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The macrofungi on a former sea floor
THE MACROFUNGI ON A FORMER SEA FLOOR P. Bremer*, C.G.N. van Zanen**, & M.T. Veerkamp***
Introduction
been planted on the polders and the changes to be expected. The mass planting of woods on mainly calcareous and pH-neutral to basic soils is unique in the Netherlands, so at the start of the survey it was difficult to predict what changes would take place. Moreover we expected that on a former sea floor a primary colonization by fungi would occur, with spores of most species arriving from outside the polders, whereas in most cases in the Netherlands a secondary colonisation has occurred with spores present in situ. Eight years after starting the inventory Tjallingii & Tjallingii-Beukers (1983) showed the importance of calcareous habitats in the polders and expected species
his paper looks at the mycota of the relatively new Dutch province of Flevoland, which is made up of three polders reclaimed from the sea since 1942. A working group of the Dutch Mycological Society (NMV), in which a number of amateur and professional mycologists collaborate, was set up in 1976 after the discovery of a large number of fruitbodies of Helvella acetabulum on one of the artificial grass-covered beaches (green shores) of Oostelijk Flevoland (see Figure 1). Questions were raised in relation to the composition of the young woods that had
T
Figure 1. The province of Flevoland with woodlands and green shores (
) .
*P. Bremer, Roelingsbeek 1, 8033 BM Zwolle [email protected]; ** G.C.N. van Zanen, De Breekstraat 36, 1024 LJ Amsterdam; *** M.T. Veerkamp, Pelikaanweg 54, 3985 RZ Werkhoven.
45
off the sea). After reclamation natural vegetation developed comprising marshes, reed-beds, willow carr and some silt-based grasslands (see Feekes & Bakker, 1954; Bakker, 1957; Jans & Drost, 1995), which were almost completely cultivated within 15 years. In Zuidelijk Flevoland 5900 ha of marshland and open water was not cultivated and is now protected as nature reserve (Oostvaardersplassen, see Figure 1). In the three polders more than 13,000 ha of woodlands were planted. This planting started in 1944 (at Voorsterbos) and the large scale planting ended in 1997. In the Noordoostpolder the woods were planted on nutrient-poor soil (peat, boulder clay, sand) but in the other two polders clay soils were singled out for planting. Nearly all the soils have a high lime content because of the millions of shellfish which died after the closure of the former Zuiderzee. To drain the polders, hundreds of km of trenches were dug in the oldest woods with densities up to 1 km per ha. On light clay soils the groundwater level can nevertheless be high in springtime. At various locations (under 5 % of the total area) seepage reaches the roots of the herb layer. Various tree and shrub species were planted, of which the most important being: Norway spruce Picea abies and Sitka spruce P. sitchensis on peaty and sandy soils, pines Pinus spp on sandy soils, pedunculate oak Quercus robur, sycamore Acer pseudoplatanus and ash Fraxinus excelsior on all soil types. Vast plantations of poplars Populus spp were planted in all the polders, especially on clay soils. Alder Alnus glutinosa was planted in combination with other species, due to its nitrogen-fixing capacity. Most species have been planted as a monoculture, but multi-species plantations can be found in nearly all larger woods as well. Approx. 270 ha of woodlands are natural and dominated by white willow Salix alba and are not exploited. Except for some forest reserves and two woodlands (Voorsterbos, Harderbos) all the stands are
from older natural woodlands to increase, e.g. species belonging to Cortinarius subg. Phlegmacium. It was expected that the number of species would be related to the age and the composition of the soil. A number of plots were monitored to assess this succession. Species associations were developing in Flevoland, reflecting the fact that various woodland types have their own characteristic mycoflora. Visiting the woodlands The working group aimed to survey the mycota of more than 70 woods and natural areas in Flevoland. Members of the working group visited the woodlands in spring and autumn. Mycological inventories were carried out at the plots, which can be recognised in the field by ditches bordering them. During 30 years there have been hundreds of visits. Since 1990 the inventory has been intensified by weekly visits to one or two areas. Some areas were visited systematically, others were sampled on an ad hoc basis. Mycologically interesting plots were visited more often than those which were poor in species on the first visit, causing bias (Bremer et al. 2000). Plots have been monitored as well (Bremer 1994, van Zanen 2000). Although most attention has been paid to woodlands, information has been collected from nature reserves, road verges, dikes and green shores as well. The area Four polders have been reclaimed since the closure of the Zuiderzee in 1932: Wieringermeerpolder (1933), Noordoostpolder (1942), Oostelijk Flevoland (1957) and Zuidelijk Flevoland (1968) (Figure 3 ). In this paper the oldest polder is excluded as it does not belong to the province of Flevoland. From about 1600 these polders were part of the sea floor covered by a layer of 1 - 4 m of brackish to salty water. This became fresh water after 1932 ( when the Zuiderzee was transformed to the IJsselmeer by the construction of a 32 km dyke cutting 46
ecological groups are all represented: ectomycorrhizal species, terrestrial saprotrophfic species, saprotrophic species on wood and parasites. The ectomycorrhizal species are chiefly associated with spruce, willow and poplar but also with oak and beech. The genera Inocybe, Hebeloma and Cortinarius are especially well represented. From each of the genera Russula and Lactarius there is only one ‘characteristic’ species and both are associated with spruce, namely Russula nauseosa and Lactarius deterrimus. The presence here of Tuber and Hymenogaster (compared to their absence elsewhere) may be explained by specialist recording at this site. The terrestrial saprotrophs are well represented with 28 species. They grow on needles (Helvella confusa, Calocybe obscurissima) and leaves (Mycena capillaris) or in humus-rich mull soils (Conocybe sordida). Other important genera are Entoloma, Psathyrella and Conocybe. Saprotrophic species on wood (e.g. eight species of Pluteus) are fewer. Two of the characteristic species are parasites: Heyderia sclerotipes and Volvariella surrecta. Species favouring acid sandy soils are generally under-represented in Flevoland. Amanita rubescens, A. citrina, Boletus badius and B. edulis for example are
used for commercial forestry, meaning that there is thinning on a five to eight year cycle. Clear felling has only taken place after infections or windthrow. Regeneration, especially of ash Fraxinus excelsior has occurred in 30 year old plantations following heavy thinning. Acer pseudoplatanus and Betula are also successful. At one of the woods (Kuinderbos, 1100 ha) 21 species of trees and shrubs had become established. Thinning has accelerated stand differentiation and the development of a varied vertical structure. In Oostelijk and Zuidelijk Flevoland various nature reserves were created, while in the latter the natural vegetation has been preserved in Oostvaardersplassen. This area is famous because of its breeding and migratory birds (Vulink, 2002). Artificial beaches have been created along the dikes over a distance of c. 31 km for recreational purposes. At the majority of these ‘green shores’ a natural grassland or sometimes even heather vegetation has developed without human interference. Half of these shores are used for recreation, the others have developed into nature areas.
The survey Characteristic species After 30 years of recording a small number of species are now known exclusively from Flevoland, occurring nowhere else in the Netherlands. Only one of these species (Tephrocybe ozes) occurs at several locations and 61 species can be categorised as ‘characteristic’ (Figure 12). These are the species that are significantly more common in Flevoland than in adjacent parts of the Netherlands. Calocybe obscurissima (28 locations, 61 % of sites in Flevoland, Figure 2), Pterula multifida (11 locations, 61 %) and Hymenogaster populetorum (16, 76 %) can be regarded as the most characteristic species. Most such species prefer calcareous sandy and/or clayey soils. The most important
Fig. 2. After 30 years of recording, distribution of Calocybe obscurissima is clearly concentrated in the area of Flevoland (highlighted in yellow).
47
could be found. After the first thinning the amount of dead wood increases enabling saprotrophic species to colonise the stands. Mycorrhizal fungi could be found at this stage as well, especially in plantations on boulder clay, sand and peat. On clay mycorrhizal fungi are rare in this and later stages of the plantation. Bremer et al. (2000) surveyed the mycorrhizal flora of some woods in Oostelijk-Flevoland. In the Hollandse Hout on a clay soil, 11 species of Inocybe were recorded, some of them associated with stands of Picea abies. Although poplars have been planted in great numbers on clay, Lactarius controversus has only been found near poplars growing on boulder clay or on road verges. Numerous hypogeous macrofungi such as Tuber maculatum and Tuber puberulum have been found in plantations of Italian poplar Populus x canadensis (Daams & de Vries 1981, de Vries 2000). Poplar stands are poor in species, with low densities of fruitbodies. Although white willow Salix alba has been planted, more attention has been paid to natural woods where Salix alba is the dominant species. In these spontaneous woods the herb layer is dominated by nettle Urtica dioica, with elder Sambucus nigra dominating the shrub layer. One plot in this habitat in the Oostvaardersplassen was monitored for eight years. Of the 113 species 58 % appeared to be wood-decomposing, 38 % humus-decomposing and 4 % mycorrhizal. Cortinarius urbicus (Fig. 7) was found almost every year. Four species of Hebeloma were less common. Pterula multifida and Ramaria abietina were growing in this plot, although they were not known before from this habitat in the Netherlands. Plantations dominated by Quercus robur on sandy, calcareous soil or boulder clay are rich in species with a high density of fruitbodies. Mycorrhizal species are common, such as Amanita phalloides, Laccaria amethystina and numerous species of Inocybe and Cortinarius subgenus Telamonia. The same holds for plantations on boulder clay. The combination
rare. The same holds for Scleroderma citrinum, although it has increased since 1990 indicating acidification of sandy soils low in shell content. In the Polyporaceae there is a group of early colonizing species such as Tyromyces (Oligoporus) spp., Trametes versicolor and Ganoderma lipsiense (= G. applanatum). Figure 4 presents a list of late colonising species. Until about 1986 Piptoporus betulinus was absent, although Betula spp. were rather common in the woods on sandy or peat soils. This species has increased markedly since 1990. Meripilus giganteus was only found for the first time about 50 years after the first planting. Taxonomic problems At the start of the survey there were a number of problem species that appeared to be new to the Netherlands. Van der Laan (1978) proved that Stereum subtomentosum had been misidentified as Stereum hirsutum. After the first finds it was shown to be common in the polders and in other parts of the Netherlands as mycologists became familiar with this species (Figure 5). Parallel stories apply to Scleroderma areolatum, Stropharia cyanea (Tjallingii-Beukers 1980) and Polyporus tuberaster (Tjallingii 1983)(Figure 13). The holotypes of some species were collected in Flevoland (e.g. Inocybe tjallingiorum, Inocybe amethystina, Psathyrella almerensis).
Habitats in Flevoland and their mycota Woodlands Immediately after planting, the luxurious original vegetation of common reed Phragmites australis, creeping thistle Cirsium arvense and great hairy willowherb Epilobium hirsutum was poor in macrofungi. Saprotrophs living on litter, such as Agrocybe pediades, Psathyrella spp. and Coprinus comatus were the most common. Within 7 12 years the canopy closed and other species 48
proved to be much poorer in mycorrhizal species, probably because of the drier habitat (Figure 6). Some types of stand are rather rare but can be mycologically important. Hornbeam Carpinus betulinus stands on boulder clay have only been planted at a few locations. At one of them hornbeam and ash are mixed and appeared to be very rich in species and fruitbodies. During 7 years 25 ectomycorrhizal species were found in a small plot, with on average 240 fruitbodies per 100 m2 per visit (Bremer 1994). In this plot grassland species such as Ramariopsis tenuiramosa, Clavulinopsis helvola and Geoglossum spp. were growing together with Amanita phalloides, Cortinarius obtusus, Leccinum griseum (= L. carpini = L. pseudoscabrum) and Lactarius circellatus. In summary we can state that the soil composition and tree layer have a dominant impact on the mycota in the mostly welldrained stands. Only at some locations has seepage had a dominant impact, with alder Alnus glutinosa becoming the prominent tree species. Here alder is accompanied by a number of mycorrhizal species such as Alnicola spp, Paxillus filamentosus, Gyrodon lividus and Lactarius lilacinus.
of Quercus robur and acid sand is confined to the Voorsterbos, where sand with a very low shell content was deposited. Here Russula amoenolens, R. ochroleuca and Scleroderma citrinum are common while Boletus parasiticus was found for the first time in the province. On clay, mycorrhiza-forming species are rare and the mycota is dominated by saprotrophic species such as Collybia dryophila and Rutstroemia firma. High densities of fruitbodies can also be found in plantations of Norway spruce and Sitka spruce. There is no herb layer in the dense stands. Here decomposer species such as Mycena spp, Micromphale perforans and Clitocybe ditopa play an important role and Helvella spp can be common. In some years Helvella elastica is dominant. Pterula multifida has been common, forming large groups. Other characteristic fungi of these stands are Heyderia abietis, Geastrum pectinatum, Russula queletii and R. nauseosa. Because of infections of Heterobasidion annosum and/or Ips graphicus (a beetle), the vitality of most stands has declined. In some stands on sandy soils poor in clay c. 70 % of the trees are infected with Heterobasidion annosum (data State Forestry Service). There is a thinning cycle of five years and clearfelling only takes place on patches less than 2-3 ha in size. Here the spruces are replaced by deciduous tree species. Spruce trees on clay soils have a better vitality but will be replaced as well. In one monitored plot of Norway spruce on clay 107 species were found within eight years, all of them saprotrophic except for Inocybe cincinnata (Figure 6). In stands of pines (almost confined to sandy soils), various characteristic species have been found including Lactarius deliciosus, Chroogomphus rutilus and Suillus luteus. Mycorrhizal species are rare under beech on clay soils, but are rather common in the similar stands on boulder clay or sandy soil. In one plot 144 species were found during eight years, 10% ectomycorrhizal, with Lactarius blennius, Russula fellea and R. mairei being most common. A plot on fine sand
Other habitats Green shores are found along the dikes at the east side of Oostelijk and Zuidelijk Flevoland (Figure 1). They vary in width from 50 m to 175 m and about 50% of these areas are used for recreation. These shores vary in altitude, mud content, texture and lime content (and concomitantly pH). Due to trampling and mowing grasslands dominate and show a gradient in species composition from the waterline to the dike. On some shores dunelike vegetation can change within a short distance to heather. Fungi characteristic of the Dutch dunes, such as Agaricus devoniensis, Psathyrella ammophila, Poronia erici and Inocybe vulpinella have been found. The shores can be rich in Hygrocybe, Entoloma and Geoglossum spp. Apart from grassland the shores are charac49
years. Lactarius, Russula and Cortinarius subg. Phlegmacium have also stabilised (although an increase was expected). Remarkably, the number of Inocybe spp. still shows a continuing increase after 22 years. The same holds for the number of hypogeous fungi. Tuber maculatum was the first species observed. Now 20 species are known, half of the total number of hypogeous species found in the Netherlands (de Vries 2000).
terised by solitary trees and shrubs, small woodlands and bonfire sites. More than 600 species have been found on these shores (van Zanen et al. 2000). Flevoland was the first area in the Netherlands where natural habitats were planned and created. So artificial marshes, areas for breeding waders (de Jong 1977), and also natural grasslands were created by digging and water management. The Oostvaardersplassen proved to be mycologically poor in species due to its clay soil. Most road verges are on clay soils. They are fully vegetated but are poor in mushrooms. On one of these verges at Zuidelijk Flevoland, Allopsalliota geesterani was found. Lactarius controversus colonised verges on sandy clay soils with poplar in the vicinity of the Kuinderbos. Some verges consist of sand rich in shells and are covered with an open grassland vegetation. Here Hygrocybe spp. and Entoloma incanum have been found in combination with e.g. purging flax Linum catharticum and eyebright Euphrasia stricta.
Dispersal Most fungi have a high capacity for dispersal. Spore length varies between 4 and 40 μm and is on average 7.9 μm (based on a sample of 313 spp. found in the Voorsterbos). We assume that nearly all species were transported by wind from nearby populations in the Netherlands or even surrounding countries. Young trees and shrubs were reared in tree nurseries in the polder, although in the older woods these came from nurseries outside Flevoland. In the Noordoostpolder various tree species were even grown from seed (Wildschut 1992). A number of species could have arrived in the rootballs but we think that most species came from outside the area by wind. Figure 10 depicts the nearest distance between localities in the Voorsterbos and possible source populations outside the polder (based on 313 species). The Voorsterbos is positioned at a small distance from woods on the ‘old land’, making it interesting for monitoring the colonisation of both fungi and woodland plant species (Bremer 2003). The majority of fungi found in the Voorsterbos have also been found nearby and all species are known from localities within a radius of 100 km. Figure 11 shows the corresponding data for a different set of species, the characteristic species listed in Figure 12. In this selected group more species had to cross a larger distance. More than 20 species had to cross at least 80 km, and in the case of Entoloma lilacinoroseum it might be more than 300 km.
The number of species Figure 8 depicts the increase in the total number of fungi since 1975. In 25 years more than 1540 taxa of macromycetes have been found (van Zanen 2000), 37% of all species found in the Netherlands. Within 15 years of starting the inventory, the annual increase of new species recorded has stabilised except in Z.-Flevoland. This polder was planted much later and the inventory started simultaneously with the planting of woodlands. Hence the increase of new species recorded here reflects both the speed of colonisation and mycological effort. In the Noordoostpolder and O.-Flevoland, most species have been present since 1975 and the increase chiefly reflects the effort of mycologists. Figure 9 depicts the increase in the number of species for various genera in all the woods involved. After the start the number of Helvella spp stabilised within four 50
are rather poor in fungi this will have only a restricted impact on the mycota as a whole. Ash and sycamore are the most successful species regenerating on clay soils while birch is the most successful on sandy soil. When no planting takes place after felling, these species will form the next generation. As ash and sycamore do not form ectomycorrhizal relationships, the abundance of mycorrhizal fungi could decline in all woods. In plantations of pedunculate oak and beech new species will appear, but as observed in the last 25 years species can decline or disappear as well. For instance Calocybe chrysenteron and Suillus collinitus have not been refound since 1980 and have probably disappeared. There is still an increase of species being recorded for the first time but, as Figure 8 shows, the rate of increase has declined and the total number of species has reached stability.
It is remarkable that such a high number of hypogeous macrofungi have been found in the young planted woods (De Vries, 2000). Hypogeous macrofungi are eaten by animals which ensure dispersal. They also form a spore-bank so transport by soil might take place as well (Kjoller & Bruns 2003).
The future As the plantations age the mycota will change although succession is difficult to assess without plots being monitored for decades. Plots have been monitored now for at most eight years. As Van Zanen (2000) pointed out, no succession has been assessed in this period, although he was able to indicate some kind of succession when species lists were available from numerous stands over a longer period of time. As stated before the area with spruce is declining. For phytopathological reasons these stands will be replaced, most of them within 15 years. With the felling of spruce the dependent mycota will almost disappear. In a number of stands no felling will take place, so the degradation of these stands can be studied. This will allow various characteristic species to survive for a longer time. Poplars will be replaced as well, but as these stands
Acknowledgements We thank David Mitchel for stimulating the writing of this paper and for his corrections to it and Dr. T. Kuyper for his comments.
Polder
Year
Area (ha)
Woods
Number of woods > 10 ha
% clay
Noordoostpolder
1941-1942
48000
1977
11
28
O.-Flevoland
1957
54000
5465
19
73
Z.-Flevoland
1968
43000
5649
15
95
145000
13091
40
Total
Fig. 3. Some characteristics of the polders forming a part of the province of Flevoland. Year = year of reclamation, Woods = area of woodlands (planted or spontaneous), % clay = percentage of woodlands situated on clay soils.
51
Late colonizing species (after 40 years)
Y
Species still absent but to be expected in the future
Early colonizing species (within 0-20 years)
Y
Intermediate colonizing species (21-40 years)
Y
Polyporus brumalis
10
Phellinus ferreus
21 Meripilus giganteus
Daedaleopsis confragosa
14
Oligoporus stipticus
23
Ganoderma lucidum
Bjerkandera fumosa
15
Heterobasidion annosum
25
Ganoderma pfeifferi
Inonotus radiatus
15
Oligoporus caesius
25
Ganoderma resinaceum
Polyporus varius
15
Phellinus robustus
25
Grifola frondosa
Trametes versicolor
15
Pycnoporus cinnabarinus
25
Phellinus igniarius
Bjerkandera adusta
17
Trametes hirsuta
25
Datronia mollis
17
Abortiporus biennis
26
Polyporus badius
17
Ischnoderma benzoinum
26
Polyporus tuberaster
17
Phaeolus schweinitzii
26
Fomitopsis pinicola
19
Phellinus conchatus
26
Ganoderma lipsiense
19
Trichaptum abietinum
27
Oligoporus subcaesius
19
Trametes suaveolens
29
Oligoporus tephroleucus
19
Trametes pubescens
33
Polyporus squamosus
19
Fomes fomentarius
37
Skeletocutis nivea
19
Laetiporus sulphureus
38
Daedalea quercina
20
Ganoderma australe
38
Hapalopilus rutilans
20
Piptoporus betulinus
38
Phellinus tuberculosus
20
Trametes gibbosa
20
50 Fistulina hepatica
Fig. 4. The colonization of Polyporaceae in Flevoland and the time in years (Y) until first appearance.
Species
Species look-alike
First year of Publication recognition
Stereum subtomentosum
Stereum hirsutum
1977
van der Laan (1978)
Stropharia cyanea
Stropharia aeruginosa
1980
Tjallingii-Beukers (1980)
Scleroderma areolatum
Scleroderma verrucosum
1980
Polyporus tuberaster
Polyporus spp.
1982
Steccherinum bourdotii
Steccherinum robustum
1985
Fig. 5. Species taxonomically unravelled during the study of the mycota in Flevoland.
52
Tjallingii (1983)
Site name
Tree species
Soil type
Area
Years
nV nA
nM %
References
Kuinderbos
Picea sitchensis
fine calcareous sand
150 1985-92
27 31
2
Kuinderbos
Fagus sylvatica
fine calcareous sand
150 1985-92
27 35
5 14.3 Bremer (2000)
Kuinderbos
Quercus robur
fine calcareous sand
150 1985-92
27 31
4 12.9 Bremer (2000)
Voorsterbos
Carpinus-Fraxinus boulder clay
70 1985-92
36 47
25 53.2 Bremer (1994)
Roggebotzand
Picea abies
clay
1000 1991-98
49 49
Revebos
Quercus robur
medium fine sand
1000 1991-98
Oostvaardersplassen
Salix alba (natural)
clay
Spijkbos (meerdijk)
6.5 Bremer (2000)
2.0
van Zanen (2000)
46 61
14 23.0
van Zanen (2000)
1000 1991-98
61 46
5 10.8
van Zanen (2000)
Populus, + various fine calcareous tree species sand
1000 1988-90
8 82
17 20.7
Veerkamp (1992)
Hollandse Hout
Populus, + various clay tree species
1000
19982000
8 64
6 9.4
Veerkamp (2001)
Houtribbos
Populus, + various sand with clay tree species
1000
19982000
8 46
11 23.9
Veerkamp (2001)
1
Fig. 6. Percentages of mycorrhizal species in plots of various stand types and one natural wood in Flevoland. nV = number of visits, nA = number of Agaricales, Boletales and Russulales, nM = number of ectomycorrhizal species, % = nM/nA x 100.
Fig. 7. Cortinarius urbicus, a species found almost every year under Salix alba in a plot in Oostvaardersplassen. Photograph © M. van der Molen.
53
Fig. 8. The total number of species (cumulative) recorded in the three reclaimed polders: Noordoostpolder (NOP), O.-Flevoland (OFL) and Z.-Flevoland (ZFl) and Flevoland as a region during 25 years.
Fig. 9. The total number of species recorded in Flevoland during 23 years, for five genera and the group of hypogeous fungi (after de Vries 2000). Within Cortinarius only the subgenus Phlegmacium has been worked out.
54
Percentage of species
Distance (in 10 km steps)
Percentage of characteristic species
Fig. 10. The distance between locations in the Voosterbos and the nearest known population for 313 species based on distribution data given in NMV (2000a,b).
Distance (in 10 km steps)
Fig. 11. The distance between locations in Flevoland and known sites outside Flevoland for the group of 61 characteristic species listed in Fig. 12, based on distribution data given in NMV (2000a,b).
55
Number of 5x5 km grid cells in which species occur d
an
e
l vo
Fl
la
Ne
r de
Number of 5x5 km grid cells in which species occur
nd l ta
To
Agaricales
d
d
lan
an
Pluteus insidiosus
r de
al
e
Ne
t To
2
3
5
40.0
Fl
%
l vo
%
Tephrocybe ozes
4
0
4
100 Tubaria confragosa
6
9
15
40.0
Cortinarius viscidulus
6
1
7
85.7 Lactarius deterrimus
6
9
15
40.0
Cortinarius romagnesii
15
6
21
71.4 Entoloma dysthales
17
26
43
39.5
Psathyrella fatua
12
6
18
66.7 Inocybe amethystina
7
11
18
38.9
Entoloma strigosissimum
11
7
18
61.1 Cortinarius urbicus
18
29
47
38.3
Calocybe obscurissima
28
18
46
60.9 Pluteus luctuosus
11
20
31
36.5
3
2
5
60.0 Pluteus chrysophaeus
6
11
17
35.3
Hebeloma sordescens
15
11
26
57.7 Melanoleuca strictipes
7
14
21
35.0
Clitocybe squamulosa
6
5
11
54.5 Inocybe ochroalba
13
25
38
34.2
Entoloma lepidissimum
3
3
6
50.0 Conocybe utriformis
16
31
47
34
Psathyrella pseudocorrugis
4
4
8
50.0 Lyophyllum gangraenosum
15
30
45
33.3
Tephrocybe confusa
7
7
14
50.0 Psathyrella perpusilla
2
4
6
33.3
Hebeloma vaccinum
17
19
36
47.2 Tephrocybe striaepilea
6
13
19
31.6
Hebeloma marginatulum
7
8
15
46.7 Conocybe aporos
27
66
93
29.0
Psathyrella seymourensis
21
25
46
45.7 Pholiota flavida
2
5
7
28.6
5
6
11
45.5 Volvariella surrecta
10
26
36
27.8
Mycena rosea
15
18
33
45.5 Bolbitius reticulatus
14
44
58
24.1
Bolbitius pluteoides
19
23
42
44.2 Mycena capillaris
12
42
54
22.2
Russula nauseosa
10
13
23
43.5 Strobilurus esculentus
18
76
94
18.9
Entoloma lanuginosipes
3
4
7
Lepiota felina
6
8
14
42.9 Pterula multifida
11
5
16
68.8
Psathyrella panaeoloides
12
16
28
42.9 Skeletocutis nivea
48
86
134
35.8
Conocybe sordida
34
46
80
42.5 Ramaria abietina
23
35
58
39.7
Hebeloma bruchetii
8
11
19
42.1 Gasteromycetes
Inocybe similis
2
3
5
40.0 Hymenogaster populetorum
16
5
21
76.2
Inocybe tjallingiorum
2
3
5
40.0 Hymnogaster olivaceus
7
7
14
50.0
Melanoleuca luteolosperma
2
3
5
40.0 Hymenogaster arenarius
6
7
13
46.2
Inocybe pruinosa
Entoloma plebejum
42.9 Aphyllophorales
Fig. 12. Characteristic species in the province of Flevoland; species with at least four 5 x 5 km grid cells occupied in the Netherlands and significantly (χ2 test) correlated with the Flevoland region. Scientific names as used in NMV 2000 (a, b). [continued on next page].
56
Number of 5x5 km grid cells in which species occur
N
nd l ta To
%
4
5
9
44.4
5
11
16
31.3
Helvella confusa
5
1
6
83.3
Heyderia sclerotipes
7
2
9
77.8
12
7
19
63.2
Peziza arvernensis
6
4
10
60.0
Tuber puberulum
9
11
20
45.0
Tuber maculatum
19
29
48
39.6
d
lan
F
o lev
Hymenogaster vulgaris Bovista limosa
rla
e ed
Ascomycotina
Hypoxylon mammatum
Fig. 12 continued.
Fig. 13. The rare Polyporus tuberaster, an early colonizer in Flevoland, showing its enormous sclerotium. Photograph © P. Bremer.
Fig. 14. Bolbitius pluteoides, a characteristic species of the province of Flevoland (see Figure 12). Photograph © M. van der Molen.
57
References Bakker, D. (1957). Oostelijk Flevoland raakt begroeid. De Levende Natuur 60: 305 310. Bremer, P. (1980). The ferns of the Kuinderbos (The Netherlands), the establishment of 23 species in a planted forest. Acta Botanica Neerlandica 29 (5/6):351-357. Bremer, P. (1994). De betekenis van greppels voor de paddestoelflora I. proefvakken op keileem. Coolia 37: 9 -22. Bremer, P. ( 2003). Een halve eeuw bosontwikkeling in het Voorsterbos, Flevolands oudste bos. De Levende Natuur 104: 16 - 23. Bremer, P., Tjallingii, F., Veerkamp, M. & van Zanen, G. (1992). Paddestoelen in Flevoland. Natura 89(8): 186 - 189. Bremer, P., van Zanen, G. & van Breemen, G. (2000). Paddestoelen in de bossen van Spijk en Bremerberg: een toepassing van GIS. Coolia 43(1): 25-37. Daams, J. & de Vries, G.A. (1981). Truffels in de Flevopolders. Coolia 24(1): 1-7. Feekes, W. & Bakker, D. (1954). De ontwikkeling van de natuurlijke vegetatie in de Noordoostpolder. Van Zee tot Land nr. 6. Zwolle. Jans, L. & Drost, H. (1995). De Oostvaardersplassen. 25 jaar vegetatieonderzoek. Flevobericht nr. 382. Rijkswaterstaat, directie Flevoland. Jong, H. de. (1977). Experiences with the manmade meadow bird reserve `Kievitslanden` in Flevoland (The Netherlands). Biological Conservation 12(1): 13 - 31. Kjoller, R. & Bruns, T.D. (2003). Rhizopogon spore bank communities within and among California pine forests. Mycologia 95(4): 603 613. Laan, H.F. van der. (1978). Komt Stereum subtomentosum in ons land ook buiten de IJsselmeerpolders voor? Coolia 21(2): 33 - 35. Nederlandse Mycologische Vereniging (NMV), (2000a).Verspreidingsatlas. I. Agaricales
Nederlandse Mycologische Vereniging (NMV), (2000b). Verspreidingsatlas. II. Aphyllophorales, Phragmobasidiomycetidae, Gasteromycetes, Ascomycotina. Tjallingii, F. (1983). Notities uit de IJsselmeerpolders (2). Polyporus lentus = Polyporus tuberaster, of: de jacht op de knol. Coolia 26(3): 62 - 73. Tjallingii-Beukers, D. (1980). De Kopergroenzwammen Stropharia aeruginosa en S. cyanea. Coolia 23(1): 10 - 14. Tjallingii, F. & Tjallingii-Beukers, D. (1983). De IJsselmeerpolders, een paddestoelparadijs. Coolia 26: 121-129. Veerkamp, M.T. (1992). Paddestoelen in bosreservaten. Hinkeloord reports 4.Flevoland. Veerkamp, M.T. (2001). Paddestoelen in acht bosreservaten. Alterra-rapport 419. Vries, G. de. (2000). De Truffels van Flevoland. In: Zanen, C.G.N.van., P. Bremer & H. van der Aa (ed.). Paddestoelen in Flevoland: page 82 - 88. Vulink, T. (2002). Hungry Herds. Van Zee tot Land 66. Rijkswaterstaat. Thesis. Wildschut, J.H. (1992). De geschiedenis van het Staatsbosbeheer in de Noordoostpolder. Historisch onderzoek naar het beheer van bossen en natuurterreinen. Staatsbosbeheer/Flevoland. Zanen, C.G.N. van. (2000). Totaallijst van paddestoelsoorten gevonden in de provincie Flevoland in de periode 1975 t/m 1999. NMV, Werkgroep Mycologisch Onderzoek IJsselmeerpolders, 84 pp. Zanen, C.G.N. van. (2000). Successie. In: Zanen, C.G.N.van., P. Bremer & H. van der Aa (ed.) Paddestoelen in Flevoland. KNNV: 37 - 56 Zanen, C.G.N.van., Bremer, P. & H. van der Aa (ed.). (2000). Paddestoelen in Flevoland. KNNV.
58
Introduction
been planted on the polders and the changes to be expected. The mass planting of woods on mainly calcareous and pH-neutral to basic soils is unique in the Netherlands, so at the start of the survey it was difficult to predict what changes would take place. Moreover we expected that on a former sea floor a primary colonization by fungi would occur, with spores of most species arriving from outside the polders, whereas in most cases in the Netherlands a secondary colonisation has occurred with spores present in situ. Eight years after starting the inventory Tjallingii & Tjallingii-Beukers (1983) showed the importance of calcareous habitats in the polders and expected species
his paper looks at the mycota of the relatively new Dutch province of Flevoland, which is made up of three polders reclaimed from the sea since 1942. A working group of the Dutch Mycological Society (NMV), in which a number of amateur and professional mycologists collaborate, was set up in 1976 after the discovery of a large number of fruitbodies of Helvella acetabulum on one of the artificial grass-covered beaches (green shores) of Oostelijk Flevoland (see Figure 1). Questions were raised in relation to the composition of the young woods that had
T
Figure 1. The province of Flevoland with woodlands and green shores (
) .
*P. Bremer, Roelingsbeek 1, 8033 BM Zwolle [email protected]; ** G.C.N. van Zanen, De Breekstraat 36, 1024 LJ Amsterdam; *** M.T. Veerkamp, Pelikaanweg 54, 3985 RZ Werkhoven.
45
off the sea). After reclamation natural vegetation developed comprising marshes, reed-beds, willow carr and some silt-based grasslands (see Feekes & Bakker, 1954; Bakker, 1957; Jans & Drost, 1995), which were almost completely cultivated within 15 years. In Zuidelijk Flevoland 5900 ha of marshland and open water was not cultivated and is now protected as nature reserve (Oostvaardersplassen, see Figure 1). In the three polders more than 13,000 ha of woodlands were planted. This planting started in 1944 (at Voorsterbos) and the large scale planting ended in 1997. In the Noordoostpolder the woods were planted on nutrient-poor soil (peat, boulder clay, sand) but in the other two polders clay soils were singled out for planting. Nearly all the soils have a high lime content because of the millions of shellfish which died after the closure of the former Zuiderzee. To drain the polders, hundreds of km of trenches were dug in the oldest woods with densities up to 1 km per ha. On light clay soils the groundwater level can nevertheless be high in springtime. At various locations (under 5 % of the total area) seepage reaches the roots of the herb layer. Various tree and shrub species were planted, of which the most important being: Norway spruce Picea abies and Sitka spruce P. sitchensis on peaty and sandy soils, pines Pinus spp on sandy soils, pedunculate oak Quercus robur, sycamore Acer pseudoplatanus and ash Fraxinus excelsior on all soil types. Vast plantations of poplars Populus spp were planted in all the polders, especially on clay soils. Alder Alnus glutinosa was planted in combination with other species, due to its nitrogen-fixing capacity. Most species have been planted as a monoculture, but multi-species plantations can be found in nearly all larger woods as well. Approx. 270 ha of woodlands are natural and dominated by white willow Salix alba and are not exploited. Except for some forest reserves and two woodlands (Voorsterbos, Harderbos) all the stands are
from older natural woodlands to increase, e.g. species belonging to Cortinarius subg. Phlegmacium. It was expected that the number of species would be related to the age and the composition of the soil. A number of plots were monitored to assess this succession. Species associations were developing in Flevoland, reflecting the fact that various woodland types have their own characteristic mycoflora. Visiting the woodlands The working group aimed to survey the mycota of more than 70 woods and natural areas in Flevoland. Members of the working group visited the woodlands in spring and autumn. Mycological inventories were carried out at the plots, which can be recognised in the field by ditches bordering them. During 30 years there have been hundreds of visits. Since 1990 the inventory has been intensified by weekly visits to one or two areas. Some areas were visited systematically, others were sampled on an ad hoc basis. Mycologically interesting plots were visited more often than those which were poor in species on the first visit, causing bias (Bremer et al. 2000). Plots have been monitored as well (Bremer 1994, van Zanen 2000). Although most attention has been paid to woodlands, information has been collected from nature reserves, road verges, dikes and green shores as well. The area Four polders have been reclaimed since the closure of the Zuiderzee in 1932: Wieringermeerpolder (1933), Noordoostpolder (1942), Oostelijk Flevoland (1957) and Zuidelijk Flevoland (1968) (Figure 3 ). In this paper the oldest polder is excluded as it does not belong to the province of Flevoland. From about 1600 these polders were part of the sea floor covered by a layer of 1 - 4 m of brackish to salty water. This became fresh water after 1932 ( when the Zuiderzee was transformed to the IJsselmeer by the construction of a 32 km dyke cutting 46
ecological groups are all represented: ectomycorrhizal species, terrestrial saprotrophfic species, saprotrophic species on wood and parasites. The ectomycorrhizal species are chiefly associated with spruce, willow and poplar but also with oak and beech. The genera Inocybe, Hebeloma and Cortinarius are especially well represented. From each of the genera Russula and Lactarius there is only one ‘characteristic’ species and both are associated with spruce, namely Russula nauseosa and Lactarius deterrimus. The presence here of Tuber and Hymenogaster (compared to their absence elsewhere) may be explained by specialist recording at this site. The terrestrial saprotrophs are well represented with 28 species. They grow on needles (Helvella confusa, Calocybe obscurissima) and leaves (Mycena capillaris) or in humus-rich mull soils (Conocybe sordida). Other important genera are Entoloma, Psathyrella and Conocybe. Saprotrophic species on wood (e.g. eight species of Pluteus) are fewer. Two of the characteristic species are parasites: Heyderia sclerotipes and Volvariella surrecta. Species favouring acid sandy soils are generally under-represented in Flevoland. Amanita rubescens, A. citrina, Boletus badius and B. edulis for example are
used for commercial forestry, meaning that there is thinning on a five to eight year cycle. Clear felling has only taken place after infections or windthrow. Regeneration, especially of ash Fraxinus excelsior has occurred in 30 year old plantations following heavy thinning. Acer pseudoplatanus and Betula are also successful. At one of the woods (Kuinderbos, 1100 ha) 21 species of trees and shrubs had become established. Thinning has accelerated stand differentiation and the development of a varied vertical structure. In Oostelijk and Zuidelijk Flevoland various nature reserves were created, while in the latter the natural vegetation has been preserved in Oostvaardersplassen. This area is famous because of its breeding and migratory birds (Vulink, 2002). Artificial beaches have been created along the dikes over a distance of c. 31 km for recreational purposes. At the majority of these ‘green shores’ a natural grassland or sometimes even heather vegetation has developed without human interference. Half of these shores are used for recreation, the others have developed into nature areas.
The survey Characteristic species After 30 years of recording a small number of species are now known exclusively from Flevoland, occurring nowhere else in the Netherlands. Only one of these species (Tephrocybe ozes) occurs at several locations and 61 species can be categorised as ‘characteristic’ (Figure 12). These are the species that are significantly more common in Flevoland than in adjacent parts of the Netherlands. Calocybe obscurissima (28 locations, 61 % of sites in Flevoland, Figure 2), Pterula multifida (11 locations, 61 %) and Hymenogaster populetorum (16, 76 %) can be regarded as the most characteristic species. Most such species prefer calcareous sandy and/or clayey soils. The most important
Fig. 2. After 30 years of recording, distribution of Calocybe obscurissima is clearly concentrated in the area of Flevoland (highlighted in yellow).
47
could be found. After the first thinning the amount of dead wood increases enabling saprotrophic species to colonise the stands. Mycorrhizal fungi could be found at this stage as well, especially in plantations on boulder clay, sand and peat. On clay mycorrhizal fungi are rare in this and later stages of the plantation. Bremer et al. (2000) surveyed the mycorrhizal flora of some woods in Oostelijk-Flevoland. In the Hollandse Hout on a clay soil, 11 species of Inocybe were recorded, some of them associated with stands of Picea abies. Although poplars have been planted in great numbers on clay, Lactarius controversus has only been found near poplars growing on boulder clay or on road verges. Numerous hypogeous macrofungi such as Tuber maculatum and Tuber puberulum have been found in plantations of Italian poplar Populus x canadensis (Daams & de Vries 1981, de Vries 2000). Poplar stands are poor in species, with low densities of fruitbodies. Although white willow Salix alba has been planted, more attention has been paid to natural woods where Salix alba is the dominant species. In these spontaneous woods the herb layer is dominated by nettle Urtica dioica, with elder Sambucus nigra dominating the shrub layer. One plot in this habitat in the Oostvaardersplassen was monitored for eight years. Of the 113 species 58 % appeared to be wood-decomposing, 38 % humus-decomposing and 4 % mycorrhizal. Cortinarius urbicus (Fig. 7) was found almost every year. Four species of Hebeloma were less common. Pterula multifida and Ramaria abietina were growing in this plot, although they were not known before from this habitat in the Netherlands. Plantations dominated by Quercus robur on sandy, calcareous soil or boulder clay are rich in species with a high density of fruitbodies. Mycorrhizal species are common, such as Amanita phalloides, Laccaria amethystina and numerous species of Inocybe and Cortinarius subgenus Telamonia. The same holds for plantations on boulder clay. The combination
rare. The same holds for Scleroderma citrinum, although it has increased since 1990 indicating acidification of sandy soils low in shell content. In the Polyporaceae there is a group of early colonizing species such as Tyromyces (Oligoporus) spp., Trametes versicolor and Ganoderma lipsiense (= G. applanatum). Figure 4 presents a list of late colonising species. Until about 1986 Piptoporus betulinus was absent, although Betula spp. were rather common in the woods on sandy or peat soils. This species has increased markedly since 1990. Meripilus giganteus was only found for the first time about 50 years after the first planting. Taxonomic problems At the start of the survey there were a number of problem species that appeared to be new to the Netherlands. Van der Laan (1978) proved that Stereum subtomentosum had been misidentified as Stereum hirsutum. After the first finds it was shown to be common in the polders and in other parts of the Netherlands as mycologists became familiar with this species (Figure 5). Parallel stories apply to Scleroderma areolatum, Stropharia cyanea (Tjallingii-Beukers 1980) and Polyporus tuberaster (Tjallingii 1983)(Figure 13). The holotypes of some species were collected in Flevoland (e.g. Inocybe tjallingiorum, Inocybe amethystina, Psathyrella almerensis).
Habitats in Flevoland and their mycota Woodlands Immediately after planting, the luxurious original vegetation of common reed Phragmites australis, creeping thistle Cirsium arvense and great hairy willowherb Epilobium hirsutum was poor in macrofungi. Saprotrophs living on litter, such as Agrocybe pediades, Psathyrella spp. and Coprinus comatus were the most common. Within 7 12 years the canopy closed and other species 48
proved to be much poorer in mycorrhizal species, probably because of the drier habitat (Figure 6). Some types of stand are rather rare but can be mycologically important. Hornbeam Carpinus betulinus stands on boulder clay have only been planted at a few locations. At one of them hornbeam and ash are mixed and appeared to be very rich in species and fruitbodies. During 7 years 25 ectomycorrhizal species were found in a small plot, with on average 240 fruitbodies per 100 m2 per visit (Bremer 1994). In this plot grassland species such as Ramariopsis tenuiramosa, Clavulinopsis helvola and Geoglossum spp. were growing together with Amanita phalloides, Cortinarius obtusus, Leccinum griseum (= L. carpini = L. pseudoscabrum) and Lactarius circellatus. In summary we can state that the soil composition and tree layer have a dominant impact on the mycota in the mostly welldrained stands. Only at some locations has seepage had a dominant impact, with alder Alnus glutinosa becoming the prominent tree species. Here alder is accompanied by a number of mycorrhizal species such as Alnicola spp, Paxillus filamentosus, Gyrodon lividus and Lactarius lilacinus.
of Quercus robur and acid sand is confined to the Voorsterbos, where sand with a very low shell content was deposited. Here Russula amoenolens, R. ochroleuca and Scleroderma citrinum are common while Boletus parasiticus was found for the first time in the province. On clay, mycorrhiza-forming species are rare and the mycota is dominated by saprotrophic species such as Collybia dryophila and Rutstroemia firma. High densities of fruitbodies can also be found in plantations of Norway spruce and Sitka spruce. There is no herb layer in the dense stands. Here decomposer species such as Mycena spp, Micromphale perforans and Clitocybe ditopa play an important role and Helvella spp can be common. In some years Helvella elastica is dominant. Pterula multifida has been common, forming large groups. Other characteristic fungi of these stands are Heyderia abietis, Geastrum pectinatum, Russula queletii and R. nauseosa. Because of infections of Heterobasidion annosum and/or Ips graphicus (a beetle), the vitality of most stands has declined. In some stands on sandy soils poor in clay c. 70 % of the trees are infected with Heterobasidion annosum (data State Forestry Service). There is a thinning cycle of five years and clearfelling only takes place on patches less than 2-3 ha in size. Here the spruces are replaced by deciduous tree species. Spruce trees on clay soils have a better vitality but will be replaced as well. In one monitored plot of Norway spruce on clay 107 species were found within eight years, all of them saprotrophic except for Inocybe cincinnata (Figure 6). In stands of pines (almost confined to sandy soils), various characteristic species have been found including Lactarius deliciosus, Chroogomphus rutilus and Suillus luteus. Mycorrhizal species are rare under beech on clay soils, but are rather common in the similar stands on boulder clay or sandy soil. In one plot 144 species were found during eight years, 10% ectomycorrhizal, with Lactarius blennius, Russula fellea and R. mairei being most common. A plot on fine sand
Other habitats Green shores are found along the dikes at the east side of Oostelijk and Zuidelijk Flevoland (Figure 1). They vary in width from 50 m to 175 m and about 50% of these areas are used for recreation. These shores vary in altitude, mud content, texture and lime content (and concomitantly pH). Due to trampling and mowing grasslands dominate and show a gradient in species composition from the waterline to the dike. On some shores dunelike vegetation can change within a short distance to heather. Fungi characteristic of the Dutch dunes, such as Agaricus devoniensis, Psathyrella ammophila, Poronia erici and Inocybe vulpinella have been found. The shores can be rich in Hygrocybe, Entoloma and Geoglossum spp. Apart from grassland the shores are charac49
years. Lactarius, Russula and Cortinarius subg. Phlegmacium have also stabilised (although an increase was expected). Remarkably, the number of Inocybe spp. still shows a continuing increase after 22 years. The same holds for the number of hypogeous fungi. Tuber maculatum was the first species observed. Now 20 species are known, half of the total number of hypogeous species found in the Netherlands (de Vries 2000).
terised by solitary trees and shrubs, small woodlands and bonfire sites. More than 600 species have been found on these shores (van Zanen et al. 2000). Flevoland was the first area in the Netherlands where natural habitats were planned and created. So artificial marshes, areas for breeding waders (de Jong 1977), and also natural grasslands were created by digging and water management. The Oostvaardersplassen proved to be mycologically poor in species due to its clay soil. Most road verges are on clay soils. They are fully vegetated but are poor in mushrooms. On one of these verges at Zuidelijk Flevoland, Allopsalliota geesterani was found. Lactarius controversus colonised verges on sandy clay soils with poplar in the vicinity of the Kuinderbos. Some verges consist of sand rich in shells and are covered with an open grassland vegetation. Here Hygrocybe spp. and Entoloma incanum have been found in combination with e.g. purging flax Linum catharticum and eyebright Euphrasia stricta.
Dispersal Most fungi have a high capacity for dispersal. Spore length varies between 4 and 40 μm and is on average 7.9 μm (based on a sample of 313 spp. found in the Voorsterbos). We assume that nearly all species were transported by wind from nearby populations in the Netherlands or even surrounding countries. Young trees and shrubs were reared in tree nurseries in the polder, although in the older woods these came from nurseries outside Flevoland. In the Noordoostpolder various tree species were even grown from seed (Wildschut 1992). A number of species could have arrived in the rootballs but we think that most species came from outside the area by wind. Figure 10 depicts the nearest distance between localities in the Voorsterbos and possible source populations outside the polder (based on 313 species). The Voorsterbos is positioned at a small distance from woods on the ‘old land’, making it interesting for monitoring the colonisation of both fungi and woodland plant species (Bremer 2003). The majority of fungi found in the Voorsterbos have also been found nearby and all species are known from localities within a radius of 100 km. Figure 11 shows the corresponding data for a different set of species, the characteristic species listed in Figure 12. In this selected group more species had to cross a larger distance. More than 20 species had to cross at least 80 km, and in the case of Entoloma lilacinoroseum it might be more than 300 km.
The number of species Figure 8 depicts the increase in the total number of fungi since 1975. In 25 years more than 1540 taxa of macromycetes have been found (van Zanen 2000), 37% of all species found in the Netherlands. Within 15 years of starting the inventory, the annual increase of new species recorded has stabilised except in Z.-Flevoland. This polder was planted much later and the inventory started simultaneously with the planting of woodlands. Hence the increase of new species recorded here reflects both the speed of colonisation and mycological effort. In the Noordoostpolder and O.-Flevoland, most species have been present since 1975 and the increase chiefly reflects the effort of mycologists. Figure 9 depicts the increase in the number of species for various genera in all the woods involved. After the start the number of Helvella spp stabilised within four 50
are rather poor in fungi this will have only a restricted impact on the mycota as a whole. Ash and sycamore are the most successful species regenerating on clay soils while birch is the most successful on sandy soil. When no planting takes place after felling, these species will form the next generation. As ash and sycamore do not form ectomycorrhizal relationships, the abundance of mycorrhizal fungi could decline in all woods. In plantations of pedunculate oak and beech new species will appear, but as observed in the last 25 years species can decline or disappear as well. For instance Calocybe chrysenteron and Suillus collinitus have not been refound since 1980 and have probably disappeared. There is still an increase of species being recorded for the first time but, as Figure 8 shows, the rate of increase has declined and the total number of species has reached stability.
It is remarkable that such a high number of hypogeous macrofungi have been found in the young planted woods (De Vries, 2000). Hypogeous macrofungi are eaten by animals which ensure dispersal. They also form a spore-bank so transport by soil might take place as well (Kjoller & Bruns 2003).
The future As the plantations age the mycota will change although succession is difficult to assess without plots being monitored for decades. Plots have been monitored now for at most eight years. As Van Zanen (2000) pointed out, no succession has been assessed in this period, although he was able to indicate some kind of succession when species lists were available from numerous stands over a longer period of time. As stated before the area with spruce is declining. For phytopathological reasons these stands will be replaced, most of them within 15 years. With the felling of spruce the dependent mycota will almost disappear. In a number of stands no felling will take place, so the degradation of these stands can be studied. This will allow various characteristic species to survive for a longer time. Poplars will be replaced as well, but as these stands
Acknowledgements We thank David Mitchel for stimulating the writing of this paper and for his corrections to it and Dr. T. Kuyper for his comments.
Polder
Year
Area (ha)
Woods
Number of woods > 10 ha
% clay
Noordoostpolder
1941-1942
48000
1977
11
28
O.-Flevoland
1957
54000
5465
19
73
Z.-Flevoland
1968
43000
5649
15
95
145000
13091
40
Total
Fig. 3. Some characteristics of the polders forming a part of the province of Flevoland. Year = year of reclamation, Woods = area of woodlands (planted or spontaneous), % clay = percentage of woodlands situated on clay soils.
51
Late colonizing species (after 40 years)
Y
Species still absent but to be expected in the future
Early colonizing species (within 0-20 years)
Y
Intermediate colonizing species (21-40 years)
Y
Polyporus brumalis
10
Phellinus ferreus
21 Meripilus giganteus
Daedaleopsis confragosa
14
Oligoporus stipticus
23
Ganoderma lucidum
Bjerkandera fumosa
15
Heterobasidion annosum
25
Ganoderma pfeifferi
Inonotus radiatus
15
Oligoporus caesius
25
Ganoderma resinaceum
Polyporus varius
15
Phellinus robustus
25
Grifola frondosa
Trametes versicolor
15
Pycnoporus cinnabarinus
25
Phellinus igniarius
Bjerkandera adusta
17
Trametes hirsuta
25
Datronia mollis
17
Abortiporus biennis
26
Polyporus badius
17
Ischnoderma benzoinum
26
Polyporus tuberaster
17
Phaeolus schweinitzii
26
Fomitopsis pinicola
19
Phellinus conchatus
26
Ganoderma lipsiense
19
Trichaptum abietinum
27
Oligoporus subcaesius
19
Trametes suaveolens
29
Oligoporus tephroleucus
19
Trametes pubescens
33
Polyporus squamosus
19
Fomes fomentarius
37
Skeletocutis nivea
19
Laetiporus sulphureus
38
Daedalea quercina
20
Ganoderma australe
38
Hapalopilus rutilans
20
Piptoporus betulinus
38
Phellinus tuberculosus
20
Trametes gibbosa
20
50 Fistulina hepatica
Fig. 4. The colonization of Polyporaceae in Flevoland and the time in years (Y) until first appearance.
Species
Species look-alike
First year of Publication recognition
Stereum subtomentosum
Stereum hirsutum
1977
van der Laan (1978)
Stropharia cyanea
Stropharia aeruginosa
1980
Tjallingii-Beukers (1980)
Scleroderma areolatum
Scleroderma verrucosum
1980
Polyporus tuberaster
Polyporus spp.
1982
Steccherinum bourdotii
Steccherinum robustum
1985
Fig. 5. Species taxonomically unravelled during the study of the mycota in Flevoland.
52
Tjallingii (1983)
Site name
Tree species
Soil type
Area
Years
nV nA
nM %
References
Kuinderbos
Picea sitchensis
fine calcareous sand
150 1985-92
27 31
2
Kuinderbos
Fagus sylvatica
fine calcareous sand
150 1985-92
27 35
5 14.3 Bremer (2000)
Kuinderbos
Quercus robur
fine calcareous sand
150 1985-92
27 31
4 12.9 Bremer (2000)
Voorsterbos
Carpinus-Fraxinus boulder clay
70 1985-92
36 47
25 53.2 Bremer (1994)
Roggebotzand
Picea abies
clay
1000 1991-98
49 49
Revebos
Quercus robur
medium fine sand
1000 1991-98
Oostvaardersplassen
Salix alba (natural)
clay
Spijkbos (meerdijk)
6.5 Bremer (2000)
2.0
van Zanen (2000)
46 61
14 23.0
van Zanen (2000)
1000 1991-98
61 46
5 10.8
van Zanen (2000)
Populus, + various fine calcareous tree species sand
1000 1988-90
8 82
17 20.7
Veerkamp (1992)
Hollandse Hout
Populus, + various clay tree species
1000
19982000
8 64
6 9.4
Veerkamp (2001)
Houtribbos
Populus, + various sand with clay tree species
1000
19982000
8 46
11 23.9
Veerkamp (2001)
1
Fig. 6. Percentages of mycorrhizal species in plots of various stand types and one natural wood in Flevoland. nV = number of visits, nA = number of Agaricales, Boletales and Russulales, nM = number of ectomycorrhizal species, % = nM/nA x 100.
Fig. 7. Cortinarius urbicus, a species found almost every year under Salix alba in a plot in Oostvaardersplassen. Photograph © M. van der Molen.
53
Fig. 8. The total number of species (cumulative) recorded in the three reclaimed polders: Noordoostpolder (NOP), O.-Flevoland (OFL) and Z.-Flevoland (ZFl) and Flevoland as a region during 25 years.
Fig. 9. The total number of species recorded in Flevoland during 23 years, for five genera and the group of hypogeous fungi (after de Vries 2000). Within Cortinarius only the subgenus Phlegmacium has been worked out.
54
Percentage of species
Distance (in 10 km steps)
Percentage of characteristic species
Fig. 10. The distance between locations in the Voosterbos and the nearest known population for 313 species based on distribution data given in NMV (2000a,b).
Distance (in 10 km steps)
Fig. 11. The distance between locations in Flevoland and known sites outside Flevoland for the group of 61 characteristic species listed in Fig. 12, based on distribution data given in NMV (2000a,b).
55
Number of 5x5 km grid cells in which species occur d
an
e
l vo
Fl
la
Ne
r de
Number of 5x5 km grid cells in which species occur
nd l ta
To
Agaricales
d
d
lan
an
Pluteus insidiosus
r de
al
e
Ne
t To
2
3
5
40.0
Fl
%
l vo
%
Tephrocybe ozes
4
0
4
100 Tubaria confragosa
6
9
15
40.0
Cortinarius viscidulus
6
1
7
85.7 Lactarius deterrimus
6
9
15
40.0
Cortinarius romagnesii
15
6
21
71.4 Entoloma dysthales
17
26
43
39.5
Psathyrella fatua
12
6
18
66.7 Inocybe amethystina
7
11
18
38.9
Entoloma strigosissimum
11
7
18
61.1 Cortinarius urbicus
18
29
47
38.3
Calocybe obscurissima
28
18
46
60.9 Pluteus luctuosus
11
20
31
36.5
3
2
5
60.0 Pluteus chrysophaeus
6
11
17
35.3
Hebeloma sordescens
15
11
26
57.7 Melanoleuca strictipes
7
14
21
35.0
Clitocybe squamulosa
6
5
11
54.5 Inocybe ochroalba
13
25
38
34.2
Entoloma lepidissimum
3
3
6
50.0 Conocybe utriformis
16
31
47
34
Psathyrella pseudocorrugis
4
4
8
50.0 Lyophyllum gangraenosum
15
30
45
33.3
Tephrocybe confusa
7
7
14
50.0 Psathyrella perpusilla
2
4
6
33.3
Hebeloma vaccinum
17
19
36
47.2 Tephrocybe striaepilea
6
13
19
31.6
Hebeloma marginatulum
7
8
15
46.7 Conocybe aporos
27
66
93
29.0
Psathyrella seymourensis
21
25
46
45.7 Pholiota flavida
2
5
7
28.6
5
6
11
45.5 Volvariella surrecta
10
26
36
27.8
Mycena rosea
15
18
33
45.5 Bolbitius reticulatus
14
44
58
24.1
Bolbitius pluteoides
19
23
42
44.2 Mycena capillaris
12
42
54
22.2
Russula nauseosa
10
13
23
43.5 Strobilurus esculentus
18
76
94
18.9
Entoloma lanuginosipes
3
4
7
Lepiota felina
6
8
14
42.9 Pterula multifida
11
5
16
68.8
Psathyrella panaeoloides
12
16
28
42.9 Skeletocutis nivea
48
86
134
35.8
Conocybe sordida
34
46
80
42.5 Ramaria abietina
23
35
58
39.7
Hebeloma bruchetii
8
11
19
42.1 Gasteromycetes
Inocybe similis
2
3
5
40.0 Hymenogaster populetorum
16
5
21
76.2
Inocybe tjallingiorum
2
3
5
40.0 Hymnogaster olivaceus
7
7
14
50.0
Melanoleuca luteolosperma
2
3
5
40.0 Hymenogaster arenarius
6
7
13
46.2
Inocybe pruinosa
Entoloma plebejum
42.9 Aphyllophorales
Fig. 12. Characteristic species in the province of Flevoland; species with at least four 5 x 5 km grid cells occupied in the Netherlands and significantly (χ2 test) correlated with the Flevoland region. Scientific names as used in NMV 2000 (a, b). [continued on next page].
56
Number of 5x5 km grid cells in which species occur
N
nd l ta To
%
4
5
9
44.4
5
11
16
31.3
Helvella confusa
5
1
6
83.3
Heyderia sclerotipes
7
2
9
77.8
12
7
19
63.2
Peziza arvernensis
6
4
10
60.0
Tuber puberulum
9
11
20
45.0
Tuber maculatum
19
29
48
39.6
d
lan
F
o lev
Hymenogaster vulgaris Bovista limosa
rla
e ed
Ascomycotina
Hypoxylon mammatum
Fig. 12 continued.
Fig. 13. The rare Polyporus tuberaster, an early colonizer in Flevoland, showing its enormous sclerotium. Photograph © P. Bremer.
Fig. 14. Bolbitius pluteoides, a characteristic species of the province of Flevoland (see Figure 12). Photograph © M. van der Molen.
57
References Bakker, D. (1957). Oostelijk Flevoland raakt begroeid. De Levende Natuur 60: 305 310. Bremer, P. (1980). The ferns of the Kuinderbos (The Netherlands), the establishment of 23 species in a planted forest. Acta Botanica Neerlandica 29 (5/6):351-357. Bremer, P. (1994). De betekenis van greppels voor de paddestoelflora I. proefvakken op keileem. Coolia 37: 9 -22. Bremer, P. ( 2003). Een halve eeuw bosontwikkeling in het Voorsterbos, Flevolands oudste bos. De Levende Natuur 104: 16 - 23. Bremer, P., Tjallingii, F., Veerkamp, M. & van Zanen, G. (1992). Paddestoelen in Flevoland. Natura 89(8): 186 - 189. Bremer, P., van Zanen, G. & van Breemen, G. (2000). Paddestoelen in de bossen van Spijk en Bremerberg: een toepassing van GIS. Coolia 43(1): 25-37. Daams, J. & de Vries, G.A. (1981). Truffels in de Flevopolders. Coolia 24(1): 1-7. Feekes, W. & Bakker, D. (1954). De ontwikkeling van de natuurlijke vegetatie in de Noordoostpolder. Van Zee tot Land nr. 6. Zwolle. Jans, L. & Drost, H. (1995). De Oostvaardersplassen. 25 jaar vegetatieonderzoek. Flevobericht nr. 382. Rijkswaterstaat, directie Flevoland. Jong, H. de. (1977). Experiences with the manmade meadow bird reserve `Kievitslanden` in Flevoland (The Netherlands). Biological Conservation 12(1): 13 - 31. Kjoller, R. & Bruns, T.D. (2003). Rhizopogon spore bank communities within and among California pine forests. Mycologia 95(4): 603 613. Laan, H.F. van der. (1978). Komt Stereum subtomentosum in ons land ook buiten de IJsselmeerpolders voor? Coolia 21(2): 33 - 35. Nederlandse Mycologische Vereniging (NMV), (2000a).Verspreidingsatlas. I. Agaricales
Nederlandse Mycologische Vereniging (NMV), (2000b). Verspreidingsatlas. II. Aphyllophorales, Phragmobasidiomycetidae, Gasteromycetes, Ascomycotina. Tjallingii, F. (1983). Notities uit de IJsselmeerpolders (2). Polyporus lentus = Polyporus tuberaster, of: de jacht op de knol. Coolia 26(3): 62 - 73. Tjallingii-Beukers, D. (1980). De Kopergroenzwammen Stropharia aeruginosa en S. cyanea. Coolia 23(1): 10 - 14. Tjallingii, F. & Tjallingii-Beukers, D. (1983). De IJsselmeerpolders, een paddestoelparadijs. Coolia 26: 121-129. Veerkamp, M.T. (1992). Paddestoelen in bosreservaten. Hinkeloord reports 4.Flevoland. Veerkamp, M.T. (2001). Paddestoelen in acht bosreservaten. Alterra-rapport 419. Vries, G. de. (2000). De Truffels van Flevoland. In: Zanen, C.G.N.van., P. Bremer & H. van der Aa (ed.). Paddestoelen in Flevoland: page 82 - 88. Vulink, T. (2002). Hungry Herds. Van Zee tot Land 66. Rijkswaterstaat. Thesis. Wildschut, J.H. (1992). De geschiedenis van het Staatsbosbeheer in de Noordoostpolder. Historisch onderzoek naar het beheer van bossen en natuurterreinen. Staatsbosbeheer/Flevoland. Zanen, C.G.N. van. (2000). Totaallijst van paddestoelsoorten gevonden in de provincie Flevoland in de periode 1975 t/m 1999. NMV, Werkgroep Mycologisch Onderzoek IJsselmeerpolders, 84 pp. Zanen, C.G.N. van. (2000). Successie. In: Zanen, C.G.N.van., P. Bremer & H. van der Aa (ed.) Paddestoelen in Flevoland. KNNV: 37 - 56 Zanen, C.G.N.van., Bremer, P. & H. van der Aa (ed.). (2000). Paddestoelen in Flevoland. KNNV.
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