Effects of earthworms on cation and phosphate mobilisation in limed peat soils under Picea sitchensis

Pores;;;ology Management ELSEVIER

Forest Ecology and Management 86 (1996) 253-258

Effects of earthworms on cation and phosphate mobilisation in limed peat soils under Picea sitchensis C.H. Robinson a7*, P. Ineson a, T.G. Piearce b, J. Parrington a b Division

a Institute of Terrestrial Ecology. Merlewood of Biological Sciences, Institute of Environmental

Research Station. Grange-over-Sands. LA1 I 6JU, 1JK and Biological Sciences, Lancaster University, Luncaster,

LA1 4YQ. UK

Accepted 5 February 1996

Abstract caliginosa was successfully introduced into limed peat monoliths in field lysimeters under a stand of Picea had been fertilised with P and K at 7.5 and 100 kg ha- ’ 5 years previously. Total earthworm biomass was sustained over the 12 months of the experiment in the limed treatments, whereas only 3% remained in the treatment without lime. Earthworm cocoons were produced in the limed treatments only. Aporrectodea caliginosa in limed soil significantly increased leachate fluxes to lower soil horizons of K+ (to 3.5 kg ha-’ year-‘), Ca2+ (to 303 kg ha-’ year-‘) and Mg*+ (to 19 kg ha-’ year-‘), compared with untreated controls (19, 8 and 4 kg ha-’ year-‘, respectively). These increased leachate Ca2+ and Mg2+ values were also significantly greater than from limed-only soils (56 and 8 kg ha-’ year-‘, respectively), and treatments in which earthworms alone were added (10 and 6 kg ha-’ year- ‘, respectively). Potassium and Mg*’ mobilised by the addition of earthworms plus lime appeared to be taken up by living roots of P. sitchensis. There was no effect of any treatment on phosphate release. Aporrectodea sitchensis which

Keywords:

Earthworms; Lime; Picea sitchensis;

Potassium; Calcium; Magnesium; Phosphate

1. Introduction

Liming has become an important way of ameliorating acidification of forest soils from natural and anthropogenicsources(Hiittl and Frielinghaus, 1994). However, the addition of lime to forest plantations has often yielded negative growth effects, which sometimesextend over decades(Dickson, 19861,and may be due to nutrient immobilisation in soil organic

* Corresponding author at: Sheffield Centre for Arctic Ecology, Department of Animal and Plant Science, 26, Taptonville Road, University of Sheffield, SlO 5BR, UK. Tel.: +44 114 282 6102; fax: + 44 114 268 2521; e-mail: [email protected]. 0378- I 127/96/$15.00 PII SO378-

matter (Popovic et al., 1988). Following application, the lime often forms a discrete layer in the soil profile remote from tree rooting depth (Robinson et al., 1992b3),and therefore may not be as effective as it could be in soil and forest amelioration. In the UK, about 80- 100000 ha of deep peat are currently planted with Picea sifchensis(Bong.) Carr. (Taylor, 1991). To ameliorate phosphorus (P) and potassium (K) deficiency on deep peats, fertilisers are routinely applied at 60 kg P ha- ’ (Taylor, 1991) and 100 kg K ha-’ (Dutch et al., 1990) at planting. Cations other than K+ are important in the nutrition of P. sifchensis, and although calcium (Ca”) deficiency is rarely found in forest crops, magnesium

Copyright 0 1996 Elsevier Science B.V. All rights reserved.

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(Mg”> deficiency can be encountered in soils in the UK (Taylor, 19911, and forest decline involves soil Mg*+ and K+ deficiencies (Hlittl and Frielinghaus, 1994). The beneficial influence of earthworms on physical properties and cation and phosphate (PO:- > mobilisation in both fertilised and unfertilised temperate soils has been extensively documented (review by Lee, 1985). There is also considerable evidence that earthworms have positive effects on plant productivity (e.g. Stockdill, 1982; AtlavinytC and ZimkuvienC, 1985). However, previous studies mainly concern soils of arable land (e.g. Curry and Byrne, 1992; Edwards et al., 19921, grassland (e.g. Knight et al., 1992; Basker et al., 1993) and deciduous forest (e.g. Anderson et al., 1985; Scheu and Parkinson, 1994). The effects of earthworms on coniferous forest soils have largely been ignored (although see Haimi and Huhta, 1990; Haimi et al., 1992; Rundgren, 1994). perhaps because of the generally lower abundance of earthworms in such soils of typically low pH (e.g. Nordstram and Rundgren, 1974; Standen, 1979; Robinson et al., 1992b). Liming of low pH afforestation sites could enhance earthworm populations by increasing immigration and reproduction and lowering mortality (Persson, 1988; Rundgren. 1994). It may be possible to introduce earthworms into limed peat soils to establish populations quickly, including species that are normally scarce or absent in coniferous soils but which are able to thrive after liming (Robinson et al., 1992b). A greater earthworm biomass in these limed peat soils, which have been subjected to normal forestry management (i.e. fertilised with P and K), could give greater cation and phosphate mobilisation and result in lime being incorporated down the soil profile to rooting depth. Potential consequences include increased tree pro-

Table 1 Numbers and biomass as a proportion months (mean 5 SE, n = 4) Treatment Earthworms Earthworms Earthworms Means

+ lime + lime + roots

followed

by different

of that present initially,

86 11996) 253-258

duction, and the amelioration of forest decline in polluted sites. We aimed to determine (1) whether the lumbrieid earthworm Apurrectodeu caliginosa (Savigny) could survive and grow in limed peat in the field for a year, and (2) whether it could mobilise K - _ Cn’ ’ , Mg’+ and PO:--P from limed peat, fertilised with P and K, under a canopy of P. sitchensis. assessed using zero-tension lysimetry. Cation and phosphate uptake by roots of P. sitehensis were also investigated.

2. Materials and methods The study site was at Kershope forest. Cumbria (National Grid Reference NY566320; 55”7’N. 3”2O’W) at 380 m, with a mean annual precipitation of 1270 mm. It was planted with P. sitchensis in 1969, on non-flushed blanket peat over carboniferous limestone. Aerial application of P at 75 kg ha-’ and K at 100 kg ha-’ was made in 1983. Full details of lysimeter design and installation are given in Robinson et al. (1992a). Zero-tension lysimeters were constructed using 18 dmJ polyethylene water tanks containing peat monoliths, 32.5 cm X 23.5 cm X 12 cm, including surface layers of P. sirchensislitter. Live, intact roots of P. sitchensis were introduced through a hole in the lysimeter wall in each of the rooted treatments in August, 4 years after fertiiiser application, and sealedin place (see Anderson et al., 1990). Leachafes were collected at fortnightiy intervals from separate11 dm3 polypropylene bottles, starting from 27 October. After 18 fortnightly samplingoccasions, treatments were randomly allocated within each of four blocks (apart from those treatments containing roots, which were allocated according to

and cocoon biomass

of Aporrectodea

Numbers (%)

Total biomass (%)

Individual (c/o)

8.3 f 8.3a 84.7 5 4.4b 91.5 + 3.7b

3.0 & 3.0a 101.5 f 10.7b 98.8 f 3.5b

9.0 + 9.0a I 1 I. 1 f. 7.7b 109.0 + 8.Ob

letters are significantly

different

(P < 0.01)

biomass

cufiginosa

in tield lysimeters Cocoon

biomass

(mg) Oa 526 + 15Ob 216 f 80b

after

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tree proximity). The treatments were addition of: earthworms, lime, living roots of P. sirchensis, earthworms plus lime, earthworms plus roots plus lime, and untreated controls. Ground limestone, containing 0.22% Mg, was applied on 31 May and 28 July in the following year, at an overall rate equivalent to 20 t ha-‘. Individual earthworms of A. caliginosa were collected, starved and weighed as detailed previously (Robinson et al., 1992a) and approximately 12 individuals (10 g per treatment>, were added on 8 July. Plastic netting (2 mm mesh) was placed over all of the lysimeters and fixed with plastic cement and strong, waterproof tape to prevent earthworm escape. Leachates from all treatments were collected as before, and analysed for K+ by flame emission spectrophotometry, Ca*+ and Mg2+ by atomic absorption spectrophotometry and PO:--P by autoanalysis using the molybdenum blue method (Allen, 1989). In December, 10 g samples of air-dried P. sitchensis litter were added to each lysimeter to simulate the annual total litter fall per lysimeter as estimated from litter traps, equivalent to 127 g m-* oven-dry mass. The last leachate samples were collected on 7 June, being 1 year after the earthworms were added. The contents of each lysimeter were hand-sorted to collect earthworms, which were washed, starved and weighed as in Robinson et al. (1992a) and cocoons, which were washed and weighed. The soils were then weighed, oven-dried at 105°C for 48 h and reweighed to measure their moisture content. Cumulative yearly leachate fluxes were calculated for each treatment during the year period from when earthworms were added until the termination of the experiment. ANOVAs and Tukey’s HSD comparison of means were used to test for treatment effects. 3. Results

Significantly more A. caliginosa individuals survived in field lysimeters in the limed earthworm Fig. I. Release of (a) K+, (b) Cazf (c) Mg*+ and(d) phosphate-P from peat lysimeters: solid line, control; dotted line, earthworms plus lime; dotted and dashed line, earthworms plus roots and lime (means. n = 4). Differences between treatments and control: * P < 0.05; **P
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treatments than in the unlimed treatment (Table 11. Although there was some mortality, the total and individual biomasses of A. caliginosa were sustained in the limed treatments (Table 1). Individual

I.2

1,Ci

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Table 2 pH values of leachates from field lysimeters and moisttire contents (76 soil dry mass) of total peat profiles (mean&SE, n= 4f Treatment

PH

Mois
Control Roots Earthworms Lime Earthworms Earthworms

3.96 -i 0.02a 3.90*0.02a 4.03 i 0.02a 4.7 I it 0.07b 5.66 + 0.08~ 5.71 f0.06c

580t31a 581 t6la 650 f 42a 540 k ma 597 i- 37a 565 t 34a

+ lime + roots + lime

Means followed (P < 0.01).

d I

by different

letters

are significantly

content

different

body mass was significantly greater with lime. Cocoons were found only in the limed treatments (Table 1). Specimens of Lumbricus eiseni Levinsen, a species which had not been introduced experimentally, and several small cocoons of a species other than A. cdiginosa, were found exclusively in treatments where lime had been applied. Fresh, starved earthworm biomass values (mean + SE, n = 4) were 5+5mg, 120+ 120mgand 110+60mg,inlimed only, earthworms plus lime, and earthworms, plus lime and roots, respectively, apart from one individual (5 + 5 mg) which was found in a rooted lysimeter. Significant effects of earthworms plus lime on Ca2+ and Mg*+ mobilisation were recorded 4 weeks and 6 weeks, respectively, after the addition of earthworms (Fig. l(b) and cc)). Yearly release of K’, Ca’ + and Mg*+ (Fig. 2(a), (b) and (c)1 and mean leachate pII (Table 2) were significantly greater in the earthworms plus lime treatment than in the control. The same treatment had a significantly greater effect on leachate losses of Kf, Ca*+ and Mg* ’ (Fig. 2(a), (b) and cc>), and on pH (Table 21, than addition of earthworms or lime alone. Liming alone significantly increased Ca2+ release (Fig. 2(b)) and leachate pH (Table 2). In the earthworms, plus lime and roots treatment, the roots appeared to take up substantial amounts of K+ and Mg2+, as shown by comparison with the earthworms plus lime treatment

Fig. 2. Yearly flux of (a) K+, (b) Ca*’ (c) Mg2+ and (di phosphate-P from lysimeters (mean + SE, n = 4). Treatment means with different letters are significantty different (P < 0.05). C. control; R, plus roots; E, plus earthworms: L, plus lime.

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(Fig. l(a) and (cl, Fig. 2(a) and (cl). Roots and earthworms alone had little effect on cation mobilisation, and no treatment had a significant effect on phosphate mobilisation (Fig. l(d) and Fig. 2(d)).

4. Discussion

Satchel1 (1955) recorded A. culiginosa in soils of pH as low as 4.7, and sparse populations have been found at pH 3.6 (BouchC et al., 1988). Aporrectodea caliginosa individuals may have escaped from unlimed lysimeters in response to acidic conditions. We have recorded such avoidance behaviour in the laboratory (Robinson et al., 1991). Indeed, the very small effect of earthworms alone on cation mobilisation suggests that earthworms escaped rapidly or died, though the latter might be expected to have had a greater effect on nutrient release than was observed (oligochaetes typically contain 0.5% K, 0.3% Ca, 0.2% Mg and 1.1% P on a dry mass basis; Allen, 1989). In our experiment it is impossible to identify whether the source of the enhanced cation leaching in the earthworms plus lime treatment, compared to the lime or earthworm alone treatments, is the fertiliser and lime applied, or the soil, or the earthworms. The enhancement could be due to preferential leaching of Kf in fertiliser and Ca*+ and Mg*+ in lime to lower layers in the soil profile via earthworm burrows. Aporrectodeu culiginosu burrows have been found to comprise highly effective waterconducting channels in loamy silt (Joschko et al., 19921, although A. culiginosu has been reported to mix lime horizontally rather than vertically (Springett, 1985). Knight et al. (1992) found that mixed populations of earthworms in pasture soils increased leaching losses of fertiliser three-fold. Robinson et al. (1992a) showed that nitrate was the dominant form of nitrogen in the earthworm plus lime and lime only monoliths, and it is possible that enhanced cation mobilisation in the earthworms plus lime treatment occurred through greater nitrate leaching (30 vs. 10 kg ha- i year- ‘1. The reason for the lack of increase in phosphate mobilisation is unclear; Mackay et al. (1982) and Mackay et al. (1983) showed an increase in the availability of P from applied phosphate fertiliser treatments in the pres-

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ence of A. culiginosu, attributable to mixing with soil in casts, and to transport down burrows carried by surface run-off water. Phosphate would be less available at the high pH occurring in limed peat soils (Brady, 1984) than under more acidic conditions. The apparent facilitation by soil invertebrates of cation uptake by living tree roots in deciduous woodland systems was shown by Anderson et al. (1985). The apparent enhanced root uptake of K+ demonstrated in the present study may have implications for increased tree productivity, since K+ deficiency in P. sitchensis is usually associated with deep peat sites (McIntosh, 1981). Enhanced root uptake of Mg*+ could be important in areas of forest decline. Whether the effect of earthworms and lime on cation and nitrogen mobilisation (Robinson et al., 1992a) is sustainable or beneficial to tree growth in the longterm is unknown. However, this investigation has shown that a population of A. culiginosu, whilst maintaining its biomass for a year in limed, fertilised peat lysimeters in the field, increased leaching of Kf, Ca2+ and Mg*+, but not phosphate, to soil layers below 12 cm depth. Enhanced K+ and Mg*+ fluxes were apparently associated with greater uptake by P. sitchensis roots.

Acknowledgements

We thank the Forest Authority for use of the Kershope site, the Chemical Services Section at the Institute of Terrestrial Ecology, Merlewood, for analysing the leachates and everyone who helped with fieldwork. Dr J. Dutch, Forest Authority, kindly provided information for use in this publication. This research was carried out whilst CHR held a Natural Environment Research Council studentship and with partial funding from the European Union.

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