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Influence of food quality on the physical and chemical properties of detritivorous earthworm casts
Applied Soil Ecology 9 (1998) 263±269
In¯uence of food quality on the physical and chemical properties of detritivorous earthworm casts Martin Flegela,*, Stefan Schradera, Haiquan Zhangb b
a Institute of Zoology, Techn. Univers., Spielmannstr. 8, D-38092 Braunschweig, Germany Research and Technology Centre, University of Kiel, HafentoÈrn, D-25761 BuÈsum, Germany
Received 26 July 1996; accepted 17 January 1997
Abstract Laboratory experiments were conducted with Lumbricus terrestris, Lumbricus rubellus and Dendrobaena octaedra to study the effects of different food sources on physical and chemical cast properties. Earthworm species were kept separately in special microcosms ®lled with a loamy soil and offered leaves of dandelion (Taraxacum of®cinale), lupin (Lupinus polyphyllus), rye (Secale cereale), alder (Alnus glutinosa), beech (Fagus sylvatica) and larch (Larix decidua), diets which differed in palatability, C/N-ratios and secondary plant compounds. Cast production was monitored in relation to earthworm species and food. Enzyme activities (acid and alkaline phosphomonesterase), texture, water stable aggregation and tensile strength of casts were compared with those of the soil. Water stable aggregation was in¯uenced by the food source and the earthworm species. The tensile strength of the casts was also species speci®c. Although D. octaedra produced the highest and L. terrestris the lowest amount of water stable aggregates, the tensile strength of the casts was lowest for D. octaedra and highest for L. terrestris. # 1998 Elsevier Science B.V. Keywords: Food quality; Earthworm casts; Phosphomonesterase activity; Water stable aggregation; Tensile strength; Texture
1. Introduction Soil invertebrates in¯uence soil properties in many ways (Wolters, 1991). Earthworms improve soil quality indirectly by creating burrow-systems which enable better gas and water ¯ow and directly by castings and mucus secretion (Lee, 1985). The cast structure is clearly distinguished from the raw soil structure (Scheffer and Schachtschabel, 1989). Since the middle of this century many authors have reported higher water stability of earthworm casts compared *Corresponding author. Tel.: 00 49 531 3912373; fax: 00 49 531 3918198. 0929-1393/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved. PII S0929-1393(97)00050-4
with the surrounding soil (Edwards and Bohlen, 1996). Water stability is one of the most important properties affecting soil detachment by rain impact (Rasiah and Kay, 1995). Because of the use of heavy machinery on forest and agricultural soils the determination of soil stability becomes more and more important to assess soil health by mechanical parameters (Braunack et al., 1979). Schrader and Zhang (1997) studied how different soils affected the ef®ciency of earthworm castings in stabilizing soil structure and concluded that the more sensitive a soil to physical disturbance the greater the effect of castings on water stable aggregation and the less their effect on tensile strength. The aim of the present study was to
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M. Flegel et al. / Applied Soil Ecology 9 (1998) 263±269
examine the in¯uence of different food sources on the cast properties of different detritivorous earthworm species in relation to their in¯uence on soil structure. 2. Material and methods 2.1. Experimental conditions A laboratory experiment was conducted in order to obtain the casts of different earthworm species fed on various food sources. The earthworms were separated into species and kept in special microcosms consisting of two parallel glass sheets ®lled with sieved soil aggregates of de®ned diameter. For each diet treatment the food was offered on the soil surface. The duration of the experiments varied between 4 and 6 weeks. Lumbricus terrestris L., Lumbricus rubellus Hoffm. and Dendrobaena octaedra (Sav.) were chosen as representatives of the detritivorous earthworm group. For each diet treatment the casts of 25 specimens of L. terrestris and L. rubellus and 56 of D. octaedra were collected and individual cast production in milligram dry weight per gram live weight and day was calculated. The experiments were carried out with the leaves of six plant species with a wide range of C/N-ratios. Fresh leaves of dandelion (Taraxacum of®cinale, N: 3.59%, C/N: 11), lupin (Lupinus polyphyllus, N: 4.50%, C/N: 9), rye (Secale cereale, N: 1.23%, C/N: 31) and alder (Alnus glutinosa, N: 2.98, C/N: 15) and half year old leaves from the litter layer of beech (Fagus sylvatica, N: 0.91%, C/N: 48) and larch (Larix decidua, N: 1.01%, C/N: 42) were collected in the vicinity of Braunschweig. The leaves were air-dried and cut into 1±2 cm2 pieces. The soil used was a Gleyic Luvisol (FAO) from the Ap-horizon of a loamy soil taken from arable land near Neuenkirchen (Lower Saxony, Germany). For detailed information on the soil see Othmer and Bork (1989). The soil aggregates used were 1±2 mm in diameter for L. terrestris, and 0.5±1 mm for L. rubellus and D. octaedra. 2.2. Chemical and biochemical measurements Nitrogen and carbon content of the leaves was analysed by the macro-elementanalyser LECO CHN-1000 (Leco, Kirchheim, Germany). The total
nitrogen content (Nt) of soil and casts was estimated by the Kjeldahl method (Kandeler, 1993). In order to include nitrate, nitrite, nitro and nitroso groups also, 25 g of salicylic acid were added per litre of sulphuric acid. Organic carbon content (Corg) of soil and casts was determined by a macro-carbonanalyser (Leco Carbon Determinator IR 12, Leco, Michigan USA). Acid (SPA) and alkaline (APA) phosphomonesterase activity (buffer-pH: 6.5 resp. 11) were analysed by the method of Tabatabai and Bremner (1969) modi®ed by Margesin (1993) at 378C. The phosphomonesterase activity was calculated in microgram nitrophenol per gram dry mass and hour [mgNP/g/h]. 2.3. Physical measurements The amount of water stable aggregates (WSA) was determined by the method of Kemper and Rosenau (1986) modi®ed by Hartge and Horn (1989) (n5). The tensile strength (TS) of air-dried aggregates was determined by the crushing-test (n50). The aggregates were placed on an electrical balance and were cracked with a monoaxial operating pressure apparatus. The force used for cracking an aggregate (F) was calculated by the equation of Dexter and Kroesbergen (1985): t 0:576 F=d2 where t is the aggregate tensile strength, F is the crushing force and d is the aggregate diameter. Soil and cast textures were determined by the method of Moschre® (1983). 3. Results and discussion 3.1. Cast production (CP) The CP of all earthworm species was strongly in¯uenced by plant species (Fig. 1). Only the CP of L. terrestris was relatively constant between 279 and 318 mg/g/d while feeding on dandelion, lupin, beech and larch. With 812 and 835 mg/g/d D. octaedra produced the highest amounts of casts while feeding on larch and beech respectively, and showed the lowest CP when offered dandelion. For D. octaedra the CP was signi®cantly negatively correlated with the C/N-ratio of the food (Rÿ0.97, p0.013) and was
M. Flegel et al. / Applied Soil Ecology 9 (1998) 263±269
265
Fig. 1. Cast production (CP) of the earthworm species for each diet treatment.
meter and a constant C/N-ratio for different aggregate sizes were also reported by Scheu et al. (1996). Corg of L. terrestris casts was at all times higher than Corg of soil aggregates, because the animals were able to feed on and digest all the diets. Corg enrichment of L. rubellus and D. octaedra casts was only recorded when the animals fed on dandelion and rye and dandelion and lupin, respectively (Table 1). Scheu and Parkinson (1994) showed that D. octaedra consumes large quantities of soil microorganisms. It was concluded that with a deterioration of diet quality this species increased its consumption of soil aggregates in order to satisfy its nutrient requirements. Because of the digestion of soil Corg, this geophagous behaviour led to reduced Corg in the casts. L. rubellus
high signi®cant negatively correlated with food consumption (Rÿ0.92, p0.009) because a deterioration in food quality provokes higher soil consumption followed by higher cast production (Flegel and Schrader, 1998). L. terrestris and L. rubellus had their highest CP with 461 and 473 mg/g/d, respectively while feeding on alder. When offered rye L. terrestris and L. rubellus produced 228 and 192 mg/g/d, respectively, the lowest amounts of casts. Shipitalo et al. (1988) reported that L. rubellus produces casts at a higher rate per unit weight of worm (80±460 mg/g/d) than L. terrestris (70±180 mg/g/d) when fed on leaves with C/N-ratios between 11 and 26. Their data for L. rubellus agree well with the CP values of 192± 473 mg/g/d in the present study, but in contrast to their studies the CP of L. terrestris in the present study (226±461 mg/g/d) showed no great difference from the CP of L. rubellus.
Table 1 Chemical properties of the earthworm casts
3.2. Chemical properties of soil and cast aggregates
Food
The C content of soil aggregates between 0.5 and 1 mm was 1.85%, Corg was 1.79% and Nt was 0.165%, higher values than those of the aggregates between 1 and 2 mm with C1.59%, Corg1.54% and Nt0.151%. The C/N-ratio of both aggregate sizes was the same (11). An increase in nitrogen and carbon content with decreasing aggregate dia-
Dandelion Lupin Rye Alder Beech Larch
L. terrestris
L. rubellus
D. octaedra
Corg [%]
Nt [%]
Corg [%]
Nt [%]
Corg [%]
Nt [%]
1.99 1.76 1.73 1.73 1.79 1.80
0.196 0.181 0.168 0.172 0.157 0.167
1.99 1.76 2.09 1.71 1.65 1.79
0.250 0.200 0.189 0.189 0.170 0.188
1.87 1.85 1.68 1.63 1.64 1.56
0.262 0.233 0.181 0.169 0.167 0.162
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M. Flegel et al. / Applied Soil Ecology 9 (1998) 263±269
Fig. 2. Amount of water stable aggregates (WSA) of the soil and the cast aggregates for each diet treatment.
might also have used soil Corg for its nutrient requirement. 3.3. Water stable aggregation (WSA) The WSA content of all cast aggregates was signi®cantly higher than the WSA (21%) of the soil aggregates (Fig. 2). Higher WSA of casts compared with the surrounding soil has been reported by several authors (summarised by Edwards and Bohlen, 1996). For all earthworm species the increase in WSA was highest when offered dandelion and lowest when fed on alder. The casts of D. octaedra had the highest WSA content (81%) followed by the casts of L. rubellus and L. terrestris with WSA content of 80 and 73%, respectively. The lowest values of WSA were determined for casts of D. octaedra and L. terrestris (40%) and for the casts of L. rubellus (42%). The WSA of the casts was correlated with their Corg (R0.79, p<0.001), a similar ®nding to that reported by Zhang and Schrader (1993). In order to compare the effects of the different earthworm species, the percent WSA increase in casts was correlated with percent change in Corg. Assuming equal Corg (dCorg0) the extrapolation (Fig. 3) showed that L. terrestris raised WSA by 37% while L. rubellus and D. octaedra increased WSA by 170 and 217%, respectively. It must be taken into account that the
Corg of the soil aggregates used for L. terrestris was about 14% lower than the Corg of the 0.5±1 mm soil aggregates used for L. rubellus and D. octaedra. The extrapolated WSA content (155%) of the casts of L. terrestris for a soil aggregate Corg of 1.79%, however, was still the lowest, while the casts of D. octaedra had the highest WSA of all earthworm species. It was concluded that the quantity of Corg is not the only factor in¯uencing WSA: passage through the earthworm intestine also improves WSA and this increase is highly species speci®c. Microorganisms play the key role in stabilizing aggregates (Lynch and Bragg, 1985). Biochemical measurements showed a signi®cant correlation between APA (R0.53, p0.024), and a highly signi®cant correlation between SPA (R0.61, p0.007) and WSA of earthworm casts (Fig. 4). Phosphomonesterases are good indicators for microbial biomass and microbial activities (Nannipieri et al., 1979; Domsch et al., 1979; Frankenberger and Dick, 1983). Thus these results agree with the investigations of Metzger et al. (1987) who found that higher microbial biomass induces greater WSA. Reasons for a microbial biomass increase in the casts are an elevated nitrogen supply (Flegel and Schrader, 1996) and microbial stimulation in the intestines of the earthworm species (Parle, 1963; Kristufek et al., 1992). The main reason for the different WSA increases might be species speci®c intestinal conditions in the three
M. Flegel et al. / Applied Soil Ecology 9 (1998) 263±269
267
Fig. 3. Correlations between the percent change in the amount of water stable aggregates in casts (dWSA) of the three earthworm species and the percent change in organic carbon content of casts (dCorg) compared with the soil.
Fig. 4. Correlation between acid (SPA) and alkaline (APA) phosphomonesterase activities of earthworm casts and their percent water stable aggregate (WSA) content.
earthworm species which cause different development of the micro¯ora. 3.4. Tensile strength (st) Like the WSA content, the t values of the casts were also species speci®c. For each diet treatment t values were highest for L. terrestris and lowest for
D. octaedra (Fig. 5). Because no statistically signi®cant in¯uence of diet could be determined, the casts of each diet treatment were added to obtain species speci®c data. Only the t of 654 kPa calculated for the casts of L. terrestris showed no signi®cant difference compared with the t of the soil aggregates. Zhang and Schrader (1993) also found no differences between the t of the cast aggregates of L. terrestris
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M. Flegel et al. / Applied Soil Ecology 9 (1998) 263±269
Fig. 5. Tensile strength (t) of soil and the cast aggregates for each diet treatment. Bars indicates the standard deviations.
compared with soil aggregates. The t values of the cast aggregates of L. rubellus and D. octaedra were 585 and 507 kPa, respectively and were different at the highest signi®cance level from the t of the soil aggregates. Therefore, only the casts of L. terrestris maintained soil t. The t of aggregates is in¯uenced by their water and clay content (Gill, 1959). Because of identical water contents of cast and soil aggregates (3%, air-dried) and equal texture patterns (clay: 18%, silt: 80% and sand: 2%), these factors are ignored in the following discussion. The t of cast aggregates decreases with raising porosity (Dexter et al., 1984). Bal (1973) characterises the cast-shape of D. octaedra as `bacillocylindric'. These casts only form a `weakly welded' cast cluster. In contrast to D. octaedra, Bal (1973) describes the shapeless casts of L. terrestris as `strongly welded'. Because the single casts of L. terrestris are joining in a very compact way, it was concluded that their porosity is similar to soil porosity and less than the porosity of the `weakly welded' casts of D. octaedra. The casts of L. rubellus might form an intermediate cast cluster. 4. Conclusions The food source strongly in¯uences consumption rates and cast production by earthworms. Stimulation
of the soil micro¯ora is an important effect of earthworms which improves the WSA of soil aggregates. Because the nutrient content of casts in¯uences the WSA increase, good digestive nutrient enriched food guarantees a high WSA elevation. The in¯uence of earthworms on WSA and tensile strength is species speci®c, but these soil properties are affected in an opposite way. Acknowledgements Prof. Dr. O. Larink is acknowledged for valuable advice. We also thank K. Brinkmann, K. Steffens, M. Kondermann and G. Schnelle for technical assistance. We were supported by the Stifterverband fuÈr die Deutsche Wissenschaft. References Bal, L., 1973. Micromorphological analysis of soils. Soil Survey Papers No. 6. Soil Survey Institute, Wageningen, The Netherlands. Braunack, M.V., Hewitt, J.S., Dexter, A.R., 1979. Brittle fracture of soil aggregates and the compaction of aggregate beds. J. Soil Sci. 30, 653±667. Dexter, A.R., Kroesbergen, B., 1985. Methodology for determination of tensile strength of soil aggregates. J. Agric. Eng. Res. 31, 139±147.
M. Flegel et al. / Applied Soil Ecology 9 (1998) 263±269 Dexter, A.R., Kroesbergen, B., Kuipers, H., 1984. Some mechanical properties of topsoils from the Ijsselmeerpolders. I. Undisturbed soil aggregates. Neth. J. Agr. Sci. 32, 205±214. Domsch, K.H., Beck, T., Anderson, J.P.E., SoÈderstroÈm, B., Parkinson, D., Trolldenier, G., 1979. A comparison of methods for soil microbial population and biomass studies. Z. Pflanzenernaehr. Bodenkd. 142, 520±533. Edwards, C.A., Bohlen, P.J., 1996. Biology and Ecology of Earthworms, 3rd ed. Chapman and Hall, London. Flegel, M., Schrader, S., 1996. The N-cycle influenced by detritivorous earthworms feeding on different litter. Transactions of the 9th Nitrogen Workshop. Braunschweig, Germany, pp. 217±220. Flegel, M., Schrader, S., 1998. Importance of food quality on selected enzyme activities in earthworm casts (Dendrobaena octaedra, Lumbricidae). Soil Biol. Biochem. (submitted). Frankenberger, W.T., Dick, W.A., 1983. Relationships between enzyme activities and microbial growth and activity indices in soil. Soil Sci. Soc. Am. J. 47, 945±951. Gill, W.R., 1959. The effects of drying on the mechanical strength of Lloyd clay. Soil Sci. Soc. Am. Proc. 23, 255±257. Hartge, K.H., Horn, R., 1989. Die physikalische Untersuchung von BoÈden, 2nd ed. Ferdinand Enke, Stuttgart. Kandeler, E., 1993. Bestimmung von Gesamtstickstoff nach È hlinger, R., Margesin, Kjeldahl. In: Schinner, F., Kandeler, E., O R. (Eds.), Bodenbiologische Arbeitsmethoden. Springer, Berlin, pp. 364±366. Kemper, W.D., Rosenau, R.C., 1986. Aggregate stability and size distribution. In: Klute, A. (Ed.), Methods of Soil Analysis, Part 1. Physical and Mineralogical Methods. Agronomy Monograph No. 9 (2nd ed.), pp. 425±442. Kristufek, V., Ravasz, K., Pizl, V., 1992. Changes in densities of bacteria and microfungi during gut transit in Lumbricus rubellus and Aporrectodea caliginosa (Oligochaeta: Lumbricidae). Soil Biol. Biochem. 24, 1499±1500. Lee, K.E., 1985. Earthworms ± Their Ecology and Relationships with Soil and Land Use. Academic Press, Sydney. Lynch, J.M., Bragg, E., 1985. Microorganisms and soil aggregate stability. Advances in Soil Sci. 2, 133±171. Margesin, R., 1993. Bestimmung der sauren und alkalischen Phosphomonesterase-AktivitaÈt. In: Schinner, F., Kandeler, E., È hlinger, R., Margesin, R. (Eds.), Bodenbiologische ArbeitsO methoden. Springer, Berlin, pp. 200±203.
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Metzger, L., Levanon, D., Mingelgrin, U., 1987. The effect of sewage sludge on soil structural stability: microbial aspects. Soil Sci. Soc. Am. J. 51, 346±351. Moschrefi, N., 1983. Ein neues Verfahren der SchlaÈmmanalyse fuÈr die Bestimmung der KorngroÈûenzusammensetzung. Mitteilgn. Dtsch. Bodenkundl. Gesellsch. 38, 115±118. Nannipieri, P., Pedrazzini, F., Arcara, P.G., Piovanelli, C., 1979. Changes in amino acids, enzyme activities and biomasses during soil microbial growth. Soil Sci. 127, 26±34. Othmer, H., Bork, H.R., 1989. Characterization of the soils at the investigation sites. Landschaftsgenese und LandschaftsoÈkologie 16, 73±86. Parle, J.N., 1963. Micro-organisms in the intestines of earthworms. J. Gen. Microbiol. 31, 1±11. Rasiah, V., Kay, B.D., 1995. Runoff and soil loss as influenced by selected stability parameters and cropping and tillage practices. Geoderma 68, 321±329. Scheffer, F., Schachtschabel, P., 1989. Lehrbuch der Bodenkunde, 12th ed. Ferdinand Enke, Stuttgart. Scheu, S., Maraun, M., Bonkowski, M., Alphei, J., 1996. Microbial biomass and respiratory activity in soil aggregates of different sizes from three beechwood sites on a basalt hill. Biol. Fertil. Soils 21, 69±76. Scheu, S., Parkinson, D., 1994. Effects of earthworms on nutrient dynamics, carbon turnover and microorganisms in soils from cool temperate forests of the Canadian Rocky Mountains ± laboratory studies. Appl. Soil Ecol. 1, 113±125. Schrader, S., Zhang, H., 1997. Earthworm casting: stabilization or destabilization of soil structure? Soil Biol. Biochem. 29, 469± 475. Shipitalo, M.J., Protz, R., Tomlin, A.D., 1988. Effect of diet on the feeding and casting activity of Lumbricus terrestris and L. rubellus in laboratory culture. Soil Biol. Biochem. 20, 233±237. Tabatabai, M.A., Bremner, J.M., 1969. Use of p-nitrophenylphosphate for assay of soil phosphatase activity. Soil Biol. Biochem. 1, 301±307. Wolters, V., 1991. Soil invertebrates ± Effects on nutrient turnover and soil structure ± A review. Z. Pflanzenernaehr. Bodenkd. 154, 389±402. Zhang, H., Schrader, S., 1993. Earthworm effects on selected physical and chemical properties of soil aggregates. Biol. Fertil. Soils 15, 229±234.
In¯uence of food quality on the physical and chemical properties of detritivorous earthworm casts Martin Flegela,*, Stefan Schradera, Haiquan Zhangb b
a Institute of Zoology, Techn. Univers., Spielmannstr. 8, D-38092 Braunschweig, Germany Research and Technology Centre, University of Kiel, HafentoÈrn, D-25761 BuÈsum, Germany
Received 26 July 1996; accepted 17 January 1997
Abstract Laboratory experiments were conducted with Lumbricus terrestris, Lumbricus rubellus and Dendrobaena octaedra to study the effects of different food sources on physical and chemical cast properties. Earthworm species were kept separately in special microcosms ®lled with a loamy soil and offered leaves of dandelion (Taraxacum of®cinale), lupin (Lupinus polyphyllus), rye (Secale cereale), alder (Alnus glutinosa), beech (Fagus sylvatica) and larch (Larix decidua), diets which differed in palatability, C/N-ratios and secondary plant compounds. Cast production was monitored in relation to earthworm species and food. Enzyme activities (acid and alkaline phosphomonesterase), texture, water stable aggregation and tensile strength of casts were compared with those of the soil. Water stable aggregation was in¯uenced by the food source and the earthworm species. The tensile strength of the casts was also species speci®c. Although D. octaedra produced the highest and L. terrestris the lowest amount of water stable aggregates, the tensile strength of the casts was lowest for D. octaedra and highest for L. terrestris. # 1998 Elsevier Science B.V. Keywords: Food quality; Earthworm casts; Phosphomonesterase activity; Water stable aggregation; Tensile strength; Texture
1. Introduction Soil invertebrates in¯uence soil properties in many ways (Wolters, 1991). Earthworms improve soil quality indirectly by creating burrow-systems which enable better gas and water ¯ow and directly by castings and mucus secretion (Lee, 1985). The cast structure is clearly distinguished from the raw soil structure (Scheffer and Schachtschabel, 1989). Since the middle of this century many authors have reported higher water stability of earthworm casts compared *Corresponding author. Tel.: 00 49 531 3912373; fax: 00 49 531 3918198. 0929-1393/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved. PII S0929-1393(97)00050-4
with the surrounding soil (Edwards and Bohlen, 1996). Water stability is one of the most important properties affecting soil detachment by rain impact (Rasiah and Kay, 1995). Because of the use of heavy machinery on forest and agricultural soils the determination of soil stability becomes more and more important to assess soil health by mechanical parameters (Braunack et al., 1979). Schrader and Zhang (1997) studied how different soils affected the ef®ciency of earthworm castings in stabilizing soil structure and concluded that the more sensitive a soil to physical disturbance the greater the effect of castings on water stable aggregation and the less their effect on tensile strength. The aim of the present study was to
264
M. Flegel et al. / Applied Soil Ecology 9 (1998) 263±269
examine the in¯uence of different food sources on the cast properties of different detritivorous earthworm species in relation to their in¯uence on soil structure. 2. Material and methods 2.1. Experimental conditions A laboratory experiment was conducted in order to obtain the casts of different earthworm species fed on various food sources. The earthworms were separated into species and kept in special microcosms consisting of two parallel glass sheets ®lled with sieved soil aggregates of de®ned diameter. For each diet treatment the food was offered on the soil surface. The duration of the experiments varied between 4 and 6 weeks. Lumbricus terrestris L., Lumbricus rubellus Hoffm. and Dendrobaena octaedra (Sav.) were chosen as representatives of the detritivorous earthworm group. For each diet treatment the casts of 25 specimens of L. terrestris and L. rubellus and 56 of D. octaedra were collected and individual cast production in milligram dry weight per gram live weight and day was calculated. The experiments were carried out with the leaves of six plant species with a wide range of C/N-ratios. Fresh leaves of dandelion (Taraxacum of®cinale, N: 3.59%, C/N: 11), lupin (Lupinus polyphyllus, N: 4.50%, C/N: 9), rye (Secale cereale, N: 1.23%, C/N: 31) and alder (Alnus glutinosa, N: 2.98, C/N: 15) and half year old leaves from the litter layer of beech (Fagus sylvatica, N: 0.91%, C/N: 48) and larch (Larix decidua, N: 1.01%, C/N: 42) were collected in the vicinity of Braunschweig. The leaves were air-dried and cut into 1±2 cm2 pieces. The soil used was a Gleyic Luvisol (FAO) from the Ap-horizon of a loamy soil taken from arable land near Neuenkirchen (Lower Saxony, Germany). For detailed information on the soil see Othmer and Bork (1989). The soil aggregates used were 1±2 mm in diameter for L. terrestris, and 0.5±1 mm for L. rubellus and D. octaedra. 2.2. Chemical and biochemical measurements Nitrogen and carbon content of the leaves was analysed by the macro-elementanalyser LECO CHN-1000 (Leco, Kirchheim, Germany). The total
nitrogen content (Nt) of soil and casts was estimated by the Kjeldahl method (Kandeler, 1993). In order to include nitrate, nitrite, nitro and nitroso groups also, 25 g of salicylic acid were added per litre of sulphuric acid. Organic carbon content (Corg) of soil and casts was determined by a macro-carbonanalyser (Leco Carbon Determinator IR 12, Leco, Michigan USA). Acid (SPA) and alkaline (APA) phosphomonesterase activity (buffer-pH: 6.5 resp. 11) were analysed by the method of Tabatabai and Bremner (1969) modi®ed by Margesin (1993) at 378C. The phosphomonesterase activity was calculated in microgram nitrophenol per gram dry mass and hour [mgNP/g/h]. 2.3. Physical measurements The amount of water stable aggregates (WSA) was determined by the method of Kemper and Rosenau (1986) modi®ed by Hartge and Horn (1989) (n5). The tensile strength (TS) of air-dried aggregates was determined by the crushing-test (n50). The aggregates were placed on an electrical balance and were cracked with a monoaxial operating pressure apparatus. The force used for cracking an aggregate (F) was calculated by the equation of Dexter and Kroesbergen (1985): t 0:576 F=d2 where t is the aggregate tensile strength, F is the crushing force and d is the aggregate diameter. Soil and cast textures were determined by the method of Moschre® (1983). 3. Results and discussion 3.1. Cast production (CP) The CP of all earthworm species was strongly in¯uenced by plant species (Fig. 1). Only the CP of L. terrestris was relatively constant between 279 and 318 mg/g/d while feeding on dandelion, lupin, beech and larch. With 812 and 835 mg/g/d D. octaedra produced the highest amounts of casts while feeding on larch and beech respectively, and showed the lowest CP when offered dandelion. For D. octaedra the CP was signi®cantly negatively correlated with the C/N-ratio of the food (Rÿ0.97, p0.013) and was
M. Flegel et al. / Applied Soil Ecology 9 (1998) 263±269
265
Fig. 1. Cast production (CP) of the earthworm species for each diet treatment.
meter and a constant C/N-ratio for different aggregate sizes were also reported by Scheu et al. (1996). Corg of L. terrestris casts was at all times higher than Corg of soil aggregates, because the animals were able to feed on and digest all the diets. Corg enrichment of L. rubellus and D. octaedra casts was only recorded when the animals fed on dandelion and rye and dandelion and lupin, respectively (Table 1). Scheu and Parkinson (1994) showed that D. octaedra consumes large quantities of soil microorganisms. It was concluded that with a deterioration of diet quality this species increased its consumption of soil aggregates in order to satisfy its nutrient requirements. Because of the digestion of soil Corg, this geophagous behaviour led to reduced Corg in the casts. L. rubellus
high signi®cant negatively correlated with food consumption (Rÿ0.92, p0.009) because a deterioration in food quality provokes higher soil consumption followed by higher cast production (Flegel and Schrader, 1998). L. terrestris and L. rubellus had their highest CP with 461 and 473 mg/g/d, respectively while feeding on alder. When offered rye L. terrestris and L. rubellus produced 228 and 192 mg/g/d, respectively, the lowest amounts of casts. Shipitalo et al. (1988) reported that L. rubellus produces casts at a higher rate per unit weight of worm (80±460 mg/g/d) than L. terrestris (70±180 mg/g/d) when fed on leaves with C/N-ratios between 11 and 26. Their data for L. rubellus agree well with the CP values of 192± 473 mg/g/d in the present study, but in contrast to their studies the CP of L. terrestris in the present study (226±461 mg/g/d) showed no great difference from the CP of L. rubellus.
Table 1 Chemical properties of the earthworm casts
3.2. Chemical properties of soil and cast aggregates
Food
The C content of soil aggregates between 0.5 and 1 mm was 1.85%, Corg was 1.79% and Nt was 0.165%, higher values than those of the aggregates between 1 and 2 mm with C1.59%, Corg1.54% and Nt0.151%. The C/N-ratio of both aggregate sizes was the same (11). An increase in nitrogen and carbon content with decreasing aggregate dia-
Dandelion Lupin Rye Alder Beech Larch
L. terrestris
L. rubellus
D. octaedra
Corg [%]
Nt [%]
Corg [%]
Nt [%]
Corg [%]
Nt [%]
1.99 1.76 1.73 1.73 1.79 1.80
0.196 0.181 0.168 0.172 0.157 0.167
1.99 1.76 2.09 1.71 1.65 1.79
0.250 0.200 0.189 0.189 0.170 0.188
1.87 1.85 1.68 1.63 1.64 1.56
0.262 0.233 0.181 0.169 0.167 0.162
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Fig. 2. Amount of water stable aggregates (WSA) of the soil and the cast aggregates for each diet treatment.
might also have used soil Corg for its nutrient requirement. 3.3. Water stable aggregation (WSA) The WSA content of all cast aggregates was signi®cantly higher than the WSA (21%) of the soil aggregates (Fig. 2). Higher WSA of casts compared with the surrounding soil has been reported by several authors (summarised by Edwards and Bohlen, 1996). For all earthworm species the increase in WSA was highest when offered dandelion and lowest when fed on alder. The casts of D. octaedra had the highest WSA content (81%) followed by the casts of L. rubellus and L. terrestris with WSA content of 80 and 73%, respectively. The lowest values of WSA were determined for casts of D. octaedra and L. terrestris (40%) and for the casts of L. rubellus (42%). The WSA of the casts was correlated with their Corg (R0.79, p<0.001), a similar ®nding to that reported by Zhang and Schrader (1993). In order to compare the effects of the different earthworm species, the percent WSA increase in casts was correlated with percent change in Corg. Assuming equal Corg (dCorg0) the extrapolation (Fig. 3) showed that L. terrestris raised WSA by 37% while L. rubellus and D. octaedra increased WSA by 170 and 217%, respectively. It must be taken into account that the
Corg of the soil aggregates used for L. terrestris was about 14% lower than the Corg of the 0.5±1 mm soil aggregates used for L. rubellus and D. octaedra. The extrapolated WSA content (155%) of the casts of L. terrestris for a soil aggregate Corg of 1.79%, however, was still the lowest, while the casts of D. octaedra had the highest WSA of all earthworm species. It was concluded that the quantity of Corg is not the only factor in¯uencing WSA: passage through the earthworm intestine also improves WSA and this increase is highly species speci®c. Microorganisms play the key role in stabilizing aggregates (Lynch and Bragg, 1985). Biochemical measurements showed a signi®cant correlation between APA (R0.53, p0.024), and a highly signi®cant correlation between SPA (R0.61, p0.007) and WSA of earthworm casts (Fig. 4). Phosphomonesterases are good indicators for microbial biomass and microbial activities (Nannipieri et al., 1979; Domsch et al., 1979; Frankenberger and Dick, 1983). Thus these results agree with the investigations of Metzger et al. (1987) who found that higher microbial biomass induces greater WSA. Reasons for a microbial biomass increase in the casts are an elevated nitrogen supply (Flegel and Schrader, 1996) and microbial stimulation in the intestines of the earthworm species (Parle, 1963; Kristufek et al., 1992). The main reason for the different WSA increases might be species speci®c intestinal conditions in the three
M. Flegel et al. / Applied Soil Ecology 9 (1998) 263±269
267
Fig. 3. Correlations between the percent change in the amount of water stable aggregates in casts (dWSA) of the three earthworm species and the percent change in organic carbon content of casts (dCorg) compared with the soil.
Fig. 4. Correlation between acid (SPA) and alkaline (APA) phosphomonesterase activities of earthworm casts and their percent water stable aggregate (WSA) content.
earthworm species which cause different development of the micro¯ora. 3.4. Tensile strength (st) Like the WSA content, the t values of the casts were also species speci®c. For each diet treatment t values were highest for L. terrestris and lowest for
D. octaedra (Fig. 5). Because no statistically signi®cant in¯uence of diet could be determined, the casts of each diet treatment were added to obtain species speci®c data. Only the t of 654 kPa calculated for the casts of L. terrestris showed no signi®cant difference compared with the t of the soil aggregates. Zhang and Schrader (1993) also found no differences between the t of the cast aggregates of L. terrestris
268
M. Flegel et al. / Applied Soil Ecology 9 (1998) 263±269
Fig. 5. Tensile strength (t) of soil and the cast aggregates for each diet treatment. Bars indicates the standard deviations.
compared with soil aggregates. The t values of the cast aggregates of L. rubellus and D. octaedra were 585 and 507 kPa, respectively and were different at the highest signi®cance level from the t of the soil aggregates. Therefore, only the casts of L. terrestris maintained soil t. The t of aggregates is in¯uenced by their water and clay content (Gill, 1959). Because of identical water contents of cast and soil aggregates (3%, air-dried) and equal texture patterns (clay: 18%, silt: 80% and sand: 2%), these factors are ignored in the following discussion. The t of cast aggregates decreases with raising porosity (Dexter et al., 1984). Bal (1973) characterises the cast-shape of D. octaedra as `bacillocylindric'. These casts only form a `weakly welded' cast cluster. In contrast to D. octaedra, Bal (1973) describes the shapeless casts of L. terrestris as `strongly welded'. Because the single casts of L. terrestris are joining in a very compact way, it was concluded that their porosity is similar to soil porosity and less than the porosity of the `weakly welded' casts of D. octaedra. The casts of L. rubellus might form an intermediate cast cluster. 4. Conclusions The food source strongly in¯uences consumption rates and cast production by earthworms. Stimulation
of the soil micro¯ora is an important effect of earthworms which improves the WSA of soil aggregates. Because the nutrient content of casts in¯uences the WSA increase, good digestive nutrient enriched food guarantees a high WSA elevation. The in¯uence of earthworms on WSA and tensile strength is species speci®c, but these soil properties are affected in an opposite way. Acknowledgements Prof. Dr. O. Larink is acknowledged for valuable advice. We also thank K. Brinkmann, K. Steffens, M. Kondermann and G. Schnelle for technical assistance. We were supported by the Stifterverband fuÈr die Deutsche Wissenschaft. References Bal, L., 1973. Micromorphological analysis of soils. Soil Survey Papers No. 6. Soil Survey Institute, Wageningen, The Netherlands. Braunack, M.V., Hewitt, J.S., Dexter, A.R., 1979. Brittle fracture of soil aggregates and the compaction of aggregate beds. J. Soil Sci. 30, 653±667. Dexter, A.R., Kroesbergen, B., 1985. Methodology for determination of tensile strength of soil aggregates. J. Agric. Eng. Res. 31, 139±147.
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