Directory UMM :Data Elmu:jurnal:A:Applied Soil Ecology:Vol13.Issue1.Sep1999:

Applied Soil Ecology 13 (1999) 87±100

Soil surface macrofaunal communities associated with earthworm
casts in grasslands of the Eastern Plains of Colombia
Thibaud DecaeÈns1,*, Lucero Mariani, Patrick Lavelle
Laboratoire d'EÂcologie 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 carimaguensis JimeÂnez 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% to ÿ76%). 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
*Corresponding author. E-mail: thibaud.decaens@univ-rouen.fr
1
Laboratoire d'EÂcologie, UFR Sciences, Universite de Rouen,
76821 Mont Saint Aignan Cedex, France.

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 organomineral structures (e.g. earthworm casts, termite
mounds and ant nests) that in¯uence hydraulic

0929-1393/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved.
PII: S 0 9 2 9 - 1 3 9 3 ( 9 9 ) 0 0 0 2 4 - 4

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T. DecaeÈns et al. / Applied Soil Ecology 13 (1999) 87±100

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 investigated (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 earthworm activity (Kirk, 1981; Szlavecz, 1985; Thompson et al., 1993), but much more investigation is
needed.
Since different invertebrate species will have differing 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 created by Martiodrilus carimaguensis JimeÂnez and
Moreno (Oligochaeta: Glossoscolecidae), a large
anecic earthworm (sensu BoucheÂ, 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 welldrained 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)80%, CEC 0.20).
The jackknife procedure is based upon computing n
values of the desired statistic by successively excluding 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 asymptotically, independently and normally distributed. Consequently, we computed a con®dence interval using a t
distribution table.
For the Shannon±Wiener index of diversity, the

^ n † and the estimates of the standard
estimates of H …H
^
error …H n † were calculated according to the following equations (Adams and McCune, 1979; Heltshe and
Forrester, 1985):
,
n
X
 where the pseudovalue i
^n ˆ
i n ˆ ;
H
iˆ1

ˆ nHn ÿ …n ÿ 1†Hnÿi ;
r
.
X
p
 2 n…n ÿ 1†:

^ n ˆ var2 =n ˆ
H
…i ÿ †

^
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):
^S ˆ S ‡ K…n ÿ 1†=n, where S is the taxonomic
richness for the whole set of samples, and K is the

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T. DecaeÈns et al. / Applied Soil Ecology 13 (1999) 87±100

number of morphotypes that were found in only one
sample (``unique
P species''). 
^S ˆ S ‡ … Rjˆ0 j2 Fj ÿ K 2 n†…n ÿ 1†=n, where Fj

is the number of samples with j unique species.
For all estimations, the 95% con®dence limits are:
estimated value st0.05(nÿ1), where t0.05(nÿ1) is the
Student distribution for nÿ1 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 contrast, sample origin largely in¯uenced invertebrate

communities, while cast ageing, had no overall signi®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 inside M. carimaguensis casts, 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 Arachnida (Table 1). Density was not signi®cantly different below casts and in the test soil during the ®rst two
months of cast ageing, while signi®cant differences
(P