Plant N capture and microfaunal dynamics from decomposing
grass and earthworm residues in soil
A. Hodge
a,*, J. Stewart
b, D. Robinson
b,c, B.S. Griths
b, A.H. Fitter
aa
Department of Biology, University of York, P.O. Box 373, York YO10 5YW, UK
b
Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, UK
c
Department of Plant and Soil Science, University of Aberdeen, Aberdeen AB24 3UU, UK
Accepted 25 April 2000
Abstract
Plant roots may be eective competitors with micro-organisms for the nutrients released from decomposing organic patches buried in soil. We aimed to establish whether this was because they were more eective at acquiring nutrients or simply because they represent a slower turnover pool. Over 30 days we followed decomposition of, and plant N capture from, dual labelled (15N/13C) earthworms (Lumbricus terrestrisL.) and grass (Lolium perenneL. shoots) added as discrete patches to soil microcosm units containingL. perenne plants. Both patches decomposed rapidly as shown by the amounts of13C, as13CO2, released into
the soil atmosphere, which peaked after 8 h for the earthworm patches and 48 h for the grass patches. In the decomposing grass patches the amounts of13C and15N remained co-varied and declined with time. No 13C added in the earthworm patches was detected in the soils, even after 3 days, con®rming that decomposition of these patches was rapid. Grass patches supported greater microfaunal (nematode and protozoan) biomass than the earthworm patches, and microfaunal biomass peaked at day 7 on both. Plant N capture from both patches increased with dry weight increment although N capture from the earthworm patch was greater than that from the grass patch. By day 30 plants had captured 29% (from earthworms) and 22% (from grass) of the N originally available in the patches. No 13C enrichments from the patches were detected in the plant tissues indicating that organic compounds were not being taken up by the plant roots. As plants only took up inorganic N from the patch, our results indicate that microbes initially out-compete plants for the added N, but with time, plants capture more of the N originally added as they represent a slower turnover pool.72000 Elsevier Science Ltd. All rights reserved.
Keywords:Decomposition; Organic patches; Earthworms (Lumbricus terrestrisL.);Lolium perenneL; Protozoa; Nematodes
1. Introduction
Decomposition of organic material in soil is a major source of plant nutrients, especially in low input eco-systems, such as pastures. A clearer understanding of the factors governing nitrogen recycling in particular is important as this nutrient is most likely to be the limit-ing factor in plant growth, in such ecosystems (Vitou-sek and Howarth, 1991). The distribution of organic
inputs, and hence nutrient availability, however, is both spatially and temporally heterogeneous at scales relevant to plant roots (Gupta and Rorison, 1975; Jackson and Caldwell, 1993; Robertson et al., 1993; Stark, 1994; Farley and Fitter, 1999). Thus, plants may bene®t from recognising and exploiting such nutrient-rich zones or patches in competition both with micro-organisms and other root systems. Mech-anisms by which roots may exploit nutrient-rich patches in competition with other root systems include localised root proliferation within the patch (Hodge et al., 1999a; Robinson et al., 1999), or increased rates of nutrient uptake per unit of root (Jackson et al., 1990). Root proliferation within a nutrient-rich patch can be
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* Corresponding author. Tel.: 432878; fax: +44-1904-432860.
triggered by nitrate ions (Zhang and Forde, 1998; Zhang et al., 1999), although root systems of dierent plant species show varying degrees of proliferation re-sponse (Campbell et al., 1991; Hodge et al., 1998; Einsmann et al., 1999). The nutrient-rich patches themselves will also vary widely in a range of charac-teristics, such as frequency, distribution and concen-tration (see Fitter, 1994) which may also in¯uence the ability of roots to exploit them. We have shown that N capture from a range of patches diering in their chemical and physical complexity was related to the C-to-N ratio of the added patches (Hodge et al., 2000a). Furthermore, 15N but not 13C, enrichments were detected in the plant tissues originating from the dual labelled (15N/13C) patches. This implies that microbes were decomposing the patches prior to plant N capture (i.e., the plants were not taking up intact organic com-pounds) and that the speed of microbial decomposition could be important in determining the resulting N cap-ture by the plants.
Nutrient-rich organic patches are zones of high mi-crobial activity and population densities (Griths et al., 1994) even in the absence of plant roots (Christen-sen et al., 1992; Griths et al., 1995). Thus, microbes may initially sequester available nutrients before roots can gain access to them. However, ultimately some of the sequestered nutrients will become available through microbial turnover and be released back into the rhizo-sphere. Roots of wheat seedlings grown in the pots containing a complex organic patch (Lolium perenne
shoot material) acquired most of their N 10±22 days after patch addition, at a time when the populations of both ¯agellates and nematodes (and hence, presumably those of other microbes) were declining (Griths et
al., 1994; van Vuuren et al., 1996). After addition of a simple organic patch (L-lysine) L. perenne seedlings captured 57±61% of the N originally available after 35 days (Hodge et al., 1999b) suggesting that, in the longer term, roots are eective competitors for released N. In this experiment, we examined the timing of patch decomposition and subsequent changes in micro-faunal biomass and plant N capture from the patch. We compared the decomposition dynamics of two patch types: grass shoots and dead earthworms, which resemble patches likely to be encountered in the natu-ral environment and which contrast in their chemical characteristics, particularly in their C-to-N ratio. Patches were added to supply the same amount of total N and were dual-labelled with 15N and 13C, so that the dynamics of plant N capture and patch de-composition could be followed.
We tested the following hypotheses:
1. Decomposition of the earthworm patch would be more rapid than that of the grass patch because of its lower C-to-N ratio. Hodge et al. (2000a) have shown that mineralisation and plant N uptake increased as C-to-N ratio decreased.
2. Microfaunal biomass, an indicator of microbial ac-tivity and biomass (AndreÂn et al., 1988; Christensen et al., 1996) would peak in the soil receiving the earthworm patch before that in the grass patch as decomposition, and hence release of N, would be more rapid in the former patch type. In the grass patch the increase in protozoan biomass would not be as steep, but sustained for longer, because of the slower rate of decomposition.
3. Plants would capture most of their N from the
Fig. 1. Amount of13C, as13CO
patches following the peak in microfaunal biomass, and N capture from the earthworm patch would be greater than from the grass patch which would release N more slowly.
2. Materials and methods
2.1. Experimental design
All experimental plants were grown in the micro-cosm units. The micromicro-cosm units consisted of a section of PVC pipe (length 20 cm, I.D. 10 cm) with a small hole cut near the top to allow insertion of a gas sampling tube (15 cm long0.3 cm I.D.) at an angle of 458 to the horizontal. Each microcosm unit was ®lled with a mixture of sand:soil as described in Hodge et al. (1999c) to a depth of 10 cm before a wooden pole (15.5 cm long2.7 cm E.D.) was placed in the centre of the microcosm tube. The purpose of this pole was to allow precise placement of the patches once the seedlings had developed suitably while ensuring mini-mal disturbance to the system. At the top of each microcosm unit the top 2 cm section (7.5 cm wide at base) of a PVC funnel was placed to direct the roots into the middle section of the tube where the organic patch was to be placed. The remaining space in the microcosm unit was ®lled with the sand:soil mixture ready for planting. The microcosm units were then placed within four large 604030 cm) freely drain-ing insulated boxes (six microcosm units per box) con-taining a mixed turf of Trifolium repens L. (white clover) and Lolium perenneL. cv. Fennema (perennial ryegrass; all seeds were supplied by Johnson Seeds, Lincolnshire, UK) plants to buer the microcosm tubes against ¯uctuations in external temperature and to produce a realistic microclimate around the micro-cosm units. Twelve L. perenne seeds were planted in each microcosm unit, with seeds germinating within 5 days and seedlings being left for a further 27 days before patches were added. The boxes were maintained in a heated glasshouse throughout.
The experiment was repeated: 12 replicate units of each patch type (grass and earthworms) were estab-lished on 11 November 1998 and a second run of 12 replicate units of each patch type set up on 6 Decem-ber 1998. The mean temperature, mean daily maxi-mum and mean daily minimaxi-mum did not vary between the two experimental runs and was 198C (SE20.1), 208C (SE20.3), and 158C (SE20.3), respectively. The plants were grown under 16 h days with natural light supplemented by 400 W halogen bulbs. Photosyntheti-cally active radiation (PAR) ¯ux was recorded weekly at noon and ranged between 50 and 320mmol mÿ2sÿ1
at plant level during the ®rst experimental run and 50± 197 mmol mÿ2 sÿ1at plant level during the second ex-perimental run.
Fig. 2. The relationship between (a) mg 15N in the decomposing grass (*) and earthworm (q) patches and (b) mg13C in the decom-posing grass (*) patch with time d. (c) The relationship between mg 15N and mg 13C in the grass (*) patch. Regression equations are
given in Table 1. Points shown in (a) and (b) are the means n6
2.2. Organic patch material
Organic material added as patches was either 320 mg of grass (Lolium perenneL. cv. Miranda shoots) or 105 mg of earthworm (Lumbricus terrestris L.) ma-terial. Both types of organic material were dual labelled with15N and13C. The grass material was pro-duced as described in Hodge et al. (1998). The labelled earthworm material was produced by keeping earth-worms in containers with soil and feeding them on a diet of 15N/13C labelled L. perenne shoot material for 10 months. The soil was changed regularly during this time. Earthworms were then removed from containers, washed and starved overnight to void their guts before being killed by freezing. Both the earthworm and grass were added as a ®nely milled powder to the microcosm units. The material was placed in the space created by removal of the wooden pole at 10 cm depth. The remainder of the space was ®lled with sand:soil mix only. The earthworm material added to the tubes con-tained 10.1% N (2.55 at.% 15N) and 40.8% C (1.34 at.% 13C), with a C-to-N ratio of 4.1:1. The grass ma-terial added contained 3.3% N (13.3 at.% 15N) and 40.4% C (3.1 at.%13C), with a C-to-N ratio of 12.2:1. Thus, 10.6 mg N was added to each microcosm unit.
Three replicates were used for each of four destructive harvests in each of the two experimental runs.
2.3. Plant and soil analysis
To follow the decomposition of the added organic patches 13C respired (as 13CO2) from the organic patches was monitored by sampling gas from within the soil. Gas samples were taken by inserting a syringe needle (11.5 cm long) into the gas sampling tube and removing 10 ml of the soil air from the patch zone. The sample was then injected into an evacuated gas sample container (PDZ-Europa Ltd, Crewe, UK) for 13
C analysis (see below). Soil gas was sampled 1, 2, 3, 4, 8, 12, 24, 48, 72, 120, 168, 240, 336, 432, 528, 624 and 720 h after patches were added.
Plant uptake of N (as 15N) and C (as 13C) was determined by destructively harvesting three micro-cosm units containing the worm or grass patch 3, 7, 14 and 30 days after patch addition. The microcosm units were removed from their containers and once the gas sampling tube had been removed, each soil core was removed intact from its tube. The core was then cut into three sections: top, middle (containing the patch zone) and bottom, each of 6 cm thickness. Roots were extracted by hand from the dierent soil sections (top, middle and bottom) and washed thoroughly. Shoots were cut at the upper surface of the top section. Roots and shoots were oven-dried at 608C, weighed, milled and analysed for total N, C,15N and13C (see below).
For analysis, the roots from all sections of the microcosm unit were combined. A subsample of the milled root and shoot material was analysed for total N, C, 15N and 13C by continuous-¯ow isotope ratio mass spectrometry (CF-IRMS). The at.% 15N and13C excess was calculated by subtracting 0.366 and 1.088 (atmospheric background), respectively, from the measured values. The percentage of the patch N orig-inally added which was captured by the L. perenne
sward was calculated as: Table 1
Parameters of linear regressions of (A) mg15N in the organic patches against time (d), (B) mg13C in the grass patch against time and (C) mg 15
N against13C remaining in the grass patcha
Regression equationycmx Independent variable (x) P F1, 28 R
aThe probability (P),Fstatistic (F) andR2values are for the signi®cance and goodness-of-®t of the regression.
Table 2
Percentage of original patch15N and13C recovered in the soil har-vested with timea
Time (day) Grass patches Earthworm patches
(%)13C (%)15N (%)15N
There was no13C enrichments detected in soil receiving the earth-worm patches at any harvest date. Mean data n6with standard errors are shown.
b
"
mg15N in plant tissue mg15N in original patch material
!
100 #
Subsamples of the soil from each tube were used for moisture content determinations (1058C) but only the middle soil section (containing the patch) was used for total C, N, 13C and 15N analysis. The soil from the middle section was also used to determine the inor-ganic N content, while top and middle sections were used to determine nematode and protozoan biomass (as described in Hodge et al., 1998).
2.4. Statistical analysis
Data on the gas samples were analysed using the
General Linear Model (repeated measurements) com-mand in SPSS v 7.0 for the period 1±72 h when all tubes were still intact. Some gas samples taken after 240 h in the second experimental run were contami-nated after sample collection; those data were dis-carded. Data from destructive harvests were analysed using the General Linear Model (factorial design) com-mand in SPSS v 7.0. In all cases, a randomised block design was used. Dierences referred to in the text were statistically signi®cant with P<0:05 as deter-mined by a Bonferroni post-hoc test, unless otherwise stated. Data on protozoa numbers in the grass patches at 7 days in the second run were incorrectly recorded and have not been used.
Plant growth in the ®rst experimental run was Fig. 3. (a) NH4+±N and (b) NO3ÿ±N concentrations (mg gÿ1) recorded at harvest from soil which had received the grass (*) or earthworm (q) patches. NH4+±N concentrations declined with time (regression equations for log NH4+±N in the grass patches (ÿ) 0.077±0.048 days,P0:002, F1, 2211:94,R232:2%and earthworm patches 0.505±0.064 days,P0:002,F1, 2213:06,R234:4%). There was no signi®cant dierence
between patch types in the soil NH4+±N concentrations recorded. Dierent letters on graph (b) indicate signi®cant P<0:05dierences between
harvest dates in the concentration of NO3ÿ±N recorded in the soil. NO3ÿ±N concentrations were higher P0:020in the earthworm than grass
greater than in the second when the solar radiation receipt was less. To allow for dierences in plant size between experimental runs the total plant dry weights at time zero (i.e. time of patch addition) were calcu-lated as the intercept of a regression analysis of natural logarithm (ln) of tissue dry weight versus time. The back-transformed value of the intercept was then sub-tracted from the tissue dry weight at all harvests to obtain the increment in growth with time. Tissue dry weight increment values and percentage of N capture from the patches were analysed by linear regressions and signi®cant dierences between the slopes of the ®tted lines for the grass and earthworm patches com-pared using the F-ratio method (Sokal and Rohlf, 1981; Potvin et al., 1990)
3. Results
3.1. Patch decomposition
Similar amounts of13C (as13CO2) were recovered in the soil gas samples in the two experimental runs. The earthworm patch decomposed more rapidly than the grass patch, with 13CO2 recovery peaking 8 h after patch addition (Fig. 1). CO2 release from the grass patch peaked 48 h after addition to the microcosm tubes, but amounts recovered were never signi®cantly greater than from the earthworm patch. Thereafter, amounts of 13CO2 recovered declined steadily in both patches (Fig. 1).
At all harvests the soil which had received the earth-worm and grass patches contained more 15N than background. In contrast, 13C enrichments were detected only in the soil which had received the grass patches and only until 14 days (Fig. 2). The amounts of15N, and for the grass patches,13C, recovered in the soil declined progressively with time (Fig. 2a and b; Table 1). The linear relationship between mg 15N and 13
C remaining in the grass patches (Fig. 2c; Table 1) suggested that release of N and C from this patch ma-terial was coupled. Since the two patch mama-terials in-itially had contained dierent 15N and 13C enrichments, the percentage of original patch N and C recovered in the soil at harvest are presented in Table 2, which shows there was a more rapid initial loss of N from the earthworm patch.
3.2. Inorganic N and microfauna
Soil NH4+±N and NO3ÿ±N concentrations diered between the two experimental runs only on day 3 in the grass patch and day 14 in the worm patch, respect-ively, when they were higher in the second experiment than the ®rst. The data from the two runs were there-fore combined. Soil NH4
+
±N concentrations declined
signi®cantly with time (Fig. 3a). There was no dier-ence P0:112in soil NH4+±N concentrations due to the patch type present. Concentrations of NO3ÿ±N were higher than those of NH4
+
±N, and peaked at 7 and 14 day (Fig. 3b), i.e. after the peak in NH4+±N concentration, suggesting active nitri®cation processes in the soil. NO3ÿ±N concentrations were greater in the soil which had received the earthworm patches than that which had received the grass patches P0:020 but there was no signi®cant interaction between patch
day P0:086).
patch (Fig. 4). On day 7 (peak of nematode numbers) in both experimental runs the population on both patch types was mainly (>95%) bacterial-feeding nematodes. The mean biomass of the bacterial-feeders from both patch types in experimental run 1 (1.08 mg gÿ1) was smaller P<0:05 than in run 2 (4.71 mg gÿ1), but there were no signi®cant dierences between the grass and earthworm patches.
3.3. Plant N capture
Plants were larger in the ®rst experimental run than the second i.e. by day 30, mean plant weight was 960 mg in the ®rst run and only 470 mg in the second. However, there was no signi®cant dierence in relative growth rate (RGR) between the experimental runs or between the two patch treatments and the combined RGR was 50 mg gÿ1 dÿ1. Total plant N concen-trations started the same in plants grown in both patch types 48:720:83 mg N gÿ1) and declined with time. This decline was steeper in the ®rst experiment where the plants were larger. By day 30 in both exper-imental runs however, plant N concentrations were higher from the earthworm than the grass patches (i.e., mean across runs = 39:221:0 mg N gÿ1 for grass patches and 42:922:0 mg N gÿ1 for earthworm patches).
Plant N capture from the patch increased linearly with plant dry weight increment over both experimen-tal runs (Fig. 5). N capture from the earthworm patch
was greater than from the grass patch. Shoots tained up to 40% of patch N, but roots never con-tained more than 2.5% of original patch N. Plant tissues were never enriched with13C from the patch.
4. Discussion
Decomposition of the earthworm patches, with a lower C-to-N ratio, was more rapid than that of the grass patches as shown by the amounts of 13CO2 recovered and analysis of the patch soil, thus con®rm-ing our ®rst hypothesis. The C-to-N ratio of the sub-strate has a large in¯uence on decomposition (Berg and Staaf, 1981) and generally net immobilisation occurs when the C-to-N ratio is >20±30:1 (Bartholo-mew, 1965), higher than the C-to-N ratio of both types of patch used in this experiment. The patches used in our experiment decomposed and released N throughout. These results also con®rm our other work on patches: at low C-to-N ratios (i.e. <4) plants cap-tured >50% of the patch N originally available within 49 days (Hodge et al., 2000a), while at higher C-to-N ratios of 21:1 and 31:1 plant N capture was substan-tially reduced to only 11% after 49 days and >6% after 35 days, respectively (Hodge et al., 1998, 2000a).
After only 3 days, 50% of earthworm N initially added was lost from the soil-plant system. By day 7 the amount of N lost had risen to 64%, more than the 50% N mineralisation of earthworm tissue after 7 days Fig. 5. Relationship between plant dry weight (D.W.) increment and percentage N capture from the grass (*) and earthworm (q) patches. The lines shown are ®tted regression lines (solid for grass data; broken for worm data) for the original data of percentage N capture from the organic patches regressed against plant D.W. increment. Regression lines were signi®cantly P<0:05dierent as determined by theF-ratio method for
reported by Christensen (1988). In contrast, 71% of the original patch N was still detectable in the soil from the grass patches. Although plant biomass pro-duction was lower in the second experimental run, de-composition of the patches did not dier between runs.
The observation that protozoan populations did not increase on the earthworm patch, in contrast to the bacterial-feeding nematodes, was unexpected. It is possible that the earthworm patches, with their high N content, may have locally altered the pH of the soil adversely aecting the protozoan, but not the nema-tode, populations. In addition, protozoan growth is aected by the species of bacteria present (Weekers et al., 1993), which may have been very dierent between the two patch types. Earthworms also have antibiotic properties which may be due to feeding on actinomy-cetes found in their gut (Brown, 1995). However, as the earthworms used in this experiment had their guts voided prior to freezing and milling, antibiotic release was probably not a signi®cant factor in our study. The soil receiving the grass material as patches supported more microfaunal biomass than that receiving the earthworm material (equal nematode biomass but greater protozoan biomass). This is not unexpected, because both substrates had relatively low C-to-N ratios, and therefore, the greater amount of C added with the grass patch (to maintain constant N) could support a larger microfaunal biomass. Nematodes in both patches peaked at day 7, which does not support our second hypothesis that earthworm patches would produce an earlier peak in microfauna due to rapid de-composition. Plant N capture from both patches at day 7 was less than 2% of the N originally available but increased over the next two harvest dates (i.e., 8± 10% at day 14 and 22±29% at day 30) when microfau-nal biomass was declining, thus partially supporting our third hypothesis. Griths et al. (1994) also observed an increase in plant N capture from a similar grass patch as ¯agellates and nematode numbers in the patch declined.
Plant N capture from the patches re¯ected their dry weight increment, although N capture was higher from the earthworm patch, which decomposed more rapidly. This result gives further support to our third hypoth-esis that N capture would be greater from the patch of lower C-to-N ratio. In addition, by the end of the ex-periment, total plant N concentrations were also higher in plants grown in the presence of an earth-worm patch. After 30 days, the plants had captured 29% (earthworms) and 22% (grass) of the N originally available, a much lower ®gure than the c. 70% capture reported by Whalen et al. (1999) using similar patch material (15N labelled Lumbricus terrestris) and the same plant species (L. perenne). However, in the study by Whalen et al. (1999) the ambient temperature
ran-ged from 20 to 278C, whereas in ours, it ranran-ged from 15 to 208C. Temperature can have a large eect on N transformations (see Swift et al., 1979) which probably explains the discrepancy in plant N capture values. In contrast, the % N capture from the grass patches agrees well with our other study using the same ma-terial added to a L. perenne sward, but altering the physical complexity and spatial placement: in that case N capture from the patch was c. 26% over 70 days (Hodge et al., 2000b).
These observations emphasise the temporal aspects of competition between microbes and plants for nitro-gen. The bulk of microbial activity was over before roots were able to grow into and exploit the patch. Previous gnotobiotic studies with microfauna have shown that microbial-feeding nematodes and protozoa enhance the cycling of N, prevent the immobilisation of N in the microbial biomass and enhance plant N uptake (Ingham et al., 1985; Griths, 1994). The assumption has been that roots would need to be pre-sent while this transformation activity was proceeding to take advantage of the N. However, we now know from numerous studies (van Vuuren et al., 1996; Hodge et al., 1998, 2000a) that roots typically prolifer-ate in a patch after the early ¯ush of microbial activity has passed and when faunal populations are declining. Thus, rather than bene®ting from the gross mineralis-ation (i.e., intercepting actively transformed N) the plants bene®t from the net mineralisation (i.e., the increased pool of mineral N) together with the slower rates of mineralisation that occur in the secondary phases of decomposition. Even in situations where the patch might occur adjacent to an active root system (e.g., the injection of slurry into an established crop, death of an earthworm in the rooting zone) the longev-ity of roots compared to microbes would enable the plant to absorb N after the initial ¯ush of microbial activity. Thus, plants may be eective competitors for N because they are a slower turnover pool than the microbes.
5. Conclusions
pre-sent in gaseous form and lost as the soil was harvested and dried. Plant N capture from the patches used in this study was in agreement with our previous work (Hodge et al., 2000a): more capture occurred from the patches with the lower C-to-N ratio. Moreover, plant N was captured only after N had been mineralised by soil microbes. Although some studies suggest that plants can take up simple organic compounds intact (NaÈsholm et al., 1998; Lipson and Monson, 1998), we have never observed this phenomenon even though such simple compounds would inevitably have been released during patch decomposition and made avail-able for uptake. However, even in the absence of direct uptake of organic N compounds plants, with time, can capture considerable amounts of N present from N-rich patches.
Acknowledgements
This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC). The Scottish Crop Research Institute receives grant-in-aid from the Scottish Executive Rural Aairs Department. We thank Michael Bonkowski, Charles Scrimgeour and Winnie Stein for their technical assistance.
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