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Nitrogen and phosphorus mobilization by the fairy ring fungus, Marasmius oreades (bolt.) fr
Sod Bid.
Biochem.
Vol. 9, pp. 239 to 241. Pergamon Press 1977. Printed in Great Britain.
NITROGEN AND PHOSPHORUS MOBILIZATION BY THE FAIRY RING FUNGUS, MARASlMlUS OREAD_ES (BOLT.) FR. R. F. FISHER Faculty of Forestry and Landscape Architecture, University of Toronto, Toronto, Ontario, Canada, M5S f Al (Accepted 18 November 1976) Summary-Chronological sampling of expanding fairy rings showed that N and P were mobilized during active mycelial extension. Soil through which the fungus had passed exhibited depressed concentrations of extractable N and P. This mav be one of a complex of factors which account for the concentric ring life form. I
INTRODUCTION Fairy rings produced by the fungus ~~ras~j~s oreodes (Bolt.) Fr. are characterized by two or three adjacent concentric zones of abnormal turf. Within the zone of most intense fungal growth, the grass is often killed, and this effect has been attributed to a lack of moisture and to hydrogen cyanide produced by the fungus (Shantz and Piemeisel, 1917; Lebau and Hawn, 1963 ; Filer, 1965). In most cases abnormally good growth of grass occurs for a time in this zone of intense mycelial activity. This is followed by a weakening and yellowing of the turf and ultimately by death of some or all of the grass in this zone. Shantz and Piemeisel (1917) and Norstadt et at. (1973) have suggested that this sequence of events may be due to the ~nerali~tion of N by the fungus. However, to the best of my knowledge, no chronological record of soil N or P changes in the expanding fairy ring exists. This investigation attempted to follow such seasonal changes in a set of typical fairy rings.
NH:-N by Nesslerization and P by the stannous chlorid~molybdenum blue procedure (Grewling and Peech, 1965). The amount in each sample was corrected for difIerences in bulk density and expressed as kg ha- I. The results were subjected to an analysis of variance and all differences described as significant were statistically significant at the 5% level. RESULTS
The analysis of variance revealed that the only significant effects were ring position and time of sampling. There was surprisingly little variation between samples from the same ring position and between the same positions in different rings. Table 1 illustrates this by presenting the mean and standard error for NHf-N, NO;-N and P by ring position at both sample times for each site. Figure 1 illustrates the NH:-N, NOT-N and P content of the surface soil beneath the ring of greener taller grass. This zone develops as the colony expands into previously unaffected soil and appears to coincide with the most rapid phase of mycelial extension. MATERIALSAND METHODS At the centre of this zone extractable NH:-N concentrations were three times those in unaffected soil. Three areas of well managed turf were selected in a 30km’ metropolitan area. Each site had been Although this concentration diminished both inmown, fertilized and sprayed with weed control wardly and outwardly from zone centre, there was chemicals. At each site three fairy rings, more than a band appro~mately 2Ocm wide with significantly 2 m in diameter, were selected for sampling, One ring more extractable NH:-N than in the normal soil. Extractable NOT-N did not increase as greatly, at each site was examined from late May onward by means of a trench across the ring.from which a new and then only the centre of the ring had si~ificantly slice of earth was removed each week. Thus the extenmore NO;-N than the normal soil. However, there sion of the mycellium and the formation of fruiting was significantly less extractable NO;-N in soil prestructures was followed. Samples were taken at the viously occupied by the fungus than in normal soil. Extractable P was also much higher in the green time of maximum mycelial extension when the rings were represented by taller, greener grass (mid July) ring. There was a band approximately 20cm wide and 5 weeks later just before fruiting when the rings in which there was significantly more P than in the were represented by yellow-brown grass. Each time unaffected soil. In addition there was a significant samples were taken at the centre of the coloured area reduction in the amount of extractable P in soil preand 10, 30, and 1OOcm inside and outside that area. viously occupied by the fungus. Figure 2 illustrates the NH:-N, NO;-N and P Five composite samples of three 5em diameter cores of the upper 10 cm of soil were taken from the concentrations in the surface soil 5 weeks later when seven sampling positions across the ring on both samthe grass in the same ring of turf had died or become pling dates. These samples were extracted with neuchlorotic. This is just before fruiting and appears to tral normal sodium acetate and the extracts analyzed. be the time of maximum biomass production by the NO;-N was determined by the brucine method, fungus. NH;-N, NOT-N and P all show a remark239
R. F. Ftsttr I<
240 Table
I. Means
and
standard
errors
at two sampling
9.X~ 0 IO 102 0.33 10.3 0.59 IO1 045 99 0.12 9 x 0.78 9.1 0.37 9 6 0.62 NO;-N
5.5 5.1 5.0 52
2(X?. , 31x3.. ,
0.45 02x 030 0.41
P
I(rl , Xx? .I ..l ix ..l
31x 3
10.2 Y5 Y.X 110 100
02x 061 0.7x 022 0.36 10.2 037 lO.4-054
dates
Ih.6 17.1 I6 1 16.X 50 47 5.0 49
O.5Y 0.22 0.56 0 52 075 050 0 25 0.38
303 30x 2X 8 2Y.7 21 25 26 24
042 029 0.x0 1 34 025 054 0.36 045
50 0.14 49 0.22 46 022 4 X 0.26 4X 031 4.4 02Y 4.6 0 36 4 6 --I) 56
62 59 55 5.x 3.0 27 33 3.0
0.22 029 0.22 0.33 0 22 A,,6 022 032
X.4 X7 X.1 X4 2.7 24 27 25
0 22 054 0.36 046 0 50 022 OI6 0 X0
9.9 0 36 105 0.43 102 051 IO? 0 50 9 2 0.22 9X- 0.16 9.4--O37 9 5-4.43
I55 160 I53 156 X6 7.7 x.0 X.1
07x 022 0.56 064 025 0.22 0 43 049
191 207 ,9X 1Y.Y 4.6 51 50 49
O.YI 1175 037 0 44 0 19 016 0 I4 0 29
DlSCLW3ION
These data demonstrate that the fairy ring fungus is capable of mobilizing N and P from surface soil. DISTANCE FROM CENTRE OF ACTIVE ZONE - cm 30
IO
0 a
10
30
-N. and
IO.1 0.22 x 9 0.28 x.3 029 9.1 a79 9 7 0.29 X0--049 9.0~ 0 37 X.9 0.80
able decrease in the formerly greener ring. The NH:-N was reduced more than 909/;, NO;-N more than 70”/, and P more than 75% from the high concentrations of 5 weeks earlier. The soil that had been occupied by the fungus in previous years continued to have extractable NH:-N, NOT-N and P concentrations significantly lower than the concentration for unaffected soil.
loo
for NH: -N, NO,
Ion
70 68
P by sate and
008 047
67 65
rmg
position
014 03Y
The work of Mathur (1970) and Norstadt et ul. (1972) has shown that M. orrcule.~ has the ability to degrade soil humus and mineralize organic N. Thus. the source of N and P that is mobilized by the expanding fairy ring is likely to be soil organic matter. The greener ring of grass often associated with fairy rings appears to follow the rapid release of N and P into the soil by the extending mycelium. As the fungal growth becomes more intense, the fungus consumes much of the available N and P. and the turf is weakened. Cyanide production and water repellency may play a part in the ensuing turf malady. however, it is clear that the poor fertility status of soil currently or previously occupied by the fungus does not favour good turf formation. It has been suggested that fairy rings occur on poorly managed soils with low non-humic sources of C and N. The soils used in this study were fertilized with seemingly adequate amounts of readily-available
DISTANCE FROM CENTRE OF ACTIVE ZONE-cm loo 30 IO 0 10 30 loo
” loo 30 10 0 10 30 IW DISTANCE FROM CENTRE OF ACTIVE ZONE-cm Fig. 1. Extractable N as NH: and NO; and extractable P in fairy rings at the time of active mycelial extension. Values with the same letter are not significantly different at the 5”; level of significance.
” loo 30 10 0 10 30 loo DISTANCE FROM CENTRE OF ACTIVE ZONE-cm Fig. 2. Extractable N as NH; and NO; and extractable P in fairy rings immediately prior to fruiting. Values with the same letter arc not significantly different at the S’,, level of significance.
241
N and P mobilization by M. oreades N and P. Mathur (1970) found that low O2 concentrations aided in the mineralization of soil humic substances by M. ore&es. It is probable that poor aeration due to compaction and irrigation was more important than low fertility in encouraging fairy ring development on the study sites. The outward movement of the ring is undoubtedly due to a complex of factors. Inertia, water repellency of the soil, and cyanide formation have been suggested as causes for the continual occupation of new soil. The depletion of readily mineralizable humic N and P substrate in soil occupied by the fungus is no doubt an additional factor favouring the invasion of previously unoccupied soil.
REFERENCES
FILERT. H. (1965) Damage to turfgrasses caused by cyanogentic compounds produced by Marasmius oreades, a fairy ring fungus. P1. Dis. Reptr. 49. 571-574. GRE;LING-T. aid M. PEECH (1965) Chemical soil tests. Agr. Exp. Stand. Bull. Cornell Univ. 960. LEBEAUJ. B. and E. J. HAWN (1963) Formation of hvdrogen cyanide by the mycelial stage of a fairy ring fuigus. Phytopathology 53, 1395-1396. MATHURS. P. (1970) Degradation of soil humus by the _ fairy ring mushroom. I’? Soil 33, 717-720. NORSTADTF. A.. C. R. FREY.and SIGG (1973) Soil urease: Paucity in the presence of the fairy ring fingus Marasmitts oreades (Bolt.) Fr. Proc. Soil Sci. Sot. Am. 37. 88&884. SHANTZH. L. and R. L. PIEMEISEL(1917) Fungus fairy rings in eastern Colorado and their effect on vegetation. J. Agr. Res. 2. 191-245.
Biochem.
Vol. 9, pp. 239 to 241. Pergamon Press 1977. Printed in Great Britain.
NITROGEN AND PHOSPHORUS MOBILIZATION BY THE FAIRY RING FUNGUS, MARASlMlUS OREAD_ES (BOLT.) FR. R. F. FISHER Faculty of Forestry and Landscape Architecture, University of Toronto, Toronto, Ontario, Canada, M5S f Al (Accepted 18 November 1976) Summary-Chronological sampling of expanding fairy rings showed that N and P were mobilized during active mycelial extension. Soil through which the fungus had passed exhibited depressed concentrations of extractable N and P. This mav be one of a complex of factors which account for the concentric ring life form. I
INTRODUCTION Fairy rings produced by the fungus ~~ras~j~s oreodes (Bolt.) Fr. are characterized by two or three adjacent concentric zones of abnormal turf. Within the zone of most intense fungal growth, the grass is often killed, and this effect has been attributed to a lack of moisture and to hydrogen cyanide produced by the fungus (Shantz and Piemeisel, 1917; Lebau and Hawn, 1963 ; Filer, 1965). In most cases abnormally good growth of grass occurs for a time in this zone of intense mycelial activity. This is followed by a weakening and yellowing of the turf and ultimately by death of some or all of the grass in this zone. Shantz and Piemeisel (1917) and Norstadt et at. (1973) have suggested that this sequence of events may be due to the ~nerali~tion of N by the fungus. However, to the best of my knowledge, no chronological record of soil N or P changes in the expanding fairy ring exists. This investigation attempted to follow such seasonal changes in a set of typical fairy rings.
NH:-N by Nesslerization and P by the stannous chlorid~molybdenum blue procedure (Grewling and Peech, 1965). The amount in each sample was corrected for difIerences in bulk density and expressed as kg ha- I. The results were subjected to an analysis of variance and all differences described as significant were statistically significant at the 5% level. RESULTS
The analysis of variance revealed that the only significant effects were ring position and time of sampling. There was surprisingly little variation between samples from the same ring position and between the same positions in different rings. Table 1 illustrates this by presenting the mean and standard error for NHf-N, NO;-N and P by ring position at both sample times for each site. Figure 1 illustrates the NH:-N, NOT-N and P content of the surface soil beneath the ring of greener taller grass. This zone develops as the colony expands into previously unaffected soil and appears to coincide with the most rapid phase of mycelial extension. MATERIALSAND METHODS At the centre of this zone extractable NH:-N concentrations were three times those in unaffected soil. Three areas of well managed turf were selected in a 30km’ metropolitan area. Each site had been Although this concentration diminished both inmown, fertilized and sprayed with weed control wardly and outwardly from zone centre, there was chemicals. At each site three fairy rings, more than a band appro~mately 2Ocm wide with significantly 2 m in diameter, were selected for sampling, One ring more extractable NH:-N than in the normal soil. Extractable NOT-N did not increase as greatly, at each site was examined from late May onward by means of a trench across the ring.from which a new and then only the centre of the ring had si~ificantly slice of earth was removed each week. Thus the extenmore NO;-N than the normal soil. However, there sion of the mycellium and the formation of fruiting was significantly less extractable NO;-N in soil prestructures was followed. Samples were taken at the viously occupied by the fungus than in normal soil. Extractable P was also much higher in the green time of maximum mycelial extension when the rings were represented by taller, greener grass (mid July) ring. There was a band approximately 20cm wide and 5 weeks later just before fruiting when the rings in which there was significantly more P than in the were represented by yellow-brown grass. Each time unaffected soil. In addition there was a significant samples were taken at the centre of the coloured area reduction in the amount of extractable P in soil preand 10, 30, and 1OOcm inside and outside that area. viously occupied by the fungus. Figure 2 illustrates the NH:-N, NO;-N and P Five composite samples of three 5em diameter cores of the upper 10 cm of soil were taken from the concentrations in the surface soil 5 weeks later when seven sampling positions across the ring on both samthe grass in the same ring of turf had died or become pling dates. These samples were extracted with neuchlorotic. This is just before fruiting and appears to tral normal sodium acetate and the extracts analyzed. be the time of maximum biomass production by the NO;-N was determined by the brucine method, fungus. NH;-N, NOT-N and P all show a remark239
R. F. Ftsttr I<
240 Table
I. Means
and
standard
errors
at two sampling
9.X~ 0 IO 102 0.33 10.3 0.59 IO1 045 99 0.12 9 x 0.78 9.1 0.37 9 6 0.62 NO;-N
5.5 5.1 5.0 52
2(X?. , 31x3.. ,
0.45 02x 030 0.41
P
I(rl , Xx? .I ..l ix ..l
31x 3
10.2 Y5 Y.X 110 100
02x 061 0.7x 022 0.36 10.2 037 lO.4-054
dates
Ih.6 17.1 I6 1 16.X 50 47 5.0 49
O.5Y 0.22 0.56 0 52 075 050 0 25 0.38
303 30x 2X 8 2Y.7 21 25 26 24
042 029 0.x0 1 34 025 054 0.36 045
50 0.14 49 0.22 46 022 4 X 0.26 4X 031 4.4 02Y 4.6 0 36 4 6 --I) 56
62 59 55 5.x 3.0 27 33 3.0
0.22 029 0.22 0.33 0 22 A,,6 022 032
X.4 X7 X.1 X4 2.7 24 27 25
0 22 054 0.36 046 0 50 022 OI6 0 X0
9.9 0 36 105 0.43 102 051 IO? 0 50 9 2 0.22 9X- 0.16 9.4--O37 9 5-4.43
I55 160 I53 156 X6 7.7 x.0 X.1
07x 022 0.56 064 025 0.22 0 43 049
191 207 ,9X 1Y.Y 4.6 51 50 49
O.YI 1175 037 0 44 0 19 016 0 I4 0 29
DlSCLW3ION
These data demonstrate that the fairy ring fungus is capable of mobilizing N and P from surface soil. DISTANCE FROM CENTRE OF ACTIVE ZONE - cm 30
IO
0 a
10
30
-N. and
IO.1 0.22 x 9 0.28 x.3 029 9.1 a79 9 7 0.29 X0--049 9.0~ 0 37 X.9 0.80
able decrease in the formerly greener ring. The NH:-N was reduced more than 909/;, NO;-N more than 70”/, and P more than 75% from the high concentrations of 5 weeks earlier. The soil that had been occupied by the fungus in previous years continued to have extractable NH:-N, NOT-N and P concentrations significantly lower than the concentration for unaffected soil.
loo
for NH: -N, NO,
Ion
70 68
P by sate and
008 047
67 65
rmg
position
014 03Y
The work of Mathur (1970) and Norstadt et ul. (1972) has shown that M. orrcule.~ has the ability to degrade soil humus and mineralize organic N. Thus. the source of N and P that is mobilized by the expanding fairy ring is likely to be soil organic matter. The greener ring of grass often associated with fairy rings appears to follow the rapid release of N and P into the soil by the extending mycelium. As the fungal growth becomes more intense, the fungus consumes much of the available N and P. and the turf is weakened. Cyanide production and water repellency may play a part in the ensuing turf malady. however, it is clear that the poor fertility status of soil currently or previously occupied by the fungus does not favour good turf formation. It has been suggested that fairy rings occur on poorly managed soils with low non-humic sources of C and N. The soils used in this study were fertilized with seemingly adequate amounts of readily-available
DISTANCE FROM CENTRE OF ACTIVE ZONE-cm loo 30 IO 0 10 30 loo
” loo 30 10 0 10 30 IW DISTANCE FROM CENTRE OF ACTIVE ZONE-cm Fig. 1. Extractable N as NH: and NO; and extractable P in fairy rings at the time of active mycelial extension. Values with the same letter are not significantly different at the 5”; level of significance.
” loo 30 10 0 10 30 loo DISTANCE FROM CENTRE OF ACTIVE ZONE-cm Fig. 2. Extractable N as NH; and NO; and extractable P in fairy rings immediately prior to fruiting. Values with the same letter arc not significantly different at the S’,, level of significance.
241
N and P mobilization by M. oreades N and P. Mathur (1970) found that low O2 concentrations aided in the mineralization of soil humic substances by M. ore&es. It is probable that poor aeration due to compaction and irrigation was more important than low fertility in encouraging fairy ring development on the study sites. The outward movement of the ring is undoubtedly due to a complex of factors. Inertia, water repellency of the soil, and cyanide formation have been suggested as causes for the continual occupation of new soil. The depletion of readily mineralizable humic N and P substrate in soil occupied by the fungus is no doubt an additional factor favouring the invasion of previously unoccupied soil.
REFERENCES
FILERT. H. (1965) Damage to turfgrasses caused by cyanogentic compounds produced by Marasmius oreades, a fairy ring fungus. P1. Dis. Reptr. 49. 571-574. GRE;LING-T. aid M. PEECH (1965) Chemical soil tests. Agr. Exp. Stand. Bull. Cornell Univ. 960. LEBEAUJ. B. and E. J. HAWN (1963) Formation of hvdrogen cyanide by the mycelial stage of a fairy ring fuigus. Phytopathology 53, 1395-1396. MATHURS. P. (1970) Degradation of soil humus by the _ fairy ring mushroom. I’? Soil 33, 717-720. NORSTADTF. A.. C. R. FREY.and SIGG (1973) Soil urease: Paucity in the presence of the fairy ring fingus Marasmitts oreades (Bolt.) Fr. Proc. Soil Sci. Sot. Am. 37. 88&884. SHANTZH. L. and R. L. PIEMEISEL(1917) Fungus fairy rings in eastern Colorado and their effect on vegetation. J. Agr. Res. 2. 191-245.