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Studies on the mycorrhizal community infecting trees in the Liphook forest fumigation experiment
Agriculture, Ecosystems and Environment, 47 ( 1993) 185-191 Elsevier Science Publishers B.V., Amsterdam
185
Studies on the mycorrhizal community infecting trees in the Liphook Forest fumigation experiment P.J.A. Shaw*,", J. Dighton b, J. Posldttb "National Power, Kelvin Avenue, LeatherheadKT22 7SE, UK bITE Merlewood, Grange-over-Sands, Cumbria LA 11 6JU, UK
Abstract
The mycorrhizal community in a long-term outdoor fumigation experiment was studied by counthag both fruitbodies and below-ground mycorrhizas. The fruitbody populations under Scots pine showed annual successional changes which were not paralleled below ground. The trend below ground was for a continuing increase in species number with stand age. No clear effects above or below ground were attributable to fumigation treatments, but the fruitbodies of Paxillus involutus tended to occur in greater numbers in SO2 treated plots. By contrast, below ground the mycorrhizas of this species were slightly adversely affected by SO2 fumigation.
Introduction The Liphook Forest fumigation experiment was established in 1985 to investigate the long-term effects of realistic concentrations of SO2 and 03 on coniferous forest ecosystems in the UK. One major line of work entails studying the responses of the mycorrhizal community to pollution stress, since under field conditions these fungi are crucial for the transfer of minerals from the soil solution to tree roots (Harley and Smith, 1983 ). The effects of acid precipitation and gaseous pollutants have been shown to reduce root growth and mycorrhizal development. Indirect effects of pollutants in reducing photosynthesis, and hence carbon allocation, to the root system may also inhibit mycorrhizal development. The effects of these have recently been reviewed by Dighton and Jansen (1990). The work described below involved both counting fruiting bodies each autumn and taking root samples to identify mycorrhizal morphotypes. The results presented here cover root harvests from 1985 to 1988, and fruitbody surveys from 1985 to 1989. *Corresponding author: Department of Environmental Science, Southlands College, Wimbledon Parkside, London SWI9 5NN, UK.
© 1993 Elsevier Science Publishers B.V. All fights reserved 016%8809/93/$06.00
186
P.J.4. Shaw et aL /Agriculture, Ecosystems and Environment 47 (1993) 185-191
Methods
Site description The experimental plots are located in Liphook Forest on the Sussex/ Hampshire border (grid ref. SU854298). The experimental area is on a 1:30 NNW facing slope where the soil was a humoferdc podsol of the Shirrel Heath series (Jarvis et al., 1984). Soil pH (distilled water) was approximately 4.1 in the organic layer and 4.0 in the bleached horizon. The area was accidentally burnt in 1976, and replanted with Corsican pine (Pinus nigra maritima) in 1982. In 1985 seven areas were cleared of vegetation and rotovated to a depth of 15 era, the iron pan was then broken by deep tining. These areas became the seven experimental plots. Each plot consisted of a circle, 50 m in diameter, surrounded by gas release pipework. Gas was released at two heights to maintain a constant concentration across the width of an inner circle 30 m in diameter (McLeod et al., 1992). Seedlings of Scots pine, Sitka spruce and Norway spruce ( 196 per species per plot) were planted in April 1985 in the inner circles at 1 m spacing. The trees were planted in six sectors, with the two sectors of each species being diametrically opposite. Harvesting has since removed eight plants per species per plot (four per sector) annually. The experimental design was an unreplicated factorial combination of two O3 treatments and three SO2 treatments, with an extra control making up the seven plots. 03 treatments consisted of an ambient and a 'high' concentration, the latter being 1.5 times the ambient O3 level. Continuous automatic monitoring allowed the 03 target to be updated twice per hour. 03 fumigation started in March 1988, but until December 1988 it was contaminated with N205 (Brown and Roberts, 1988). Subsequently, a water scrubber was installed to control this problem. The SO2 treatments were based on a 2 year dataset collected from Bottesford, a rural town in the English Midlands (Martin and Barber, 1981 ). This dataset contains half-hourly means throughout the year for SO2 and other gases, and was used to set corresponding half-hourly targets at Liphook. The 'low' SO2 treatment was 1.5 times the Bottesford data, while the 'high' treatment was 3 times this data. The annual means for ambient, low and high SO2 plots are approximately 4 p.p.b., 14 p.p.b, and 24 p.p.b., respectively. SO2 fumigation commenced in May 1987 and has continued approximately uninterrupted since.
Root surveys Following an annual harvest of trees for biometric analysis, the root systems of each cut plant were sampled for analysis of mycorrhizal morphotypes. In 1985 the whole root system was sampled, but in subsequent years this
P.J.A. Shaw et al. /Agriculture, Ecosystems and Environment 47 (1993) 185-191
18 7
proved impractical and instead roots were collected from a hole, 10 cm X 10 cm X 15 cm deep, 15 cm west of the cut stump. Roots were washed, fixed in 1.2% glutaraldehyde, and morphotypes defined by comparison with a reference collection maintained at ITE Medewood. Subsequently, mycorrhizas synthesised under pure culture conditions were compared with the reference samples, allowing a few types to be identified to species.
Fruitbody surveys Each plot was checked at intervals of approximately 2 weeks from late August to November, and any fruitbodies found were recorded and marked (with white paint unless the cap was too viscid, in which case it was sliced with a scalpel). Most fungi were identified on the spot but doubtful specimens were returned to the laboratory for detailed examination. The diffuse crustose hymenium of Thelephora terrestris was noted but could not be quantified owing to its growth habit. Results
Mycorrhizal morphotypes Up to the 1988 harvest, 11 types had been distinguished on Sitka spruce, 13 on Norway spruce and 14 on Scots pine. Only three types (all on Scots pine) have yet been identified to genus. There were no significant treatment effects on any morphotype, and little change from year to year except for the appearance of some minor types in 1987 and 1988. When the data were ordinated with principal components analysis (PCA), no trends emerged for Norway spruce or Sitka spruce, but for Scots pine the score on the first principal axis reflected the SO2 treatment (Fig. 1 ). The associated eigenvector had positive loaclings for the Paxillus, Cenococcum and Suillus morphs. There is no significance test for eigenvector elements, but the largest loading is that of Paxillus, suggesting that it is associated with non-SO2 plots. However, there was no clear trend and ANOVA showed no significant effects.
Fruitbody surveys No fruitbodies were found during 1985, reflecting the immaturity of the trees. In 1986, Laccaria laccata, Paxillus involutus and Thelephora terrestris emerged in all plots and under all tree species. From 1987 onwards, almost all fruitbody production occurred under the Scots pines, and the subsequent data analyses refer solely to the pine sectors. The initial community reappeared along with Suillus bovinus and Gomphidius roseus (often in mixed clumps). This pattern was repeated in 1988, with the addition of significant
18 8 F i r
P.J.A. Shaw et aL / Agriculture, Ecosystems and Environment 47 (1993) 185-191
t.0 0.8. 0.6
p 0.4 r i 0.2. n c 0.0 i p -0.2 -0.4 a -0,~
-0.8 s -1 . O 1 A
2 H
3 L
4 A
5 H
b L
7 A
PLOT S02
Fig. 1. Plot mean scores for the first principal component of the morphotype data for the period 1985-1988. Gas treatments are abbreviated as follows: A, ambient; L, low; H, high. Table 1 Counts of ectomycorrhizal fruitbodies in the Scots pine sectors of the Liphook plots for the period 1986-1989. Results from all plots have been pooled Fungal species
Paxillus involutus La~caria laccata
Suillus bovinus Gomphidius roseus Suillus variegatus Boletus subtomentosus Suillus luteus
Year 1986
1987
1988
1989
117 567 0 0 0
132 2765 219 99 2
20 3868 2982 431 151
21 182 5823 896 534
0 0
7 0
18 4
17 12
numbers of Suillus variegatus, Suillus luteus and Boletus subtomentosus. In 1989, Suillus species were the dominant fruitbodies. The results for the pine sectors of all plots (pooled) are given in Table 1. There were no significant effects of treatment on any one species. When the data were ordinated by PCA the first axis again appeared to show an SO2 effect (Fig. 2). The plot means resemble those for the morphotype PCA (Fig. 1 ), but now the eigenvector loads show P. involutus to have a negative loading, i.e. it fruited preferentiaUy in SO2-treated plots (Fig. 3). Again, ANOVA found the relationship between this fungus and SO2 to be non-significant. No relationship was found between fruitbody emergence and morphotype distribution, although frultbody appearance has often been assumed to act as an indicator of belowground species distribution on roots. A similar discrepancy has been found in birch stands where the mycorrhizas on roots did not correspond to the emergent fruitbodies (Dighton et al., 1990).
P.J.A. Shaw et al. / Agriculture, Ecosystems and Environment 47(1993) 185-191 F i r s f
189
3.
2
P i
I
n C i p
O,
a
-1.
x I
$ -2. I A
2 H
3 L
4 R
5 H
b L
7 A
PLOT S02
Fig. 2. Plot mean scores for the first principal component of the fruitbody data for the period 1985-1988. Gas treatments are abbreviated as follows: A, ambient; L, low; H, high. Species
•
Gomphid ius roseus
O. 2 4 4
Laccar ia laccata
-0.028
Paxillus involutus
l
-0.318
so,,,o,bo,iou,
l
O. 358
so,,,us
l
0.483 0.400
sp
l
Boletus subtomentosus
. . . . . -1,0
-0.8
-O,E
,
,
-O 4
-O 2
O. 45q
I
0.18q i
,
,
O.O
Eigenvector load inll
Fig. 3. Eigenvector loadings for the first principal component of the fruitbody data for the period 1985-1988.
Discussion The overriding trend in the fruitbody data is a change from a community dominated by Laccaria laccata, P. involutus and T. terrestris (all ubiquitous in the Northern Hemisphere) to a mixed community of 'early stage' fungi (Last et al., 1987). The occurrence of a succession of mycorrhizal species fruiting as a host tree matures is a well-known phenomenon (Marks and Foster, 1967; Mason et al., 1983; Last et al., 1984; Dighton et al., 1986), although comprehensive lists are not yet available for any tree species. The majority of studies have in-
190
P.Z A. Shaw et aL /Agriculture, Ecosystems and Environment 47 (1993) 185-191
volved visiting stands of widely differing ages on soils that are assumed to be reasonably similar, and the work presented above is unusual in being based on annual surveys of the same site. Richardson (1970) found that pine forests should be visited at intervals of 3-5 days to be confident of recording all toadstools. This and the density of the foliage from 1988 onwards means that the fruitbody counts from Liphook cannot be regarded as absolute, but they provide a useful index of the sporocarp population. The absence of a clear pollutant effect on this process agrees with the observations of Termorshuizen and Shaffers (1987) that under Scots pine in the Netherlands, mycorrhizal fruitbodies were depressed by air pollution in mature stands (50 years) but not in young stands (5-13 years). The first principal axis of the PCA on the Liphook carpophore data picked up its major trend, namely the succession away from nursery species (which had negative eigenvector loadings; Fig. 3 ). It also appeared to show a trend for SO2 to slow this succession down, and although the SO2 effect was not significant for any species, P. involutus fruited in the largest numbers in SO2-treated plots. The work at Liphook is unique in complementing the fruitbody surveys with annual monitoring of mycorrhizal infections on the tree roots. There was no clear change in morphotype composition corresponding to the fruitbody succession, implying that the changes in fruitbody emergence are due to physiological changes in the mycorrhizal symbiosis. The ordination of the Scots pine morphotype data shows a tentative effect due to SO2 and suggests a negative effect of SO2 on the P. involutus morph. This agrees with the observations of Dighton and Skeffington (1987) that acidic irrigation decreased the number of root tips of Scots pine with a brown coralloid morph ('Type F' ), later identified as P. involutus. Termorshuizen and Shaffers (1989) also noted that coralloid mycorrhizas were significantly negatively related to SO2 concentrations in the Netherlands, but did not identify their morphs to species. It is, however, hard to reconcile this decrease in P. involutus below ground with the increase in its fruitbodies found in the SO2-treated plots. It is hoped that further research will solve this apparent paradox.
Acknowledgements We thank M.R. Holland for assistance during field sampling and A.R. McLeod for discussions. This work is published with the permission of National Power plc. The Liphook project now forms part of the Joint Environmental Programme of National Power plc and Powergen plc. Financial support was received from the commission of the European Communities for part of this study.
P.J.A. Shaw et al. /Agriculture, Ecosystemsand Environment 47 (I 993) 185-191
191
References Brown, K.A. and Roberts, T.M., 1988. Effects of ozone on foliar leaching in Norway spruce (Picea abies L. Karst): confounding effects due to N205 production during ozone generation. Environ. PoUut., 55: 55-73. Dighton, J. and Jansen, A.E., 1990. Atmospheric pollutants and ectomycorrhizas, more questions than answers. Environ. Pollut. Dighton, J. and Skeffington, R.A., 1987. Effects of artificial acid precipitation on the ectomycorrhizae of Scots pine seedlings. New Phytol., 107: 191-202. Dighton, J., Poskitt, J.M. and Howard, D.M., 1986. Changes in the occurrence ofbasidiomycete fruitbodies during forest stand development with specific reference to mycorrhizal species. Trans. Br. Mycol. Soc., 87: 163-171. Dighton, J., Mason, P.A. and Poskitt, J., 1990. Field use of 32p to measure phosphate uptake by birch mycorrhiza. New Phytol., 116: 655-661. Harley, J.L. and Smith, S.E., 1983. Mycorrhizal Symbiosis. Academic Press, London. Jarvis, M.G., Allen, R.H., Fordham, F.J., Hazelden, J., Moffat, A.J. and Sturdy, R.G., 1984. Soils and their use in South East England. Bull 15, Soil Survey of England and Wales, Harpenden, UK. Last, F.T., Mason, P.A., Ingleby, K. and Fleming, L.V., 1984. Succession of fruitbodies of sheathing mycorrhizal fungi associated with Betula pendula. For. Ecol. Manage., 9: 229-234. Last, F.T., Dighton, J. and Mason, P.A., 1987. Successions of sheathing mycorrhizal fungi. Trends Ecol. Evol., 2: 157-161. Marks, G.C. and Forster, R.C., 1967. Succession of mycorrhizal associations on individual roots of radiata pine. Aust. For., 31: 193. Martin, A. and Barber, F.R., 1981. Sulphur dioxide, oxides of nitrogen and ozone measured continuously for two years at a rural site. Atmos. Environ., 15: 567-578. Mason, P.A., Wilson, J., Last, F.T. and Walker, C., 1983. The concept of succession in relation to the spread of sheathing mycorrhizal fungi on inoculated tree seedlings growing in unsterile soil. Plant Soil, 71: 247-256. McLeod, A.R., Shaw, P.J.A. and Holland, M.R., 1992. The Liphook forest fumigation project: Studies of the sulphur dioxide and ozone effects on coniferous trees. For. Ecol. Manage., 51: 121-127. Richardson, M.J., 1970. Studies on Russula emetica and other agarics in a Scots pine plantation. Trans. Br. Mycol. Soc., 55:217-229. Termorshuizen, A.J. and Schaffers, A.P., 1987. Occurrence of carpophores of ectomycorrhizal fungi in selected stands ofPinus sylvestris in the Netherlands in relation to stand vitality and air pollution. Plant Soil, 104:209-217. Termorshuizen, A.J. and Schaffers, A.P., 1989. The relation in the field between fruitbodies of mycorrhizal fungi and their mycorrhizas. Agric. Ecosyst. Environ., 28:509-512.
185
Studies on the mycorrhizal community infecting trees in the Liphook Forest fumigation experiment P.J.A. Shaw*,", J. Dighton b, J. Posldttb "National Power, Kelvin Avenue, LeatherheadKT22 7SE, UK bITE Merlewood, Grange-over-Sands, Cumbria LA 11 6JU, UK
Abstract
The mycorrhizal community in a long-term outdoor fumigation experiment was studied by counthag both fruitbodies and below-ground mycorrhizas. The fruitbody populations under Scots pine showed annual successional changes which were not paralleled below ground. The trend below ground was for a continuing increase in species number with stand age. No clear effects above or below ground were attributable to fumigation treatments, but the fruitbodies of Paxillus involutus tended to occur in greater numbers in SO2 treated plots. By contrast, below ground the mycorrhizas of this species were slightly adversely affected by SO2 fumigation.
Introduction The Liphook Forest fumigation experiment was established in 1985 to investigate the long-term effects of realistic concentrations of SO2 and 03 on coniferous forest ecosystems in the UK. One major line of work entails studying the responses of the mycorrhizal community to pollution stress, since under field conditions these fungi are crucial for the transfer of minerals from the soil solution to tree roots (Harley and Smith, 1983 ). The effects of acid precipitation and gaseous pollutants have been shown to reduce root growth and mycorrhizal development. Indirect effects of pollutants in reducing photosynthesis, and hence carbon allocation, to the root system may also inhibit mycorrhizal development. The effects of these have recently been reviewed by Dighton and Jansen (1990). The work described below involved both counting fruiting bodies each autumn and taking root samples to identify mycorrhizal morphotypes. The results presented here cover root harvests from 1985 to 1988, and fruitbody surveys from 1985 to 1989. *Corresponding author: Department of Environmental Science, Southlands College, Wimbledon Parkside, London SWI9 5NN, UK.
© 1993 Elsevier Science Publishers B.V. All fights reserved 016%8809/93/$06.00
186
P.J.4. Shaw et aL /Agriculture, Ecosystems and Environment 47 (1993) 185-191
Methods
Site description The experimental plots are located in Liphook Forest on the Sussex/ Hampshire border (grid ref. SU854298). The experimental area is on a 1:30 NNW facing slope where the soil was a humoferdc podsol of the Shirrel Heath series (Jarvis et al., 1984). Soil pH (distilled water) was approximately 4.1 in the organic layer and 4.0 in the bleached horizon. The area was accidentally burnt in 1976, and replanted with Corsican pine (Pinus nigra maritima) in 1982. In 1985 seven areas were cleared of vegetation and rotovated to a depth of 15 era, the iron pan was then broken by deep tining. These areas became the seven experimental plots. Each plot consisted of a circle, 50 m in diameter, surrounded by gas release pipework. Gas was released at two heights to maintain a constant concentration across the width of an inner circle 30 m in diameter (McLeod et al., 1992). Seedlings of Scots pine, Sitka spruce and Norway spruce ( 196 per species per plot) were planted in April 1985 in the inner circles at 1 m spacing. The trees were planted in six sectors, with the two sectors of each species being diametrically opposite. Harvesting has since removed eight plants per species per plot (four per sector) annually. The experimental design was an unreplicated factorial combination of two O3 treatments and three SO2 treatments, with an extra control making up the seven plots. 03 treatments consisted of an ambient and a 'high' concentration, the latter being 1.5 times the ambient O3 level. Continuous automatic monitoring allowed the 03 target to be updated twice per hour. 03 fumigation started in March 1988, but until December 1988 it was contaminated with N205 (Brown and Roberts, 1988). Subsequently, a water scrubber was installed to control this problem. The SO2 treatments were based on a 2 year dataset collected from Bottesford, a rural town in the English Midlands (Martin and Barber, 1981 ). This dataset contains half-hourly means throughout the year for SO2 and other gases, and was used to set corresponding half-hourly targets at Liphook. The 'low' SO2 treatment was 1.5 times the Bottesford data, while the 'high' treatment was 3 times this data. The annual means for ambient, low and high SO2 plots are approximately 4 p.p.b., 14 p.p.b, and 24 p.p.b., respectively. SO2 fumigation commenced in May 1987 and has continued approximately uninterrupted since.
Root surveys Following an annual harvest of trees for biometric analysis, the root systems of each cut plant were sampled for analysis of mycorrhizal morphotypes. In 1985 the whole root system was sampled, but in subsequent years this
P.J.A. Shaw et al. /Agriculture, Ecosystems and Environment 47 (1993) 185-191
18 7
proved impractical and instead roots were collected from a hole, 10 cm X 10 cm X 15 cm deep, 15 cm west of the cut stump. Roots were washed, fixed in 1.2% glutaraldehyde, and morphotypes defined by comparison with a reference collection maintained at ITE Medewood. Subsequently, mycorrhizas synthesised under pure culture conditions were compared with the reference samples, allowing a few types to be identified to species.
Fruitbody surveys Each plot was checked at intervals of approximately 2 weeks from late August to November, and any fruitbodies found were recorded and marked (with white paint unless the cap was too viscid, in which case it was sliced with a scalpel). Most fungi were identified on the spot but doubtful specimens were returned to the laboratory for detailed examination. The diffuse crustose hymenium of Thelephora terrestris was noted but could not be quantified owing to its growth habit. Results
Mycorrhizal morphotypes Up to the 1988 harvest, 11 types had been distinguished on Sitka spruce, 13 on Norway spruce and 14 on Scots pine. Only three types (all on Scots pine) have yet been identified to genus. There were no significant treatment effects on any morphotype, and little change from year to year except for the appearance of some minor types in 1987 and 1988. When the data were ordinated with principal components analysis (PCA), no trends emerged for Norway spruce or Sitka spruce, but for Scots pine the score on the first principal axis reflected the SO2 treatment (Fig. 1 ). The associated eigenvector had positive loaclings for the Paxillus, Cenococcum and Suillus morphs. There is no significance test for eigenvector elements, but the largest loading is that of Paxillus, suggesting that it is associated with non-SO2 plots. However, there was no clear trend and ANOVA showed no significant effects.
Fruitbody surveys No fruitbodies were found during 1985, reflecting the immaturity of the trees. In 1986, Laccaria laccata, Paxillus involutus and Thelephora terrestris emerged in all plots and under all tree species. From 1987 onwards, almost all fruitbody production occurred under the Scots pines, and the subsequent data analyses refer solely to the pine sectors. The initial community reappeared along with Suillus bovinus and Gomphidius roseus (often in mixed clumps). This pattern was repeated in 1988, with the addition of significant
18 8 F i r
P.J.A. Shaw et aL / Agriculture, Ecosystems and Environment 47 (1993) 185-191
t.0 0.8. 0.6
p 0.4 r i 0.2. n c 0.0 i p -0.2 -0.4 a -0,~
-0.8 s -1 . O 1 A
2 H
3 L
4 A
5 H
b L
7 A
PLOT S02
Fig. 1. Plot mean scores for the first principal component of the morphotype data for the period 1985-1988. Gas treatments are abbreviated as follows: A, ambient; L, low; H, high. Table 1 Counts of ectomycorrhizal fruitbodies in the Scots pine sectors of the Liphook plots for the period 1986-1989. Results from all plots have been pooled Fungal species
Paxillus involutus La~caria laccata
Suillus bovinus Gomphidius roseus Suillus variegatus Boletus subtomentosus Suillus luteus
Year 1986
1987
1988
1989
117 567 0 0 0
132 2765 219 99 2
20 3868 2982 431 151
21 182 5823 896 534
0 0
7 0
18 4
17 12
numbers of Suillus variegatus, Suillus luteus and Boletus subtomentosus. In 1989, Suillus species were the dominant fruitbodies. The results for the pine sectors of all plots (pooled) are given in Table 1. There were no significant effects of treatment on any one species. When the data were ordinated by PCA the first axis again appeared to show an SO2 effect (Fig. 2). The plot means resemble those for the morphotype PCA (Fig. 1 ), but now the eigenvector loads show P. involutus to have a negative loading, i.e. it fruited preferentiaUy in SO2-treated plots (Fig. 3). Again, ANOVA found the relationship between this fungus and SO2 to be non-significant. No relationship was found between fruitbody emergence and morphotype distribution, although frultbody appearance has often been assumed to act as an indicator of belowground species distribution on roots. A similar discrepancy has been found in birch stands where the mycorrhizas on roots did not correspond to the emergent fruitbodies (Dighton et al., 1990).
P.J.A. Shaw et al. / Agriculture, Ecosystems and Environment 47(1993) 185-191 F i r s f
189
3.
2
P i
I
n C i p
O,
a
-1.
x I
$ -2. I A
2 H
3 L
4 R
5 H
b L
7 A
PLOT S02
Fig. 2. Plot mean scores for the first principal component of the fruitbody data for the period 1985-1988. Gas treatments are abbreviated as follows: A, ambient; L, low; H, high. Species
•
Gomphid ius roseus
O. 2 4 4
Laccar ia laccata
-0.028
Paxillus involutus
l
-0.318
so,,,o,bo,iou,
l
O. 358
so,,,us
l
0.483 0.400
sp
l
Boletus subtomentosus
. . . . . -1,0
-0.8
-O,E
,
,
-O 4
-O 2
O. 45q
I
0.18q i
,
,
O.O
Eigenvector load inll
Fig. 3. Eigenvector loadings for the first principal component of the fruitbody data for the period 1985-1988.
Discussion The overriding trend in the fruitbody data is a change from a community dominated by Laccaria laccata, P. involutus and T. terrestris (all ubiquitous in the Northern Hemisphere) to a mixed community of 'early stage' fungi (Last et al., 1987). The occurrence of a succession of mycorrhizal species fruiting as a host tree matures is a well-known phenomenon (Marks and Foster, 1967; Mason et al., 1983; Last et al., 1984; Dighton et al., 1986), although comprehensive lists are not yet available for any tree species. The majority of studies have in-
190
P.Z A. Shaw et aL /Agriculture, Ecosystems and Environment 47 (1993) 185-191
volved visiting stands of widely differing ages on soils that are assumed to be reasonably similar, and the work presented above is unusual in being based on annual surveys of the same site. Richardson (1970) found that pine forests should be visited at intervals of 3-5 days to be confident of recording all toadstools. This and the density of the foliage from 1988 onwards means that the fruitbody counts from Liphook cannot be regarded as absolute, but they provide a useful index of the sporocarp population. The absence of a clear pollutant effect on this process agrees with the observations of Termorshuizen and Shaffers (1987) that under Scots pine in the Netherlands, mycorrhizal fruitbodies were depressed by air pollution in mature stands (50 years) but not in young stands (5-13 years). The first principal axis of the PCA on the Liphook carpophore data picked up its major trend, namely the succession away from nursery species (which had negative eigenvector loadings; Fig. 3 ). It also appeared to show a trend for SO2 to slow this succession down, and although the SO2 effect was not significant for any species, P. involutus fruited in the largest numbers in SO2-treated plots. The work at Liphook is unique in complementing the fruitbody surveys with annual monitoring of mycorrhizal infections on the tree roots. There was no clear change in morphotype composition corresponding to the fruitbody succession, implying that the changes in fruitbody emergence are due to physiological changes in the mycorrhizal symbiosis. The ordination of the Scots pine morphotype data shows a tentative effect due to SO2 and suggests a negative effect of SO2 on the P. involutus morph. This agrees with the observations of Dighton and Skeffington (1987) that acidic irrigation decreased the number of root tips of Scots pine with a brown coralloid morph ('Type F' ), later identified as P. involutus. Termorshuizen and Shaffers (1989) also noted that coralloid mycorrhizas were significantly negatively related to SO2 concentrations in the Netherlands, but did not identify their morphs to species. It is, however, hard to reconcile this decrease in P. involutus below ground with the increase in its fruitbodies found in the SO2-treated plots. It is hoped that further research will solve this apparent paradox.
Acknowledgements We thank M.R. Holland for assistance during field sampling and A.R. McLeod for discussions. This work is published with the permission of National Power plc. The Liphook project now forms part of the Joint Environmental Programme of National Power plc and Powergen plc. Financial support was received from the commission of the European Communities for part of this study.
P.J.A. Shaw et al. /Agriculture, Ecosystemsand Environment 47 (I 993) 185-191
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