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Effects of litter treatments on the sporophore production of beech forest macrofungi
Mycol. Res. 95 (9): 1137-1139 (1991)
1137
Printed in Great Britain
Effects of litter treatments on the sporophore production of beech forest macrofungi
GERMUND TYLER Department of Ecology, Soil Ecology Group, University of Lund, Ostra Vallgatan 14, S- 22361 Lund, Sweden
Removal of annual litter fall during two consecutive years in a Swedish beech forest increased the sporophore production of mycorrhizal Russula species considerably in both years, whereas sporophore production by most decomposer agarics was greatly reduced. In plots supplied with twice the annual amount of litter, Mycena capillaris was more abundant than in untreated control plots, otherwise sporophore production of decomposers was usually greatest in the controls.
Sporophore production by forest macrofungi is subjected to spatial patterns which cannot easily be explained merely by variability of forest stand structure, soil chemical properties, or the flux of throughfall water. An extensive lO-yr study of sporophore diversity and production in deciduous forest of south Sweden (Tyler 1985, 1989) revealed that much of the general between-site distribution differences of many fungi can be accounted for by a combination of base saturation (or soil pH), together with the organic matter content of the topsoil, and the presence of particular tree species. Within an apparently uniform forest stand, however, local distribution patterns of sporophore production seem to be superimposed on patterns influenced by soil chemistry or forest stand structure. The microtopography of the ground often promotes an uneven accumulation of leaf litter, which is particularly evident in beech forests often characterized by a comparatively low litter decomposition rate. That several decomposer fungi seem to be favoured by above-average amounts of soil surface litter is far from remarkable. The more ample substrate and less variable temperature and higher water availability may be factors of importance. Less easily understood and previously not reported is the observation that sporophore abundance of many other taxa, particularly species belonging to some mycorrhizal genera (Russula Pers. ex S. F. Gray, Inocybe Fr., Tricholoma (Fr.) Que!.), often seems to be greater on surfaces with below-average litter accumulation. The purpose of this study was to test the validity of these general observations experimentally, by means of removing or increasing the amount of soil surface litter in a beech forest with, under otherwise undisturbed conditions, a reasonably uniform litter supply. MATERIALS AND METHODS The site of the experiment was in the interior of a large, mature (age 110-140 yr) stand of pure beech (Fagus sylvatica 72
L) with a closed canopy. It is situated ca 40 km E of Lund, south Sweden. The soil is a deep glacifluvial sand deposit (clay content 3-5 %), the soil profile a dystric cambisol transition to arenosoL The top 5 cm is highly acid, pH-0'2 M KCl being 3'3-3'5, base saturation 12-18 %, and the organic matter content 10-15 %. The field layer is sparse, mainly with some Stellaria nemorum Land Dxalis acetosella L, with no shrubs present. In Nov. 1988, after litter fall, 30 circular plots (each 5 m2 ) were distributed within an area of 0'3 ha, in a stratified random way rejecting plots with margins within 2 m from any beech trunk The current autumn litter was removed from 10 of the plots and supplied to 10 other plots, the remaining 10 plots being left untouched as controls. In April 1989 some litter which had blown into the uncovered plots during the winter was removed and supplied similarly. The same procedure was repeated using the same plots in Nov. 1989 and April 1990. Macrofungal sporophores were recorded on 10 occasions in 1989 (15 July-20 Oct.) and on 8 occasions in 1990 (10 Aug.-20 Oct.). Dry weather made earlier observations in 1990 less meaningful; otherwise weather conditions during the observation periods did not deviate greatly from normaL The sporophores were detached from the substratum but left within the plots unless needed for microscopic determination. RESULTS The total number of species observed was 47; most of them, however, produced few sporophores. Only some taxa were frequent enough to justify a statistical treatment of the data (Table I). Sporophore production by species of the mycorrhizal genus Russula proved to be distinctly higher in the uncovered plots than in the controls or in plots supplied with extra litter. The mycorrhizal Lactarius subdulcis BulL ex Fr., on the contrary, produced least sporophores where the litter had been removed. These findings are fully consistent with my general field MYC 95
Litter treatments and sporophore production
1138
Table 1_ Mean number of species and sporophores of the main taxa per observation plot (5 m') in untreated controls and treatments (-litter, with tests for significant differences between treatments for 1989 + 1990. Untreated
-
n = 10
n = 10
1989 Mean number of species per 5 m' Mean number of sporophores per 5 m' Russula spp.• Laclarius subdulcis Bull. ex Fr. Collybia butyracea (Bull. ex Fr.) QwH. Flammulaster carpophila (Fr.) Earle Mycena capillaris (Schum. ex Fr.) Kummer Mycena cinerella Karst. Mycena galopus (Pers. ex Fr.) Kummer Psalhyrella (Fr.) Quel. spp. Marasmius alliaceus (Jacq. ex Fr.) Fr. Mycena sanguinolenta (A. &< S. ex Fr.) Kummer
1990
Litter
+
+ t;Uer)
LiUer
n = 10
1989 + 199O(A)
1989
1990
1989 + 1990(B)
1989
1990
1989 + 1990(C)
7'6
8'5
II-2
5'4
4'7
7·ga
6'6
6-2
8'8"
0'7 4'8 2'2 5'9 4'4 2'2 4'9 0'5 0'4 0'5
0'9 6'3 II'3 3'0 38 5'4 9'4 0'1 0'4 0-4
1'6 II'1 13"5 8'9 42 7'6 14'3 0'6 0'8 0'9
2'0 0'9 0'3 0-2
5'5 0'2 1'1 0'0 0'8 1'8 0'9
7'5 h' I-I'
0'2 0'9 0'9 1'6 6'3 0'7 2'8 1'2 0'6 0'3
0'4 2-1 3-7
0'6 3'0" 4'6" 2-7' 116" 1'0'\ 5-8' 1-5
0'1 0'5 I-I 0-2 0'2 0-7
0'1 1-0
1·4 ae
0'2"" 0'9h ' 2'3' 2'0' 0'2 0'3 1'7
1'1 IIO 0'3 3'0 0'3 0'9 0'2
1'5 0-5
, B ,., A, P < 0'01; h B ,., A. P < 0'001; , C ,., A. P < 0'05; " C ,., A. P < 0-01; , B ,., C. P < 0'05; r B ,., C. P < 0'001. • Mainly R. fellea Fr. and R. ochroleuca (Pers.) Fr.
observations. Among the decomposer species (Collybia butyracea (Bull. ex Fr.) Que!', Flammulaster carpophila (Fr.) Earle, Mycena galopus (Pers. ex Fr.) Kummer, and Mycena cinerella Karst.) more sporophores were usually produced in the undisturbed controls with minimum production in the uncovered plots. A few species, Mycena capillaris (Schum. ex Fr.) Kummer, two species of Psathyrella (Fr.) Que!. and possibly Marasmius alliaceus Oacq. ex Fr.) Fr., were most common in plots supplied with extra litter. Extra litter seemed, however, to cause some disturbance of sporophore production by most decomposers. Mycena sanguinolenta (A. & S. ex Fr.) Kummer was the only decomposer with maximum sporophore abundance in the uncovered plots, though the total number was low and differences not fully significant. On average, the sum of decomposer sporophores (excl. Mycena capillaris) observed per 5 m was 58 for untreated controls, 25 for plots with extra litter and 13 for uncovered plots_ In all the quantitatively more important fungi, the relative difference between controls and treatments in sporophore numbers observed was similar in both years (Table 1).
DISCUSSION No experiments designed to study the influence of litter removal or addition on the fructification of deciduous forest macrofungi seem to have been reported previously. Mejstrik & Dominik (1969) considered humus quality and quantity the most important factor for the formation of forest mycorrhiza_ Litter and humus are often considered key factors in ectomycorrhizal activity, partly owing to an ability to buffer wide variations in pH, moisture and temperature (Harvey, Larsen & Jurgensen, 1980), and strong positive effects of soil organic matter or organic amendments on the abundance of ectomycorrhiza have been reported (Mikola, 1973). Therefore, the beneficial effect of litter removal on the sporophore production by mycorrhizal fungi reported here might have been unpredicted.
The mechanisms governing increased sporophore production by certain mycorrhizal species on litter removal are not obvious. Antagonism between ectomycorrhiza and decomposer fungi is known to occur, though mainly in disfavour of the decomposers. According to Gadgil & Gadgil (1975) ectomycorrhizal fungi may penetrate the litter layer, inhibit the activity of the litter decomposers and thereby contribute to the formation of mor conditions. Antibiotics and other secondary metabolites produced by litter decomposing fungi inhibit the growth of other fungi (Wicklow, 1981; Hintikka, 1982) and could have an important influence on mycorrhizal development. Thus removing litter could reduce antagonism by removing a large share of the decomposers. The possibility should, however, not be disregarded that purely mechanical or climatic differences created by the differences in litter cover might regulate sporophore production of mycorrhizal fungi. As the fruitbodies of most species of Russula usually originate from deeper parts of the topsoil than the litter layer, a stimulating effect on sporophore development from soil climate variability might be of significance for these species. More elaborate field experiments involving a consideration of soil climatic variability owing to uneven litter accumulation might elucidate some of these questions. The observed stimulatory effect of litter removal on sporophore production of mycorrhizal fungi tells us very little about the influence of the litter on other characteristics of the symbiotic relationship. Repeated litter removal, however, deprives the soil of a substantial part of the recirculating mineral nutrients and nitrogen, thereby possibly increasing the dependence of the trees on these poor forest soils on well functioning mycorrhizae. The old and widely accepted theory of a reverse relationship between soil fertility and the development of edomycorrhizae might be valid in this context.
G. Tyler REFERENCES Gadgil. R. L. &; Gadgil. P. D. (1975). Suppression of litter decomposition by mycorrhizal roots of Pinus radiata. New Zealand Journal of Forest Science 5, 31-41. Harvey, A. E., Larsen, M.). &; Jurgensen, M F. (1980). Ecology of ectomycorrhizae in northern Rocky Mountain forests. General Technical
Report, Inter-mountain Forest Range Experimental Station, INT-90, 189-208. Hintikka, V. (1982). The colonization of litter and wood by basidiomycetes in Finnish forests. In Decomposer Basidiomycetes: Their Biology and Ecology (ed. ). C. Frankland, J. N. Hedger &; M. J. SWift), pp. 227-239. Cambridge University Press: Cambridge, U.K. Mejstrik. V. &; Dominik. T. (1969). The ecological distribution of mycorrhiza of beech. New Phytologist 68, 689-700.
1139 Mikola, P. (1973). Mycorrhizal symbiosis in forestry practice. In Ectomycorrhime, their Ecology and Physiology (ed. G. C. Marks &; T. T. Kozlowski), pp. 383-411. Academic Press: New York. Tyler, G. (1985). Macrofungal flora of Swedish beech forest related to soil organic matter and acidity characteristics. Forest Ecology and Management 10,13-29. Tyler, G. (1989). Edaphical distribution patterns of macrofungal species in deciduous forest of south Sweden. Acta Oecologica, Oecologia Generalis 10, 309-326. Wicklow, D. T. (1981). Interference competition and the organization of fungal communities. In The Fungal Community - its Organizntion and Role in the Ecosystem (ed. D. T. Wicklow &; G. C. Carroll), pp. 351-375. Marcel Dekker: New York.
(Received for publication 19 November 1990)
71-2
1137
Printed in Great Britain
Effects of litter treatments on the sporophore production of beech forest macrofungi
GERMUND TYLER Department of Ecology, Soil Ecology Group, University of Lund, Ostra Vallgatan 14, S- 22361 Lund, Sweden
Removal of annual litter fall during two consecutive years in a Swedish beech forest increased the sporophore production of mycorrhizal Russula species considerably in both years, whereas sporophore production by most decomposer agarics was greatly reduced. In plots supplied with twice the annual amount of litter, Mycena capillaris was more abundant than in untreated control plots, otherwise sporophore production of decomposers was usually greatest in the controls.
Sporophore production by forest macrofungi is subjected to spatial patterns which cannot easily be explained merely by variability of forest stand structure, soil chemical properties, or the flux of throughfall water. An extensive lO-yr study of sporophore diversity and production in deciduous forest of south Sweden (Tyler 1985, 1989) revealed that much of the general between-site distribution differences of many fungi can be accounted for by a combination of base saturation (or soil pH), together with the organic matter content of the topsoil, and the presence of particular tree species. Within an apparently uniform forest stand, however, local distribution patterns of sporophore production seem to be superimposed on patterns influenced by soil chemistry or forest stand structure. The microtopography of the ground often promotes an uneven accumulation of leaf litter, which is particularly evident in beech forests often characterized by a comparatively low litter decomposition rate. That several decomposer fungi seem to be favoured by above-average amounts of soil surface litter is far from remarkable. The more ample substrate and less variable temperature and higher water availability may be factors of importance. Less easily understood and previously not reported is the observation that sporophore abundance of many other taxa, particularly species belonging to some mycorrhizal genera (Russula Pers. ex S. F. Gray, Inocybe Fr., Tricholoma (Fr.) Que!.), often seems to be greater on surfaces with below-average litter accumulation. The purpose of this study was to test the validity of these general observations experimentally, by means of removing or increasing the amount of soil surface litter in a beech forest with, under otherwise undisturbed conditions, a reasonably uniform litter supply. MATERIALS AND METHODS The site of the experiment was in the interior of a large, mature (age 110-140 yr) stand of pure beech (Fagus sylvatica 72
L) with a closed canopy. It is situated ca 40 km E of Lund, south Sweden. The soil is a deep glacifluvial sand deposit (clay content 3-5 %), the soil profile a dystric cambisol transition to arenosoL The top 5 cm is highly acid, pH-0'2 M KCl being 3'3-3'5, base saturation 12-18 %, and the organic matter content 10-15 %. The field layer is sparse, mainly with some Stellaria nemorum Land Dxalis acetosella L, with no shrubs present. In Nov. 1988, after litter fall, 30 circular plots (each 5 m2 ) were distributed within an area of 0'3 ha, in a stratified random way rejecting plots with margins within 2 m from any beech trunk The current autumn litter was removed from 10 of the plots and supplied to 10 other plots, the remaining 10 plots being left untouched as controls. In April 1989 some litter which had blown into the uncovered plots during the winter was removed and supplied similarly. The same procedure was repeated using the same plots in Nov. 1989 and April 1990. Macrofungal sporophores were recorded on 10 occasions in 1989 (15 July-20 Oct.) and on 8 occasions in 1990 (10 Aug.-20 Oct.). Dry weather made earlier observations in 1990 less meaningful; otherwise weather conditions during the observation periods did not deviate greatly from normaL The sporophores were detached from the substratum but left within the plots unless needed for microscopic determination. RESULTS The total number of species observed was 47; most of them, however, produced few sporophores. Only some taxa were frequent enough to justify a statistical treatment of the data (Table I). Sporophore production by species of the mycorrhizal genus Russula proved to be distinctly higher in the uncovered plots than in the controls or in plots supplied with extra litter. The mycorrhizal Lactarius subdulcis BulL ex Fr., on the contrary, produced least sporophores where the litter had been removed. These findings are fully consistent with my general field MYC 95
Litter treatments and sporophore production
1138
Table 1_ Mean number of species and sporophores of the main taxa per observation plot (5 m') in untreated controls and treatments (-litter, with tests for significant differences between treatments for 1989 + 1990. Untreated
-
n = 10
n = 10
1989 Mean number of species per 5 m' Mean number of sporophores per 5 m' Russula spp.• Laclarius subdulcis Bull. ex Fr. Collybia butyracea (Bull. ex Fr.) QwH. Flammulaster carpophila (Fr.) Earle Mycena capillaris (Schum. ex Fr.) Kummer Mycena cinerella Karst. Mycena galopus (Pers. ex Fr.) Kummer Psalhyrella (Fr.) Quel. spp. Marasmius alliaceus (Jacq. ex Fr.) Fr. Mycena sanguinolenta (A. &< S. ex Fr.) Kummer
1990
Litter
+
+ t;Uer)
LiUer
n = 10
1989 + 199O(A)
1989
1990
1989 + 1990(B)
1989
1990
1989 + 1990(C)
7'6
8'5
II-2
5'4
4'7
7·ga
6'6
6-2
8'8"
0'7 4'8 2'2 5'9 4'4 2'2 4'9 0'5 0'4 0'5
0'9 6'3 II'3 3'0 38 5'4 9'4 0'1 0'4 0-4
1'6 II'1 13"5 8'9 42 7'6 14'3 0'6 0'8 0'9
2'0 0'9 0'3 0-2
5'5 0'2 1'1 0'0 0'8 1'8 0'9
7'5 h' I-I'
0'2 0'9 0'9 1'6 6'3 0'7 2'8 1'2 0'6 0'3
0'4 2-1 3-7
0'6 3'0" 4'6" 2-7' 116" 1'0'\ 5-8' 1-5
0'1 0'5 I-I 0-2 0'2 0-7
0'1 1-0
1·4 ae
0'2"" 0'9h ' 2'3' 2'0' 0'2 0'3 1'7
1'1 IIO 0'3 3'0 0'3 0'9 0'2
1'5 0-5
, B ,., A, P < 0'01; h B ,., A. P < 0'001; , C ,., A. P < 0'05; " C ,., A. P < 0-01; , B ,., C. P < 0'05; r B ,., C. P < 0'001. • Mainly R. fellea Fr. and R. ochroleuca (Pers.) Fr.
observations. Among the decomposer species (Collybia butyracea (Bull. ex Fr.) Que!', Flammulaster carpophila (Fr.) Earle, Mycena galopus (Pers. ex Fr.) Kummer, and Mycena cinerella Karst.) more sporophores were usually produced in the undisturbed controls with minimum production in the uncovered plots. A few species, Mycena capillaris (Schum. ex Fr.) Kummer, two species of Psathyrella (Fr.) Que!. and possibly Marasmius alliaceus Oacq. ex Fr.) Fr., were most common in plots supplied with extra litter. Extra litter seemed, however, to cause some disturbance of sporophore production by most decomposers. Mycena sanguinolenta (A. & S. ex Fr.) Kummer was the only decomposer with maximum sporophore abundance in the uncovered plots, though the total number was low and differences not fully significant. On average, the sum of decomposer sporophores (excl. Mycena capillaris) observed per 5 m was 58 for untreated controls, 25 for plots with extra litter and 13 for uncovered plots_ In all the quantitatively more important fungi, the relative difference between controls and treatments in sporophore numbers observed was similar in both years (Table 1).
DISCUSSION No experiments designed to study the influence of litter removal or addition on the fructification of deciduous forest macrofungi seem to have been reported previously. Mejstrik & Dominik (1969) considered humus quality and quantity the most important factor for the formation of forest mycorrhiza_ Litter and humus are often considered key factors in ectomycorrhizal activity, partly owing to an ability to buffer wide variations in pH, moisture and temperature (Harvey, Larsen & Jurgensen, 1980), and strong positive effects of soil organic matter or organic amendments on the abundance of ectomycorrhiza have been reported (Mikola, 1973). Therefore, the beneficial effect of litter removal on the sporophore production by mycorrhizal fungi reported here might have been unpredicted.
The mechanisms governing increased sporophore production by certain mycorrhizal species on litter removal are not obvious. Antagonism between ectomycorrhiza and decomposer fungi is known to occur, though mainly in disfavour of the decomposers. According to Gadgil & Gadgil (1975) ectomycorrhizal fungi may penetrate the litter layer, inhibit the activity of the litter decomposers and thereby contribute to the formation of mor conditions. Antibiotics and other secondary metabolites produced by litter decomposing fungi inhibit the growth of other fungi (Wicklow, 1981; Hintikka, 1982) and could have an important influence on mycorrhizal development. Thus removing litter could reduce antagonism by removing a large share of the decomposers. The possibility should, however, not be disregarded that purely mechanical or climatic differences created by the differences in litter cover might regulate sporophore production of mycorrhizal fungi. As the fruitbodies of most species of Russula usually originate from deeper parts of the topsoil than the litter layer, a stimulating effect on sporophore development from soil climate variability might be of significance for these species. More elaborate field experiments involving a consideration of soil climatic variability owing to uneven litter accumulation might elucidate some of these questions. The observed stimulatory effect of litter removal on sporophore production of mycorrhizal fungi tells us very little about the influence of the litter on other characteristics of the symbiotic relationship. Repeated litter removal, however, deprives the soil of a substantial part of the recirculating mineral nutrients and nitrogen, thereby possibly increasing the dependence of the trees on these poor forest soils on well functioning mycorrhizae. The old and widely accepted theory of a reverse relationship between soil fertility and the development of edomycorrhizae might be valid in this context.
G. Tyler REFERENCES Gadgil. R. L. &; Gadgil. P. D. (1975). Suppression of litter decomposition by mycorrhizal roots of Pinus radiata. New Zealand Journal of Forest Science 5, 31-41. Harvey, A. E., Larsen, M.). &; Jurgensen, M F. (1980). Ecology of ectomycorrhizae in northern Rocky Mountain forests. General Technical
Report, Inter-mountain Forest Range Experimental Station, INT-90, 189-208. Hintikka, V. (1982). The colonization of litter and wood by basidiomycetes in Finnish forests. In Decomposer Basidiomycetes: Their Biology and Ecology (ed. ). C. Frankland, J. N. Hedger &; M. J. SWift), pp. 227-239. Cambridge University Press: Cambridge, U.K. Mejstrik. V. &; Dominik. T. (1969). The ecological distribution of mycorrhiza of beech. New Phytologist 68, 689-700.
1139 Mikola, P. (1973). Mycorrhizal symbiosis in forestry practice. In Ectomycorrhime, their Ecology and Physiology (ed. G. C. Marks &; T. T. Kozlowski), pp. 383-411. Academic Press: New York. Tyler, G. (1985). Macrofungal flora of Swedish beech forest related to soil organic matter and acidity characteristics. Forest Ecology and Management 10,13-29. Tyler, G. (1989). Edaphical distribution patterns of macrofungal species in deciduous forest of south Sweden. Acta Oecologica, Oecologia Generalis 10, 309-326. Wicklow, D. T. (1981). Interference competition and the organization of fungal communities. In The Fungal Community - its Organizntion and Role in the Ecosystem (ed. D. T. Wicklow &; G. C. Carroll), pp. 351-375. Marcel Dekker: New York.
(Received for publication 19 November 1990)
71-2