Foraging by deep-burrowing earthworms degrades surface
soil structure of a ¯uventic Hapludoll in Ohio
W.D. Shuster
a, S. Subler
b, E.L. McCoy
a,*aSchool of Natural Resources, The Ohio State University, OARDC, Wooster, OH 44691, USA bSoil Ecology Laboratory, Department of Entomology, The Ohio State University, Columbus, OH 43210, USA
Received 11 December 1998; received in revised form 24 September 1999; accepted 10 January 2000
Abstract
The presence of deep-burrowing earthworms can affect soil structure and in®ltration, therefore in¯uencing agricultural productivity. We investigated the effects of deep-burrowing earthworm species on soil structure at the surface of chisel-plowed or ridge-tilled cropping systems in Pike County, OH, planted to corn (Zea mays L.). Earthworm populations were experimentally manipulated in ®eld enclosures by adding predominantly deep-burrowingLumbricus terrestrisL., or leaving enclosures unmodi®ed in each tillage system. In 1995, after 2 years of bi-annual additions, we measured surface residue cover, dry sieved aggregates (DSA)- and water-stable aggregates (WSA), and carbon and nitrogen concentration of aggregates by size class, in each treatment combination. Also, in 1998, we used tension in®ltrometry to examine crusting effects at the soil surface among earthworm treatments in the chisel-plow treatment. Earthworm additions yielded increased density and biomass ofL. terrestristhan ambient controls, and to a greater extent in the ridged corn±soybean (Glycine maxL. Mess.)± wheat (Triticum aestivum L.) (CSW) than corn±soybean (CS) rotation. Percentage residue cover in CS cropping decreased with earthworm additions. Earthworm additions decreased the geometric mean weight diameter (GMWD) of DSA and WSA in chisel-plow treatment compared to no additions. Earthworm additions in¯uenced carbon-to-nitrogen (C/N) ratios for smaller DSA and WSA. Water-stable aggregate C/N decreased with size class. The overall effect of earthworm additions was an increase in deep-burrowing earthworms, a decrease in surface residue cover, and more pronounced crusting, which decreased mesopore conductivity.#2000 Elsevier Science B.V. All rights reserved.
Keywords:Soil aggregation; Earthworms; Crop residue; Crusting; Carbon
1. Introduction
Earthworms comprise a major proportion of the total invertebrate biomass in temperate, terrestrial ecosystems (Edwards and Bohlen, 1996), and can
in¯uence soil chemical, biological, and physical pro-cesses. In this study, we address the possibility that certain earthworm species may impact on surface soil aggregation, with implications for surface crusting and subsequent erosion.
Earthworms have been observed to increase the number and water stability of macroaggregates, and improve in®ltration (Mackay and Kladivko, 1985; Blanchart, 1994; Ketterings et al., 1997). Historically, *Corresponding author. Tel.: 1-330-263-3884; fax:
1-330-263-3658.
E-mail address: [email protected] (E.L. McCoy)
the presence of earthworms is associated with improvements in, rather than degradation, of soil tilth and cropping conditions. The anecic species Lumbri-cus terrestrisL. is active at the soil surface where it forages, and below the surface where burrows extend the earthworm's in¯uence deep into the soil pro®le. Anecic earthworms have been shown to affect soil structure by foraging (Shaw and Pawluk, 1986), bur-rowing (Pitkanen and Nuutinen, 1997), and casting (Shipitalo and Protz, 1988). By foraging and creating middens, deep-burrowing earthworms change the spa-tial distribution of coarse organic matter at the soil surface (Shaw and Pawluk, 1986; Gallagher and Wol-lenhaupt, 1997; Pitkanen and Nuutinen, 1997; Wil-loughby et al., 1997). Moreover, in a corn cropping system, Subler and Kirsch (1998) found that 96% of total coarse organic matter in surface soil present after the fall corn harvest was concentrated around earth-worm middens by the early spring.
Middens are highly localized patches of soil, casts, and coarse organic matter in various stages of proces-sing. As foraging activities proceed, earthworms can decrease the area of soil surface protected by residual coarse organic matter. Without residue cover, the soil surface is vulnerable to degradation by increased exposure to weathering (Freebairn et al., 1991) and may form surface crusts or seals. Also, earthworms can process organic matter, producing unique bypro-ducts like burrow linings and casts which contain temporary or transient aggregate binding compounds (Tisdall et al., 1978; Shaw and Pawluk, 1986). These carbon compounds can bind soil particles together, thereby reducing the effects of water slaking and inhibiting crust formation. Therefore, given appropri-ate organic matter resources, earthworms can in¯uence soil aggregation. However, another effect of residue consolidation is to increase the spatial heterogeneity of carbon resources at the soil surface and within the soil matrix. Yet, earthworm foraging activities result in a patchy distribution of the organic resources neces-sary for the production of carbonaceous transient binding agents (Tisdall et al., 1978). This could limit the availability of these binding agents at small spatial scales, and would therefore in¯uence the formation of soil aggregates that are resistant to slaking. The con-sequences oforganicmatterforagingbydeep-burrowing earthworms could include the exposure of a consider-able amount of soil surface area to increased weathering.
The conditions under which deep-burrowing earth-worm species contribute to the improvement or degra-dation of surface soil structure are not well understood, nor widely studied. The purpose of this study was to assess earthworm effects on formation of surface crusts. We measured the size-distribution, stability and carbon and nitrogen concentrations of soil aggregates, and unsaturated hydraulic conductiv-ity of crusted and non-crusted surfaces. These mea-sures were analyzed for indications of whether earthworm additions have the potential to change soil structure in row-crop production systems typical to the midwestern US.
2. Materials and methods
2.1. Soil, climate and cropping systems
The study site was located at the Ohio Management Systems Evaluation Area (MSEA) (Ward et al., 1994) near Piketon, OH (398020N, 838020W). Soils at this ¯ood plain site are predominantly Huntington silt loam (US taxonomy: ®ne-silty, mixed, mesic ¯uventic Hapludoll; FAO classi®cation: Haplic Chernozem), with landscape slopes ranging between 2 and 5%. A typical particle-size analysis of these soils yield 210 g kgÿ1 sand (50±2000mm), 550 g kgÿ1 silt (2± 50mm), and 240 g kgÿ1clay (<2mm) (Nokes et al., 1997). Soil organic carbon concentrations average 15.8 g kgÿ1 in the surface 150 mm. Average annual precipitation at this site is 900 mm, with 570 mm of this occurring over the growing season. On an average, there are 170 days per year without a killing frost (Nokes et al., 1997).
rebuilt on the second cultivation. Wheat was planted on and between ridges remaining from the soybean crop. Vetch was planted after wheat harvest, and killed with glyphosate (1.75 l haÿ1) before planting corn was planted the next season. Each management system was replicated (n3) in 0.4 ha treatment in a complete randomized block design.
2.2. Earthworm treatments
In November 1993, four 6.16.1 m2 enclosures were constructed in each replicate cropping system treatment (Subler et al., 1997). The enclosures con-sisted of corrugated plastic sheeting inserted into the ground to a depth of approximately 50 mm, with 250 mm extending above the soil surface. In each replicate cropping system treatment, one pair of enclo-sures was designated for earthworm population assessments, while the other pair was used for soil sampling. For each pair of enclosures, one received earthworm additions (addition), and the other enclo-sure, to which no earthworms were added, was estab-lished as a control (ambient). Each spring and fall, earthworms were added at a rate of 100 individuals per square meter. These additions were started in the fall of 1993, and continued through the fall of 1997. Earthworms used in addition treatments were col-lected from a no-till corn ®eld in Columbus, OH. These earthworms were predominantly immature and adultL. terrestris.
Earthworm populations were assessed at the begin-ning of this study, from 28 to 30 March 1995. In each enclosure, soil was removed from four pits (each 380380150 mm3 deep). This soil was then hand sorted for earthworms. Deep-burrowing earthworms were driven out of their burrows by saturation of the excavated surface at 150 mm with a formalin solution. Earthworms surfacing within one half-hour were col-lected. All earthworms were preserved in formalin, and retained for identi®cation. Earthworms were iden-ti®ed to the levels of species (adults) or genus (juve-niles) (Schwert, 1990). Earthworm samples were placed in tared 20 ml scintillation vials, dried for 24 h at 608C, weighed, then ashed in a muf¯e furnace at 5008C, and weighed again. The difference between the dry and the ash weight is the ash-free dry weight (AFDW), and is a measure of earthworm biomass, corrected for soil in the earthworm gut.
2.3. Assessment of surface residue cover
To assess percentage residue cover at small spatial scales, we used a modi®ed line-transect method. A 35 mm camera loaded with Kodak Ektachrome 200 (ASA) ®lm was used to record four images covering a 1.20.8 m2 area, 1.5 m from the soil surface, at randomly selected locations, in each cropping earthworm treatment combination. A meter stick was placed on the soil surface for each image, and served as a reference scale. These images were pro-jected onto a white surface, and the slide projector zoom control adjusted so that the meter stick appear-ing in each image was a meter long on the projected image. We then placed a meter stick on the image and counted the cumulative centimeters intercepted by pieces of residue, where the cumulative number of counts was equal to the percent residue cover. To position the meter stick on the image, we used a random number table to determine horizontal and vertical distance from the center of the image, and a tilt angle in degrees. We used ®ve sets of coordinates to make ®ve counts on each image.
2.4. Soil sampling and analysis
In the spring of 1995, undisturbed soil cores, each 105 mm in diameter and 150 mm deep, were taken from the surface soil at randomly assigned locations in each earthworm treatment, two each, at in-row (IR) and between-row (BR) positions. This arrangement yielded a total of 24 observations, i.e. three replica-tionstwo cropping systems (CS, CSW)two earth-worm treatments (addition, ambient)two samples for each row position (IR, BR). Bulk soil samples to 150 mm depth were also collected with soil texture determined by the pipette method (Gee and Bauder, 1986). Gravimetric antecedent soil water contents were determined to 150 mm depth.
The ®eld-moist 150105 mm2soil cores were care-fully broken apart along natural ®ssures and rooting channels. Coarse organic matter was removed in this process. Field-moist aggregates were passed through a 10 mm sieve, and air-dried.
Samples were shaken at 60 cycles per second for 3 min with a 2 mm amplitude. The geometric mean weight diameter (GMWD) (Hillel, 1982) of aggre-gate distributions was calculated from weights of aggregates retained in each size class with the equation:
wherewiis the weight of aggregates in a size class of average diameterxi, over the size classesi1,. . .,n. To determine total carbon (C) and nitrogen (N), a 2 g sub-sample was taken from each size class, pul-verized in a ball-mill and analyzed by dry combustion on a Carlo-Erba 1500 C/N Analyzer (Carlo-Erba Stru-mentazioni, Milan, Italy).
The remaining air-dry aggregates were separated through 8 and 5 mm sieves to obtain a 50 g sub-sample of 5±8 mm particles. These larger particles were examined for water stability by wet sieving samples in a nest of sieves which were mechanically raised and lowered in a column of water (Yoder, 1936). Air-dry aggregates were spread out on a 5 mm sieve, wetted by capillary rise, then sieved at 30 oscillations per minute for 20 min. This process separated larger aggregates into 5±8, 2±5, 1±2, 0.5±1, 0.25±0.5, <0.25 mm size classes of water-stable aggregates (WSA). WSA in each size class were transferred to tared beakers, oven-dried at 1058C and weighed. We calculated percentage WSA retained in each size class and water-stable GMWD. A 2 g sub-sample was taken from each size class of WSA, pulverized in a ball-mill and analyzed for total C and N concentrations. The remainder of each sample was dispersed with a solution of sodium hexametaphosphate to determine percentage sand in each size class of WSA.
2.5. Determination of unsaturated hydraulic conductivity
In 1998, we used tension in®ltrometers ®tted with 80 mm bases (Soil Measurement Systems, Tucson, AZ) to measure water ¯ux at ÿ5, ÿ30, ÿ60, and ÿ150 mm heads on crusted (undisturbed) and non-crust (non-crust removed to 20 mm depth) surfaces. Only two replications could be used in this experiment, due to ¯ooding in one of the blocks. After preparation of the soil surface, an 80 mm (i.d.) ring was pressed
3 mm into the soil. To estimate contribution of sur-face-connected macropores, this ring was ®lled with 10 mm water and the in®ltration time was recorded. Also, this protocol enabled the soil surface to be pre-wetted to reduce time-to-bubbling at high tensions in dry soils. After water had in®ltrated, surface-con-nected macropores were covered with 150-mesh nylon fabric to prevent occlusion from contact material or erosion of macropore walls. We then applied a2 mm layer of ®ne sand contact material, saturating the sand with water from a spray bottle. The ring was removed, revealing the sand lens on which the tension in®lt-rometer was placed. In order to minimize the potential for air entrapment in smaller pores, tensions were run highest to lowest (150±5 mm suction head), and for at least 25 min at each tension. Measurements on crusted and non-crusted soil surfaces were made at three randomly chosen positions for each earthworm treat-ment in CS treattreat-ments only. In an attempt to measure in®ltration at 0 mm, tension in®ltrometers were run at a slightly negative head of approximatelyÿ5 mm. We did this to minimize the effects of small variations in elevation, which can result in positive pressure heads. These positive pressure heads, albeit small, appeared to cause ¯ooding at the in®ltration site, preventing reliable measurements of ¯ux.
2.6. Calculations and statistics
Tests for treatment effects were conducted by mixed-model analysis of variance (ANOVA) proce-dures. These tests were used to determine signi®cance of main effects (block, earthworm and cropping sys-tem) and their interactions. The cropping system effect was tested by comparing its mean square with crop-ping systemblock as the error term. Earthworm and earthwormcropping system effects were tested for signi®cance with cropping systemearthworm -block as the error term. In order to equalize sample variances before running analysis of variance proce-dures, a log10 transform was applied to earthworm
software (SAS Institute, 1989) was used for all sta-tistical analyses in this study.
The procedure of Logsdon and Jaynes (1993) was used to calculate unsaturated hydraulic conductivity. The steady state in®ltration rateQ(mm3sÿ1) atÿ30, ÿ60, and ÿ150 mm was ®t to the equation:
Q
pr2
K 0exp ah 4K 0exp ah pra
where r is the in®ltrometer radius (mm) and h the negative head (mm). Non-linear regression was employed to obtainK(0) (mm sÿ1), a ®tted saturated hydraulic conductivity anda(mmÿ1), a ¯ow-weighted porosity index. These parameters were used to esti-mate hydraulic conductivity at ÿ30, ÿ60 and ÿ150 mm with the equation:
K h K 0exp ah
Unsaturated hydraulic conductivity estimates were log10transformed prior to statistical analysis. In this
study, we de®ne mesopore conductivity as the differ-ence between log-transformed hydraulic conductivity atÿ30 andÿ60 mm head. Similarly, micropore con-ductivity is de®ned as the difference between log-transformed hydraulic conductivity at ÿ60 and ÿ150 mm head.
Tests of signi®cance were performed on unsaturated hydraulic conductivity by analysis of variance with block, earthworm and surface treatment (crust and non-crust) as main effects. Earthworm and surface crust treatment effects were tested with the residual error as the error term.
3. Results and discussion
3.1. Earthworm additions
Earthworm additions increased the density of the deep-burrowing L. terrestris in corn±soybean (CS) and corn±soybean±wheat (CSW) rotations by 2.9 and 16.0 individuals per square meter, respectively, over ambient treatment (Table 1). There was also a signi®cant interaction between earthworm treatment and rotation for both earthworm density and AFDW. The average biomass of L. terrestrisindividuals was 237 mg per individual for CS, and 397 mg per indi-vidual for CSW cropping.
Deep-burrowing earthworm populations were suc-cessfully established in addition treatment, with higher earthworm biomass supported by CSW crop-ping than by CS. The average biomass ofL. terrestris individuals varied with rotation, and indicated thatL. terrestrisindividuals were larger in CSW than in CS. This may be a result of differences in the amount of and variety of residue in each system, and the extent to which these were foraged by earthworms. Moreover, the greater numbers of L. terrestris individuals in the CSW were probably due to the overall greater amount of food, as residue inputs, in the CSW rotation. In similar tillage systems, Jordan et al. (1997) found similar differences in earthworm populations with about one-®fth the density of earthworms in CS than CSW cropping systems. These differences were attributed to tillage-induced earthworm mortality, although Jordan et al.
Table 1
Means of density and AFDW for deep-burrowing (i.e. soil depth <150 mm)L. terrestrisearthworms under different crop rotations for spring 1995
Rotation Earthworm treatment Earthworm density (individual per square meter) AFDW (mg mÿ2)
CSa Ambient 0 0
Addition 2.9 689
CSWb Ambient 0 0
Addition 16.0 6354
Treatment p>F p>F
Analysis of variance Rotation <0.01 0.09
Earthworm <0.01 0.03
Rotationearthworm <0.01 <0.01
(1997) handsorted soil for earthworms to 150 mm depth, ®nding noL. terrestris.
3.2. Surface residue cover and distribution
The addition of deep-burrowing earthworms to the CS rotation led to a 44% decrease in surface cover compared with ambient treatment in CS cropping (Table 2). Furthermore, the foraging activity of deep-burrowing earthworms decreased percentage residue cover from 34 to 19 (Table 2). This level of percent residue cover is below the threshold of residue cover (i.e. 30%) (Nokes et al., 1997) for adequate protection of erodible soils, established by the United States Department of Agriculture, Natural Resource Conservation Service. This decrease with earthworm additions was characterized by the piling of residues in and around earthworm midden structures, with a concomitant clearing of the soil surface. Also, the CSW rotation had a much higher percentage residue cover than CS.
Over the period 1991±1995, Nokes et al. (1997) measured percent plant residue remaining on the soil surface before planting using a line-transect method. The line-transect method involves counting the cumu-lative number of 30 cm intervals intercepted by resi-due, with a 30 m tape. Based on this sampling protocol, and over the time period 1991±1995, surface residue coverage was signi®cantly greater in CS than in CSW. The rotation effect on residue compared with that of the present study is surprising considering the measurements were conducted at the same location. Yet, in our experiment, percent residue cover was
assessed at much smaller scales. These measurements would be dependent on small-scale variation such as earthworm activity, and localized yield differences. Although there was signi®cant variation among treat-ment blocks, the analysis of variance indicates that deep-burrowing earthworm activity had a stronger in¯uence on residue cover than this between-block variation.
3.3. Distribution and stability of soil aggregates
Earthworm additions signi®cantly (p0.03) decreased the GMWD of DSA (Table 2) in chisel-plowed, CS treatments. The GMWD of DSA was not affected by earthworm additions in the ridge-tilled, CSW treatments where DSA GMWD was similar to that for the ambient earthworm treatment for CS cropping. A decrease in GMWD is equivalent to a shift in the aggregate size distribution towards smaller aggregate sizes.
Earthworm additions in CS cropping signi®cantly (p0.08) reduced water-stable GMWD. However, WSA GMWD for CSW cropping was not affected by earthworm additions (Table 2). Also, the GMWD of WSA in the CSW treatment was similar to that for the ambient earthworm treatment for CS cropping. There was a slight, non-signi®cant, decrease in the antecedent soil water content in the earthworm addi-tion treatments at the time of sampling (Table 2).
Other workers (Mackay and Kladivko, 1985; Ket-terings et al., 1997) found that earthworm additions improved soil structure by increasing the size and stability of soil macroaggregates. Although
observa-Table 2
Residue cover, indices of aggregation, and antecedent soil water content (ASWC) as in¯uenced by crop rotation and earthworm treatments (NS: not signi®cant)
Rotation Earthworm treatment Residue cover (%) DSA GMWD (mm) WSA GMWD (mm) ASWC (g kgÿ1)
Corn±soybean (CS) Ambient 34 1.43 0.93 180
Addition 19 1.12 0.73 140
Corn±soybean±wheat (CSW) Ambient 99 1.42 0.94 190
Addition 91 1.32 0.84 160
Treatment p>F p>F p>F p>F
Analysis of variance Block 0.06 NS NS NS
Earthworm 0.02 0.03 0.10 NS
Rotation <0.001 0.08 NS NS
tions were made at similar times after earthworm addition treatments were implemented (ca. 1 year), the initial conditions and the manner in which earth-worm additions were administered differed between that of Ketterings et al. (1997) and the present study. Ketterings et al. (1997) conducted their study in a no-till ®eld with high initial populations ofL. terrestris; earthworm treatments were not signi®cantly different and contained up 365 earthworms per square meter, of which 52% wereL. terrestris. Moreover, Ketterings et al. (1997) used handsorting of soil to determine the composition of earthworm communities, which may have undersampled the deep-burrowingL. terrestris. These experimental conditions contrasted with our site, which had no initial L. terrestris populations, and lower L. terrestris populations in the addition treatment. Although the amount of coarse organic matter in Ketterings et al. (1997) did not differ across earthworm treatments, this is not a measure of percent surface cover. Therefore, any potential improvements in soil structure and could depend on the relationship betweenL. terrestris populations and the amount of residue produced by the various cropping systems, thereby in¯uencing the nature and extent of changes in soil structure in these two ®eld experiments.
Additions of L. rubellus were shown to improve macroaggregate stability (Mackay and Kladivko, 1985) of an aquic Argiudoll, which had been amended with various types and amounts of incorporated crop residue. WhileL. rubellusmay have been effective in reducing the amount and size of incorporated residue recovered at various time intervals over nearly 2 months, change in surface residue cover was not studied. Also, the increased soil±residue contact resulting from the incorporation protocol would enhance the breakdown of residue. Furthermore, the speciesL. rubellusandL. terrestrisbelong to distinct ecological groups; the former is considered an epigeic species, and the latter an anecic species. Epigeic species are not as aggressive as anecic species in their foraging habits, and tend to form smaller middens from surface residue. Moreover,L. terrestrisare gen-erally more aggressive in their consolidation and consumption of raw residues, compared withL. rubel-lus, whose in¯uence is limited by its smaller size and shorter longevity (Edwards and Bohlen, 1996). In contrast to the present study, differences in the experi-mental setting, placement of residues, and earthworm
species were probably major in¯uences on the pre-servation of soil structure.
3.4. Distribution of C and N in soil aggregates
In both the chisel and ridge-till, earthworm addi-tions decreased mean DSA C concentraaddi-tions for all size classes by 21±25% (Table 3); but these decreases were not signi®cant. There was little variation in N concentration among DSA size classes, although slight, non-signi®cant decreases were observed with earthworm additions (Table 3). Earthworm additions signi®cantly (p<0.05) increased the C/N ratio of DSA in the <0.106 mm size range by 6% in CS, and 2% in CSW.
Overall, WSA C and N concentrations were greater than in DSA (Table 3), and tended to be lower in the CS cropping system than CSW. Also, the WSA C/N ratio was greater in CSW cropping systems compared with that of CS (Table 3). Earthworm additions in the CS rotation signi®cantly (p<0.05) reduced by 11% the C/N ratio of the 0.25±0.5 mm WSA size range. Decreases in WSA C/N ratio were positively corre-lated (p<0.01) with WSA size range for both CS and CSW rotations.
Water stability of soil aggregates is strongly in¯u-enced by the C content of the dry sieved material (Ketterings et al., 1997). In the present study, WSA resulting from dry sieved material were comparatively enriched in C. Further, these WSA had lower C/N ratios than did their parent dry sieved material and consequently the C was more labile. This was parti-cularly true as WSA size decreased. Lower C/N ratios may also indicate that the C pool is more processed and may act as binding agents, thereby preserving soil structure (Ketterings et al., 1997). Also, by eliminating a source of aggregate-stabilizing C compounds, removal of coarse organic matter from the surface may have exacerbated the degradation of aggregates. However, the extent or permanence of these stabiliz-ing compounds cannot be evaluated due to the short-term nature of this experiment. Furthermore, more work is needed to determine the role of carbonaceous substances in aggregation processes under various cropping conditions.
and N concentrations in aggregates. However, the destabilization of macroaggregates yielded an aggre-gate distribution of predominantly smaller, WSA, which were enriched with labile C. Furthermore, the type of C contained in these aggregates may indicate the existence of a new pool of relatively labile, unprotected C. Moreover, the fate of this C pool could be better characterized by mineralization studies, which include incubations of both stable and unstable aggregates.
Also, the earthworm treatment effects observed for smaller size classes of aggregates may have been confounded by the presence of casts, which were rich in C and N compounds. The availability of this more labile cast material, coupled with an enhanced micro-bial biomass due to earthworm activity (Marinissen and de Ruiter, 1993), could increase the concentration of microbial byproducts in soil aggregates. Although earthworm populations were much higher in CSW cropping than CS, we found no signi®cant difference in C/N ratio among cropping systems. This may indicate that casts were not a factor.
3.5. Unsaturated hydraulic conductivity
We applied tension in®ltrometry to better charac-terize the hydraulic properties of surface crusts in the CS treatments, especially in terms of determining the signi®cance of crust formation in the earthworm treatments. We found that earthworm additions resulted in increased mesopore conductivity compared with that of the ambient treatment (Table 4). Yet, the increase in mesopore conductivity from crust removal was greater with earthworm additions than for the ambient conditions. This suggests a more pronounced crusting, disrupting mesopore conductivity, in the earthworm addition treatments than in the ambient treatments. Further, micropore conductivity with sur-face crust intact was greater in the addition treatment compared with that of the ambient treatment appar-ently due to a shift toward small pore sizes in the addition treatments.
The signi®cant decrease in mean aggregate size noted earlier would have resulted in a concomitant decrease in mean inter-aggregate pore size, and
Table 3
Means and analysis of variance for total carbon and nitrogen concentration (g kgÿ1) and C/N ratio for DSA and WSA
Rotation Earthworm
treatment
DSAa WSA
5±8 mm 2±5 mm 1±2 mm 0.5±1 mm 0.25±0.5 mm
Carbon
CS Ambient 16.4 18.0 18.8 18.8 17.1 16.1
Addition 12.1 14.4 16.3 16.1 12.0 10.3
CSW Ambient 20.0 21.6 20.6 21.1 18.1 18.0
Addition 15.0 18.6 19.2 20.0 17.7 15.8
Nitrogen
CS Ambient 1.2 1.8 1.9 1.9 1.7 1.6
Addition 0.9 1.9 2.0 4.3 2.0 1.8
CSW Ambient 1.7 1.6 1.7 1.8 1.6 1.5
Addition 1.2 1.6 1.7 1.7 1.3 1.4
C/N ratio
CS Ambient 13.7 9.9 9.7 9.9 9.2 9.3
Addition 13.4 9.2 9.7 9.3 8.2 7.5
CSW Ambient 12.0 11.0 10.4 10.5 9.8 9.9
Addition 12.2 11.3 11.0 10.9 10.8 10.0
Treatment p>F p>F p>F p>F p>F p>F
Analysis of variance (C/N ratio) Rotation NS NS NS NS NS NS
Earthworm 0.02 NS NS 0.04 NS 0.03
aWith the exception of the certain size ranges in DSA, there were no signi®cant differences within a rotationearthworm treatment
consequently, a ®ner pore structure. Further, the degra-dation of larger aggregates often leads to the formation of crusted layers (Ela et al., 1992; Fox and Le Bis-sonnais, 1998) which can occlude mesopores and macropores. An additional consequence of the more pronounced crust effect observed in the treatments where earthworms were added would be the signi®-cant increase in micropore conductivity.
3.6. Overall discussion and implications
Given typical midden densities of 20±100 middens per square meter (Subler and Kirsch, 1998) the pro-portion of soil area under middens is fairly small. However, unless midden density or sampling size is extremely high, a random sampling can underestimate the in¯uence of these structures. In this study, random sampling may have favored the measurement of non-midden soil where C sources would appear to have been depleted, compared with those of midden soil which had high concentrations of carbonaceous mate-rial. Samples taken closer to one another yield similar properties compared with samples taken farther apart. Further, depending on this scale of spatial variation, an appropriate ®ne-scale sampling grid would better characterize soil properties, and account for this spatial heterogeneity.
In the present study, the paradox is that one con-sequence of deep-burrowing earthworm activity may have been to locally increase the C content of the surface soil, while depleting C resources in the bulk (non-midden) soil. Furthermore, the addition of
deep-burrowing earthworms structured or piled surface residue cover, compared with ambient distributions. This small-scale variation would not be entirely accounted for in larger-scale assessments. Another example of this scale dependence is that both meso-pore and macromeso-pore conductivity would also be affected by the scale at which tension in®ltration measurements were made, and the frequency of these measurements in a given area. Measurements of ¯ux at different tensions were made along random transects which may, or may not have been, near middens. Although our approach to measuring unsaturated hydraulic conductivity did not explicitly consider variance due to distance from middens, it is suggested that high mesopore and macropore conductivity events were related to the presence of middens. An approach to sampling which incorporates higher sam-pling frequencies on a uniform grid, at set distances from a midden, might better clarify the extent and degree to which deep-burrowing earthworms affect unsaturated hydraulic conductivity at the soil surface. By not specifying variance at different distances from the midden, a traditional analysis of variance will tend to re¯ect an in¯ated mean square error, thereby increasing the possibility of committing a type II error.
4. Conclusions
We found that additions of deep-burrowing earth-worms increased the biomass of deep-burrowers, com-pared with ambient controls. The foraging habits of
Table 4
Means and analysis of variance of differences between log10-transformed unsaturated hydraulic conductivity in the chisel-till, CS rotation as
in¯uenced by earthworm and in®ltration surface surface conditions
Earthworm treatment
Surface Mesopore conductivity [K(ÿ30)±K(ÿ60)] log10(mm sÿ1)
Micropore conductivity
[K(ÿ60)±K(ÿ150)] log10(mm sÿ1)
Ambient Crust 0.1 0.3
Crust removed 0.4 1.1
Addition Crust 0.2 0.5
Crust removed 0.8 2.2
Treatment p>F p>F
Analysis of variance Earthworm 0.09 0.10
Crust <0.01 <0.01
these deep-burrowing earthworms led to a reduction and consolidation of crop residues, thereby exposing a greater proportion of the soil surface particularly for CS cropping. Further, these surface conditions resulted in decreased size and stability of macroag-gregates, and promoted surface crusting in a chisel-tilled, CS rotation. Also, the presence of these earth-worms in¯uenced the C/N ratio of disaggregated dry-stable material and smaller-sized WSA.
The long-term fate of this soil degradation is depen-dent upon factors such as the proportion of deep-burrowing species to other earthworm species, and access to a stable and abundant food supply. Cropping systems can also affect the density and foraging activity of earthworms, especially in terms of the type and frequency of tillage. These factors directly impact the formation, density, and life expectancy of mid-dens, which are accumulations of particulate and coarse organic matter. Furthermore, this small-scale phenomenon may evolve into larger-scale patches with implications for degrading cropping conditions at the ®eld scale. Moreover, the impacts of earthworm foraging activities underscore the importance of con-sidering the effects of soil faunal communities in management of organic matter resources, and their role in controlling erosion. More research will be needed to determine how earthworms may affect an optimal residue management recommendation for crop production in the midwestern US.
Acknowledgements
The authors Tina McKeegan and Sharon Iacavone for their help in the ®eld, and with laboratory analyses. We also thank Melinda Smith (Kansas State Univer-sity), whose comments improved earlier versions of this paper. This project was supported by a grant from the United States Department of Agriculture.
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