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pH preferences of red-listed gasteromycetes in calcareous sandy grasslands: Implications for conservation and restoration
fungal ecology 3 (2010) 357–365
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journal homepage: www.elsevier.com/locate/funeco
pH preferences of red-listed gasteromycetes in calcareous sandy grasslands: Implications for conservation and restoration Pa˚l Axel OLSSONa,*, Tim Krone SCHNOORa, Sven-A˚ke HANSONb a
Plant Ecology and Systematics, Ecology Building, Lund University, SE-223 62 Lund, Sweden Birkagatan 49, SE-256 55 Helsingborg, Sweden
b
article info
abstract
Article history:
Species diversity in sandy grasslands is threatened by decalcification and eutrophication.
Received 28 September 2009
To determine the most appropriate conditions for red-listed gasteromycete fungi in such
Revision received 18 January 2010
grasslands, we investigated their pH preferences in this habitat in southern Sweden.
Accepted 3 February 2010
During two winters soil samples were collected from the vicinity of mycelia of these
Available online 24 April 2010
species. Chemical analysis revealed that none of the fungi occurred in sandy habitats with
Corresponding editor:
a pH lower than 5, although pH values between 4 and 5 are very common in sandy
Jacob Heilmann-Clausen
grasslands in the area. We found niche differentiation within the genus Tulostoma in that two out of four species occurred mainly in soils with high lime content, while one had
Keywords:
a broad niche and one occurred mainly in soils low in lime and with a pH below 7.5. Also in
Conservation
the genus Geastrum, some species occurred at high lime content, while most Geastrum as
Disciseda
well as two Disciseda species preferred soils with only low amounts of lime. We conclude
Gasteromycetes
that many species prefer areas with neutral to slightly acid soil. The results were compared
Geastrum
with data for key plant species collected in a previous study of calcareous sandy grasslands
Sandy grassland
and this showed that these in general had a wider pH range than the studied fungi. The
Soil pH
results highlight the importance of varying pH levels in protected areas and that the
Tulostoma
transition zone between lime-containing topsoil and complete decalcification is a preferred environment for many red-listed fungi as well as plants. ª 2010 Elsevier Ltd and The British Mycological Society. All rights reserved.
Introduction Semi-natural calcareous grasslands are some of the most species-rich communities in Europe. In Europe, calcareous soils and low P availability are usually associated with high plant species diversity (Janssens et al. 1998; Ewald 2003; Olsson & Tyler 2004; Wassen et al. 2005). Grazing by cattle, sheep and horses is used to manage calcareous grasslands for conservation (Schla¨pfer et al. 1998; Poschlod & WallisDeVries 2002). Conservation targets are typically endangered invertebrates,
birds or vascular plants whereas fungi are rarely considered. Basidiomycete fungi are a species-rich group with different functions in ecosystems. Many are symbiotic, while others are saprotrophs. Soil acidification restricts many fungal species in forests, and pH, base cation content and organic matter seem to be among the best abiotic predictors of fungal distribution (Ru¨hling & Tyler 1990). This also applies to the gasteromycete Lycoperdon perlatum, which is sensitive to the acidification of forests in northern Europe (Hansen 1989). Most gasteromycetes occur in grasslands,
* Corresponding author. Tel.: þ46 46 222 4247. E-mail address: [email protected] (P.A. Olsson). 1754-5048/$ – see front matter ª 2010 Elsevier Ltd and The British Mycological Society. All rights reserved. doi:10.1016/j.funeco.2010.01.004
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and sandy grasslands in particular hold a unique set of redlisted gasteromycetes. It has been shown that the unique sandy vegetation in southeast Sweden holds a large number of gasteromycetes from the genera Tulostoma, Geastrum and Disciseda (Hanson & Jeppson 2005). The Tulostoma species in particular are closely connected with tree-less, base-rich, sandy grasslands (Hanson 2008). It is generally found that different Tulostoma species often grow at the same sites and also together with other gasteromycetes such as Disciseda and Geastrum (Kers 1975; Brochmann et al. 1981; Wright 1987; Do¨rfelt & Bresinsky 2003). However, even if many species grow at the same sites, local variation may still be large in sandy habitats (Ma˚rtensson & Olsson 2010). It has been observed that in particular Tulostoma kotlabae and Tulostoma melanocyclum often grow close to Tulostoma brumale (Hanson 2008) and Disciseda candida close to Geastrum schmidelii (Hanson 2009), while other species seldom do. The gasteromycetes in sandy soils are favoured by some level of soil disturbance, natural or man-made (Kreisel 1987; Do¨rfelt & Bresinsky 2003; Hanson 2008), and T. brumale, for example, occurs on roadside slopes (Krieglsteiner 2000; Do¨rfelt & Bresinsky 2003; Hanson 2008) as well as in semi-natural grasslands where soil disturbance may be caused by grazers. Many of the gasteromycetes are favoured by sloping ground and occur mostly on south-facing slopes, although some variation between the species may occur (Brochmann et al. 1981; Hanson 2008). The Tulostoma species are often found close to bryophytes of the genus Syntrichia, and there has been speculation whether Tulostoma species may grow in symbiosis with them (Andersson 1950; Wright 1987). The soil pH has a profound effect on all organisms and processes in the soil. It influences the solubility of toxic metals and mineral nutrients and, hence, may lead to chemical stress at extreme values and influences nutrient availability to plants. At a pH below 5, Al and Mn are released into the soil solution inhibiting the growth of many plants (Foy & Flemming 1978). In alkaline soil, on the other hand, phosphorus and iron availability decreases, restricting the distribution of many plant species (Grime & Hutchinson 1967; Kinzel 1983; Tyler 1992; Tyler & Olsson 1993). In southern Sweden, sandy grasslands show high variation in soil pH over distances as short as a few meters (Ma˚rtensson & Olsson 2010). Sandy grasslands occur on glaciofluvial deposits and on dunes, often near the coast. In certain areas, the sand contains calcium carbonate, in which case alkaline conditions prevail. Other sandy soils are strongly acid. There seem to be few sandy soils of intermediate pH (Rozema et al. 1985; Tyler 2005; Olsson et al. 2009) due to the very low base cation buffering capacity of sand once the original lime has been depleted; cation exchange capacity is very low as a result of the low content of clay and organic matter in sandy soils. The sandy grasslands of southern Sweden have a long history of human land use. Extensive arable rotation practices with prolonged fallow have prevailed until the early 20th century. Today, the areas are kept open mainly by grazing. In the area, the proportion of non-arable open land decreased from 79 % in 1862 to 51 % in 1960 (Mattiasson 1974). This was mainly due to sand-binding pine plantations, which during the same period increased from 3 to 38 % of the total land area. The calcareous sandy grasslands are threatened by a number of factors such as acidification (Roem & Berendse 2000),
P. A. Olsson et al.
nitrogen deposition (Bobbink et al. 1998), fertilization and reduced intensity of management (Olsson 1994), which may eventually lead to vegetation changes and the loss of many rare species (Tamis et al. 2005). Inappropriate land use may change the vegetation structure irreversibly (Marrs & Britton 2000). Semi-natural grassland may be converted into intensive farmland or be used for building houses and roads. Our purpose was to investigate the variation in pH and lime preferences in red-listed gasteromycetes in xeric sand calcareous grasslands, protected under the EU directive (code 6120). By this we expected to gain information about the best management regime to protect this threatened group of fungi. We hypothesised that species that often grow together have similar pH preferences, while species that seldom grow directly together have not. Based on earlier findings we therefore hypothesised that: (1) T. brumale, T. melanocyclum and T. kotlabae have similar pH preferences; (2) Tulostoma fimbriatum differs from these (Hanson 2008); and (3) D. candida and G. schmidelii have similar pH preferences (Hanson 2009). We also compared the preferences of the red-listed gasteromycetes with those of the key plant species in the habitat to find out if their preferences were the same when it comes to soil chemical properties. This was done since at present the vascular plants are used as main indicators of the habitat type. The main focus was on pH and lime content, but we also analysed soil minerals to investigate if any of the fungi had any particular preferences in this respect.
Materials and methods Study area The study area was coastal eastern Scania (Ska˚ne), between the cities of Kristianstad and Simrishamn in southernmost Sweden (Fig 1). The area is about 80 km long and 35 km wide, between 55 400 and 56 100 N, and 13 900 and 14 300 E. The areas with calcareous sandy grasslands (including ‘‘xeric sand calcareous grasslands’’ protected under the Natura 2000 EU habitat directive as habitat 6120), vary in size between 15 m2 and 90 000 m2 (Olsson 1994). The ecosystem is characterised by an open sward, which appears to depend on regular disturbance of the surface soil layer. These sandy calcareous grasslands have developed on glaciofluvial sand with little eolian redistribution. Weathering of lime deposits gave rise to lime-rich sand on many coastal sites in eastern Scania and on the Baltic islands. Since the end of the Weichselian glaciation c. 15 000 BP, this material has been continuously subjected to weathering. The depletion of lime may have increased during recent years due to acid rain. Only a few places with typical vegetation of calcareous sandy grasslands occur today, constituting a total of less than 50 ha (Olsson 1994; Tyler 2005). Koeleria glauca is a species of xeric sand calcareous grasslands in Sweden, as is Dianthus arenarius ssp. arenarius, that is endemic to the Baltic region. Xeric sand calcareous grasslands are replaced by heath-like vegetation as the soil becomes acidified. Acidic sandy grassland is mainly characterised by the grass Corynephorus canescens and it is similar to grey dune vegetation elsewhere (e.g. Bruun & Ejrnæs 2000; Provoost et al. 2004; Frederiksen et al. 2006).
pH preferences of red-listed gasteromycetes
359
Fig 1 – Map showing the investigation area in eastern Scania, southernmost Sweden. The dots denote approximately areas with calcareous sandy grasslands. Note that, in most cases, plots are distributed over a much larger area than each dot shows. Scale bar [ 10 km, dark grey [ urban areas, light grey [ areas of igneous rock.
The soil type of the xeric sand calcareous grassland is a pararendzina characterised by a thin humus-enriched layer on top of CaCO3-containing sand. On degenerated pararendzina, the layer containing calcium carbonate occurs as a deep C-horizon below a B-horizon, which is enriched with iron but with virtually no calcium carbonate. If depletion continues, a podzoloid soil type develops and the ecosystem changes into a Calluna heath. Earlier studies in the area have shown that the most common pH values of sandy grasslands in the study are those between 4 and 5 and that soils with pH above 7 are rare (Olsson 1974).
Sampling strategy The study was based on knowledge from a survey that has been going on since 1994, in which the occurrence of fungi – particularly gasteromycetes has been recorded in sandy grasslands of eastern Scania (Hanson & Jeppson 2005). During the winters 2007 (2006-12-27 to 2007-04-02) and 2008 (2007-0919 to 2008-02-10) all sites were visited and soil samples
(0–10 cm) were collected within mycelia of each species in the genera Tulostoma, Geastrum and Disciseda. The gasteromycetes usually develop fruit bodies during the autumn. They are persistent, however, and can be found during the whole winter and late in spring. They can even persist until the following summer, but they are then less easy to find due to the vegetation, and some of them may blow away. In the first season we collected 130 soil samples from 33 different sites and in the second season 108 samples from 33 sites. In total, samples were collected from 51 different sites. Soil was sampled only once within each mycelium. The numbers of samples reflect the number of mycelia studied, but in some cases more than one species occurred at the same spot. Some of the sites were large, such as certain military training fields and nature reserves, and at these sites there were many mycelia, and therefore more samples were taken from these sites to reflect the distribution of the species in the sandy grasslands. All species in the sandy grasslands except one (Geastrum striatum) are nationally red-listed (Ga¨rdenfors 2005). The
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following species were included (with their red-list status): Disciseda bovista (EN), D. candida (VU), Geastrum berkeleyi (EN), Geastrum floriforme (CR), Geastrum minimum (VU), Geastrum pseudolimbatum (CR), Geastrum saccatum (EN), G. schmidelii (NT), T. brumale (NT), T. fimbriatum (EN), T. kotlabae (EN) and T. melanocyclum (CR).
Additional data sets To compare with the distribution of plant species, we analysed the distribution of some important key plants of sandy grasslands. These data come from a previous study (Olsson et al. 2009) where 136 plots of calcareous sandy grassland were analysed for the vegetation composition. We also analysed the whole of this data set, which reflects the distribution of both calcareous and decalcified sandy soils in calcareous areas. To widen the picture we analysed the data from Olsson (1974) and his ‘‘Studies on south Swedish sand vegetation’’, which includes both calcareous and noncalcareous areas. The areas in both these studies were intensively surveyed for the gasteromycetes in the present study.
Soil chemical analyses Soil samples were stored frozen until further treatment. All 236 samples were analysed for pH (10 g of soil was suspended in 30 ml of distilled water and pH was measured electrometrically in supernatants obtained through 2 hr extraction in a rotator). In 171 soil samples from both seasons the total amounts of Ca, Mg, and P were determined using ICP-AES (Inductively Coupled Plasma-Atomic Emission Spectrometry) after extraction in hot H2SO4. The concentration of Ca was recalculated to CaCO3 concentration, assuming that most of the calcium in the soils is present as CaCO3. The total Ca content was recalculated to lime content (CaCO3), assuming that all Ca was present as CaCO3. From all the 106 soil samples from the second season we analysed the total amounts of Ca, Mg, P, B, K, Mn, Cd, Zn, Cu and Pb using the same method as described above.
Statistical methods We divided each data set for pH into intervals of 0.25 pH units and thus obtained a frequency at each interval. The distribution of mycelia in relation to lime content was analysed after dividing the data into logarithmic intervals to achieve a more normally distributed data set. The occurrence of each species as an effect of soil pH was modelled using GAM models (Ejrnæs 2000) with the mgcv-package (Wood 2004) in R (R Development Core Team 2008). Models used Poisson distributions throughout, since data consisted of counts. We used principal component analysis (PCA), as implemented in the program CANOCO (ter Braak 1986), to identify the relations between soil elements and occurrences of the different fungal species.
P. A. Olsson et al.
Results The soil samples with mycelia showed a pH distribution between 5 and 9, skewed towards alkaline pH values. There was a strong relation between soil pH and lime content in the analysed soils. With lime content below a few percent, the pH dropped drastically (Fig 2A). There was a positive linear relation between lime and total Mg content (Fig 2B) and total P content (Fig 2C). T. brumale and T. melanocyclum were, with few exceptions, restricted to the alkaline pH range and this resulted in narrow unimodal response curves (Fig 3A). T. kotlabae and T. fimbriatum both frequently occurred from pH 8 and down to 6, but the predicted response curves for these two species were not significant (P > 0.05). The genus Geastrum as a whole had a pH range in the sandy grasslands with a predicted frequency peak between 6 and 7 (Fig 3A), with a significant (P 0.05) unimodal relation for the species that was most commonly found in the sandy grasslands, G. schmidelii, while the response curves for neither the other Geastrum species nor Disciseda spp. were significant. Within the Geastrum genus, G. saccatum, G. pseudolimbatum and G. floriforme only occurred at pH below 7 and G. berkeleyi at pH above 7, but the records for these species were too few to allow modelling of response curves. Three of the tested plant species showed significant (P 0.05) bimodal response curves to pH in sandy grasslands (Fig 3B), mainly due to the lack of plots with intermediate pH (Fig 3C). The main indicator for calcareous sandy grasslands in the region, K. glauca, showed a wide pH range from 5 to around 9.5. D. arenarius had a distribution similar to that of K. glauca. On the other hand, Festuca polesica and Alyssum alyssoides seemed restricted mainly to plots with alkaline pH and showed significant (P 0.05) unimodal or truncated unimodal response curves to pH. The acid tolerant species C. canescens had a distribution similar to that of K. glauca in these areas, but with the highest peak at acid soil pH. T. brumale and T. melanocyclum occurred, frequently above 10 % lime (Fig 4). The predicted unimodal lime response curves of these two species were clearly separated from those of Geastrum spp. and Disciseda spp., which had significant (P 0.05) monotone response curves at low lime content. Geastrum species mainly occurred with a lime content lower than 1 %, with G. berkeleyi, G. minimum and G. schmidelii being the only species occurring in soils with more than 1 % lime. No significant (P > 0.05) response curves were obtained for T. fimbriatum and T. kotlabae, but the results indicate that they often occur at lower lime content than T. brumale and T. melanocyclum. T. fimbriatum never occurred in soil with more than 2 % lime, and was thus distinguished from the most common species in the genus, T. brumale. PCA analysis of soil elemental composition revealed that the first ordination axis explained 66 % of the variation between samples (Fig 5). PCA axis 1 was closely related to Ca and Mg content. A second PCA axis explained 13 % of the variation and was related to the metals Pb, Cu, Zn, Cd, and Mn. The total content of P, K and B showed relation both to axis 1 and axis 2. Three of the Tulostoma species (T. brumale, T. melanocyclum and partly T. kotlabae) were in general distributed to the right in the ordination and the others,
pH preferences of red-listed gasteromycetes
A
9
361
A
R2 = 0.73
8.5
G. schmidelii*, n=35 Disciseda spp NS, n=18 Geastrum spp NS, n=28 T. fimbriatum NS, n=15 T. kotlabae NS, n=16 T. melanocyclum**, n=25 T. brumale***, n=116
Predicted frequency
0.3
8
7.5
pH (H2O)
0.35
7 6.5
0.25 0.2 0.15 0.1 0.05
6
0 5.5
B
0.3 C. canescens**, n=70 D. arenarius**, n=41 K. glauca***, n=102 F. polesica**, n=18 A. alyssoides***, n=36
5 2500
0.25
Predicted frequency
B y = 450 + 29x R2 = 0.56
Mg (µg g-1)
2000
1500
0.2
0.15
0.1
0.05 1000
0
C 0.15 500
Predicted frequency
Olsson-74***, n=95 Olsson-09***, n=137
0 1200
C
y = 370 + 9.8x R2 = 0.14
Total P (µg g-1)
1000
0.1
0.05
800
0
600
4
5
6
7
8
9
pH (H2O) 400
200
0
0
10
20
30
40
50
CaCO3 (%) Fig 2 – The chemical properties of all soils sampled (n [ 171) in the vicinity of mycelia of Tulostoma spp., Geastrum spp. and Disciseda spp. in calcareous sandy grasslands of eastern Scania. (A) The relation between total CaCO3 and pH fitted to a Gaussian function (P < 0.001), (B) the relation between CaCO3 and total Mg content subjected to a linear regression (P < 0.001), (C) the relation between CaCO3 and total P content subjected to a linear regression (P < 0.001).
Fig 3 – Predicted pH response curves of (A) gasteromycetes and (B) plants, and (C) the distribution of sites in calcareous sandy grasslands of eastern Scania. Geastrum spp. represents the combined frequencies of five species (G. pseudolimbatum, n [ 4, G. saccatum, n [ 5, G. floriforme, n [ 3, G. minimum, n [ 6, G. berkeleyi, n [ 8, G. striatum, n [ 1) and Disciseda spp. represents two species (D. candida, n [ 14, D. bovista, n [ 4). The data for the plants presented in (B) comes from a study of a total of 136 plots collected in a previous study (Olsson et al. 2009) and re-analysed here. The site data comes from one study of calcareous sandy grasslands (Olsson et al. 2009) and from one study of sandy habitats in general in the region (Olsson 1974).
P. A. Olsson et al.
2.0
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G. schmidelii**, n=15 Disciseda spp*, n=14 Geastrum spp**, n=17 T. fimbriatum NS, n=15 T. kotlabae NS, n=13 T. melanocyclum***, n=25 T. brumale***, n=63
PCA 2 (13 %)
0.5
Pb
Cd Mn K
P Mg
Ca
0.3
-1.0
Predicted frequency
0.4
Cu Zn
0.2
-2.0 0.1
0
1
10
100
Lime content (%) Fig 4 – Predicted lime response curves of gasteromycetes in calcareous sandy grasslands of eastern Scania. Geastrum spp. represents the combined frequencies of five species (G. pseudolimbatum, n [ 3, G. saccatum, n [ 3, G. floriforme, n [ 3, G. minimum, n [ 4, G. berkeleyi, n [ 4) and Disciseda spp. represents two species (D. candida, n [ 11, D. bovista, n [ 3).
including T. fimbriatum and partly T. kotlabae to the left, reflecting the preference for high soil lime content of three of the Tulostoma species. There was little indication of preferences or avoidance of metals in the soils, except that D. candida seemed to grow in soils with higher metal contents than the other species did.
Discussion Although the studied gasteromycetes often occur together (Brochmann et al. 1981; Do¨rfelt & Bresinsky 2003), we found strong support for the hypothesis that within sites they have different pH preferences. Kers (1975) found that T. brumale might occur in the same places as Disciseda in Sweden, but in microhabitats distinct from each other, which can be explained by the differences in pH preferences found in our study. With this result we highlight the importance of a dynamic management regime that creates or maintains a variation in soil conditions and successional stages within habitats in order to preserve a high biodiversity. It seems as many of the red-listed fungal species in calcareous sandy grasslands of southern Sweden are adapted to pH between 6 and 7.5, and all sites with red-listed gasteromycetes of the genera Tulostoma, Geastrum and Disciseda had pH between 5 and 9. The distribution was rather skewed and the peak was therefore between 7.5 and 8.5. This distribution differs from the general pH pattern of the sandy grasslands in the area, where the most common pH values are between 4 and 5 (Olsson 1974). The pH preference curves of the gasteromycetes also differed from those of most of the rare plants in the same habitat by being narrower. The skewness in our
PCA 1 (66 %)
3.0
Fig 5 – PCA ordination of soil elements in samples from the second season (n [ 106 soil samples from 121 records of fungal mycelia, since in some cases more than one species occurred at the same spot). Each soil sample from the vicinity of mycelia is represented by a dot and an indication of the fungal species present in the spot the sample was taken from. TB [ Tulostoma brumale, TM [ T. melanocyclum, TK [ T. kotlabae, TF [ T. fimbriatum, DC [ Disciseda candida, DB [ D. bovista, GS [ Geastrum schmidelii, GF [ G. floriforme, GP [ G. pseudolimbatum, GM [ G. minimum, GB [ G. berkeleyi, Gsa [ G. saccatum.
gasteromycete material was due to the fact that the most common species, T. brumale, showed a clear preference for alkaline soils, and hardly occurred in sites with low lime contents. On the other hand, most of the other species had an optimum below pH 7. A pH of 5.5 is generally considered as the boundary between acidic and non-acidic conditions and acidification below this level may lead to loss of species, and reduced biodiversity (Tyler 1996; Pa¨rtel 2002; Pa¨rtel et al. 2004). Also in these particular sandy areas there is a drop in the number of plant species in general, and of red-listed plant species below pH 5 (Olsson et al. 2009). Since these studies together with the present study show that the optimal pH for high diversity of both plants and fungi in grasslands is between 6 and 7.5, this has important implications for management and restoration measures. In earlier studies, it has been shown that intermediate pH levels are rare in sandy grasslands and dune systems (Rozema et al. 1985; Tyler 2005; Olsson et al. 2009), a fact that was to be expected due to low cation buffering, once the lime is depleted (Brady & Weil 2008). Thus, the rareness of the red-listed gasteromycetes may reflect that they occupy an intermediate state in the succession during acidification of calcareous sandy grasslands. Since most of these species seem to be sensitive to high lime content, their preferred habitat is rare and unstable, threatened by further acidification (Mattiasson 1974; Rozema et al. 1985). It might be that these species have evolved in areas where intermediate pH values are more common, and the fact that we consider them as species of calcareous soils may be due to the fact that noncalcareous soils in this part of the world tend to be very acid. The studied fungal species, as well as many plants growing in the calcareous sandy habitats, immigrated from the south and southeast after the last ice age (Sterner 1922). In southern
pH preferences of red-listed gasteromycetes
Europe insolation is stronger, which prevents acidification and this may explain why many plants (Sterner 1922; Tyler 1996) as well as fungi grow mainly in calcareous areas even though they avoid high lime content. The acidification of calcareous soils was in earlier landscapes prevented by erosion and soil disturbance (Poschlod & WallisDeVries 2002). Increased soil disturbance is therefore needed to prevent acidification of calcareous soils. Here we show that restoration should not be made in areas that are slightly acidified, since these may host many rare species. Our study shows that many of the species would have problems in habitats restored to high lime content. Restoration measures may best be implemented in areas where acidification has brought the pH to below 5, or in areas degenerated due to fertilization or tree plantation. Restoration measures creating a slightly acidic habitat from a strongly acidic one could be achieved using mild types of soil perturbation if base-rich material is present within the disturbance depth or if the organic layer is mixed with mineral soil. It may also be that the creation of sloping ground favours the fungal species and gives a more stable pH environment due to stronger insolation and less decalcification (Brochmann et al. 1981; Hanson 2008). The fact that the studied species are at the risk of going extinct, and that they often grow on sloping ground, may reflect that sloping ground has been more common in ancient landscapes and that the present landscape has been flattened due to modern agricultural practice and less erosion. Disciseda, on the other hand, seems to prefer flat ground and small-scale disturbance caused by trampling of horses (Hanson 2009) or people (Kers 1975). Within Tulostoma, T. fimbriatum preferred soil with the lowest lime content, which distinguished it from the other three species in the genus. Slope aspect shows very little difference between the Tulostoma species (Brochmann et al. 1981; Kreisel 1984; Hanson 2008). There are in general no mycelia growing on slopes facing N, NE or NW, and this seems to be the same for all the studied Tulostoma species. This may be due to more vegetation and more rapid accumulation of humus on the less drought-exposed north slopes. In the present study most species showed a typical hump-shaped distribution in relation to soil factors. However, in some cases, such as for T. kotlabae, the distribution was wide and flat and it could be worthwhile to investigate whether this reflects genetic differences between populations, in particular since the taxonomy of these fungal groups is under consideration (Wright 1987; Moreno et al. 1997). Calcareous soils may lead to a limited availability of elements such as P or Fe (Kinzel 1983). Acid soils on the other hand may lead to high solubility of metals such as Mn, Zn and Cu (Foy & Flemming 1978). While some fungi are sensitive to metals such as Cu, others accumulate metals and mycorrhizal fungi may protect plants from toxicity in contaminated soils (Brown & Wilkins 1985). The total amounts of metals we measured explained only a small part of the variation between samples. Further studies could also include the measurement of soluble metals and thus shed further light on the relations between Disciseda species and high metal availability. Sunhede (1989) measured pH in soil samples taken where Geastrum species occurred. He reported pH values generally
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lower than in our study. This may be due to differences in sampling strategy. Sunhede sampled the organic layer, while we sampled to a depth of 10 cm, irrespective of depth of the organic layer. Since organic matter is more acid than mineral soil, this may explain the differences between our studies. For example, Sunhede (1989) gave a pH range of 4.8–7.5 for G. schmidelii, while we found a pH range of 5.5–8.5. All gasteromycetes in this study can be considered as saprotrophs and there is no evidence for mycorrhizal formation, although they may grow near pines and other trees in sand dunes. Sunhede (1989) considered the thin organic layer as the substrate for the Geastrum species, though he showed that mycelium reached far below this layer. Fungal mycelia are capable of bidirectional translocation (Olsson 1995) and may thus forage for carbon energy in the organic soil and at the same time for mineral nutrients in the mineral soil. Ring formation in G. schmidelii (Sunhede 1989), T. fimbriatum (Hanson 2008) and D. bovista (Hanson 2009) indicates that the fungi form large mycelia with a possible diameter of more than 10 m. Such large mycelia are unlikely to grow only in the organic layer since this is often sparse and disrupted (Olsson et al. 2009) and may exhibit extreme temperatures during the summer. Thus the main carbon substrate may be the organic layer and this may be where the mycelia proliferate during fruit body formation (Sunhede 1989), but it is also likely that there is a less visible mycelium in lower soil layers.
Recommendations for management and restoration Drastic measures such as soil perturbation (Dolman & Sutherland 1994) may be important for the persistent preservation of sandy grasslands. Several observations indicate that the Tulostoma species (Hanson 2008) and Disciseda species (Kers 1975; Hanson in press) need at least 25 yr to establish mycelia large enough to form fruit bodies. Kers (1975) stated that Disciseda species did not occur in places created during the last 50 yr, but the occurrence of Disciseda as well as T. brumale on roadsides may indicate that they establish in shorter times (Hanson 2008, 2009). It is currently not known how long it takes for the Geastrum species to establish their mycelia, but the ring formation by G. schmidelii (Sunhede 1989) illustrates the ability of mycelia to be long-lived. Overall there is only vague indications of the establishment times for gasteromycetes in sandy soils and more knowledge could be gained from studies in the future in restored areas. Such knowledge is important for implementing disturbance regimes of sandy grasslands, and also to know when to expect results of restoration. The long time needed for the establishment of mycelia makes restoration measures difficult to interpret and emphasises the importance of using soil chemistry as an immediate indicator of restoration success that in a longer time perspective will favour different types of organisms. A system with regular cultivation and short-period fallowing may disfavour the red-listed gasteromycetes and they may not be able to recolonize (Hanson 2008, 2009). Frequent occurrence of gasteromycetes along former field margins (Hanson 2008) may indicate that those have been refuges in former agricultural landscapes. We conclude that few of the red-listed gasteromycetes are specialised to the typical initial stage of the habitat named
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‘‘xeric sand calcareous grasslands’’. Instead most of them seem specialised on intermediate types of calcareous sandy grasslands. However, the intermediate pH conditions between 6 and 7.5 are hardly possible without the presence of calcareous or sedimentary bedrock as parent material. The present results give support for a dynamic management of sandy grasslands and indicate that the decalcification process in calcareous topsoil favours a high biodiversity. Diversity in calcareous grassland depends on a variation in management types and a heterogeneous sward structure (Woodcock & Pywell 2010). Variation in pH is another effect of variation in succession stage and will also support diversity in calcareous grasslands as shown in this study of the gasteromycetes. For the management of sandy habitats with red-listed gasteromycetes we suggest that grazing animals such as horses could be enough for creating small-scale disturbance. However, since habitats are vulnerable it is important also to create new habitats suitable for fungal colonisation. This could be achieved by careful topsoil removal in areas with too high nutrient levels, and in areas that are slightly acidified. In strongly acidified areas, on the other hand, more drastic measures such as deep perturbation and slope creation are recommended. Restoration measures could be performed close to known habitats, which will facilitate spread. The present study gives important information on the soil preferences of the red-listed gasteromycetes and this could be used as a guide in habitat restoration.
Acknowledgements This study was made possible through financial support from Region Ska˚ne, The Swedish Environmental Protection Agency, The Swedish Research Council and Formas. We thank Ingvar Ma˚nsson and Carl-Gustav Bengtsson for their help in the search for the gasteromycetes, Mikael Jeppson, who verified species determination for several of the specimens.
references
Andersson O, 1950. Larger fungi on sandy grass heaths and sand dunes in Scandinavia. Botaniska Notiser Supplement 2: 2. Bobbink R, Hornung M, Roelofs JGM, 1998. The effect of air-borne nitrogen pollutants on species diversity in natural and seminatural European vegetation. Journal of Ecology 86: 717–738. Brady NC, Weil RR, 2008. The Nature and Properties of Soils. Pearson Prentice Hall, NJ, USA. Brochmann C, Rustan OH, Brandrud TE, 1981. The genus Tulostoma (Gasteromycetes) in Norway. Blyttia 39: 209–226. Brown MT, Wilkins DA, 1985. Zinc tolerance of mycorrhizal Betula. New Phytologist 99: 101–106. Bruun HH, Ejrnæs R, 2000. Classification of dry grassland vegetation in Denmark. Journal of Vegetation Science 11: 585–596. ter Braak CJF, 1986. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67: 1167–1179. Dolman PM, Sutherland WJ, 1994. The use of soil disturbance in the management of Breckland grass heaths for nature conservation. Journal of Environmental Management 41: 123–140.
P. A. Olsson et al.
¨ kologie Do¨rfelt H, Bresinsky A, 2003. Die Verbreitung und O ausgewa¨hlter Makromyceten Deutchlands. Zeitchrift fu¨r Mykologie 69: 177–286. Ejrnæs R, 2000. Can we trust gradients extracted by detrended correspondence analysis? Journal of Vegetation Science 11: 565–572. Ewald J, 2003. The calcareous riddle: why are there so many calciphilous species in the Central European flora? Folia Geobotanica 38: 357–366. Foy CD, Flemming AL, 1978. The physiology of plant tolerance to excess available aluminium and manganese in acid soils. In: Jung GA (ed), Crop Tolerance to Suboptimal Soil Conditions. American Society of Agronomy, Madison, WI, pp. 301–328. Frederiksen L, Kollmann J, Vestergaard P, Bruun HH, 2006. A multivariate approach to plant community distribution in the coastal dune zonation of NW Denmark. Phytocoenologia 36: 321–342. Ga¨rdenfors U, 2005. The 2005 Red List of Swedish Species. Artdatabanken, Uppsala, Sweden. Grime JP, Hutchinson TC, 1967. The incidence of lime-chlorosis in natural vegetation of England. Journal of Ecology 55: 557–566. Hansen PA, 1989. Species response curves of macrofungi along a mull/mor gradient in Swedish beech forests. Vegetatio 82: 69–78. ˚ , 2008. An ecological study of Tulostoma species in Hanson S-A sandy habitats in SE Sweden (in Swedish). Svensk Mykologisk Tidskrift 29: 93–109. ˚ , 2009. An ecological study of Disciseda species in Hanson S-A sandy habitats in SE Sweden (in Swedish). Svensk Mykologisk Tidskrift 30: 17–32. ˚ , Jeppson M, 2005. Gasteromyceter i o¨stra Ska˚nes Hanson S-A sandsta¨ppsomra˚den – en sammanfattning av elva a˚rs inventeringsarbete. Svensk Mykologisk Tidskrift 26: 61–83. Janssens F, Peeters A, Talloowin JRB, Bakker JP, Bekker RM, Fillat F, Oomes MJM, 1998. Relationship between soil chemical factors and grassland diversity. Plant and Soil 202: 69–78. Kers LE, 1975. The genus Disciseda (Gasteromycetes) in Sweden. Svensk Botanisk Tidskrift 69: 405–438. Kinzel H, 1983. Influence of limestone, silicates and soil pH on vegetation. In: Lange OL, Nobel PS, Osmond CB, Ziegler HJ (eds), Physiological Plant Ecology III. Springer, Berlin, pp. 201–244. Kreisel H, 1984. Die Stielboviste (Gattung Tulostoma) der Deutschen Demokratischen Republik und Westberlins. Hercynia 21: 396–416. Kreisel H (ed), 1987. Pilzflora der Deutchen Demokratischen Republik. Basidiomycetes (Gallert-, Hut- und Bauchpilze) Fischer, Jena, Germany. Krieglsteiner GJ (ed), 2000. Die Großpilze Baden-Wu¨rttembergs. Band 2. Sta¨nderpilze: Leisten-, Keulen-, Korallen-, und Stoppelpilze, Bauchpilze, Ro¨hrlings- und Ta¨ublingsartige pilze. Ulmer, Stuttgart (Hohenheim), Germany. Marrs R, Britton A, 2000. Conservation problems on Breckland heaths: from theory to practice. Biological Conservation 95: 143–151. Ma˚rtensson L-M, Olsson PA, 2010. Soil chemistry of local vegetation gradients in sandy calcareous grasslands. Plant Ecology 206: 127–138. Mattiasson G, 1974. Sandsta¨pp. Vegetation, dynamik och sko¨tsel. Meddelanden fra˚n Avdelningen fo¨r Ekologisk Botanik, Lunds universitet 2: 1–40. Moreno G, Alte´s A, Ochoa C, Wright JE, 1997. Notes on type materials of Tulostoma. Some species with mixed holotypes. Mycological Research 101: 957–965. Olsson H, 1974. Studies on south Swedish sand vegetation. Acta Phytogeographica Suecica 60: 176. Olsson K-A, 1994. Sandsta¨pp i Ska˚ne – ett upprop. Lunds Botaniska Fo¨rening Medlemsblad 2: 4–13.
pH preferences of red-listed gasteromycetes
Olsson PA, Ma˚rtensson LM, Bruun HH, 2009. Acidification of sandy grasslands – consequences for plant diversity. Applied Vegetation Science 12: 350–361. Olsson PA, Tyler G, 2004. Occurrence of non-mycorrhizal plant species in south Swedish rocky habitats is related to exchangeable soil phosphate. Journal of Ecology 92: 808–815. Olsson S, 1995. Mycelial density profiles of fungi on heterogeneous media and their interpretation in terms of nutrient reallocation patterns. Mycological Research 99: 143–153. Pa¨rtel M, 2002. Local plant diversity patterns and evolutionary history at the regional scale. Ecology 83: 2361–2366. ¨ , Tuvi E-L, 2004. Conservation Pa¨rtel M, Helm A, Ingerpuu N, Reier U of Northern European plant diversity: the correspondence with soil pH. Biological Conservation 120: 525–531. Poschlod P, WallisDeVries MF, 2002. The historical and socioeconomic perspective of calcareous grasslands – lessons from the distant and recent past. Biological Conservation 104: 361–376. Provoost S, Ampe C, Bonte D, Cosyns E, Hoffmann M, 2004. Ecology, management and monitoring of grey dunes in Flanders. Journal of Coastal Conservation 10: 33–42. R Development Core Team, 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0. http://www.R-project.org (accessed 12.09.09). Roem WJ, Berendse F, 2000. Soil acidity and nutrient supply ratio as possible factors determining changes in plant species diversity in grassland and heathland communities. Biological Conservation 92: 151–161. Rozema J, Laan P, Broekman R, Ernst WHO, Appelo CAJ, 1985. On the lime transition and decalcification in the coastal dunes of the province of north Holland and the island of Schiermonnikoog. Acta Botanica Neerlandica 34: 393–411. ˚ , Tyler G, 1990. Soil factors influencing the distribution Ru¨hling A of macrofungi in oak forests of southern Sweden. Holarctic Ecology 13: 11–18.
365
Schla¨pfer M, Zoller H, Ko¨rner C, 1998. Influences of mowing and grazing on plant species composition in calcareous grassland. Botanica Helvetica 108: 57–67. Sunhede S, 1989. Geastraceae (Basidiomycotina); morphology, ecology and systematics with special emphasis on the North European species. Synopsis Fungorum 1: 1–534. Sterner R, 1922. The continental flora of South Sweden. Geografiska Annaler 4: 221–441. Tamis WLM, van’t Zelfde M, van der Meijden R, Groen CLG, Udo de Haes HA, 2005. Ecological interpretation of changes in the Dutch flora in the 20th century. Biological Conservation 125: 211–224. Tyler G, 1992. Inability to solubilize phosphate in limestone soils – key factor controlling calcifuge habit of plants. Plant and Soil 145: 65–70. Tyler G, 1996. Mineral nutrient limitations of calcifuge plants in phosphate sufficient limestone soil. Annals of Botany 77: 649–656. Tyler G, Olsson PA, 1993. The calcifuge behaviour of Viscaria vulgaris. Journal of Vegetation Science 4: 29–36. Tyler T, 2005. The Bryophyte flora of Scanian sand-steppe vegetation and its relation to soil pH and phosphate availability. Lindbergia 30: 11–20. Wassen MJ, Venterink HO, Lapshina ED, Tanneberger F, 2005. Endangered plants persist under phosphorus limitation. Nature 437: 547–550. Wood SN, 2004. Stable and efficient multiple smoothing parameter estimation for generalized additive models. Journal of the American Statistical Association 99: 673–686. Woodcock BA, Pywell RF, 2010. Effects of vegetation structure and floristic diversity on detrivore, herbivore and predatory invertebrates within calcareous grasslands. Biodiversity and Conservation 19: 81–95. Wright JE, 1987. The Genus Tulostoma (Gasteromycetes) – a World Monograph. Bibliotheca Mycologia, vol. 113. J. Cramer, Berlin. 1–338.
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pH preferences of red-listed gasteromycetes in calcareous sandy grasslands: Implications for conservation and restoration Pa˚l Axel OLSSONa,*, Tim Krone SCHNOORa, Sven-A˚ke HANSONb a
Plant Ecology and Systematics, Ecology Building, Lund University, SE-223 62 Lund, Sweden Birkagatan 49, SE-256 55 Helsingborg, Sweden
b
article info
abstract
Article history:
Species diversity in sandy grasslands is threatened by decalcification and eutrophication.
Received 28 September 2009
To determine the most appropriate conditions for red-listed gasteromycete fungi in such
Revision received 18 January 2010
grasslands, we investigated their pH preferences in this habitat in southern Sweden.
Accepted 3 February 2010
During two winters soil samples were collected from the vicinity of mycelia of these
Available online 24 April 2010
species. Chemical analysis revealed that none of the fungi occurred in sandy habitats with
Corresponding editor:
a pH lower than 5, although pH values between 4 and 5 are very common in sandy
Jacob Heilmann-Clausen
grasslands in the area. We found niche differentiation within the genus Tulostoma in that two out of four species occurred mainly in soils with high lime content, while one had
Keywords:
a broad niche and one occurred mainly in soils low in lime and with a pH below 7.5. Also in
Conservation
the genus Geastrum, some species occurred at high lime content, while most Geastrum as
Disciseda
well as two Disciseda species preferred soils with only low amounts of lime. We conclude
Gasteromycetes
that many species prefer areas with neutral to slightly acid soil. The results were compared
Geastrum
with data for key plant species collected in a previous study of calcareous sandy grasslands
Sandy grassland
and this showed that these in general had a wider pH range than the studied fungi. The
Soil pH
results highlight the importance of varying pH levels in protected areas and that the
Tulostoma
transition zone between lime-containing topsoil and complete decalcification is a preferred environment for many red-listed fungi as well as plants. ª 2010 Elsevier Ltd and The British Mycological Society. All rights reserved.
Introduction Semi-natural calcareous grasslands are some of the most species-rich communities in Europe. In Europe, calcareous soils and low P availability are usually associated with high plant species diversity (Janssens et al. 1998; Ewald 2003; Olsson & Tyler 2004; Wassen et al. 2005). Grazing by cattle, sheep and horses is used to manage calcareous grasslands for conservation (Schla¨pfer et al. 1998; Poschlod & WallisDeVries 2002). Conservation targets are typically endangered invertebrates,
birds or vascular plants whereas fungi are rarely considered. Basidiomycete fungi are a species-rich group with different functions in ecosystems. Many are symbiotic, while others are saprotrophs. Soil acidification restricts many fungal species in forests, and pH, base cation content and organic matter seem to be among the best abiotic predictors of fungal distribution (Ru¨hling & Tyler 1990). This also applies to the gasteromycete Lycoperdon perlatum, which is sensitive to the acidification of forests in northern Europe (Hansen 1989). Most gasteromycetes occur in grasslands,
* Corresponding author. Tel.: þ46 46 222 4247. E-mail address: [email protected] (P.A. Olsson). 1754-5048/$ – see front matter ª 2010 Elsevier Ltd and The British Mycological Society. All rights reserved. doi:10.1016/j.funeco.2010.01.004
358
and sandy grasslands in particular hold a unique set of redlisted gasteromycetes. It has been shown that the unique sandy vegetation in southeast Sweden holds a large number of gasteromycetes from the genera Tulostoma, Geastrum and Disciseda (Hanson & Jeppson 2005). The Tulostoma species in particular are closely connected with tree-less, base-rich, sandy grasslands (Hanson 2008). It is generally found that different Tulostoma species often grow at the same sites and also together with other gasteromycetes such as Disciseda and Geastrum (Kers 1975; Brochmann et al. 1981; Wright 1987; Do¨rfelt & Bresinsky 2003). However, even if many species grow at the same sites, local variation may still be large in sandy habitats (Ma˚rtensson & Olsson 2010). It has been observed that in particular Tulostoma kotlabae and Tulostoma melanocyclum often grow close to Tulostoma brumale (Hanson 2008) and Disciseda candida close to Geastrum schmidelii (Hanson 2009), while other species seldom do. The gasteromycetes in sandy soils are favoured by some level of soil disturbance, natural or man-made (Kreisel 1987; Do¨rfelt & Bresinsky 2003; Hanson 2008), and T. brumale, for example, occurs on roadside slopes (Krieglsteiner 2000; Do¨rfelt & Bresinsky 2003; Hanson 2008) as well as in semi-natural grasslands where soil disturbance may be caused by grazers. Many of the gasteromycetes are favoured by sloping ground and occur mostly on south-facing slopes, although some variation between the species may occur (Brochmann et al. 1981; Hanson 2008). The Tulostoma species are often found close to bryophytes of the genus Syntrichia, and there has been speculation whether Tulostoma species may grow in symbiosis with them (Andersson 1950; Wright 1987). The soil pH has a profound effect on all organisms and processes in the soil. It influences the solubility of toxic metals and mineral nutrients and, hence, may lead to chemical stress at extreme values and influences nutrient availability to plants. At a pH below 5, Al and Mn are released into the soil solution inhibiting the growth of many plants (Foy & Flemming 1978). In alkaline soil, on the other hand, phosphorus and iron availability decreases, restricting the distribution of many plant species (Grime & Hutchinson 1967; Kinzel 1983; Tyler 1992; Tyler & Olsson 1993). In southern Sweden, sandy grasslands show high variation in soil pH over distances as short as a few meters (Ma˚rtensson & Olsson 2010). Sandy grasslands occur on glaciofluvial deposits and on dunes, often near the coast. In certain areas, the sand contains calcium carbonate, in which case alkaline conditions prevail. Other sandy soils are strongly acid. There seem to be few sandy soils of intermediate pH (Rozema et al. 1985; Tyler 2005; Olsson et al. 2009) due to the very low base cation buffering capacity of sand once the original lime has been depleted; cation exchange capacity is very low as a result of the low content of clay and organic matter in sandy soils. The sandy grasslands of southern Sweden have a long history of human land use. Extensive arable rotation practices with prolonged fallow have prevailed until the early 20th century. Today, the areas are kept open mainly by grazing. In the area, the proportion of non-arable open land decreased from 79 % in 1862 to 51 % in 1960 (Mattiasson 1974). This was mainly due to sand-binding pine plantations, which during the same period increased from 3 to 38 % of the total land area. The calcareous sandy grasslands are threatened by a number of factors such as acidification (Roem & Berendse 2000),
P. A. Olsson et al.
nitrogen deposition (Bobbink et al. 1998), fertilization and reduced intensity of management (Olsson 1994), which may eventually lead to vegetation changes and the loss of many rare species (Tamis et al. 2005). Inappropriate land use may change the vegetation structure irreversibly (Marrs & Britton 2000). Semi-natural grassland may be converted into intensive farmland or be used for building houses and roads. Our purpose was to investigate the variation in pH and lime preferences in red-listed gasteromycetes in xeric sand calcareous grasslands, protected under the EU directive (code 6120). By this we expected to gain information about the best management regime to protect this threatened group of fungi. We hypothesised that species that often grow together have similar pH preferences, while species that seldom grow directly together have not. Based on earlier findings we therefore hypothesised that: (1) T. brumale, T. melanocyclum and T. kotlabae have similar pH preferences; (2) Tulostoma fimbriatum differs from these (Hanson 2008); and (3) D. candida and G. schmidelii have similar pH preferences (Hanson 2009). We also compared the preferences of the red-listed gasteromycetes with those of the key plant species in the habitat to find out if their preferences were the same when it comes to soil chemical properties. This was done since at present the vascular plants are used as main indicators of the habitat type. The main focus was on pH and lime content, but we also analysed soil minerals to investigate if any of the fungi had any particular preferences in this respect.
Materials and methods Study area The study area was coastal eastern Scania (Ska˚ne), between the cities of Kristianstad and Simrishamn in southernmost Sweden (Fig 1). The area is about 80 km long and 35 km wide, between 55 400 and 56 100 N, and 13 900 and 14 300 E. The areas with calcareous sandy grasslands (including ‘‘xeric sand calcareous grasslands’’ protected under the Natura 2000 EU habitat directive as habitat 6120), vary in size between 15 m2 and 90 000 m2 (Olsson 1994). The ecosystem is characterised by an open sward, which appears to depend on regular disturbance of the surface soil layer. These sandy calcareous grasslands have developed on glaciofluvial sand with little eolian redistribution. Weathering of lime deposits gave rise to lime-rich sand on many coastal sites in eastern Scania and on the Baltic islands. Since the end of the Weichselian glaciation c. 15 000 BP, this material has been continuously subjected to weathering. The depletion of lime may have increased during recent years due to acid rain. Only a few places with typical vegetation of calcareous sandy grasslands occur today, constituting a total of less than 50 ha (Olsson 1994; Tyler 2005). Koeleria glauca is a species of xeric sand calcareous grasslands in Sweden, as is Dianthus arenarius ssp. arenarius, that is endemic to the Baltic region. Xeric sand calcareous grasslands are replaced by heath-like vegetation as the soil becomes acidified. Acidic sandy grassland is mainly characterised by the grass Corynephorus canescens and it is similar to grey dune vegetation elsewhere (e.g. Bruun & Ejrnæs 2000; Provoost et al. 2004; Frederiksen et al. 2006).
pH preferences of red-listed gasteromycetes
359
Fig 1 – Map showing the investigation area in eastern Scania, southernmost Sweden. The dots denote approximately areas with calcareous sandy grasslands. Note that, in most cases, plots are distributed over a much larger area than each dot shows. Scale bar [ 10 km, dark grey [ urban areas, light grey [ areas of igneous rock.
The soil type of the xeric sand calcareous grassland is a pararendzina characterised by a thin humus-enriched layer on top of CaCO3-containing sand. On degenerated pararendzina, the layer containing calcium carbonate occurs as a deep C-horizon below a B-horizon, which is enriched with iron but with virtually no calcium carbonate. If depletion continues, a podzoloid soil type develops and the ecosystem changes into a Calluna heath. Earlier studies in the area have shown that the most common pH values of sandy grasslands in the study are those between 4 and 5 and that soils with pH above 7 are rare (Olsson 1974).
Sampling strategy The study was based on knowledge from a survey that has been going on since 1994, in which the occurrence of fungi – particularly gasteromycetes has been recorded in sandy grasslands of eastern Scania (Hanson & Jeppson 2005). During the winters 2007 (2006-12-27 to 2007-04-02) and 2008 (2007-0919 to 2008-02-10) all sites were visited and soil samples
(0–10 cm) were collected within mycelia of each species in the genera Tulostoma, Geastrum and Disciseda. The gasteromycetes usually develop fruit bodies during the autumn. They are persistent, however, and can be found during the whole winter and late in spring. They can even persist until the following summer, but they are then less easy to find due to the vegetation, and some of them may blow away. In the first season we collected 130 soil samples from 33 different sites and in the second season 108 samples from 33 sites. In total, samples were collected from 51 different sites. Soil was sampled only once within each mycelium. The numbers of samples reflect the number of mycelia studied, but in some cases more than one species occurred at the same spot. Some of the sites were large, such as certain military training fields and nature reserves, and at these sites there were many mycelia, and therefore more samples were taken from these sites to reflect the distribution of the species in the sandy grasslands. All species in the sandy grasslands except one (Geastrum striatum) are nationally red-listed (Ga¨rdenfors 2005). The
360
following species were included (with their red-list status): Disciseda bovista (EN), D. candida (VU), Geastrum berkeleyi (EN), Geastrum floriforme (CR), Geastrum minimum (VU), Geastrum pseudolimbatum (CR), Geastrum saccatum (EN), G. schmidelii (NT), T. brumale (NT), T. fimbriatum (EN), T. kotlabae (EN) and T. melanocyclum (CR).
Additional data sets To compare with the distribution of plant species, we analysed the distribution of some important key plants of sandy grasslands. These data come from a previous study (Olsson et al. 2009) where 136 plots of calcareous sandy grassland were analysed for the vegetation composition. We also analysed the whole of this data set, which reflects the distribution of both calcareous and decalcified sandy soils in calcareous areas. To widen the picture we analysed the data from Olsson (1974) and his ‘‘Studies on south Swedish sand vegetation’’, which includes both calcareous and noncalcareous areas. The areas in both these studies were intensively surveyed for the gasteromycetes in the present study.
Soil chemical analyses Soil samples were stored frozen until further treatment. All 236 samples were analysed for pH (10 g of soil was suspended in 30 ml of distilled water and pH was measured electrometrically in supernatants obtained through 2 hr extraction in a rotator). In 171 soil samples from both seasons the total amounts of Ca, Mg, and P were determined using ICP-AES (Inductively Coupled Plasma-Atomic Emission Spectrometry) after extraction in hot H2SO4. The concentration of Ca was recalculated to CaCO3 concentration, assuming that most of the calcium in the soils is present as CaCO3. The total Ca content was recalculated to lime content (CaCO3), assuming that all Ca was present as CaCO3. From all the 106 soil samples from the second season we analysed the total amounts of Ca, Mg, P, B, K, Mn, Cd, Zn, Cu and Pb using the same method as described above.
Statistical methods We divided each data set for pH into intervals of 0.25 pH units and thus obtained a frequency at each interval. The distribution of mycelia in relation to lime content was analysed after dividing the data into logarithmic intervals to achieve a more normally distributed data set. The occurrence of each species as an effect of soil pH was modelled using GAM models (Ejrnæs 2000) with the mgcv-package (Wood 2004) in R (R Development Core Team 2008). Models used Poisson distributions throughout, since data consisted of counts. We used principal component analysis (PCA), as implemented in the program CANOCO (ter Braak 1986), to identify the relations between soil elements and occurrences of the different fungal species.
P. A. Olsson et al.
Results The soil samples with mycelia showed a pH distribution between 5 and 9, skewed towards alkaline pH values. There was a strong relation between soil pH and lime content in the analysed soils. With lime content below a few percent, the pH dropped drastically (Fig 2A). There was a positive linear relation between lime and total Mg content (Fig 2B) and total P content (Fig 2C). T. brumale and T. melanocyclum were, with few exceptions, restricted to the alkaline pH range and this resulted in narrow unimodal response curves (Fig 3A). T. kotlabae and T. fimbriatum both frequently occurred from pH 8 and down to 6, but the predicted response curves for these two species were not significant (P > 0.05). The genus Geastrum as a whole had a pH range in the sandy grasslands with a predicted frequency peak between 6 and 7 (Fig 3A), with a significant (P 0.05) unimodal relation for the species that was most commonly found in the sandy grasslands, G. schmidelii, while the response curves for neither the other Geastrum species nor Disciseda spp. were significant. Within the Geastrum genus, G. saccatum, G. pseudolimbatum and G. floriforme only occurred at pH below 7 and G. berkeleyi at pH above 7, but the records for these species were too few to allow modelling of response curves. Three of the tested plant species showed significant (P 0.05) bimodal response curves to pH in sandy grasslands (Fig 3B), mainly due to the lack of plots with intermediate pH (Fig 3C). The main indicator for calcareous sandy grasslands in the region, K. glauca, showed a wide pH range from 5 to around 9.5. D. arenarius had a distribution similar to that of K. glauca. On the other hand, Festuca polesica and Alyssum alyssoides seemed restricted mainly to plots with alkaline pH and showed significant (P 0.05) unimodal or truncated unimodal response curves to pH. The acid tolerant species C. canescens had a distribution similar to that of K. glauca in these areas, but with the highest peak at acid soil pH. T. brumale and T. melanocyclum occurred, frequently above 10 % lime (Fig 4). The predicted unimodal lime response curves of these two species were clearly separated from those of Geastrum spp. and Disciseda spp., which had significant (P 0.05) monotone response curves at low lime content. Geastrum species mainly occurred with a lime content lower than 1 %, with G. berkeleyi, G. minimum and G. schmidelii being the only species occurring in soils with more than 1 % lime. No significant (P > 0.05) response curves were obtained for T. fimbriatum and T. kotlabae, but the results indicate that they often occur at lower lime content than T. brumale and T. melanocyclum. T. fimbriatum never occurred in soil with more than 2 % lime, and was thus distinguished from the most common species in the genus, T. brumale. PCA analysis of soil elemental composition revealed that the first ordination axis explained 66 % of the variation between samples (Fig 5). PCA axis 1 was closely related to Ca and Mg content. A second PCA axis explained 13 % of the variation and was related to the metals Pb, Cu, Zn, Cd, and Mn. The total content of P, K and B showed relation both to axis 1 and axis 2. Three of the Tulostoma species (T. brumale, T. melanocyclum and partly T. kotlabae) were in general distributed to the right in the ordination and the others,
pH preferences of red-listed gasteromycetes
A
9
361
A
R2 = 0.73
8.5
G. schmidelii*, n=35 Disciseda spp NS, n=18 Geastrum spp NS, n=28 T. fimbriatum NS, n=15 T. kotlabae NS, n=16 T. melanocyclum**, n=25 T. brumale***, n=116
Predicted frequency
0.3
8
7.5
pH (H2O)
0.35
7 6.5
0.25 0.2 0.15 0.1 0.05
6
0 5.5
B
0.3 C. canescens**, n=70 D. arenarius**, n=41 K. glauca***, n=102 F. polesica**, n=18 A. alyssoides***, n=36
5 2500
0.25
Predicted frequency
B y = 450 + 29x R2 = 0.56
Mg (µg g-1)
2000
1500
0.2
0.15
0.1
0.05 1000
0
C 0.15 500
Predicted frequency
Olsson-74***, n=95 Olsson-09***, n=137
0 1200
C
y = 370 + 9.8x R2 = 0.14
Total P (µg g-1)
1000
0.1
0.05
800
0
600
4
5
6
7
8
9
pH (H2O) 400
200
0
0
10
20
30
40
50
CaCO3 (%) Fig 2 – The chemical properties of all soils sampled (n [ 171) in the vicinity of mycelia of Tulostoma spp., Geastrum spp. and Disciseda spp. in calcareous sandy grasslands of eastern Scania. (A) The relation between total CaCO3 and pH fitted to a Gaussian function (P < 0.001), (B) the relation between CaCO3 and total Mg content subjected to a linear regression (P < 0.001), (C) the relation between CaCO3 and total P content subjected to a linear regression (P < 0.001).
Fig 3 – Predicted pH response curves of (A) gasteromycetes and (B) plants, and (C) the distribution of sites in calcareous sandy grasslands of eastern Scania. Geastrum spp. represents the combined frequencies of five species (G. pseudolimbatum, n [ 4, G. saccatum, n [ 5, G. floriforme, n [ 3, G. minimum, n [ 6, G. berkeleyi, n [ 8, G. striatum, n [ 1) and Disciseda spp. represents two species (D. candida, n [ 14, D. bovista, n [ 4). The data for the plants presented in (B) comes from a study of a total of 136 plots collected in a previous study (Olsson et al. 2009) and re-analysed here. The site data comes from one study of calcareous sandy grasslands (Olsson et al. 2009) and from one study of sandy habitats in general in the region (Olsson 1974).
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2.0
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G. schmidelii**, n=15 Disciseda spp*, n=14 Geastrum spp**, n=17 T. fimbriatum NS, n=15 T. kotlabae NS, n=13 T. melanocyclum***, n=25 T. brumale***, n=63
PCA 2 (13 %)
0.5
Pb
Cd Mn K
P Mg
Ca
0.3
-1.0
Predicted frequency
0.4
Cu Zn
0.2
-2.0 0.1
0
1
10
100
Lime content (%) Fig 4 – Predicted lime response curves of gasteromycetes in calcareous sandy grasslands of eastern Scania. Geastrum spp. represents the combined frequencies of five species (G. pseudolimbatum, n [ 3, G. saccatum, n [ 3, G. floriforme, n [ 3, G. minimum, n [ 4, G. berkeleyi, n [ 4) and Disciseda spp. represents two species (D. candida, n [ 11, D. bovista, n [ 3).
including T. fimbriatum and partly T. kotlabae to the left, reflecting the preference for high soil lime content of three of the Tulostoma species. There was little indication of preferences or avoidance of metals in the soils, except that D. candida seemed to grow in soils with higher metal contents than the other species did.
Discussion Although the studied gasteromycetes often occur together (Brochmann et al. 1981; Do¨rfelt & Bresinsky 2003), we found strong support for the hypothesis that within sites they have different pH preferences. Kers (1975) found that T. brumale might occur in the same places as Disciseda in Sweden, but in microhabitats distinct from each other, which can be explained by the differences in pH preferences found in our study. With this result we highlight the importance of a dynamic management regime that creates or maintains a variation in soil conditions and successional stages within habitats in order to preserve a high biodiversity. It seems as many of the red-listed fungal species in calcareous sandy grasslands of southern Sweden are adapted to pH between 6 and 7.5, and all sites with red-listed gasteromycetes of the genera Tulostoma, Geastrum and Disciseda had pH between 5 and 9. The distribution was rather skewed and the peak was therefore between 7.5 and 8.5. This distribution differs from the general pH pattern of the sandy grasslands in the area, where the most common pH values are between 4 and 5 (Olsson 1974). The pH preference curves of the gasteromycetes also differed from those of most of the rare plants in the same habitat by being narrower. The skewness in our
PCA 1 (66 %)
3.0
Fig 5 – PCA ordination of soil elements in samples from the second season (n [ 106 soil samples from 121 records of fungal mycelia, since in some cases more than one species occurred at the same spot). Each soil sample from the vicinity of mycelia is represented by a dot and an indication of the fungal species present in the spot the sample was taken from. TB [ Tulostoma brumale, TM [ T. melanocyclum, TK [ T. kotlabae, TF [ T. fimbriatum, DC [ Disciseda candida, DB [ D. bovista, GS [ Geastrum schmidelii, GF [ G. floriforme, GP [ G. pseudolimbatum, GM [ G. minimum, GB [ G. berkeleyi, Gsa [ G. saccatum.
gasteromycete material was due to the fact that the most common species, T. brumale, showed a clear preference for alkaline soils, and hardly occurred in sites with low lime contents. On the other hand, most of the other species had an optimum below pH 7. A pH of 5.5 is generally considered as the boundary between acidic and non-acidic conditions and acidification below this level may lead to loss of species, and reduced biodiversity (Tyler 1996; Pa¨rtel 2002; Pa¨rtel et al. 2004). Also in these particular sandy areas there is a drop in the number of plant species in general, and of red-listed plant species below pH 5 (Olsson et al. 2009). Since these studies together with the present study show that the optimal pH for high diversity of both plants and fungi in grasslands is between 6 and 7.5, this has important implications for management and restoration measures. In earlier studies, it has been shown that intermediate pH levels are rare in sandy grasslands and dune systems (Rozema et al. 1985; Tyler 2005; Olsson et al. 2009), a fact that was to be expected due to low cation buffering, once the lime is depleted (Brady & Weil 2008). Thus, the rareness of the red-listed gasteromycetes may reflect that they occupy an intermediate state in the succession during acidification of calcareous sandy grasslands. Since most of these species seem to be sensitive to high lime content, their preferred habitat is rare and unstable, threatened by further acidification (Mattiasson 1974; Rozema et al. 1985). It might be that these species have evolved in areas where intermediate pH values are more common, and the fact that we consider them as species of calcareous soils may be due to the fact that noncalcareous soils in this part of the world tend to be very acid. The studied fungal species, as well as many plants growing in the calcareous sandy habitats, immigrated from the south and southeast after the last ice age (Sterner 1922). In southern
pH preferences of red-listed gasteromycetes
Europe insolation is stronger, which prevents acidification and this may explain why many plants (Sterner 1922; Tyler 1996) as well as fungi grow mainly in calcareous areas even though they avoid high lime content. The acidification of calcareous soils was in earlier landscapes prevented by erosion and soil disturbance (Poschlod & WallisDeVries 2002). Increased soil disturbance is therefore needed to prevent acidification of calcareous soils. Here we show that restoration should not be made in areas that are slightly acidified, since these may host many rare species. Our study shows that many of the species would have problems in habitats restored to high lime content. Restoration measures may best be implemented in areas where acidification has brought the pH to below 5, or in areas degenerated due to fertilization or tree plantation. Restoration measures creating a slightly acidic habitat from a strongly acidic one could be achieved using mild types of soil perturbation if base-rich material is present within the disturbance depth or if the organic layer is mixed with mineral soil. It may also be that the creation of sloping ground favours the fungal species and gives a more stable pH environment due to stronger insolation and less decalcification (Brochmann et al. 1981; Hanson 2008). The fact that the studied species are at the risk of going extinct, and that they often grow on sloping ground, may reflect that sloping ground has been more common in ancient landscapes and that the present landscape has been flattened due to modern agricultural practice and less erosion. Disciseda, on the other hand, seems to prefer flat ground and small-scale disturbance caused by trampling of horses (Hanson 2009) or people (Kers 1975). Within Tulostoma, T. fimbriatum preferred soil with the lowest lime content, which distinguished it from the other three species in the genus. Slope aspect shows very little difference between the Tulostoma species (Brochmann et al. 1981; Kreisel 1984; Hanson 2008). There are in general no mycelia growing on slopes facing N, NE or NW, and this seems to be the same for all the studied Tulostoma species. This may be due to more vegetation and more rapid accumulation of humus on the less drought-exposed north slopes. In the present study most species showed a typical hump-shaped distribution in relation to soil factors. However, in some cases, such as for T. kotlabae, the distribution was wide and flat and it could be worthwhile to investigate whether this reflects genetic differences between populations, in particular since the taxonomy of these fungal groups is under consideration (Wright 1987; Moreno et al. 1997). Calcareous soils may lead to a limited availability of elements such as P or Fe (Kinzel 1983). Acid soils on the other hand may lead to high solubility of metals such as Mn, Zn and Cu (Foy & Flemming 1978). While some fungi are sensitive to metals such as Cu, others accumulate metals and mycorrhizal fungi may protect plants from toxicity in contaminated soils (Brown & Wilkins 1985). The total amounts of metals we measured explained only a small part of the variation between samples. Further studies could also include the measurement of soluble metals and thus shed further light on the relations between Disciseda species and high metal availability. Sunhede (1989) measured pH in soil samples taken where Geastrum species occurred. He reported pH values generally
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lower than in our study. This may be due to differences in sampling strategy. Sunhede sampled the organic layer, while we sampled to a depth of 10 cm, irrespective of depth of the organic layer. Since organic matter is more acid than mineral soil, this may explain the differences between our studies. For example, Sunhede (1989) gave a pH range of 4.8–7.5 for G. schmidelii, while we found a pH range of 5.5–8.5. All gasteromycetes in this study can be considered as saprotrophs and there is no evidence for mycorrhizal formation, although they may grow near pines and other trees in sand dunes. Sunhede (1989) considered the thin organic layer as the substrate for the Geastrum species, though he showed that mycelium reached far below this layer. Fungal mycelia are capable of bidirectional translocation (Olsson 1995) and may thus forage for carbon energy in the organic soil and at the same time for mineral nutrients in the mineral soil. Ring formation in G. schmidelii (Sunhede 1989), T. fimbriatum (Hanson 2008) and D. bovista (Hanson 2009) indicates that the fungi form large mycelia with a possible diameter of more than 10 m. Such large mycelia are unlikely to grow only in the organic layer since this is often sparse and disrupted (Olsson et al. 2009) and may exhibit extreme temperatures during the summer. Thus the main carbon substrate may be the organic layer and this may be where the mycelia proliferate during fruit body formation (Sunhede 1989), but it is also likely that there is a less visible mycelium in lower soil layers.
Recommendations for management and restoration Drastic measures such as soil perturbation (Dolman & Sutherland 1994) may be important for the persistent preservation of sandy grasslands. Several observations indicate that the Tulostoma species (Hanson 2008) and Disciseda species (Kers 1975; Hanson in press) need at least 25 yr to establish mycelia large enough to form fruit bodies. Kers (1975) stated that Disciseda species did not occur in places created during the last 50 yr, but the occurrence of Disciseda as well as T. brumale on roadsides may indicate that they establish in shorter times (Hanson 2008, 2009). It is currently not known how long it takes for the Geastrum species to establish their mycelia, but the ring formation by G. schmidelii (Sunhede 1989) illustrates the ability of mycelia to be long-lived. Overall there is only vague indications of the establishment times for gasteromycetes in sandy soils and more knowledge could be gained from studies in the future in restored areas. Such knowledge is important for implementing disturbance regimes of sandy grasslands, and also to know when to expect results of restoration. The long time needed for the establishment of mycelia makes restoration measures difficult to interpret and emphasises the importance of using soil chemistry as an immediate indicator of restoration success that in a longer time perspective will favour different types of organisms. A system with regular cultivation and short-period fallowing may disfavour the red-listed gasteromycetes and they may not be able to recolonize (Hanson 2008, 2009). Frequent occurrence of gasteromycetes along former field margins (Hanson 2008) may indicate that those have been refuges in former agricultural landscapes. We conclude that few of the red-listed gasteromycetes are specialised to the typical initial stage of the habitat named
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‘‘xeric sand calcareous grasslands’’. Instead most of them seem specialised on intermediate types of calcareous sandy grasslands. However, the intermediate pH conditions between 6 and 7.5 are hardly possible without the presence of calcareous or sedimentary bedrock as parent material. The present results give support for a dynamic management of sandy grasslands and indicate that the decalcification process in calcareous topsoil favours a high biodiversity. Diversity in calcareous grassland depends on a variation in management types and a heterogeneous sward structure (Woodcock & Pywell 2010). Variation in pH is another effect of variation in succession stage and will also support diversity in calcareous grasslands as shown in this study of the gasteromycetes. For the management of sandy habitats with red-listed gasteromycetes we suggest that grazing animals such as horses could be enough for creating small-scale disturbance. However, since habitats are vulnerable it is important also to create new habitats suitable for fungal colonisation. This could be achieved by careful topsoil removal in areas with too high nutrient levels, and in areas that are slightly acidified. In strongly acidified areas, on the other hand, more drastic measures such as deep perturbation and slope creation are recommended. Restoration measures could be performed close to known habitats, which will facilitate spread. The present study gives important information on the soil preferences of the red-listed gasteromycetes and this could be used as a guide in habitat restoration.
Acknowledgements This study was made possible through financial support from Region Ska˚ne, The Swedish Environmental Protection Agency, The Swedish Research Council and Formas. We thank Ingvar Ma˚nsson and Carl-Gustav Bengtsson for their help in the search for the gasteromycetes, Mikael Jeppson, who verified species determination for several of the specimens.
references
Andersson O, 1950. Larger fungi on sandy grass heaths and sand dunes in Scandinavia. Botaniska Notiser Supplement 2: 2. Bobbink R, Hornung M, Roelofs JGM, 1998. The effect of air-borne nitrogen pollutants on species diversity in natural and seminatural European vegetation. Journal of Ecology 86: 717–738. Brady NC, Weil RR, 2008. The Nature and Properties of Soils. Pearson Prentice Hall, NJ, USA. Brochmann C, Rustan OH, Brandrud TE, 1981. The genus Tulostoma (Gasteromycetes) in Norway. Blyttia 39: 209–226. Brown MT, Wilkins DA, 1985. Zinc tolerance of mycorrhizal Betula. New Phytologist 99: 101–106. Bruun HH, Ejrnæs R, 2000. Classification of dry grassland vegetation in Denmark. Journal of Vegetation Science 11: 585–596. ter Braak CJF, 1986. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67: 1167–1179. Dolman PM, Sutherland WJ, 1994. The use of soil disturbance in the management of Breckland grass heaths for nature conservation. Journal of Environmental Management 41: 123–140.
P. A. Olsson et al.
¨ kologie Do¨rfelt H, Bresinsky A, 2003. Die Verbreitung und O ausgewa¨hlter Makromyceten Deutchlands. Zeitchrift fu¨r Mykologie 69: 177–286. Ejrnæs R, 2000. Can we trust gradients extracted by detrended correspondence analysis? Journal of Vegetation Science 11: 565–572. Ewald J, 2003. The calcareous riddle: why are there so many calciphilous species in the Central European flora? Folia Geobotanica 38: 357–366. Foy CD, Flemming AL, 1978. The physiology of plant tolerance to excess available aluminium and manganese in acid soils. In: Jung GA (ed), Crop Tolerance to Suboptimal Soil Conditions. American Society of Agronomy, Madison, WI, pp. 301–328. Frederiksen L, Kollmann J, Vestergaard P, Bruun HH, 2006. A multivariate approach to plant community distribution in the coastal dune zonation of NW Denmark. Phytocoenologia 36: 321–342. Ga¨rdenfors U, 2005. The 2005 Red List of Swedish Species. Artdatabanken, Uppsala, Sweden. Grime JP, Hutchinson TC, 1967. The incidence of lime-chlorosis in natural vegetation of England. Journal of Ecology 55: 557–566. Hansen PA, 1989. Species response curves of macrofungi along a mull/mor gradient in Swedish beech forests. Vegetatio 82: 69–78. ˚ , 2008. An ecological study of Tulostoma species in Hanson S-A sandy habitats in SE Sweden (in Swedish). Svensk Mykologisk Tidskrift 29: 93–109. ˚ , 2009. An ecological study of Disciseda species in Hanson S-A sandy habitats in SE Sweden (in Swedish). Svensk Mykologisk Tidskrift 30: 17–32. ˚ , Jeppson M, 2005. Gasteromyceter i o¨stra Ska˚nes Hanson S-A sandsta¨ppsomra˚den – en sammanfattning av elva a˚rs inventeringsarbete. Svensk Mykologisk Tidskrift 26: 61–83. Janssens F, Peeters A, Talloowin JRB, Bakker JP, Bekker RM, Fillat F, Oomes MJM, 1998. Relationship between soil chemical factors and grassland diversity. Plant and Soil 202: 69–78. Kers LE, 1975. The genus Disciseda (Gasteromycetes) in Sweden. Svensk Botanisk Tidskrift 69: 405–438. Kinzel H, 1983. Influence of limestone, silicates and soil pH on vegetation. In: Lange OL, Nobel PS, Osmond CB, Ziegler HJ (eds), Physiological Plant Ecology III. Springer, Berlin, pp. 201–244. Kreisel H, 1984. Die Stielboviste (Gattung Tulostoma) der Deutschen Demokratischen Republik und Westberlins. Hercynia 21: 396–416. Kreisel H (ed), 1987. Pilzflora der Deutchen Demokratischen Republik. Basidiomycetes (Gallert-, Hut- und Bauchpilze) Fischer, Jena, Germany. Krieglsteiner GJ (ed), 2000. Die Großpilze Baden-Wu¨rttembergs. Band 2. Sta¨nderpilze: Leisten-, Keulen-, Korallen-, und Stoppelpilze, Bauchpilze, Ro¨hrlings- und Ta¨ublingsartige pilze. Ulmer, Stuttgart (Hohenheim), Germany. Marrs R, Britton A, 2000. Conservation problems on Breckland heaths: from theory to practice. Biological Conservation 95: 143–151. Ma˚rtensson L-M, Olsson PA, 2010. Soil chemistry of local vegetation gradients in sandy calcareous grasslands. Plant Ecology 206: 127–138. Mattiasson G, 1974. Sandsta¨pp. Vegetation, dynamik och sko¨tsel. Meddelanden fra˚n Avdelningen fo¨r Ekologisk Botanik, Lunds universitet 2: 1–40. Moreno G, Alte´s A, Ochoa C, Wright JE, 1997. Notes on type materials of Tulostoma. Some species with mixed holotypes. Mycological Research 101: 957–965. Olsson H, 1974. Studies on south Swedish sand vegetation. Acta Phytogeographica Suecica 60: 176. Olsson K-A, 1994. Sandsta¨pp i Ska˚ne – ett upprop. Lunds Botaniska Fo¨rening Medlemsblad 2: 4–13.
pH preferences of red-listed gasteromycetes
Olsson PA, Ma˚rtensson LM, Bruun HH, 2009. Acidification of sandy grasslands – consequences for plant diversity. Applied Vegetation Science 12: 350–361. Olsson PA, Tyler G, 2004. Occurrence of non-mycorrhizal plant species in south Swedish rocky habitats is related to exchangeable soil phosphate. Journal of Ecology 92: 808–815. Olsson S, 1995. Mycelial density profiles of fungi on heterogeneous media and their interpretation in terms of nutrient reallocation patterns. Mycological Research 99: 143–153. Pa¨rtel M, 2002. Local plant diversity patterns and evolutionary history at the regional scale. Ecology 83: 2361–2366. ¨ , Tuvi E-L, 2004. Conservation Pa¨rtel M, Helm A, Ingerpuu N, Reier U of Northern European plant diversity: the correspondence with soil pH. Biological Conservation 120: 525–531. Poschlod P, WallisDeVries MF, 2002. The historical and socioeconomic perspective of calcareous grasslands – lessons from the distant and recent past. Biological Conservation 104: 361–376. Provoost S, Ampe C, Bonte D, Cosyns E, Hoffmann M, 2004. Ecology, management and monitoring of grey dunes in Flanders. Journal of Coastal Conservation 10: 33–42. R Development Core Team, 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0. http://www.R-project.org (accessed 12.09.09). Roem WJ, Berendse F, 2000. Soil acidity and nutrient supply ratio as possible factors determining changes in plant species diversity in grassland and heathland communities. Biological Conservation 92: 151–161. Rozema J, Laan P, Broekman R, Ernst WHO, Appelo CAJ, 1985. On the lime transition and decalcification in the coastal dunes of the province of north Holland and the island of Schiermonnikoog. Acta Botanica Neerlandica 34: 393–411. ˚ , Tyler G, 1990. Soil factors influencing the distribution Ru¨hling A of macrofungi in oak forests of southern Sweden. Holarctic Ecology 13: 11–18.
365
Schla¨pfer M, Zoller H, Ko¨rner C, 1998. Influences of mowing and grazing on plant species composition in calcareous grassland. Botanica Helvetica 108: 57–67. Sunhede S, 1989. Geastraceae (Basidiomycotina); morphology, ecology and systematics with special emphasis on the North European species. Synopsis Fungorum 1: 1–534. Sterner R, 1922. The continental flora of South Sweden. Geografiska Annaler 4: 221–441. Tamis WLM, van’t Zelfde M, van der Meijden R, Groen CLG, Udo de Haes HA, 2005. Ecological interpretation of changes in the Dutch flora in the 20th century. Biological Conservation 125: 211–224. Tyler G, 1992. Inability to solubilize phosphate in limestone soils – key factor controlling calcifuge habit of plants. Plant and Soil 145: 65–70. Tyler G, 1996. Mineral nutrient limitations of calcifuge plants in phosphate sufficient limestone soil. Annals of Botany 77: 649–656. Tyler G, Olsson PA, 1993. The calcifuge behaviour of Viscaria vulgaris. Journal of Vegetation Science 4: 29–36. Tyler T, 2005. The Bryophyte flora of Scanian sand-steppe vegetation and its relation to soil pH and phosphate availability. Lindbergia 30: 11–20. Wassen MJ, Venterink HO, Lapshina ED, Tanneberger F, 2005. Endangered plants persist under phosphorus limitation. Nature 437: 547–550. Wood SN, 2004. Stable and efficient multiple smoothing parameter estimation for generalized additive models. Journal of the American Statistical Association 99: 673–686. Woodcock BA, Pywell RF, 2010. Effects of vegetation structure and floristic diversity on detrivore, herbivore and predatory invertebrates within calcareous grasslands. Biodiversity and Conservation 19: 81–95. Wright JE, 1987. The Genus Tulostoma (Gasteromycetes) – a World Monograph. Bibliotheca Mycologia, vol. 113. J. Cramer, Berlin. 1–338.