Species abundance of earthworms in arable and pasture
soils in south-eastern Australia
P.M. Mele
a, M.R. Carter
b,*aInstitute for Integrated Agricultural Development, R.M.B. 1145, Chiltern Valley Road, Rutherglen, Vic., Australia bAgriculture and Agri-Food Canada, Research Centre, Charlottetown, PEI, Canada CIA 7M8
Received 15 November 1997; accepted 10 December 1998
Abstract
Earthworms play an important role in soil ecology and can serve as practical indicators in land quality evaluation. The abundance and distribution of earthworms were determined in 84 cropping and pasture soils in north-east Victoria and southern New South Wales (NSW), Australia. Overall, an average density of 89 earthworms mÿ2
was found, with an average species richness of 1±2 per site, indicating relatively low abundance and species poverty. Introduced lumbricid earthworms,
Aporrectodea trapezoidesandA. caliginosawere the most widely distributed (88% and 61% of all sites, respectively) and numerically dominant (respective population densities of 35.8 and 32.1 mÿ2). Soils under pasture supported on average 3.2
times more earthworms than those under cropping. The age structure of populations varied with species, introduced lumbricids and acanthodrilids displayed an adult-dominant structure and the native megascolecids displayed a juvenile-dominant population. Indigenous earthworms belonged to a single genus,Spenceriella. Whilst not occurring in high densities these indigenous earthworms were widespread in their distribution and their numbers were negatively correlated with soil P, K, and Mg suggesting an adaptation to low levels of soil fertility. Although the relationship between earthworm densities and mean annual total precipitation (MATP) was not close (r20.35), of the 33 sites containing >100 earthworms mÿ2
, 25 received MATP in excess of 600 mm. Correlations between earthworm densities and a range of physical and chemical parameters were generally poor. This may highlight the short-comings of these parameters in describing distribution patterns.#1999 Elsevier Science B.V. All rights reserved.
Keywords:Earthworm distribution; Exotic and native earthworm species; Arable; Pasture; Soil properties;Spenceriella
1. Introduction
Earthworms can signi®cantly improve the fertility and plant productivity of dryland agricultural soils in Australia. Superior in®ltration and bioporosity in cropping (Tisdall, 1985; Carter et al., 1994) and orchard soils (Tisdall, 1978) have been related to
greater earthworm abundance. Accelerated ameliora-tion of acid soils through lime burial (Baker et al., 1993a) and reductions in the severity of both take-all (Stephens et al., 1994a) and bare-patch (Stephens et al., 1994b) diseases of wheat have been all attributed to the activity of earthworms. Some research has also de®ned agricultural factors affecting activity such as grazing (Lobry de Bruyn and Mele, 1993) and tillage (Rovira et al., 1987; Carter et al., 1994; Mele and Carter, 1999), and climatic factors related to rainfall
*Corresponding author. Tel.: 566-6869; fax: +1-902-566-6821; e-mail: carterm@em.agr.ca
distribution (Baker, 1997; Lobry de Bruyn and King-ston, 1997).
Some earthworm species have been implicated more strongly in soil improvement than others. This has been largely attributed to variation in the ecolo-gical functions of individual species (Lee, 1985). The recent focus on earthworms as practical indicators of sustainable agricultural management (Lobry de Bruyn, 1997), has highlighted basic knowledge gaps in terms of what earthworms are and what physical, chemical and agricultural management factors in¯u-ence their distribution and abundance. Knowledge on the ecological appropriateness of species encountered will aid in the selection of species to supplement existing populations.
Although several surveys exist in Australia that determine the species distribution of earthworms in agricultural and urban land (Mele et al., 1993), very few have attempted to quantify species abundance. Baker et al. (1992) attempted to relate species abun-dance to a suite of soil physical and chemical para-meters, while other studies have attempted to relate dominant earthworm species to a range of soil and agronomic conditions (Bucker®eld et al., 1997) or to aspects of soil structural stability (Ketterings et al., 1997). In order to quantify the impact of earthworms in arable agricultural land and to investigate the potential for manipulation of earthworm fauna, the factors that effect species distribution and abundance must be de®ned and quanti®ed.
The purpose of this study was to characterise earth-worm fauna in both cropping and pasture soils in north-eastern Victoria and southern New South Wales (NSW). The speci®c objectives of the study were to: (1) determine the abundance and distribution of earth-worms, (2) assess earthworm age structure, and (3) relate overall and species abundance of earthworms to a range of standard soil physical and chemical parameters.
2. Materials and methods
A survey of the earthworm fauna in 84 cropping and pasture soils in north-eastern Victoria and southern NSW (Fig. 1) was undertaken in 1990 during the cool wet season (August±October) when species tend to concentrate in the surface soil. This is the period of peak earthworm activity (Baker et al., 1992, 1993b).
The survey area, which comprised approximately 200 km2, is generally characterised by a modi®ed mediterranean climate with wet, frosty winters (mean annual total precipitation 300±1000 mm) and hot dry summers with extended periods of summer drought. The soil morphology was dominately duplex, with texture contrasts between the A and B horizons (Stace et al., 1968).
The passive earthworm sampling procedure of Baker et al. (1992) was adopted. At each site, two parallel transect lines, each approximately 50 m long and 10 m apart were measured so that samples could be taken every 10 m with a total of 10 sampling points. At each sampling point, a block of soil (0.1 m2 by 0.1 m) was removed and the soil ®nely hand-sifted to collect all earthworm lifestages including cocoons. Specimens from each block were placed into indivi-dual containers of 70% ethanol for preservation pend-ing identi®cation.
Prior to microscopic identi®cation, all specimens were rinsed in water, placed in fresh 70% ethanol and identi®ed using a WILD M3C1 dissecting micro-scope (magni®ed 10±40 times) with an endoscopic light source (Intralux 5000, Volpi1). Introduced spe-cies were classi®ed according to Sims and Gerard (1985) and indigenous species to the level of genus using Jamieson (1974) where applicable. Lifestages were separated as adults (clitellate), subadults (non-clitellate, sexual pores present), juveniles (non-clitel-late, sexual pores absent) and cocoons. Fresh weight (biomass) was determined for each lifestage and for overall population at each site.
A composite soil sample from each sampling point was also collected at each site. Soil was dried (408C, 24 h) and either ground (<2 mm) for chemical ana-lyses (with the exception of pH, >2 mm, and organic C and total N, 0.25 mm) or sieved (1±2 mm), for phy-sical analyses. Soil organic C was measured by an improved chromic acid digestion and spectrophoto-metric procedure (Heanes, 1984), while total N was determined by dry combustion using a LECO CNS analyser. Soil available K (i.e., Skene K) and P (i.e., NaHCO3, Olsen P) were determined according to the
respective methods of Skene (1956) and Olsen and Sommers (1982). Soil pH was determined using both 0.01 M CaCl2 and distilled water. Exchangeable
cations (Ca, Mg, Na, and K) were extracted with 1 M NH4OAc (1 : 10, soil : extractant) and the cations
determined by ICP-AES analysis (Rayment and Hig-ginson, 1992). Soil particle size distribution was determined for clay (%), sand (%, >500 mm, 250± 500 mm and <250 mm), and silt (%), using the pipette method after removal of soil organic matter, in accor-dance with Day (1965) in a constant temperature environment (2518C). Soil water aggregate stabi-lity was determined by an adaption of the method of Kemper (1965). A 10 g soil sample was placed on a 0.5 mm sieve and immersed gently followed by 20 consecutive vertical motions (20 cm) at a rate of one cycle per second. Aggregates retained on the sieve were weighed after oven drying (1058C, 24 h) and a stability index calculated by expressing the aggregate weight as a percentage of the original oven dry weight. To correct for sand >0.5 mm, oven dried aggregates were sieved (0.5 mm sieve) in 0.5 M NaOH, redried (1058C, 24 h), and calculated as above. Gravimetric water (wt.%), average annual precipitation and where possible, crop and pasture history data were also collected.
Multiple regression step-down analyses were employed on earthworm population density values to derive parsimonious equations of signi®cant relation-ships with soil chemical and physical variables (Genstat 5, 1987). A multiple regression analysis was also per-formed on mean annual total precipitation and earth-worm density data sets using precipitation values taken from MetAccess1
Analysing Weather records (Bureau of Meteorology and CSIRO; Horizon Technology Pty Ltd). Table CurveTMwas used to derive a correlation coef®cient (Jandel Scienti®c, copyright 1991).
3. Results
3.1. Earthworm species and abundance
Earthworm fauna in north-eastern Victoria and southern NSW contained at least 10 species belonging to three families (Table 1). Six of these species were introduced Lumbricidae and three were introduced Acanthrodrilids. A single indigenous genus, Spencer-iella, was also identi®ed with a further six different morphs categorised (G. Dyne, personal communica-tion, 1991). The total average species abundance (all sites combined) varied widely from densities of 35.8 mÿ2
for Aporrectodea caliginosato <1 mÿ2
for
A. tuberculata and Octolasion cyaneum. When con-sidered separately, pasture sites (n47) contained, on average, more than three times the total number of earthworms of cropping sites (n37), with 168.6 mÿ2
(range 5±802 mÿ2
) compared to
51.9 mÿ2
(range 0±338 mÿ2
). The lumbricid,A. tra-pezoideswas the most widely distributed occupying 86% of all sites surveyed, followed by the acanthro-drilids, Microscolex dubius, M. phosphoreus and another lumbricid, A. caliginosa, occupying 61%, 56%, and 49% of all sites, respectively. Although individual species were not identi®ed, native species such as Spenceriella occupied 45% of all sites and coexisted with introduced earthworm species at many sites. The densities of all species declined in the order;
A. caliginosa>A. trapezoides>Spenceriella spp. >
A. rosea>M. phosphoreus>M. dubius>Lumbricus rubellus. Both A. caliginosaandA. trapezoideswere more abundant in pasture than cropping soils, being 4.8 and 3.9 times greater, respectively in pasture sites.
Spenceriellaspecies were 6.7 times more abundant in pasture soils than in cropping soils whilst other lum-bricids, A. rosea and L. rubellus were only slightly more abundant in pasture soils. In contrast, the acan-throdrilids,M. dubiusandM. phosphoreuswere 2 and 1.1 times more abundant, respectively, in cropping soils than in pasture soils.
3.2. Earthworm age structure
At the time of sampling, the age structure of the earthworm population varied widely between species (Fig. 2). The two most abundant species,A. caliginosa
adults representing the greatest proportion of both populations followed closely by juveniles. Similarly
M. dubius and M. phosphoreus populations were dominated by adults. However, in contrast to the lumbricids, juveniles of these species represented less than 1% of their populations. The age structure ofA. roseawas more even. For the native genus, the popu-lation structure was the reverse of the introduced species with juveniles being the dominant component of the population and adults comprising the minor proportion.
The number of cocoons recovered across the survey area was highly variable. They were more prevalent at the pasture sites (77% of the pasture sites contained cocoons), compared to the cropping sites (Fig. 3). This high percentage under pasture could be attributed to the high number of cocoons recovered from four out of the 47 pasture sites.
3.3. Earthworm abundance and soil properties
Multiple regression step-down analyses on total earthworm population densities (numbers mÿ2
) and biomass with a range of soil physical and chemical variables indicated generally poor relationships (sig-ni®cant r2 range from 0.53 to 0.1), particularly for
fresh biomass. A relatively strong positive association (r20.46) was found among total earthworm popula-tion densities and pH (Ca and H2O), soil moisture and
aggregate stability (all species densities combined). This association was most strongly re¯ected by A. caliginosa, where the highest regression coef®cient of 0.53 was recorded. Other signi®cant correlations had an r2 value below 0.3. Multiple regression for L. rubellus (r20.29) included a positive association with organic C (%) and a negative association with Skene K. Acanthodrilid species were positively asso-ciated (r2of 0.18±0.29) with pH (Ca) and exchange-able Ca, but negatively so with exchangeexchange-able Mg.
Spenceriella species were negatively correlated with Olsen P and more strongly so with Skene K (r20.26).
When only clitellate (i.e., adult) specimens were considered in a multiple regression step-down analy-sis, there was a relatively strong positive association (r20.42) between total earthworm densities and soil moisture (wt.%). This was also re¯ected in densities of
A. caliginosa (r20.63) and A. trapezoides
(r20.30). Densities of clitellate A. rosea, were associated (r20.25) negatively with % sand content of all size grades. M. phosphoreusdensities were in¯uenced by the largest number of measured
Table 1
Earthworm population densities (number mÿ2) in crop and pasture soils of north-east Victoria and south NSW
Species Crop Pasture Average all sites
Sitesa MeanSE Max. Sites MeanSE Max. MeanSE
Lumbricidae
Aporrectodea caliginosa 13 11.56.9 225 27 55.822.2 743 35.812.3
A. trapezoides 29 12.53.5 118 43 48.38.8 267 32.15.3
A. tuberculata 2 <1 1 3 <1 7 <1
A. rosea 8 9.24.1 101 13 10.04.7 131 9.63.0
Octolasion cyaneum 2 <1 1 4 <1 23 <1
Lumbricus rubellus 3 1.51.0 30 4 2.41.6 59 2.11.0
Acanthodrilidae
Microscolex dubius 21 4.31.6 56 25 2.10.5 14 3.10.8
M. phosphoreus 24 6.61.5 34 26 5.82.2 83 6.11.3
Microscolexspp. 2 <1 1 3 <1 7 <1
Megascolecidae
Spenceriellaspp.b 11 5.5
1.8 32 27 36.812.1 364 22.26.8
Unidentified spp. 9 1.20.6 22 8 <1 8 <1
variables being positively associated (r20.42) (in descending order) with exchangeable Ca, % coarse sand (equal weighting), % ®ne sand, silt and clay, and negatively with aggregate stability.
3.4. Earthworm abundance and mean annual total precipitation
Multiple regression analysis of earthworm density and mean annual total precipitation yielded anr2value of 0.23. With the exclusion of two outliers, the corre-lation could be improved (r20.35) (Fig. 4). Below an average annual precipitation value of 600 mm, earthworm densities were less than 200 mÿ2
, with the exception of two sites. Above 600 mm, 14 sites contained earthworm densities above 200 mÿ2
.
Fig. 2. The average age structure of the different earthworm species found in soil samples expressed as the percentage of the total number of earthworms in the population.
4. Discussion
An overall average density of 89 earthworms mÿ2, with 61% of all sites containing less than 100 mÿ2and an average species richness of 1±2 per site, contrasts sharply with the average density of 400 mÿ2and 5±10 species per site recorded for European soils (Lee, 1985). The numerical dominance of the introduced Lumbricidae, particularly A. caliginosa, A. trape-zoides, and A. rosea and their average densities in agricultural soils of south-eastern Australia, however, coincides with the results of a survey by Baker et al. (1992) of southern South Australia and western Victoria.
Overall species population densities varied widely across the survey area with a maximum density of 802 mÿ2(fresh biomass 140.9 g mÿ2) found in a high rainfall pasture site (915 mm average annual precipi-tation), and a minimum density of 0 mÿ2found in a lower rainfall lupin (Lupinus L.) crop site (562 mm average annual precipitation). At the former site, 93% of the 802 mÿ2
earthworms wereA. caliginosa. Simi-larly, distribution of all species was also generally patchy. A notable exception wasA. trapezoides, whose distribution was most widespread, occurring at 78% and 91% of all crop and pasture sites, respectively (or
at 86% of all sites overall). This is in contrast with the ®ndings of Baker et al. (1993a) who reported thatA. trapezoidesoccurred in less than 30% of the soils used for cereal production. Two species belonging to the Acanthodrilidae,M. phosphoreusandM. dubiuswere also relatively widespread in distribution, particularly
M. phosphoreuswhich was found in 65% and 55% of all crop and pasture sites, respectively. The observa-tion thatA. caliginosawas less widespread in occur-rence than A. trapezoides is consistent with the observation of Baker et al. (1995) for Australia and France where such a difference was attributed to the ability of A. trapezoides to tolerate hotter and drier conditions. Surprisingly and contrary to the ®ndings of Baker et al. (1992), the indigenous species, Spencer-iella, were relatively widespread in distribution occur-ring in 30% and 57% of crop and pasture sites, respectively (or 49% of all sites). At some cropping sites they were also numerically dominant, despite harsh soil treatments such as tillage. Such resilience in disturbed soil conditions may re¯ect an adaptation to infertile soils (low organic matter) and soils prone to extreme wetting and drying cycles, a re¯ection per-haps of the type of soil (i.e., duplex) at most of the cropping sites in the survey region, and the overall climatic conditions characterised by lengthy periods
of summer drought. These conditions may provide a competitive advantage for native species.
Although data assessing population structure over a single season can be misleading and inconclusive, it can serve to contrast the seasonal breeding patterns of the different species encountered (Baker et al., 1992; Baker, 1996). Based on previous Australian surveys, there is a gradual transition from juvenile-dominant to adult-dominant populations as the season progresses (Lobry de Bruyn and Mele, 1993). In this survey, the contrasting population age structures of different species suggest that breeding cycles may be staggered in agricultural soils where resources are limited or may re¯ect an ecological adaptation to climatic extremes of temperature. For example, the four intro-duced species (A. trapezoides,A. caliginosa,M. phos-phoreus and M. dubius) all have adult-dominant populations whilst the native Spenceriella spp. has juvenile-dominant populations. The contrasting dom-inance in age structure of native compared to intro-duced earthworms over the peak activity period may re¯ect seasonal differences in reproduction, feeding patterns and/or tolerance to the drier and warmer conditions later in the season.
The highly variable recovery of cocoons may in part re¯ect the imprecision in the recovery technique but also the highly variable soil conditions in the survey area. The marked difference in the incidence of cocoons in pasture compared to cropping soils may indicate that breeding is more conducive in soils under pasture where disturbance is limited and food is pre-sumably more abundant.
The much higher average population densities of earthworms found under pasture compared to crops is similar to the ®ndings of Fraser et al. (1996) in a survey of the Canterbury Plains in New Zealand, where there were two times more earthworms under pasture soils than cropping soils. This difference is perhaps attributable to the higher quantity of plant material in pasture soils, the relatively minimal soil disturbance, and absence of earthworm mortality due to cultivation (BostroÈm, 1995). Indirectly, the above differences between pasture and cropping soils, may re¯ect the tendency for crop sites to be located in areas receiving lower annual precipitation. This trend was evident for all species except M. dubius and M. phosphoreuswhich were more abundant in crops than pastures.
The wide variation in species density and abun-dance in this survey indicates the importance of local factors. The attempt here to relate a series of soil physical and chemical parameters to earthworm spe-cies abundance and distribution is based on the assumption that these parameters represent habitat characteristics of the earthworm. The fact that rela-tionships between these parameters and either fresh biomass or population densities (total and clitellate) were generally poor indicates that this assumption does not hold (i.e., the selected parameters do not accurately describe the soil habitat or are not overly critical to earthworm population). Generally, this agrees with the conclusions of Bucker®eld et al. (1997).
In the few cases where signi®cant regressions were recorded between soil parameters and earthworm abundance, different variables in¯uenced individual species differently. Regional variations in gravimetric soil moisture and pH were the most important vari-ables associated with total abundance and abundance ofA. caliginosa. Aggregate stability was also related positively with the population density of both total and
A. caliginosa. When only adults were considered, total earthworm densities and densities of A. caliginosa
were associated with soil moisture. The generally poor relationship between soil moisture and all other spe-cies may re¯ect the fact that most soils were at ®eld capacity when sampled.
Although there was a poor relationship (r20.35) between earthworm densities and mean annual total precipitation, 77% of sites with less than 600 mm of average annual precipitation contained less than 100 earthworms mÿ2
. In contrast, 77% of sites with greater than 600 mm of rainfall contained earthworm densi-ties of greater than 100 mÿ2
. This coincides with the ®ndings of Baker (1997) who indicated a strong threshold of 600 mm annual average precipitation under which earthworm densities declined markedly. Thus, mean annual total precipitation appears to be a useful determinant of earthworm abundance.
affected by coarse sand. Bucker®eld et al. (1997) noted that earthworm density, in dryland cropping in southern Australia, was inversely correlated with levels of coarse sand. Baker et al. (1992) also demon-strated the strong adverse effect of % sand content in soils of the Mt. Lofty Ranges, South Australia, how-ever, only withA. caliginosaandA. trapezoides. The abrasive nature of such soils for earthworm passage was suggested as a possible explanation. Khalaf El-Duweini and Ghabbour (1965) also concluded that decreases in density ofA. trapezoideswas related to the water-holding-capacity of coarse textured soils. Baker et al. (1992) also reported the importance of pH as a determinant of M. dubius densities, which is consistent with that observed here for totalM. dubius
densities. In contrast adultM. phosphoreus densities were related positively with coarse sand, silt and clay content and negatively with aggregate stability, Olsen P and exchangeable K. Similarly,M. dubiuswas also related negatively to aggregate stability. Such obser-vations suggest that both these acanthodrilids, parti-cularly M. phosphoreus, can tolerate poor soil conditions and may represent primary colonisers in degraded soils. The preference for self-fertilisation lends support to this (Lee, 1985). Interestingly, total densities of the indigenousSpenceriellaspecies were negatively related to Olsen P, Skene K and exchange-able soil magnesium contents, re¯ecting an adaptation to Australia's naturally infertile soils (particularly the low P contents) (Stace et al., 1968).
The dominance of introduced species may be due to the competitive advantage they have in disturbed environments. As indicated in Mele and Carter (1999), site history, particularly cultivation can have a major impact on earthworm densities. Because densities of native species were low, it is dif®cult to draw any conclusions regarding compositional changes.
5. Conclusions
The low abundance and species poverty reported in this survey indicates the enormous scope for popula-tion enhancement and species diversi®capopula-tion through relocation of existing species, and introduction of new species in south-eastern Australia. It also suggests a need to reassess agricultural management options
particularly in relation to crop stubble treatment (Mele et al., 1993) to increase earthworm activity. The surprisingly widespread occurrence of native Spen-ceriellaspp. suggests a need for further investigation of its agronomic importance. At present, nothing is known about its lifecycle and seasonal activities.
The largely unsuccessful attempt to identify soil physico-chemical factors that in¯uence earthworm distribution and abundance means that explanations for these features will remain largely anecdotal. Stan-dard soil physical and chemical parameters are not useful as predictors of earthworm abundance and distribution in this study.
Acknowledgements
The authors are grateful for the technical assistance of a large team, particularly G. Ronnfeldt, D. Pierce and J. Sandral; to Dr. G. Dyne for identi®cation of indigenous earthworm species; and to funding bodies, Grains Research and Development Corporation (GRDC) and Rural Industry Research and Develop-ment Corporation (RIRDC) for providing ®nancial assistance.
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