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Collembola populations in an organic crop rotation: Population dynamics and metabolism after conversion from clover-grass ley to spring barley
Pedobiologia 44, 502–515 (2000) © Urban & Fischer Verlag http://www.urbanfischer.de/journals/pedo
PROCEEDINGS OF VTH INTERNATIONAL SEMINAR ON APTERYGOTA, CORDOBA 1998
Collembola populations in an organic crop rotation: Population dynamics and metabolism after conversion from clover-grass ley to spring barley Henning Petersen Natural History Museum, Mols Laboratory, Femmøller, DK 8400 Ebeltoft, Denmark Accepted: 10. December 1999
Summary Population dynamics of earthworms, enchytraeids, mites and collembolans were assessed over two years as part of a collaborative research project in an organic crop rotation at the agricultural Research Centre Foulum, Jutland, Denmark. The Collembola study presented here is restricted to the first growth season of a two-year study, i.e from just before conversion of a two year old clover-grass ley to seedbed until harvest of the barley crop. The results refer mostly to the four most abundant species. The project included experimental reductions of earthworm populations to test the effects on interactions between earthworms and mesofauna. Expulsion by electro-shocking resulted in modest reductions in earthworm density and biomass. No significant effect of the reduction was observed on the collembolan populations. Total collembolan density and density, mean weight per specimen, biomass and population metabolism of the four most abundant species decreased markedly between the first and second sampling date as an effect of the mechanical disturbance, and inversion of soil layers caused by soil preparation. The depth distribution for all Collembola species was inverted from highest concentration in the 0–10 cm layer to highest concentration in the 10–20 cm soil layer. After a population minimum in May, the density, mean weight, biomass and metabolism increased more or less regularly according to species. The net loss of biomass after conversion implied a mobilization of 5 mg N.m-2 from dead collembolan tissues. Together with an estimate for nitrogen due to excretion, the contribution of Collembola to nitrogen mobilization through the growth season was estimated tentatively as 10 mg.m-2. This amount was negligible compared with the cone-mail: [email protected]
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tribution of earthworms. The possibility that indirect catalytic effects of collembolan activity could have any significant effect on nutrient availability for plants was not resolved but the collembolan population metabolism showed no obvious synchrony with the nutrient requirements of the crop. Key words: Collembola, organic farming, earthworm interaction, biomass, population metabolism, nitrogen flux
Introduction Organic farming has gained increasing popularity during the last decades with the background of a growing public concern about contamination of food and environment by pesticides and other chemicals used in conventional agriculture. This is happening in Europe and globally. In Denmark, where agriculture is a main national product the interest in organic farming has increased markedly from the early nineties where less than 1 % of agricultural land was grown organically until the end of the decade when – in 1998 – 3.7 % of the agricultural land was converted to organic farming (Anonymous 1999). This increase depends on the willingness of the population to pay a higher price for the products. This was most convincingly proved for milk products where 20 % of the liquid milk sold in Denmark in 1998 was produced by organic farms (Anonymous 1999). This is the background for a large research effort initiated jointly by the Danish Ministry of Environment and the Ministry for Foodstuffs, Agriculture and Fishery, with the purpose of understanding basic ecological processes in organic farming systems and improving the agricultural methods and practices needed to optimize economic returns and environmental benefits. The fundamental idea of organic farming is to involve natural ecological processes, so practices used should aim at supporting and utilizing ecological processes as far as possible. The research programmes in organic farming are organized as an inter-institutional centre “Danish Research Centre for Organic Farming (DARCOF)”. A subproject within this organization is a field experiment seeking information on (1) the timing of population development and metabolism of soil meso- and macrofauna in relation to nitrogen dynamics and the growth of crop plants and (2) the interaction between earthworms and the mesofauna. The first hypothesis advanced is that the soil fauna, by feeding on microfungi and bacteria, may help to mobilize nitrogen and other nutrients and thus make them available for uptake by plant roots. Experimental evidence for such an indirect catalytic effect has been provided by Anderson et al. (1985), Hanlon & Anderson (1979), Ineson et. al. (1982) and Setälä & Huhta (1990, 1991). Furthermore, nutrients may be stored in the biomass of soil animals and released by excretion or following the death of the animals (Ausmus et al. 1976; Christensen 1987). The timing of these processes in relation to the demands of the crop plants is important for the most efficient utilization of manure and the prevention of leaching to the deeper soil layers and the ground water. The second hypothesis is because earthworms are, in terms of biomass and activity, by far the most important group of soil animals in the agricultural system studied here. In a long-term study carried out in the same experimental farm as the pre-
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sent experiment Christensen & Mather (1997) found a mean of 31 earthworms per m2 in the conventionally-farmed corn field, just before conversion to organic farming practice in 1986. During the following 11 years of organic farming the earthworm densities increased rapidly and reached a maximum of more than 600 per m2 in the clover-grass field of the organic crop rotation in 1977, i.e. a 20 times increase during a decade. It was envisaged that such a large earthworm population might influence other organisms in the soil. Therefore, in order to quantify effects on the soil biota, nitrogen turnover and plant growth it was attempted to include an experimental reduction of earthworms as a treatment in the experiment. Preliminary results are presented on the development of the collembolan population from the first part of the study period, i.e. from immediately before the plowing of the two year old grass-clower sward to the harvest of the barley sown after the soil preparation. Population density estimates are presented for all species and biomass and metabolic rates are presented for the four most abundant collembolan species.
Materials and Methods The experiment was in a field with an organic crop rotation (Field S02) at the Agricultural Research Centre Foulum near Viborg, Jutland, April 1997 – March 1999 . The present results are based on the first five samplings in 1997. The first of these was April 1 1997 in the clover-grass field just before conversion to seedbed. The soil preparation included rotary-tilling of the clover-grass sward followed by plowing, packing and harrowing. The field was sown with barley, peas and rye grass but peas were avoided within the experimental plots. The following four samples were in the succeeding barley-rye grass field (May 20, June 9, July 7 and August 14). The last sampling coincided with harvest. The experiment was arranged as a randomized block design with 5 blocks, each with 2 plots (4 × 3 m). Part of the earthworm population was expelled by electro-shocking (Bohlen et al. 1995) from one randomly chosen plot in each pair just after sowing in April 1997. The other plot was an unmanipulated control. Each plot was surrounded by a plastic barrier to prevent migration of earthworms. Two sampling quadrats (0.25 m2) were selected randomly within each plot for each sampling date. Cylindrical soil cores (surface area: 79 cm2, depth: 0–10 cm and 10–20 cm) were sampled for microarthropod extraction on the same dates and within the same sampling quadrats as soil samples used for extraction of earthworms and Enchytraeidae and samples for measurement of nitrogen pools. Microarthropods were extracted in modified high gradient funnel extractors (Gjelstrup & Petersen 1987). The surface temperature was increased gradually from 30°C to 60°C during an extraction period of 10 days. Mean dry weights per individual were based on body length measurements of randomlyselected specimens representing each species at each sampling date. Only the results for the four most abundant species/species groups, i.e. Mesaphorura spp. (mostly M. macrochaeta Rusek 1976), Folsomia fimetaria (Linné 1758), Isotoma notabilis Schäffer 1896, and Isotoma anglicana Lubbock 1862 (distinguished from I. viridis Bourlet 1839 according to Fjellberg 1980). The number of replicated measurements depended on the availability of suitably extended specimens and varied between samples. The number of specimens measured in each sample were 25–39 for Mesaphorura spp., 22–33 for F. fimetaria, 24–38 for I. notabilis and 10–25 for I. anglicana. The mean dry weights were calculated using regression equations reported in Petersen (1975). The equations for F. quadrioculata were used for F. fimetaria and the equation for juvenile I. notabilis was used for all sizes of I. anglicana. Biomass was obtained by multiplication of density by mean individual dry weight.
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The mean respiratory rate per individual as oxygen consumption was calculated from the individual dry weights and the mean soil temperature in 10 cm depth during the period from 10 days before to 10 days after each sampling date according to regression equations in Petersen (1981). The respiration of Mesaphorura spp., F. fimetaria and I. anglicana was calculated using the regression equations reported for Tullbergia krausbaueri, Folsomia quadrioculata s.l. and I. notabilis, respectively. Population respiration representing the sampling dates was calculated by multiplication of mean individual respiratory rate by density of individuals. Carbon and nitrogen contents of the collembolan biomass were calculated using the percentages in relation to dry weight, i.e. 52.4 % and 11.8 %, respectively, reported by Persson (1983). Reference is made to unpublished results of carbon- and nitrogen flux based on efficiencies and carbon/nitrogen- ratios used in Persson (1983), Hunt et al. (1987) and Ruiter et al. (1993).
Results Although about a third of the earthworm biomass was removed from the treatment plots by a fairly intensive electro-extraction, the reduction in earthworm populations observed in these plots, compared with the non-treated control plots, was only statistically significant in the first (biomass) and third sample (biomass and density) following electro-extraction (O.M. Christensen & J.G. Mather in prep.). The numbers of total Collembola in the earthworm manipulated and control plots did not differ significantly on any sampling date (Fig. 1) and the preliminary conclusion is that the relatively small population reduction of earthworms did not result in any observable effects on collembolan population density. Consequently, the data gained from the earthworm-manipulated plots and the control plots were pooled in the following data analysis.
Fig. 1. Comparison between collembolan mean densities in plots where earthworm populations were reduced with electro-extraction and unmanipulated control plots. Number of replicates: 5. Error bars: standard error of mean density
The populations of Collembola decreased markedly in both manipulated and control plots between the first sampling in April and the second sampling in May (Fig.1). The decrease amounted to 70 % of the density measured on the first sampling date. In the beginning of that period, soil preparation and sowing were done and the strong decrease in collembolan numbers was probably caused by these physical disturbances and the subsequent exposure of the bare soil surface. The decrease was very marked in the uppermost 10 cm of the soil and an increase occurred in the 10–20 cm horizon
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Fig. 2. Mean density of total Collembola in 2 depths (full drawn line: 0–10 cm, dotted line: 10–20 cm). Number of replicates: 10. Error bars: standard error of mean density
Fig. 3. Mean density of 4 collembolan taxa in 2 depths (full drawn line: 0–10 cm, dotted line: 10–20 cm). Number of replicates: 10. Error bars: standard error of mean density
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(Fig. 2). This resulted in an inversion of the depth distribution which remained for the rest of the investigation period. The strong decrease in the surface soil Collembola population between the first and second sampling was repeated for the four most abundant collembolan taxa in the present habitat (Fig. 3): Mesaphorura spp., F. fimetaria, I. notabilis and I. anglicana. These species together made up 71–87 % of the total Collembola populations. In Mesaphorura spp. and F. fimetaria, the largest population density occurred in the deeper soil layer for the rest of the study period while I. anglicana and later I. notabilis changed to be predominant in the surface layers during the summer. There were marked differences in time patterns between species for the mean individual dry weights (Fig. 4) but for all taxa a population decrease occurred between the sampling dates before and after soil preparation in the spring indicating a change from populations dominated by large adults, to populations dominated by small juveniles. During the remainder of the spring and summer the mean individual dry weights increased and then decreased. These changes in population structure can be ascribed to varying combinations of mortality and multiplication. The population biomass of the four species increased for a shorter or longer time after the initial decrease following soil preparation (Fig. 5). For Mesaphorura spp. a second decrease occurred in the July sample and in I. notabilis a decrease was observed in the August sample. Together the biomass of the four common species decreased by 42 mg (dry weight).m-2 or 90 % of the initial biomass during the period when the clover-grass sward was ploughed and the soil prepared for the barley crop (Table 1). The sum of the biomass decreased during the following periods by 5 mg (dry weight).m-2. The net losses of carbon and nitrogen from the four species were calculated as 22 and 5 mg.m-2, respectively, during the first period (Table 1) and 25 and 6 mg.m-2, respectively, during the whole period. The changes in respiration rates of the four collembolan populations through the period (Fig. 6) were the results of changes in population density, mean size distribution and mean soil temperatures from 10 days before the sampling dates to 10 days after. Except for Mesaphorura spp. the population respiration reached a minimum in May and June. The sum of the respiration rates of these four most abundant species increased steadily from the May – to the August sample where the respiration rate was higher (1.2 µl.m-2.day-1) than at the initial sampling date (0.9 µl.m-2.day-1). Table 1. Initial biomass and net losses ± standard error of mean (mg.m-2) for the four most abundant collembolan taxa during spring 1997 when the grass-clover sward was converted to a spring barley field. – Dwt: biomass or net loss as dry weigt, C: carbon content, N: nitrogen content. Means and standard errors based on 10 replicates per sample Species
Mesaphorura spp. F. fimetaria I. notabilis I. anglicana Sum 4 taxa
Biomass April 1 ——————— Dwt 3.78 ±00.62 18.44 ±08.73 5.01 ±01.13 20.49 ±08.54 47.71 ±13.08
Net Loss April 1 – May 20 ———————————————————— Dwt C N 3.21 ±00.68 1.68 ± 0.35 0.38 ± 0.08 15.49 ±08.72 8.12 ± 4.57 1.83 ± 1.03 3.69 ±01.14 1.93 ± 0.60 0.44 ± 0.14 20.06 ±08.54 10.51 ± 4.48 2.37 ± 1.01 42.45 ±13.33 22.24 ± 6.99 5.01 ± 1.57
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Fig. 4. Mean dry weight per specimen in µg of 4 collembolan taxa in 0–20 cm depth. Number of replicates: 10. Error bars: standard error of mean dry weight
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Fig. 5. Mean population biomass (dry weight) in mg.m-2 for 4 collembolan taxa in 0–20 cm depth. Number of replicates: 10. Error bars: standard error of mean biomass
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Fig. 6. Mean population metabolic rate: Oxygen consumption in ml.m-2.day-1 for 4 collembolan taxa in 0–20 cm depth. Number of replicates: 10. Error bars: standard error of mean
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Discussion Conventional farming practices rely to a large extent on methods which aim at controlling or altering the natural state of the soil environment. Conversely, organic farming is based on the best possible utilization of naturally-occurring ecological processes in soil. One of the most important of these processes, relevant to organic farming, is the decomposition of dead plant material and organic manure to provide nutrients to crop plants. The microflora, fungi and bacteria, are mainly responsible for this process but the soil fauna may contribute significantly to the nutrient flux both directly (e.g. Hunt et al. 1987; Christensen 1987), and indirectly, as catalyzers (e.g. Anderson et al. 1985; Hanlon & Anderson 1979; Ineson et. al. 1982; Lussenhop 1992; Seastedt 1984 and Setälä & Huhta 1990, 1991). With that background it seems interesting to attempt a quantification of the role of the soil fauna related to nutrient mobilization in organic fields and to which degree the timing of the effects of the soil fauna is synchronized with the needs of the crop plants for available nutrients. The whole complex of soil invertebrates is involved in these processes and each taxon may have a specific role although present knowledge is restricted to a crude classification into trophic levels and ecotypes related to size of specimens (micro- , meso-, macrofauna) and preferred microhabitats (e.g. soil depth). One objective of the present study was to investigate interactions between the important faunal groups and the consequences of such interactions on the performance of the soil community in relation to nitrogen transfer. The experimental reduction of earthworms included in the present field experiment failed to show any effects on the density of Collembola during the first five months. However, laboratory microcosm experiments included in the same research project as the present study (J. Filser & P.H. Krogh in prep.) have demonstrated effects of interactions between mesofauna taxa on nitrogen uptake in barley plants. The effects of the fauna on soil processes depend on the size of populations. It may be expected that the density and biomass of the fauna in organic field soils are larger than in the soil of conventionally-managed agricultural fields because of the use of organic fertilizers, the avoidance of pesticides and the use of crop rotations including grass- and clover leys or fallow. This seems to be confirmed for the earthworms although great variations have been found between organic farms in Denmark due to e.g. soil type and time since conversion from conventional to organic farming (Christensen & Mather 1997). Krogh (1994) monitored the microarthropod populations in one conventional, two integrated and one organic field system at the Research Centre Foulum, Jutland, through 6 years. He found that Collembola were most abundant in the organic and integrated grain system but significantly less abundant in the integrated forage system and the conventional system. The population size, however, was strongly dependent on the composition of different crops in the rotations and it was suggested that the use of chemical fertilizers and pesticides was less important than the crops in the rotation and type of cultivation practices such as mulching, plowing and harrowing. Thus, the microarthropods were almost three times as abundant in the organic clover grass ley as in the annual crops and fallow fields of the same farming system. On the other hand, Petersen & Gjelstrup (1995) found long-lasting inhibition of collembolan population growth in field mesocosms sprayed with recommended dosages of the insecticide dimethoate. The present study did not aim at a comparison between organic and conventional
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agricultural systems and the data on collembolan population size obtained so far does not provide evidence that organic farming practice “per se” favours collembolan populations in comparison with conventional farming systems with similar crop rotation, cultivation practice and use of organic fertilizers. The greatest abundance of Collembola was in the clover-grass field before soil preparation (12.300.m-2) and at harvest in August (17.900.m-2) and the lowest in May (3.600.m-2). The population density in August was similar to the mean density from several fields during six years in the organic farming system (16.900.m-2) reported by Krogh (1994). Collembolan numbers reported from conventional cereal fields, supplied with chemical fertilizers, are generally lower. Thus, the conventional system studied by Krogh (1994) had a 6-year mean of 6.800.m-2, Lagerlöf & Andrén (1991) reported 11.300.m-2 as a 5-year mean for September samplings in a Swedish barley field supplied with 120 kg N.ha-1.year-1 and Hendrix et al. (1986) reported 6.200.m-2 for a conventionally tilled sorghum/rye cropping system i Georgia, U.S.A. However, conventional grass- and lucerne ley fields, in a study by Lagerlöf & Andrén (1991), developed collembolan faunas with population densities comparable to or higher than the August sample of the present study (16.500 and 30.400.m-2, respectively) and no-tillage systems of the Georgia study (Hendrix et al. 1986) contained a mean of 14.700.m-2. After a steep decrease, following the conversion of the clover-grass field, the biomass of the four most abundant Collembola species increased steadily through the spring and summer but, contrary to the density, the biomass was still much lower in August (15.1 mg (dry weight).m-2) than in early spring because of the dominance of small juvenile specimens. The biomass in August was only a little higher than the mean of September samples, from the conventional, fertilized barley field studied by Lagerlöf & Andrén (1991), and similar to the conventional tillage treatment reported by Hendrix et al. (1986), while the initial biomass in April was similar to the biomass reported for the Swedish lucerne field (Lagerlöf & Andrén 1991) and the no-tillage treatment of the Georgian study (Hendrix et al. 1986). A Dutch study (Ruiter et al. 1993) reported the carbon contents of Collembolan populations which shows that Collembolan biomass in both conventional and integrated farming systems (in both systems more than 100 mg dwt.m-2) was more than twice as high as the highest biomass found in the present study. The soil fauna may cause mobilization of nutrients such as nitrogen in both direct and indirect ways. Thus, their most important direct contributions are excretion of nutrients as part of the metabolic flux, and death in other ways than by predation, where easily decomposable and nutrient rich animal tissue becomes available for rapid mineralization (Christensen 1987). Several indirect effects include: stimulation of microbial turnover and mobilization of nutrients by comminution of dead organic material and grazing on microbial colonies (e.g. Hanlon & Anderson 1979; Ineson et al. 1982; Lussenhop 1992), alterations of the composition of microflora, e.g. by selective grazing or transport of spores (Setälä & Huhta 1991; Lussenhop 1992; Visser 1985) and changes of the physical and chemical structure of the soil matrix. In the present study, a minimum estimate of the contribution to nitrogen mobilization through mortality of the four most common collembolan species was calculated as 5 mg.m-2 from the net decrease of biomass during the period between April 1 and May 20 (Table 1). For the whole period reported here, i.e. April 1 to August 14, the sum of net nitrogen mobilization through mortality amounted to 6 mg.m-2. The strong disturbance including inversion of the upper 20 cm of the soil caused by soil prepara-
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tion which probably explains most of the net decrease of total collembolan density and density and biomass of the four most abundant species during the period between the two first samplings, but also the long exposure of the more or less bare soil surface during the first part of that period may have contributed to the decline of the collembolan population. The observed biomass decrease was a net loss and does not include the loss of biomass produced during the period. Calculations of nitrogen fluxes through excretion (Petersen et al. in prep.) based on population respiration data and parameters of efficiencies and C/N-ratios borrowed from the literature (Persson 1983; Hunt et al. 1987) resulted in flux rates for the four common species during the five spring and summer months considered here which amounted to 2.4–2.8 mg N.m-2. Together with the amount of nitrogen mobilized through death af animals, including N in dead biomass produced between sampling dates, the nitrogen mobilization as a direct contribution by Collembola populations during spring and summer may be tentatively estimated as about 10 mg N.m-2. This is more than the 2.6 mg N.m-2.yr-1 (death: 1.1 mg.m-2.yr-1, inorganic N: 1.5 mg.m-2.yr-1) reported for Collembola by Hunt et al. (1987) and about half of 0.21 kg N.ha-1.yr-1 reported by Ruiter et al. (1993). Ruiter et al. described the contributions by Collembola and other microarthropods as negligible, in their conventional and integrated farming systems, in comparison with the contribution by especially amoebae and bacterivorous nematodes. In the farming systems studied by Ruiter et al. (1993) earthworms were rare or missing. In the present study earthworms were extremely abundant in the clover-grass field before conversion to seedbed and the earthworm densities and biomass were strongly reduced after the soil preparation. Although the calculation of earthworm contributions to the nitrogen flux are not yet available the direct contribution of Collembola to nitrogen mineralization is certainly extremely small in comparison. Results from a conventionally-cultivated Danish farm fertilized, by inorganic as well as organic fertilizers (Christensen 1987), which had an earthworm population size approaching that of the site studied here showed that the annual N-output as excreted ammonia was 450 mg.m-2.yr-1 and the input from dead earthworm tissue was 3,600 mg.m-2.yr-1. Although the direct contribution of Collembola to nitrogen fluxes in the organic farming system were small it is still possible that the indirect effect through interactions with the microflora is ecologically significant, especially when considering the close attachment of the collembolan fauna to the rhizosphere (Lussenhop 1992). Seastedt (1984) reported increases in decomposition rates of tree leaf litter from a number of studies from 4 to 69 % attributable to the effect of microarthropods. Beare et al. (1992) found that exclusion of fungal-feeding microarthropods from surface litter, in fields with no-tillage treatment, had little effect (less than 5 % reduction) on litter decomposition but that the microarthropods were more important in mobilizing nitrogen by grazing on the litter inhabiting fungi. Both direct effects and possible indirect catalytic effects on nitrogen mobilization, through interaction with microflora are correlated with the metabolic activity of the population as for instance expressed by the repiratory rate. The population respiration of the four most common species presented here dropped steeply together with the density and biomass between first and second sampling in spring as the effect of soil preparation. Thereafter, it increased and was higher in August than at the initial sampling before conversion of the clover-grass to seed bed.
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The requirement of the crop plants for available nutrients was correlated with growth and was therefore highest during spring and early summer. During the periods considered in the present paper, a close timing between collembolan activity and the need of the crop plants for available nutrients which might support hypotheses concerning an important role of these abundant soil animals was not apparent. Instead, a considerable drop in population biomass, and consequently a strong decrease in population metabolism, was observed during the time when the plants germinated and started growth. The drop in population biomass was the consequence of large mortality due to the mechanical disturbance and inversion of the soil, which made most of the collembolan tissue available for mineralization by the microflora. However, the amount of nutrients made available for plants from dead collembolan corpses appears negligible as compared to the simultaneous input of dead earthworm tissue.
Acknowledgements The study is part of project I.7. “Interaction between soil fauna, nitrogen dynamics, and plant growth – Experimental research and simulation modelling” under the Danish Centre for Organic Farming (DARCOF) and was financed by the The Strategic Environmental Research Programme (SMP) and the Natural History Museum, Aarhus. The other participants in the project are acknowledged for perfect cooperation and profitable discussions during the course of the project. Research Centre Foulum with the experimental farm Foulumgaard, is thanked for carrying out the practical field work and providing temperature data. Ole M. Christensen and Janice G. Mather, University of Aarhus, are thanked for allowing unpublished data on earthworms from the site to be quoted in the present paper. Laboratory technician Anni Kjeldsen and Anne Birgitte Raghner, Mols Laboratory, are thanked for indispensable technical assistance in the field and in the laboratory.
References Anderson, J.M., Huish, S.A., Ineson, P., Leonard, M.A., Splatt, P.R. (1985) Interactions of invertebrates, micro-organisms and tree roots in nitrogen and mineral element fluxes in deciduous woodland soils. In: Fitter, A.D. (ed) Ecological interactions in soil. Blackwell Scientific Publications, Oxford, pp. 377–392. Anonymous (1999) Action plan II. Developments in organic farming. The Danish Directorate for Development. The Danish Ministry of Food, Agriculture and Fisheries (english summary). 47 pp. Ausmus, B.S., Edwards, N.T., Witkamp, M. (1976) Microbial immobilisation of carbon, nitrogen, phosphorus and potassium: implications for forest ecosystem processes. In: Anderson, J.M., Macfadyen, A. (eds) The role of terrestial and aquatic organisms in decomposition processes. Blackwell Scientific Puplications, Oxford, pp. 397–416. Beare, M.H., Parmelee, R.W., Hendrix, P.F., Cheng, W., Coleman, D.C., Crossley, D.A., Jr. (1992) Microbial and faunal interactions and effects on litter nitrogen and decomposition in agroecosystems. Ecological Monographs 62, 569–591. Bohlen, P.J., Parmelee, R.W., Blair, J.M., Edwards, C.A., Stinner, B.R. (1995) Efficacy of methods for manipulating earthworm populations in large-scale field experiments in agroecosystems. Soil Biology and Biochemistry 27, 993–999. Christensen, O. (1987) The effect of earthworms on nitrogen cycling in arable soils. In: Striganova, B.R. (ed) Soil Fauna and Soil Fertility. Proceedings of the 9th International Colloquium on Soil Zoology, Moscow. Nauka, pp. 106–118.
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Christensen, O.M., Mather, J.G. (1997) Regnorme som øko-ingeniører i jordbruget: fra konventionelt til økologisk jordbrug. (Earthworms as eco-engineers in agriculture: from conventional to organic agriculture). In: Kristensen, E.S. (ed.) Økologisk planteproduction. SP rapport 15, 135–142 (in Danish). Fjellberg, A. (1980) Identification keys to Norwegian Collembola. Norsk Entomologisk Forening, Ås, 152 pp. Gjelstrup, P., Petersen, H. (1987) Jordbundens mider og springhaler (Mites and springtails in the soil). Natur og Museum, Århus 26(4), 31pp. (in Danish). Hanlon, R.D.G., Anderson, J.M. (1979) The effect of Collembola grazing on microbial activity in decomposition of leaf litter. Oecologia (Berlin) 38, 93–99. Hendrix, P.F., Parmelee, R.W., Crossley, D.A.,Jr., Coleman, D.C., Odum, E.P., Groffman, P.M. (1986) Detritus food webs in conventional and no-tillage agroecosystems. BioScience 36, 374–380. Hunt, H.W., Coleman, D.C., Ingham, E.R., Ingham, R.E., Elliott, E.T., Moore, J.C., Rose, S.L., Reid, C.P.P., Morley, C.R. (1987) The detrital food web in a shortgrass prairie. Biology and Fertility of Soils 3, 57–68. Ineson, P., Leonard, M.A., Anderson, J.M. (1982) Effect of collembolan grazing upon nitrogen and cation leaching from decomposing leaf litter. Soil Biology and Biochemistry 14, 601–605. Krogh, P.H. (1994) Microarthropods as bioindicators. A study of disturbed populations. PhD thesis. National Environmental Research Institute, Silkeborg, Denmark, 96 pp. Lagerlöf, J., Andrén, O. (1991) Abundance and activity of Collembola, Protura and Diplura (Insecta, Apterygota) in four cropping systems. Pedobiologia 35, 337–350. Lussenhop, J. (1992) Mechanisms of microarthropod-microbial interactions in soil. Advances in Ecological Research 23, 1–33. Persson, T. (1983) Influence of soil animals on nitrogen mineralisation in a northern Scots pine forest. In: Lebrun, Ph., André, H.M., De-Medts, A., Grégoire-Wibo, C., Wauthy, G. (eds) New trends in soil biology. Dieu-Brichart, Ottignies-Louvain-La-Neuve, pp. 117–126. Petersen, H. (1975) Estimation of dry weight, fresh weight and calorific content of various Collembola species. Pedobiologia 15, 222–243. Petersen, H. (1981) The respiratory metabolism of Collembola species from a Danish beech wood. Oikos 37, 273–286. Petersen, H., Gjelstrup, P. (1985) Development of a semi-field method for evaluation of laboratory tests as compared to field conditions. In: Løkke, H. (ed) Effects of pesticides on meso- and microfauna in soil. Bekæmpelsesmiddelforskning fra Miljøstyrelsen 8. Danish Environmental Protection Agency, Copenhagen, pp. 67–142. Ruiter, P.C. de, Moore, J.C., Zwart, K.B., Bouwman, L.A., Hassink, J., Bloem, J., Vos, J.A. de, Marinissen, J.C.Y., Didden, W.A.M., Lebbink, G., Brussard, L. (1993) Simulation of nitrogen mineralization in the below-ground food webs of two winter wheat fields. Journal of Applied Ecology 30, 95–106. Seastedt, T.R. (1984) The role of microarthropods in decomposition and mineralization processes. Annual Revue of Entomology 29, 25–46. Setälä, H., Huhta, V. (1990) Evaluation on the soil fauna impact on decomposition in a simulated forest soil. Biology and Fertility of Soils 10, 163–169. Setälä, H., Huhta, V. (1991) Soil fauna increase Betula pendula growth: Laboratory experiments with Coniferous Forest floor. Ecology 72, 665–671. Visser, S. (1985) Role of the soil invertebrates in determining the composition of soil microbial communities. In: Fitter, A.D. (ed) Ecological interactions in soil. Blackwell Scientific Publications, Oxford, pp. 297–317.
PROCEEDINGS OF VTH INTERNATIONAL SEMINAR ON APTERYGOTA, CORDOBA 1998
Collembola populations in an organic crop rotation: Population dynamics and metabolism after conversion from clover-grass ley to spring barley Henning Petersen Natural History Museum, Mols Laboratory, Femmøller, DK 8400 Ebeltoft, Denmark Accepted: 10. December 1999
Summary Population dynamics of earthworms, enchytraeids, mites and collembolans were assessed over two years as part of a collaborative research project in an organic crop rotation at the agricultural Research Centre Foulum, Jutland, Denmark. The Collembola study presented here is restricted to the first growth season of a two-year study, i.e from just before conversion of a two year old clover-grass ley to seedbed until harvest of the barley crop. The results refer mostly to the four most abundant species. The project included experimental reductions of earthworm populations to test the effects on interactions between earthworms and mesofauna. Expulsion by electro-shocking resulted in modest reductions in earthworm density and biomass. No significant effect of the reduction was observed on the collembolan populations. Total collembolan density and density, mean weight per specimen, biomass and population metabolism of the four most abundant species decreased markedly between the first and second sampling date as an effect of the mechanical disturbance, and inversion of soil layers caused by soil preparation. The depth distribution for all Collembola species was inverted from highest concentration in the 0–10 cm layer to highest concentration in the 10–20 cm soil layer. After a population minimum in May, the density, mean weight, biomass and metabolism increased more or less regularly according to species. The net loss of biomass after conversion implied a mobilization of 5 mg N.m-2 from dead collembolan tissues. Together with an estimate for nitrogen due to excretion, the contribution of Collembola to nitrogen mobilization through the growth season was estimated tentatively as 10 mg.m-2. This amount was negligible compared with the cone-mail: [email protected]
0031–4056/00/44/03–04–502 $ 12.00/0
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tribution of earthworms. The possibility that indirect catalytic effects of collembolan activity could have any significant effect on nutrient availability for plants was not resolved but the collembolan population metabolism showed no obvious synchrony with the nutrient requirements of the crop. Key words: Collembola, organic farming, earthworm interaction, biomass, population metabolism, nitrogen flux
Introduction Organic farming has gained increasing popularity during the last decades with the background of a growing public concern about contamination of food and environment by pesticides and other chemicals used in conventional agriculture. This is happening in Europe and globally. In Denmark, where agriculture is a main national product the interest in organic farming has increased markedly from the early nineties where less than 1 % of agricultural land was grown organically until the end of the decade when – in 1998 – 3.7 % of the agricultural land was converted to organic farming (Anonymous 1999). This increase depends on the willingness of the population to pay a higher price for the products. This was most convincingly proved for milk products where 20 % of the liquid milk sold in Denmark in 1998 was produced by organic farms (Anonymous 1999). This is the background for a large research effort initiated jointly by the Danish Ministry of Environment and the Ministry for Foodstuffs, Agriculture and Fishery, with the purpose of understanding basic ecological processes in organic farming systems and improving the agricultural methods and practices needed to optimize economic returns and environmental benefits. The fundamental idea of organic farming is to involve natural ecological processes, so practices used should aim at supporting and utilizing ecological processes as far as possible. The research programmes in organic farming are organized as an inter-institutional centre “Danish Research Centre for Organic Farming (DARCOF)”. A subproject within this organization is a field experiment seeking information on (1) the timing of population development and metabolism of soil meso- and macrofauna in relation to nitrogen dynamics and the growth of crop plants and (2) the interaction between earthworms and the mesofauna. The first hypothesis advanced is that the soil fauna, by feeding on microfungi and bacteria, may help to mobilize nitrogen and other nutrients and thus make them available for uptake by plant roots. Experimental evidence for such an indirect catalytic effect has been provided by Anderson et al. (1985), Hanlon & Anderson (1979), Ineson et. al. (1982) and Setälä & Huhta (1990, 1991). Furthermore, nutrients may be stored in the biomass of soil animals and released by excretion or following the death of the animals (Ausmus et al. 1976; Christensen 1987). The timing of these processes in relation to the demands of the crop plants is important for the most efficient utilization of manure and the prevention of leaching to the deeper soil layers and the ground water. The second hypothesis is because earthworms are, in terms of biomass and activity, by far the most important group of soil animals in the agricultural system studied here. In a long-term study carried out in the same experimental farm as the pre-
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sent experiment Christensen & Mather (1997) found a mean of 31 earthworms per m2 in the conventionally-farmed corn field, just before conversion to organic farming practice in 1986. During the following 11 years of organic farming the earthworm densities increased rapidly and reached a maximum of more than 600 per m2 in the clover-grass field of the organic crop rotation in 1977, i.e. a 20 times increase during a decade. It was envisaged that such a large earthworm population might influence other organisms in the soil. Therefore, in order to quantify effects on the soil biota, nitrogen turnover and plant growth it was attempted to include an experimental reduction of earthworms as a treatment in the experiment. Preliminary results are presented on the development of the collembolan population from the first part of the study period, i.e. from immediately before the plowing of the two year old grass-clower sward to the harvest of the barley sown after the soil preparation. Population density estimates are presented for all species and biomass and metabolic rates are presented for the four most abundant collembolan species.
Materials and Methods The experiment was in a field with an organic crop rotation (Field S02) at the Agricultural Research Centre Foulum near Viborg, Jutland, April 1997 – March 1999 . The present results are based on the first five samplings in 1997. The first of these was April 1 1997 in the clover-grass field just before conversion to seedbed. The soil preparation included rotary-tilling of the clover-grass sward followed by plowing, packing and harrowing. The field was sown with barley, peas and rye grass but peas were avoided within the experimental plots. The following four samples were in the succeeding barley-rye grass field (May 20, June 9, July 7 and August 14). The last sampling coincided with harvest. The experiment was arranged as a randomized block design with 5 blocks, each with 2 plots (4 × 3 m). Part of the earthworm population was expelled by electro-shocking (Bohlen et al. 1995) from one randomly chosen plot in each pair just after sowing in April 1997. The other plot was an unmanipulated control. Each plot was surrounded by a plastic barrier to prevent migration of earthworms. Two sampling quadrats (0.25 m2) were selected randomly within each plot for each sampling date. Cylindrical soil cores (surface area: 79 cm2, depth: 0–10 cm and 10–20 cm) were sampled for microarthropod extraction on the same dates and within the same sampling quadrats as soil samples used for extraction of earthworms and Enchytraeidae and samples for measurement of nitrogen pools. Microarthropods were extracted in modified high gradient funnel extractors (Gjelstrup & Petersen 1987). The surface temperature was increased gradually from 30°C to 60°C during an extraction period of 10 days. Mean dry weights per individual were based on body length measurements of randomlyselected specimens representing each species at each sampling date. Only the results for the four most abundant species/species groups, i.e. Mesaphorura spp. (mostly M. macrochaeta Rusek 1976), Folsomia fimetaria (Linné 1758), Isotoma notabilis Schäffer 1896, and Isotoma anglicana Lubbock 1862 (distinguished from I. viridis Bourlet 1839 according to Fjellberg 1980). The number of replicated measurements depended on the availability of suitably extended specimens and varied between samples. The number of specimens measured in each sample were 25–39 for Mesaphorura spp., 22–33 for F. fimetaria, 24–38 for I. notabilis and 10–25 for I. anglicana. The mean dry weights were calculated using regression equations reported in Petersen (1975). The equations for F. quadrioculata were used for F. fimetaria and the equation for juvenile I. notabilis was used for all sizes of I. anglicana. Biomass was obtained by multiplication of density by mean individual dry weight.
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The mean respiratory rate per individual as oxygen consumption was calculated from the individual dry weights and the mean soil temperature in 10 cm depth during the period from 10 days before to 10 days after each sampling date according to regression equations in Petersen (1981). The respiration of Mesaphorura spp., F. fimetaria and I. anglicana was calculated using the regression equations reported for Tullbergia krausbaueri, Folsomia quadrioculata s.l. and I. notabilis, respectively. Population respiration representing the sampling dates was calculated by multiplication of mean individual respiratory rate by density of individuals. Carbon and nitrogen contents of the collembolan biomass were calculated using the percentages in relation to dry weight, i.e. 52.4 % and 11.8 %, respectively, reported by Persson (1983). Reference is made to unpublished results of carbon- and nitrogen flux based on efficiencies and carbon/nitrogen- ratios used in Persson (1983), Hunt et al. (1987) and Ruiter et al. (1993).
Results Although about a third of the earthworm biomass was removed from the treatment plots by a fairly intensive electro-extraction, the reduction in earthworm populations observed in these plots, compared with the non-treated control plots, was only statistically significant in the first (biomass) and third sample (biomass and density) following electro-extraction (O.M. Christensen & J.G. Mather in prep.). The numbers of total Collembola in the earthworm manipulated and control plots did not differ significantly on any sampling date (Fig. 1) and the preliminary conclusion is that the relatively small population reduction of earthworms did not result in any observable effects on collembolan population density. Consequently, the data gained from the earthworm-manipulated plots and the control plots were pooled in the following data analysis.
Fig. 1. Comparison between collembolan mean densities in plots where earthworm populations were reduced with electro-extraction and unmanipulated control plots. Number of replicates: 5. Error bars: standard error of mean density
The populations of Collembola decreased markedly in both manipulated and control plots between the first sampling in April and the second sampling in May (Fig.1). The decrease amounted to 70 % of the density measured on the first sampling date. In the beginning of that period, soil preparation and sowing were done and the strong decrease in collembolan numbers was probably caused by these physical disturbances and the subsequent exposure of the bare soil surface. The decrease was very marked in the uppermost 10 cm of the soil and an increase occurred in the 10–20 cm horizon
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Fig. 2. Mean density of total Collembola in 2 depths (full drawn line: 0–10 cm, dotted line: 10–20 cm). Number of replicates: 10. Error bars: standard error of mean density
Fig. 3. Mean density of 4 collembolan taxa in 2 depths (full drawn line: 0–10 cm, dotted line: 10–20 cm). Number of replicates: 10. Error bars: standard error of mean density
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(Fig. 2). This resulted in an inversion of the depth distribution which remained for the rest of the investigation period. The strong decrease in the surface soil Collembola population between the first and second sampling was repeated for the four most abundant collembolan taxa in the present habitat (Fig. 3): Mesaphorura spp., F. fimetaria, I. notabilis and I. anglicana. These species together made up 71–87 % of the total Collembola populations. In Mesaphorura spp. and F. fimetaria, the largest population density occurred in the deeper soil layer for the rest of the study period while I. anglicana and later I. notabilis changed to be predominant in the surface layers during the summer. There were marked differences in time patterns between species for the mean individual dry weights (Fig. 4) but for all taxa a population decrease occurred between the sampling dates before and after soil preparation in the spring indicating a change from populations dominated by large adults, to populations dominated by small juveniles. During the remainder of the spring and summer the mean individual dry weights increased and then decreased. These changes in population structure can be ascribed to varying combinations of mortality and multiplication. The population biomass of the four species increased for a shorter or longer time after the initial decrease following soil preparation (Fig. 5). For Mesaphorura spp. a second decrease occurred in the July sample and in I. notabilis a decrease was observed in the August sample. Together the biomass of the four common species decreased by 42 mg (dry weight).m-2 or 90 % of the initial biomass during the period when the clover-grass sward was ploughed and the soil prepared for the barley crop (Table 1). The sum of the biomass decreased during the following periods by 5 mg (dry weight).m-2. The net losses of carbon and nitrogen from the four species were calculated as 22 and 5 mg.m-2, respectively, during the first period (Table 1) and 25 and 6 mg.m-2, respectively, during the whole period. The changes in respiration rates of the four collembolan populations through the period (Fig. 6) were the results of changes in population density, mean size distribution and mean soil temperatures from 10 days before the sampling dates to 10 days after. Except for Mesaphorura spp. the population respiration reached a minimum in May and June. The sum of the respiration rates of these four most abundant species increased steadily from the May – to the August sample where the respiration rate was higher (1.2 µl.m-2.day-1) than at the initial sampling date (0.9 µl.m-2.day-1). Table 1. Initial biomass and net losses ± standard error of mean (mg.m-2) for the four most abundant collembolan taxa during spring 1997 when the grass-clover sward was converted to a spring barley field. – Dwt: biomass or net loss as dry weigt, C: carbon content, N: nitrogen content. Means and standard errors based on 10 replicates per sample Species
Mesaphorura spp. F. fimetaria I. notabilis I. anglicana Sum 4 taxa
Biomass April 1 ——————— Dwt 3.78 ±00.62 18.44 ±08.73 5.01 ±01.13 20.49 ±08.54 47.71 ±13.08
Net Loss April 1 – May 20 ———————————————————— Dwt C N 3.21 ±00.68 1.68 ± 0.35 0.38 ± 0.08 15.49 ±08.72 8.12 ± 4.57 1.83 ± 1.03 3.69 ±01.14 1.93 ± 0.60 0.44 ± 0.14 20.06 ±08.54 10.51 ± 4.48 2.37 ± 1.01 42.45 ±13.33 22.24 ± 6.99 5.01 ± 1.57
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Fig. 4. Mean dry weight per specimen in µg of 4 collembolan taxa in 0–20 cm depth. Number of replicates: 10. Error bars: standard error of mean dry weight
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Fig. 5. Mean population biomass (dry weight) in mg.m-2 for 4 collembolan taxa in 0–20 cm depth. Number of replicates: 10. Error bars: standard error of mean biomass
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Fig. 6. Mean population metabolic rate: Oxygen consumption in ml.m-2.day-1 for 4 collembolan taxa in 0–20 cm depth. Number of replicates: 10. Error bars: standard error of mean
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Discussion Conventional farming practices rely to a large extent on methods which aim at controlling or altering the natural state of the soil environment. Conversely, organic farming is based on the best possible utilization of naturally-occurring ecological processes in soil. One of the most important of these processes, relevant to organic farming, is the decomposition of dead plant material and organic manure to provide nutrients to crop plants. The microflora, fungi and bacteria, are mainly responsible for this process but the soil fauna may contribute significantly to the nutrient flux both directly (e.g. Hunt et al. 1987; Christensen 1987), and indirectly, as catalyzers (e.g. Anderson et al. 1985; Hanlon & Anderson 1979; Ineson et. al. 1982; Lussenhop 1992; Seastedt 1984 and Setälä & Huhta 1990, 1991). With that background it seems interesting to attempt a quantification of the role of the soil fauna related to nutrient mobilization in organic fields and to which degree the timing of the effects of the soil fauna is synchronized with the needs of the crop plants for available nutrients. The whole complex of soil invertebrates is involved in these processes and each taxon may have a specific role although present knowledge is restricted to a crude classification into trophic levels and ecotypes related to size of specimens (micro- , meso-, macrofauna) and preferred microhabitats (e.g. soil depth). One objective of the present study was to investigate interactions between the important faunal groups and the consequences of such interactions on the performance of the soil community in relation to nitrogen transfer. The experimental reduction of earthworms included in the present field experiment failed to show any effects on the density of Collembola during the first five months. However, laboratory microcosm experiments included in the same research project as the present study (J. Filser & P.H. Krogh in prep.) have demonstrated effects of interactions between mesofauna taxa on nitrogen uptake in barley plants. The effects of the fauna on soil processes depend on the size of populations. It may be expected that the density and biomass of the fauna in organic field soils are larger than in the soil of conventionally-managed agricultural fields because of the use of organic fertilizers, the avoidance of pesticides and the use of crop rotations including grass- and clover leys or fallow. This seems to be confirmed for the earthworms although great variations have been found between organic farms in Denmark due to e.g. soil type and time since conversion from conventional to organic farming (Christensen & Mather 1997). Krogh (1994) monitored the microarthropod populations in one conventional, two integrated and one organic field system at the Research Centre Foulum, Jutland, through 6 years. He found that Collembola were most abundant in the organic and integrated grain system but significantly less abundant in the integrated forage system and the conventional system. The population size, however, was strongly dependent on the composition of different crops in the rotations and it was suggested that the use of chemical fertilizers and pesticides was less important than the crops in the rotation and type of cultivation practices such as mulching, plowing and harrowing. Thus, the microarthropods were almost three times as abundant in the organic clover grass ley as in the annual crops and fallow fields of the same farming system. On the other hand, Petersen & Gjelstrup (1995) found long-lasting inhibition of collembolan population growth in field mesocosms sprayed with recommended dosages of the insecticide dimethoate. The present study did not aim at a comparison between organic and conventional
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agricultural systems and the data on collembolan population size obtained so far does not provide evidence that organic farming practice “per se” favours collembolan populations in comparison with conventional farming systems with similar crop rotation, cultivation practice and use of organic fertilizers. The greatest abundance of Collembola was in the clover-grass field before soil preparation (12.300.m-2) and at harvest in August (17.900.m-2) and the lowest in May (3.600.m-2). The population density in August was similar to the mean density from several fields during six years in the organic farming system (16.900.m-2) reported by Krogh (1994). Collembolan numbers reported from conventional cereal fields, supplied with chemical fertilizers, are generally lower. Thus, the conventional system studied by Krogh (1994) had a 6-year mean of 6.800.m-2, Lagerlöf & Andrén (1991) reported 11.300.m-2 as a 5-year mean for September samplings in a Swedish barley field supplied with 120 kg N.ha-1.year-1 and Hendrix et al. (1986) reported 6.200.m-2 for a conventionally tilled sorghum/rye cropping system i Georgia, U.S.A. However, conventional grass- and lucerne ley fields, in a study by Lagerlöf & Andrén (1991), developed collembolan faunas with population densities comparable to or higher than the August sample of the present study (16.500 and 30.400.m-2, respectively) and no-tillage systems of the Georgia study (Hendrix et al. 1986) contained a mean of 14.700.m-2. After a steep decrease, following the conversion of the clover-grass field, the biomass of the four most abundant Collembola species increased steadily through the spring and summer but, contrary to the density, the biomass was still much lower in August (15.1 mg (dry weight).m-2) than in early spring because of the dominance of small juvenile specimens. The biomass in August was only a little higher than the mean of September samples, from the conventional, fertilized barley field studied by Lagerlöf & Andrén (1991), and similar to the conventional tillage treatment reported by Hendrix et al. (1986), while the initial biomass in April was similar to the biomass reported for the Swedish lucerne field (Lagerlöf & Andrén 1991) and the no-tillage treatment of the Georgian study (Hendrix et al. 1986). A Dutch study (Ruiter et al. 1993) reported the carbon contents of Collembolan populations which shows that Collembolan biomass in both conventional and integrated farming systems (in both systems more than 100 mg dwt.m-2) was more than twice as high as the highest biomass found in the present study. The soil fauna may cause mobilization of nutrients such as nitrogen in both direct and indirect ways. Thus, their most important direct contributions are excretion of nutrients as part of the metabolic flux, and death in other ways than by predation, where easily decomposable and nutrient rich animal tissue becomes available for rapid mineralization (Christensen 1987). Several indirect effects include: stimulation of microbial turnover and mobilization of nutrients by comminution of dead organic material and grazing on microbial colonies (e.g. Hanlon & Anderson 1979; Ineson et al. 1982; Lussenhop 1992), alterations of the composition of microflora, e.g. by selective grazing or transport of spores (Setälä & Huhta 1991; Lussenhop 1992; Visser 1985) and changes of the physical and chemical structure of the soil matrix. In the present study, a minimum estimate of the contribution to nitrogen mobilization through mortality of the four most common collembolan species was calculated as 5 mg.m-2 from the net decrease of biomass during the period between April 1 and May 20 (Table 1). For the whole period reported here, i.e. April 1 to August 14, the sum of net nitrogen mobilization through mortality amounted to 6 mg.m-2. The strong disturbance including inversion of the upper 20 cm of the soil caused by soil prepara-
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tion which probably explains most of the net decrease of total collembolan density and density and biomass of the four most abundant species during the period between the two first samplings, but also the long exposure of the more or less bare soil surface during the first part of that period may have contributed to the decline of the collembolan population. The observed biomass decrease was a net loss and does not include the loss of biomass produced during the period. Calculations of nitrogen fluxes through excretion (Petersen et al. in prep.) based on population respiration data and parameters of efficiencies and C/N-ratios borrowed from the literature (Persson 1983; Hunt et al. 1987) resulted in flux rates for the four common species during the five spring and summer months considered here which amounted to 2.4–2.8 mg N.m-2. Together with the amount of nitrogen mobilized through death af animals, including N in dead biomass produced between sampling dates, the nitrogen mobilization as a direct contribution by Collembola populations during spring and summer may be tentatively estimated as about 10 mg N.m-2. This is more than the 2.6 mg N.m-2.yr-1 (death: 1.1 mg.m-2.yr-1, inorganic N: 1.5 mg.m-2.yr-1) reported for Collembola by Hunt et al. (1987) and about half of 0.21 kg N.ha-1.yr-1 reported by Ruiter et al. (1993). Ruiter et al. described the contributions by Collembola and other microarthropods as negligible, in their conventional and integrated farming systems, in comparison with the contribution by especially amoebae and bacterivorous nematodes. In the farming systems studied by Ruiter et al. (1993) earthworms were rare or missing. In the present study earthworms were extremely abundant in the clover-grass field before conversion to seedbed and the earthworm densities and biomass were strongly reduced after the soil preparation. Although the calculation of earthworm contributions to the nitrogen flux are not yet available the direct contribution of Collembola to nitrogen mineralization is certainly extremely small in comparison. Results from a conventionally-cultivated Danish farm fertilized, by inorganic as well as organic fertilizers (Christensen 1987), which had an earthworm population size approaching that of the site studied here showed that the annual N-output as excreted ammonia was 450 mg.m-2.yr-1 and the input from dead earthworm tissue was 3,600 mg.m-2.yr-1. Although the direct contribution of Collembola to nitrogen fluxes in the organic farming system were small it is still possible that the indirect effect through interactions with the microflora is ecologically significant, especially when considering the close attachment of the collembolan fauna to the rhizosphere (Lussenhop 1992). Seastedt (1984) reported increases in decomposition rates of tree leaf litter from a number of studies from 4 to 69 % attributable to the effect of microarthropods. Beare et al. (1992) found that exclusion of fungal-feeding microarthropods from surface litter, in fields with no-tillage treatment, had little effect (less than 5 % reduction) on litter decomposition but that the microarthropods were more important in mobilizing nitrogen by grazing on the litter inhabiting fungi. Both direct effects and possible indirect catalytic effects on nitrogen mobilization, through interaction with microflora are correlated with the metabolic activity of the population as for instance expressed by the repiratory rate. The population respiration of the four most common species presented here dropped steeply together with the density and biomass between first and second sampling in spring as the effect of soil preparation. Thereafter, it increased and was higher in August than at the initial sampling before conversion of the clover-grass to seed bed.
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The requirement of the crop plants for available nutrients was correlated with growth and was therefore highest during spring and early summer. During the periods considered in the present paper, a close timing between collembolan activity and the need of the crop plants for available nutrients which might support hypotheses concerning an important role of these abundant soil animals was not apparent. Instead, a considerable drop in population biomass, and consequently a strong decrease in population metabolism, was observed during the time when the plants germinated and started growth. The drop in population biomass was the consequence of large mortality due to the mechanical disturbance and inversion of the soil, which made most of the collembolan tissue available for mineralization by the microflora. However, the amount of nutrients made available for plants from dead collembolan corpses appears negligible as compared to the simultaneous input of dead earthworm tissue.
Acknowledgements The study is part of project I.7. “Interaction between soil fauna, nitrogen dynamics, and plant growth – Experimental research and simulation modelling” under the Danish Centre for Organic Farming (DARCOF) and was financed by the The Strategic Environmental Research Programme (SMP) and the Natural History Museum, Aarhus. The other participants in the project are acknowledged for perfect cooperation and profitable discussions during the course of the project. Research Centre Foulum with the experimental farm Foulumgaard, is thanked for carrying out the practical field work and providing temperature data. Ole M. Christensen and Janice G. Mather, University of Aarhus, are thanked for allowing unpublished data on earthworms from the site to be quoted in the present paper. Laboratory technician Anni Kjeldsen and Anne Birgitte Raghner, Mols Laboratory, are thanked for indispensable technical assistance in the field and in the laboratory.
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