Micromorphic observation of soil alteration by earthworms

Agriculture, Ecosystems and Environment, 34 ( 1991 ) 363-370

363

Elsevier Science Publishers B.V., Amsterdam

Micromorphic observation of soil alteration by earthworms L.T. West ~, P.F. Hendrix I and R.R. Bruce 2 ~Department of Agronomy and Institute of Ecology, University of Georgia, Athens, GA (U.S.A.) 2USDA-ARS Southern Piedmont Conservation Research Center, Watkinsville, GA (U.S.A.) (Accepted for publication 5 July 1990)

ABSTRACT West, L.T., Hendrix, P.F. and Bruce, R.R., 1991. Micromorphic observation of soil alteration by earthworms. Agric. Ecosystems Environ., 34: 363-370. Thin section methodology was used to examine soils from laboratory experiments and from experimental field plots for effects of earthworms on soil microfabrics. Samples of loamy sand or sandy clay loam were incubated with the earthworm Lumbricus rubellus. Field samples of similar soil texture were collected from experimental plots treated with conventional or no-tillage management for 5 years. All samples were subjected to thin sectioning and microscopic examination for fabric and porosity characteristics. In both sandy and clayey soil, fewer and smaller voids were present adjacent to earthworm channels compared with bulk soil. Additionally, clay domains in the clayey soil were oriented into a porostriated b-fabric adjacent to the earthworm channel, suggesting that compaction and reorientation of the soil occurred as the channels were formed. In the sandy soil, plasma (clay, organic matter, and clay-organic complexes) coatings were observed along the channel walls, and two forms of earthworm castings were observed; ( 1 ) castings deposited within channels and composed of coarse sand grains that had been depleted of plasma; and (2) castings deposited on the surface which appeared to have fewer coarse sand grains and more plasma bridging between sand grains, compared with bulk soil. These grain size and plasma relationships between channel and surface castings suggest that earthworms passed coarse sand grains through their gut and deposited them in the channel. Plasma removed from the coarse grains appeared to be incorporated with plasma associated with the finer sand and deposited along the channel wall or as castings at the soil surface. Similar features were observed in and around macropores from field soils, suggesting similar effects of earthworms in relatively undisturbed soils from no-tillage agroecosystems. Particle reorientation along channel walls, compaction of particles adjacent to channel walls, and organic linings may limit water movement from earthworm burrows into the bulk soil, with possible impacts on solute movement and retention in the soil.

INTRODUCTION

Earthworm activities are known to affect soil physical properties (Edwards and Lofty, 1977; Satchell, 1983; Lee, 1985). Mechanisms for earthworm effects on bulk properties of soil appear to involve microstructural changes in 0167-8809/91/$03.50

© 1991 - - Elsevier Science Publishers B.V.

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soil fabric, but there have been only a few systematic studies at this scale (Shaw and Pawluk, 1986; Shipitalo and Protz, 1987 ). This paper presents the results of laboratory and field studies that use soil thin section methodology to examine earthworm effects on soil structure. Our objectives are: ( 1 ) to present a m e t h o d to evaluate earthworm effects on soil microfabrics under controlled conditions; (2) to describe soil microfabrics characteristic of earthworm activity and relate these to bulk properties of soils from differently textured surface horizons of Ultisols in the southeastern U.S.A.; and (3) to identify similar microfabrics in field soils inhabited by earthworms. METHODS

Laboratory study Samples were collected from the Ap horizon of two Typic Kanhapludults near Athens, Georgia. Textures of the two soils were loamy sand and sandy clay loam. Samples were air dried and gently crushed to pass a 2-mm sieve. Eighteen 100 g samples of each soil were placed in 120 cm 3 polyethylene specimen cups that were perforated on the bottom and lined with 1-mm mesh nylon screen. A 0.5 g sample of dried rye (Secale cereal ) straw ground to pass a l - m m sieve was added to the surface of 14 replicates of each soil. All cups were wetted to field capacity and one adult earthworm (Lumbricus rubellus) was added to 10 of each texture that contained rye straw. Eight cups of each soil (four with and four without straw) served as controls without earthworms. All cups were incubated for 42 days at 20-25 °C with regular watering to maintain adequate soil water. At the end of the incubation period, watering ceased and the soil was allowed to air dry slowly. After drying, one cup from each treatment combination was impregnated with epoxy resin (Scotchcast No. 3: 3M C o m p a n y ) with 0.3% fluorescent additive (Uvitex, OB; Ciba-Geigy). Thin sections were cut and polished to 0.03 m m thickness by standard techniques (Murphy, 1986). Water-stable aggregate size distribution was determined on eight replicates of each texture with earthworms and on three replicates of the other two treatments (rye alone and no a m e n d m e n t ) . The entire content of each cup was gently placed on the top of a nest of sieves (2.0, 0.250, 0.106 and 0.053 m m ), pre-wetted in place for 10 min, and then agitated in water for 3 min in a reciprocating apparatus with a 2 cm stroke at 33 cycles min-1. Soil fractions remaining on each sieve were air dried, weighed and expressed as percentages of total weight retained on all sieves. Soil that passed all sieves (1-2%) was calculated by difference between weight of material retained and total sample weight.

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Fieldstudy Field studies were conducted at the end of a 5-year renovation experiment consisting of three management treatments (conventional-tillage soybeans with winter fallow, conventional-tillage grain sorghum with winter fallow, and no-tillage grain sorghum double cropped with winter crimson clover) imposed on three soil erosion classes (slight, moderate and severe). The experimental design was randomized complete blocks with erosion class as the main plots and management treatments as the split sub-plots. Management treatments were replicated three times within each erosion class (see Langdale et al., 1991 ). Earthworms were hand-sorted from duplicate 10 cm diameter× 15 cm deep core samples collected from each plot. Earthworms and cocoons were enumerated, freeze dried and then ashed at 500°C for 4 h to measure ash-free dry weight biomass. Samples for water-stable aggregate measurement were collected from 0-1.5, 1.5-3.0 and 3.0-8.0 cm depths. Water-stable aggregate percentage was determined by immersion of a 5 g air-dry sample of the 1-2 mm separate into water and gently oscillating the sample for 5 min on a 0.25mm sieve. Water-stable aggregates were considered to be the portion of the sample remaining on the sieve after correction for primary particles. Water infiltration rates were determined in situ with a sprinkler infiltrometer at a rainfall rate of about 60 m m h - i over a 1 h period. Undisturbed soil samples were collected from the 0-5 cm depth for impregnation and thin-section preparation, as described previously. RESULTS AND DISCUSSION

Laboratory study Earthworm channels in the two soils ranged from 3 to 8 m m in diameter. In thin section of both sandy (Fig. 1A) and clayey (Fig. 1B ) soil, fewer and smaller voids were present immediately adjacent to the earthworm channels as compared with bulk soil. Additionally, clay domains in the clayey soil were oriented into a porostriated b-fabric (Bullock et al., 1985) adjacent to the earthworm channel (Fig. 1C). These features suggest that compaction and reorientation of the soil occurred as the channels were formed. In the clayey soil, material redeposited as subsurface casts by earthworms within the channel also had porostriated b-fabric suggesting sequential deposition of the casts along the channel wall (Fig. 1D). Shaw and Pawluk ( 1986 ) reported similar striated microfabrics in soils altered by earthworm activity. In the sandy soil, plasma coatings (clay, organic matter and clay-organic complexes ) were observed along the earthworm channel walls (Fig. 2A ). Two forms of earthworm castings were observed in thin section in the sandy soil:

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Fig. 1. Thin section micrographs of earthworm-induced microfabrics. (A) Compaction along channel wall in sandy soil; note fewer voids (v) adjacent to channel (c). ( B) Compaction along channel wall in clayey soil. (C) Porostriated b-fabric surrounding earthworm channel; arrows point to clay domains. (D) Porostriated b-fabric in channel infiiling; arrows point to clay domains; extreme left side of photo is bulk soil. (A) and (B) partially crossed polars; (C) and (D) cross polarized light. Bar length= 1 mm. ( 1 ) castings deposited within channels composed of coarse sand grains that had been depleted of plasma (Fig. 2A); and (2) castings deposited on the surface that appeared to have fewer coarse sand grains and more plasma bridging sand grains as compared with the bulk soil (Fig. 2B). Plasma may have been r e m o v e d from the coarse grains, incorporated with plasma associated with the finer sand, and deposited along the channel wall or as castings at the soil surface. Water-stable aggregate size distributions were affected by earthworm activity (Table 1 ). Abundance o f aggregates > 2 m m increased while that of 0.252 m m aggregates decreased relative to controls. The difference was m o r e pronounced in the sandy soil. The larger aggregates were primarily fragments of soil surrounding earthworm channels that are postulated to be bound by organic material. Particle rearrangement adjacent to the channels m a y also contribute to water-stable aggregate formation.

Field study A m o n g the m a n a g e m e n t systems, the no-till grain sorghum treatment had the greatest earthworm abundance ( m a t u r e Octolasion cyaneum and numer-

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Fig. 2. Thin section micrographs of earthworm-induced microfabrics. (A) Plasma lining along channel wall (arrow) in sandy soil and casting (f) within channel that has had sand grains stripped of plasma. (B) Surface casting ( f ) in sandy soil; note finer size of sand grains and plasma bridges between grains. (C) Compaction along channel wall in field soil. (D) Plasma lining on channel wall in field soil. (A) Plain polarized light; (B), (C) and (D) partially crossed polars. Bar length = 1 mm. TABLEI Water-stable aggregate size distribution from incubated treatments (% of dry weight )t Treatment

n

Size fraction (mm) 2 >2

2-0.25

0.25-0.106

0.106-0.053

Sand/OM/W Sand/OM Sand

8 3 3

20 (1.9) 6 (0.9) 3 (0.4)

65 (1.4) 79 (0.6) 80 (0.9)

14 (1.1) 14 (0.5) 16 (0.6)

I (0.I) 1 (0.2) 1 (0.1)

Clay/OM/W Clay/OM Clay

8 3 3

33 (5.3) 24 (4.9) 13 (2.8)

48 (6.3) 57 (1.8) 61 (1.5)

18 (2.7) 18 (2.9) 23 (1.7)

1 (0.2) 1 (0.3) 2 (0.1)

~Percentages are not corrected for primary particles. OM = rye straw applied to surface; W = earthworm added. 2Standard error in parentheses.

ous immatures). This management system also had significantly higher amounts of water-stable aggregates and infiltration rates (Table 2 ). Among erosion classes, relationships among the variables were not as clear. The high

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TABLE 2 Earthworm numbers, water-stable aggregates, and relative infiltration for erosion classes and cropping systems in the field study Earthworms (No. m -2 )

Water-stable aggregates (%>0.25 ram)

Infiltration (% of rainfall)

Cropping system CT Soybean CT Sorghum NT Sorghum

127 a ~ 180 a 307 b 2

50 a 50 a 76 b

69 a 66 a 100 b

Erosion classes Slight Moderate Severe

60 a 301 b 255 b

53 a 57 a 66 b

84 a 73 b 79 ab

~Means followed by the same letter are not significantly different at P=0.05. 2Significant at P = 0.07.

sand content of the slightly eroded soil probably accounts for high water infiltration and low earthworm abundance. Conversely, high aggregate stability and worm abundance in the more eroded soil may be related to high clay and organic matter content (see Langdale et al., 1991 ). Channels with diameters similar to those made by earthworms in the laboratory were common in undisturbed samples from the upper 5 cm of the field plots. These channels also had microfabric features similar to those associated with earthworm channels in the laboratory - compaction adjacent to the channels (Fig. 2C), porostriated b-fabric, and isolated organic linings on channel walls (Fig. 2D). Although plant roots or soil fauna other than earthworms form macropores, the similarity of these channels to microfabrics observed in the laboratory and the abundance of earthworms in the field plots suggest that the observed features resulted from earthworm activity. DISCUSSION

Soil microfabric analysis has been shown to be a valuable tool for evaluating soil modification from biotic activity (Shaw and Pawluk, 1986; Kretzschmar, 1987, Kooistra, 1991 ). In this study, identifiable soil fabric features associated with earthworm activity varied between clayey and sandy textured soils. Compaction of the soil surrounding earthworm channels was identified in both soils, but clay domain reorientation associated with channel walls in the clayey soil was not observed in the sandy soil. This difference is attributed to lack of sufficient clay in the sandy soil to allow observation of clay reorienration. Similarly, organic coatings on channel walls and concentration of

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plasma in castings observed in the sandy soil were probably also present in the clayey soil but may have been masked by the abundant plasma in this soil. Staining techniques should be valuable for evaluating organic concentrations in soils with appreciable contents of fine materials. Increased water stability of earthworm castings and channel walls is postulated to result from grain bridging by organic-enriched material. This bridging may be enhanced by grain reorientation along channel walls. In the field plots, no-till management induced greater earthworm abundance compared with conventional tillage, as has been observed in other studies (Lee, 1985; Parmelee et al., 1991 ). This effect is attributed to increased organic matter, reduced soil disturbance, and improved habitat conditions under no tillage. Corresponding increases in soil aggregation and water infiltration are postulated to be due, at least partially, to increased earthworm activity. Channels produced by earthworms would be expected to increase the rate of infiltration and saturated hydraulic conductivity in the soil. Particle reorientation along channel walls, compaction of particles adjacent to channel walls, and organic linings, however, may limit movement of water and solutes from channels into the bulk soil. This could have appreciable impact on solute movement, as many adsorption sites may be unavailable to solutes moving rapidly in channels. ACKNOWLEDGEMENTS

This study was supported by USDA-ARS and by grant BSR-8818302 from the National Science Foundation. David Radcliffe provided helpful comments on the manuscript. REFERENCES Bullock, P., Fedoroff, N., Jongerius, A., Stoops, G. and Tursina, T., 1985. Handbook for Soil Thin Section Description. Waine Research Publications, Wolverhampton, pp. 88-94. Edwards, C.A. and Lofty, J.R., 1977. The Biology of Earthworms. Chapman and Hall, London, pp. 190-202. Kooistra, M., 1991. A micromorphological approach to the interactions between soil structure and soil biota. Agric. Ecosystems Environ., 34:315-328. Kretzschmar, A., 1987. Observations of the microscopic features of earthworm activity. In: Fedoroff, N., Bresson, L.M. and Courty, M.A., (Editors), Soil Micromorphology. Association Frangaise pour l'l~tude du Sol, Paris, pp. 325-330. Langdale, G.W., West, L.T., Bruce, R.R., Miller, W.P. and Thomas, A.W., 1991. Conservation tillage to sustain productive soil properties. Catena, in review. Lee, K.E., 1985. Earthworms: Their Ecology and Relationships with Soils and Land Use. Academic Press, Sydney. Murphy, C.P., 1986. Thin Section Preparation of Soils and Sediments. A B Academic Publishers, Berkhamsted, pp. 55-111. Parmelee, R.W., Beare, M.H., Cheng, W.X., Hendrix, P.F., Rider, S.J., Crossley, Jr. D.A. and

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Coleman, D.C., 1991. Earthworms and enchytraeids in conventional and no-tillage agroecosystems: A biocide approach to assess their role in organic matter breakdown. Biol. Fert. Soils, in press. Satchell, J.E. (Editor), 1983. Earthworm Ecology: From Darwin to Vermiculture. Chapman and Hall, London. Shaw, C. and Pawluk, S., 1986. The development of soil structure by Octolasion tyrtaeum, Aporrectodea turgida and Lumbricus terrestris in parent materials belonging to different textural classes. Pedobiologia, 29: 327-339. Shipitalo, M.J. and Protz, R., 1987. Comparison of morphology and of a soil under conventional and zero tillage. Can. J. Soil Sci., 67: 445-456.