Soil Science Society of America Journal 64:222-228 (2000)
© 2000 Soil Science Society of America
DIVISION S-3-SOIL BIOLOGY & BIOCHEMISTRY
Regeneration of Earthworm Populations in a Degraded Soil by Natural and Planted Fallows under Humid Tropical Conditions
G. Tiana,
J.A. Olimaha,b,
G.O. Adeoyeb and
B.T. Kanga
a Soil Fertility Unit, Resource and Crop Management Div., International Inst. of Tropical Agriculture (IITA), Ibadan, Nigeria, c/o L.W. Lambourn & Co., 26 Dingwall Road, Croydon CR9 3EE, UK
b Dep. of Agronomy, Univ. of Ibadan, Ibadan, Nigeria
g.tian{at}cgiar.org
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ABSTRACT
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Earthworm populations (predominantly Hyperiodrilus africanus and Eudrilus eugeniae) were sampled monthly for 1 yr during 1994 and 1995 in natural regrowth vegetation fallow (dominated by the natural fallow shrub Chromolaena odorata L.), planted fallow (the woody species Senna siamea Lam., Leucaena leucocephala Lam., and Acacia leptocarpa), and intercropped maize (Zea mays L.)–cassava (Manihot esculenta Crantz) established in 1989 in a degraded Alfisol (Oxic paleustalf) in southwestern Nigeria. Compared to leaves of Chromolaena (3.3% N), N concentrations were lower in those of Senna and Acacia, and higher in Leucaena. Acacia and Leucaena had higher polyphenol relative to the natural fallow (2%). The lignin was lower in Leucaena than the natural fallow leaves (14%). For 65% of the sampling dates, earthworm numbers under all fallows were significantly higher than under continuous maize–cassava. The mean earthworm numbers (no. m-2) during the rainy season (April–October) decreased in the following order: Chromolaena (147), Senna (131), Leucaena (92), Acacia (80), and maize–cassava (14). Earthworm fresh weights in fallow plots were higher than in the maize–cassava plot, though this was significant for only 4 out of 11 sampling dates. Higher earthworm numbers and biomass in fallow plots were attributed to higher litterfall, lower soil temperature, and higher soil moisture. The mean earthworm numbers were directly correlated with the mean soil moistures (
, P < 0.05) in fallow plots and N/polyphenol ratios of fallow litterfall (
, P < 0.05). Increase in earthworm population by fallows led to an increase in leaf-litter decomposition, soil organic matter, available P, and extractable cations and pH; and a decrease in soil bulk density and penetrometer resistance in the fallow plots.
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INTRODUCTION
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FALLOW WITH VEGETATION is known as a biological approach to regenerating the fertility of degraded soil in the humid tropics. During the fallow period, plant nutrients are taken up from various soil depths and stored in the fallow vegetation. The nutrients depleted during cropping are replenished with those from fallow vegetation. The litterfall from the fallow vegetation increases soil organic matter content. The groundcover by fallow vegetation enhances the soil biological activity. Replenishment of soil organic matter and regeneration of biological activity led to an increase in soil porosity and a reduction in soil compaction. Traditional farmers in the humid tropics use fallow with natural regrowth vegetation (natural fallow), mainly shrub species (Chromolaena odorata L.), for soil regeneration.
Throughout the years, researchers have attempted to plant selected herbaceous or woody species to replace natural vegetation for soil regeneration (Kang et al., 1997). Advantages of planted woody fallow include efficient nutrient pumping from the subsoil because of the deep rooting system, high biomass production, nutrient accumulation, and production of timber and fuel-wood for income generation. On the other hand, a large proportion of the biomass from planted woody fallow (72 to 95%, F.K. Salako and G. Tian, unpublished data) is partitioned into wood. This brings up a question of whether the planted woody fallow could still promote the restoration of a degraded soil, while accumulating biomass and nutrients in the wood. A long-term study was therefore initiated at the International Institute of Tropical Agriculture (IITA), Ibadan, Nigeria, to determine the ability of selected woody species to regenerate soil. The monitoring of earthworm populations was chosen as part of an ongoing study because of the dramatic decline in the earthworm population with soil degradation (Tian, 1998).
Earthworms contribute to soil processes through fecal excretion (casts), burrowing, feeding, and digestion. Casts are nutrient-rich and are an intimate mixture of soil, water, and microbial cells (Linden et al., 1994). Earthworm burrows provide pathways for root exploration (Logsdon and Linden, 1992). Earthworms are known to accelerate plant residue decomposition in the tropics (Tian et al., 1995) and play a role in converting plant residue into soil organic matter (Lee, 1985; Lavelle, 1988). Lavelle and Martin (1992) elaborated the short-term and long-term effects of earthworms on soil organic matter dynamics in a tropical soil.
Temperature, moisture, and food supply are major components of the earthworm habitat (Edwards and Bohlen, 1996). With the return of cropped land to fallow with vegetation, the earthworms' habitat is improved because of lower soil temperature, higher soil moisture, and better food supply, leading to a potential increase in earthworm populations. Since planted woody fallows have a different canopy structure, groundcover, litterfall, and biomass partitioning than the Chromolaena, they create different earthworm habitats, leading to different restoration of the earthworm population. The present study quantifies the earthworm populations under natural and planted fallow, and examines linkages between the earthworm population with the chemical composition and the decomposition rates of leaf litter, soil temperature, and soil moisture induced by the fallow species. The contribution of the earthworm population to the restoration of other soil properties is discussed in this paper.
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Materials and methods
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Experimental Design
This investigation was carried out at the International Institute of Tropical Agriculture (IITA), Ibadan, Nigeria (3°54'E, 7°30'N, 213-m altitude), which is in the forest–savanna transitional zone of tropical Africa. The site has a 30-yr average of 1312 mm of rainfall with a bimodal distribution and a mean annual temperature of 26.2°C. The rainy season is from April to October with low precipitation in August. The experimental site was cleared from a secondary forest in 1978 and was cultivated continuously until 1989, resulting in the degradation of the soil at the site (Hulugalle, 1992). The soil at the experimental site is classified as an Alfisol (Oxic paleustalf). The surface soil texture is a sandy loam overlying sandy clay or clay subsoil. The soil characteristics of the experimental site are shown in Table 1
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Table 1 Characteristics of the surface soil (0–15 cm) under natural and planted fallow, and continuous maize–cassava cropping, sampled in 1996 (F.K. Salako and G. Tian, unpublished data, 1995)
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Fifteen herbaceous shrub and woody species were planted in May 1989 in a randomized complete block design with four replications, along with the natural regrowth vegetation dominated by Chromolaena and continuous maize–cassava intercropping. Chromolaena is a perennial shrub that is native to Central and South America; it arrived in West Africa from Asia in the 1940s. Every year, maize (40000 plants ha-1) was intercropped with cassava (10000 plants ha-1) in the continuous cropping plot. Each plot size measured 12 by 8 m. By 1994, most herbaceous and shrub species had not survived the annual 5-mo dry season. Observations on the earthworm population were made in three of the surviving planted woody fallows (species Senna siamea, Leucaena leucocephala, and Acacia leptocarpa), Chromolaena, and continuous maize–cassava cropping. No-tillage was used for all treatments; however, five times each year, hand-hoe weeding was done in the maize–cassava plots.
Leaf Chemical Analysis
The fully matured leaves (blades and petioles) from the natural and planted fallow were collected from four replicate plots in June 1994. The leaf samples were oven-dried at 60°C and ground to pass a 0.5-mm mesh sieve. Total C was determined by dry combustion (CHN-Leco analyzer, Leco, St. Joseph, MI). Total N was determined by micro-Kjeldahl digestion followed by distillation and titration. Using the same digestion solution for N, P was measured colorimetrically by a spectrophotometer, K was measured by flame photometry, and Ca and Mg were measured using atomic absorption spectrophotometer (Okalebo et al., 1993). Extractable polyphenols were determined by the Folin-Denis method (Anderson and Ingram, 1993). Lignin was determined by the acid detergent fiber method (Goering and van Soest, 1970). All chemical analyses were done with two replicates, from which the mean and standard errors were calculated.
Soil Microclimate
Surface (0–10 cm) soil moisture was measured gravimetrically at 2-wk intervals, and soil temperature at a 10-cm depth was measured biweekly using a temperature probe. All measurements were made at 1100 h. There were four temperature measurements per plot. A composite sample from 10 locations per plot was taken for gravimetric soil moisture determinations. The LSD (0.05) was calculated from four replicates to determine the treatment effect on soil moisture and temperature.
Leaf Decomposition
The same fresh leaves (equivalent to 45 g of dry material) used for chemical analysis were placed in a litterbag measuring 30 by 30 cm with a mesh size of 5 mm, which was large enough to allow access to most soil animals (Tian et al., 1992). To prevent compression of plant residues inside the litterbags, pieces of wood (3 cm in diam.) were placed inside the four edges of the litterbags. Twenty litterbags per species were prepared to allow five samplings with four replications on each sampling date. The litterbags were placed on the surface under the corresponding species on 18 July 1994. Samples were taken at 6, 13, 27, 49, and 98 days after placement. At each sampling, the plant residues were water-washed, oven-dried, and weighed to determine the remaining material. The single exponential equation,
(where Y is the percentage of remaining initial plant material at time [t]), was used to calculate the decomposition rate constant (k) (Wieder and Lang, 1982).
Earthworm Sampling
Populations of earthworms (predominantly Hyperiodrilus africanus and Eudrilus eugeniae) were sampled monthly from May 1994 to April 1995. Sampling was done using 30- by 30- by 30-cm soil monoliths from which earthworms were sorted by hand (Anderson and Ingram, 1993). Two monoliths were taken from each plot on every sampling date. Since most earthworms in the region are Hyperiodrilus africanus (Madge, 1969), the number of other species was included into the former as total earthworm numbers. Earthworm numbers were normalized by log10 (x + 1) transformation, and the fresh earthworm weight was transformed by square root before ANOVA. Since earthworms in the region are not active during the dry season—from November to March (Madge, 1969)—the mean of the earthworm population was calculated for the rainy season months: May to October 1994 and April 1995. Linear regression analyses were made between soil moisture and temperature, chemical composition or decomposition rates of leaf litter, and mean earthworm populations.
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Results
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Chemical Composition of Natural and Planted Woody Fallow
Chromolaena leaves had high N, low polyphenols, and intermediate lignin content; Senna leaves had low N, low polyphenol, and high lignin contents; Leucaena leaves had high N, high polyphenol, and low lignin content; and Acacia had low N and high polyphenol and lignin content (Table 2)
. Phosphorus, K, and Mg contents were highest in Chromolaena leaves, whereas Ca was the highest in Senna leaves.
Soil Temperature and Moisture
For nearly all sampling dates, soil moistures in the fallow treatments were significantly higher than those in maize–cassava (Fig. 1)
. The Chromolaena maintained consistently higher soil moisture than the planted woody fallow during the rainy season. There was little difference in soil moisture content among the fallow treatments during the dry seasons. For treatments with the planted woody fallow, soil moisture was relatively higher under Senna and relatively lower under Acacia during the rainy season; however, such differences were significant on only a few occasions. Soil temperatures in all fallow treatments were significantly lower than in maize–cassava (Fig. 2)
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Fig. 1 Dynamics of soil moisture content (g g-1) in natural and planted fallows and continuous maize–cassava during the 1994–1995 season. The treatment difference was significant for all sampling dates, except for 22 Mar. and 5 April. Bar A represents LSD (0.05) for the observation on 20 July (rainy season) and Bar B for 21 Dec. 1994 (dry season)
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Fig. 2 Dynamics of soil temperature in the natural and planted fallows and continuous maize–cassava during the 1994–1995 season. The treatment difference was significant for all sampling dates. Bar A represents LSD (0.05) for the observation on 20 July (rainy season) and Bar B for 21 Dec. 1994 (dry season)
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Leaf Decomposition
A rapid loss of leaf material in litterbags was observed with Chromolaena, Leucaena, and Senna during the initial decomposition stage (Fig. 3)
. Chromolaena leaves decomposed fastest, and hardly any material remained in the litterbags at 98 d. Acacia decomposed slowest. Leucaena leaves decomposed faster during the first four sampling dates, compared with Senna. The decomposition rate constants declined in the following order: Chromolaena > Senna > Leucaena > Acacia (Table 2).
Earthworm Population and Biomass
The earthworm populations during 1994–1995 rainy and dry season are shown in Table 3
. Earthworm numbers were higher in fallow treatments than in maize–cassava for 65% of the sampling dates. The mean earthworm number (no. m-2) during the rainy season increased in the following order: maize–cassava (14), Acacia (80), Leucaena (92), Senna (131), and Chromolaena (147). The mean earthworm numbers during the rainy season were positively correlated with soil moisture in the fallow treatments (Fig. 4)
and the N/polyphenol ratios of the plant leaves (Fig. 5) .
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Table 3 Effect of natural and planted fallows on earthworm numbers in a degraded Alfisol under regeneration (1994–1995)
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Fig. 4 Correlation between mean earthworm numbers and soil moisture contents during the rainy season (May–Oct. 1994 and April 1995)
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Fig. 5 Correlation between mean earthworm numbers during the rainy season (May–Oct. 1994 and April 1995) and N/polyphenol ratio of the leaves from the natural and planted fallows
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The seasonal changes in earthworm biomass were correlated with those of earthworm number (Table 4)
. All fallow treatments supported higher earthworm biomass compared with maize–cassava. In October 1994 and March 1995, earthworm biomass in Chromolaena was significantly higher than in Leucaena. The mean earthworm biomass during the rainy season was 2.2, 1.6, 1.5, and 1.6 times higher in Chromolaena, Senna, Leucaena, and Acacia, respectively, than in maize–cassava.
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Table 4 Effect of natural and planted fallows on earthworm fresh weight in a degraded Alfisol under regeneration (1994–1995)
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Discussion
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Differences in earthworm populations between natural or planted fallow and continuous maize–cassava cropping clearly indicates the restorative effect of vegetative fallow on the earthworm population lost during continuous cropping. This is related to changes in food supply and microclimate that are favorable to earthworms when the land is returned to fallow. The epigeic and anecic earthworms feed on surface litter; endogeic earthworms feed on soil organic matter (Lavelle et al., 1994). Since litterfall is the main source of surface litter and soil organic matter, it could influence the food supply to earthworms. According to Kang et al. (1997), the annual (1992–1993) litterfall (t ha-1 yr-1) from the fallows were 8.8 (Chromolaena), 10.3 (Senna), 9.7 (Leucaena), and 9.0 (Acacia). With continuous cropping, the litterfall from maize and cassava was estimated to be 4 t ha-1. High litter input in the fallowed treatments led to better food supply to earthworms; this partially contributes to higher earthworm number and biomass. Tian et al. (1993) reported that application of plant residues with various chemical compositions all increased earthworm populations.
As reported earlier, soil temperatures were lower and soil moistures were higher in treatments with fallow vegetation than treatments with maize–cassava. Lower runoff and evaporation and higher interception, stemflow, and throughfall largely contributed to higher soil moisture in fallow treatments, compared with that cropped, despite possibly higher water loss through transpiration by fallow. The good soil microclimate created by fallow vegetation could partially account for high earthworm populations. According to Edwards and Bohlen (1996), soil moisture can influence earthworm numbers and biomass. Wood (1974) reported a strong positive correlation between earthworm biomass and increased soil moisture content for surface soil-inhabiting earthworm species surveyed at 18 different sites on Mt. Kosciusko in southeastern Australia. The significant correlation observed between soil moisture and earthworm populations further confirmed the importance of soil moisture for earthworms, even in the humid tropics. Since soil temperature was generally above the optimum temperature described by Edwards and Bohlen (1996), reductions in soil temperature by fallow vegetation could increase earthworm activity. The permanent shading of the tree hedgerows was identified as the most important factor enhancing earthworm casting activity in Leucaena leucocephala alley cropping (Hauser, 1993). Kang et al. (1994) observed that earthworm activity was affected by woody species cover through its effects on microclimate and leaf-litter quality.
Evans and Guild (1948) investigated the influence of food source on earthworm cocoon production and found that earthworms fed on N-rich diets grew faster and produced more cocoons than those with N-poor diets. Litter rich in protein is more readily accepted by earthworms than that deficient in protein (Edwards and Bohlen, 1996). The polyphenol concentration is another important parameter of food palatability to earthworms. There is an inverse relation between the palatability of litter and its total polyphenol content (Satchell, 1967). The palatability of oak and beech leaves could be increased by washing out water-soluble polyphenols (Edwards and Lofty, 1977). Hendrikson (1990) observed that the number of earthworms was correlated negatively with the C/N and polyphenol concentration of plant materials. The observed high correlation between earthworm numbers and N/polyphenol in the current study further confirmed the interactive role of N and polyphenols in influencing tropical earthworm populations.
Higher earthworm population was associated with the leaves of plant species with greater decomposition rates (Fig. 6)
. This is attributed to the influence of decomposition on the suitability of substrates as a food source for earthworms. The particle size of food materials influenced the food consumption by earthworm (Edwards and Bohlen, 1996). Materials with high decomposition rates, such as Chromolaena, provided more palatable food for the earthworms. On the other hand, there was the interactive effects of fallow leaf-litter quality, earthworm population, and decomposition rate. The high-quality litter improved the earthworm population, possibly leading to accelerated residue decomposition. The litterbags provided access to earthworms, so it is reasonable to infer that greater earthworm numbers under the fallow with higher-quality leaf litter could have accelerated its decomposition of the higher-quality material (Fig. 6). Earthworms were one of several important macrofauna participating in litter decomposition in secondary forest (Tian, 1998).
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Fig. 6 Correlation between decomposition rate constants of the leaves from the natural and planted fallows and mean earthworm numbers during the rainy season (May–Oct. 1994 and April 1995)
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Surface soil (0–15 cm) in fallow plots was higher in pH, organic C, available P, and extractable cations, and lower in bulk density and penetrometer resistance than in the maize–cassava plot (Table 1). The increase in earthworm populations possibly contributed to the regeneration of these properties in the degraded soil through casting and burrowing activity. The total worm casts ranged from 18 to 117 t ha-1 yr-1, as reported by Hauser (1993) and Kang et al. (1994). De Vleeschauwer and Lal (1981) observed that earthworm casts contain more organic C, total N, available P, and exchangeable cations than the parent soil from which the casts were derived. The casts also had a higher pH value than the corresponding surface soil (Kang et al., 1994). The burrowing activity of earthworms creates stable and continuous macropores that reduce soil compaction. Lal (1987) reported that eliminating earthworms led to high soil bulk density and massive structure.
Based on these results, we can conclude that vegetative fallow can improve earthworm populations in the degraded Alfisols in the humid tropics. Planted woody fallow, producing 84 to 157 t dry matter ha-1, compared with 9.4 t ha-1 for Chromolaena (F.K. Salako and G. Tian, unpublished data), could still regenerate the earthworm population of a degraded soil to the level of a nondegraded soil of the region (Tian et al., 1993). The fallow species conserved soil moisture, which would increase earthworm populations. Those fallow species producing leaf litter with low polyphenol and high N appear to have a high ability to enhance the earthworm population. Regeneration of earthworm populations has contributed partially to the improvement in soil chemical and physical properties and an increase in litter decomposition rate. Senna, which produced 80% higher biomass than the other three woody species studied, had a relatively higher ability to regenerate the earthworm population.
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ACKNOWLEDGMENTS
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We thank S. Hauser and F. Schulthess for providing useful comments on early versions of the manuscript of the paper during the internal review process.
Received for publication July 8, 1998.
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ABSTRACT
INTRODUCTION
