- Email: [email protected]
Influence of sewage waste on the abundance of earthworms in pastures in south-eastern Australia
European Journal of Soil Biology 38 (2002) 233−237 www.elsevier.com/locate/ejsobi
Influence of sewage waste on the abundance of earthworms in pastures in south-eastern Australia Geoff Baker a,*, David Michalk b, Wendy Whitby a, Sue O’Grady b a
CSIRO Entomology, P.O. Box 1700, Canberra, A.C.T. 2601, Australia b NSW Agriculture, Forest Rd, Orange, NSW 2800, Australia Received 18 August 2000; accepted 4 May 2001
Abstract The use of biosolids in pasture-based livestock production is being considered for disposal of human sewage waste in New South Wales (NSW), Australia. An experiment was commenced in 1992 near Goulburn to assess some of the risks associated with the application of dewatered biosolids (DWB) to pastures. DWB was applied to infertile, acidic soils at the rates of 30, 60 and 120 tonnes ha–1 and compared to a fertilised and limed control. In 1999, earthworm abundance was low in control plots (7.5 worms m–2). Application of DWB increased abundance, peaking at 60.0 worms m–2 in the 30 tonnes ha–1 treatment, with no significant difference between the three rates of DWB. The earthworm fauna consisted of exotic Lumbricidae and Acanthodrilidae (most commonly Aporrectodea trapezoides (Duges) and Microscolex dubius (Fletcher)) and native Megascolecidae (most commonly Spenceriella macleayi (Fletcher)). Species composition varied with rate of DWB. Two lumbricids (A. longa (Ude) and A. caliginosa (Sav.)), which were not previously present at the site, were inoculated together in replicated cages in each of the DWB treatments. Three months later, more A. longa were recovered than A. caliginosa (90% cf. 69%), but there was no influence of DWB on the survival of either species. The total biomass of recovered worms also did not vary in relation to DWB. The inoculation of A. longa and A. caliginosa increased pasture production in all the fields (overall increase = 46%). The inoculation of A. longa and A. caliginosa also decreased the abundance and biomass of local earthworms. © 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Earthworms; Sewage waste; Pastures; Australia; Aporrectodea spp.
1. Introduction Disposal of human sewage sludge by environmentally acceptable means poses a very great challenge world-wide. However, safe and profitable disposal of such sludge, as biosolids, has been achieved in Europe and North America through its addition to pastures [1,11,15]. The disposal of biosolids in this way is now being considered in New South Wales (NSW), Australia [10]. A grazing experiment was commenced in 1992 near Goulburn to assess the benefits and risks associated with the application of dewatered biosolids (DWB) to pastures grazed by sheep [12,13]. Part
* Corresponding author. Fax: +61-02-6246-4000. E-mail address: [email protected] (G. Baker).
of the assessment of the impact of the DWB at Goulburn was to measure the abundance and diversity of the resident earthworm fauna 7 years after application. This work is presented here. In addition, the abilities of two exotic species, the endogeic Aporrectodea caliginosa (Sav.) and the anecic A. longa (Ude) (Lumbricidae), to survive and influence pasture production when introduced to the Goulburn site, were investigated. Both A. caliginosa and A. longa are known to contribute significantly to soil structure, fertility and plant production elsewhere in Australian pastures [2–6]. There have been only a few previous studies on the influence of human sewage on earthworm communities in the field, although species such as Eisenia fetida (Sav.) have been commonly used for the breakdown of sewage in vermicomposting industries [9]. Curry [8] noted that field
© 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. PII: S 1 1 6 4 - 5 5 6 3 ( 0 2 ) 0 1 1 5 1 - 2
234
G. Baker et al. / Eur. J. Soil Biol. 38 (2002) 233–237
communities of earthworms, because of the large quantities of soil and plant litter they ingest, might be at risk from the effects of the high levels of heavy metals (e.g. Cu, Zn, Ni, Cd) commonly found in sewage sludge. Morgan and Morgan [14] reported that heavy metals are accumulated to varying degrees by earthworms with different burrowing behaviours (e.g., epigeic, endogeic and anecic). Butt [7] found that sewage reduced the survival of several species of earthworms in laboratory cultures but he dismissed this result as an artifact of the enclosed nature of his cultures and a build up of ammonia or soluble salts within them. In the field, the abundance and biomass of the anecic A. longa increased with sewage application, but no changes were detected for epigeic and endogeic species [7]. The increases in the abundance and biomass of A. longa were attributed to an increased availability of dead plant matter, resulting from the sewage application. A similar increase in the abundance of another anecic species (Lumbricus terrestris Linn.) was also reported by Tomlin et al. [17].
2. Materials and methods The site, “Kentgrove South”, is located near Goulburn in the southern tablelands of NSW and covers a series of three hill formations with altitudes ranging from 650 to 680 m. Three soil types, roughly corresponding with the three hills, occur at the site: Hill A, Alfisol—sub-order Aeric Kandiaqualf; Hill B, Alfisol—sub-order Typic Natraqualf; Hill C, Inceptisol—sub-order Oxic Ustropept [16]. These soils are representative of 80% of the area targeted for land application of DWB in NSW. Average rainfall for the site is 669 mm year–1, with no marked seasonal pattern. Air temperatures vary from 28.2/13.4 (max./min.) in summer to 11.2/1.3 in winter. When the trial was set up in 1992, the site was an unimproved pasture dominated by native red grass (Bothriochloa macra). Four treatments were duplicated on each hill. The control consisted of an initial incorporation of 2.5 tonnes lime ha–1 followed by 400 kg ha–1 of 50:50 lime/superphosphate. A maintenance superphosphate input of 250 kg ha–1 was applied every year thereafter. For the other treatments, dried anaerobically digested DWB (28% solid) was applied at the rates of 30, 60 or 120 tonnes ha–1 as a once only application and incorporated (top 10 cm) within 24 h of application. The sizes of the plots varied, but were approximately 1.4 ha. In autumn 1993, all plots were sown with a pasture mixture comprised mostly of subterranean and white clover (Trifolium subterraneum and T. repens), cocksfoot (Dactylis glomerata), phalaris (Phalaris aquatica), perennial ryegrass (Lolium perenne), and ryecorn (Secale cereale). Merino ewes commenced grazing at 5 ewes plot–1 in late 1993, stocking rate was increased to 10 plot–1 in 1994, and a differential stocking rate (up to 10 ewes plot–1 for the 120 tonnes DWB ha–1 treatment) was adopted from late
1995 onwards to cater for plot differences in pasture production. Further site details are available in Joshua et al. [10] and Michalk et al. [13]. In October (spring) 1999, 10 soil samples (each 0.1 m2 in area × 10 cm deep) were taken along a transect in the middle of all plots on Hill A and within one 30 tonnes DWB ha–1 plot on each of Hills B and C. Samples were taken 10 m apart and hand-sorted for earthworms, which were preserved in 70% ethanol and later identified and weighed. Twenty PVC cages [3] were constructed in each of six of the plots surveyed for earthworms. Cages were set in one replicate of each treatment on Hill A and one 30 tonnes DWB ha–1 treatment on each of Hills B and C. The cages consisted of 20 cm lengths of 30 cm diameter PVC pipe, driven 15 cm into the soil. The undisturbed soil within the pipe sections was enclosed with curtain mesh strapped taut across the bottom edge and draped over 30 cm high metal frames (to allow pasture growth) and again strapped to the top edge. Cages were constructed in early July 1999. Fifteen A. longa and 15 A. caliginosa, both collected from a pasture in north-western Tasmania, were added to each of 10 cages, chosen at random, within each plot during early August. The other 10 cages in each plot received no worms. The fresh mass of the A. longa and A. caliginosa used in the experiment was 2.03 g and 0.49 g, respectively (after being kept for 24 h on moist tissue paper to void gut contents). There were no significant differences between the plots in the mass of the worms used (F = 0.03, P > 0.05 for A. longa and F = 1.39, P > 0.05 for A. caliginosa, for treatments on Hill A; and F = 0.83, P > 0.05 for A. longa and F = 0.42, P > 0.05 for A. caliginosa, across the three hills). In late October, after the herbage had been cut to within approximately 3cm above the soil surface within each cage, the soil cores were hand-sorted for worms. These worms were then identified and weighed fresh (again after 24 h on moist tissue paper). Herbage was oven-dried at 60 °C and weighed. Remnant DWB was frequently observed in the hand-sorted soil within the cages, especially within the fields with higher application rates.
3. Results 3.1. Earthworm survey Earthworm numbers (all species combined) were much lower in the control plots on Hill A than in the other plots (Fig. 1; F = 4.46, P < 0.01 for the four Hill A treatments). There were no differences between replicate plots (F = 0.98, P > 0.05). No other differences in total numbers were apparent between the four treatments or the three hills. Differences in earthworm biomass between treatments mirrored those for numbers (F = 3.92, P < 0.05 for Hill A treatments). Six earthworm species were found at the site; three exotic species, A. trapezoides (Duges) (Lumbricidae), and Microscolex dubius (Fletcher) and M. phosphoreus
G. Baker et al. / Eur. J. Soil Biol. 38 (2002) 233–237
235
Fig. 1. Abundance of local worms in fields with different amounts of DWB incorporated into the soils on three hills at Goulburn. Vertical bars indicate SE. Data for replicate fields on Hill A have been pooled.
3.2. Cage experiment
The average final mass worm–1 was lower for A. caliginosa in the 60 tonnes DWB ha–1 treatment on Hill A (81.9% of the starting mass) compared with the average mass under other rates of DWB (F = 5.63, P < 0.005). No differences were found for the average final mass worm–1 for A. longa across DWB rates (F = 0.48, P > 0.05), nor for either species across the soil types (F = 1.14, P > 0.05 and F = 2.95, P > 0.05 for A. caliginosa and A. longa, respectively). Overall, the average final mass worm–1 was 0.44 and 1.99 g for A. caliginosa and A. longa, respectively (i.e. 89.8 and 98.0% of the initial starting mass).
There was no influence of DWB application or soil type on the survival of A. caliginosa or A. longa (F = 0.25, P > 0.05 for A. caliginosa and F = 1.81, P > 0.05 for A. longa, for treatments on Hill A; F = 2.33, P > 0.05 for A. caliginosa and F = 1.94, P > 0.05 for A. longa, across the three hills). More A. longa were recovered than A. caliginosa (overall 89.7 and 68.8%, respectively) (F = 35.14, P < 0.001 for treatments on Hill A; F = 38.47, P < 0.001 across the three hills). Similarly, there was no influence of DWB application on the final biomass of A. caliginosa or A. longa, nor of soil type for A. caliginosa (F = 0.37, P > 0.05 for A. caliginosa and F = 1.21, P> 0.05 for A. longa, for treatments on Hill A, and F = 0.73, P > 0.05 for A. caliginosa across the three hills). The final biomass of A. longa did vary between the hills with less biomass being recovered per cage from Hill C compared with Hill A (F = 4.23, P < 0.05). Hill B was intermediate.
Local earthworm species (A. trapezoides, M. dubius, M. phosphoreus, S. macleayi, Spenceriella sp. and Heteroporodrilus sp.) were also found in the cages when they were dismantled during October. Their abundance on Hill A (total for all the six species combined) increased with the rate of DWB (F = 9.18, P < 0.05) and was reduced in the presence of A. caliginosa and A. longa (F = 6.66, P < 0.05). On the other hand, no effect of A. caliginosa and A. longa on the abundance of local worms within the cages was detected across the three hills using the 30 tonnes DWB ha–1 treatments (F = 0.02, P > 0.05), nor did local worm numbers vary between hills per se (F = 0.76, P > 0.05). The biomass of local worms in cages also increased with rate of DWB on Hill A (F = 2.86, P < 0.05) and was reduced in the presence of A. caliginosa and A. longa (F = 11.68, P < 0.005). Biomass of local worms in cages did not vary between hills (F = 0.52, P > 0.05) nor was any effect of
(Duges) (Acanthodrilidae), and three native species, Spenceriella macleayi (Fletcher), Spenceriella sp., and Heteroporodrilus sp. (Megascolecidae). Species composition varied between treatments, with S. macleayi most common in the control, and 30 and 60 tonnes DWB ha–1 treatments (51.2–87.5% of collections), but M. dubius predominant under 120 tonnes DWB ha–1 (74.1% of collection). A. trapezoides was most common in the 30 tonnes DWB ha–1 treatment on Hill A (30.9% of collection).
236
G. Baker et al. / Eur. J. Soil Biol. 38 (2002) 233–237
Fig. 2. Dry weight of herbage harvested from cages with and without inoculated earthworms (Aporrectodea longa and A. caliginosa). Cages were set in fields with different amounts of DWB incorporated into the soils on three hills at Goulburn. Vertical bars indicate SE.
4. Discussion
abundance of other endogeic and epigeic species in response to sewage application in the UK. The pretreatment of the soil on Hill A at Goulburn with DWB had no influence on the survival of either A. longa or A. caliginosa when they were introduced. Whether or not these two species would have survived as well if introduced earlier (< 7 years after the DWB application) is of course unknown. Greater recovery of A. longa compared with A. caliginosa has been observed generally across several introductions [4] irrespective of DWB application and is yet to be understood. Both species were collected from the same site in Tasmania for this study. Some of the interspecific difference in recovery may simply be explained by variable collection efficiency. A. longa is a bigger worm than A. caliginosa.
The effect of DWB on local earthworm abundance and biomass was positive at Goulburn, at least on Hill A where relevant comparisons were made. The soil on Hill A was low in fertility at the start of the trial [13]. The addition of organic matter, either directly through the application of the DWB per se or indirectly through induced increases in pasture production [12], probably encouraged higher earthworm numbers. The burrowing behaviour of S. macleayi is poorly understood, but A. trapezoides and M. dubius, the other two most common species at Goulburn, are endogeic and epigeic, respectively. The positive responses of A. trapezoides and M. dubius to either small or large applications of DWB are in contrast to Butt’s [7] report of no changes in
The observed increases in pasture production (overall 46%), induced by the introduction of A. longa and A. caliginosa, were comparable with those reported elsewhere in south-eastern Australia [5] and serve to further highlight the potential advantages to be gained through improved management of such species as resources. However, the results reported here also demonstrate that the introduction of these exotic species may lead to a reduction in local earthworm fauna and should be undertaken with caution. Other research (G. Baker et al., Eur. J. Soil Biol. 38 (2002) 39–42) has also noted that the introduction of A. longa to Australian pastures can reduce the abundance of local fauna. Nonetheless, it seems that this impact is likely to be small and overshadowed by the benefits to be gained through in-
A. caliginosa and A. longa inoculation detected across the three hills (F = 1.13, P > 0.05). On Hill A, herbage yield varied with rate of DWB (F = 6.88, P < 0.001) and with and without added worms (Fig. 2; F = 12.78, P < 0.001). Herbage yield was greatest in the control and 120 tonnes DWB ha–1 treatments, and where A. caliginosa and A. longa were added. Herbage yield also varied between hills (F = 5.73, P < 0.01), with yields higher on Hill A than on Hills B and C (Fig. 2), and again between treatments with and without worms (F = 8.92, P < 0.005). Overall, the inoculation of A. caliginosa and A. longa increased herbage yield by 46.0%.
G. Baker et al. / Eur. J. Soil Biol. 38 (2002) 233–237
creased functional biodiversity and improved soil properties and plant yield. Michalk et al. [12] reported that pasture production increased with DWB application on Hill A at Goulburn. A similar pattern was not found in this study, with high plant yields in the control as well as in the 120 tonnes DWB ha–1 treatment site. This inconsistency between the studies may simply reflect the sites selected for the worm study and the very small area occupied by the earthworm cages compared with the more general surveys conducted by Michalk et al. [12] across the plots.
Acknowledgements We wish to thank Sydney Water and LWRRDC for financial support and Jacqueline Piercy, Jill Clapperton and Dale Chalker for their assistance with the work.
[6]
[7]
[8]
[9]
[10]
[11] [12]
References [1]
[2]
[3]
[4]
[5]
R. Aquilar, S.R. Loftin, P.R. Fresquez, Rangeland restoration with treated municipal sewage sludge, in: C.E. Clapp, W.E. Larson, R.H. Dowdy (Eds.), Sewage Sludge: Land Utilization and the Environment, SSSA Miscellaneous Publication, 1994, pp. 211–220. G.H. Baker, The ecology, management, and benefits of earthworms in agricultural soils, with particular reference to southern Australia, in: C.A. Edwards (Ed.), Earthworm Ecology, St Lucie Press, Boca Raton, 1998, pp. 229–257. G.H. Baker, V.J. Barrett, P.J. Carter, J.P. Woods, Method for caging earthworms for use in field experiments, Soil Biol. Biochem. 28 (1996) 331–339. G.H. Baker, P.J. Carter, V.J. Barrett, Survival and biomass of exotic earthworms, Aporrectodea spp. (Lumbricidae), when introduced to pastures in south-eastern Australia, Aust. J. Agr. Res. 50 (1999) 1233–1245. G.H. Baker, P.J. Carter, V.J. Barrett, Influence of earthworms, Aporrectodea spp. (Lumbricidae), on pasture production in south-eastern Australia, Aust. J. Agr. Res. 50 (1999) 1247–1257.
[13]
[14]
[15] [16] [17]
237
G.H. Baker, P.J. Carter, V.J. Barrett, Influence of earthworms, Aporrectodea spp. (Lumbricidae), on lime burial in pasture soils in south-eastern Australia, Aust. J. Soil Res. 37 (1999) 831–845. K.R. Butt, Effects of thermally dried sewage granules on earthworms and vegetation during pot and field trials, Biores. Techn. 67 (1999) 149–154. J.P. Curry, The invertebrate fauna of grassland and its influence on productivity. II. Factors affecting the abundance and composition of the fauna, Grass Forage Sci. 42 (1987) 197–212. C.A. Edwards, The use of earthworms in the breakdown and management of organic wastes, in: C.A. Edwards (Ed.), Earthworm Ecology, St Lucie Press, Boca Raton, 1998, pp. 327–354. W.D. Joshua, D.L. Michalk, I.H. Curtis, M. Salt, G.J. Osborne, The potential for contamination of soil and surface waters from sewage sludge (biosolids) in a sheep grazing study, Australia, Geoderma 84 (1998) 135–156. MAFF, Review of the rules for sewage sludge application to agricultural land, MAFF Publications, London, 1993. D.L. Michalk, I.H. Curtis, C.M. Langford, P.C. Simpson, J.T. Seaman, Effects of sewage sludge on pasture production and sheep performance, in: M. Asghar (Ed.), Proc. 8th Aust. Agronom. Conf., Toowoomba, Qld, 1996, pp. 429–432. D.L. Michalk, I.H. Curtis, J.T. Seaman, C.M. Langford, P.C. Simpson, G.J. Osborne, Benefits and risks associated with the application of biosolids to pastures grazed by sheep, in: G.J. Osborne, R.L. Parkin, D.L. Michalk, A.M. Grieve (Eds.), Biosolids Research in NSW, NSW Agriculture, Orange, NSW, 1996, pp. 62–84. J.E. Morgan, A.J. Morgan, Heavy metal concentrations in the tissues, ingesta and faeces of ecophysiologically different earthworm species, Soil Biol. Biochem. 24 (1992) 1691–1697. S.R. Smith, Agricultural Recycling of Sewage Sludge and the Environment, CAB International, Wallingford, 1996. Soil Survey Staff, Keys to Soil Taxonomy, 8th ed., USDA, Washington, DC, 1998. A.D. Tomlin, R. Protz, R.R. Martin, D.C. McCabe, R.J. Lagace, Relationships amongst organic matter content, heavy metal concentrations, earthworm activity, and soil microfabric on a sewage sludge disposal site, Geoderma. 57 (1993) 89–103.
Influence of sewage waste on the abundance of earthworms in pastures in south-eastern Australia Geoff Baker a,*, David Michalk b, Wendy Whitby a, Sue O’Grady b a
CSIRO Entomology, P.O. Box 1700, Canberra, A.C.T. 2601, Australia b NSW Agriculture, Forest Rd, Orange, NSW 2800, Australia Received 18 August 2000; accepted 4 May 2001
Abstract The use of biosolids in pasture-based livestock production is being considered for disposal of human sewage waste in New South Wales (NSW), Australia. An experiment was commenced in 1992 near Goulburn to assess some of the risks associated with the application of dewatered biosolids (DWB) to pastures. DWB was applied to infertile, acidic soils at the rates of 30, 60 and 120 tonnes ha–1 and compared to a fertilised and limed control. In 1999, earthworm abundance was low in control plots (7.5 worms m–2). Application of DWB increased abundance, peaking at 60.0 worms m–2 in the 30 tonnes ha–1 treatment, with no significant difference between the three rates of DWB. The earthworm fauna consisted of exotic Lumbricidae and Acanthodrilidae (most commonly Aporrectodea trapezoides (Duges) and Microscolex dubius (Fletcher)) and native Megascolecidae (most commonly Spenceriella macleayi (Fletcher)). Species composition varied with rate of DWB. Two lumbricids (A. longa (Ude) and A. caliginosa (Sav.)), which were not previously present at the site, were inoculated together in replicated cages in each of the DWB treatments. Three months later, more A. longa were recovered than A. caliginosa (90% cf. 69%), but there was no influence of DWB on the survival of either species. The total biomass of recovered worms also did not vary in relation to DWB. The inoculation of A. longa and A. caliginosa increased pasture production in all the fields (overall increase = 46%). The inoculation of A. longa and A. caliginosa also decreased the abundance and biomass of local earthworms. © 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Earthworms; Sewage waste; Pastures; Australia; Aporrectodea spp.
1. Introduction Disposal of human sewage sludge by environmentally acceptable means poses a very great challenge world-wide. However, safe and profitable disposal of such sludge, as biosolids, has been achieved in Europe and North America through its addition to pastures [1,11,15]. The disposal of biosolids in this way is now being considered in New South Wales (NSW), Australia [10]. A grazing experiment was commenced in 1992 near Goulburn to assess the benefits and risks associated with the application of dewatered biosolids (DWB) to pastures grazed by sheep [12,13]. Part
* Corresponding author. Fax: +61-02-6246-4000. E-mail address: [email protected] (G. Baker).
of the assessment of the impact of the DWB at Goulburn was to measure the abundance and diversity of the resident earthworm fauna 7 years after application. This work is presented here. In addition, the abilities of two exotic species, the endogeic Aporrectodea caliginosa (Sav.) and the anecic A. longa (Ude) (Lumbricidae), to survive and influence pasture production when introduced to the Goulburn site, were investigated. Both A. caliginosa and A. longa are known to contribute significantly to soil structure, fertility and plant production elsewhere in Australian pastures [2–6]. There have been only a few previous studies on the influence of human sewage on earthworm communities in the field, although species such as Eisenia fetida (Sav.) have been commonly used for the breakdown of sewage in vermicomposting industries [9]. Curry [8] noted that field
© 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. PII: S 1 1 6 4 - 5 5 6 3 ( 0 2 ) 0 1 1 5 1 - 2
234
G. Baker et al. / Eur. J. Soil Biol. 38 (2002) 233–237
communities of earthworms, because of the large quantities of soil and plant litter they ingest, might be at risk from the effects of the high levels of heavy metals (e.g. Cu, Zn, Ni, Cd) commonly found in sewage sludge. Morgan and Morgan [14] reported that heavy metals are accumulated to varying degrees by earthworms with different burrowing behaviours (e.g., epigeic, endogeic and anecic). Butt [7] found that sewage reduced the survival of several species of earthworms in laboratory cultures but he dismissed this result as an artifact of the enclosed nature of his cultures and a build up of ammonia or soluble salts within them. In the field, the abundance and biomass of the anecic A. longa increased with sewage application, but no changes were detected for epigeic and endogeic species [7]. The increases in the abundance and biomass of A. longa were attributed to an increased availability of dead plant matter, resulting from the sewage application. A similar increase in the abundance of another anecic species (Lumbricus terrestris Linn.) was also reported by Tomlin et al. [17].
2. Materials and methods The site, “Kentgrove South”, is located near Goulburn in the southern tablelands of NSW and covers a series of three hill formations with altitudes ranging from 650 to 680 m. Three soil types, roughly corresponding with the three hills, occur at the site: Hill A, Alfisol—sub-order Aeric Kandiaqualf; Hill B, Alfisol—sub-order Typic Natraqualf; Hill C, Inceptisol—sub-order Oxic Ustropept [16]. These soils are representative of 80% of the area targeted for land application of DWB in NSW. Average rainfall for the site is 669 mm year–1, with no marked seasonal pattern. Air temperatures vary from 28.2/13.4 (max./min.) in summer to 11.2/1.3 in winter. When the trial was set up in 1992, the site was an unimproved pasture dominated by native red grass (Bothriochloa macra). Four treatments were duplicated on each hill. The control consisted of an initial incorporation of 2.5 tonnes lime ha–1 followed by 400 kg ha–1 of 50:50 lime/superphosphate. A maintenance superphosphate input of 250 kg ha–1 was applied every year thereafter. For the other treatments, dried anaerobically digested DWB (28% solid) was applied at the rates of 30, 60 or 120 tonnes ha–1 as a once only application and incorporated (top 10 cm) within 24 h of application. The sizes of the plots varied, but were approximately 1.4 ha. In autumn 1993, all plots were sown with a pasture mixture comprised mostly of subterranean and white clover (Trifolium subterraneum and T. repens), cocksfoot (Dactylis glomerata), phalaris (Phalaris aquatica), perennial ryegrass (Lolium perenne), and ryecorn (Secale cereale). Merino ewes commenced grazing at 5 ewes plot–1 in late 1993, stocking rate was increased to 10 plot–1 in 1994, and a differential stocking rate (up to 10 ewes plot–1 for the 120 tonnes DWB ha–1 treatment) was adopted from late
1995 onwards to cater for plot differences in pasture production. Further site details are available in Joshua et al. [10] and Michalk et al. [13]. In October (spring) 1999, 10 soil samples (each 0.1 m2 in area × 10 cm deep) were taken along a transect in the middle of all plots on Hill A and within one 30 tonnes DWB ha–1 plot on each of Hills B and C. Samples were taken 10 m apart and hand-sorted for earthworms, which were preserved in 70% ethanol and later identified and weighed. Twenty PVC cages [3] were constructed in each of six of the plots surveyed for earthworms. Cages were set in one replicate of each treatment on Hill A and one 30 tonnes DWB ha–1 treatment on each of Hills B and C. The cages consisted of 20 cm lengths of 30 cm diameter PVC pipe, driven 15 cm into the soil. The undisturbed soil within the pipe sections was enclosed with curtain mesh strapped taut across the bottom edge and draped over 30 cm high metal frames (to allow pasture growth) and again strapped to the top edge. Cages were constructed in early July 1999. Fifteen A. longa and 15 A. caliginosa, both collected from a pasture in north-western Tasmania, were added to each of 10 cages, chosen at random, within each plot during early August. The other 10 cages in each plot received no worms. The fresh mass of the A. longa and A. caliginosa used in the experiment was 2.03 g and 0.49 g, respectively (after being kept for 24 h on moist tissue paper to void gut contents). There were no significant differences between the plots in the mass of the worms used (F = 0.03, P > 0.05 for A. longa and F = 1.39, P > 0.05 for A. caliginosa, for treatments on Hill A; and F = 0.83, P > 0.05 for A. longa and F = 0.42, P > 0.05 for A. caliginosa, across the three hills). In late October, after the herbage had been cut to within approximately 3cm above the soil surface within each cage, the soil cores were hand-sorted for worms. These worms were then identified and weighed fresh (again after 24 h on moist tissue paper). Herbage was oven-dried at 60 °C and weighed. Remnant DWB was frequently observed in the hand-sorted soil within the cages, especially within the fields with higher application rates.
3. Results 3.1. Earthworm survey Earthworm numbers (all species combined) were much lower in the control plots on Hill A than in the other plots (Fig. 1; F = 4.46, P < 0.01 for the four Hill A treatments). There were no differences between replicate plots (F = 0.98, P > 0.05). No other differences in total numbers were apparent between the four treatments or the three hills. Differences in earthworm biomass between treatments mirrored those for numbers (F = 3.92, P < 0.05 for Hill A treatments). Six earthworm species were found at the site; three exotic species, A. trapezoides (Duges) (Lumbricidae), and Microscolex dubius (Fletcher) and M. phosphoreus
G. Baker et al. / Eur. J. Soil Biol. 38 (2002) 233–237
235
Fig. 1. Abundance of local worms in fields with different amounts of DWB incorporated into the soils on three hills at Goulburn. Vertical bars indicate SE. Data for replicate fields on Hill A have been pooled.
3.2. Cage experiment
The average final mass worm–1 was lower for A. caliginosa in the 60 tonnes DWB ha–1 treatment on Hill A (81.9% of the starting mass) compared with the average mass under other rates of DWB (F = 5.63, P < 0.005). No differences were found for the average final mass worm–1 for A. longa across DWB rates (F = 0.48, P > 0.05), nor for either species across the soil types (F = 1.14, P > 0.05 and F = 2.95, P > 0.05 for A. caliginosa and A. longa, respectively). Overall, the average final mass worm–1 was 0.44 and 1.99 g for A. caliginosa and A. longa, respectively (i.e. 89.8 and 98.0% of the initial starting mass).
There was no influence of DWB application or soil type on the survival of A. caliginosa or A. longa (F = 0.25, P > 0.05 for A. caliginosa and F = 1.81, P > 0.05 for A. longa, for treatments on Hill A; F = 2.33, P > 0.05 for A. caliginosa and F = 1.94, P > 0.05 for A. longa, across the three hills). More A. longa were recovered than A. caliginosa (overall 89.7 and 68.8%, respectively) (F = 35.14, P < 0.001 for treatments on Hill A; F = 38.47, P < 0.001 across the three hills). Similarly, there was no influence of DWB application on the final biomass of A. caliginosa or A. longa, nor of soil type for A. caliginosa (F = 0.37, P > 0.05 for A. caliginosa and F = 1.21, P> 0.05 for A. longa, for treatments on Hill A, and F = 0.73, P > 0.05 for A. caliginosa across the three hills). The final biomass of A. longa did vary between the hills with less biomass being recovered per cage from Hill C compared with Hill A (F = 4.23, P < 0.05). Hill B was intermediate.
Local earthworm species (A. trapezoides, M. dubius, M. phosphoreus, S. macleayi, Spenceriella sp. and Heteroporodrilus sp.) were also found in the cages when they were dismantled during October. Their abundance on Hill A (total for all the six species combined) increased with the rate of DWB (F = 9.18, P < 0.05) and was reduced in the presence of A. caliginosa and A. longa (F = 6.66, P < 0.05). On the other hand, no effect of A. caliginosa and A. longa on the abundance of local worms within the cages was detected across the three hills using the 30 tonnes DWB ha–1 treatments (F = 0.02, P > 0.05), nor did local worm numbers vary between hills per se (F = 0.76, P > 0.05). The biomass of local worms in cages also increased with rate of DWB on Hill A (F = 2.86, P < 0.05) and was reduced in the presence of A. caliginosa and A. longa (F = 11.68, P < 0.005). Biomass of local worms in cages did not vary between hills (F = 0.52, P > 0.05) nor was any effect of
(Duges) (Acanthodrilidae), and three native species, Spenceriella macleayi (Fletcher), Spenceriella sp., and Heteroporodrilus sp. (Megascolecidae). Species composition varied between treatments, with S. macleayi most common in the control, and 30 and 60 tonnes DWB ha–1 treatments (51.2–87.5% of collections), but M. dubius predominant under 120 tonnes DWB ha–1 (74.1% of collection). A. trapezoides was most common in the 30 tonnes DWB ha–1 treatment on Hill A (30.9% of collection).
236
G. Baker et al. / Eur. J. Soil Biol. 38 (2002) 233–237
Fig. 2. Dry weight of herbage harvested from cages with and without inoculated earthworms (Aporrectodea longa and A. caliginosa). Cages were set in fields with different amounts of DWB incorporated into the soils on three hills at Goulburn. Vertical bars indicate SE.
4. Discussion
abundance of other endogeic and epigeic species in response to sewage application in the UK. The pretreatment of the soil on Hill A at Goulburn with DWB had no influence on the survival of either A. longa or A. caliginosa when they were introduced. Whether or not these two species would have survived as well if introduced earlier (< 7 years after the DWB application) is of course unknown. Greater recovery of A. longa compared with A. caliginosa has been observed generally across several introductions [4] irrespective of DWB application and is yet to be understood. Both species were collected from the same site in Tasmania for this study. Some of the interspecific difference in recovery may simply be explained by variable collection efficiency. A. longa is a bigger worm than A. caliginosa.
The effect of DWB on local earthworm abundance and biomass was positive at Goulburn, at least on Hill A where relevant comparisons were made. The soil on Hill A was low in fertility at the start of the trial [13]. The addition of organic matter, either directly through the application of the DWB per se or indirectly through induced increases in pasture production [12], probably encouraged higher earthworm numbers. The burrowing behaviour of S. macleayi is poorly understood, but A. trapezoides and M. dubius, the other two most common species at Goulburn, are endogeic and epigeic, respectively. The positive responses of A. trapezoides and M. dubius to either small or large applications of DWB are in contrast to Butt’s [7] report of no changes in
The observed increases in pasture production (overall 46%), induced by the introduction of A. longa and A. caliginosa, were comparable with those reported elsewhere in south-eastern Australia [5] and serve to further highlight the potential advantages to be gained through improved management of such species as resources. However, the results reported here also demonstrate that the introduction of these exotic species may lead to a reduction in local earthworm fauna and should be undertaken with caution. Other research (G. Baker et al., Eur. J. Soil Biol. 38 (2002) 39–42) has also noted that the introduction of A. longa to Australian pastures can reduce the abundance of local fauna. Nonetheless, it seems that this impact is likely to be small and overshadowed by the benefits to be gained through in-
A. caliginosa and A. longa inoculation detected across the three hills (F = 1.13, P > 0.05). On Hill A, herbage yield varied with rate of DWB (F = 6.88, P < 0.001) and with and without added worms (Fig. 2; F = 12.78, P < 0.001). Herbage yield was greatest in the control and 120 tonnes DWB ha–1 treatments, and where A. caliginosa and A. longa were added. Herbage yield also varied between hills (F = 5.73, P < 0.01), with yields higher on Hill A than on Hills B and C (Fig. 2), and again between treatments with and without worms (F = 8.92, P < 0.005). Overall, the inoculation of A. caliginosa and A. longa increased herbage yield by 46.0%.
G. Baker et al. / Eur. J. Soil Biol. 38 (2002) 233–237
creased functional biodiversity and improved soil properties and plant yield. Michalk et al. [12] reported that pasture production increased with DWB application on Hill A at Goulburn. A similar pattern was not found in this study, with high plant yields in the control as well as in the 120 tonnes DWB ha–1 treatment site. This inconsistency between the studies may simply reflect the sites selected for the worm study and the very small area occupied by the earthworm cages compared with the more general surveys conducted by Michalk et al. [12] across the plots.
Acknowledgements We wish to thank Sydney Water and LWRRDC for financial support and Jacqueline Piercy, Jill Clapperton and Dale Chalker for their assistance with the work.
[6]
[7]
[8]
[9]
[10]
[11] [12]
References [1]
[2]
[3]
[4]
[5]
R. Aquilar, S.R. Loftin, P.R. Fresquez, Rangeland restoration with treated municipal sewage sludge, in: C.E. Clapp, W.E. Larson, R.H. Dowdy (Eds.), Sewage Sludge: Land Utilization and the Environment, SSSA Miscellaneous Publication, 1994, pp. 211–220. G.H. Baker, The ecology, management, and benefits of earthworms in agricultural soils, with particular reference to southern Australia, in: C.A. Edwards (Ed.), Earthworm Ecology, St Lucie Press, Boca Raton, 1998, pp. 229–257. G.H. Baker, V.J. Barrett, P.J. Carter, J.P. Woods, Method for caging earthworms for use in field experiments, Soil Biol. Biochem. 28 (1996) 331–339. G.H. Baker, P.J. Carter, V.J. Barrett, Survival and biomass of exotic earthworms, Aporrectodea spp. (Lumbricidae), when introduced to pastures in south-eastern Australia, Aust. J. Agr. Res. 50 (1999) 1233–1245. G.H. Baker, P.J. Carter, V.J. Barrett, Influence of earthworms, Aporrectodea spp. (Lumbricidae), on pasture production in south-eastern Australia, Aust. J. Agr. Res. 50 (1999) 1247–1257.
[13]
[14]
[15] [16] [17]
237
G.H. Baker, P.J. Carter, V.J. Barrett, Influence of earthworms, Aporrectodea spp. (Lumbricidae), on lime burial in pasture soils in south-eastern Australia, Aust. J. Soil Res. 37 (1999) 831–845. K.R. Butt, Effects of thermally dried sewage granules on earthworms and vegetation during pot and field trials, Biores. Techn. 67 (1999) 149–154. J.P. Curry, The invertebrate fauna of grassland and its influence on productivity. II. Factors affecting the abundance and composition of the fauna, Grass Forage Sci. 42 (1987) 197–212. C.A. Edwards, The use of earthworms in the breakdown and management of organic wastes, in: C.A. Edwards (Ed.), Earthworm Ecology, St Lucie Press, Boca Raton, 1998, pp. 327–354. W.D. Joshua, D.L. Michalk, I.H. Curtis, M. Salt, G.J. Osborne, The potential for contamination of soil and surface waters from sewage sludge (biosolids) in a sheep grazing study, Australia, Geoderma 84 (1998) 135–156. MAFF, Review of the rules for sewage sludge application to agricultural land, MAFF Publications, London, 1993. D.L. Michalk, I.H. Curtis, C.M. Langford, P.C. Simpson, J.T. Seaman, Effects of sewage sludge on pasture production and sheep performance, in: M. Asghar (Ed.), Proc. 8th Aust. Agronom. Conf., Toowoomba, Qld, 1996, pp. 429–432. D.L. Michalk, I.H. Curtis, J.T. Seaman, C.M. Langford, P.C. Simpson, G.J. Osborne, Benefits and risks associated with the application of biosolids to pastures grazed by sheep, in: G.J. Osborne, R.L. Parkin, D.L. Michalk, A.M. Grieve (Eds.), Biosolids Research in NSW, NSW Agriculture, Orange, NSW, 1996, pp. 62–84. J.E. Morgan, A.J. Morgan, Heavy metal concentrations in the tissues, ingesta and faeces of ecophysiologically different earthworm species, Soil Biol. Biochem. 24 (1992) 1691–1697. S.R. Smith, Agricultural Recycling of Sewage Sludge and the Environment, CAB International, Wallingford, 1996. Soil Survey Staff, Keys to Soil Taxonomy, 8th ed., USDA, Washington, DC, 1998. A.D. Tomlin, R. Protz, R.R. Martin, D.C. McCabe, R.J. Lagace, Relationships amongst organic matter content, heavy metal concentrations, earthworm activity, and soil microfabric on a sewage sludge disposal site, Geoderma. 57 (1993) 89–103.