Changes in spatial distribution of fungal propagules associated with invertebrate activity in soil

Soil Eiol. Biochem. Vol. 16,No. 6. pp. 601-604, Printed in Great Britain. All rights reserved

1984 Copyright

c

003%0717/84 $3.00 + 0.00 1984 Pergamon Press Ltd

CHANGES IN SPATIAL DISTRIBUTION OF FUNGAL PROPAGULES ASSOCIATED WITH INVERTEBRATE ACTIVITY IN SOIL JOHN LUSSENHOP Department of Biological Sciences, University of Illinois at Chicago, Box 4348, Chicago, IL 60680, U.S.A.

and DONALD T. WICKLOW Northern Regional Research Center, ARS-USDA, 1815 N. University Street, Peoria, IL 61604, U.S.A. (Accepted 23 February

1984)

fungal species density and aggregation had changed 6 months after spring burning and raking in a Wisconsin prairie. Fungal species density had increased by 29% in burned relative to raked or undisturbed plots; species density was highest at the soil surface in burned and raked plots, and lowest at the surface in undisturbed plots. Fungal propagules of the same species were less aggregated in burned and raked plots than in undisturbed. These changes imply greater mixing of fungal propagules in soil of burned and raked plots than in undisturbed plots. The physical effects of burning and raking and the properties of fungal spores do not account for the changes. It is argued that soil invertebrates are responsible for the mixing because: (1) at any depth in soil, density of mites and collembola increased concurrently with fungal species density; and (2) path analysis shows that fungal species density is equally associated with microarthropod density and root biomass after burning, but after raking, fungal species Summary-Soil

density was more strongly associated with root biomass than microarthropods.

INTRODUCTION The number of fungal species is highest at the soil surface (Warcup, 1967), and propagules of most

species are dispersed, not aggregated in soil (Dobbs and Hinson, 1960). Most authors explain these observations by arguing that invertebrates transport microbial propagules. Evidence that this distributional pattern is caused by soil invertebrate transport of microbial propagules is two-fold. First, mites, as well as collembola and other insects, are known to transport propagules of terrestrial fungi (Wallace, 1978; Beute and Benson, 1979). Second, soil invertebrates carry viable propagules externally and in their guts (Edwards and Lofty, 1977; Harding and Stuttard, 1974), and they move throughout soil horizontally and vertically enough to effect dispersal (Berthet, 1964; Wallwork, 1976). But the only demonstrations of propagule transport are for earthworms. Pasteur observed that earthworms transport anthrax spores from buried animals to the soil surface (ValleryRadot, 1933). Earthworms dispersed spores of four fungal species throughout boxes of sterile soil (Hutchinson and Kamal, 1956), and moved genetically marked Rhizobium japonicum and Pseudo monas putida downwards through vertical laboratory soil columns (Madsen and Alexander, 1982). What effects on spatial distribution of fungal propagules do soil invertebrates have? We show that change in fungal density and aggregation is associated with change in microarthropod density and argue that there is a causal relationship. MATERIALS AND

METHODS

We studied a prairie in the University of Wisconsin 601

Arboretum (Madison, Wisconsin) that has been burned every other year since 1950 (Cottam and Wilson, 1966). In 1969 nine 100m2 plots were laid out; thereafter in April 1970, 1972 and 1974 the same three experimental plots were burned biennially, the same three were left undisturbed, and 3 others were raked and clipped to remove all surface vegetation. Two 19 cm2 x 9 cm soil cores were randomly collected from all plots on 28 March, 7 May, 7 July and 4 November 1974: these were the source of data in the present study. Four additional soil cores were collected from each plot at the same time from which roots (> 0.5 mm) and fine particulate organic matter (45-500 pm) were sieved after microarthropod extraction (Lussenhop, 1981). The post-fire Ascomycete bloom in this prairie has been studied by Wicklow (1973, 1975) using different plots. Soil cores were placed in individual sterile plastic containers, transported to the laboratory in a portable ice chest, and stored at -7°C. Four gram (dry weight) samples were removed from the surface, 3 cm and 6 cm of each of the 18 soil cores giving 54 samples per collection date. Each 4 g soil sample was placed in a sterile food homogenizer containing 196 ml of 0.2% aqueous agar and mixed for 1 min. Fungal populations were quantified by evenly distributing 1.Oml of an appropriate dilution of the soil suspension over the surface of peptone-dextroseyeast extract agar (Papavizas and Davey, 1959) to which 30mgl-’ of streptomycin and 30mgl-’ of chlorotetracycline were added to restrict bacterial growth. Forty randomly-selected isolates from each sample were subcultured onto potato dextrose agar slants for identification. We derived two kinds of data from cultures after

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JOHN LUSSENHOP and DONALD T. WICKLOW

due to a change in depth distribution of the common species isolated from each treatment. Treatments also affected aggregation of fungal propagules in November, but not in May or July. Aggregation increases with depth in burned and raked plots, and decreases with depth in undisturbed plots (Fig. 1). Thus aggregation is negatively correlated with species density (r = -0.91, P
Treo tment Burn

depth 0 3 6

Rake

A

0 3 6

Undlsfurbed

0 3 6 I

I

I

10 Spectes

derwty

I

1

I

20 1number/g) ( S2/

I

I 5 Aggregation I

of

I

I

I

10

isolales/specles)

Fig. Species density and aggregation of in November, weeks after burning raking. Each bar is on 6 soil samples. Statistical differences species density are described in text. Letters indicate aggregation differences < 0.05) determined a ratio test (David and Moore, 1954). Density of from all treatments (hollow bars) and of were not, is

Fungal propagule dispersal 960

I

Undisturbed

Fine particulate organic matter

0 53

0.88

083

Burn organic

matter

0 66 to.65

Roats

_

Fungal species density

-073

0.76

I

Rake

0.66 f.0.64

Fungal - species density

-0.47

Fig. 2. A path model

603

soil; was lowest in raked plots (Lussenhop, In burned and raked between the and November collections (Lusthe same period when fungal species and aggregation changed. Since and fine particulate for fungal growth and reproduction, we as a result of root growth (Fig. Roots may be the cause of in microarthropod numbers following and movement by greater number of in burned and raked by dispersing fungal propagules. This indirect effect of roots via microarthropods is also included in Fig. 2. boxes and arrows in Fig. 2 are our structural on the basis of we calculated the appropriate path coefficients and used to evaluate direct indirect effects as in the following two paragraphs. Higher fungal is associated in burned and raked but not in 2). Moreover, the indiof roots-the effect via fine particulate and microarthropods-is added to direct effect, the total effects, for burn and 1.24 for rake, are undisturbed conditions (-0.45). (For burn, the total effect equals direct effect, 0.66, plus two indirect of fungal species is in burn to a lesser extent, but not in undisturbed treatment. positive association between roots and microarthropods in in a positive indirect effect, and a total effect (1.22) to the total effect of roots. In the negative association between and microarthropods (reflecting lack of root biomass change in raked plots) results in negative indirect effects a small (0.33) total our data and model, to path analysis, show and microarthropod density to the increase in and roots to increased fungal species

and microarthropod density to in burned, raked and undisturbed plots. Effects of the independent variable on the dependent variables indicated by path coefficients and 95% Student-r confidence (N = 9). Associated is a residual to the square of unexplained variation.

not affected by in any month (Lussenhop, and (c) previous studies at the the plant canopy becomes and thereafter the same in and undisturbed treatments (C. Brown, unpublished M.Sc. of Wisconsin, 1967). We next examined two indirect effects of and raking on but not raking, increased root biomass in top cm

We speculate of fungal propagule dispersal is reduced spore concentration, in turn reduces chance of by pathogenic fungi. Soil management practices or movement .of fungal propagules thus decomposition spread of by a National Science Foundation We thank David Mertz statistical advice, and the University of for help in and permission to the Curtis Prairie. REFERENCES

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JOHN LUSSENHOFand DONALD T. WICKLOW

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