Soil pH preferences and the influences of soil type and temperature on the survival and growth of Aporrectodea longa (Lumbricidae)

Pedobiologia 47, 745–753, 2003 © Urban & Fischer Verlag http://www.urbanfischer.de/journals/pedo

The 7th international symposium on earthworm ecology · Cardiff · Wales · 2002

Soil pH preferences and the influences of soil type and temperature on the survival and growth of Aporrectodea longa (Lumbricidae) Geoff H. Baker* and Wendy A. Whitby CSIRO Entomology, P.O. Box 1700, Canberra, A.C.T. 2601, Australia Submitted September 6, 2002 · Accepted March 5, 2003

Summary The potential of the deep-burrowing earthworm, Aporrectodea longa, to improve the functional diversity of soil communities, soil properties and plant production if introduced in high rainfall pastures in south-eastern Australia has been recognised previously. This paper reports on suitable soil types, pH and temperature regimes for the culturing of A. longa and develops predictions as to where A. longa might best establish. Laboratory experiments show that A. longa will survive and grow to maturity when reared in the laboratory in a commercially available sand: loam mix, supplemented with sheep dung for food. Survival, development of cocoons and growth of hatchling earthworms was, overall, optimal at 15 °C. Few cocoons survived two months in air-dried soil. Earthworms showed a strong aversion to soil pH below 4.5. The development time required for cocoons at soil temperatures likely to be experienced in the field in southern Australia (e.g. 15–20 weeks at 10 °C) is discussed in terms of likely establishment success. Key words: Aporrectodea longa, soil pH, temperature, preference, development

Introduction The earthworm fauna of agricultural soils in southern Australia is dominated by accidentally introduced European species (Baker 1998a,b). They are patchy in distribution, low in abundance and poor in diversity. The fauna generally lacks anecic species. However, one such introduced species, Aporrectodea longa (Ude) (Lumbricidae), is common in northern Tasmania, but rare on mainland Australia. Previous research has shown that A. longa can, if given the chance, colonise high rainfall pastures on mainland Australia, increase pasture production and greatly enhance the burial of

surface-applied lime and thus assist in ameliorating soil acidity, which is a major agricultural problem in the region (Baker et al. 1999a,b,c). The work reported here was part of a study aimed at developing methods to rear and introduce A. longa to pastures in southern Australia, and to predict where A. longa might best establish. This paper focuses particularly on determining optimal temperatures and soil pH for A. longa. Satchell (1967) reported that A. longa inhabits soils in the field with pH > 4.5 (presumably measured in water) and Laverack (1961) noted that A. longa rejects

*E-mail corresponding author: [email protected]

0031-4056/03/47/05–06–745 $15.00/0

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soils and solutions with pH < 4.5. Bouché (1972) classified A. longa in France as a “neutrophile”, with a preferred soil pH = 6.7. Jefferson (1959) described A. longa as preferring neutral and alkaline soils in northern England. However, Baker et al. (1999a) introduced A. longa, within cages, to several sites with acid soils (pH in CaCl2 = 4.5–5.3) in southern Australia and recorded high levels of survival at most sites five months later. The addition of lime to these soils did not affect the survival or biomass of A. longa. Several studies have shown that earthworm development is inversely related to temperature (Lee 1985; Butt 1991, 1997). Evans & Guild (1948) suggested that A. longa may take a year to reach maturity at the temperatures it experiences in the field in the U.K. Butt (1993) studied the growth and reproduction of A. longa in laboratory cultures in the U.K. with a view to developing methods to rear this species for inoculation into reclaimed land. He reared A. longa in moist loamy sand, plus paper pulp, cattle solids and yeast for food, and reported that the complete life cycle could be achieved in six months. He found that maturity was reached, at an average of 3.9 g fresh weight, within 4 months from hatching, when earthworms were reared at 20 °C. However, noting the upper lethal temperature limit for A. longa is 25.7 °C (Miles 1963) and his own work showing that hatching of cocoons is less successful at 20 °C than at 15 °C, Butt recommended rearing temperatures for A. longa should not exceed 15 °C. On the other hand, Lofs-Holmin (1982) reared A. longa in clay plus farmyard manure and reported maturity was reached at a fresh weight of < 1.5 g after 2 months at 15 °C. What role the different food, and the rate at which it was replenished, played in determining the contrasting development rates in these two studies is unknown. In addition, Jensen & Holmstrup (1997) suggested that development rates may vary genetically between field populations of earthworms. Lee (1985) argued that peregrine earthworms that become established in various parts of the world may develop different temperature optima according to local selection pressures. The same may be the case for soil pH preferences. With this in mind, we assessed the temperature and soil pH preferences of A. longa in Australian populations when devising rearing methods for them.

Materials and Methods Effect of soil type

A laboratory experiment was run to determine if there was likely to be an advantage, in the short term, in rearing A. longa in soils collected directly from the field Pedobiologia (2003) 47, 745–753

(beneath pastures) compared with commercially blended sandy loams (as available from garden centres). Soil types used included 1) loam : sand (50 : 50) + peat (pH in CaCl2 = 4.23), 2) sand : loam (80 : 20) (pH = 7.01), 3) yellow clay loam (Alfisol) (pH = 6.57), and 4) red-brown earth (Alfisol) (pH = 4.76). The first two soils were supplied commercially; the latter two were collected from the University of Adelaide, Waite Campus, South Australia. The soils were added to 2.2 L plastic flower pots and maintained at a constant temperature (15 °C) in a dark room. For each soil type, the equivalents of either 2 kg air dried soil or 1.5 kg air dried soil + 0.5 kg air dried sheep dung (collected from stock paddocks at the Waite Campus) were added to each pot. The dung and soil were mixed evenly. The soil and soil + dung were watered to a gravimetric moisture content of 25 %. There were ten replicate pots for each soil and soil + dung treatment (thus 80 pots). Treatments were randomly arranged on benches. Four large juvenile A. longa were added to each pot, after first being kept on moist filter paper overnight (to void their guts) and weighed. These earthworms were collected originally from beneath a pasture at “Woolnorth” near Smithton in northern Tasmania, but were cultured in moist soil (yellow clay loam) in the laboratory for several months prior to the experiment. The tops of the pots were covered with fine curtain mesh which was secured with elastic bands. Soil moisture was maintained by watering to original weight at weekly intervals. The survival and biomass of the earthworms were measured after 2 months. The earthworms were again kept overnight on moist filter paper before being weighed.

Effect of temperature Large juvenile A. longa, also from “Woolnorth”, were cultured for 8 weeks at 5 constant temperatures (5, 10, 15, 20 and 25 °C) in moist sandy loam available from a commercial garden supplier (40 % river loam, 60 % compost). The survival and biomass of the earthworms were then determined, as above. The earthworms were kept in 2.2 L plastic pots filled with the soil mix, with five worms per pot. There were 5 replicate pots for each treatment. The soil mix was maintained at approximately 25 % gravimetric soil moisture, with weekly watering to initial weight. Sheep dung (50 g) was added on top of the sandy loam in each pot and lucerne straw (25 g) was mixed through. Several hundred cocoons of A. longa were collected from the pasture in northern Tasmania on three separate occasions (early October 1998, mid July 1999, and mid September 1999) and placed in groups of about 50

Soil conditions and the development of Aporrectodea

in small jars (125 ml) containing moist commercial soil mix (see above). The 1998 collection (n = 498 cocoons) was kept in the dark at 15 °C and checked every 1–2 weeks for hatchlings until February 1999. Hatchlings (in groups of 10–15 individuals) were then transferred to larger pots (2.2 L) containing moist commercial soil mix, with an additional 250 ml of sheep dung added to the surface. The hatchlings were reared for a further 15 months. The survival, biomass (fresh weight, gut content included) and state of maturity of the earthworms were assessed 6 weeks and 6, 9, 12 and 15 months after hatching. The soil and dung were replaced at 6 and 12 months. Similarly, the July 1999 collection (n = 278) was maintained in the dark at 15 °C and checked regularly for hatchlings until November 1999. Groups of hatchlings were transferred as before to larger pots when found. The survival, fresh biomass and state of maturity of these earthworms were measured 6 weeks and 6 and 9 months after hatching. The September 1999 collection (n = 1,250) was divided into groups of 50 cocoons and each group was cultured in a separate small jar at one of five constant temperatures (5, 10, 15, 20 and 25 °C). There were five replicate jars for each temperature. Each jar was checked for hatchlings every week until early December, when hatching had seemingly tapered off at 15–25 °C, but had barely begun at 5–10 °C. The culturing at 15–25 °C was then terminated. Two of the pots of cocoons being cultured at 5 and 10 °C were transferred to 15 °C and these were maintained until mid March 2000, when hatching in them too appeared to have ceased. The remaining 3 pots left at the original 5 and 10 °C were further cultured until June 2000. Fifty of the earliest hatchlings emerging at each original temperature setting were transferred to larger pots, in groups of approximately ten worms, and maintained at the same temperatures to which they had already been exposed. The survival, fresh biomass and state of maturity of these hatchlings were measured 6 weeks and 6 months after hatching. Effect of air-drying soil

One hundred cocoons, also collected in Tasmania in September 1999, were placed in moist soil in two small jars and the soil was air-dried in the dark. Fifty cocoons were cultured at 10 °C and fifty at 15 °C. The soil was checked weekly for hatchlings. After 9 weeks, when the soil moisture had reached 4.3 and 3.6 % at 10 and 15 °C respectively, the soil in the jars was remoistened to its original moisture level (25 %), and maintained at that moisture content for another 26 weeks, during which time further checks were made at weekly intervals for hatchlings.

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Effect of soil pH

Five field soils with contrasting textures and chemical characteristics were each amended with varying amounts of lime (nil, 2.5, 5, 7.5 and 10 t ha-1) to create 5 variants of soil pH per soil type. For each soil type, the soil pH variants thus created were placed in pairs of equal volume in replicated plastic boxes (2 L) with mesh lids, in all possible paired combinations. The soils with different pH were separated within each box by a facial tissue. The soils in the boxes were maintained at approximately 25 % soil moisture and 15 °C. The selections of soil pH by A. longa (large juveniles) were recorded one week after the earthworms (n = 6 per box) were added at the interface between the two pH choices. There were five replicate boxes for each soil pH choice offered. The five soils were taken from the top 10 cm of 1) a red-brown earth (Alfisol) at Waite Campus, University of Adelaide, South Australia, 2) a grey clay (Vertisol) at the CSIRO Experiment Station at Ginninderra, Australian Capital Territory, 3) a red earth (Ultisol) at Neville, New South Wales, 4) a solodic soil (Alfisol) at Oolong, New South Wales, and 5) a brown alluvial soil (Entisol) at Cooma, New South Wales. After mixing in the lime, the soils were kept moist and allowed to equilibrate for 2–3 months before running the choice experiments. Soil pH (in CaCl2) was measured for two replicate samples taken from each pH regime using a PHM92 Lab pH meter (Radiometer, Copenhagen). The five pH variants established for the grey clay from Ginninderra (see above; pH range = 4.1–6.7) were also used to measure the influence of soil pH on growth of A. longa. Large juvenile earthworms were added to plastic pots (2.2 L) containing one of the pH variants of the grey clay. There were ten replicate pots for each soil pH. Five earthworms were added to each pot. Additional food (50 g sheep dung and 25 g finely chopped lucerne straw) was added on top (dung) or mixed through (straw) the soil in each pot. The soil mix was maintained at approximately 25 % moisture and kept at 15 °C. Earthworms were weighed (after voiding gut contents) at the start of the experiments and again after rearing for 8 weeks.

Results Effect of soil type

There were no differences in initial biomass of earthworms as allotted to the various treatments (One Way ANOVA, F = 1.51, P > 0.05, mean biomass of individ– ± S.E.) nor in ual earthworms overall = 0.96 ± 0.02 g, × Pedobiologia (2003) 47, 745–753

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the survival across all eight treatments (F = 1.99, P > 0.05, overall = 90.9%). Final biomass of the earthworms was lower in the loam/sand/peat mix than in the other three soil types, but only in the presence of dung (One way ANOVA across all eight treatments, F = 37.86, P < 0.001) (Fig. 1). The addition of dung increased biomass. Without the addition of dung, earthworms lost biomass (mean final biomass of individual earthworms = 0.78 ± 0.03, F = 19.26, P < 0.001). No adult earthworms were recovered in pots without dung. Adult earthworms were found in 17 pots with dung (2 in the loam/sand/peat mix, 4 in the sand/loam mix, 5 in the yellow clay loam and 6 in the red-brown earth). Cocoons were found in two pots (one pot each for the yellow clay loam and the red-brown earth, each with dung). Effect of temperature

Nearly all earthworms survived at 5–20 °C (93 %), whilst 80 % died at 25 °C. There were no differences in initial biomass of earthworms across all treatments (F = 1.86, P > 0.05, mean biomass of individual earthworms overall = 1.41± 0.03 g). There was also no difference in final biomass of individual earthworms at 5–20° C (F = 0.67, P > 0.05, mean biomass of individual earthworms = 1.55 ± 0.08 g), but the few (5) earthworms that survived at 25 °C were substantially smaller (0.78 ± 0.04 g). All were in just one pot. Most of the cocoons collected in early October 1998 hatched by the end of December 1998 (Fig. 2), assuming one hatchling/cocoon (Butt 1993 reported > 1 hatchling/cocoon was negligible for A. longa). Overall, 99.0 % hatched by early February 1999. Sur-

vival of these hatchlings to 6 weeks and 6, 9, 12 and 15 months was 99.0, 98.9, 96.1, 94.7 and 94.5 % respectively. Adult earthworms were first found at 12 months (14.4 % of those being reared) and more had matured at 15 months (35.6 %). The average biomass per earthworm was 0.08, 0.41, 1.00, 1.33 and 1.55 g at 6 weeks and 6, 9, 12 and 15 months respectively. The average biomass per adult earthworm at 15 months was 2.03 g (range = 1.35–3.47 g). There was no evidence to suggest the time of hatching affected subsequent growth or level of maturity (data not presented here). Most of the cocoons collected in mid July 1999 hatched by early October 1999, with 93.9 % hatched by mid November 1999 (Fig. 2). Survivals of these hatchlings to 6 weeks and 6 and 9 months were 96.6, 96.6 and 95.8 % respectively. Adult earthworms were only found at 9 months (33.2 %). The average biomass per earthworm was 0.15, 0.78 and 1.56 g at 6 weeks, and 6 and 9 months respectively. The average biomass per adult earthworm at 9 months was 2.21 g (range = 1.48–3.22 g). Again, there was no evidence to suggest the time of hatching influenced subsequent growth or level of maturity. The hatching of cocoons collected in mid September 1999 varied with temperature (Fig. 3). Most cocoons cultured at 15–25 °C had hatched by early November 1999, with those maintained at 20 °C hatching quickest. Fewer cocoons hatched at 25 °C (46.0 % by early December), compared with 15 °C (87.2 %) and 20 °C (73.6 %). Hatching at 5 and 10 °C was much slower than at the higher temperatures, but comparable in success to that observed at 15 and 20 °C (94.0 % at 5 °C and 84.0 % at 10 °C by June 2000). Moving cocoons from 5 and 10 °C to 15 °C hastened their hatch-

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Fig. 1. Average final biomass worm-1 (g) for Aporrectodea longa reared in loam/sand/peat commercial mix (P), sand/loam commercial mix (SL), yellow clay loam (YCL) and red-brown earth (RBE). D indicates addition of sheep dung. Different letters above each histogram indicate significant differences (P < 0.05) between treatments.

Soil conditions and the development of Aporrectodea

ing. Hatching of cocoons collected in July 1999 was slower than that observed for collections made in October 1998 and September 1999 (Fig. 2). Notably, the cocoons collected in July 1999, unlike those collected on the other two occasions, were virtually all a bright yellow in colour, indicative of being freshly laid. Survival of the hatchlings was high at 5–15 °C (96–100 % after 6 months), moderate at 20 °C (78 % after 6 months), but very low at 25 °C, with only ten individuals surviving to 6 weeks and two to 6 months at the highest temperature. The biomass per earthworm was greatest at 20 °C (Data transformed to log10 for analyses: F = 201.8, P < 0.001 at 6 weeks; F = 181.3, P < 0.001 at 6 months) (Fig. 4). Adult earthworms were only found in the 20 °C treatment, at 6 months (28.2 % of the survivors). The average biomass per adult earthworm was 1.75 g (range = 1.48-2.21 g).

Effect of air-drying soil

Six of the cocoons that were air-dried at 10° C, but none of those at 15° C, hatched when the soil was remoistened. Effect of soil pH

Every soil pH regime had an equal opportunity to be selected by A. longa. The worms showed a strong aversion to soil pH below 4.5, little discrimination between 4.5 and 7.0, and a slight aversion to soils above 7.0 (Multinomial test, X2 = 180.13, P < 0.001) (Fig. 5). There were no differences in the initial biomass of the earthworms added to each variant of soil pH for the grey clay from Ginninderra (F = 0.65, P > 0.05, mean biomass of individual earthworms = 1.37 ± 0.02 g). Fig. 2. Cumulative percentage of cocoons hatched through time when reared at 15° C in the laboratory following collections in northern Tasmania in early October 1998, mid July 1999 and mid September 1999

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Fig. 4. Average biomass per earthworm-1 (g) for Aporrectodea longa reared in the laboratory at various temperatures for 6 weeks and 6 months. Different letters above each histogram indicate significant differences (P < 0.05) between treatments within the one time interval

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There were also no differences in final biomass (F = 1.48, P > 0.05, mean biomass = 1.77 ± 0.03 g). Virtually all the earthworms survived (96.0 %).

Discussion The results of this study suggested commercially available sand: loam mixes can be as useful for rearing A. longa as field collected soils. The addition of peat may reduce the performance of A. longa and perhaps should be avoided. Transport of A. longa in moist peat Pedobiologia (2003) 47, 745–753

(c.f. Sphagnum moss) has been unsuccessful (G. Baker, unpublished data), perhaps because of greater acidity of the former substrate. Similar results to those reported here for evaluating soil types under a constant temperature regime have been obtained in a glasshouse in which temperature varied, but was not allowed to exceed 25 °C (G. Baker, unpublished data). The hatching of A. longa cocoons from Tasmania was generally high (> 70 %), except for those cocoons cultured at 25 °C. This contrasts with lower levels reported by Butt (1993) (< 70 %), Holmstrup et al. (1996) (35 %) and Pedersen & Bjerre (1991) (25 %). Holmstrup et al. (1996) commented that this low co-

Soil conditions and the development of Aporrectodea

coon viability in A. longa may be an artefact of culturing because they had observed high (90 %) hatchability in field collected cocoons. The poor survival of A. longa worms and cocoons at 25 °C in the present study is in agreement with the lethal temperature limit determined by Miles (1963). Holmstrup et al. (1996) measured incubation time for cocoons of A. longa at 10, 15 and 20 °C, and found it was inversely related with temperature (means of 125, 69 and 50 days respectively, which is comparable with data provided by Butt 1993). Holmstrup (1999) recorded faster incubation rates for A. longa cocoons (e.g. 54 d at 15 °C). In the present study, the hatching of cocoons varied with time of collection as well as inversely with temperature. The cocoons collected in September and October would most probably have been deposited in the soil over a longer period of time than those collected in July, which is close to the likely start of A. longa’s breeding season in northern Tasmania. Only very limited data are available to indicate when A. longa deposits cocoons in the soil in Tasmania (Lobry de Bruyn & Mele 1996), but other Aporrectodea spp. do so from about July onwards elsewhere in southern Australia, following autumn and early winter rains (e.g. Baker et al. 1992). It is reasonable to assume this is also the case for A. longa. Given this, it is likely that the incubation times recorded here for the July cocoon collection are more accurate than those obtained later in the year. Later collections will probably include a greater proportion of older cocoons and thus are likely to provide underestimates. The average incubation time for cocoons collected in July and cultured at 15° C was approximately 10 weeks. This corresponds closely with the data provided by Butt (1993) and Holmstrup et al. (1996) for laboratory reared cocoons. The optimum temperature range for culturing cocoons from Tasmania was 15–20 °C (slightly higher viability at 15 °C; slightly faster development at 20 °C). Optimal growth of hatchlings occurred at 20 °C. These findings are close to Butt’s (1993) recommendation of 15 °C for rearing A. longa, but differ from the optimum of 10–12 °C suggested by Nordstrum (1975). Daugbjerg (1988) found that A. longa preferred 10–15 °C in choice tests. We measured the time taken for hatchlings to develop to adults on three occasions. Adults were first recorded at 9 months from hatching when reared at 15 °C and 6 months at 20 °C. Minimum fresh biomass for an adult was 1.35 g. These development times were substantially greater than those reported by LofsHolmin (1982), Butt (1993) and Lowe & Butt (2002). The biomass of adults, however, was comparable with that recorded by Lofs-Holmin (1982), but much less than that reported by Butt (1993). Variations in food

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availability/quality and degree of crowding in culture may help explain these differences. Soil temperature and moisture data are unavailable for “Woolnorth”, but soil temperatures recorded near Elliott, northern Tasmania, which has a slightly cooler and wetter climate than “Woolnorth”, average 8.6 °C (at 10 cm depth) from July to October (i.e. less than optimum for cocoon and earthworm development). Soil temperatures peak at 17.6 °C in February, which seems close to optimum for A. longa. Evaporation exceeds rainfall from November to March at Elliott and this is likely to also be the case at “Woolnorth”. At “Woolnorth”, the soil noticeably dries out in November after vigorous pasture growth in spring. Earthworms then become hard to find near the soil surface as they retreat deeper down the profile to aestivate. Critical soil moisture levels for survival of A. longa cocoons and hatchlings are not known, but the preliminary studies reported here suggest that most cocoons do not tolerate air-drying of soil. It thus seems likely that only those cocoons produced early in the breeding season at “Woolnorth” would hatch and survive before surface soils dry out in late spring. An estimate of 15–20 weeks incubation time for cocoons at “Woolnorth” (at approximately 10° C soil temperature) is not unreasonable given data from this study and provided in Holmstrup et al. (1966) and Holmstrup (1999). Whilst A. longa clearly flourishes at “Woolnorth” (densities of 146 worms m-2 have been recorded there under dung pats) (Baker et al. 2002), it may not cope so well at some other sites in southern Australia where soils dry out more quickly in spring and less time is available for cocoon development. For example, A. longa has been introduced to pastures near Orange in New South Wales but failed to establish there. Although annual rainfall at Orange is similar to that at “Woolnorth” (approximately 1,000 mm year-1), evaporation greatly exceeds rainfall in both April and October at the NSW site (i.e. a month later in autumn and a month earlier in spring than in northern Tasmania). More research is needed to elucidate the climatic factors controlling cocoon and hatchling survival in spring and summer and hence the critical length of the recruitment “season” for A. longa. Such research, put in context with information on local soil properties and agricultural management practices that impinge on soil microclimates, would help refine predictions of A. longa’s potential distribution in Australia (Baker 1998b). Lee (1959) reported that A. longa cocoons survived “dry” summers in New Zealand to hatch successfully in autumn with the onset of rain. This result is somewhat surprising in view of the observation reported here of poor survival of A. longa cocoons following air-drying, but Lobry de Bruyn & Mele (1996) Pedobiologia (2003) 47, 745–753

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provided data showing that small numbers of A. longa cocoons can be found in summer at “Woolnorth” (viability was, however, not reported). Perhaps some cocoons do survive at “Woolnorth” to hatch early in the next autumn when soils again become moist. Prolonged survival of cocoons through dry summers has been reported for some earthworms (e.g. Microscolex dubius) (Doube & Auhl 1998). The results of the present study suggest that very acidic soils should be avoided when rearing A. longa and that A. longa may not establish in such soils in the field, unless they are first ameliorated with lime. The avoidance of soil pH lower than 4.5 matches well with previous studies in Europe and conforms with inoculation successes thus far in Australia. Acknowledgements.This work was funded by the Land and Water Resources Research & Development Corporation. We wish to thank staff of the Australian Bureau of Meteorology for providing climatic data.

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