ELSEVIER BioresourceTechnology67 (1999) 149-154

blOl BOUl (t TC(fllIOLOG1'

Effects of thermally dried sewage granules on earthworms and vegetation during pot and field trials

Kevin R. Butt* Biosystems Research Group, The Open University, Milton Keynes MK7 6AA, U.K.

Received 8 April 1998; revised 12 May 1998; accepted 19 May 1998

Abstract

Trials with thermally dried sewage granules investigated their effects on a variety of earthworm species in laboratory and field situations. Initial laboratory results from small pots suggested that deleterious effects to earthworms might result from field application of granules. A field trial showed that this was not the case. After 9 months, earthworm population size and structure in permanent grassland was not affected by sewage granule applications, at rates up to twice guideline level (8 tonnes per hectare). Earthworm numbers in control plots and those with sewage applied were not significantly different (p > 0.05). A significant increase in biomass production of vegetation (p <0.001) was recorded where granules were applied. Deep burrowing species of earthworm appeared to benefit from an increased availability of plant material. © 1998 Elsevier Science Ltd. All rights reserved.

Keywords: Earthworms; Grassland; Dried sewage granules

1. Introduction

With a growing requirement to find alternative disposal routes for sewage sludge (European Community, 1991), disposal to land is once more a prime option. However, many forms of sewage can be produced (Coombes, 1993), some of which are less noxious and permit land application more easily. Narrowing of agricultural utilisation windows for sludge, caused by changes in agricultural practices and the need to limit nitrate leaching has increased the requirement to produce sludge cakes and dried sludges. Beneficial recycling of such material to agricul- tural land is usually the most economic disposal outlet for inland sewage treatment works (MAFF, 1993). Recycling of sludge to land provides farmers with the opportunity to reduce costs of inorganic fertiliser appli- cation. Only some 42% of the 1 million tonnes (dry solids) of sewage sludge produced annually in the U.K. is beneficially recycled to less than 1% of agricultural land (MAFF, 1993).

In 1991, one U.K. Water Company, Wessex Water, invested in a plant to process sewage sludge using a

*Current address: Department of Environmental Management, University of Central Lancashire, Preston PR1 2HE, U.K.

new technology. The Swiss-built, automated equipment produces a material which is dried (at temperatures exceeding 450°C), pasteurised and sieved into odour- less, even-sized (approx. 1-3 mm) granules, which results in a volume reduction to one-twentieth (Martinson, 1994). To date, the final product has been used as a fertiliser by the Forestry Commission, by British Coal (on reclamation sites) and on golf courses.

1.1. Earthworms: an overview

Around 30 species of earthworm are found in Britain (Sims and Gerard, 1985) and these can be sub-divided into three groups. These morpho-ecological groupings, described by Bouch6 (1977), relate to several factors including; general size, shape and pigmentation, burrow construction, position in the soil profile, source of food, and reproductive potential.

The three types are;

1. Epiges: these are litter dwelling, have a small body size and exhibit a high reproductive rate. For example, Eisenia fetida (brandlings), Lumbricus rubellus (red worms). These are 'muck' or 'compost' worms which live within organic material.

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150 K.R. Butt/Bioresource Technology 67 (1999) 149-154

2. Endoges: these create horizontal branching burrows in the soil, have a variable body size and are weakly pigmented. For example, Allolobophora chlorotica (green worms) Aporrectodea caliginosa (grey worms).

3. Aneciques: these are deep burrowing, have a large body size, are strongly pigmented, show surface feeding and surface casting behaviour, and exhibit a low reproductive rate in the field. For example, Aporrectodea l o n g a (black-headed worms), Lumbricus terrestris (lob worms).

From this outline it is apparent that the three groups will have different effects on the soils in which they are found. Their requirements will exclude some from certain types of soil, but all three earthworm types can co-exist and could be encountered in most mature soils.

This paper describes both laboratory-based pot trials and field trials to determine the effects of sewage granules on earthworms from all three morpho- ecological groupings. The field work also determined vegetation production, as the fertilising capability of sewage sludges is well known (Dutch and Wolsten- holme, 1994).

2.1.3. Experiment 3 (Aneciques) (a) Individual A. longa, L. terrestris and Octolasion

cyaneum (blue-grey worms), all found in British pasture land, were fed with 5.0g of sewage granules. Five replicates were set up per species with one hatchling per pot.

(b) Field-collected A. longa and L. terrestris (mean mass 0.85 g) were fed at three treatment levels of 2.5, 5.0 and 10.0 g of sewage granules. (These levels of application approximate to 0.32, 0.64 and 1.28 dry kg per m2.) The feed was then moistened. There were four replicates per treatment per species. Inspection occurred every 2weeks with sampling on a monthly basis. An equal amount of granules was added after a period of 2 months.

It was thought that a true reflection of the effects of dried granule application could be obtained only by conducting relatively large scale, field trials. It was determined that as much useful information as possible would be gathered from the trials, so effects on both fauna and flora were examined.

2.2. Field trials

2. Methods

2.1. Pot trials

A series of experiments were conducted using five species of earthworms from the three groups. In all experiments, unless stated, hatchling worms from stock sources (Butt, 1993) were provided with moistened sewage granules as feed within 0.3-1 plastic pots. For endoge and anecique worms, the biogranules were provided upon the surface of 150 g of a moistened sterilised loamy soil, whereas epiges were fed directly with granules. All pots were maintained in temperature controlled incubators at 15°C and were inspected and moistened every 2 weeks. Sampling involved counting the worms present, weighing them and assessing their general and reproductive condition.

2.2.1. Field sites Two areas, located within the Open University (OU)

campus were selected for use. These were adjacent to playing fields on permanent grassland beside the River Ouzel (National Grid Reference SP 883373) and on frequently disturbed grassland at the 'East gate field site' (National Grid Reference SP 889368). A silty- loam soil was present at the River site (pH 7.0) and a mixture of soil types, predominantly a loamy sand at the East gate site (pH 6.5). Prior to experimentation each site had been maintained by the OU ground staff and mown on a monthly basis, or as required. Mowing occurred immediately before granule application (March 1994) and then the areas were not mown for 2 months to permit vegetation biomass production.

2.Z2. Experimental design A randomised block design was used incorporating

four treatments:

2.1.1. Experiment 1 (Epiges) Approximately 20 hatchling E. fetida were provided

with 75 g of granules, moistened in a 0.3-1 pot (four replicates). These were sampled after a period of 4 weeks

2.1.2. Experiment 2 (Endoges) Hatchling A. chlorotica (four per pot) were provided

with three treatments of 2.5, 5.0 or 10.0 g of granules as feed. There werg" six replicates per treatment. All were sampled after a period of 8 weeks.

Control (no sewage granules applied); 1/2r (0.4 kg granules per m 2) x (0.8 kg granules per m 2) 2x (1.6 kg granules per m 2)

The basic rate of application (x) was determined by reference to advised rates for agricultural spreading of no more than 250 kg per ha of total nitrogen (MAFF, 1991) and from the nitrogen content of the granules (see Table 1).

Each of these treatments was replicated twice (two plots) within each of three blocks at both field sites.

K.R. Butt/Bioresource Technology 67 (1999) 149-154 151

Table 1 Analysis of sewage sludge granules (all figure mg/kg unless stated)

Dry matter Total nitrogen Total phosphorus (g/kg) (g/kg)

937 32.2 19900

Total magnesium Total potassium pH Organic carbon (%)

4500 400 6.7 21.6

(Analyses conducted by ADAS, Cambridge.)

Each experimental plot covered an area of 5 x5 = 25 m 2, and all plots were at least 2m from neighbouring plots. Blocks were separated by a distance of 5 m. At the river site a minimum distance of 10 m was maintained between the experimental area and the river bank. (A total area of 1200 m 2 was there- fore employed.)

2.2.3. Baseline survey of earthworms Three months before field application of granules

(December 1993), information relating to earthworm communities was gathered from both field sites. This was achieved by cutting turves of regular size (0.1 m z) to a depth of 0.1 m, and extracting all worms from the turf by hand-sorting and wet sieving of soil in the laboratory. Immediately after cutting, dilute (0.4%) formaldehyde was applied to the area from where turf removal had occurred in order to extract deeper burrowing species. For details of methodology, see Edwards and Bohlen (1996).

2.2.4. Vegetation assessment Two months after granule application, visual differ-

ences in the sward height of vegetation between the treatment plots was apparent. To quantify this, samples from a 0.25 x 0.25 m area (n = 5) were cut, 1 cm above ground level, from each treatment, at both field sites. Dry mass of the collected material (mainly grass species) was then determined following standard MAFF (1981) procedures.

2.2.5. Earthworm sampling Earthworm communities were sampled 9months

after sewage granule application (December 1994) to provide comparable data with the baseline information collected a year earlier. At the later date, samples from the river site, only, were taken. This was because of redevelopment at the East Gate site. Six replicate samples of the four treatments were taken (one per plot). These were collected as described in the baseline survey. The species found, numbers, biomass and age structure of populations were recorded. Other macro- fauna were also recorded if present in large numbers.

2. 2. 6. Statistical analyses Dry mass production of vegetation from the different

plots was analysed using a one-way analysis of variance

and the two sites were also compared. A similar analysis of variance of total number, total mass, and number of the dominant earthworm species present before and after granule application was also under- taken for the River Ouzel site.

3. Results and discussion

3.1. Pot trials

3.1.1. Experiment 1 All of the earthworms survived, grew and remained

healthy. This was the type of result expected for this species, as E. fetida inhabits material with a high organic content, and previous successful research (Hartenstein, 1983) has involved feeding this worm with sewage.

3.1.2. Experiment 2 After 2 months, hatching survival rates were 40, 13

and 0% in pots provided with 2.5, 5.0 and 10.0 g of sewage granules, respectively. Those A. chlorotica surviving were also of lower masses compared to growth of the same species with dried cattle manure as feed (Butt, 1997).

3.1.3. Experiment 3(a) After a period of 4 weeks, all of the hatching A.

longa, L. terrestris and O. cyaneum provided with granules as feed were dead. Other hatchlings provided with alternative organic feeds survived to this stage under similar conditions and showed relatively rapid growth (Butt, 1993).

3.1.4. Experiment 3(b) At the higher level of application (10 g/pot), half of

the field-collected A. longa and L. terrestris had perished after 2 months, and all were dead after 3 months. No mortality was recorded at the two lower levels of application, but in all cases, a decrease in earthworm mass was observed over the 3omonth period. Under the given experimental conditions growth and reproduction of these species would be

152 K.R. Butt/Bioresource Technology 67 (1999) 149-154

expected with a suitable feed source, as shown by Butt (1993).

3.2. Baseline survey of field earthworms

1. East gate site: eight species of earthworm were found. These were A. chlorotica, A. caliginosa, A. longa, Aporrectodea rosea, Dendrobaena octaedra, Lumbricus festivus, L. rubellus, and L. terrestris. The mean earthworm number was 422___72.4 per m 2, comprising a mass of 176.1±16.4g per m 2. The dominant species constituting 49% by number was the endogeic species A. caliginosa. (A. chlorotica made up only 11% of the total.)

2. River Ouzel site: six species of earthworm were found. These included five of those located at the East gate site (A. chlorotica, A. longa, A. rosea, L. rubellus, and L. terrestris) plus Octolasion cyaneum. The mean earthworm number was 288 + 28.6 per m E,

comprising a mass of 109.4_9.2g per m s. The dominant species constituting 64% by number was the endogeic species A. chlorotica. (A. caliginosa was not found during sampling.)

This showed the presence of a healthy community comprising all three morpho-ecological groups at each of the two field sites. The greater number of species at the East gate site reflected the frequently disturbed nature of the area. The community at the River site, dominated numerically by A. chlorotica and gravimet- rically by A. longa appeared more stable.

3.3. Vegetation assessment

Results of biomass production, 2months after granule application are shown for both field sites in Fig. 1. Statistically significant results were obtained (p<0.001) when comparing the dry mass production across treatments at each site. In general, a greater sewage granule application led to significantly increased plant production. At the river site, produc- tion for the same rate of application was greater than that at the East gate site for all treatments.

Increased biomass production was expected, given the constituent elements of the sewage granules, many of which are plant nutrients (see Table 1). Use of similarly treated sewage sludge as a fertiliser for containerised bedding plants led to equally good growth compared with water-soluble or controlled- release fertilisers (Cox, 1995). However, in these experiments the pelletised sewage was thought to have a low nitrogen mineralising rate, which although preventing excessive leaching, led to low plant-available nitrogen.

3. 4. Field earthworms and dried sewage granules

Six species of earthworm, representing all three morpho-ecological groupings were located 9 months after granule application. These were A. chlorotica, A. caliginosa, A. longa, A. rosea, L. rubellus, and L. terres- tris. Fully mature adults and juveniles of each species were encountered. The largest individual located (L.

0.4

+

0.6

a

0.2

b T

c

B

0 0.4 0 .8 1.6

I I ~ i . I

S e w a g e granu le app l i ca t ion ( K g / m 2 )

Fig. 1. Vegetation productiion at two field sites 2 months after sewage granule application (I , East Gate site; o, River Ouzel site). (Similar letters above bars for a given site denote that a significant difference was not present (p > 0.05)).

K.R. Butt/Bioresource Technology 67 (1999) 149-154 153

terrestris) had a mass of 3.43 g. Tuff cutting and formal- dehyde extraction accounted respectively, for 89.8 and 10.2% of all earthworms located (total n = 492).

Deep burrowing, anecique species accounted for approximately one-third of the earthworms found and the remainder were almost all endogeic species. A. chlorotica formed 95% of the latter. Only 3% of the total were epigeic and were represented solely by the species L. rubellus.

Numbers of earthworms across all treatments were lower than those recorded in the baseline survey. This, however, was not unexpected as fluctuations in popula- tion size are influenced by numerous environmental factors (Sims and Gerard, 1985). O. cyaneum, a relatively uncommon species was not located in any treatment plot following granule application.

The numbers and masses of each species represented across the four treatments are shown in Tables 2 and 3,

Table 2 Earthworm numbers (m 2) from a grassland site beside the River Ouzel 9 months after sewage granule treatments were applied in December 1994 (to nearest whole number)

Species Treatment

Control 1/2x x 2x Mean of all treatments

A. chlorotica 118 102 138 122 120 A. caliginosa 2 3 0 3 2 A. longa 35 32 45 47 40 A. rosea 0 8 5 2 4 L. rubellus 7 2 8 8 6 L. terrestris 13 10 2 13 10 L. spp. 27 28 20 25 25

Totals 202 185 218 220 207

L. spp. = juvenile Lumbricus too small to determine species. x = 0.8 kg/m 2 application of dried sewage granules.

Table 3 Earthworm masses (g/m 2) from a grassland site beside the River Ouzel 9 months after sewage granule treatments were applied

Species Treatment

Control 1/2x x 2x Mean of all treatments

A. chlorotica 31.0 24.2 37.5 25.3 29.5 A. caliginosa 0.5 2.4 0.0 0.8 0.9 A. longa 51.0 50.8 61.8 72.6 59.1 A. rosea 0.0 1,5 0.5 0.4 0.6 L. rubeUus 1.3 0,5 1.8 1.5 1.3 L. terrestris 9.5 24,9 0.6 33.2 17.1 L. spp. 2.7 9,7 4.7 5.8 5.7

Totals 96.0 114.0 1 0 6 . 9 1 3 9 . 6 114.2

L. spp. = juvenile Lumbricus too small to determine species. x = 0.8 kg/m 2 application of dried sewage granules.

respectively. The mean number of earthworms ranged between 185 and 220 per m 2 and did not differ signifi- cantly across the treatments (t9 > 0.05). Similarly, no significant difference between the numbers of the most abundant species (A. chlorotica) was found. Only numbers of A. longa increased markedly at higher levels of application, accompanied by an increase in total mass of the same species. This type of increase has- previously been reported for L. terrestris in Canadian soils by Tomlin et al. (1993), in communities dominated by this species and subjected to sewage applications of 200 kg per hectare per year. Other authors have reported that endogeic species (particu- larly A. chlorotica) show the most positive responses to applications of organic materials (Cotton and Curry, 1980) and sewage sludge in particular (Cuendet and Ducommun, 1990). It is proposed that at the River Ouzel site this species of earthworm, which was already dominant, was present at a level approaching the carrying capacity for this system.

It is thought that the increases brought about in A. longa (and L. terrestris) populations were almost certainly a direct result of increased dead vegetation on the soil surface (following mowing). These species, which feed by pulling dead material into the soil, could have increased through a number of possible means: increased reproduction, immigration or a combination of both. In a field trial in Australia, Yeates (1995) found that earthworm populations were greatly increased by the application of sewage sludge. However, the interpretation from this study was that increased soil moisture content from the spay-irrigated sludge was the prime causal agent and the species of earthworm concerned were not identified.

No increase in the number of epigeic earthworm species occurred at any level of sewage granule applica- tion in the current work. This suggests that at the rates used within the given treatments, little material was available for use by such species which thrive in condi- tions of excess organic material. Other organisms may be able to make more rapid use of this resource. For example, one other group of the macro-fauna was also found during sampling. Large masses of Dipteran (True fly) larvae (maggots) were located within some of the turves which had received the higher level (1.6 kg per m 2) of granule application.

Results obtained from the field trial are in contrast to those obtained from the simple, small-scale labora- tory experiments. The laboratory-based studies had negative effects on all soil dwelling earthworms and only favoured litter-dwelling species. These adverse effects were almost certainly caused by the non-natural conditions associated with the pot trials. For example, the enclosed nature of pot experiments and the raised temperature may have led to a build up of ammonia, to which earthworms are particularly sensitive (Edwards,

154 K.R. Butt/Bioresource Technology 67 (1999) 149-154

1988). Also a build up of soluble salts may have caused problems, as demonstrated for containerised plants by Cox (1995). The absence of other organisms in the sterilised soil and absence of plants may have been important factors. Although pot trials were a sensible forerunner of more resource-using field work, the apparent success of earthworm populations under field conditions means that decisions made on the use of certain organic wastes (resources) should not neces- sarily be made until a range of realistic large-scale experimental work has been undertaken.

From this relatively simple field trial, it is suggested that, within the limits of the treatments used, applica- tion of thermally dried sewage granules should have a positive impact on earthworm communities. Increases in size and number of larger, anecique species could be enhanced by the use of sewage granules as a fertiliser treatment. Further investigations on different soil types over a longer period of time would prove useful in terms of monitoring community changes in earthworms and other soil organisms.

Acknowledgements

The field trial for this research was funded by Wessex Water. Joanne Davenport assisted with field sampling.

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