Growth Rates of Aporrectodea Caliginosa (Oligochaetae: Lumbricidae) As Inﬂuenced by Soil Temperature and Moisture in Disturbed and Undisturbed Soil Columns

ARTICLE IN PRESS

Pedobiologia 50 (2006) 207—215

www.elsevier.de/pedobi

Growth rates of Aporrectodea caliginosa (Oligochaetae: Lumbricidae) as inﬂuenced by soil temperature and moisture in disturbed and undisturbed soil columns

Nikita S. Eriksen-Hamel, Joann K. WhalenÃ

Department of Natural Resource Sciences, Macdonald Campus, McGill University, 21,111 Lakeshore Road, Ste-Anne-de-Bellevue, Quebec, H9X 3V9, Canada

Received 8 May 2005; accepted 26 October 2005

KEYWORDS Summary Earthworms; Earthworm growth is affected by fluctuations in soil temperature and moisture and Aporrectodea hence, may be used as an indicator of earthworm activity under field conditions. caliginosa; There is no standard methodology for measuring earthworm growth and results Instantaneous obtained in the laboratory with a variety of food sources, soil quantities and growth rate; container shapes cannot easily be compared or used to estimate earthworm growth Temperature; in the field. The objective of this experiment was to determine growth rates of the Moisture; endogeic earthworm Aporrectodea caliginosa (Savigny) over a range of temperatures Container shape (5–20 1C) and soil water potentials (5to54 kPa) in disturbed and undisturbed soil columns in the laboratory. We used PVC cores (6 cm diameter, 15 cm height) containing undisturbed and disturbed soil, and 1 l cylindrical pots (11 cm diameter, 14 cm height) with disturbed soil. All containers contained about 500 g of moist soil. The growth rates of juvenile A. caliginosa were determined after 14–28 days. The instantaneous growth rate (IGR) was affected significantly by soil moisture, temperature, and the temperature moisture interaction, ranging from 0.092 to 0.037 d1. Optimum growth conditions for A. caliginosa were at 20 1C and 5kPa water potential, and they lost weight when the soil water potential was 54 kPa for all temperatures and also when the temperature was 5 1C for all water potentials. Growth rates were significantly greater in pots than in cores, but the growth rates of earthworms in cores with undisturbed or disturbed soil did not differ significantly. The feeding and burrowing habits of earthworms should be considered when

ÃCorresponding author. Tel.: +1 514 398 7943; fax: +1 514 398 7990. E-mail address: [email protected] (J.K. Whalen).

208 N.S. Eriksen-Hamel, J.K. Whalen

Introduction of soil in containers with volumes ranging from 0.12 to 2.2 l (Butt et al., 1994; Whalen and Parmelee, Earthworms are known to accelerate nutrient 1999; Baker and Whitby, 2003). In these studies, mineralization and improve soil fertility in tempe- loose soil was packed or placed into the container rate agroecosystems (Lee, 1985; Edwards and before earthworms were added. Bohlen, 1996). The contribution of various earth- We hypothesize that earthworm growth rates will worm species to nutrient mineralization is affected differ when earthworms are grown in disturbed soil by their feeding habits and life-history strategies, than in undisturbed soil. An undisturbed soil core because individuals from different ecological obtained from the field will likely contain some groups are active in different parts of the burrows and macropores that facilitate earthworm soil profile when environmental conditions are movement and reduce their energy expenditure in favourable (Bouche´, 1977; Brown et al., 2004). moving through soil, thereby increasing growth Furthermore, earthworm-mediated nutrient miner- rates. Containers may constrain earthworm move- alization may be related to their activity and ment, reducing the energy used to burrow and growth (Marinissen and de Ruiter, 1993). Earthworm increasing the energy allocated for growth. Whalen growth rates are very responsive to fluctuations in and Parmelee (1999) reported that growth rates of soil temperature and moisture, and may be used to Aporrectodea tuberculata (Eisen) were similar in estimate activity and dynamics of earthworm 0.12 l laboratory pots and 7.9 l field cores, but populations (Buckerfield et al., 1997). In temperate juvenile Lumbricus terrestris L. had slower growth agricultural soils, earthworm growth is fastest at rates in field cores than in laboratory cultures. The soil temperatures from 15–20 1C when the soil amount of soil and shape of the culture vessel used moisture is close to field capacity (Daniel in laboratory studies should provide growth data et al., 1996; Holmstrup, 2001; Wever et al., 2001; that is representative of earthworm activity under Baker and Whitby, 2003). However, soil tempera- field conditions. tures range from about 0–25 1C and there may be The objectives of our experiment were: (1) to periodic flooding and drought during the crop determine how growth rates of Aporrectodea growing season. Researchers wishing to estimate caliginosa were influenced by soil temperature nutrient mineralization from earthworms require and moisture; and (2) to determine whether detailed information on how earthworm growth earthworm growth rates were influenced by soil rates fluctuate with changing soil temperature and disturbance and culture vessel shape. moisture conditions. There is no standard methodology for measuring earthworm growth rates. A review of the literature reveals that growth rates for the major lumbricid Materials and methods earthworm species have been determined using a variety of food sources, amounts of soil and Collection of earthworms and soils containers (Butt, 1997; Fayolle et al., 1997; Whalen and Parmelee, 1999; Booth et al., 2000). When Juvenile individuals of A. caliginosa were col- provided with abundant organic matter with a high lected by hand sorting in September 2003 from N content, earthworms grow faster than when they fields under alfalfa (Medicago sativa L.) and receive a restricted amount of food or one with a soybean (Glycine max (L.) Merrill) production at low N content (Bostro¨m and Lofs-Holmin, 1986; the Macdonald Campus Farm of McGill University, Bostro¨m 1988; Daniel, 1991). Many earthworms Ste-Anne-de-Bellevue, Que´., Canada. Earthworms grow faster when they consume finely ground than were reared for about 6 weeks at room tempera- coarsely ground organic substrates (Bostro¨m and ture (20 1C) in soil from the field site, moistened to Lofs-Holmin, 1986; Lowe and Butt, 2003). Little is near field capacity. Newly emerged earthworms known of the relationships between the amounts of (o0.25 g) and pre-clitellite earthworms (40.70 g) soil or the shape of the culture vessel may have on were excluded from the analysis as their earthworm growth rates. Growth rates have been growth rates may not be truly representative of measured commonly in the laboratory in 40–2000 g juvenile earthworms. Yet, fewer than 20% of the ARTICLE IN PRESS

Earthworm growth rates in soil columns 209 earthworms in this study were excluded from the 24 h. The next day the earthworms were washed, analysis due to being smaller or larger than the gently blotted dry with paper towels and weighed desired size range (0.25–0.70 g). (gut-free fresh weight). One earthworm was added The soil was a sandy-loam mixed, frigid Typic to each pot, which was then sprayed with approxi- Endoquent of the Chicot series taken from a ﬁeld mately 3 ml water to remoisten the earthworm and under soybean production. It had a pH (H2O) of 6.3, soil surface. Pots were placed into controlled a C content of 30.2 g C kg1, and contained climate incubators at four temperatures in dark- 580 g kg1 sand, 300 g kg1 silt and 120 g kg1 clay. ness for the duration of the experiment. Soils were air-dried to about 10% gravimetric Earthworms were reared in pots for 8 weeks and moisture content (200 kPa matric potential) be- were removed every 13–15 days for weight mea- fore use. The earthworm food was composted surements. At each weighing, earthworms were cattle manure containing about 383 g C kg1 and washed, placed on a moistened paper to void their 19.9 g N kg1 (Carlo Erba Flash NC Soils Analyzer, guts for 24 h, weighed (gut-free fresh weight) and Milan, Italy). then returned to the same pot for 13–15 days. Washing and keeping the earthworms on a moistened paper for 24 h insures that the earthworms Calculation of soil moisture content from different soil moisture treatments have equal hydration status when weighed. Before returning Four soil gravimetric moisture contents (15%, earthworms to the pots, about 1 g (dry matter 20%, 25%, and 30%) were used to test earthworm basis) of manure was added to the soil surface, pots growth in response to moisture conditions. Since were weighed and tap water was added to replace matric potential is a more meaningful way to moisture lost through evaporation. When dead express biological water availability, we converted earthworms were found, they were removed and the gravimetric moisture content to matric poten- a replacement earthworm of similar weight and age tial using the Rosetta software program (Schaap, class was added to the pot. The growth rates for 2000). A SSCBD (texture and bulk density) pedo- replacement earthworms were considered to be transfer function was used to predict the para- missing values in the statistical analysis. meters necessary for calculating matric potential using the van Genuchten function for water retention (van Genuchten, 1980; Schaap et al., Core experiment 1998). The calculated matric potentials (7stan- dard deviation, S.D.) were 5(71), 11 (72), The experiment was designed as a completely 23 (74), 54 (714) kPa, corresponding to 30%, randomised factorial design with three tempera- 25%, 20%, and 15% gravimetric moisture content, tures (10, 15 and 20 1C), three soil water potentials respectively. (5, 11 and 23 kPa), and two soil disturbance treatments (undisturbed and disturbed) with eight Pot experiment replicates of each treatment. Each replicate core was soil in a PVC plastic tube with an internal This experiment involved a completely rando- diameter of 6 cm, a height of 15 cm and a volume of mised factorial design with four temperatures 0.425 l. Disturbed soil cores contained sieved (5, 10, 15, and 20 1C), and four soil water potentials (o10 mm mesh) soil that was packed to a bulk (5, 11, 23, and 54 kPa), for a total of 16 density of 1.2370.01 g cm3 (S.E.) (n ¼ 72), equi- factorial treatments. Each treatment was repli- valent to the bulk density found in the undisturbed cated 10 times. Each replicate pot was a 1-l cores. This was achieved by gently pounding the cylindrical plastic pot (11 cm diameter, 14 cm core on the lab bench until the desired bulk density height) with a perforated lid containing 400–480 g was achieved. Undisturbed soil cores, taken from of air dry soil (sieved o10 mm mesh, 500 g of moist the same ﬁeld site, were obtained by hammering soil), and 3 g (dry matter basis) of manure (sieved the PVC tube into the ground above a visible o4 mm mesh). The manure was mixed into the top earthworm burrow and digging out the core. Fine 5 cm of the soil where endogeic earthworms plastic mesh (1.5 mm) was secured with elastic typically consume their food. The food and soil bands on both ends of the core to prevent soil mixture was incubated for 2–5 days before adding losses. Undisturbed soil cores were kept in a cold the earthworm. room at 0 1C for 6 weeks to kill any earthworms that Juvenile earthworms with a mean mass of may have been collected in the core. Each core 0.3570.11 g (S.D.) (n ¼ 1028) were washed and contained between 300 and 425 g of air dry soil placed on moistened paper to void their guts for (400–600 g of moist soil after adding different ARTICLE IN PRESS

210 N.S. Eriksen-Hamel, J.K. Whalen amounts of tap water based on the moisture Statistical analysis treatments). Juvenile earthworms were washed and placed on The effect of temperature, moisture, container moistened paper to void their guts for 24 h, then type, sampling time and the temperature mois- removed, washed, gently blotted dry with paper ture interaction on earthworm growth rates from towels and weighed (gut-free fresh weight). Earth- the pot and core study were evaluated using the worms added to the undisturbed and disturbed soil PROC MIXED function of SAS software (SAS Institute, cores had a mean gut-free fresh biomass of 2001). The MIXED procedure uses generalized least 0.4370.14 g (S.D.) (n ¼ 59), and 0.3870.11 g squares to estimate and test for fixed effects in the (S.D.) (n ¼ 61), respectively. One earthworm was model, which is superior to the ordinary least added per core, and 5 g dry matter of manure was squares used by the GLM procedure, and is the placed on the soil surface. The surface of the soil in preferred method for analysis of animal growth each core was sprayed with approximately 3 ml experiments with repeated measures data since it water to remoisten the earthworm and soil surface. can handle missing data in an unbalanced design Cores were placed in controlled climate incubators (Wang and Goonewardene, 2004; Spilke et al., in darkness for 28 days, then earthworms were 2005). The difference between least square means removed from each core, placed on a moistened of significant treatment effects were evaluated at paper to void their guts for 24 h, and their gut-free the 95% confidence level using the LSMEANS fresh weights determined. Replicates with dead statement in SAS. Regression lines were fitted using earthworms were excluded from the statistical the PROC REG function of SAS. analysis.

Calculation of earthworm growth rates Results Earthworm growth rates are commonly reported as either average growth rates or relative growth Mortality rates, and while these measurements may be useful for laboratory experiments in which the growth of Earthworm mortality in the pot study was an age-specific cohort is followed to maturity, they generally less than 8%, although in soils at assume that earthworm growth through time is a 54 kPa water potential there was up to 26% continuous linear function (Whalen, 1998). It has mortality. In the core study, mortality ranged from been well established that earthworm growth 0–28.5%, and was not different in the intact and through time follows a logistic curve (Phillipson packed cores. and Bolton, 1977; Daniel et al., 1996). As an earthworm approaches maturity, a greater propor- tion of the energy from food resources is likely used Temperature and moisture effects on in the formation of sexual organs and reproduction earthworm growth rather than the formation of new tissues (Daniel et al., 1996). Instantaneous growth rates (IGR, d1), In the pot study, soil temperature (F ¼ 26:1, which assume that growth proceeds logistically Po0:0001), moisture (F ¼ 23:8, Po0:0001) and the rather than linearly, are better able to account for interactions between temperature and moisture these factors by calculating the change in an (F ¼ 4:1, Po0:0001) were all significant factors individual’s growth during an infinitely short time affecting growth. Growth rates were significantly interval (Pertrusewicz and Macfayden, 1970; Diehl affected (F ¼ 4:8, Po0:003) by the repeated and Audo, 1995). The IGR was calculated using the weight measurements on the same individual. This equation, indicates a change in growth rate as the individual earthworm grows. The change in growth rates as an ¼ ð Þ IGR ln Wf=W i =Dt, (1) individual changes in weight is a common relation- where Wi and Wf are initial and final earthworm ship in many earthworm and animal growth studies mass (g), respectively, and Dt is the growth interval (McElroy et al., 1997; Mir et al., 1998; Wang and measured in days (Brafield and Llewellyn, 1982). Goonewardene, 2004). All earthworms lost weight The IGR was calculated for 14- and 28-day growth when placed in soil with a water potential of intervals in the pot study, and for a 28-day interval 54 kPa, so the growth data for this treatment in the core study. The effects of container shape on were excluded from Fig. 1. Growth was negative earthworm growth were assessed using the IGR (indicating weight loss) at 5 1C, regardless of the calculated for a 28-day growth interval. moisture content, and at 10 1C when the soil water ARTICLE IN PRESS

Earthworm growth rates in soil columns 211

0.012 10 °C G 0.012 0.010 F F 0.008 0.008 0.006 ) ) EF -1

-1 DE 0.004 0.004 CD CD 0.002 BCD BC 0.000 IGR(d 0.000 IGR (d A A AB -0.002 -0.004 -0.004 -0.008 -0.006 0 5 10 15 20 25 30 35 40 45 50 55 5101520 Moisture (-kPa) ° Temperature ( C) 15 °C 0.012 -23 kPa -11 kPa -5kPa 0.008 )

Figure 1. Inﬂuences of soil temperature and moisture on -1 0.004 the instantaneous growth rate (IGR) of A. caliginosa in 7 0.000

pots. Values are shown as mean S.E. (n ¼ 10). Columns IGR (d with the same letters did not differ significantly -0.004 (Po0:05). -0.008 0 5 10 15 20 25 30 35 40 45 50 55 Moisture (-kPa) potential was 11 and 23 kPa (Fig. 1). The IGR 20 °C 0.012 was greatest at 5 and 11 kPa water potential. 0.008 ) Effects of container on growth -1 0.004 0.000 IGR (d In the core study, soil moisture (F ¼ 63:0, -0.004 P 0:0001) was the most significant factor affecting o -0.008 growth, followed by soil temperature (F ¼ 34:3, 0 5 10 15 20 25 30 35 40 45 50 55 Po0:0001), the interactions between temperature Moisture (-kPa) and moisture (F ¼ 10:7, Po0:0001) and container ●■pot disturbed soil core ▲ undisturbed soil type (F ¼ 4:9, Po0:008). A paired means comparison test showed that growth rates in the pot study Figure 2. Effects of container type, soil temperature and were greater than in disturbed soil cores soil water potential on the instantaneous growth rate (P ¼ 0:017) and undisturbed soil cores (P ¼ 0:006). (IGR) of A. caliginosa. Values are shown as mean7S.E. However, the growth rates obtained from undisturbed and disturbed soil cores were not significantly different. cally with rising water potential when the soil In soils at 10 1C, earthworm growth rates were temperature was 10–20 1C, but growth remained positive at water potentials greater than 11 kPa negative at 5 1C for all water potentials. Growth (Fig. 2A). In soils at 15 and 20 1C, positive growth rates were significantly greater at 5 kPa than at rates were observed at dryer conditions in pots 11 kPa when the soil temperature was 10–20 1C, (23 kPa) than cores (11 to 15 kPa) (Fig. 2B and but were not different between water potentials of C). Logistic growth describes best earthworm 11 and 23 kPa for temperatures between 5 and growth in pots at all three temperatures, whereas 15 1C. In other experiments soil temperature and earthworm growth in disturbed and undisturbed moisture interacted significantly to influence the cores were described best by linear equations at growth of A. tuberculata (Wever et al., 2001) and 10 1C, and both linear and logistic equations at L. terrestris (Berry and Jordan, 2001). They found 15 1C and 20 1C(Table 1). that earthworm growth rates were influenced more by soil moisture at higher temperatures (20 1Cor higher) than at lower temperatures. In our study, Discussion earthworms lost weight when the soil water potential was lower than 11 kPa at 10 1C, and The rates of growth of A. caliginosa were 23 kPa at 15 and 20 1C, suggesting that there may influenced by interactions between soil tempera- be critical moisture levels for earthworm growth. ture and moisture. Growth rates increased logisti- Holmstrup (2001) reported a significant reduction ARTICLE IN PRESS

212 N.S. Eriksen-Hamel, J.K. Whalen

Table 1. Regression equations describing the instantaneous growth rate (IGR) for A. caliginosa as a function of soil water potential (c) for each container type and soil temperature conditions presented in Fig. 2

10 1C Pot IGR ¼0.0042 Ln(c)+0.011 R2 ¼ 0:986 Disturbed core IGR ¼0.0002c+0.0029 R2 ¼ 0:989 Undisturbed core IGR ¼0.0004c+0.004 R2 ¼ 0:940 15 1C Pot IGR ¼0.0034Ln(c)+0.0118 R2 ¼ 0:991 Disturbed core IGR ¼0.0001c+0.0024 R2 ¼ 0:953 Undisturbed core IGR ¼0.0073Ln(c)+0.0195 R2 ¼ 0:958 20 1C Pot IGR ¼0.007Ln(c)+0.022 R2 ¼ 0:967 Disturbed core IGR ¼0.0079Ln(c)+0.0218 R2 ¼ 0:997 Undisturbed core IGR ¼0.0007c+0.0123 R2 ¼ 0:985

Lines were ﬁtted through the average IGR values at each water potential.

in weight of adult and juvenile A. caliginosa when reported that the IGR of Nicodrilus caliginosus the water potential was lower than 12 and (a variant name for A. caliginosa, Reynolds 19 kPa, respectively. At water potentials lower (1977)) was 0.019–0.028 d1 at 15–20 1C and than 19 kPa, all juveniles entered diapause and optimal soil moisture, while earthworms lost lost weight. Similar results were obtained for other weight at temperatures below 12 1C, similar to species in laboratory studies. A. trapezoides our ﬁndings. avoided soil with a water potential less than Differences in the IGR of A. caliginosa in these 15 kPa in sandy loam and 25 kPa in loam (Doube studies may be explained by the initial body mass of and Styan, 1996), and A. longa lost weight at water the earthworm. Earthworm growth rates are potentials lower than 40 kPa (Kretzchmar and related inversely to their initial body masses, Bruchou, 1991). where rates of weight gain decrease as the initial The earthworm growth rates in this experiment body masses of earthworms increase (Daniel et al., ranged from 0.092 to 0.037 d1, and were slightly 1996; Whalen and Parmelee, 1999). Mazantseva slower than those reported elsewhere (Whalen and (1982) showed that the IGR was 50% less for 20–30- Parmelee, 1999; Booth et al., 2000). The growth day-old earthworms than for newly emerged earth- rates for A. tuberculata (Whalen and Parmelee, worms. The earthworms used in many previous 1999) were 2–3 times faster (0.0108–0.0167 d1) studies were smaller than those used in this study, than those in this experiment at 10 1C and water which may explain why they reported faster growth potentials from 5to23 kPa. The growth rates rates for A. caliginosa. for A. tuberculata (Wever et al., 2001) ranged from Other factors that may affect growth rates are 0.05 to 0.05 d1 at 20 1C and from 0.007 to the quantity of soil, shape of the container and 0.015 d1 at 15 1C in soils with moisture contents of ﬂuctuating temperature regimes. Some researchers 10–25%. These results agree with our values kept earthworms in 40 g (Whalen and Parmelee, obtained at similar moisture contents (water 1999) and 100 g of soil (Wever et al., 2001), which is potentials from 11 to 23 kPa). Booth et al. 10–25 times less than the quantity used in other (2000) measured growth rates for A. caliginosa over experiments (Booth et al., 2000). We demonstrated the same range of gravimetric moistures (15–30%) that growth rates of earthworms in pots were and temperatures (5–20 1C) as we did, but with greater than those of earthworms in soil cores. It is more variability in their experiment. In their important to consider the behaviour of earthworms experiment, optimal conditions for earthworm when selecting a container for measuring earth- growth were at 10–15 1C in soils with 25–30% worm growth rates. The soil cores had half the moisture content, and the IGR ranged from diameter of the pots, which may have forced the 0.026–0.063 d1. Earthworms lost weight when earthworms to burrow vertically, contrary to the the soil moisture was 15%, regardless of tempera- natural habits of this endogeic species to build ture (Booth et al., 2000). Mazantseva (1982) temporary, shallow horizontal burrows (Francis ARTICLE IN PRESS

Earthworm growth rates in soil columns 213 et al., 2001; Je´gou et al. 2001). Uvarov (1995) tested, but the upper limit for survival of many showed that earthworms kept in cultures at a lumbricid species is around 25 1C, because many constant temperature (15 1C) lost more weight than life history parameters, such as growth rates, those kept in cultures at a fluctuating temperature cocoon production, and time to reach sexual regime (10–20 1C). However, the effects of differ- maturity, decrease at temperatures above 20 1C ent fluctuating temperature regimes on weight loss (Butt, 1991; Daniel et al., 1996; Berry and Jordan, were not significant until after 4 months in culture 2001; Baker and Whitby, 2003). Furthermore, we (Uvarov, 1995). Since our earthworms were kept for showed that earthworm growth rates were influ- only 8 weeks in controlled climate incubators, we enced by the shape of the container used. Further assume that there was no effect of a constant work is needed to establish standard experimental temperature regime on growth rates. parameters (i.e., food source, growth interval, The treatment effects of container type are not quantity of soil and shape of container) that ensure entirely due to the shape of the container only. To laboratory measurements of earthworm growth maintain an undisturbed soil it was not possible to rates are representative of those in the field. mix the food into the top 5 cm of the soil as in the pot study. Therefore, the pot and cores have different shapes and placement of food. However, since endogeic earthworms typically consume more Acknowledgements humified organic matter in the mineral horizons of the soil (Edwards and Bohlen, 1996), the placement We would like to thank Jonathan Perreault, of fresh organic matter on the surface would most Barbara Sawicki, Simon Lacombe, Vale´rie Campeau likely have had little effect on available food and Fre´de´ric Leduc for assistance in the laboratory resources. The volume of soil in each container and field collection of earthworms. We also thank was small compared to how much soil an earth- two anonymous reviewers for their careful reading worm could burrow through, therefore regardless of a previous version and their detailed suggestions of where the food was placed it was still easily to improve the quality of this paper. Financial accessible to the earthworm. Visual observations assistance was from Natural Sciences and Engineer- confirmed that earthworms were active throughout ing Research Council (NSERC), and the Fonds the containers and came into contact with the Que´bećois de la Recherche sur la Nature et les surface applied food. We assume that the different Technologies (FQRNT). placement of food in the two container types could be a considered a minor source of error. Soil disturbance did not affect the growth of A. caliginosa because the IGR did not differ References between disturbed and undisturbed soil cores. Since the amounts of soil were similar in both pot Baker, G.H., Whitby, W.A., 2003. Soil pH preferences and and core studies, we suggest that the container the influences of soil type and temperature on the shape influenced earthworm growth more than soil survival and growth of Aporrectodea longa (Lumbrici- disturbance. It appears that the presence of intact dae). Pedobiologia 47, 745–753. Berry, E.C., Jordan, D., 2001. Temperature and soil earthworm burrows and other macropores in moisture content effects on the growth of Lumbricus undisturbed soil cores did not increase A. caliginosa terrestris (Oligochaeta: Lumbricidae) under labora- growth. Capowiez and Belzunces (2001) reported tory conditions. Soil Biol. Biochem. 33, 133–136. that earthworm burrow systems are individual Booth, L.H., Heppelthwaite, V., McGlinchy, A., 2000. The structures, rarely used by other earthworms. They effect of environmental parameters on growth, suggest that abandoned burrows may be recolo- cholinersterase activity and glutathione S-transferase nised only by earthworms from the same ecological activity in the earthworm (Aporrectodea caliginosa). class. The undisturbed soil cores were obtained Biomarkers 5, 46–55. above a surface burrow, most likely created by an Bostro¨m, U., 1988. Growth and cocoon production by the anecic earthworm, and were probably not used by earthworm Aporrectodea caliginosa in soil mixed with the endogeic A. caliginosa species introduced into various plant materials. Pedobiologia 32, 77–80. Bostro¨m, U., Lofs-Holmin, A., 1986. Growth of earth- the core. worms (Allolobophora caliginosa) fed shoots and roots Our study confirms that temperature and moist- of barley, meadow fescue and lucerne. Studies in ure strongly influence earthworm growth rates and relation to particle size, protein, crude fiber content activity. Optimum environmental conditions for and toxicity. Pedobiologia 29, 1–12. growth of A. caliginosa were 20 1C and a water Bouche´, M.B., 1977. Strategies lombriciennes. In: Lohm potential of 5 kPa. Higher temperatures were not U., Persson, T. (Eds.), Soil Organisms as Components of ARTICLE IN PRESS

214 N.S. Eriksen-Hamel, J.K. Whalen

Ecosystems. Ecological Bulletins (Stockholm) 25, assessed through the 3D reconstruction of the burrow 122–132. systems. Geoderma 102, 123–137. Brafield, A.E., Llewellyn, M.J., 1982. Animal Energetics. Kretzchmar, A., Bruchou, C., 1991. Weight response to Blackie and Son Ltd., Glasgow. the soil water potential of the earthworm Aporrecto- Brown, G.G., Edwards, C.A., Brussard, L., 2004. How dea longa. Biol. Fertil. Soils 12, 209–212. earthworms affect plant growth: burrowing into the Lee, K.E., 1985. Earthworms: Their Ecology and Relation- mechanisms. In: Edwards, C.A. (Ed.), Earthworm ships with Land Use. Academic Press, Sydney. Ecology. CRC Press LLC, Boca Raton, FL, pp. 13–50. Lowe, C.N., Butt, K.R., 2003. Influence of food particle Buckerfield, J.C., Lee, K.E., Davoren, C.W., Hannay, size on inter- and intra-specific interactions of J.N., 1997. Earthworms as indicators of sustainable Allolobophora chlorotica (Savigny) and Lumbricus production in dryland cropping in southern Australia. terrestris (L.). Pedobiologia 47, 574–577. Soil Biol. Biochem. 29, 547–554. Marinissen, J.C.Y., de Ruiter, P.C., 1993. Contribution Butt, K., 1991. The effects of temperature on the of earthworms to carbon and nitrogen cycling in intensive production of Lumbricus terrestris (Oligo- agro-ecosystems. Agric. Ecosyst. Environ. 47, chaeta: Lumbricidae). Pedobiologia 35, 257–264. 59–74. Butt, K.R., 1997. Reproduction and growth of the Mazantseva, G.P., 1982. Growth patterns in the earth- earthworm Allolobophora chlorotica (Savingy, 1826) worm Nicodrilus caliginosus (Oligochaeta: Lumbrici- in controlled environments. Pedobiologia 41, 369–374. dae) during the first year of life. Pedobiologia 23, Butt, K.R., Frederickson, J., Morris, R.M., 1994. The life 272–276. cycle of the earthworm Lumbricus terrestris L. McElroy, T.C., Presley, M.L., Diehl, W.J., 1997. Genotypes (Oligochaeta: Lumbricidae) in laboratory culture. of multiple allozyme loci interact with an experi- Eur. J. Soil Biol. 30, 49–54. mental environment to affect growth in juvenile Capowiez, Y., Belzunces, L., 2001. Dynamic study of the earthworms (Eisenia fetida andrei). Comp. Biochem. burrowing behaviour of Aporrectodea nocturna and Physiol. 118, 437–446. Allolobophora chlorotica: interactions between earth- Mir, Z., Mir, P.S., Acharya, S.N., Zaman, M.S., Taylor, worms and spatial avoidance of burrows. Biol. Fertil. W.G., Mears, G.W., McAllister, T.A., Goonewardene, Soils 33, 310–316. L.A., 1998. Comparison of alfalfa and fenugreek Daniel, O., 1991. Leaf-litter consumption and assimila- (Trigonella foenum graecum) silages supplemented tion by juveniles of Lumbricus terrestris L. (Oligo- with barley grain on performance of growing steers. chaeta, Lumbricidae) under different environmental Can. J. Anim. Sci. 78, 343–349. conditions. Biol. Fertil. Soils 12, 202–208. Pertrusewicz, K., Macfayden, A., 1970. Productivity of Daniel, O., Kohli, L., Bieri, M., 1996. Weight gain and Terrestrial Animals. Principles and Methods. Black- weight loss of the earthworm Lumbricus terrestris L. well, Oxford. at different temperatures and body weights. Soil Biol. Phillipson, J., Bolton, P.J., 1977. Growth and cocoon Biochem. 28, 1235–1240. production by Allolobophora rosea (Oligochaeta: Diehl, W.J., Audo, M.C., 1995. Detecting heterozygosity- Lumbricidae). Pedobiologia 17, 70–82. growth relationships: how should growth be com- Reynolds, J.W., 1977. The Earthworms (Lumbricidae puted? Ophelia 43, 1–13. and Sparganophilidae) of Ontario. Life Sciences Mis- Doube, B., Styan, C., 1996. The response of Aporrectodea cellaneous Publication. Royal Ontario Museum, rosea and Aporrectodea trapezoides (Oligochaeta: Toronto. Lumbricidae) to moisture gradients in three soil SAS Institute Inc, 2001. SAS Procedures Guide, Version types in the laboratory. Biol. Fertil. Soils 23, 8.0. SAS institute, Cary, North Carolina. 166–172. Schaap, M.G., 2000. Rosetta Version 1.2. US Salinity Edwards, C.A., Bohlen, P.J., 1996. Biology and Ecology of Laboratory ARS-USDA, Riverside, CA, USA www.ussl. Earthworms, third ed. Chapman & Hall, London. ars.usda.gov/models/rosetta/rosetta.htm. Fayolle, L., Michaud, H., Cluzeau, D., Stawiecki, J., Schaap, M.G., Leij, F.A., van Genuchten, M.T., 1998. 1997. Influence of temperature and food source Neural network analysis for hierarchical prediction of on the life cycle of the earthworm Dendrobaena soil water retention and saturated hydraulic conduc- veneta (Oligochaeta). Soil Biol. Biochem. 29, tivity. Soil Sci. Soc. Am. J. 62, 847–855. 747–750. Spilke, J., Piepho, H.P., Hu, X., 2005. Analysis of Francis, G.S., Tabley, F.J., Butler, R.C., Fraser, P.M., unbalanced data by mixed linear models using the 2001. The burrowing characteristics of three MIXED Procedure of the SAS system. J. Agron. Crop Sci. common earthworm species. Aus. J. Soil Res. 39, 191, 47–54. 1453–1465. Uvarov, A.V., 1995. Responses of an earthworm species to Holmstrup, M., 2001. Sensitivity of life history para- constant and diurnally fluctuating temperature re- meters in the earthworm Aporrectodea caliginosa to gimes in laboratory microcosms. Eur. J. Soil. Biol. 31, small changes in soil water potential. Soil Biol. 111–118. Biochem. 33, 1217–1223. van Genuchten, M.T., 1980. A closed-form equation for Je´gou, D., Capowiez, Y., Cluzeau, D., 2001. Interactions predicting the hydraulic conductivity of unsaturated between earthworm species in artificial soil cores soils. Soil Sci. Am. J. 44, 892–898. ARTICLE IN PRESS

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Wang, Z., Goonewardene, L.A., 2004. The use of MIXED Whalen, J.K., 1998. Effects of earthworms on nitrogen models in the analysis of animal experiments with flux and transformations in agroecosystems. Unpub- repeated measures data. Can. J. Anim. Sci. 84, 1–11. lished Ph.D. Thesis, Ohio State University, Columbus, Wever, L.A., Lysyk, T.J., Clapperton, M.J., 2001. The OH, USA. influence of soil moisture and temperature on the Whalen, J.K., Parmelee, R.W., 1999. Growth of Aporrec- survival, aestivation, growth and development of todea tuberculata (Eisen) and Lumbricus terrestris L. juvenile Aporrectodea tuberculata (Eisen) (Lumbrici- under laboratory and field conditions. Pedobiologia dae). Pedobiologia 45, 121–133. 43, 1–10.