Potential of the Silpho Moor experimental birch plots as a habitat for Lumbricus terrestris

Soil Biof. Biochem. Vol. 12, pp. 317 to 323 Pergamon Press Ltd 1980. Printed in Great Britain

POTENTIAL OF THE SILPHO MOOR EXPERIMENTAL BIRCH PLOTS AS A HABITAT FOR LUMBRICUS TERRESTRIS J. E.

SATCHELL

Institute of Terrestrial Ecology, Merlewood Research Station, Grange-over-Sands,

Cumbria LA1 1 6JU, U.K.

(Accepted 23 February 1980) Summary-It is argued that the podzol of Silpho Moor could be converted under birch to a typical brown earth only if it could sustain an earthworm population with a Lumbricus terresbis biomass of not less than 100 g m-*. No worms of this species were found under experimental birch plots 30 yr old. The presence of podzolizing species in the ground vegetation; the low pH of the raw humus layer; the low Ca and N supply in the soil, litter and rainfall; and the impeded soil drainage lead to the conclusion that colonization by L. terrestrisis unlikely.

INTRODUCTION

the Seventh Approximation and, following Duchaufour (1948), use the term “brown forest soil with a mull type of humus”, a concept which cannot be expressed with absolute certainty in current terminology. Avery’s (1973) soil classification, substantially based on the USDA system, distinguishes between Brown earth (sensu stricro) in the major group “Brown Soils” and Brown podzolic soils (podzolic brown earths) in the major group “Podzolic soils”. Although recent work (Miles, 1978), suggests that birch can transform podzol to podzolic brown earth, Dimbleby’s usage of “brown earth” is more in the sense of the forest brown earth of other writers of the period, the typical brown earth (sensu stricto) of Avery. It must be concluded that Dimbleby’s proposition can best be expressed in the form that, under the influence of a change of vegetation from heather moor to birch wood, the Cleveland Hills podzols can develop into typical brown earths.

From a study of birch stands of different ages on podzolic soils formerly under heather, Dimbleby (1952a) concluded that: “As the birch stands develop, the old heather raw humus becomes activated and eventually destroyed, and when this occurs a mull horizon develops in the mineral soil. Striking changes in soil fauna are recorded, species characteristic of deciduous woodland appear surprisingly soon after colonization by birch. It is estimated that it takes 60-100 yr for the raw humus to be converted to mull”. The experimental plots described in the two preceding papers were set up by Dimbleby to test these conclusions. Since the plots were only 30 yr old in 1978 they can as yet neither confirm nor refute his conclusions but some inferences can be drawn from their development so far. From the time of P. E. Muller, the characteristic soil fauna of forest brown earth with mull humus has been recognized as being the earthworms which ingest mineral and organic material and, in so doing, contribute to the formation of mull humus and a stable soil structure. Jacks (1963) expressed the view that “though crumb-mull structure can be produced in grasslands without earthworms, they appear to be essential for its formation in at least temperate forest soils”. It seems equally tenable that the species of earthworms which promote the formation of crumbmull structure only survive in brown earths. The question of whether Silpho Moor, under the influence of birch, could become a brown earth can thus be transposed to whether it can become capable of sustaining a mull earthworm population.

Mull earthwormfauna

DEFINITIONS Brown earth

Recent papers on soil amelioration by birch (e.g. Miles, 1978) use the soil type nomenclature of the USDA soil classification (Seventh Approximation and later amendments). Dimbleby’s publications predate

The earthworm faunas of mull soils in Britain characteristically include several or all of the following species: Lumbricus terrestris, L. rubellus, Allolobophora caliginosa, A. longa, A. rosea, A. chlorotica and Dendrobaena rubida agg. In woodland sites where mull earthworm faunas flourish, the biomass is dominated by L. terrestris which is the species mainly responsible for burying plant remains below the soil surface. L. rubellus also occurs in acid woodlands where it usually lives permanently in the litter layer without entering the mineral horizons. The Allolobophora species are all totally subterranean in habit except for A. longa, which deposits a proportion of its faeces as wormcasts on the soil surface, and the woodland Dendrobaena species occur in surface organic matter. L. terrestris, because of its leaf burying habit, the size and surface opening of its burrows, and its dominance in terms of population metabolism, is uniquely important in maintaining the mull condition in forest soils. Consideration of the potential of Silpho

317

318

J. E. SATCHELL

Moor as an earthworm habitat can thus be confined in the present context to its potential suitability for this species. Characteristics

of brown earths in the vicinity of Silpho

Moor To define the chemical composition and earthworm biomass characteristic of brown earths near the Sitpho Moor experiment, sites were sought on the same geological formation, viz. the Lower Calcareous Grit on the Hackness outlier of the Tabular Hills, and which had remained under mixed woodland and escaped the podzolizing effect of heather. It was found that none have survived on the summit plateau. The soils on the steep slopes overlying the Grit and fringing the plateau are, except where flushed from the lower Jurassic Limestone above, podzols, brown podzolic soils or intermediates. Brown earths were found on a number of woodland sites, in flushed situations, further down the geological succession on the Oxford Clay and Kellaways Beds, and on the alluvial banks of the River Derwent. The earthworm sampling programme required access to water and the following four sites were therefore selected: Haggland Wood (Grid Ref. 959921), 0.5 km west of Silpho village immediately below Silpho Quarry. The site is on a soiifluxion slope strongly flushed from the base of the Lower Jurassic Limestone exposed immediately above it. Mercurialis, Primula and other calciphile species dominate the field layer and Fraxinus is abundant in the overstorey. Below the influence of the limestone the soil shows a rather sharp transition to an acid brown earth with mor humus and a Deschampsiu~exuosa dominated sward. Thirlsey Bottom {Grid. Ref. 975910), l.Okm north east of Hackness Hall. A flat valley floor below Thirlsey Quarry, strongly flushed from the Lower Jurassic Limestone with Allium, Mercurialis and Chrysosplenium splendens seasonally dominant in the ground layer. Fraxinus, Acer pseudoplatanus and Fagus dominate the overstorey. Hilda Wood (Grid Ref. 971908), 0.3 km north of Hackness Hall. A flushed streamside site was selected near the lower boundary of this wood with a ground layer dominated in spring by AEIium ursinum under mixed deciduous woodland canopy, In both this and the two preceding sites the soils are basically acid brown earths enriched by flushed ground water. Forge Valley (Grid Ref. 9838721, beside the River Derwent on a low alluvial terrace below Spiker’s Hill. A&urn, I~ercurjalis, Anemone nemorosa and Filipendulu u~rn~ria dominate the vernal aspect under a mixed canopy of Fraxjnus, Ulmus, Quercus and Acer pseudoplatat7us.

Samples were collected for chemical analysis from a profile pit in each of the four sites in March 1977 and were analysed by the methods previously described (Satehell, 1980a). The sites were also sampled in March 1977 for earthworms using the formaldehyde method as described in Satchel1 (~98Ob). From the four woods together the following species were recorded: Allolobophora caliginosa, A. chlorotica, A. longa, A. rosea, Lumbricus terrestris, L. rubellus, L. castaneus, Dendro-

3

CI”IN---

000000

5dddddd tl +I -t-I +i +I Cl +I --000b00ch UN--*-O

5

d d d d 6 6

Birch plots as a habitat for Lumbricus terrestris

319

Table 2. Earthworm biomass in four deciduous woodlands on brown earth soils (g m-’ preserved weight)

Lumbricus spp Others Total

Haggland Wood

Thirlsey Bottom

Hilda Wood

Forge

19.1 k 13.2 20.3 ) 3.3 100.0 + 15.8

92.7 f 16.8 20.8 f 6.4 113.5 + 21.7

103.2 f. 16.0 30.3 * 4.5 133.5 * 17.7

78.8 & 8.2 25.5 t 3.2 104.3 + 9.6

baena rubida, D. mammalis, Octolasion cyaneum, Eiseniella tetraedra.

From the biomass (preserved weight) estimates obtained (Table 2), the average weight of Lumbricus species present in these soils appears to be about 86 gm-* but as it is known that not all the worms present are recovered by the formaldehyde extraction method, 100 g m -’ is probably a better estimate. CHANGES BECOME

REQUIRED

FOR

HABITABLE

SILPHO

MOOR

TO

BY L. TERRESTRlS

Despite the substantial literature on L. terrestris, there are aspects of its ecology which are poorly understood and it seems prudent to assume that many chemical and physical characteristics of brown earth soils are important in maintaining stable populations of this species although the causal relationships may not have been fully established. For Silpho Moor to become a brown earth, habitable by L. terrestris, there would have to be a change in the composition of plant leachates, a reduction of acidity, an improvement in the nutrient content of the soil and the nutritional value of the litter, and an increase in soil aeration. Leachates inducing mor formation and podzolization

Certain specific properties of podzols and raw humus such as low nutrient content, acidity and poor aeration are known to be inimical to the species of earthworms associated with mull soils or may be considered so with some confidence. These are discussed later. It may be assumed however that podzols possess other properties which are also likely to be unfavourable to mull earthworms although the nature of their ecological effect is not yet understood. For convenience, these unknown factors can be defined as plant leachates acting indirectly on earthworm ecology by inducing mor formation and podzolization. From sections of Calluna litter, Handley (1954) observed that its vascular tissue decomposes first, leaving a residue of mesophyll cell walls apparently coated with some protective material. He showed that when the leaves die, the cytoplasmic protein becomes stabilized by polyphenolic substances by a process similar to the tanning of animal hides. He found that this process was not confined to Calluna leaves and that gelatin treated with leaf extracts from morforming species was generally more resistant to decomposition than gelatin treated with leaf extracts from mull-forming species. Besides precipitating mesophyll cell protein in a stable form, polyphenols and possibly other complexing substances percolating from surface litter bring about solution of sesquioxides, reduction of ferric iron and formation of soluble metal-organic complexes (Bloomfield, 1957). Podzolization seems unlikely to be

Valley

arrested until a change in the chemical composition of the plant litter reduces the tanning of leaf litter protein and stops the downward movement of sesquioxides by “cheluviation”. Table 3 shows the phenolic content of birch and heather leaves and litter from Silpho Moor and other sites. The concentration of soluble tannins in birch litter depends on the age of the litter and falls from 334% in fresh litter to < 1% after 6 weeks. Dead heather shoots from Silpho contained about 3% soluble tannins but, being of unknown age, could have been weathered for a long period before collection. A better indication of the podzolizing effect of leachates and litter combined is obtained by comparison of the soluble tannin content of growing leaves, 334% in birch but up to 12% in heather. These concentrations strongly suggest an amelioration of podzolization under the influence of birch litter. The depodzolizing process may also be affected by changes in the ground vegetation. In the Silpho birch plots, Calluna is slowly disappearing from the ground flora but in substantial areas is being replaced by Vaccinium (Satchell, 1980a, Table 9), a species similarly rich in polyphenols (Handley, 1954) and with very similar decomposition characteristics (Mangenot, 1966). Deschampsia Jlexuosa is also becoming dominant in the ground flora of the birch plots and Pigott (1970) has described the development of podzol from brown earth under the influence of this species on the Derbyshire limestone. Since D.jIexuosa was dominant in the field layer and V. myrtillus locally frequent in Dimbleby’s 60 yr-old birch stand, their occurrence in the Silpho experimental plots cannot be regarded as transitory and the net effect on podzolization of the change of vegetation on the experimental plots remains uncertain. Acidity L. terrestris rarely occurs in the field at acidities greater than pH 4.3 (Satchell, 1967) and Laverack (1961) has shown that the threshold pH for stimulation of the body wall by acid solutions lies at about 4.34.1. The mean pH of the O-3 cm horizon of the birch plots in 1960 (Satchell, 1980a) ranged from 3.4 to 3.8 so, for the soil to become habitable by L. terrestris, the birch treatment would have to raise the pH between about 0.5 and 1 unit. Repeat measurements in 1975 showed a pH range from 3.3 to 3.5, not significantly different from the values obtained 15 yr previously. Similar observations have been made on an older site, a 60yr-old birch plantation on Suffield Moor. This site, about 2 km from Silpho Moor, was formerly heather moor and the plantation can be dated from estate records. The pH of the raw humus, measured by Rennie (1955) was 3.2, that of Silpho Moor being then 3.1. Rennie commented “the growth of birch not

320

J. E. SATCHELL only increases the depth of the existing raw humus, but builds upon it weights of extremely acid litter far greater than those already existing under the Caiha”. The 40 yr site in Dimbleby’s age series of birch stands had a 5 cm deep layer of birch litter of pH 3.6 which is comparable with the 30yr birch plots on Silpho Moor. At Silpho there are no indications at present of an amelioration of acidity such that the soil could become habitable by Lumhricus tetwstris.

Calcium. In many soils pH is closely correlated with Ca content and the literature holds conflicting views on whether the absence of eutrophic earthworm species from the most acid soils is attributable to the acidity or to insufficiency of available Ca to meet the requirements of earthworm metabolism (Jefferson. 1956; Laverack, 1963). The population densities of e~thworm populations of several species in experimental grass plots at Rothamsted (SatchelI, 1955) were as closely correlated with exchangeable Ca as with pH, Ca accounting for 4761% of the population variance and pH for 48862%. The plot on which the lowest population of L. terrestris was recorded (excluding one where only a single specimen was found), contained in the upper 23 cm horizon 1.41 m-equiv of exchangeable Ca 100 g- ’ soil. Assuming a soil bulk density of 0.9 g crns3, this is equivalent to 761 kg ha- 1 to 30 cm. This is close to the value of 567 kg ha-’ (Table 4) estimated by Rennie (1955) as the amount of available Ca in the O-25 cm horizon of a forest brown earth at Thornton Dale in the Cleveland Hills. Concentrations of extractable Ca in the four brown earths selected for comparison with Silpho Moor ranged from 1100 mg 100 g- ’ throughout the upper 40 cm in Haggland Wood to 84 mg 100 g- 1 in the lO-20cm horizon of the Forge Valley site. In this latter site the mean concentration to 30 cm depth was 98mg lOOg_*, equivalent at an assumed specific gravity of 0.9 g crne3 to 2646 kg ha-i. The mean concentration in the upper 30cm of the four profile pits sampled in the Silpho Callunetum was ~9.6 mg 1OOg-‘, equivalent to < 259 ka ha-‘. To reach the concentration in the Forge Valley site, the Calluneturn would therefore have to receive at least an additional 2387 kg ha- i. Two mechanisms can be envisaged by which the Ca content of the litter and A horizon could increase under birch wood vegetation: by transfer of Ca reserves from the B horizon and by retention of the Ca input from rain. Dimbleby (1952b) attached considerable importance to the capacity of the root system of birch to absorb mineral nutrients from unleached soil below the ironpan as the source of base enrichment of the litter layer. The concentration of exchangeable Ca throughout the B horizon at Silpho is < 1.5 mg 100 g- I and only 3.5 mg 100 g- ’ in the Be/C horizon at 60-70 cm. The Ca was estimated as 142 mg 100 g- ’ at 30-45 cm and 131 mg lOOg_’ at 45-75 cm, equivalent to 5454 kg ha-’ from 30-75 cm. About 44% of the total Ca reserve in the B-C horizon down to the maximum rooting depth would thus be adequate to raise the con~entratio~ of exchangeable Ca in the 0-30cm horizon to that found in the Forge Valley. However.

Birch plots as a habitat for Lumbricus terrestris

321

Table 4. Selected chemical data from Rennie (1955) Nutrient content of Silpho Moor soil

Total (kg ha-‘)

0-ironpan (28 cm) @50 cm

Calcium Available (kg ha-‘)

Potassium Available (kg ha-‘)

Phosphorus Total Available (kg ha- ‘) (kg ha- ‘)

Nitrogen Total (kg ha-‘)

96 227

11 15

7 13

60 164

8 9

3387 3900

842 ND

567 1547

4 13

124 238

11 21

791 1045

Nutrient content of a brown earth at Thornton Dale G25 cm O-50 cm

ND = not determined. there is virtually no organic matter in the Silpho subsoil and the parent rock is a quartz sandstone, with very rare Ca-bearing ferromagnesian minerals and most of the Ca present in Na-Ca felspars (plagioclase). Dimbleby envisaged the formation of mull under birch in 6&1OOyr and there is no evidence that Ca can enter the labile pool in sufficient quantity during this period from such a relatively slow-weathering mineral. The input of Ca in precipitation has been measured in weekly rainwater samples collected on Silpho Moor by Allen et nl. (1968) who estimated that the total Ca content of the rainfall from May 1965 to May 1966 was 9.8 kg ha-‘. If none of this input were lost by leaching or held out of circulation in the plant biomass, the total Ca content of the A horizon could reach that of a brown earth in about 60 yr. Since Ca mobility will remain high while the acid raw humus layer persists, a much longer time must be envisaged for formation of brown earth soil. Nitrogen The protein requirement of L. terrestris is met partly from the plant remains pulled into its burrow openings and partly from ingested soil. The proportion of the N requirement of a L. terrestris population

Table 5. Calcium concentrations in four profiles on the Silpho Callunetum Profile

1

2

3

4

Total Ca (mg 100 g-r)* 400 01 + Of 240 Oh 220 Ea 210 Bh 130 BFe 100 Bsg 94 Be/C

290 240 110 160 130 120 100

220 120 110 120 140 110 130

220 150 150 130 290 290 loo

Extractable Ca (mg 100 g-r)? 55 01 + Of 12 Oh L1.5 Ea < 1.5 Bh 41.5 BFe cl.5 Bsg < 1.5 Be/C

50 14 11.5 c 1.5 11.5 <1.5 < 1.5

67 10 <1.5 <1.5 cl.5 < 1.5 5.0

66 7.7 t1.5 <1.5 <1.5 <1.5 5.0

* Extracted in HF/HNOs + HClOJH#04. t Extracted in NH40Ac at pH 7.

which might be met by soil and litter ingestion cannot be estimated with any precision because of uncertainties about the feeding behaviour, assimilation efficiency and N excretion rate of earthworms under field conditions, but an informed guess can be made as follows: (1) The dry weight of the gut contents of L. terrestris of various sizes collected from a mixed hardwood stand was on average 29% of the dry weight of the whole worm. Regression analysis gave the relation 1 g dry weight = 5.5 g live weight (Satchell, 1970) so the gut contents of a population of 1OOg live weight would weigh about 5.27 g. (2) Food passes through the gut of L. terrestris in about 20-24 h (Parle, 1963; Satchell, 1970). (3) Feeding activity is restricted by soil temperature and moisture to perhaps 200 days yr-‘. (4) A population of 100 g m-’ biomass might therefore ingest approximately 1 kg soil rn-’ yr- ‘. (5) The average N content of the upper 3 cm horizon of the birch plots is at present 1.41% of the oven dry weight and occurs mainly in the raw humus. If this became mineralized it would be partly withdrawn into plant biomass and from comparison with other forest soils, the N content of the O-5 cm horizon of developing mull soil might be reasonably estimated as 0.7%. (6) If the L. terrestris population ingested soil only from this upper, most N-rich horizon, it might therefore ingest about 7 g N me2 yr-t. (7) It is impracticable to estimate the assimilation efficiency of L. terrestris directly because its selective feeding behaviour makes the nature of the material ingested uncertain. From a systems analysis of litter decomposition by L. terrestris in a mesic mixed forest, Reichle (1971a) estimated that 19% of the material ingested was assimilated, a value within the range of l&20% expected for the assimilation efficiency of saprovores generally (Reichle, 1971b). Of the estimated7gNm-2yr-1 ingested, 1.33 g might therefore by assimilated. (8) Lakhani and Satchel1 (1970) estimated the relative productivity of two populations of L. terrestris as 33W80mgg-’ yr-’ and 42&560 mgg-’ yr-l. Assuming an average of 450 mg g-i yr- ‘, tissue production by a population with 100 g me2 biomass can be estimated as 45 g mW2yr-‘. The N content of L. terrestris tissue has been estimated (Satchell, 1963) as 1.75% of the fresh weight so the N requirement for tissue production of 45 g would be about 0.79 g.

322

J. E.

SATCHELL

(9) Needham (1957) determined the mean rate of N excretion by L. terrestris under experimental conditions as 269 pg g- 1day- ‘. When soil temperatures are taken into account this leads (Satchell, 1963) to an estimate for a biomass of lOOgm_’ of 2.72gm-2yr-‘. (10) The above values lead to estimates of a possible N requirement of 3.5 g me2 yr- ’ and an assimilable soil N supply of 1.33 gm-’ yr-‘. (11) The mean N content of four birch leaf litter samples, one sample from each birch plot, collected after leaf fall in 1975 (Satchell, 1980a, Table 5) was 0.94%. Assuming an annual leaf litter fall of 2.5 kg ha-’ (the rate at which litter was applied to the experimental plots), the N input from birch leaf litter would be 2.35 gm-’ yr-‘. (12) Field layer production in woodlands is commonly about 20% of tree and shrub litter fall (Bray and Gorham, 1964) so the N content of the whole leaf litter input may be approximately 3 g me2 yr- ‘. (13) Even if the earthworms consumed the whole of this litter production and had an assimilation efficiency of 19% they would derive only 0.57 g rn-’ yr- ’ from it. (14) From (10) and (13), there appears to be an assimilable N supply of up to 1.9 g mm2 yr-l to meet a requirement of 3.5 g mm2 yr-‘. (15) The N input from precipitation was estimated by Allen et al. (1968) as 1.3 gm-‘yr-‘. If all of this were converted to organic matter and consumed by the earthworms at an assimilation efficiency of 19% it would yield 0.25 g mm2 yr- ’ of N. (16) Even on the unlikely assumption that the earthworm population could consume the entire N supply of the soil, the leaf litter and the rainfall, the available estimates suggest that only about 60% of the earthworms’ N demand could be met. Aeration Lumbricus terrestris can survive long periods of immersion in water but only if the water is well aerated (Raffy, 1930; Roots, 1956). As shown by Satchel1 (1980b), Silpho Moor is periodically waterlogged with O,-deficient water. Examination of the four profile pits on the Callunetum after the winter of 1975-76 showed that drainage impedance occurred at about the level of the iron pan where water ran out laterally below the overlying soil. The impedance appears to be caused partly by the pan itself and partly by the compact subsoil described from elsewhere on the Hackness Moors by Yeatman (1955). The hardpan varies in depth between about 15 and 16 cm and is frequently convoluted where it divides the illuvial horizon from the compact material below. To effect the improvement in drainage and aeration requisite for the survival of L. terrestris, the roots of the birch trees would have to decompose or disrupt the iron pan and penetrate the compact subsoil. Radiocarbon dating of the humic material associated with the iron pan and the organic layer overlying it gave mean age estimates (D. Harkness, Personal Communication) of respectively 1497 and 1153 yr B.P. and suggests that this material is not readily biodegradable. No mechanism by which the birch rhizosphere microflora could decompose it in a few decades has been described. Moreover, as seen in the profile

pits on the birch plots, the roots are confined in the main to the A horizon, spreading out horizontally where they meet the iron pan. There is no indication at present that the birch will penetrate either the iron pan or the compact subsoil to an extent likely to improve the drainage. CONCLUSION

Thirty years after the experimental plots were set up neither Lumbricus terrestris nor any other mullsoil species of earthworm has invaded the birch plots. Although the birch trees provide a less podzolizing litter than Calhma, the ground vegetation beneath them is dominated by Deschampsia flexuosa and Vaccinium myrtillus which are thought also to be podzolizing species. A new and extremely acid raw-humus layer has developed under the birch trees since the original raw humus layer was destroyed by screefing. The Ca and N requirements of a Lumbricus terrestris population of 100 g m- ’ appear to be considerably more than could be supplied by the soil, litter and rainfall. There is no evidence of movement of iron out of the iron pan under birch and the drainage of the site remains impeded causing periodically anaerobic conditions. There is thus no evidence so far from this experiment that birch has or can ameliorate the soil to a condition tolerable to Lumbricus terrestris. If, as is suggested, the podzol could only be transformed to a brown earth through the pedogenic activities of earthworms of this species, then a brown earth cannot be expected to develop. Acknowledgements-I

am much indebted to Professor G. W. me to participate in his experiment and to the staff of the Forestry Commission at Langdale Forest for their assistance in the field, generously given over a number of years.

Dimbleby for inviting

REFERENCES

ALLEN S. E., CARISLE A., WHITE E. J. and

EVANS C. C.

(1968) The plant nutrient content of rainwater. Journal of Ecology 56,497-504. ASKKXATION OF OFFICIAL ANALYTICAL CHEMISTS (1970) OSJicial Methods of Analysis. AOAC, Washington, D.C. AVERY B. W. (1973) Soil classification in the soil survey of England and Wales. Journal of Soil Science 24, 324-337. BLCKIMFIELDC. (1957) The possible significance of polyphenols in soil formation. Journal of the Science of Food and

Agriculture 8, 389-392.

BRAY J. R. and GORHAM E. (1964) Litter production in forests of the world. Advances in Ecological Research 2, 101-57. DIMBLEBYG. W. (1952a) Soil regeneration in the north east Yorkshire Moors. Journal ofEcology 40, 331-354. DIMBLEBYG. W. (1952b) The historical status of moorland in north east Ybrkshire. New Phytologist 51, 349-354. DUCHAUFOUR P. (1948) Recherches Ccologiqpes sur la ChCnaie Atlantique Franqaise. Annales de I’Ecole Nationale des Eaux et For& et de la Station de Recherches et Expkiences Forestit+es 11, 5-332. FORSYTH W. G. C. (1955) Cacao polyphenol substances 3. Separation and estimation on paper chromatograms. Biochemical Journal 60, 108-l 11. HANDLEY W. R. C. (1954) Mull and Mar Formation in Relation to Forest Soils. Forestry Commission Bulletin 23, 115 pp.

Birch plots as a habitat for Lu~ricus HEAL0. W., LATTERP. M. and HOWSONG. (1978) A study of the rates of decomposition of organic matter. In Production Ecology of British Moors and Montane Grasslands. (0. W. Heal and D. F. Perkins, Eds), pp. 136159.

Springer, Berlin. JACKS G. V. (1963) The biological nature of soil productivity. Soils and Fertilizers 26, 147-150. JEFFER~~~~ P. (1956) Studies on the earthworms of turf. journal of&e Snorts Turf Research institute 9. 166-179. LAKHANIK. II. and SATCHELL J. E. (1970) Production by Lumbricus terrestris (L.). Journal of Animal Ecology 39, 473-492.

LAVERAC~~ M. S. (1961) Tactile and chemical perception in earthworms II. Responses to acid pH solution. Comparative Biochemistry and Physiology 2, 22-34.

LAVERACK M. S. (1963) Tke Physiology of Earthworms. Pergamon Press, Oxford. LONG C. (1961) Biochemists handbook. Spans, London. MANGENOT M, F. (1966) Etude mi~obiolo~que des litieres (Commentaires sur les don&s experimentales recueillies a 1’E.N.S.A.N. depuis 1963). Bulletin-Ecole Nationale Superieure d’Agronomie, Nancy 8, 113-125. MILES J. (1978) The influence of trees on soil properties. Institute of Terrestrial Ecology: Annual Report 1977, 7-11.

Moss R. and PARKINSONJ. A. (1972) The digestion of heather (Calluna vulgaris) by red grouse (Lagopus lagopus scotticus). 285-298.

British

Journal

of

Nutrition

27,

NEEDHAMA. E. (1957) Components of nitrogenous excreta in the earthworms Lumbricus terrestris (L.) and Eisenia foetida (Savigny). Journal of Experimental Biology 34, 4255446.

PARLE J. N. (1963) Micro-organisms in the intestines of earthworms. Journal of General Microbiology 31, l-l 1. PICGOTC. D. (1970) Soil formation and development on the carboniferous limestone of Derbyshire. Journal of Ecofogy 58, 529-540.

R~FFYA. (1930) La respiration des vets de terre dans l’eau. Action de le teneur en oxygene et de la lumi&re sur intensite de la respiration pendant l’immersion. Comptes Rendu Hebdomadaire des Seances Sciences, Paris 105, 862-864.

de l’dcademie

des

terrestris

323

REICHLED. E. (1971a) Systems analysis as applied to ecological processes-a mechanism for synthesis, integration and interpretation of IBP woodlands ecosystem research. In Systems Analysis in Northern Coniferous Forests (T. Rosswall. Ed.). vv. 12-28. Swedish Natural Science Research ConnciL’Stbckholm. REICHLED. E. (197lb) Energy and nutrient metabolism of soil and litter invertebrates. In productivity of Forest Ecosystems (P, Duvigneau~ Ed.), pp. 465-478. UNESCO, Paris. RENNIEP. J. (1955) The uptake of nutrients by mature forest growth. Plant and Soil I, 49-95. ROOTSB. I. (1956) The water relations of earthworms II. Resistance to desiccation and immersion, and behaviour when submerged and when allowed a choice of environment. Journal of Experimental Biology 33, 294. SATCHELL J. E. (1955) Some aspects of earthworm ecology. In Soit Zoology (D. K. McE. Kevan, Ed.) pp. 180-201. Butterworths, London. SATCHELLJ. E. (1963) Nitrogen turnover by a woodland population of Lwmbricus terrestris. In Soii Organisms (J. Doeksen and J. Van der Drift. Eds.). VD. 6(X6. North Holland, Amsterdam. SATCAELLJ. E. (1967) Lumbricidae. In Soil Biology (A. Burges and F. Raw, Ed%), pp. 259-322. Academic Press, London. SATCHELLJ. E. (1970) Measuring population and energy flow in earthworms. In Method; of Study in Soil Ecoto$y (J. Phillioson. Ed.). DD.261-267. UNESCO. Paris. S.&XELL J. E. ‘(198~~).~il and vegetation changes in experimental birch plots on a Calluna podzol. Soil Biology & Biochemistry 12, 303-310.

SATCHELL J. E. (1980b) Earthworm populations of experimental birch plots on a Calluna podzol. Soil Biology & Biochemistry 12, 311-316.

SATCHELLJ. E. and LOWE D. G. (1967) Selection of leaf litter by Lumbricus terrestris. In Progress in Soil Biology (0. GralTand J. E. Satchell, Eds.), pp. 102-117. Vieweg, Braunschweig. YEATMAN C. W. (1955) Tree Root ~e~lopment on Upland Heaths. Forestry Commission Bulletin 21, HMSO, London.