Vol. 12, pp. 31
PergamonPress Ltd1980. Pnntedm GreatBritain
EARTHWORM POPULATIONS OF EXPERIMENTAL PLOTS ON A CALLUNA PODZOL
J. E. SATCHELL Institute of Terrestrial Ecology, Merlewood Research Station, Grange-over-Sands, Cumbria LA1 1 6JU, U.K. (Accepted 23 February 1980) Summary-Experimental plots set up by G. W. Dimbleby to test the effect of birch on the soil of a podzolized heather moor were sampled for earthworms after 8, 10 and 27 yr. Of 213 worms collected, one was Dendrobaenaoctaedra (Savigny, 1826) and the remainder were Bimastoseiseni (Levinsen, 1884). No worms were found on the heather control plots and a single specimen only was taken on plots screefed and sown with Molinia. The population density on plots treated with birch litter, taking 1 yr with another, averaged approximately 1.7 worms m-’ with a biomass < 1 g m-*. On the Callunetum surrounding the experimental plots worms were sampled by a trapping method. Only B. eiseni was found. On the Callunetum and on the experimental plots worm numbers were correlated with the calcium content of the O-3 cm soil horizon. Parts of the experimental site and surrounding Callunetum are subject to intermittent waterlogging. The development of the earthworm population in these areas appears to be restricted by occasional reducing conditions in the upper organic horizon.
An experiment to test the effect of birch on a podzolized heather moor in north east Yorkshire was set up by G. W. Dimbleby in 1948. Details of the site and experimental treatments are given in Satchel1 (198Oa) together with observations on changes in the soil and vegetation in the following 30yr. The present paper describes observations on the earthworm populations of the experimental plots and the surrounding Callunetum. EARTHWORM
Sampling methods The experimental plots were sampled in 1956, 1958 and 1975. Only two species of earthworm, Bimastos eiseni (Levinsen, 1884) and Dendrobaena octaedra (Savigny, 1826), both occupying the surface horizons of litter, raw humus and superficial mineral soil, were found. The populations were aggregated and of very low density and it is impracticable to obtain precise population estimates under these conditions by existing methods. In 1956, the vermifuge properties of dilute formalin were not yet widely known and the potassium permanganate method (Evans and Guild, 1947), now obsolete, was used. The earthworms collected were preserved in 4% formalin, the effects of which are discussed in Satchel1 (1971). In 1975, potassium permanganate was again used to ensure comparability with previous sampling but an additional set of samples was taken by the formaldehyde method as a basis for comparison in possible future studies. Neither hand sorting, the potassium permanganate method, nor the formaldehyde method extracts all the earthworms present (Nelson and Satchell, 1962; Satchell, 1971) but the results obtained are not suspected of bias in relation to the plot treatments.
All plots were sampled in October 1956 and again in October 1958, respectively 8 and 10 yr after the experiment began. On each occasion, five quadrats, each 1 m’, were sampled on each plot or half plot. The growing heather or Molinia was cut and removed from each quadrat and the surface litter of birch leaves, heather or Molinia was collected and carefully searched. Potassium permanganate solution at the concentration recommended by Evans and Guild (1947), 2 g l- ‘, was then applied in three lots of 8 1 at 10 min intervals. In 1975 the same procedure was followed but, on the birch plots, after removal of the litter, 10 quadrats were treated with permanganate and 10 with 0.55’% formaldehyde solution. The treatments showed no significant difference, the permanganate quadrats yielding 7 worms and the formaldehyde quadrats 8 worms (excluding those collected by hand from the litter), so the data were combined. As the birch plots were so dense in 1975 as to be difficult to penetrate, the quadrat size was reduced to 0.5 m2, allowing the quadrat frame to be placed more easily between the birch stems. The samples were taken a little later than in the previous years, in the first week of November, but before the completion of leaf fall. By 1975, application of birch litter to the heather plots (treatment B) had been discontinued, heather had recolonised the originally bare screefed plots (treatment S), and Molinia (treatment G) had been found to have no effect on the earthworm population. Sampling was therefore confined to the four plots with growing birch trees (treatments BS and BSG) and the four control plots (treatment C). Treatment G was ignored although some of the quadrats contained Molinia. Population densities From all the quadrats sampled in 1956, 138 8. eiseni and 1 D. octaedra were collected and, in 1958, from quadrats adjacent to those sampled in 1956 and 311
of the same area and number, 46 B. eiseni and 9 D. octaedra were collected. The difference is within the limits of year-to-year variation normally encountered in earthworm populations (Satchel], 1967) and is not interpreted as indicating a change in habitat. In 1975, 19 worms, all B. eiseni, were collected from the 20 quadrats under birch and none from the 20 quadrats not under birch; indicating populations respectively of 1.9 rnd2 and < 1 ms2. In all years the populations fell clearly into two classes, those of plots receiving birch litter and those of plots not receiving birch litter, none of the other treatments showing any significant effect on earthworm numbers (Table 1). On the plots not receiving birch litter, one worm was found in 40 quadrats in 1956 and none in 1958 and 1975. On the plots receiving birch litter there was considerable variation both within and between plots but pooling all the results from all the birch litter plots sampled in all three years yields a population estimate of 212 worms 130me2 or 1.63 rnm2. The biomass of this population is estimated as approximately 0.22 g m- ’ preserved weight. Earthworm distribution in relation to soil conditions Many contemporary ecologists would regard attempts to relate population densities to instant measurements of a few physical and chemical characteristics of the environment as somewhat naive. A simple multivariate analysis based on general considerations of earthworm ecology and readilyavailable facilities was nevertheless used, the ecology of the dominant species, Bimastos eiseni, being virtually unknown. In April 1960, four soil samples, each of two combined cores, 5 cm dia and 3 cm deep, were taken from each of the 16 plots previously sampled for earthworms. Their pH, loss on ignition (SSOC), N content (Kjeldahl digestion followed by distillation) and Ca content (titration with EDTA using ammonium purpurate as indicator) were determined (see Satchell, 1980a). It was thought that these would have changed little since the earthworm populations had been sampled, particularly in the relationships between plots, and the data from the different years could therefore legitimately be analysed together. For analysis in relation to soil conditions, the number of worms in each plot was taken to be the total of the number collected in the 5 quadrats sampled in 1956 and in the 5 quadrats sampled in 1958. Inspection of the data showed no relationship Table
Block Treatment* Control (C) Screefed, grassed (S&G) Birch (B) Birch, screefed (BS) Birch, screefed, grassed (BSG)
ab/wx 1956 1958
cd/wx 1956 1958
between earthworm distribution and pH. Simple regressions (Tables 2 and 3) of earthworm numbers on Ca and N content and loss on ignition, were significant at the 5% level only for Ca. In multiple regressions with two independent variables, addition of loss on ignition, but not of N, significantly increased the variance accounted for. In a regression with three independent variables addition of Ca to N and loss on ignition increased the variance accounted for significantly. The results suggest that the observed earthworm distribution was positively correlated with the Ca content of the surface soil and litter and negatively correlated with the amount of soil and litter organic matter. The earthworm populations of the birch plots in 1975 were no higher than those sampled in 1956 and 1958 and this is in conformity with the chemical data which show no amelioration of the organic horizons as an earthworm habitat (Satchell, 1980a). Position effect In the multiple regressions, earthworm numbers are negatively related to loss on ignition, indicating that conditions which are conducive to a build up of organic matter are inimical to earthworm survival. Inspection of the data showed that the relationship is independent of plot treatment and might therefore reflect variations in the site. This was supported by a strong position effect in the earthworm distribution which may be roughly demarcated by a line between the NW and SE corners of the experimental block. Considering only the plots receiving birch litter, the mean earthworm density north east of this line was 3.26 worms me2 in 1956 and 1.21 worms m -2 in 1958 and, south west of the line, 0.64 worms m-* in 1956 and 0.41 worms mm2 in 1958. An extension of this distribution pattern was found outside the experimental block.
Description of the area The experimental block is bounded by a forest road about 5 m wide and is surrounded to the south and west by a wide expanse of undisturbed Callunetum containing, in a wetter position west of the block, a small proportion of Eriophorum uaginatum. North of the block, a narrow area of disturbed Callunetum separates the plots from another forest road, beyond the experimental cd/v 1956 1958
from 5 quadrats,
ab/yz 1956 1958
1m* Nom-’ 1975
* For details see Satchel1 1980a. ND not determined.
Earthworm populations of birch plots on a podzol
Table 2. Regressions of worm numbers on soil variables
Data from experimental plots Regression coefficients Log Log Log % LOI % Ca %N
(1) (2) (3) (4) (5)
1.983 0.716 - 1.256 4.417 12.720
- 3.458 1.093
(11) (12) (13) (14) (15) (16) (17)
2.861 0.866 0.215 6.294 6.321 1.234 7.532
0.521 0.359 0.257 0.634 0.704
- 2.896 4.064
0.636 0.429 0.336 0.769 0.745 0.438 0.797
1.001 1.284 1.143
Data from Callunetum Regression coefficients Log Log Log % LOI %N %Ca - 1.136 - 0.934 - 3.044 -2.244 - 3.233
- 0.493 1.072 0.268 0.657
- 1.285 1.867
** ** **
* Significant at 5% level. ** Significant at 1% level. *** Significant at 0.1% level.
which is a young conifer plantation which has been deep ploughed. Another forest road runs about 40m from the edge of the block on its eastern side through Callunetum which has been disturbed by bulldozer tracks. The forest roads were made by removing the surface soil and vegetation with a bulldozer and this material now forms low mounds fringing both sides of the two outer roads. It forms a low continuous mound around the outer edge of the road and is covered by a dense and luxuriant growth of heather.
the traps on the north and east sides of the block yielding an average of 21.7 worms per trap and those on the south and west averaging 9.0 worms per trap. Soil samples were taken from 20 trapping positions, selected to provide a range in the number of worms trapped, for chemical analysis as previously described (Table 4). Soil pH varied between 3.2 and 3.9 and showed no relationship to earthworm distribution. Simple and
Earthworms were collected in the area surrounding the plots by a trapping method utilising earthenware seed trays, 20cm dia and 5 cm deep. Holes were drilled in the bottoms of the trays for drainage and each tray was then filled to a depth of about 4cm with Calluna raw humus which had been collected on the site and broken up by hand. Each tray was then filled to the top with dried, milled cow dung and set into the ground, level with the soil surface. After l-2 months the trays were searched for earthworms and the raw humus and dung were changed to prevent cocoons hatching in the traps. Sixty-four traps were set out in four sets of 16, one set on each side of the experimental block. Each set comprised four rows of four traps with rows 25 m apart and traps 10m apart in each row, the nearest traps to the plots being placed at the outer edge of the mounds of road spoil (Fig. 1). Earthworm distribution in relation to soil conditions
From nine collections made between October 1957 and November 1958, 571 worms were collected, all B. eiseni. Their distribution showed the same position effect as was observed on the experimental block, with
Table 3. Significance of added parameters
Experimental plots Equations compared F (d.f.)
N LOI N LOI N LOI Ca
4-l 5-l 6-3 6-2 7-5 74 7-6
2.845 5.760 1.836 0.828 0.171 2.410 7.728
(1,13) (1,13) (1,13) (1,13) (1,12) (1,12) (1912)
14-11 15-11 1613 16-12 17-15 17-14 17-16
7.750 5.716 1.655 0.159 3.529 1.925 19.477
(1917) (1,17) (1,17) (1.17) (1916) (1,16) (1, 16)
Ca N Ca N Ca LO1
J. E. SATCHELL
Table 4. Chemical analyses of the upper 3 cm horizon of the Callunetum at points adjacent to earthworm traps No. of worms taken in trap 0
2 2 3 3 4 5 1
9 11 13 14 15 17 22 23 28 43 47
3.40 3.61 3.58 3.21 3.19 3.20 3.40 3.30 3.35 3.75 3.12 3.22 3.50 3.35 3.32 3.65 3.90 3.78 3.12 3.70
82.1 75.8 71.1 90.8 68.0 84.9 74.2 91.0 81.1 13.9 46.1 23.6 63.2 70.0 71.7 19.9 24.3 18.3
44.9 0.06 39.2 0.05 40.0 0.04 45.9 0.04 36.9 0.02 44.8 0.06 40.6 0.05 42.0 0.06 45.1 0.08 8.7
1.26 0.93 1.05 1.21 1.03 1.23 1.12 1.30 1.39 0.21 0.65 0.41 1.03 1.11 1.12 0.37 0.78 0.41 0.66 0.89
35.6 42.2 38.1 31.9 35.8 36.4 36.3 32.3 32.5 41.4 32.6 32.0 33.1 35.0 34.7 30.3 27.4 30.0 26.4 32.3
multiple regressions of the total numbers of earthworms taken from each trap on soil parameters were again calculated (Tables 2 and 3). Calcium. The simple regression on Ca gave an r value of only 0.336 but the addition of Ca to loss on ignition in a two parameter regression increased the variance accounted for significantly. Adding Ca to N in a two parameter regression and to loss on ignition and N in a three parameter regression did not increase the amount of variance accounted for significantly and the values are consequently inconclusive. The concentration of Ca in the upper 3 cm horizon is extremely low throughout the plots and the Calluneturn, the range recorded in 1960 extending from
on + 0.457
(%LOI) with r = 0.891) and hence negatively with the worm numbers. The relationship was confirmed by two additional sets of results. In November 1957, the weight loss on drying of the entire contents of 64 worm traps which had been in the field for 2 months was determined and in September 1958, the moisture content at the 64 trapping positions was determined from a pair of soil samples taken adjacent to each trap to a depth of 3 cm. Figure 1 shows the close correspondence between positions with relatively high and low moisture content and the areas of high and low earthworm densities. The correlation between loss on ignition and moisture content of the soil cores shows that the amount of water present is largely determined by the thickness of the raw humus layer but the difference in moisture contents of the traps must reflect variations in the drainage of the site since the material in all the traps was the same. Oxidation-reduction potential. Since earthworms are generally capable of withstanding prolonged immersion in water provided its aeration is adequate, there seemed no reason to suppose that excessive water, per se, could account for the relatively low numbers of earthworms trapped in the wetter parts of the site. If, however, a combination of standing water and peaty organic matter led to reducing conditions and the liberation of H,S, the surface horizons would become temporarily toxic and earthworm populations which might have developed during more favourable periods would be destroyed. The occurrence of reducing conditions near the soil surface was demonstrated on 15 November 1961 when the moor was extremely wet with standing water present on the plots and on the Callunetum. Four soil blocks, each approximately 40 cm square x 20cm deep, were cut with a spade from the Callunetum, two from wet positions west of the plots and two from dry positions east of the plots. The blocks were packed tightly in polythene bags and were returned to the laboratory for redox measurement. Mr C. Urquhart obtained the readings shown in Table 5 from measurements made at 135°C. The readings indicate fully oxidizing conditions throughout the dry samples and reducing conditions probably throughout wet sample 2 and at 2 cm depth and below in wet sample 1. The wet samples but not the dry samples smelled strongly of H,S. Redox potentials had been measured in the Callunetum by G. W. Dimbleby in September 1959. They indicated oxidizing conditions at all points but this was not unexpected since the measurements were made after a long spell of dry weather. Redox measurements were again made in the field on 29 and 30 November 1961. On the first occasion the moor was wet but free of standing water. Readings were taken at 20 of the trapping stations in the Callunetum at depths of 1 and 2 cm. No difference at these depths was found between positions east and west of the plots, and there was no correlation between the measurements obtained and the number of worms caught at the trapping stations. On the second occasion, after a night’s heavy rain, there was again standing water in depressions on the moor. Readings were taken at 1, 2 and 4 cm depths at five trapping stations west of the plots and at five
Earthworm populations of birch plots on a podzol
moisture content of 5oil samples > 70%
(a) Soil moisture content (%).
(b) Total worms from 9 collections Ott 1957-NOV 1958 *Worms m-’ on birch plots-average of 1956 atid 1958 samples. Fig. 1. Distribution of worms in relation to soil moisture.
J. E. SATCHELL
Table 5. Oxidation-reduction
1 cm 2cm 4cm
Dry sample 1 Eh (mV) After Initial 60sec 330 332 315
340 350 350
potentials of Callunetum samples
Dry sample 2 Eh (mV) After Initial 60 set 410 415 390
430 412 405
corresponding trapping positions east of the plots, the mean soil temperature being 6.1”C. No difference was
detected between the two sets of measurements at the 1 and 2cm depths. At 4cm, conditions were more reducing west of the plots, the mean Eh values being East (8 worms per trap) 279.2mV, West (2.2 worms per trap) 174.2 mV. On 29 November, potentials in the upper 1 cm of the moor measured at 20 points ranged from 260 to 430 Eh (mV). The following morning, after heavy rain, the range had dropped at 16 points measured at the same depth to 12&170 Eh (mV). The readings suggest that conditions of extremely low O2 tension occur occasionally even in the surface layer of Culluna litter which B. eiseni inhabits and it seems likely that this situation is commoner west of the plots where earthworm populations are low than east of the plots where they are higher. THE BIRCH PLOTS EARTHWORM
Soil samples taken in 1975 from the upper 3 cm horizon of the four plots now under birch (treatments BS and BSG) and from the four heather control plots indicated that the birch has not materially improved the site as an earthworm habitat. This is supported by the 1975 sampling results which show that the earthworm populations have neither increased nor diversified since they were first sampled in 1956.
Wet sample 1 Eh (mV) After Initial 60sec 280 130 105
330 110 105
Wet sample 2 Eh (mV) After Initial 60 set 110 135 180
150 170 205
On the BS plots where decomposition of the original raw humus had been activated by screefing, an even thicker raw humus layer has now developed. It has a mean pH of 3.35 and a C to N ratio not significantly different from that of the O-3 cm horizon of the heather control plots. The potential of the birch plots as a habitat for mull species of earthworms is discussed in Satchell, 1980b). REFERENCES
EVANSA. C. and GUILD W. J. McL. (1947) Studies on the relationship between earthworms and soil fertility I. Biological studies in the field. Annals of Applied Biology 34, 307-330.
NELSONJ. M. and SATCHELL J. E. (1962) The extiaction of Lumbricidae from soil with special reference to the hand-sorting method. In Progress in Soil Zoology (P. W. Murphy, Ed.), pp. 294-299. Butterworths, London. SATCHELLJ. E. (1967) Lumbricidae. In Soil Biology (A. Burges and F. Raw, Eds), pp. 259-322. Academic Press, London. SAKHELL J. E. (1971) Earthworms. In Methods of Study in Quantitative Soil Ecology: Population, Production and Energy Flow (J. Phillipson, Ed.), pp. 107-127. Blackwell,
Oxford. SATCHELL J. E. (1980a) Soil and vegetation changes in experimental birch plots on a Calluna podzol. Soil Biology & Biochemistry 12, 303-310.
SATCHELLJ. E. (1980b) Potential of the Silpho Moor experimental birch plots as a habitat for Lumbricus terrestris. Soil Biology & Biochemistry 12, 317-323.