Complementary ability of three European earthworms (Lumbricidae) to bury lime and increase pasture production in acidic soils of south-eastern Australia

Applied Soil Ecology 26 (2004) 257–271

Complementary ability of three European earthworms (Lumbricidae) to bury lime and increase pasture production in acidic soils of south-eastern Australia K.Y. Chan a,∗ , G.H. Baker b , M.K. Conyers a , B. Scott a , K. Munro a a

Organic Wastes Recycling Unit, NSW Agriculture, Locked Bag 4, Richmond NSW 2753, Australia b CSIRO Entomology, P.O. Box 1700, ACT, Canberra, Australia Received 3 April 2003; received in revised form 12 December 2003; accepted 15 December 2003

Abstract Mechanical incorporation of surface-applied lime (CaCO3 ) to ameliorate subsoil acidity is often not feasible because of damage to plants and erosion hazards. This paper presents results of a field cage experiment comparing the influences of three exotic European earthworm species (Aporrectodea longa, A. caliginosa and A. trapezoides) on lime incorporation and pasture production over two seasons, on two acidic soil types under pastures on the central tablelands of New South Wales, Australia. A. trapezoides was least effective in increasing pH of soil below 2.5 cm and survived poorly compared with A. caliginosa. The latter was most effective at 2.5–10 cm whilst A. longa was more effective at 10–15 cm depth. Similar complementary increases in the level of mineralisable nitrogen (MN) by both earthworm species were also observed. There was evidence suggesting that the survival of A. longa was improved by the presence of A. caliginosa. Earthworms improved pasture growth at only one site. Crown Copyright © 2004 Published by Elsevier B.V. All rights reserved. Keywords: Aporrectodea spp.; Soil acidity; Mineralisable nitrogen; Stratification; Bioturbation

1. Introduction Soil acidification is a serious form of land degradation in Australia and many other parts of the world (Chartres et al., 1992; Von Uexkull and Mutert, 1995). The central and southern tablelands of New South Wales, Australia have some of the most acidic soils (pH < 4.5) in the country and acidification of pasture soils is adversely affecting pasture production (Helyar et al., 1990). Williams (1980) reported a decline in pH of up to one unit in 50 years under clover pasture on the southern tablelands of New South Wales. Amelio∗ Corresponding author. Tel.: +61-2-4588-2108; fax: +61-2-4578-2528. E-mail address: [email protected] (K.Y. Chan).

ration with lime (CaCO3 ) is the most common method used to redress the problem. However, because of its low solubility, lime has to be brought into close contact with the soil to neutralise the acidity. In permanent pasture, surface-applied lime tends to remain in situ and its downward movement to the root zone is very slow (Helyar, 1991). Mechanical incorporation of lime into the root zone by tillage is often not feasible because of potential damage to the pasture, and in many areas within the tablelands, mechanical incorporation of surface-applied lime is inappropriate due to risk of erosion on steep slopes. Alternative methods are, therefore, urgently needed to assist the incorporation of surface-applied lime. Research has highlighted the ability of some earthworm species to bury lime and increase soil pH

0929-1393/$ – see front matter. Crown Copyright © 2004 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.apsoil.2003.12.004

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(Springett, 1985; Baker et al., 1999a). The mechanisms involved are not clearly understood but the effectiveness of lime incorporation varies between species and sites. Baker et al. (1999a) demonstrated that Aporrectodea longa (Ude) (Lumbricidae) could increase soil pH to 15–20 cm depth through the burial of surface-applied lime, whereas A. caliginosa (Savigny) and A. trapezoides (Duges) did the same but were effective only within the top 5 cm of soil. Their work was conducted within one earthworm season (winter–spring in the Mediterranean climate of south-eastern Australia) in a range of high rainfall pastures throughout south Australia and Victoria. Variability in lime burial between sites could be partly explained by rainfall patterns, but could also have been due to differences in soil types and earthworm survival following introduction (Baker et al., 1999b). More research covering a greater range of soil types over an observation period of greater than one season should help to improve the understanding of the potential of various earthworm species to bury lime and offset soil acidity at depth and the factors influencing this process. Furthermore, the potential of using a mixture of earthworm species with different burrowing behaviours, rather than simply considering single species effects, has not previously been assessed. This paper presents results of a field experiment comparing the influences of three exotic earthworm species (A. longa, A. caliginosa and A. trapezoides) on lime incorporation and pasture production, over two seasons on two contrasting soil types, under pastures on the central tablelands of New South Wales, Australia. In addition to studying their effects as single species, a mixed population of A. longa and A. caliginosa was included. These two species are widespread in pastures throughout their native Europe (Sims and

Gerard, 1985) and often occur together in Tasmania and New Zealand (Springett, 1992; Baker et al., 2002).

2. Materials and methods 2.1. Sites and soils The experiment was conducted at two sites on the central and southern tablelands of New South Wales, Australia with contrasting soil types (Table 1). At Neville, 50 km south of Orange (33◦ 19 S, 149◦ 5 E), the soil was a red earth (Ultisol). At Oolong, 30 km east of Yass (34◦ 52 S, 148◦ 54 E), the soil was a duplex, solodic soil (Alfisol). Both sites had previously been under long-term pastures. The site at Oolong had never been cultivated while at Neville it had been occasionally cropped but had been under pasture for the previous 20 years. The soils at both sites are strongly acidic in the surface 10 cm (pHCa = 3.9 and 4.1, respectively, for Neville and Oolong). At Neville, the soil pH was approximately 4.1 down to 20 cm depth and then increased gradually to 5.0 at 80 cm depth. At Oolong, the soil pH increased to 4.5 at 25 cm depth and 5.8 at 80 cm depth. Whilst the soil at Neville is a gradational soil with clay content increasing more or less continuously with depth (from 25% at 0–10 cm to 60% at 80 cm depth), the soil at Oolong is a duplex soil with about 16% clay at 0–25 cm which then increases abruptly to 35% at about 25 cm depth as it changes from the A to B horizon. General soil sampling indicated that both sites are dominated by native earthworms (Spenceriella spp., Megascolecidae). No exotic Lumbricidae have previously been found near the trial sites, except for a very low population density of A. trapezoides (<20 m−2 ) at Oolong.

Table 1 Selected soil properties of the 0–10 cm layer at Neville and Oolong, NSW, Australia Sites

Soil type

pHa

ESPb (%)

OCc (g kg−1 )

Available Pd (mg kg−1 )

Clay (g kg−1 )

Silt (g kg−1 )

Fine sand (g kg−1 )

Coarse sand (g kg−1 )

Neville Oolong

Ultisol Alfisol

4.1 3.9

1.3 2.0

26.6 17.5

7 9

250 170

200 100

530 390

20 340

a

pH in 1:5 0.01 M CaCl2 . ESP: exchangeable sodium percentage. c OC: organic carbon. d Available phosphorus (Olsen P). b

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2.2. Cage experiment Earthworm cages (Baker et al., 1996) were installed at each site during May 1998. The cages were made from sections of PVC pipe (30 cm diameter × 20 cm long) which were pushed 15 cm into the soil using a vibrating plate compactor (Wacker® ). The sections of PVC pipe, containing undisturbed soil cores, were then excavated and the soil was fractured across the bottom edge of the pipes. The bottom ends of the PVC sections were enclosed using fine nylon mesh fixed in place with packaging straps and buckles and the PVC and the soil therein were then returned to the original holes and the surrounding soil tamped down firmly. These cages were arranged adjacent to each other in rows of 15, with 1 m between rows allowing easy access to individual cages. There were two control and seven earthworm treatments, with 15 replicate cages for each, arranged in a randomised block design. The treatments were: (1) Control I; (2) Control II; (3) A. caliginosa, low density; (4) A. caliginosa, high density; (5) A. longa, low density; (6) A. longa, high density; (7) A. trapezoides, low density; (8) A. trapezoides, high density and (9) Mixed species, A. caliginosa and A. longa. Control I was a treatment with no lime and no introduced earthworms, whereas Control II had lime applied but no introduced earthworms. Low and high densities were 15 and 30 earthworms per cage, respectively, and were equivalent to 212 and 424 worms per square metre. For the Mixed species treatment, 15 A. caliginosa together with 15 A. longa were placed in each cage. Both A. caliginosa and A. longa were collected from Woolnorth in northwest Tasmania and A. trapezoides was collected from Temora, NSW. The earthworms were maintained in moist soil in a cool room for approximately 7 days prior to inoculation into the cages. The pasture at Oolong was a degraded pasture dominated by silver grass (Vulpia spp.) and native grasses. At Neville, the existing pasture was inadvertantly sprayed out just prior to the commencement of the experiment and so the individual cages were seeded with a mixture of subterranean clover (Trifolium subterraneum) and cocksfoot (Dactylis glomerata) 2 weeks before the introduction of earthworms and lime application. In July 1998, either 15 or 30 earthworms of the different species were added to the appropriate individual cages. After all the earthworms

259

had completely entered the soil, 28.3 g of agricultural fine lime (CaCO3 , equivalent to a lime application rate of 4 t/ha) was evenly applied onto the soil surface of all the cages with the exception of those which had been designated Control I. The application rate was sufficient to raise the pH (CaCl2 ) of the surface soil (0–10 cm) to 5.5, a recommended practice for the region. During the course of the experiment, all the PVC sections were covered with nylon mesh bags which were placed over wire frames (approximately 30 cm high) and strapped to the tops of the PVC to prevent the escape or invasion of earthworms across the soil surface and to protect from predatory birds. 2.3. Soil sampling and earthworm measurements In November 1998, 10 cages from each of the nine treatments were sampled for soils and earthworms. Two small soil cores (2.5 cm diameter and 15 cm long) were collected from each cage using a stainless steel soil corer when the soil was still moist. Any litter present on the surface of the cores was removed, collected in a plastic bag and later weighed after drying at 80 ◦ C for 48 h. Each soil core was sectioned into five layers, 0–2.5 cm, 2.5–5.0 cm, 5.0–7.5 cm, 7.5–10 cm and 10–15 cm depth. Sectioning was carried out by carefully pushing out fixed lengths of soil cylinders using teflon blocks of 2.5 and/or 5.0 cm long and cutting with a sharp knife. The two samples from the same depth within each cage were bulked to form a composite sample. The cage was then dismantled and the remaining soil hand-sorted to collect all the surviving earthworms. The extracted earthworms were stored in 70% alcohol and the number of the different earthworm species was counted in the laboratory. The soil samples were weighed, air-dried at 36 ◦ C and re-weighed. Using this information, the air-dried soil water content and dimension of the soil sections, bulk density of the soil at different depths was calculated. The remaining five cages for each treatment were left in the field for another season until November 1999 when soil samples and surviving earthworms were collected as described above. 2.4. Pasture production measurements Pasture cuts for dry matter determination were carried out twice during the first season, once in

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Table 2 Annual rainfall, dates of commencement and termination of experiments, and dates for pasture cuts within cages at Oolong and Neville Year

1998 1999

Oolong

Neville

Rainfall (mm)

Start

End

Pasture cut

Rainfall (mm)

Start

End

Pasture cut

758 710

20/7 –

10–13/11 25–27/10

30/9, 3/11 18/10

1122 1227

21/7 –

25–27/11 15–17/11

27/10, 23/11 21/10

September/October and then again in November, just before the dismantling of the cages (Table 2). Only one pasture cut was carried out in the second season, in October, just prior to the termination of the experiment. 2.5. Soil pH measurements The air-dried soil samples were mixed thoroughly and first passed gently through a 6.3 mm sieve. Half of the sample was then ground to pass through a 2 mm sieve. Soil pH was determined, using the <2 mm soil, in 0.01 M CaCl2 (Raymont and Higginson, 1992). 2.6. Mineralisable nitrogen (MN) Mineralisable nitrogen was determined using the anaerobic incubation method of Keeney (1984) for the soils collected from three treatments, namely Control II, A. longa (high density) and Mixed species at both sites in 1998. Keeney’s method measures organic forms of nitrogen which become available after mineralisation (Waring and Bremner, 1964). 2.7. Statistical analysis Treatment differences for the same year were compared using one way analysis of variance (Genstat 5, 1993) and the means were compared using the least significance differences at 5% probability (LSD0.05 ). For comparison between different years for the same earthworm species, paired t-tests were used. Differences were significant at P < 0.05 unless otherwise stated. 3. Results 3.1. First season 3.1.1. pH Fig. 1 shows the soil pH at the end of the first season at five different depths for the various treatments. For

Control I (no lime), pH remained below 4 (3.8–3.9) from 0 to 15 cm depth at Oolong, whilst at Neville, pH was 4.67 at 0–2.5 cm but dropped to 3.9 in the lower soil layers. The effect of earthworm density (15 versus 30 worms per cage) on pH was not significant at either site. Therefore, data at each site for A. caliginosa, A. longa and A. trapezoides at both densities were averaged and compared to the other treatments using one way analysis of variance. Control II (cages with lime, but no introduced worms) and all the earthworm treatments had significantly higher pHs at the soil surface (0–2.5 cm) than Control I at both sites, a direct result of surface application of lime. However, amongst all the limed treatments, A. longa had the lowest pH at this depth, indicating a greater ability of this earthworm either to remove lime from the soil surface or to bring up unlimed soil material from below. At Oolong, the pH of the soil in Control II was significantly higher than that of Control I throughout the full depth of sampling (e.g. 4.35 versus 3.77 at 2.5–5.0 cm and 4.28 versus 3.85 at 10–15 cm depth) (Fig. 1a). This indicates considerable downward movement of surface-applied lime even in the absence of any introduced earthworms. To assess the additional effects of the introduced earthworms for depths below 2.5 cm, we compared the pH of the different earthworm treatments with those of Control II at the different soil depths. Significant differences (P < 0.05) were observed but they varied with earthworm species (Fig. 1a). For A. caliginosa, pH was significantly higher at 2.5–5.0 cm (4.60 versus 4.35) and 5.0–7.5 cm (4.29 versus 4.02). For A. longa, a significant difference in pH was detected only at 10–15 cm (4.50 versus 4.28). No significant differences in pH were detected in the cases of A. trapezoides and Mixed species treatments (Fig. 1a). At Neville, in the absence of the introduced earthworms, there was negligible movement of the surface-applied lime down the soil profile in Control

K.Y. Chan et al. / Applied Soil Ecology 26 (2004) 257–271

261

(a) Oolong 6

control 1CI control 2CII limed/Atlimed/At limed/Aclimed/Ac limed/A.llimed/Al limed/mixed limed/Ac+Al

pHCaCl

2

*

5

*

* *

4

*

* 0-2.5

2.5-5.0

*

*

* 5-7.5

7.5-10

10-15

Soil depth (cm) (b) Neville *

pHCaCl

2

6

5

* * * *

* *

*

*

*

4 0-2.5

2.5-5.0

5-7.5

7.5-10

10-15

Soil depth (cm) Fig. 1. pH profiles with different earthworm treatments compared to the limed and non-limed controls after the first season (1998) at the two investigation sites (a) Oolong and (b) Neville ((∗ ) significantly different (P < 0.05) from Control II; At: A. trapezoides; Ac: A. caliginosa and Al: A. longa).

II (compare pH for Control I and Control II between 2.5 and 15 cm depth in Fig. 1b). A significant influence of A. trapezoides was detected in this soil, but only in the 2.5–5.0 cm layer (4.18 versus 4.07). For the A. caliginosa and A. longa treatments, a similar pattern to that observed at Oolong was found, in that

A. caliginosa was effective in significantly increasing pH at shallow depths (2.5–7.5 cm) whereas A. longa was effective at greater depths (7.5–15 cm). In particular, A. longa increased pH by 0.5 at 10–15 cm. For the Mixed species treatment, significantly higher pH was found at 2.5–5.0 cm, 5.0–7.5 cm and 10–15 cm

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Table 3 Dry matter production of pasture (g m−2 ) from the cage experiments in the 1998 and 1999 seasons Treatments

CI CII Atlow Athigh Aclow Achigh Allow Alhigh Mixed LSD0.05

Oolong

Neville

1998

1999

1998

1999

509 590 620 634 611 650 719 708 676

642 615 604 675 754 776 918 718 805

410 426 430 491 502 466 497 487 502

527 527 611 479 503 646 468 584 595

64

152

ns

ns

CI: unlimed control; CII: limed control; At: A. trapezoides; Ac: A. caliginosa; Al: A. longa; low and high, respectively, refer to low and high density earthworms treatments; Mixed: mixed species treatment.

depths. The increases in pH were similar in magnitude to those recorded for the A. caliginosa treatment at the shallower depths, but lower than that for A. longa at 10–15 cm (Fig. 1). 3.1.2. Pasture production At Oolong, total dry matter production was significantly higher for all the limed treatments compared with Control I during 1998 (Table 3). Amongst the limed treatments, only the A. longa (at both densities) and the Mixed species treatments had significantly higher yields (approximately 20%) than Control II. In contrast, no significant differences in pasture yield were detected amongst all the treatments at Neville. 3.1.3. Survivals of introduced earthworms and effects on resident populations At the end of the first season, given the short time interval since inoculation, very few young earthworms (new generation) would have hatched and been included in the sampling. Survivals of the introduced earthworms were, therefore, estimated from the numbers of earthworms found at sampling, expressed as percentages of initial numbers introduced. A. caliginosa had the highest survival percentage (>80% across all treatments) of the three introduced earthworm species at both sites, considerably higher than those for A. longa and A. trapezoides (40–70%) (Fig. 2).

In the Mixed species treatment, with 15 A. longa and 15 A. caliginosa per cage, percentage survival of A. longa was significantly (P < 0.05) higher than that of A. longa at low density alone (70.3% versus 54.3%, averaged over the two sites). This suggests that the survival of A. longa was improved by the presence of A. caliginosa. On the other hand, recovery of A. caliginosa in the Mixed treatment remained similar to that in the A. caliginosa low density treatment (average 88%) and did not differ between the two sites. At both sites, the resident earthworms were Australian native species (Spenceriella spp., Megascolecidae). The average densities of these native earthworms in the cages were 76 and 90 individuals per square metre (Neville and Oolong, respectively). The densities of the native species did not vary significantly across the experimental and control treatments. 3.1.4. Litter and mineralisable nitrogen Accumulation of surface litter was only found at Oolong. Significantly less litter was present in all the introduced earthworm treatments compared with Control II, with the exception of the treatment with A. caliginosa at low density (Table 4). On average, the introduced earthworms removed the equivalent of 6.06 t ha−1 of litter during the experiments. Interestingly, 6.1 t ha−1 of surface litter was found to be removed by earthworms in one season in a pasture in New Zealand (Syers et al., 1979). In the present case, the largest reduction in litter was found in the high Table 4 Amount of litter sampled from the soil surface of the different treatments at the Oolong site at the end of the first year Treatments

Litter (t ha−1 )

CI CII Atlow Athigh Aclow Achigh Allow Alhigh Mixed

8.91 10.85 5.95 4.24 8.12 5.34 3.65 2.66 3.58

LSD0.05

3.16

CI: unlimed control; CII: limed control; At: A. trapezoides; Ac: A. caliginosa; Al: A. longa; low and high, respectively, refer to low and high density earthworms treatments; Mixed: mixed species treatment.

K.Y. Chan et al. / Applied Soil Ecology 26 (2004) 257–271

263

Earthworm abundance (% of numbers inoculated)

Earthworm abundance (% of number inoculated)

1998 100 90

At-low At-h Ac-low Ac-h mixed Al-low Al-h

(a)

80

lsd0.05

70 60 50 40 30 20 10 0 Oolong

Neville

Sites 1999 100 90

(b)

80 70

lsd0.05

60 50 40 30 20 10 0 Oolong

Neville

Sites

Fig. 2. Abundance of earthworms (expressed as percentage of number inoculated) in the different treatments at the end of (a) 1998 and (b) 1999 season (At: A. trapezoides; Ac: A. caliginosa; Al: A. longa; low, high refer, respectively, to the low and high density treatments; Mixed: mixed species treatment).

264

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density A. longa treatment, where 8.19 t ha−1 of litter was lost from the soil surface, presumably carried into the subsoil and at least partly consumed by the earthworms. Average mineralisable nitrogen at the end of the first season varied with soil depth for the Control II, A. longa (high density) and Mixed species treatments (Fig. 3). As there was no statistical difference (P = 0.05) between sites, MN data for the two sites were, therefore, averaged and presented (Fig. 3). In all these treatments, MN was highest at the soil surface and decreased rapidly with depth. Compared to the Control II, A. longa significantly (P < 0.05) reduced MN at shallow depth (2.5–5.0 cm) but increased it at 10–15 cm. In contrast, MN was significantly higher at the soil surface in the Mixed species treatment compared with the other two treatments, and similar to that with A. longa, at depths >7.5 cm.

3.2. Second season 3.2.1. pH At the end of the second season at Oolong, pH varied significantly between Control I and Control II only at the soil surface (0–2.5 cm depth) (Fig. 4a), suggesting little downward movement of lime in the absence of introduced earthworms. As in 1998, soil pH did not vary with earthworm densities in 1999, and therefore, data for the different densities were pooled. Soil pH was lower at the soil surface in the presence of A. longa compared with Control II. Below 2.5 cm depth, A. trapezoides increased pH only at 2.5–5.0 cm depth, whilst A. caliginosa did so down to 10 cm depth. At 10–15 cm depth, a significantly (P < 0.05) higher pH was detected in the Mixed species treatment (4.52 versus 4.07) (Fig. 4a). The Mixed species treatment also had a significantly higher pH than Control II at

Mineralisable N 0

10

20

30

40

50

60

70

0

lsd0.05

2

Depth (cm)

4

6

8

limed -nil worm limed-longa limed-mixed worm

10

12

14

Fig. 3. Mineralisable nitrogen profiles under the A. longa and Mixed species treatments compared with the limed control at the end of 1998 season.

K.Y. Chan et al. / Applied Soil Ecology 26 (2004) 257–271

265

(a) Oolong

6

*

2

pHCaCl

Control 1 Control 2 limed/At limed/Ac limed/Al limed/mixed

5

* * *

*

*

* *

4

0-2.5

2.5-5.0

5-7.5

7.5-10

10-15

Soil depth (cm)

(b) Neville

pHCaCl

2

6

5

* *

* **

*

*

* *

4

0-2.5

2.5-5.0

5-7.5

7.5-10

10-15

Soil depth (cm) Fig. 4. pH profiles under different earthworm treatments compared with the limed and non-limed controls after the second season (1999) at the two investigation sites (a) Oolong and (b) Neville ((∗ ) significantly different (P < 0.05) from Control II; At: A. trapezoides; Ac: A. caliginosa; Al: A. longa).

2.5–5.0 cm depth. The soil pH of the A. longa treatment was not significantly different from Control II below 2.5 cm depth (Fig. 4a). At Neville, there was again little evidence of downward movement of the surface-applied lime below 2.5 cm in the absence of introduced earthworms. Soil

pH only differed significantly between the Control I and Control II treatments at 0–2.5 cm depth (Fig. 4b). Below 2.5 cm depth, A. trapezoides significantly increased pH only in the 2.5–5.0 cm layer (4.38 versus 4.19 in Control II) and A. caliginosa increased pH down to 10 cm depth (e.g. at 2.5–10 cm depth, 4.76

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K.Y. Chan et al. / Applied Soil Ecology 26 (2004) 257–271

(a) Oolong 0.6

0-2.5 cm 2.5 -5.0 cm 5.0 -7.5 cm 7.5 - 10 cm 10 -15 cm

* 0.4

*

pH99-98

*

*

0.2

**

0.0

* **

-0.2

-0.4

**

*

-0.6 Ac

Al

Mixed

CI

CII

Treatments

(b) Neville 0.6

0.4

pH99-98

0.2

*

* *

*

0.0

-0.2

*

* -0.4

*

-0.6 Ac

Al

*Mixed

CI

CII

Treatments Fig. 5. Changes in pH between 1999 and 1998 season at the different depths under different earthworm treatments and the controls at the two investigation sites (a) Oolong and (b) Neville ((∗ ) indicates the changes in pH are significant (P < 0.05)).

K.Y. Chan et al. / Applied Soil Ecology 26 (2004) 257–271

versus 4.19 in Control II). Both the A. longa and Mixed species treatments had similar pH and both were significantly (P < 0.05) higher in the 2.5–5.0 cm layer (4.41 versus 4.19) and in particular, in the 10–15 cm layer (pH 4.64 versus 4.20) than Control II (Fig. 4b). In Fig. 5, changes in soil pH between the two seasons (1999 value minus 1998 value) for the Control I, Control II, A. caliginosa, A. longa and Mixed species treatments are presented to assess the additional effect of the second season. At Neville, significant reduction in pH in the 0–2.5 cm layer in 1999 was observed in all the treatments with the exception of A. caliginosa. For Control II, pH remained unchanged for depths below 2.5 cm at Neville. However, at Oolong, significant decreases in pH were observed at all depths to 15 cm (Fig. 5). At both sites, in 1999, significant additional increases in pH due to A. caliginosa were detectable over the 2.5–10 cm layer. For the 10–15 cm layer, a significant increase in pH was only detected in the Mixed species treatment (Fig. 5). In fact, the latter treatment was the only one in which significant increases in pH over the 2.5–7.5 cm as well as 10–15 cm depths were recorded. In contrast, no significant increase in pH was detected in A. longa treatment with the exception of 2.5–5.0 cm at the Neville site (Fig. 5). 3.2.2. Pasture production In the absence of introduced earthworms, no pasture response was detected as a result of lime application at either site (Table 3). At Neville, no difference was detected between Control II and the different earthworm treatments. However, at Oolong, the A. caliginosa (high density), A. longa (low density) and the Mixed species treatments had significantly higher pasture production than Control II, thus indicating significant earthworm effects. The highest dry matter production was detected in the low density A. longa treatment, which was 49% higher in 1999 than in Control II (Table 3). There was no evidence to suggest an additive effect on pasture production from the addition of A. caliginosa and A. longa together. 3.2.3. Abundance of introduced earthworms and effects on resident populations The Aporrectodea collected from the cages in 1999 represented survivors from the original inoculation plus recruits. It was not possible to separate these co-

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horts within the cages. By the end of the 1999 season, population densities had declined most for A. trapezoides (numbers of earthworms dropping to <20% of those inoculated at both sites, Fig. 2b). Highest densities were recorded for A. caliginosa, at both sites (approximately 60% of the number inoculated). The abundance of A. longa was lower than that of A. caliginosa at both sites (ranged between 13 and 47% of the number inoculated). No resident native earthworms were found in any of the treatments at Neville in 1999. At Oolong, an average of 50 native earthworms per square metre was found in 1999 (about half of that found in the previous year, i.e. 90 m−2 ) and no effect of introduced earthworms on the abundance of the natives was detectable.

4. Discussion The results of this study support earlier findings of the effectiveness of some earthworms, particularly Lumbricidae, in lime burial and hence in increasing the pH of the subsurface soil (Springett, 1985; Baker et al., 1999a). Because of the likely differences in buffering capacities between soils at Oolong and Neville, it is not legitimate to compare the effectiveness of lime burial between different sites based directly on pH differences. However, relative effects of the different earthworm treatments on pH were similar at the two sites even though they were different soil types and had different management histories. In the absence of introduced earthworms, downward movement of surface-applied lime was negligible below 2.5 cm even after 18 months, except in the first season at Oolong. This could be due to the sandier surface soil at Oolong and the heavy rainfall in the early part of the first season when lime was freshly applied. The magnitude of the pH increases due to the three introduced earthworm species at the different depths were comparable to those reported earlier for a range of sites in south Australia and Victoria, where variability between sites was high (Baker et al., 1999a). A. trapezoides was much less effective in this study than reported earlier for one site in south Australia (Baker et al., 1993). The latter authors reported a pH increase of 0.8 unit at 4–6 cm depth within one season at an introduction rate of 424 individuals per square metre. With a pH of 4.0 in the 0–20 cm layer, the

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soils used in the present study were at the lower end of the pH range of the soils studied by Baker et al. (1999a). According to Lee (1985), earthworms are rare in soils with pH < 4.0–4.5 and are generally absent where pH < 3.5. Edwards and Lofty (1975) considered that the lower tolerable limit of pH for most species is 4.2. It is worthwhile pointing out that both Lee (1985) and Edwards and Lofty (1975) did not specify whether their pH results were measured in water or in calcium chloride solution, and the difference between the two methods could be as much as 0.5 pH unit. Nevertheless, it is probable that the poor performance of A. trapezoides in this study might be related to a lower tolerance for soil acidity compared with A. longa and A. caliginosa but further research is needed to confirm this. Surveys of high rainfall pastures throughout south Australia, Victoria and southern New South Wales (Baker et al., 1992b; Baker, 1998a; Baker and Chan, unpublished data) have failed to show correlations between earthworm abundance and soil pH, but few strongly acidic sites (pH ≤ 4) have been included in such work. Another possible reason for the different behaviour of A. trapezoides was the fact that it was collected from a different site to the other two species, which came from the same site. The present results demonstrated the different but complementary abilities of A. longa and A. caliginosa to bury lime. A. longa was mainly effective in increasing pH at 10–15 cm depth whereas A. caliginosa was effective at 2.5–10 cm. The “best” treatment appeared to be the Mixed species one with significant pH increases in the shallower (2.5–5.0 cm and 5.0–7.5 cm) as well as the deeper (10–15 cm) layers. The cage design with a mesh installed at 15 cm depth to prevent escape of inoculated earthworms was based on earlier research findings on the depth distribution of A. caliginosa (and A. trapezoides) in south Australia (e.g. Baker et al., 1992a) and the results of several surveys throughout south Australia, Victoria and southern New South Wales (e.g. Baker et al., 1992b) which suggest the same species rarely are active below 10 cm depth in the cooler, wetter months (usually in fact closer to the soil surface). Our experience in Woolnorth, Tasmania, where A. longa is numerous, also suggests this species is rarely found below about 15 cm in the soil profile in winter and early spring.

Across seven sites in south Australia and Victoria, Baker et al. (1999a) reported percentage survival for introduced A. longa, A. caliginosa and A. trapezoides after one season of 75, 64 and 50%, respectively. In the present study, after one season, percentage survivals of A. longa, A. caliginosa and A. trapezoides averaged across the two sites were 49, 85 and 55%, respectively. After two seasons, A. caliginosa was also more abundant than the other two species, with numbers equivalent to 60% of original inoculations collected at both sites, compared to 13–47% for A. longa and <20% for A. trapezoides. The lower abundances of all the introduced earthworms detected at the end of the second season could have been partly due to their inability to move deeper into the soil profiles during the summer months due to cage design. Therefore, results of the first season should reflect the ability of the different introduced species because all the three species of earthworms were expected to be active in the top 15 cm layer of the soil. However, in the light of the possibility of reduced abundance due to the cage design, results of the second season could have been partly confounded. Ecologically, A. longa is classified as an anecic species whereas A. caliginosa is an endogeic species (Lee, 1985). Anecic species live deep in the soil but come to the surface to collect plant litter which they drag into their burrows. They are thus important in burying surface litter. This superior ability was demonstrated in this research by A. longa at Oolong in its removal of 8.19 t ha−1 of litter from the soil surface during a 4-month period. Endogeic species primarily inhabit mineral soil horizons, burrowing more horizontally than anecic species and feeding more on partially decomposed organic matter already buried beneath the soil surface. Given these different feeding and burrowing behaviours of the earthworms, the different distributions of lime with depth are perhaps not surprising. Whether the lime is actively transported by the worms or is washed passively down burrows by rainwater is not known (Baker et al., 1999a). The presence of A. caliginosa improved the survival of A. longa. The reason for this is not known. In contrast, Dalby (1996) and Baker et al. (2002) could show no influence of the addition of A. caliginosa on the survival of A. longa in glasshouse experiments, whilst the growth of A. longa was in fact reduced. On the other hand, the presence of A. longa did not

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influence the survival of A. caliginosa in the present study. Similarly, Dalby (1996) and Baker et al. (2002) could not demonstrate any effect of A. longa addition on the survival of A. caliginosa in glasshouse cultures, but they did find significant reduction in the growth of A. caliginosa. When A. longa has been introduced to field sites along with A. caliginosa or added to sites where A. caliginosa is already common, it has reduced the abundance and biomass of the latter species on some occasions (Dalby, 1996; Baker et al., 2002). Perhaps A. longa and A. caliginosa compete for resources, albeit to a minor extent (Dalby et al., 1998). The complementary role of A. caliginosa and A. longa was also evident in the mineralisable nitrogen profiles. MN was generally highest at all soil depths in the Mixed species treatment. Whilst A. longa reduced MN at shallow depths, this decrease was seemingly offset by A. caliginosa. The increase in MN recorded down to 15 cm depth in the Mixed species treatment compared to Control II was equivalent to 9.4 kg ha−1 (calculated from MN and bulk density data to 15 cm depth). The fact that such shifts in MN happened in “an earthworm season” (in 4 months) indicates the potential impact that earthworms can have on carbon and nitrogen recycling and movement in the soil profile. Under permanent pasture, stratification of soil properties such as pH, organic carbon, nitrogen and other nutrients are often reported in many Australian soils (Young et al., 1995). This could be a consequence of a lack of mixing of the soil profiles due to the absence of appropriate fauna. The effectiveness of some earthworm species in bioturbation is well documented (Lee, 1985). The strongly stratified soil profiles found under many Australian pastures could be due to the absence of such earthworm species. Improving earthworm diversity may, therefore, yield additional benefits to soil fertility, as well as improving lime burial. Baker et al. (1999c) recorded very variable, but overall positive, effects on pasture production after introducing A. longa, A. caliginosa and A. trapezoides to cages, as used in this study, at several sites throughout south Australia and Victoria. They suggested several factors which may have contributed to this variable response, including differential survival of earthworms. In the present study, the reason for the failure of the earthworms to influence pasture production at Neville, in contrast to the increases recorded at Oolong, are unclear. Survival of the earthworms

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was reasonably similar at the two sites. Possibly the factors limiting pasture production at Neville, unlike Oolong, were beyond the influence of earthworms, at least over the period the experiment was conducted. The fact that Oolong, unlike Neville, had never been cultivated before may have provided an opportunity for the introduced earthworms to have differential effects on soil structure at the two sites. The magnitude of the increases in pasture production recorded at Oolong (20–50%) and the biases towards the treatments with A. longa, and to a lesser extent A. caliginosa, are in accordance with findings from other, similar studies in southern Australia (Baker et al., 1999c). However, A. longa is a much larger earthworm than A. caliginosa and A. trapezoides. The biomass per individual at the start of the experiment was in the ratio of 3.5:1.6:1.0, respectively, for A. longa, A. trapezoides and A. caliginosa. Therefore, whilst similar numbers of each earthworm species were added to the cages at Oolong, biomasses varied greatly between treatments. Baker et al. (1999c) demonstrated that, per unit biomass, A. caliginosa and A. trapezoides in fact improved plant production to a much greater extent than A. longa. Although other studies (Syers and Springett, 1983; Temple-Smith et al., 1993; Baker, 1998b) have shown that adding A. longa to A. caliginosa populations can provide additional pasture production, there was no similar evidence for additive effects in this study. There was, however, a trend in this direction at Oolong in the second season, when the Mixed species treatment yielded an increase in pasture production of 31%, compared with 23% for the low density A. caliginosa treatment. Note, however, both increases were much less than the 49% recorded for the low density A. longa treatment. The poor performance of A. trapezoides, relative to A. caliginosa, in terms of pasture production (as well as lime burial), could be explained, at least in part, by its poorer survival. It is interesting to note that whilst A. caliginosa did not increase pasture production significantly in the first season of the trial at Oolong, it did so in the second. This finding adds credence to Baker et al.’s (1999c) comment that one season may be insufficient to adequately demonstrate an earthworm’s potential contribution to pasture production, even in a small soil volume such as in the cages used here. Several authors (Stockdill, 1982; Temple-Smith et al.,

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1993) have shown it may take several years for pasture production benefits to be demonstrable following earthworm introductions at the field scale. The introduction of lumbricid earthworms did not influence the abundance of native megascolecid species at either Neville or Oolong. Disappearance of native earthworms at Neville in 1999 was unlikely to be due to the introduced earthworms as none was also found in the control treatments. Baker et al. (1999b) also failed to demonstrate an influence of introduced lumbricid species on the abundance of resident megascolecids in other sites in southern Australia, although they did report a reduction in the biomass of native species at one site. More commonly, interactions between introduced lumbricids (see comments above) and other exotic species (e.g. Microscolex dubius (Acanthodrilidae)) have been demonstrated (Baker et al., 1999b; Dalby, 1996; Dalby et al., 1998). The biology of native earthworms in Australia is poorly understood (Abbott, 1994). The potential for competition between them and exotic species is, therefore, difficult to gauge. The abundance of megascolecid earthworms in the cages at the end of 1999 was markedly reduced at Oolong and was nil at Neville. Reasons for this are not known. Possibly the cage design, with a mesh installed at 15 cm depth thereby preventing deep burrowing to avoid surface aridity in summer, was limiting for these species. At least one of the native species at Neville appeared to naturally burrow much deeper into the soil profile than the bottom of the PVC cages.

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