Agroforestry Systems 44: 141–149, 1999. 1999 Kluwer Academic Publishers. Printed in the Netherlands.
Spatial and temporal distribution of earthworms in a temperate intercropping system in southern Ontario, Canada G. W. PRICE* and A. M. GORDON Department of Environmental Biology, University of Guelph, Guelph, Ontario, Canada, N1G 2W1 (*Author for correspondence: E-mail:
[email protected])
Key words: ash, maple, poplar, soil macro-fauna Abstract. Earthworms are known to increase soil bulk density, soil porosity, mixing of organic matter, and to strengthen aggregation of soil particles. They perform important functions in the maintenance and stabilization of the soil matrix. Historically, temperate intercropping research has focused on the above-ground benefits of adding trees into the agricultural landscape. Earthworm research in temperate intercropping systems has been non-existent to date. More emphasis on studying below-ground components, such as earthworms, is required in order to better understand the mechanisms of intercropping ecosystem function. The purpose of this study was to examine seasonal changes in distribution and abundance of earthworms under a temperate intercropping system in southwestern Ontario, Canada. Sampling occurred during the spring and summer of 1997 at the University of Guelph’s Agroforestry Research Station, Guelph, Ontario. Earthworm samples were collected at various distances from the tree rows. Significant variation in both earthworm biomass and density were found between the three tree species sampled. Total mean earthworm density was 182 m–2 within the poplar rows, 71 m–2 within the silver maple rows, and 90 m–2 within the white ash rows. A marked difference was also observed in the distribution of earthworms within the tree rows and the field area. For example, total mean density within the tree rows for poplar was 182 individuals m–2, as compared to total mean densities of 117 and 95 individuals m–2, two metres and six metres into the field from the tree, respectively.
Introduction Physical, chemical, and biological factors contribute to the development and maintenance of soil structure and fertility (Edwards and Bohlen, 1997). In particular, earthworms have been found to greatly increase organic matter mixing and decomposition processes in the soil profile, which is of obvious importance in many agricultural systems (Lavelle, 1988; Edwards and Bohlen, 1997). Most of the studies in earthworm ecology have focused on conventional and minimum tillage agriculture systems, as well as the distribution of earthworms in pastures (De St. Remy and Daynard, 1982; Tomlin et al., 1992; Springett and Gray, 1997). Under no-till practices, larger densities of earthworms have been found to increase organic matter turnover rates, nitrogen mineralization rates, and soil porosity through their burrowing and feeding
142 activities (Lee, 1985; Willems et al., 1996). On the other hand, declines in soil productivity and agricultural yields may be linked to reductions in earthworm populations on land under conventional tillage (Lee, 1985; Doube et al., 1994). Little is known about the role of earthworms in agroforestry systems, especially in temperate regions. In the past four decades, research in agroforestry systems has focused mainly on crop productivity and techniques for on-farm implementation (e.g. Williams and Gordon, 1992) rather than below ground interactions, although this is changing (Nair, 1989; Ong and Huxley, 1996). Reports that soil macro fauna can improve soil bulk density, decomposition of soil organic matter, and stability of the soil in cropped fields highlights the need for further agroforestry research in this area (Tian, 1992; Hauser, 1993; Kang et al., 1994). Research conducted in England, using soil invertebrates as soil health indicators, observed clear correlations between the higher organic matter levels within poplar (P. trichocarpa) rows in a silvoarable agroforestry system and increases in invertebrate population densities and body size (Park et al., 1994). The primary purpose of this research was to examine the effects of tree presence and tree species on the spatial and temporal distribution of earthworm populations under a temperate intercropping system, in southwestern Ontario, Canada. It was hypothesized that the moderating effects of trees on the localized microclimate and the additional organic matter from tree leaf litter would create a habitat for earthworms buffered from climatic extremes in temperature and moisture, especially during the summer period.
Materials and methods In 1997, a field experiment was started to examine the distribution of earthworms in the soils of an 11-year-old temperate intercropping site, planted with Acer saccharinum, Fraxinus americana, and Populus spp. in combination with soybean (Glycine max L. & M.), at the University of Guelph’s Agroforestry Research Station in Guelph, Ontario, Canada. Sampling was conducted in May and August. The soils consist of sandy loams with an Ap horizon ranging in depth from 28 to 53 cm. The research fields cover a 30 ha area and consist of 10 different tree species intercropped with maize, wheat, and soybean on yearly rotations. The area receives approximately 700 mm of rainfall annually. Earthworm population estimates were made using 0.25 × 0.25 quadrats in transects, perpendicular to the tree rows, at 2 m and 6 m into the field on either side of the tree and at 1.5 m and 3.5 m within the tree rows (Figure 1). Three blocks of eight trees were randomly selected around the field for each species and four trees within each block were sampled. We collected earthworms by mixing 50 ml formaldehyde (37% V/V) and 10 L of water and initially applying 5 L of the solution into each quadrat; the remaining solution
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Figure 1. Diagrammatic representation of sampling layout in the field, Ontario, Canada.
was applied until no more worms appeared. All earthworms were counted and later air-dried and weighed in the laboratory. The total dry weight per quadrat was used for statistical analysis. The earthworms were preserved in small containers filled with a 5% formaldehyde solution for identification at a later date. Three random quadrats were also selected for each sample tree and dug up to a depth of 40 cm to assess the error in sampling associated with using the formalin technique. The individuals captured were not included in the surface area population estimate but were used to establish to what depth and accuracy the formalin treatment was effective. In the spring, the average number of individuals missed was approximately 40% relative to the total number caught in each trap. The summer samples appear to have been fully effective to 40 cm in depth. The experiment was designed as a randomly complete block design (RCBD) with subsampling and statistical analysis was conducted using PC SAS version 6.04 (SAS, 1989).
Results Distinct patterns of spatial and temporal earthworm distributions were observed in the spring and summer samples (Figures 2 and 3). During the spring, earthworm dispersal patterns were unique to each tree species treat-
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Figure 2. Spring (May 1997) total mean density and total mean biomass of earthworms sampled under a temperate intercrop for (a) Poplar, (b) Maple, and (c) Ash treatments in southern Ontario, Canada. (S.E. = ±1)
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Figure 3. Summer (August 1997) mean density and total mean biomass of earthworms sampled under a temperate intercrop for (a) Poplar, (b) Maple, and (c) Ash treatments in southern Ontario, Canada. (S.E. = ±0.85)
146 ment. The highest total mean density of earthworms, in both seasons, was found within the tree rows under poplar. The poplar treatment also displayed a pattern of increasing earthworm biomass and density from the field towards the tree rows. The highest total mean biomass for all treatment positions, however, was observed under the white ash trees. The white ash treatment displayed total mean biomass and density values increasing with distance from the tree rows, but with only minor differences occurring between the near tree and field treatments. In the silver maple treatment, total mean earthworm biomass was greater close to the tree rows and total mean density was not significantly different between the other treatments. However, the two-metre treatment for silver maple had a higher total mean density. Interestingly, the mean biomass values for the intra-row and near tree treatments did not exhibit high variation between them, despite the differences in density. The summer data reflects a greater uniformity in the dispersal pattern of the earthworms throughout all the tree species. In all the treatments, greater earthworm densities and biomass were found closer to the tree rows. The total number of earthworms collected in summer was approximately 60–70% lower than in spring. Table 1 presents the average dry weight per individual for each season and tree species treatment. These values were taken to represent differing maturity levels of the earthworms collected. A number of different studies comparing mature versus immature earthworm numbers and biomass, for various species, had biomass values ranging from 0.26–1.00 g m–2 for juveniles and 1.50–4 g m–2 for mature individuals (De St. Remy and Daynard, 1982; Tomlin et al., 1992; Tomlin et al., 1995). For example, the springtime poplar sample within the tree row had a mean value of 0.98 g m–2 per individual, while the values for the equivalent silver maple and white ash samples are 2.22 and 2.39 g m–2 per individual respectively. These values Table 1. Seasonal average individual earthworm biomass (g m–2) for three tree species collected in 1997, Ontario, Canada. Tree species
Poplar
Maple
Ash
Spring Within 2m 6m
0.98 1.51 1.06
2.22 1.71 1.27
2.39 2.20 2.26
Summer Within 2m 6m
2.07 2.07 1.99
2.58 2.21 1.37
2.68 2.46 2.13
The values are calculated from the total mean values for earthworm density and biomass displayed in Figures 2 and 3. Within = samples collected within the tree row; 2 m = samples collected on both sides near the tree bases; 6 m = samples collected in the middle of the alley on both sides of the trees.
147 suggest that in the spring, poplar may have larger densities of juvenile earthworms closer to the tree rows while a species like silver maple might have more mature individuals closer to the tree rows and more juveniles in the field. The summer values show a greater uniformity of mature individuals throughout all the samples and the dispersal patterns, shown in Figures 2 and 3, suggest that many of them have migrated closer to the tree rows.
Discussion The differences in earthworm density and biomass may be explained by variations in the microclimatic conditions created around the trees compared to conventional agricultural fields. Variations in the nutrient composition of the soil due to the addition of tree leaf litter may also have contributed to the earthworm distributions observed. The average air temperature in the spring was approximately 17 °C and summer values ranged from 26 °C–30 °C. The increase in ambient temperatures in the summer, as well as a reduction in rainfall, likely forced the earthworms to burrow deeper into the soil and into a state of aestivation (Edwards and Lofty, 1977). In the field, differences in tree height and canopy cover were also observed, but not measured in this study, particularly for silver maple and poplar trees. The silver maple and poplar trees had much greater leaf area and shade range compared to white ash trees. However, the white ash trees did have a strong canopy cover but were not as tall as the poplar or silver maples. All three tree species have rapidly decomposing leaf litter which becomes available to the earthworm populations early in the growing season (Thevathasan and Gordon, 1997; Kimmins, 1997). This availability of food early in the season may have contributed to the numbers of earthworms found close to the trees in the spring. For white ash, however, it may be possible that slower decomposition or higher phenolic compound content in the leaves accounts for the relatively high and stable numbers of earthworms observed during both seasons (Figures 2 and 3). Currently, a study is underway comparing the total volume and nutritional content of the leaf litterfall for each of the three species. Earthworm densities and biomass were higher for the same sampling period under the intercropping conditions in this study as compared to a previous study conducted on four well drained forested sites in southern Ontario (Tomlin et al., 1992). For example, in Donnybrook, a sandy loam area just south of Guelph, numbers ranged from 90 individuals m–2 in the spring to approximately 20 individuals m–2 in the summer under similar tree species and soil types as found in this study. The differences in maturity of earthworms found under the three tree species may be explained by availability and distribution of food resources, as well as the moderating effects attributed to tree presence. Since, leaf litter decomposition is quite rapid and leaf nitrogen content is high under poplar (Thevathasan and Gordon, 1997), earthworm juveniles may be able to thrive
148 in larger numbers near the tree rows than further out in the field. This is further evidenced by the changes in average individual earthworm biomass under poplar from the spring to the summer.
Conclusion Clear variations in the distribution of earthworm populations were apparent from samplings of the three tree species. Clear patterns of earthworm distribution with relation to distance away from the tree row was also observed. A recent survey of single-tree influences on soil properties (Rhoades, 1997) highlights the importance of understanding the interactions that can occur between trees and soil micro- and macro-organisms. The short-term indications are that tree selection under intercropping may have important ramifications on the abundance and distribution of soil organisms present (Park et al., 1994). More importantly, tree presence may have very positive stabilizing influences with respect to earthworm populations and their ecological dynamics within the soil matrix. A further study of earthworm burrow interactions for each of the three species, as well as continued seasonal sampling of earthworm populations, is being conducted. More research is needed on the interactions between soil macro fauna and trees within agroforestry systems. The challenge for agroforesters in the future will be to integrate all the available above- and below-ground information into suitable ecological models.
References De St. Remy EA and Daynard TB (1982) Effects of tillage methods on earthworm populations in monoculture corn. Canadian Journal of Soil Science 62: 699–703 Doube BM, Buckerfield JC and Kirkegaard JA (1994) Short-term effects of tillage and stubble management on earthworm populations in cropping systems in southern New South Wales. Australian Journal of Agricultural Research 45: 1587–1600 Edwards CA and Lofty JR (1977) Biology of Earthworms. Chapman and Hall, London Edwards CA and Bohlen PJ (1997) Biology and Ecology of Earthworms, pp 55–180. Chapman and Hall, London Hauser S (1993) Distribution and activity of earthworms and contribution to nutrient recycling in alley cropping. Biology and Fertility of Soils 15: 16–20 Kang BT, Akinnifesi FK and Pleysier JL (1994) Effect of agroforestry woody species on earthworm activity and physicochemical properties of worm casts. Biology and Fertility of Soils 18: 193–199 Kimmins JP (1997) Forest Ecology. MacMillan Publishing Co, New York, 596 pp Lavelle P (1988) Earthworm activities and the soil system. Biology and Fertility of Soils 6: 237–251 Lee KE (1985) Earthworms: Their Ecology and Relationships with Soils and Land Use. Academic Press, New York Nair PKR (ed) (1989) Agroforestry Systems in the Tropics. Kluwer Academic Publishers, The Netherlands
149 Ong CK and Huxley P (eds) (1996) Tree–Crop Interactions. CAB International, Wallingford, UK Park J, Newman SW and Cousins SH (1994) The effects of poplar (P. trichocarpa x deltoides) on soil biological properties in a silvoarable system. Agroforestry Systems 25: 111–118 Rhoades CC (1997) Single-tree influences on soil properties in agroforestry: lessons from natural forest and savanna ecosystems. Agroforestry Systems 35: 71–94 SAS version 6.04 (1989) SAS Institute Inc Springett JO and Gray R (1997) The interaction between plant roots and earthworm burrows in pasture. Soil Biology and Biochemistry 29(3/4): 621–625 Thevathasan N and Gordon AM (1997) Poplar leaf biomass distribution and nitrogen dynamics in a poplar–barley intercropped system in southern Ontario, Canada. Agroforestry Systems 37: 79–90 Tian G (1992) Biological Effects of Plant Residues with Contrasting Chemical Composition on Plant and Soil under Humid Tropical Conditions, pp 69–86. Kluwer Academic Press, Wageningen Tomlin AD, McCabe D and Protz R (1992) Species composition and seasonal variation of earthworms and their effect on soil properties in Southern Ontario, Canada. Soil Biology and Biochemistry 24(12): 1451–1457 Tomlin AD, Tu CM and Miller JJ (1995). Response of earthworms and soil biota to agricultural practices in corn, soybean, and cereal rotations. Acta Zool Fenn 196: 195–199 Willems JJ, Marinissen JC and Blair J (1996) Effects of earthworms on nitrogen mineralization. Biology and Fertility of Soils 23: 57–63 Williams PA and Gordon AM (1992) Potential of intercropping as an alternative land use system in temperate North America. Agroforestry Systems 19: 253–263
