN Red List Criteria (IUCN, 1994), Bankera violascens and H. spongiosipes could be considered Critically Endangered in Scotland (restricted to a single locality); H. aurantiacum, H. auratile, H. concrescens, Phellodon confluens and S. scabrosus could be considered Endangered (< 5 localities), and H. caeruleum, H. scrobiculatum, Phellodon melaleucus, Phellodon niger and S. glaucopus could be considered Vulnerable (< 10 localities). The other five species (see Table 1) would not be considered threatened according to these criteria.

This research represents the first attempt to provide a comprehensive account of the pattern of distribution of hydnoid fungi in Scotland. Results indicate that these fungi are predominantly found in the native pinewoods of eastern and central areas, most notably Speyside and Deeside. Very few records of these fungi are available for pinewoods in southern or western areas. The reasons for this pattern of distribution are unclear. It is possible that climatic factors are partly responsible, eastern pinewoods tending to receive lower rainfall than those situated further west (Steven and Carlisle, 1959). The contrasting postglacial history of eastern and western pinewoods in Scotland (Sinclair et al., 1998) may also have been influential. One contributory factor to this pattern is undoubtedly recorder bias. Although there has been a long history of fungal exploration in Scotland (Watling, 1983a, b, 1986, 1997), attention has focused on a relatively small proportion of sites. For example, significant mycological forays were held in the Speyside area in 1890, 1900, 1912 and 1927 (Watling, 1983a, b), which generated a number of early records of hydnoid taxa. The native pinewoods of this area have been repeatedly visited for more than a century and are now relatively well known mycologically. However, many native pinewoods, such as the majority of those in western areas, appear never to have been surveyed for fungi. It is this bias in recording effort that the field survey described here sought to redress. Few fungal surveys have been undertaken in the UK with the aim of mapping species distributions (Mitchel and Wright, 2000). Most analyses of fungal distribution

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Fig. 4. The microsite characteristics associated with sporomes of hydnoid fungi as recorded in the field survey, with respect to (a) diameter at breast height (dbh) of neighbouring trees, and (b) the percentage cover of bare ground. These data are illustrated as box plots; the line inside the box represents the median, the box extents indicate the 25th and 75th percentiles; capped bars indicate the 10th and 90th percentiles, and symbols mark data outside the 10th and 95th percentiles.

Fig. 5. The relationship between number of hydnoid fungal species and woodland area. Data for number of species were derived from field survey data pooled together with all available previous records. The sites examined were those listed on the Caledonian Pinewood Inventory (Forestry Commission, 1994), which was also used as a source for the area estimates. Results of regression analysis: r2=0.69, P <0.001, n=50; equation: y=0.00593x 0.268.

(e.g. the Gasteromycetes, Pegler et al., 1995) have relied upon collation of records made casually by individuals or on organised forays (Watling, 1990; Cannon, 1997). Although a substantial effort was made in the field survey

to improve on the geographical coverage of previous records, the results must clearly be interpreted with caution. Even though a survey methodology was adopted which maximised the probability of locating the

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Table 1 Status of hydnoid fungi in Scotlanda Name

No. 10 km sq in Scotland pre-1970

No. 10 km sq in Scotland post-1970

Recorded from plantation forestsb

Associated host speciesb

Bankera fuligineo-alba Bankera violascens

14 0

15 1

Yes Yes

Pine (Pinus sylvestris) Norway spruce (Picea abies)

Hydnellum auratile Hydnellum aurantiacum Hydnellum caeruleum Hydnellum concrescens

0 5 9 8

2 3 8 2

No Yes Yes Yes

6 10 3 0

12 17 5 1

Yes Yes Yes No

Pine Pine Pine and Arctostaphylos uva-ursi Oak (Quercus sp.); occurrence in association with pine needs confirming Pine Pine and possibly birch (Betula sp.) Pine Oak

Phellodon confluens Phellodon melaleucus

2 6

2 5

No Yes

Phellodon niger Phellodon tomentosus

3 6

9 14

Yes Yes

Oak; association with pine needs confirming Generally associated with pine but apparently also broadleaves (oak, birch) Pine, spruce (Picea spp.) and oak Pine; also Douglas fir, Pseudotsuga menziesii

Sarcodon glaucopus Sarcodon imbricatusc Sarcodon scabrosus

0 14 2

7 24 2

No Yes Yes

Pine Pine Pine

Hydnellum ferrugineum Hydnellum peckii Hydnellum scrobiculatum Hydnellum spongiosipes

a

The number of 10 km squares refers to the total number of grid squares plotted using the Ordnance Survey coordinates for the UK, using the pooled data both for the field survey and records collated from other sources. b Based on both survey data and compilation of previous records. Excluded species, not currently considered native to Scotland (Pegler et al., 1997, Newton et al., 2002): Hydnellum compactum, H. mirabile, Sarcodon fuligineoviolaceus, S. regalis, S. versipellis. c Scottish records may all be referable to S. squamosus (Johannesson et al., 1999) but this requires confirmation (Newton et al., 2002).

target species, absence of records from a particular site does not reliably indicate whether or not the fungus is actually present. Production of sporomes is highly seasonal, and many fungal species only fruit sporadically. Such behaviour implies that many years surveying activity may be required to detect the presence of certain species in a particular area, and greatly complicates the collection of quantitative information on fungal distribution and abundance (Watling, 1990, 1995; Cannon, 1997). With these caveats, the survey data suggest substantial differences between hydnoid species in their relative abundance. In particular, Bankera fuligineoalba, Hydnellum peckii, Phellodon tomentosum and Sarcodon imbricatum appear to be markedly more widespread than the other taxa native to Scotland. Other species, particularly Hydnellum aurantiacum, H. auratile, Sarcodon glaucopus and S. scabrosus, appear to be substantially less abundant, in terms of the number of localities, and should therefore be accorded higher conservation priority in future. The results also indicate clearly that many hydnoid species are not restricted to native (semi-natural) pinewoods, but may also occur in plantations. For example in the field survey, seven species were located on plantation

sites. This finding has important implications for the conservation of these fungi in Scotland. At present, substantial efforts are being directed towards the expansion of native pinewood areas, both through planting and encouragement of natural regeneration (Aldhous, 1995; Newton and Humphrey, 1997). Although little information is available concerning the ability of fungi to colonise newly available habitat, the availability of a nearby source of colonists may be of particular importance. For example, Humphrey et al. (2000) found that the number of threatened fungal species encountered in Scottish plantation forests was inversely related to the distance from the nearest native pinewood. The association of hydnoid fungi with pine woodland reflects their status as mycorrhizal symbionts of Pinus sylvestris (Danielson, 1984; Visser, 1995; Pegler et al., 1997). Many ectomycorrhizal fungi display marked preferences for particular host tree species (Newton and Haigh, 1998). However the results of the current field survey suggest strongly that not all hydnoid species exclusively form associations with pine. Some species appear to be associated with both conifers and broadleaves (e.g. Phellodon melaleucus, Phellodon niger). Interestingly, some hydnoid species have been

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recorded in association with exotic conifers in Scotland (e.g. Bankera violascens, Phellodon tomentosus, Phellodon niger) highlighting the potential value of commercial forestry plantations for fungal conservation (Humphrey et al., 2000; Ferris et al., 2000). Of particular interest was the apparent association of Hydnellum caeruleum with the ericaceous shrub Arctostaphylos uva-ursi, observed on a completely treeless site. The ability of some fungi to ‘switch hosts’ and form mycorrhizal relationships with selected shrubby species has been documented previously (Watling, 1981, 1988). This observation is of conservation significance as it suggests that populations of hydnoid fungi could persist even after a site has been deforested, by forming associations with non-tree species, potentially providing a source of mycorrhizal inoculum for reforestation efforts. Another aspect to emerge during this investigation is that the western oakwoods of Scotland provide a suitable habitat for some hydnoid species; records made of Hydnelium concrescens, H. spongiosipes and Phellodon confluens appear to be particularly associated with broadleaved woodland, much as in southern England (Dickson, 2000). Further survey work is urgently required in the western oakwoods of Scotland to assess more fully their importance as a habitat for hydnoid fungi. Results of the field survey also supported preliminary observations that sporomes of hydnoid fungi tend to be associated with particular microsites, characterised by exposed mineral soil free from organic material, on sandy, gravelly or shingle substrates. These microsites were most often associated with streamsides, tracksides, gravel pits, quarries, shingle banks and road cuts. Hintikka and Na¨ykki (1967) provide a detailed account of the sites associated with Hydnellum ferrugineum in Finland, and report that the species is generally associated with dry pine forests on sandy soil, on sites with low organic matter content and a lack of shrubs such as Calluna and Vaccinium, a finding consistent with the results from the current survey. Similarly Arnolds (1989) reports that in the Netherlands, hydnoid fungi are associated with pine plantations on dry, acid and often sandy sites, low in organic matter, and are also found particularly on roadsides. The sites described by Danielson (1984) and Visser (1995) in Canadian Pinus banksiana forests are again very similar, being characterised by mineral soils low in organic matter. The reasons for this association are not clear, but it appears that hydnoid fungi may be particularly intolerant of high nitrogen availability (Arnolds, 1989), a suggestion supported by experimental removal of organic matter in forest soils (Baar and Kuyper, 1993, 1995, 1998; Devries et al., 1995), although the precise mechanisms involved in this response have not yet been elucidated. These current data indicate that the hydnoid species recorded tend to occur in stands within the range

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25–50 cm dbh. In general, these fungi are thought to be associated with ‘mature’ forests. For example, in Fennoscandia, Hydnellum ferrugineum typically produces sporomes in forests of 50–150 years in age (Dahlberg and Stenlid, 1995; Hintikka and Na¨ykki, 1967), whereas in The Netherlands, Arnolds (1989) states that hydnoid fungi are restricted to sites over 40 years old. Similar data have been obtained in Canada (Danielson, 1984; Visser, 1995). In the current survey, populations of hydnoid fungi tended to be associated most often with mid-rotation stands rather than trees of great maturity; on several occasions sporomes of a variety of species were found in association with relatively immature stands (< 30 years old). These results therefore do not support the hypothesis that hydnoid fungi are restricted to forest stands that are mature. One of the key objectives of this research was to examine whether hydnoid fungi in Scotland are in decline. Few sources of data are available which permit changes in abundance over time to be evaluated. The recently published account of these fungi in the UK (Pegler et al., 1997) provides general comments on both status (rarity) and distribution within the UK, but no distribution maps or lists of accessions are given. The assessment of decline depends critically on previous records of these taxa. Records of hydnoid fungi have to be treated cautiously because of both taxonomic and nomenclatural confusion. Some pairs of taxa are particularly difficult to differentiate, either on morphological or microscopic characteristics, particularly Hydnellum ferrugineum/H. spongiosipes, H. scrobiculatum/H. concrescens, and Hydnellum aurantiacum/H. auratile (Dickson, 2000; Newton et al., 2002). Such problems greatly complicate the interpretation of previous records. As a result, only those records supported by voucher specimens deposited in herbaria can be accepted with full confidence. Even then, some taxa cannot be differentiated by microscopic inspection of exsiccata (Pegler et al., 1997) and therefore all records of such species are open to some doubt. Comparison of corrected and cross-checked early records with those made more recently (> 1970) provided evidence for declines in only four species. In most cases, the declines recorded were very slight; the more substantial decline recorded for H. concrescens may reflect the fact that this species has almost certainly been confused with H. scrobiculatum in the past. The substantial increases in abundance recorded in some of other species are largely attributable to an increase in recording effort, including the results of the current field survey. To assess whether species have actually disappeared from particular localities, during the field survey we explicitly targeted a number of sites that had yielded early records, but for which no recent (post-1970) records were available. For example, at least nine

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species of hydnoid fungi were recorded in pine plantations in Moray during the late nineteenth century, an area that does not appear to have been visited subsequently by mycologists (Newton et al., 2002). In the current survey, two species (Sarcodon imbricatus and Hydnelium peckii) were relocated, confirming that hydnoid fungi are still present in the area. Other sites in the Spey valley which were known to mycologists in the late nineteenth and early twentieth centuries as important sites for hydnoid fungi remain so today (Newton et al., 2002). Given the changes in pinewood habitat that have occurred over the past century, the suggestion that hydnoid fungi can persist on a site over such long periods is surprising. Many native pinewoods, including mycologically important Speyside woodlands such as Abernethy and Rothiemurchus, were heavily logged and burnt during the early twentieth century, particularly during wartime (Steven and Carlisle, 1959). Many of the populations of hydnoid fungi recorded in the present survey were associated with trees that have subsequently established in these degraded woodlands, either through planting or natural regeneration. The lack of evidence suggesting declines in the majority of taxa is at variance with the situation in The Netherlands (Arnolds, 1989) and the Czech Republic (Hrouda, 1999), where many hydnoid species appear to have undergone substantial declines in recent decades. However, in Norway, only three species appear to have declined, namely H. aurantiacum, H. peckii and H. suaveolens (Gulden and Hanssen, 1992). As recorded for Scotland, hydnoid species in Norway are most abundant in the drier eastern parts of the country, which also tend to be less affected by aerial pollution (Gulden and Hanssen, 1992). The trends in abundance of hydnoid fungi in Scotland may therefore have more in common with the situation in Scandinavia (Gulden and Hanssen, 1992) than in the more polluted areas of central Europe, such as The Netherlands. Despite the lack of evidence for declines, some hydnoid fungi in Scotland may still be considered of conservation concern, on the basis of restricted patterns of distribution. The current results suggest that in Scotland, five species (B. fuligineoalba, H. ferrugineum, H. peckii, Phellodon tomentosus and S. imbricatus) need not be considered as threatened with extinction, in contrast to previous reports (Ing, 1992). The other 12 species could be considered to be of conservation concern, on the basis of the small number of localities recorded. However, it is likely that further populations of all species could be located by additional fieldwork. Future conservation action relating to these fungi is likely to focus on implementation of the Biodiversity Action Plan (BAP), which aims to maintain populations at all extant sites, and to experimentally establish

new populations in expanding native pinewoods. The results of the current investigation have highlighted the importance of native pinewood habitat in the upper Speyside area as of national importance. All of the hydnoid species associated with conifers are present in this area, and two species (Bankera violascens, Hydnellum auratile) have not been recorded anywhere else in the UK. The relationship recorded here between woodland size and number of hydnoid species suggests that the Speyside area may be of particular importance simply because the largest pinewood remnants are located here. This finding also suggests that conservation efforts should focus on increasing the area of available habitat and increasing the connectivity between remaining woodland fragments. If most species of hydnoid fungi are able to colonise plantations, as suggested by the current results, there may be little need for artificial establishment of new populations in expanding native pinewoods, as suggested by the BAP. However, additional information is required on the rate of colonisation of newly established pinewoods by hydnoid fungi. The data presented here suggest that there are differences between hydnoid species in colonising ability, which has implications for their conservation management. Information is also required on the impacts of habitat management interventions (e.g. thinning of forest stands; vehicular access; reduction of deer populations) on populations of hydnoid fungi. It is conceivable that some forms of soil disturbance, such as sod cutting (Baar and Kuyper, 1993), may be beneficial to the maintenance of these species. The need for additional information to provide a firmer foundation for conservation management is highlighted by the case of Bankera violascens. Many of the native pinewoods of Scotland are currently being restored by the removal of non-native conifers that were extensively planted within them during the twentieth century (Hamilton, 1995). B. violascens was recently recorded for the first time in the UK (Pegler et al., 1997) from a single site in association with the non-native conifer Norway spruce (Picea abies). Subsequent removal of the spruce, as part of conservation action to improve the native woodland habitat on the site, appears to have resulted in extinction of this fungus in the UK. Despite several visits to the site during the current survey, the species was not encountered. Such results suggest that management of forest stands in which hydnoid fungi are present should be undertaken with great caution, if further losses of populations or species are to be avoided.

Acknowledgements This paper is dedicated to the memory of the late John Lovell, a keen mycologist who generously assisted

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with the field surveys. Financial support was provided by Scottish Natural Heritage as a contribution towards the Biodiversity Action Plan for these fungi. We thank all of the mycologists who so generously assisted with this project, particularly Arthur Newton, Dave Savage, Rosemary Smith and Marysia Stamm for assistance with field surveys; Alan Outen, Elizabeth Farquharson, Mary Clarkson, Bruce Ing, Peter Orton, Peter Marren and especially Gordon Dickson, for exchange of information and personal records; and the British Mycological Society for access to foray records. Thanks are also extended to the many landowners who granted permission to visit their woodlands, and to local SNH staff throughout Scotland for assistance in arranging the field visits. B.G. Jonsson and an anonymous reviewer helped improve the text. References Aldhous, J.R. (Ed.), 1995. Our Pinewood Heritage. Forestry Commission, Alice Holt Lodge, Surrey, UK. Anon, 1994. Biodiversity: the UK Action Plan. Cm2428. HMSO, London. Anon, 1999. UK Biodiversity Group. Tranche 2 Action Plans. Volume III—Plants and Fungi. English Nature, Peterborough, UK. Arnolds, E., 1989. Former and present distribution of stipitate hydnaceous fungi (Basidiomycetes) in the Netherlands. Nova Hedwigia 48, 107–142. Arnolds, E., 1991. Mycologists and nature conservation. In: Hawksworth, D.L. (Ed.), Frontiers in Mycology. Proceedings of Fourth International Mycological Congress. CAB International, Wallingford, pp. 243–264. Arnolds, E., de Vries, B., 1993. Conservation of fungi in Europe. In: Pegler, D.N., Boddy, L., Ing, B., Kirk, P.M. (Eds.), Fungi of Europe: Investigation, Recording and Conservation. Royal Botanic Gardens, Kew, pp. 211–230. Baar, J., Kuyper, T.W., 1993. Litter removal in forests and effect on mycorrhizal fungi. In: Pegler, D.N., Boddy, L., Ing, B., Kirk, P.M. (Eds.), Fungi of Europe, Investigation, Recording and Mapping. Royal Botanic Gardens, Kew, pp. 275–286. Baar, J., Kuyper, T.W., 1995. Restoration of aboveground ectomycorrhizal flora in stands of Pinus sylvestris (Scots pine) in The Netherlands by removal of litter and humus. Restoration Ecology 6 (3), 227–237. Baar, J., Kuyper, T.W., 1998. Restoration of an aboveground ectomycorrhizal flora in stands of Pinus sylvestris (Scots pine) in The Netherlands by removal of litter and humus. Restoration Ecology 6, 227–237. Bunce, R.G.H., Jeffers, J.N.R. (Eds.), 1977. Native Pinewoods of Scotland. Proceedings of Aviemore Symposium, 1975. Institute of Terrestrial Ecology, Cambridge. Cannon, P.F., 1997. Strategies for rapid assessment of fungal diversity. Biodiversity and Conservation 6, 669–680. Cannon, P., 1998. Database of British fungal records from literature sources. Mycologist 12 (1), 25–26. Dahlberg, A., Stenlid, J., 1995. Spatiotemporal patterns in ectomycorrhizal populations. Canadian Journal of Botany 73, S1222– S1230. Danielson, R.M., 1984. Ectomycorrhizal associations in jack pine stands in northeastern Alberta. Canadian Journal of Botany 62, 932–939. Dennis, R.W.G., 1986. Fungi of the Hebrides. Royal Botanic Garden, Kew, Richmond, Surrey.

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