Soil surface macrofaunal communities associated with earthworm
casts in grasslands of the Eastern Plains of Colombia
Thibaud DecaeÈns
1,*, Lucero Mariani, Patrick Lavelle
Laboratoire d'EÂ cologie des Sols Tropicaux, ORSTOM/Unidad Suelos y Plantas, CIAT, 32 Av. Varagnat, 93143 Bondy Cedex, France
Received 14 January 1999; received in revised form 12 April 1999; accepted 20 April 1999
Abstract
Earthworms are known to modify life conditions for other soil organisms through their drilospheric activities. The effects of a large anecic species,Martiodrilus carimaguensisJimeÂnez and Moreno, on soil macrofaunal communities were investigated in a natural and a man-made grassland of the Eastern Plains of Colombia. Invertebrates were sampled by a standard hand sorting method at different spatial scales: (i) at the scale of a few centimetres during the course of one year, we compared the dynamics of the density, biomass, diversity and individual weights of macroinvertebrates in earthworm surface casts, in the soil located below casts and in a control soil without casts; (2) at the scale of a few decimetres and at a ®xed time, macroinvertebrates were sampled in soil monoliths with different densities of casts on their surfaces.
Macroinvertebrates colonised casts 4 and 6 weeks after their formation in the pasture and the savanna, respectively. In the two grasslands, at the spatial scale of the cast, macroinvertebrate density was signi®cantly higher below casts (1660± 5310 ind mÿ2) than in the control soil (400±1700 ind mÿ2), while no differences were recorded in biomass, richness, diversity
and evenness. The presence of casts at the soil surface increased the relative dominance of epigeic populations (185% to
250%) at the expense of larger endogeic species (ÿ39% toÿ76%). Individual weights of invertebrates were lower in casts (1.2±5.7 g indÿ1) and the underlying soil (8.2±11.1 g indÿ1) when compared with the control soil (25.0±39.6 g indÿ1). These results were mainly con®rmed at the larger spatial scale. Taxonomic richness was positively correlated with the number of casts at the soil surface at the scale of a few decimetres, while diversity was unchanged and evenness decreased. These results were mainly attributed to the creation of new habitats (macropores, galleries) by earthworm activity and to the concentration of litter and soil organic matter in casts. They support the ``Nested Biodiversity Hypothesis'' according to which soil ecosystem engineers may have determinant effects on the abundance and diversity of other soil organisms.#1999 Elsevier Science B.V. All rights reserved.
Keywords: Martiodrilus carimaguensis; Ecosystem engineers; Soil biodiversity; Soil macrofauna; Tropical savanna; Grass-legume pastures
1. Introduction
Among the numerous soil-inhabiting organisms, a few large invertebrates (mainly earthworms, termites
and ants) can have an important impact on many processes that determine soil fertility. These key functional species, de®ned as ``ecosystem engineers'' (sensu Jones et al., 1994), produce a large variety of macropores (e.g. galleries, chambers) and organo-mineral structures (e.g. earthworm casts, termite mounds and ant nests) that in¯uence hydraulic *Corresponding author. E-mail: thibaud.decaens@univ-rouen.fr
1Laboratoire d'E cologie, UFR Sciences, Universite de Rouen,
76821 Mont Saint Aignan Cedex, France.
properties, macroaggregation and organic matter dynamics in soil (Anderson, 1995; Lavelle, 1996, 1997).
Through their mechanical and feeding activities, ecosystem engineers are reputed to modify living conditions for other smaller and less mobile soil organisms, and hence in¯uence their abundance and diversity (Hypothesis of Nested Biodiversities, Lavelle, 1996). The effects of earthworms on soil micro¯oral activity have been widely investiga-ted (Barois and Lavelle, 1986, Scheu, 1987, 1993; Daniel and Anderson, 1992), and have been referred to as the ``Sleeping Beauty Paradox'' (Lavelle, 1996). However, explicit information on the impacts of earthworms on the diversity and community structure of microbial communities is fragmentary at best (Parkinson and McLean, 1998). Some studies have examined the positive or negative effects that earthworms may have on micro- and mesoinvertebrate communities (see review by Brown, 1995; also Marinissen and Bok, 1988; Loranger et al., 1999), but their impacts on macrofaunal communities have been little investigated. A few isolated studies have revealed positive responses by some groups to earth-worm activity (Kirk, 1981; Szlavecz, 1985; Thomp-son et al., 1993), but much more investigation is needed.
Since different invertebrate species will have differ-ing impacts and therefore different functions in the soil (Lavelle, 1996), it is necessary to develop an understanding of the role of biodiversity in soils, and of the condition necessary for its maintenance. For this purpose, it is essential to (i) clearly identify the links existing among species and (ii) test to what extent the presence of a given species may in¯uence that of others.
The aim of this study was to evaluate the effects on soil macrofaunal communities of the structures cre-ated by Martiodrilus carimaguensis JimeÂnez and Moreno (Oligochaeta: Glossoscolecidae), a large anecic earthworm (sensuBoucheÂ, 1977) of the Eastern Plains of Colombia. This species is the only one at the research site that casts signi®cantly at the soil surface (JimeÂnez et al., 1998b). Experiments were conducted at different scales of time and space in a natural savanna and a man-made pasture derived from savanna.
2. Material and methods
2.1. Study area
The study was carried out at the CIAT-CORPOICA research station of Carimagua (48370 N, 71819 W), located in the phyto-geographic unit of the well-drained isohyperthermic savannas of the Eastern Plains of Colombia. The climate is subhumid tropical with an annual mean temperature and rainfall of 268C and 1300 mm, respectively, and a dry season from November to March. Native vegetation is determined by topography: open savannas in the uplands (``altos'' and ``planos''), and gallery forests or ¯ooded savannas in the low-lying areas (``bajos''). Soils are Oxisols (Tropeptic Haplustox Isohyperthermic) in the uplands and Ultisols (Ultic Aeric Plintaquox) in the low-lying areas. Both are highly aggregated and characterised by their low chemical fertility (pH (H2O)<5, Al satura-tion>80%, CEC <5 meq 100 gÿ1) (CIAT data).
2.2. Experimental plots
Soil macrofauna were sampled in two different systems on a well drained upland Oxisol:
1. A Trachypogon vestitus Anders. native savanna, protected from grazing for four years and managed traditionally by burning every year during the dry season.
2. A three year-old pasture planted withBrachiaria humidicola (Rendle), Arachis pintoi Krap and Greg,Stylosanthes capitataVog. andCentrosema acutifoliumBenth., grazed by cattle at an average stocking rate of 2.0 animal units. haÿ1.
.
2.3. Experimental design
Soil ecosystem engineers in¯uence soil processes at large spatial and temporal scales through the produc-tion of physical structures (e.g. earthworm casts, termite mounds, galleries) (Lavelle, 1996, 1997; Anderson, 1995). Hence, their effects can be de®ned as a microscale regulation of macroscale processes (Anderson, 1995). For this reason, two different experiments were conducted, in order to describe the effects of ageing casts of M. carimaguensis on macroinvertebrate communities (i) at the scale of their
own structure (a few cm), and (ii) at the scale of the experimental plot.
2.3.1. Study at the cast scale
The experiment was started at the onset of the rainy season (May 1996), during the peak of earthworm activity. In both systems, 160 casts ofM. carimaguen-siswere labelled in the ®eld using small metal plates and divided into eight groups of 20 contiguous casts. During this operation, special attention was paid to identify the recently deposited casts (i.e. fresh and small faeces). This thereby ensured the presence of one earthworm in each of the labelled galleries, and avoided any cumulative effects that might result from the presence of a large cast on the soil surface before the beginning of the experiment. Since earthworms were not eliminated from their burrows, most of them remained, adding excreta to the same casts during the ®rst days of the experiment. After a few days of excretion, casts can range up to 10 cm diameter and 15 cm high. When earthworms abandoned their bur-rows, the casts started drying at the soil surface.
Soil macrofauna (i.e. invertebrates larger than 2 mm) were sampled 0, 7, 14 days and 1, 2, 3.5, 5, 6.5, 8, 9.5 and 11 months after the beginning of cast production. At each date, one cast was randomly chosen from each of the eight groups of 20. For each cast, we sampled (i) the cast, (ii) the underlying soil, located directly below the cast and (iii) a control soil, located 20 cm away from the cast. Soil was sampled using a 10 cm diameter and 10 cm deep aluminium cylinder. Casts and soil were carefully hand-sorted in a large 4060 cm plastic tray and macroinvertebrates were collected and preserved in 70% alcohol.
In order to accurately describe the community structure, invertebrates were identi®ed at the order or family level and then separated according to mor-photype (sensu Oliver and Beattie, 1995), i.e. mor-phologically distinct taxa (see Appendix). Then, density (individuals. mÿ2) and biomass (g. of fresh matter. mÿ2) were calculated for 11 larger taxonomic and functional units (Table 1). The functional classi-®cation commonly used for earthworms was followed (BoucheÂ, 1977) because it covers the functional char-acteristics of most of the soil macrofauna: endogeics are species that live exclusively in the soil pro®le (mostly earthworms, rhizophagous Coleoptera lar-vae); anecic are species that live in the soil and have
a surface feeding activity (earthworms, termites and ants); epigeics are species that live in the litter layer (earthworms, termites, ants and litter-dwelling arthro-pods). Biomass was corrected for losses resulting from ®xation in alcohol, i.e. 19% for earthworms and termites, 9% for ants, 11% for Coleoptera, 6% for Arachnida and Myriapoda, and 13% for other arthro-pod groups (DecaeÈns et al., 1994).
2.3.2. Study at the plot scale
In the early months of the rainy season (June 1997± July 1997), 20 soil monoliths of 252530 cm were randomly taken at each site. The casts ofM. carima-guensispresent on the surface of the monoliths were separated into fresh and dry and counted, then mono-liths were dug out with a spade and divided into four successive strata (i.e. litter, 0±10, 10±20, 20±30 cm). Each stratum was hand-sorted using the procedure described for the cast experiment (method recom-mended by the Tropical Soil Biology and Fertility programme, Anderson and Ingram, 1993).
2.4. Data processing
The structure of the macroinvertebrate communities was described using indices available in the literature. These indices were calculated for each subsample origin (i.e. cast, soil and control soil) of each experi-mental plot with the total number of individuals recorded during the whole experiment. Since compar-isons between these indices require a common sample size to be meaningful (Hurlbert, 1971), we did not compared soil samples of known size and cast samples for which size was not clearly estimated.
Sùrensen's index of similarity (Cs) was used to compare the taxonomic composition (i.e. morphotype composition) of macrofaunal communities in the soil and the control soil, within and between each experi-mental plot (Sùrensen, 1948; Legendre and Legendre, 1979):
Cs2j= ab;
wherejis the number of morphotypes common to the two samples, a and b are the total number of mor-photypes recorded for each sample, respectively.
Table 1
Mean macroinvertebrate biomass (g of fresh matter. mÿ2) and density (individuals. mÿ2) recorded in the casts ofMartiodrilus carimaguensis, the underlying soil and the control
soil, in the pasture and savanna (ÿnot present)
Ecological groups and taxonomic units
Native savanna Pasture
Casts Underlying soil Control soil Casts Underlying soil Control soil Biomass Density Biomass Density Biomass Density Biomass Density Biomass Density Biomass Density
Endogeics
Oligochaeta 0.004 0.1 7.60 28.7 10.39 25.5 0.001 0.1 19.36 65.3 38.34 39.8
(0.004) a (0.1) a (3.00) b (6.8) b (4.72) b (8.0) b (0.001) a (0.1) a (6.67) b (13.1) c (12.13) c (9.8) b
Coleoptera ± ± 0.02 4.8 0.07 8.0 ± ± 0.28 30.2 0.04 9.55
(0.01) (2.7) a (0.06) (3.5) b (0.09) c (8.3) c (0.02) b (3.8) b
Total endogeics 0.004 0.1 7.62 33.5 10.46 33.5 0.001 0.1 19.64 95.5 38.38 49.4
(0.004) a (0.1) a (3.28) b (5.8) b (5.25) b (9.8) b (0.001) a (0.1) a (8.40) b (25.9) c (10.30) b (11.2) b
Anecics
Isoptera 0.001 1.0 2.69 1231.9 0.49 300.8 0.031 20.5 13.83 4776.2 3.74 1483.0
(0.001) a (0.7) a (0.57) b (264.4) b (0.18) c (101.2) a (0.015) c (7.6) a (4.05) d (673.8) c (1.19) b (178.3) b
Hymenoptera 0.005 3.1 0.12 55.7 0.11 33.4 0.007 24.2 4.01 173.5 1.11 122.6
(0.003) a (1.9) ac (0.08) a (22.4) bc (0.07) a (13.8) C (0.003) a (14.9) ac (3.21) b (50.0) de (0.99) ab (59.6) ce
Total anecics 0.006 4.1 2.81 1287.6 0.60 334.2 0.038 44.7 17.84 4949.7 4.85 1605.3
(0.003) a (2.5) a (0.50) b (221.9) b (0.21) a (127.0) c (0.014) a (19.5) d (6.01) c (900.5) e (1.86) bc (315.6) b
Epigeics
Isoptera 0.026 17.0 0.29 326.3 ± ± ± ± ± ± ± ±
(0.015) a (10.6) a (0.25) a (298.3) a
Coleoptera ± ± 0.79 15.9 0.19 17.5 ± ± 0.73 47.8 2.19 9.6
(0.04) a (7.3) a (0.15) a (7.1) a (0.22)a (9.5) ba (1.61) a (3.8) ca
Myriapoda 0.000 0.1 0.00 1.6 0.04 6.4 0.008 0.1 4.13 154.4 0.56 3.2
(0.000) a (0.1) ac (0.00) a (1.6) b (0.02) a (3.1) c (0.008) a (0.1) a (1.23) b (107.3) d (0.04) a (2.3) abc
Arachnida ± ± 0.92 11.1 0.01 1.6 0.000 0.1 0.15 1.8 ± ±
(0.75) a (5.7) a (0.01) a (1.6) b 0.000 a (0.1) ab (0.15) a (1.7) ab
Isopoda 0.001 0.1 0.00 1.6 ± ± ± ± ± ± ± ±
(0.001) a (0.1) a (0.00) a (1.6) a
Diptera 0.03 8.0 ± ± ± ± 0.02 17.5 0.05 3.2
(0.02) a (6.6) a (0.02) a (16.1) a (0.04) a (2.3) a
Others 0.001 0.2 0.00 1.6 0.0l 4.8 0.002 0.5 0.75 44.6 0.28 8.0
(0.001) a (0.1) a (0.00) a (1.6) a (0.01) a (3.9) a (0.001) a (0.2) a (0.23) b (10.7) b (0.14) a (3.5) a
Total epigeics 0.028 17.4 2.03 366.1 0.25 30.3 0.010 0.7 5.78 266.1 3.08 24.0
(0.016) a (11.6) a (0.82) ab (127.0) b (0.15) a (5.8) a (0.008) a (0.4) a (1.34) b 116.5) b (1.94) b (10.7) a
Total 0.038 21.4 11.56 1657.9 11.31 397.9 0.048 45.5 43.11 5309.4 45.80 1699.8
(0.017) a (10.8) a (3.13) b (383.4) b (4.71) b (102.5) a (0.018) a (16.5) a (8.23) c (689.9) c (12.17) c (183.5) d Standard errors in parenthesis; different letters indicate significant differences (Fisher PLSD), within and between systems, atP<0.05.
90
T
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Èns
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/Applied
Soil
Ecology
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(1999)
indices of diversity (Pielou, 1966):
H ÿX
n
i1
pilog2pi;
wherepi is the frequency of theimorphotype;
H0H=log2S:
2.5. Statistical analysis
2.5.1. Quantitative data
The normality of data frequency distribution was tested using the Kolmogorov±Smirnov test (Lilliefors, 1967). Data were transformed before analysis to reduce the asymmetry of the frequency distribution if necessary. The normalisation of data was achieved using the Box±Cox transformation (Sokal and Rohlf, 1995) which isy(xdÿ1)/. The normality test and the
parameters estimation were done using the program VerNorm 3.0 from the ``R package'' developed by Legendre and Vaudor (1991).
A three-way analysis of variance (ANOVA) was performed on the ®xed main effects system, sample origin (i.e. cast, underlying soil or adjacent soil) and cast age. Analyses were performed for biomass and density of the three functional categories and the total macrofauna. Eight analyses were thus performed, and each analysis involved seven tests (three main effects and four interactions). The Bonferroni procedure for nested tests (Cooper, 1968) was used to prevent sta-tistical error: the adjusted 0.05, 0.01 and 0.001 sig-ni®cant levels were respectively 0.001 [0.05/(87)], 0.0002 [0.01/(87)] and 0.00002 [0.001/(87)]. Additional comparisons of mean density and biomass were performed using a Fisher PLSD test.
Simple linear regressions were performed to test the relationships between the numbers of casts on the soil surface and the macrofaunal community found in the underlying soil monoliths. Data normality was tested with the above described Kolmogorov±Smirnov test. This test was performed for each situation giving a suf®cient number of samples (at least four). Data processed with these tests comprised macrofaunal density, biomass and taxonomic richness (S) and diversity (H), the percentage of individuals inhabiting the super®cial 0±10 cm soil layer, and the density of earthworms, termites, and other groups of macroin-vertebrates. For diversity indices, we also computed
jackknife estimates as described below. Normality was tested at the probability level of 5% for all distribu-tions, except forHpseudovalues in the savanna with ®ve casts at the sample surface. The signi®cances of allr-coef®cients were tested separately at the follow-ing signi®cance levels: 0.05, 0.01 and 0.001.
2.5.2. Diversity indices
A ®rst-order generalised jackknife procedure (Tukey, 1958) was used to improve the estimate of taxonomic richness (S) and diversity (H), and generate con®dence intervals in order to compare macroinver-tebrate communities for those aspects. As no refer-ences were found that mention the use of such test for evenness (H0) and Sùrensen's index (Cs), less rigor was possible in comparing them. When comparing these indices, only the larger differences were inter-preted (i.e. >0.20).
The jackknife procedure is based upon computingn
values of the desired statistic by successively exclud-ing one of the n samples. The average of these estimates is used to reduce the bias in the statistic, and the variability among these values is used to estimate its standard error (Sokal and Rohlf, 1995). Tukey (1958) conjectured that the pseudovalues () obtained using the jackknife procedure are asympto-tically, independently and normally distributed. Con-sequently, we computed a con®dence interval using at
distribution table.
For the Shannon±Wiener index of diversity, the estimates ofH H^nand the estimates of the standard error H^nwere calculated according to the follow-ing equations (Adams and McCune, 1979; Heltshe and Forrester, 1985):
For the taxonomic richness, the estimates of S ^S
and the estimates of the standard error ^S were calculated according to the following equations (Heltshe and Forrester, 1983):
^
number of morphotypes that were found in only one sample (``unique species'').
^SS PR
j0j2FjÿK2
n nÿ1=n, where Fj is the number of samples withj unique species.
For all estimations, the 95% con®dence limits are: estimated valuest0.05(nÿ1), wheret0.05(nÿ1)is the Student distribution fornÿ1 degrees of freedom.
3. Results
3.1. Effects of cast ageing on macroinvertebrate communities at the cast scale
Whatever the sample origin, macroinvertebrate density and biomass were signi®cantly higher in the pasture than in the native savanna (Table 1). By con-trast, sample origin largely in¯uenced invertebrate
communities, while cast ageing, had no overall sig-ni®cant effect except in the case of anecic biomass (Tables 2 and 3).
Invertebrates (mainly termites and ants) were found inside casts from 4 to 6 weeks after their deposition, respectively, in the pasture and the savanna (Fig. 1). The density of invertebrates found insideM. carima-guensiscasts, however, was very low when compared with that found in soil (Table 1). In both systems, the density of the three ecological categories and of the overall macroinvertebrate communities were signi®-cantly higher below casts than in the control soil. This was especially the case for earthworms (Oligochaeta), endogeic Coleoptera, Isoptera, Myriapoda and Ara-chnida (Table 1). Density was not signi®cantly differ-ent below casts and in the test soil during the ®rst two months of cast ageing, while signi®cant differences (P<0.05) occurred after this period (Fig. 2). The total
Table 2
Three-way analyses of variance for macroinvertebrate density
Source DF Endogeic D. Anecic D. Epigeic D. Total D.
Sample origin (a) 2 35.83b 201.66c 36.07b 400.96c
Cast age (b) 9 1.27 NS 1.14 NS 2.33 NS 2.18 NS
ab 18 2.51b 1.30 NS 1.78 NS 1.27 NS
System (c) 1 8.31a 133.82c 19.06b 121.85c
ac 2 4.87a 18.50b 8.03b 23.55b
bc 9 1.29 NS 3.20a 2.85a 3.77b
abc 18 2.52b 0.78 NS 1.82 NS 0.73
Error mean squares 420 257.67 2.47 33.77 1.76
F-ratios and error mean squares are presented. Each test is significant at the Bonferroni-corrected probability (overall probability/(nof variablenof tests)) for overall significant levels of 0.05, 0.01 and 0.001 (Ddensity).
Overall significant level:aP<0.05;bP<0.01;cP<0.001; NSnon-significant.
Table 3
Three-way analyses of variance for macroinvertebrate biomass
Source DF Endogeic B. Anecic B. Epigeic B. Total B.
Sample origin (a) 2 23.61b 140.25c 49.83b 3.28 NS
Cast age (b) 9 2.12 NS 4.56b 1.55 NS 0.18 NS
ab 18 1.37 NS 1.42 NS 2.13a 0.88 NS
System (c) 1 12.98b 100.97c 35.24b 0.09 NS
ac 2 2.36 NS 22.77b 12.80b 0.06 NS
bc 9 2.05 NS 4.75b 1.57 NS 0.74 NS
abc 18 0.94 NS 1.38 NS 0.76 NS 1.00 NS
Error mean squares 420 4292378.90 2403961.78 4.12E21 4215.40
F-ratios and error mean squares are presented. Each test is significant at the Bonferroni-corrected probability (overall probability/(nof variablenof tests)) for overall significant levels of 0.05, 0.01 and 0.001 (Bbiomass).
Overall significant level:aP<0.05;bP<0.01;cP<0.001; NSnon-significant.
Fig. 1. Dynamics overtime of macroinvertebrate density in casts of Martiodrilus carimaguensis from pasture and savanna (vertical barsstandard errors).
number of individuals found inside casts or in the underlying soil was not signi®cantly modi®ed by cast ageing (Table 2). However, signi®cant increases over time were observed in casts for epigeic arthropods in the pasture (P0.0264), for endogeic species in the underlying soil in the two systems (P0.0024), and for endogeic and epigeic Coleoptera found below casts in the pasture (P0.0001 and P 0.0235, respec-tively).
Individual weights of macroinvertebrates were sig-ni®cantly lower (P0.0009) inside and below casts than in adjacent soil (Fig. 3), while the biomass of the overall macrofauna remained unchanged (Table 1). Signi®cant differences, however, were observed for some groups. In the pasture, earthworm biomass was lower below the casts than in the control soil, whilst contrary for endogeic Coleoptera, Isoptera and Myriapoda.
The contributions to density and biomass of the three ecological categories were greatly affected by the surface casting activity of M. carimaguensis
(Fig. 4(a) and (b)). The density and biomass of cast inhabiting communities were dominated by epigeic species in the savanna (80.7% and 76.3%, respec-tively) and anecic species in the pasture (98.2% and
77.1%, respectively). In the soil, irrespective of the system or sample origin, density was dominated by anecic (76.3±95.6%), while biomass was dominated by endogeic species (45.4±92.5%). The contribution to density and biomass of epigeic and anecic popula-tions was higher when communities were located below casts than in the control soil. On the contrary, the endogeic community decreased in the presence of surface casts ofM. carimaguensis.
Changes in taxonomic diversity and richness must be considered with extreme caution, because of the high estimated variances. This high variance is due to the high number of ``unique species'', i.e. morpho-types that were found in only one sample (Heltshe and Forrester, 1983), and can be interpreted as the effect of an inadequate unit sample sizes. The number of morphotypes was higher in soil below casts compared with soil without casts, but this result was not statis-tically signi®cant (Table 4). No signi®cant difference was observed for diversity and evenness when com-paring the soil located below casts and the control soil. In the two systems, Sùrensen's indices of similarity (Table 5) revealed an important disparity between the taxonomic composition of cast fauna and that of soil whatever the subsample location. In both systems,
Fig. 3. Mean individual weights of macroinvertebrates collected in the casts ofMartiodrilus carimaguensis, the underlying soil and the control soil, from pasture and savanna. Different letters mean significant differences (Fisher PLSD) atP<0.05 (Ccasts; USunderlying soil; CScontrol soil; vertical barsstandard errors).
communities living in the underlying soil and in the control soil had the most similar taxonomic composi-tion.
3.2. Effects of surface casts on macroinvertebrate communities at the plot scale
Most of the previously described effects of surface casts on the below-ground macroinvertebrate commu-nities were con®rmed at the plot scale (Table 6). In
biomass in the savanna. Neither the vertical distribu-tion nor the individual weights of macroinvertebrates was affected by the number of casts recorded at the soil surface.
In the two systems, the presence of casts at the soil surface stick with the relative numeric dominance of anecic species (185% to 250%, Table 6) at the expense of larger endogeic species (ÿ39% to 76%). No signi®cant effect was observed on the relative contribution of each functional category to biomass. Epigeic species did not respond in a signi®cant way. The number of casts at the sample surface was signi®cantly correlated with the taxonomic diversity (H) and richness (S) of the underlying macroinverte-brate communities in the savanna (Table 6). On the contrary, no signi®cant effects were observed in the case of the pasture.
4. Discussion
All the observed casts of M. carimaguensis were colonised by macroinvertebrates following the aban-donment of the burrow by the earthworm. Only a small number of species were found living inside casts, mostly belonging to ecological categories adapted to surface living conditions (i.e. anecics and epigeics). This means that only a few specialised (i.e. small and mobile) species are able to live inside surface faeces. In comparison to the population observed in the soil, the number of invertebrates collected in old casts (up to 21.4 and 45.5 ind mÿ2, respectively, in the savanna and the pasture) was of secondary importance.
In the two systems, the presence of earthworm casts was correlated with signi®cant modi®cations of sub-terranean macrofaunal communities. This result could possibly be due to a common response of earthworms and other macroinvertebrates to the presence of ``hot spots'' (e.g. nutrient rich resources) in the ®eld. How-ever, invertebrate density increased gradually in the underlying soil during cast ageing, demonstrating that the presence of casts was certainly responsible for the changes observed. An alternative explanation could be that earthworms might ®nd ``hot spots'' at a faster rate than other invertebrates. This seem improbable, con-sidering the relatively low mobility of earthworms when compared with active foragers such as termites or litter dwelling arthropods.
The presence of earthworm casts on the soil surface led mainly to an increase in the population densities of small-sized invertebrates in the underlying top soil (317% and 212%, respectively, in the savanna and the pasture). Earthworm casting activity may enhance Table 4
Results of the jackknife estimates of Shannon±Wiener index (H) and taxonomic richness (S)
System Sample origin DF Taxonomic richness (R) Shannon index (H) Evenness (H0) Calculated Estimated Calculated Estimated
Savanna Casts 7 12 19.88 (2.79) ± 1.43 1.52 (0.58) ± 0.40
Underlying soil 7 38 55.38 (2.63) b 2.75 3.17 (0.35) a 0.53 Control soil 7 31 45.00 (3.50) b 3.20 3.54 (0.50) a 0.65
Pasture Casts 7 17 27.50 (4.18) ± 2.57 3.44 (0.38) ± 0.63
Underlying soil 7 53 73.13 (5.83) b 1.95 2.07 (0.19) b 0.34
Control 7 39 55.63 (4.17) b 2.09 2.23 (0.36) ab 0.40
Calculated and estimated values are presented, with the corresponding estimated standard errors (in parenthesis). Comparisons were made only between samples with similar size (soil samples). Different letters indicate significant differences (Fisher PLSD) atP<0.05.
Table 5
Numbers of common species and Sùrensen's index of similarity comparing species composition of macroinvertebrate collected in the casts ofMartiodrilus carimaguensis, the underlying soil and the control soil, from pasture and savanna
Compared
living conditions for a large number of species, as indicated by the positive response in taxonomic rich-ness and diversity to the increased number of casts at the soil surface. However, this effect was only sig-ni®cant in the case of the savanna. This suggests that earthworm activity may have a greater impact where unsuitable conditions occur at the soil surface (for example absence of a litter layer in the savanna submitted to periodic ®res), and little or no effects where living conditions for surface invertebrates are favourable (this is the case in the pasture).
To explain how earthworms can in¯uence macro-invertebrate communities, two hypotheses may be formulated, that refer to trophic and structural mod-i®cations of the soil due to the formation of earthworm structures:
(i) Firstly, some invertebrate species may preferen-tially live inside casts or in the underlying soil because of changes in the quantity and quality of their energy resource. Casts ofM. carimaguensishave high organic matter content (Guggenberger et al., 1996; Rangel et al., 1999; DecaeÈns et al., 1999), and may represent a valuable food substrate for small polyhumic
earth-worms and humivorous termites. Root biomass is locally increased below casts (DecaeÈns et al., 1999), and may be bene®cial to larvae of rhizophagous Coleoptera. Some litter dwelling species such as Iso-poda and DiploIso-poda can be preferentially attracted by compositional changes in surface litter processed by earthworms (Szlavecz, 1985). Small predatory species (Chilopoda, Arachnida) can ®nd high prey densities, of micro- and mesofaunal species taking advantage of earthworm-enhanced life conditions (Brown, 1995; Loranger et al., 1999).
(ii) Other species may respond to changes in soil structure, and to the creation by earthworm activity of new speci®c microhabitats. Macropores that result from earthworm activity have been considered as habitats for some micro- and mesoinvertebrate species (Haukka, 1991, Loranger et al., 1999). Kirk (1981) reported large numbers of corn root worm ( Diabro-tica: Coleoptera) eggs in earthworm burrows. During the experiment, ants and termites were commonly observed using galleries as communication ways. In the post-®re savanna environment, totally lacking in protection for surface living invertebrates (i.e. litter Table 6
Results of linear regressions between number of dry casts ofMartiodrilus carimaguensison the soil surface and the characteristics of the underlying macroinvertebrate community, from pasture and savanna
Data set Savanna Pasture
Intercept Slope r Intercept Slope r
Macroinvertebrate density (ind per sample) ÿ7.50 7.54 0.87c 2.59 7.24 0.87c
Macroinvertebrate biomass (g. per sample) ÿ0.60 0.23 0.45a 0.58 0.14 0.42 NS
Oligochaeta density (ind. per sample) 0.22 1.52 0.66b 3.05 0.69 0.38 NS
Oligochaeta biomass (g. per sample) 0.04 0.19 0.38NS 0.52 0.12 0.35 NS Isoptera density (ind. per sample) ÿ6.93 4.88 0.71c ÿ0.10 4.88 0.68b
Isoptera biomass (g. per sample) ÿ0.02 0.03 0.36 NS 0.01 0.01 0.45 NS Density of other groups (ind. per sample) ÿ0.79 1.15 0.42 NS ÿ0.45 1.68 0.35 NS Biomass of other groups (g. per sample) ÿ0.06 0.23 0.45a 0.58 0.14 0.42 NS
Anecic contribution to density (% of density) 34.54 7.76 0.52a 43.07 10.25 0.69b
Anecic contribution to biomass (% of biomass) 41.84 5.59 0.27 NS 46.29 5.79 0.28 NS Endogeic contribution to density (% of density) 61.01 ÿ8.91 0.58a 49.59 ÿ9.59 0.64b
Endogeic contribution to biomass (% of biomass) 53.22 ÿ5.66 0.27 NS 51.60 ÿ5.91 0.28 NS Epigeic contribution to density (% of density) 4.45 1.15 0.17 NS 7.09 ÿ0.65 0.21NS Epigeic contribution to biomass (% of biomass) 2.10 0.13 0.07 NS 4.94 0.07 0.01 NS Percentage of individuals in the 0±10 cm soil layer 98.75 ÿ2.78 0.35 NS 88.03 ÿ3.84 0.33 NS
Individual weigh (mg) 0.05 ÿ0.00 0.16 NS 0.08 ÿ0.01 0.29 NS
Taxonomic richness (JE*of S means) 2.34 3.72 0.94c 10.58 0.81 0.31 NS
Shannon Wiener index (JE*of H means) 2.13 0.28 0.84b 2.63 ÿ0.03 0.13 NS NSnon-significant;aP<0.05;bP<0.01;cP<0.001.
and herbaceous layer), earthworm structures may be used as speci®c refuges by litter-dwelling arthropods, and could help their maintenance and/or rapid reco-lonisation of the soil surface after ®re.
Most of the present results suggest that the presence ofM. carimaguensiscasts on the soil surface prefer-entially enhanced epigeic and anecic populations, to the detriment of endogeics. This may be due to: (i) the concentration of organic resources near the soil sur-face in aboveground casts and (ii) the creation of new speci®c habitats at the soil surface. Structures created underground (burrows and underground casts) may have different effects on other invertebrate groups such as a small polyhumic earthworm (Ocnerodrili-dae) that was commonly found feeding on M. car-imaguensis casts, down to 70 cm in depth (JimeÂnez et al., 1998a).
5. General conclusions
The results presented in this study support Lavelle (1996) hypothesis of nested biodiversities, according to which ecosystem engineers (sensu Jones et al., 1994) determine the structure of smaller organism communities.
In this study, we have demonstrated that the casts of an anecic earthworm species can have signi®cant effects on macrofaunal communities inhabiting the underlying soil. When super®cial, their presence results in a global increase in macroinvertebrate den-sity, and favours small epigeic and anecic species, at the expense of larger endogeics. We hypothesise these results are due to modi®cations in: (i) the size and abundance of speci®c microhabitats for smaller inver-tebrate species (cast cracks, galleries), and (ii) the location and dynamics of the organic resource com-monly used by a large part of the soil community (carbon in casts and gallery cortex). Earthworm effects, however, are not restricted to the soil surface. A large proportion of their structures is created under-ground, and hence may act on other invertebrate species at different depths in the soil. Future research should investigate this aspect to permit the develop-ment of a good overview of the impacts of earthworms on soil biodiversity.
The production of biogenic structures by large earthworms seems to be an important factor in
deter-mining the structure of soil macroinvertebrate com-munities. But is this effect the same on other functional groups of soil organisms? And what are the implications of other species of ecosystem engi-neers in such process? Termite mounds, for example, commonly accommodate a high number of inverte-brate species (Wood and Sands, 1978), but there is still a lack of studies to describe this phenomenon. A typology of biogenic structures, and of their effects on soil organisms, is a necessary step in the description of the links existing between engineers and other functional groups.
Colonisation of large casts by other invertebrates may be critical for the conservation and dynamics of soil organic matter and regulation of soil physical properties. When eating large and compact earthworm casts, small invertebrates may prevent their excessive accumulation on the soil surface, which otherwise could lead to a super®cial soil compaction and affect plant growth negatively (Rose and Wood, 1980; Chau-vel et al., 1999). They may thus re-activate organic matter dynamics by making organic resources avail-able to microorganisms that were sequestered in dry casts (Lavelle, 1996). Testing this hypothesis is now critical to identify invertebrate functions in terms of their impacts on soil properties, and to assess the real functional signi®cance of biodiversity in the soil system.
Acknowledgements
The authors thank R.J. Thomas and D.K. Friesen (CIAT) for their technical and ®nancial support; A.V. Spain (CSIRO), I Poudevigne (University of Rouen) and J.P. Rossi (ORSTOM) for making useful sugges-tions on a ®rst version of this paper; E. Baudry, X. Graves and E. Mariani for great help in computing jackknife estimates.
Appendix
List of the classes, orders and families, and number of morphotypes identi®ed for each, in the casts of
Martiodrilus carimaguensis, the underlying soil and the control soil, from pasture and savanna are shown in Table 7.
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Taxonomic units Native savanna Pasture
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Wasp families 0 0 0 0 1 1
Coleoptera Elateridae 0 4 3 0 4 2
Melolontidae 0 1 1 0 1 1
Carabidae 0 1 1 0 3 2
Chrysomelidae 0 1 3 0 1 2
Staphvlinidae 0 1 0 0 3 2
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Chilopoda Geophilomorpha Geophilidae 1 0 1 0 1 1
Scolopendromorpha Scolopendridae 0 1 1 0 1 0
Arachnida Araneida Unidentified families 0 5 1 1 1 0
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