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Soil Eio[. Biochem. Vol. 29, No. 3/4, pp. 409-412, 1997 0 1997 Elsevier Science Ltd. All rights reserved Printed in Great Britain PII: S0038-0717(%)00172-1 003%0717/97 $17.00 + 0.00

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EARTHWORM EFFECTS ON SOIL RESPIRATION IN CORN AGROECOSYSTEMS RECEIVING DIFFERENT NUTRIENT INPUTS M. L. SCHINDLER

WESSELLS,’ P. J. BOHLEN,‘* D. A. MCCARTNEY: S. SUBLER’ and C. A. EDWARDS’ ‘Ohio State University, Department of Entomology, Columbus, OH 45210, U.S.A., *Institute of Ecosystem Studies, Millbrook, NY 12545, U.S.A. and ‘Ohio Agricultural Research and Development Center, Department of Entomology, Wooster, OH 44691, U.S.A. (Accepted

26 June 1996)

Summary-Available evidence suggests that earthworms enhance the mineralization of carbon in soil, but there are few data from field experiments that demonstrate that earthworms increase soil respiration under natural environmental conditions. We measured soil respiration (CO2 flux) during 1993-1994 in 20-m* field enclosures in which earthworm populations had been decreased, increased, or left unmodified (the latter serving as a control). The enclosures were in corn agroecosystems receiving one of three different nutrients: legume cover crop, cow manure or inorganic fertilizer (NH4N0s). Soil respiration was measured in the enclosures by the static diffusion method. Earthworms had significant effects on

soil respiration, but their effects varied seasonally and were influenced by environmental conditions. There were significant differences in respiration rates among earthworm treatments on seven of the 24 sampling dates, and where significant differences did occur, respiration rates were greatest in plots with increased populations and lowest in plots with decreased populations. Most of the significant effects of earthworms on soil respiration were observed during the growing season (June-August) of 1994. A severe drought in the summer of 1993 decreased overall respiration rates relative to 1994, and also inhibited earthworm activity. Soil respiration was significantly greater, during the growing season, in the organically-amended plots than in plots treated with inorganic fertilizer; there were no differences in soil respiration among nutrient treatments in the autumn or in the spring before amendments were added. Our results show that earthworms had a significant influence on soil respiration in the field, but that their influence was seasonal, depended on environmental conditions, and was affected by temporal patterns in C supply. 0 1997 Elsevier Science Ltd

INTRODUCTION

Soil respiration, as measured by the net heterotrophic production of COz, is an important measure of aerobic microbial activity and carbon flux through terrestrial ecosystems (Coleman, 1973). The CO2 produced from the soil results from the mineralization of organic matter, a process in which soil microflora play a dominant role (Satchell, 1983). Earthworms can increase carbon flux from terrestrial ecosystems by contributing directly to soil respiration (Ruz-Jerez et al., 1992) or by stimulating microbial activity (Barois and Lavelle, 1986). Conversely, earthworms can decrease carbon flux by promoting soil aggregation, leading to long term carbon storage in the system (Blanchart, 1992; Q. Ketterings, unpub. thesis, Wageningen Agricultural University, 1992; Lavelle and Martin, 1992). The balance of these processes determines the overall influence of earthworms on net storage or loss of soil carbon in terrestrial ecosystems. *Author for correspondence.

It is important to consider the influence of earthworms on soil respiration in agroecosystems, because of the importance of earthworms to soil fertility and their potential effects on the management of soil carbon. Mineralization of carbon is coupled to the mineralization of other nutrients, which may positively affect plant growth. Different management practices can lead to differences in soil carbon content, and may interact with earthworm populations in ways that have implications for carbon loss or storage in agricultural soils. Microcosm studies have shown that earthworms tend to increase soil respiration, despite a concurrent decrease in microbial biomass (Wolters and Joergensen, 1992; Bohlen and Edwards, 1995). Although microcosm experiments have been useful in providing a detailed understanding of earthworm influences on C mineralization under controlled environmental conditions, field experiments are essential to assess the long-term influence of earthworms on the temporal patterns of C flux under variable environmental conditions. Field experiments are also needed to determine the net influence of earth409

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M. L. Schindler Wessells et al.

on C storage and loss in terrestrial ecosystems. Our objective was to investigate the influence of different earthworm population densities on soil respiration in corn agroecosystems which received inorganic or organic nutrient inputs. worms

MATERIALS

AND METHODS

Field site

The experiment was conducted at the Ohio Agricultural Research and Development Center in Wooster, Ohio. Plots were established on a flat, well drained Fragiudulf soils of the Canfield series, which are well-drained silt loams with an impenetrable fragipan at 40-75 cm and a pH of 6.3. Twelve maize (Zea mqs) plots were established in 1992, each receiving annually one of three possible nitrogen inputs: animal manure, hairy vetch as a leguminous winter cover crop, or ammonium nitrate (NH4N0s) commercial fertilizer. Each nutrient treatment was replicated four times within the field in a randomized complete block design. Each replicate plot contained three 20-m2 enclosures in a split plot design in which earthworm populations had been either decreased, left unmodified, or increased. In spring, 1994 there was about a 75% reduction in earthworm numbers in the enclosures with reduced populations, whereas there was 50% increase in earthworm biomass, with no significant increase in earthworm number, in enclosures to which earthworms had been added. Species of earthworms in the plots were: Aporrectodea tuberculata (Eisen), Lumbricus terrestris (L), L. rubeflus (Hoffmeister), and A. trupezoides (Duges). Details of the earthworm population manipulations and nutrient additions can be found in Bohlen et al. (1995). Respiration measurements

Soil respiration was measured by the static diffusion method (Brown and MacFayden, 1969) using COz traps containing a 25 ml NaOH solution. Each enclosure within each replicate plot contained two respirometers consisting of a 15-cm dia PVC pipe driven 5 cm into the ground. The CO2 traps were Table 1. Results of the repeated-measures

placed into the respirometers, which were covered with a rubber cap and sealed with a metal clamp, for 24-h incubation periods. The amount of COz evolved during the incubation period was determined by titrating the NaOH traps to neutrality with HCl after adding 3 N BaC12 (Anderson, 1982). Soil respiration was measured on a total of 24 dates from April 1993 to November 1994. The data were analyzed by a repeated measures analysis of variance for a split plot design. There was a significant earthworm x date interaction in the repeated measures analysis, so individual analysis of variance tests were done for each nutrient treatment and sample date (SAS Institutes, 1990). Differences among means for the different earthworm treatments were determined with Tukey’s HSD mean separation test (P < 0.05).

RESULTS

There was no overall significant effect of earthworms on soil respiration in the repeated measures ANOVA (Table 1). However, there was a significant interaction between date and earthworm treatments; separate ANOVA tests for each date revealed that the earthworm treatments had a sig-. nificant effect on soil respiration on seven of the 24 sampling dates (Fig. 1). In April, 1993, plots with increased populations had higher respiration than plots with decreased populations, and in early May, plots with increased populations had significantly greater respiration than control plots. In September 1993 soil respiration was significantly lower in plots with decreased populations than in control plots. Overall effects of earthworms on soil respiration were greater in 1994 than in 1993. In 1994, plots with increased earthworm populations had significantly greater respiration rates than did plots with decreased populations throughout June and July. There was a significant interaction between nutrient source and date that can be explained by differences in the seasonal patterns of CO* flux among nutrient treatments. Overall, respiration rates were greater in the organically-fertilized plots than in those which received NH4N03 fertilizer. Differences

analysis of variance for all sampling

source

DF

Mean square

Block Nutrient treatment (N) Error (nutrient treatment) Earthworm treatment (E) NxE Error (earthworm treatment) Date (D) DxN DxE DxNxE Error

3 2 6 2 4 18 23 46 46 92 621

0.04788 0.73019 0.04615 0.17960 0.00918 0.00927 3.63666 0.01421 0.01085 0.00536 0.00569

‘F-values

marked with an asterisk are statistically

significant

(P < 0.05).

dates during

1993-1994 F value”

15.9; 1.94 0.99 638.65* 2.5’ 1.91* 0.94

Earthworm effects on soil respiration

AMJJASONDJFMAMJJASOND

Month(1993-1994)

Fig. 1. The degree to which CO2 output from enclosures with increased or decreased earthworm populations differed from enclosures with unmodified populations during the study period. Asterisks indicate days on which the highest and lowest values were significantly different (P < 0.05). In each of these cases, the intermediate value did not differ significantly from the two extremes. between the inorganic and organically-fertilized plots were greatest during the growing season, following the incorporation of the nutrient amendments into the soil. Differences between the nutrient treatments were negligible in the spring of both years, prior to fertilization, and again in the autumn. Time of year (date) had a significant effect on respiration rates with rates being greatest in the growing skason (May-October), and greater overall in 1994 than in 1993 (Table 1, Fig. 2).

DISCUSSION

Earthworms had a significant influence on soil respiration in our field experiment, but their effect varied seasonally and was influenced strongly by environmental conditions. The clearest results were for the 1994 growing season, immediately after spring tillage and incorporation of nutrient amendments. In both years, differences in respiration among earthworm treatments were greatest over the summer months, when C resources were abundant and the biological activity high, with differences diminishing in the autumn. Thus, seasonal patterns

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I

I

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Month(1993-1994) Fig. 2. The effect of the different nutrient amendments on total soil respiration during the study period. Values for each nutrient amendment are averaged over all earthworm treatments.

411

in the effects of earthworms on respiration may be due, in part, to temporal patterns in resource availability. From early June to August 1994, the C flux was significantly and consistently greater in enclosures with increased earthworm populations than in those with decreased populations, and was greater than in the control enclosures during the same period (Fig. 1). In the 1993 growing season, by contrast, soil respiration in enclosures with increased populations was not greater than in those with decreased populations and was actually lower than in control plots on several sample dates. The main difference between the two growing seasons was the severe drought that occurred in 1993. The drought not only reduced overall soil respiration rates, which were much lower in 1993 than in the 1994 growing season (Fig. 2), but also inhibited earthworm activity. Adequate rainfall in the growing season of 1994 stimulated earthworm activity, enabling earthworms to exert more influence over total soil respiration during that period. The increases in soil respiration due to earthworms resulted either from the direct contribution of earthworm respiration to total heterotrophic respiration or from stimulation of microbial respiration by etrthworm activity. Earthworms generally contribute only about 5-6% to the overall heterotrophic respiration in soil (Barley and Kleinig, 1964; Satchell, 1967; Ruz-Jerez et al., 1992; Edwards and Bohlen, 1996), but have been reported to account for up to 30% of the total heterotrophic respiration, during winter and early spring, in a notillage agroecosystem with large earthworm populations (Hendrix et al., 1987). Earthworms can also stimulate microbial respiration. Earthworms increased microbial respiration by IO-15% in a laboratory incubation of coniferous forest floor material (Haimi and Huhta, 1990). In a pot study, in which earthworms significantly increased decomposition of grass and clover residues, it was estimated that half of the increase in decomposition was due to stimulation of microbial activity (Barley and Jennings, 1959). Such increases in microbial respiration can occur despite an accompanying decrease in overall microbial biomass, indicating that earthworm activity can lead to a smaller, more metabolically active microbial biomass (Wolters and Joergensen, 1992). We have evidence of this phenomenon in our field experiment, in which microbial biomass-N was generally highest in those plots with decreased earthworm populations (Blair et al., this volume), but soil respiration was sometimes lowest in those plots. The increases in soil respiration and concomitant decrease in microbial biomass due to earthworms was also observed in a microcosm experiment designed to simulate the field treatments described in this study (Bohlen and Edwards, 1995).

M. L. Schindler Wessells et al.

412

The type of nutrient added to the plots had a significant influence on soil respiration, with the plots that received organic nutrients having higher respiration rates than those that received inorganic fertilizer (Fig. 2). This difference occurred during peak respiration following the incorporation of the fertilizers in late spring. The extra C source added with the organic fertilizers provided fuel for microbial respiration, but the stimulatory effect of this added C did not persist into the late autumn and did not carry over to the following spring. Corn residues added to the plots in the autumn accounted for the largest C source for decomposers in these systems and apparently overrode any lingering difference due to the organic nutrient inputs. Our results indicate that the influences of earthworms on soil respiration may lead to a long-term carbon loss from agroecosystems, unless there is a concomitant mechanism to increase carbon storage, such as an increase in plant growth or protection of carbon in stable soil aggregates. However, seasonality in the influences of earthworms on carbon flux, and the dependence of such effects on variable environmental conditions, suggest that the relation of earthworms to carbon flux is complex. The net outcome of earthworm activity on carbon storage and loss is uncertain. Our data indicate that the influence of earthworms on carbon flux depends not only on environmental conditions, but also on the temporal patterns in carbon supply. The influence of earthworms on carbon flux is an important biological phenomenon which needs to be investigated further, in field experiments, if we are to assess fully the importance of earthworms as regulators of carbon storage and loss in terrestrial ecosystems. REFERENCES

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