Applied Soil Ecology 83 (2014) 177–185

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Applied Soil Ecology

journal homepage: www.elsevier.com/locate/apsoil

Soil macroinvertebrate communities and ecosystem services in

deforested landscapes of Amazonia
Raphael Marichal a,b,e,∗ , Michel Grimaldi b , Alexander Feijoo M. c , Johan Oszwald d ,
Catarina Praxedes e , Dario Hernan Ruiz Cobo c , Maria del Pilar Hurtado f ,
Thierry Desjardins b , Mario Lopes da Silva Junior g , Luiz Gonzaga da Silva Costa g ,
Izildinha Souza Miranda g , Mariana Nascimento Delgado Oliveira g , George G. Brown h ,
Stéphanie Tsélouiko a , Marlucia Bonifacio Martins e , Thibaud Decaëns i , Elena Velasquez j ,
Patrick Lavelle a,b,f
a
Université Pierre et Marie Curie (UPMC-Univ Paris 6), UMR BIOEMCO 211, Centre IRD Ile de France, 32 Av. Henri Varagnat, 93143 Bondy Cedex, France
b
IRD, UMR BIOEMCO 211, Centre IRD Ile de France, 32 Av. Henri Varagnat, 93143 Bondy Cedex, France
c
Universidad Tecnológica de Pereira, Apartado Aéreo 97, Pereira, Colombia
d
Université de Rennes 2, UMR CNRS LETG 6554, Laboratory of Geography and Remote Sensing COSTEL, France
e
Museu Paraense Emilio Goeldi (MPEG), Coordenação de Zoologia, Av. Perimetral, n◦ 1901, CEP 66077-530 Terra Firme, Belém, Pará, Brazil
f
Centro Internacional de Agricultura Tropical (CIAT), TSBF LAC, ap aereo, 6713 Cali, Colombia
g
Universidade Federal Rural da Amazonia (UFRA), 2501 Av. Presidente Tancredo Neves, 66077-530 Bairro Montese, Belém, Pará, Brazil
h
Embrapa Florestas, Estrada da Ribeira, Km. 111, C.P. 319, Colombo PR 83411-000, Brazil
i
Université de Rouen, ECODIV, Faculté des Sciences & des Techniques, Bâtiment IRESE A, Place Emile Blondel, F-76821 Mont Saint Aignan Cedex, France
j
Universidad Nacional de Colombia, Carrera 32 No 12-00 Chapinero, Vía Candelaria, Palmira, Valle del Cauca, Colombia

a r t i c l e i n f o a b s t r a c t

Article history: Land use changes in the Amazon region strongly impact soil macroinvertebrate communities, which
Received 7 December 2012 are recognized as major drivers of soil functions (Lavelle et al., 2006). To explore these relations, we
Received in revised form 2 May 2014 tested the hypotheses that (i) soil macrofauna communities respond to landscape changes and (ii) soil
Accepted 16 May 2014
macrofauna and ecosystem services are linked. We conducted a survey of macrofauna communities and
Available online 4 June 2014
indicators of ecosystem services at 270 sites in southern Colombia (department of Caqueta) and north-
ern Brazil (state of Pará), two areas of the Amazon where family agriculture dominates. Sites represented
Keywords:
a variety of land use types: forests, fallows, annual or perennial crops, and pastures. At each site we
Landscape
Macro-invertebrates
assessed soil macroinvertebrate density (18 taxonomic units) and the following ecosystem service indi-
Soil services cators: soil and aboveground biomass carbon stock; water infiltration rate; aeration, drainage and water
Amazonia storage capacities based on pore-size distribution; soil chemical fertility; and soil aggregation. Signifi-
cant covariation was observed between macrofauna communities and landscape metric data (co-inertia
analysis: RV = 0.30, p < 0.01, Monte Carlo test) and between macrofauna communities and ecosystem
service indicators (co-inertia analysis: RV = 0.35, p < 0.01, Monte Carlo test). Points located in pastures
within 100 m of forest had greater macrofauna density and diversity than those located in pastures with
no forest within 100 m (Wilcoxon rank sum test, p < 0.01). Total macroinvertebrate density was signifi-
cantly correlated with macroporosity (r2 = 0.42, p < 0.01), as was the density of specific taxonomic groups:
Chilopoda (r2 = 0.43, p < 0.01), Isoptera (r2 = 0.30, p < 0.01), Diplopoda (r2 = 0.31, p < 0.01), and Formicidae
(r2 = 0.13, p < 0.01). Total macroinvertebrate density was also significantly correlated with available soil
water (r2 = 0.38, p < 0.01) as well as other soil-service indicators (but with r2 < 0.10). Results demonstrate
that landscape dynamics and composition affect soil macrofauna communities, and that soil macro-
fauna density is significantly correlated with soil services in deforested Amazonia, indicating that soil
macrofauna have an engineering and/or indicator function.
© 2014 Elsevier B.V. All rights reserved.

∗ Corresponding author at: CIRAD, UR 34 Perennial Crops, Av. de l’Agropolis, TA B-34/02, 34398 Montpellier Cedex 5, France. Tel.: +33 467616524.
E-mail address: raphael.marichal@cirad.fr (R. Marichal).

http://dx.doi.org/10.1016/j.apsoil.2014.05.006
0929-1393/© 2014 Elsevier B.V. All rights reserved.
178 R. Marichal et al. / Applied Soil Ecology 83 (2014) 177–185
1. Introduction
Deforestation is still intense in Amazonia (INPE-PRODES, 2010).
Deforestation has diverse, though largely related, origins: road
construction, wood exploitation, cattle ranching, and smallholder
settlements (Le Tourneau, 2004). As forest is lost, landscape frag-
mentation increases (Ferraz et al., 2005), with significant negative
effects on biodiversity (Laurance et al., 2001). Many studies have
shown the importance of land use (Barros et al., 2002; Decaens
et al., 2004; Lavelle and Pashanasi, 1989; Mathieu et al., 2004, 2005;
Rossi et al., 2010) and the influence of spatial heterogeneity at
small scales, from grass tufts to land use effects on soil macrofauna
(Mathieu et al., 2009). The role of landscape properties has rarely
been addressed (Decaëns, 2010). Carvalho and Vasconcelos (1999)
showed that species richness and density of litter-dwelling ants
decreases with forest fragmentation, while Louzada et al. (2010)
observed that landscape configuration influenced dung beetle com-
munities in Amazonian savannas. Beyond local effects at the plot
scale, effects of landscape changes on soil macrofauna communities
in deforested areas of Amazonia remain largely ignored.
The loss in diversity observed at small scales (Mathieu et al.,
2005) likely affects ecosystem services, which are defined as the
benefits people obtain from ecosystems (Millennium Ecosystem
Assessment, 2005). Soil macrofauna has an acknowledged influ-
ence on soil formation, soil hydraulic properties, flood and erosion
control, nutrient cycling, and primary production through direct
and indirect plant stimulation and carbon dynamics (Brussaard
et al., 2007; Lavelle, 2002; Lavelle et al., 1997, 2006). Earthworms,
for example, are expected to greatly affect water-related ser-
vices through their intense bioturbation and burrowing activities
(Lavelle et al., 1997). Although soil macrofauna is broadly used as an
indicator of soil quality (Rousseau et al., 2012, 2010; Ruiz-Camacho
et al., 2009; Turbe et al., 2010; Vasconcellos et al., 2013; Velasquez
et al., 2007a), few studies have directly assessed the link between
soil ecosystem services and soil macrofauna communities in the
field (van Eekeren et al., 2010).
To fill this gap, we tested the following two hypotheses:
(i) Soil macrofauna communities respond to landscape composi-
tion and dynamics. Abundance and diversity of soil macrofauna
is expected to decrease with landscape degradation.
(ii) Soil macrofauna and the delivery of ecosystem services are
correlated, mainly through the densities of soil engineers
(earthworms, termites, ants) and soil processes.
To test these hypotheses, we surveyed macrofauna communi-
ties and ecosystem services in the diversity of landscapes found in a
gradient of land-use intensification in deforested areas of Amazonia
in Colombia and Brazil.
2. Materials and methods
2.1. Study sites
Sampling was conducted in two regions of Brazil and Colombia.
In each country, three groups of nine farms were chosen that cor-
respond to landscape units with different histories of colonization.
Brazilian sites, located in the center of Pará State, were recently
colonized: Palmares II is an old “fazenda” which was invaded by
the “Movimento dos Trabalhadores rurais sem Terra – MST” (Land-
less Workers’ Movement). Farms in Pacajá are located on a trail
(“Travessão Sul 338”) perpendicular to the Trans-Amazonian high-
way. The Maçaranduba region is occupied by a group of former
agro-extractivist farmers who increasingly rely on cattle ranch-
ing. Deforestation started in 1990, 1994 and 1997 in the three
landscape units, respectively. The three Colombian landscape units,
located in the Caquetá Department (southwestern Colombia),
are representative of three dominant farming systems: conven-
tional livestock breeding in long-established degraded pastures,
agrosylvo-pastoral and agro-forestry systems in the Canelos, Bal-
canes and Aguadulce regions, respectively. Deforestation started
between 1940 and 1950 at all three Colombian sites.
On each of the 54 farms chosen, five sampling points were
located equally along a transect corresponding to the longest diag-
onal of the farm, thus representing a total of 270 points (135 in
each country). The distance between points (ca. 200 m) was equal
to 1/6 of the transect length and varied according to farm area.
Macrofauna and soil were sampled from April to June 2008.
2.2. Macrofauna sampling
The TSBF method (Anderson and Ingram, 1993) was used to
sample soil invertebrates. At each of the 270 points, a central soil
monolith (25 cm × 25 cm, 20 cm deep) was dug, and two additional
soil monoliths (25 cm × 25 cm, 10 cm deep) were dug 5 m east and
west from the central monolith. Thus, one sampled unit was com-
posed of 3 monoliths. Overall, 810 monoliths were extracted and
hand-sorted.
Macrofauna (groups in which more than 90% of individuals are
visible to the naked eye) in the litter and soil was hand-sorted and
preserved in 4% formaldehyde. All individuals were then sorted,
counted and classified into the following taxonomic units: Formi-
cidae, Isoptera, Blattaria, Diptera, Isopoda, Dermaptera, Hemiptera,
Homoptera, Coleoptera (adults and larvae), Orthoptera, Lepi-
doptera (larvae), Diptera (larvae), Araneae, Opiliones, Chilopoda,
Diplopoda, Gastropoda, and Oligochaeta.
2.3. Land use and landscape analysis
A remote sensing approach was used to characterize landscape
dynamics from 1990 to 2007 for each site. Landsat TM and ETM+
(30-m spatial resolution, spectral recording adapted to land cover
identification) were acquired during the dry season for each site
(1990, 1994, 1998, 2002 and 2007). Field validation measurements
were taken in 2007 and 2008 to classify landscape elements. Each
geolocated measurement was linked to the spectral signature of
each landscape element. A confusion matrix determined eight opti-
mal classes of landscape elements.
For each site, supervised classification was performed with the
2007 Landsat image. The spectral signature of each landscape ele-
ment allowed us to reconstitute previous images (1990, 1994, 1998,
and 2002). Five classifications for each site from 1990 to 2007 were
produced by supervised classifications.
Nine farms were analyzed on each site. Multivariate analysis
was used to explain temporal dynamics of patches on each farm.
Three-dimensional matrices were built with x (farm), k (land cover)
and t (date). Then, the ACT (STATIS) method (Lavit et al., 1994) was
used to identify the (in)stability of spatial patterns over time (each
acquisition is integrated into a date-table). This method is based
on a date-table correlation to identify a trade-off (inter-structural
step). The second step (intra-structural step) identifies trade-off
reproducibility within each date-table. Similar date-tables indicate
similar landscape spatial structure. This method alone, however,
cannot explain the complexity of spatial organization within the
agricultural mosaic. Several landscape metrics were necessary to
analyze the spatial organization of the landscape (Lausch and
Herzog, 2002). Three groups of landscape metrics were identified:
fragmentation metrics (“Total Area” (ha), “Edge Density” (m ha−1 ),
and “Mean Patch Density” (m ha−1 )), diversity metrics (“Patch
Richness”, “Shannon’s Diversity”, “Shannon’s Eveness”, and “Dom-
inance index”) and fractal metrics (“perimeter/area”, “Mean Shape
 R. Marichal et al. / Applied Soil Ecology 83 (2014) 177–185 179

Table 1 2.5. Carbon stock

Land uses and simplified classification of land uses. X corresponds to land use that
exists in the landscape, but was not sampled for soil macrofauna.
Total carbon and nitrogen contents of the soil were measured
Land use code Land use Simplified classification with a CHNS analyzer on composite samples taken in four trenches
P1 Pasture Pastures along a transect (50 m), in the 0–10, 10–20 and 20–30 cm layers
P2 Pasture with babaçu (Attalea Pastures below the soil surface. These values were adjusted by the bulk den-
speciosa) sity measured in the same trenches and depths to estimate soil
P3 Pasture with trees Pastures
carbon stock.
P4 Pasture with scattered trees Pastures
C Crop Crops Allometric equations were used to estimate the carbon stock
O Orchard Tree plantations of aboveground biomass in trees (diameter at breast height, dbh
CP Cocoa plantation Tree plantations ≥10 cm) and bushes (dbh <10 cm, height >2 m) after measuring
AP açaï (Euterpe oleracea) Tree plantations
the diameter and estimating the height of each tree and bush on
plantation
PP African palm-tree plantation Tree plantations 50 m × 10 m and 50 m × 5 m plots, respectively, centered on each
AP Agroforestry plantation Tree plantations point (Silva Costa et al., 2012).
SP Fodder shrub plantation Tree plantations
YFP Young fallow after pasture Fallows after pastures
OFP Old fallow after pasture Fallows after pastures 2.6. Indices of soil quality
YFC Young fallow after crop Fallows after crops
OFC Old fallow after crop Fallows after crops Four indices of soil quality were calculated (Velasquez et al.,
B Babaçus Tree plantations 2007a,b) which combine several soil morphological (aggregation),
F3 Burned forest Forests
F2 Exploited forest Forests
physical, chemical, and organic matter characteristics measured
F1 Forest Forests at all points. Soil aggregates with distinct morphology and origin
LF Lowland forest Forests (physical, biogenic and root aggregates) and other soil com-
LP Lowland pasture Pastures ponents (plant and charcoal debris, stones) from a soil core
LB Lowland bush X
10 cm × 10 cm × 5 cm deep were separated and weighed after dry-
BS Bare soil X
R River or pond X ing according to the method of Velasquez et al. (2007a) and
Velasquez et al. (2007b). Sheer strength resistance and vertical
resistance of the surface horizon were measured in the field with
a hand torcometer and a penetrometer, respectively, and were
Index”). Landscape metrics were calculated using the software
repeated at 4 locations. Particle-size distribution and chemical
package FRAGSTATS (McGarigal et al., 2002). Class area, patch rich-
properties of the 0–10 cm soil horizon were measured on a com-
ness and a summary index of landscape integrity, all representing
posite of two pits. The chemical properties measured were pH H2 O;
land-use dynamics (1990–2007), were calculated in a 100 m radius
CEC (cation exchange capacity); exchangeable K+ , Ca2+ , Mg2+ , Al3+
centered on each of the five sampling points in every transect.
and NH4 + ; and extractable phosphorus (Mehlich extractable), using
From these metrics, 3D matrices were built to monitor land-
standard methodologies (Pansu and Gautheyrou, 2006). Each indi-
scape spatial organization and temporal dynamics at the farm scale.
cator was quantified over a common range of 0.1–1.0 (Table 3).
Ward’s hierarchical ascending method was applied to farm facto-
rial coordinates using principal component analysis (PCA) and CoA
(STATIS). 2.7. Indicators of soil water services: infiltration, available water
Farms were classified based on a PCA that included landscape and macroporosity
elements and landscape spatial organization in 2007. Two factorial
analyses using ACT (STATIS) were applied to a multidimensional Soil water infiltration rate (INFIL) was measured with the
date-table for the years 1990–2002 (Oszwald et al., 2011). In some Beerkan test (Lassabatere et al., 2006) (250 cm3 of water poured in
analyses, the 24 land-use types were reduced to 6 broad classes: a simple ring 20 cm in diameter inserted into the soil to a depth
forests, tree plantations, crops, fallows after crop, fallows after pas- of about 1 cm). This test was repeated four times near the soil
ture, and pastures (Table 1). pits. Measurements of water retention capacities at different water
potentials followed a specific sampling protocol: cores with undis-
turbed structure were taken from one of the five points on each
2.4. Ecosystem service assessment farm (4 replicates). Water matrix potentials were −0.3 kPa, −1 kPa,
−3 kPa, −10 kPa, −30 kPa, −100 kPa, −300 kPa, −1600 kPa and were
Carbon stocks in soil and plant biomass, soil hydrodynamic measured with the sandbox method (0 to −10 kPa) and the Richards
properties and indicators of soil quality were measured at each pressure-plate apparatus (−30 kPa to −1600 kPa). From these mea-
sampling point (Tables 2 and 3). Several soil properties were mea- surements, multiple linear regression models were generated to
sured down to a depth of 30 cm since earthworms and roots may estimate water retention capacities at different water potentials
reach this depth and consequently affect these variables. from the simplest soil variables measured at all points (all soil

Table 2
Indicators of soil ecosystem services measured: description, units and ranges.

Variable Description Unit Range

−1
SCS030 Soil carbon stock 0–30 cm deep Mg.ha 25.1–86.6
Physical Indicator of physical soil quality None 0.1–1.0 (arbitrary)
Chemical Indicator of chemical soil quality None 0.1–1.0 (arbitrary)
Morphological Indicator of morphological soil quality None 0.1–1.0 (arbitrary)
Organic Indicator of organic soil quality None 0.1–1.0 (arbitrary)
AW010 Plant-available soil water 0–10 cm deep Cm 0.2–1.5
Macro010 Soil macroporosity 0–10 cm deep Cm 0.7–2.9
BCStree Tree and shrub carbon biomass Mg.ha−1 0–1163
INFIL Water infiltration into the soil mm.h−1 16.18–10330.2
180 R. Marichal et al. / Applied Soil Ecology 83 (2014) 177–185

Table 3
Indicators of soil ecosystem services (mean ± SE) among land uses.

Variable Forests Fallows after crops Fallows after pasture Tree plantations Pastures Crops

Chemical 0.40 ± 0.03 0.47 ± 0.05 0.48 ± 0.02 0.52 ± 0.01 0.49 ± 0.01 0.59 ± 0.05
Physical 0.49 ± 0.40 0.38 ± 0.05 0.48 ± 0.04 0.49 ± 0.03 0.48 ± 0.02 0.46 ± 0.05
Organic 0.54 ± 0.02 0.49 ± 0.02 0.62 ± 0.04 0.66 ± 0.03 0.61 ± 0.01 0.55 ± 0.03
Morphological 0.33 ± 0.01 0.34 ± 0.03 0.36 ± 0.02 0.40 ± 0.02 0.43 ± 0.01 0.36 ± 0.03
SCS030 (Mg.ha−1 ) 45.06 ± 1.55 41.65 ± 2.28 51.84 ± 1.94 53.19 ± 1.60 50.43 ± 0.92 43.88 ± 2.43
BCStree (Mg.ha−1 ) 156.59 ± 26.23 48.78 ± 14.76 48.01 ± 13.50 48.95 ± 12.46 6.48 ± 1.43 1.06 ± 0.47
INFIL (mm.h−1 ) 2471.02 ± 290.48 1738.94 ± 384.52 2408.69 ± 461.58 3114.89 ± 605.84 786.02 ± 132.1 2189.36 ± 517.25
AW010 (cm) 0.67 ± 0.03 0.62 ± 0.06 0.88 ± 0.04 0.99 ± .04 0.87 ± 0.02 0.76 ± 0.05
Macro010 (cm) 1.74 ± 0.06 2.02 ± 0.13 1.68 ± 0.07 1.64 ± 0.05 1.64 ± 0.03 1.8 ± 0.1

physical characteristics, CEC and carbon content). Soil macrop-
orosity and plant-available soil water to a depth of 10 cm were
calculated as the water volume drained between saturation and
−10 kPa (pF2) and between −30 kPa (pF 2.5) and −1600 kPa (pF
4.2), respectively.
2.8. Statistical analyses
(agrosylvo-pastoral) to 1038.7 ± 141.5 ind. m−2 (Maçaranduba)
(Fig. 1b). Formicidae, the most abundant taxa, had densi-
ties varying from 54.9 ± 5.9 ind. m−2 (Colombian “Conventional”)
to 403.8 ± 103.8 ind. m−2 (Maçaranduba), while Isoptera density
ranged from 9.2 ± 5.5 ind. m−2 (Colombian “Conventional”) to
382.3 ± 83.0 ind. m−2 (Maçaranduba) (Table 4).

Soil fauna abundance was converted into density per square
meter (ind. m−2 ) for each site. Since the pantropical earthworm
Pontoscolex corethrurus (Glossoscolecidae), native to the Guiana
Shield (Righi, 1984), has a different response to ecosystem distur-
bance than native earthworms (Marichal et al., 2010), we divided
earthworms into two categories for the analysis: P. corethrurus
and native earthworms. This resulted in a total of 18 taxonomic
units. Since the Shapiro–Wilk test (Siegel and Castellan, 1988)
indicated non-normality of the data, we used the non-parametric
Kruskal–Wallis rank sum test (Hollander and Wollfe, 1973; Kruskal
and Wallis, 1952) to compare macrofauna density and diversity
among landscape units. We used the non-parametric Wilcoxon
rank sum test to compare soil macrofauna diversity and density
at points in pastures within 100 m of a forest to those at points
in pastures further than 100 m from a forest. All tables had 270
rows, containing data measured at each point. The soil macrofauna,
landscape metrics, ecosystem services and soil ecosystem services
directly influenced by soil macrofauna had 20, 26, 9 and 8 rows,
respectively. We performed PCA of macrofauna community data,
ln(x + 1) transformed to reduce the effect of dominant taxonomic
units, and tested the effect of land use types with a Monte Carlo test
(Manly, 1991). Co-inertia analyses were performed to test covaria-
tions among datasets (Doledec and Chessel, 1994; Dray et al., 2003).
All statistical analyses were performed with R software (Ihaka and
Gentleman, 1996; R Development Core Team, 2009) using the pack-
ages ade4 (Chessel et al., 2004; Dray and Dufour, 2007; Dray et al.,
2007) and vegan (Oksanen et al., 2008) for multivariate analysis.
3. Results
In total, we collected 26,375 invertebrates (6001 in Colombia
and 20,374 in Brazil). Mean density was 520.9 ± 38.4 (S.E.) ind. m−2 .
Maximum density was 5301.0 ind. m−2 in a primary Brazilian for-
est, with a minimum of 21.3 ind. m−2 in a degraded Colombian
pasture.
3.1. Soil macroinvertebrate density and diversity among
“landscape units”
The mean number of taxonomic units per sample var-
ied significantly among landscape units (Kruskal–Wallis rank
sum test, p < 0.01), from 5.0 ± 0.3 taxa per sample (Colom-
bian “Conventional”) to 10.0 ± 0.3 taxa per sample (Pacajá)
(Fig. 1a). Mean density varied significantly among “landscape units”
(Kruskal–Wallis rank sum test, p < 0.01), from 208.6 ± 23.4 ind. m−2
3.2. Effect of land use on soil macroinvertebrate communities
The first two axes of the PCA for macroinvertebrate commu-
nities accounted for 33.3% of the explained inertia (25.3% and
8.0%, respectively, Fig. 2). Axis 1 clearly contrasted the pantropi-
cal earthworm P. corethrurus, on the positive side of the axis, with
all other taxa, especially Diplopoda, Chilopoda, Gastropoda, Formi-
cidae, Coleoptera and Isoptera, on the negative side. The projection
of sites on the factorial plane suggested that the first axis represents
a land-use gradient, from primary forest (F), fallows after crops (Fc),
cultures (C) to fallows after pastures (Fp), tree plantation (Tp) and
pastures (P). Differences in communities with different types of
land use were significant (20% of variance explained, p < 0.01, Monte
Carlo test) despite the lack of a visible effect along Axis 2, which
ranked sites mainly according to Araneae and Blattaria density.
3.3. Landscape and soil macroinvertebrate communities
Significant covariation (co-inertia analysis: RV = 0.30, p < 0.01,
Monte Carlo test) was observed among macrofauna communi-
ties and landscape metrics. The first axis of the co-inertia analysis
(81.4% variance explained, Fig. 3) associated high densities of
litter-dwelling invertebrates (Diplopoda, Chilopoda, Gastropoda,
Collembola) with forest (F1: primary, F2: exploited, LF: low lying
and F3: burned forest) and percentage of fallow areas and patch
richness. The second axis of the co-inertia analysis (4.9% of vari-
ance explained) associated P. corethrurus density with palm-tree
plantations, agroforestry plantations, and percentage of pastures
with scattered trees. Formicidae, native earthworms and Isoptera
densities inversely covaried with pasture, fodder shrub plantations
and orchards.
Pasture points located within 100 m of a forest had greater
macrofauna density and diversity than pasture points more than
100 m from a forest (Wilcoxon rank sum test, p < 0.01). These
points may, however, have other types of land use such as fal-
lows or crops, which stresses the importance of forest. The density
of Homoptera, Coleoptera, Formicidae, Isoptera, Diptera, Isopoda,
Chilopoda, Diplopoda and Gastropoda followed a similar pattern
(Table 5). Only the density of Isopoda and P. corethrurus were
higher at pasture points more than 100 m from forest than at points
within 100 m (Wilcoxon rank test, p < 0.05), whereas native earth-
worms, Dermaptera, Hemiptera, Orthoptera, Lepidoptera, Blattaria
and Araneae and Opiliones showed no significant differences.
Points in forests with no pasture within 100 m had higher diversity
(Wilcoxon rank test, p = 0.058) and Diplopoda density (Wilcoxon
 R. Marichal et al. / Applied Soil Ecology 83 (2014) 177–185 181

Fig. 1. Taxa per sample (a) and density (b) of soil macrofauna (all groups) under landscape units (logarithmic scale). The boxplots show the lower quartile, the median and
the upper quartile, with whiskers extending to the most extreme data point unless outliers (more than 1.5 times the interquartile range) are present, which are indicated as
open circles. Ind: individuals. (p < 0.01, Kruskal–Wallis rank sum test).

rank sum test, p < 0.05) than those with pasture within 100 m. No
significant differences were observed for the other groups (Table 6).
3.4. Soil macrofauna and ecosystem services
Significant covariation (RV = 0.35, p < 0.01, Monte Carlo test)
was also observed among macrofauna communities and the indi-
cators of ecosystem services (Fig. 4). The first axis of co-inertia
explained 91.6% of the variance and associated Isoptera, Formicidae
and native earthworm densities with macroporosity and infiltrabil-
ity. P. corethrurus density was associated with the morphological
indicator. The second axis of the co-inertia analysis explained
only 2.8% of the variance. Total macroinvertebrate density was
significantly correlated with macroporosity (r2 = 0.42, p < 0.01), par-
ticularly Chilopoda (r2 = 0.43, p < 0.01), Isoptera (r2 = 0.30, p < 0.01)
and Diplopoda (r2 = 0.31, p < 0.01) densities. P. corethrurus density,
located on the opposite side of axis 1, was significantly but barely
correlated with soil aggregation as measured by the morphological
index (r2 = 0.04, p < 0.05). Macrofauna communities also covaried,
although to a lesser extent (RV = 0.34, p < 0.01, Monte Carlo test),
with the set of ecosystem services assumed to be influenced by fau-
nal activities: carbon stocks; water infiltration; plant-available soil
water; macroporosity created by biological activities; soil organic
matter; and soil physical quality, aggregation and fertility mea-
sured by organic, physical, morphological and chemical indicators.
4. Discussion
4.1. Macroinvertebrates, land use and landscape composition
Density and diversity of soil macrofauna were higher in the
less deforested landscape units (Brazilian units of Pacajá and
Maçaranduba, with 40–70% of forest remaining) than in almost
completely deforested areas (Colombian landscapes, with <10%
of forest remaining). They were significantly influenced by land
use at the sampling points. Density of all taxa except P. corethru-
rus decreased along a gradient of deforestation and land-use
intensification, from landscapes dominated by forests and/or

Table 4
Mean densities (ind. m−2 ) of macrofauna taxonomic groups among landscape units. Standard error in parentheses.

Country Brazil Colombia

Landscape unit Maçaranduba Pacaja Palmares Agroforesty Agrosylvo-pastoral Conventional

Dermaptera 2.4 (0.7) 0.4 (0.4) 0.2 (0.2) 0(0) 0(0) 0(0)
Hemiptera 7.8 (2.3) 3.1 (0.7) 13.4 (3.1) 3.2 (0.9) 3.1 (0.6) 2.5 (0.6)
Homoptera 1.2 (0.5) 2 (0.6) 0.9 (0.4) 0(0) 0(0) 0(0)
Coleoptera 62.9 (5.8) 60.6 (7.9) 64.4 (5.4) 6.5 (1.3) 10.9 (2) 14.5 (2.5)
Formicidae 403.8 (103.8) 314.6 (83.7) 130 (19.7) 59.6 (7.3) 51.7 (4.6) 54.9 (5.9)
Isoptera 382.3 (83.0) 312 (72.5) 179 (52.7) 62.8 (13.0) 10.1 (5.0) 9.2 (5.5)
Orthoptera 0.8 (0.3) 1.1 (0.4) 2.3 (0.6) 0.4 (0.2) 1.7 (0.6) 1.4 (0.4)
Lepidoptera (larvae) 3 (1.4) 0.7 (0.3) 2.1 (0.7) 0.6 (0.3) 1.2 (0.5) 1.4 (0.7)
Diptera 10.1 (3.9) 9.7 (1.5) 5.1 (0.9) 0.1 (0.1) 0.1 (0.1) 0.5 (0.5)
Dictyoptera 2.8 (0.6) 2.7 (0.6) 3.6 (0.8) 3.1 (0.7) 5 (1.1) 3.1 (0.9)
Araneae 15.5 (2.7) 9.7 (1.4) 19.1 (3.2) 6.6 (1.2) 10.9 (3.1) 10.5 (2)
Opiliones 0.2 (0.2) 0.6 (0.3) 0.1 (0.1) 1.7 (0.6) 0.6 (0.3) 0(0)
Isopoda 5.1 (2.7) 2.3 (0.6) 10 (2.5) 3 (1.3) 2.7 (1) 2.6 (2)
Native earthworms 43.3 (6.3) 26.9 (4.4) 46.7 (12) 41.2 (6.1) 24.8 (6.1) 17.8 (3.7)
P. corethrurus 35 (7.7) 13.9 (2.6) 2.4 (1.8) 83.7 (13.9) 82.6 (20.5) 109.3 (20.8)
Chilopoda 18.8 (2.7) 36.6 (5.2) 33.7 (4.8) 1.3 (0.5) 0.4 (0.2) 0.4 (0.2)
Diplopoda 36.5 (7.9) 23 (3.7) 19.4 (3.2) 0.5 (0.3) 3 (1.2) 0.4 (0.2)
Gastropoda 7.2 (1.9) 11.3 (3.9) 12.4 (2.8) 0(0) 0(0) 0(0)
182 R. Marichal et al. / Applied Soil Ecology 83 (2014) 177–185

Fig. 2. Ordination of the sampled sites in the factorial plane of a principal component analysis of community structure. (a) Correlation circle. Homo: Homoptera, Col:
Coleoptera, Isopt: Isoptera, Ara: Araneae, Orth: Orthoptera, Lepi: Lepidoptera, N. earth: native earthworms, Derm: Dermaptera, Diplo: Diplopoda, Dip: Diptera, Blat: Blattaria,
Chilo: Chilopoda, Gast: Gastropoda, For: Formicidae, Isopo: Isopoda, Hemi: Hemiptera, Opi: Opiliones. (b) Ordination of the sampled sites in the plane defined by the first two
axes. Letters correspond to the barycenters of sites sampled in each type of land use: F: forests, Fc: fallows after crop, Fp: fallow after pasture, C: crops, Tp: tree plantations,
P: pastures (Monte Carlo test on land uses significant, p < 0.01, Observation = 0.13).

secondary and planted tree covers to landscapes dominated by especially pastures (Barros et al., 2003; Lavelle et al., 1987; Marichal
annual crops and pastures. Densities of Diplopoda, Chilopoda and et al., 2010; Rossi et al., 2010; Sanchez-de Leon et al., 2004). Fallows
Gastropoda, mostly associated with litter abundance in forested derived from pastures or crops were distinctly different, the latter
areas, decreased with deforestation. Formicidae and Isoptera fol- being projected closer to forests on PCA axes 1 and 2 than the for-
lowed a similar trend. An opposite trend was observed for the mer. Soil compaction during the pasture stage (Barros et al., 2003;
earthworm P. corethrurus, an invasive species from the Guyanese Desjardins et al., 2000) probably had an impact on soil fauna at the
Shield (Righi, 1984) associated with human-created land uses, fallow stage. Furthermore, since pastures are generally established
after the crop phase, more time may have elapsed since deforesta-
Table 5 tion. This is probably another reason why fallows after crops, which
Mean macrofauna densities (ind. m−2 ) ± SE at pasture points with and without forest
within a 100 m radius. Table 6
Mean macrofauna densities (ind. m−2 ) ± SE at forest points with and without pasture
Pastures: forest within 100 m radius Wilcoxon
within a 100 m radius.
test
No Yes Forest: pasture within 100 m radius Wilcoxon
Total macrofauna 279.40 ± 26.09 650.00 ± 102.99 *** test
No Yes
Dermaptera 0.16 ± 0.11 1.18 ± 0.87 ns
Hemiptera 3.10 ± 0.52 4.15 ± 1.71 ns Total macrofauna 966.10 ± 211.30 808.20 ± 195.43 ns
Homoptera 0.00 ± 0.00 0.99 ± 0.40 ***
Dermaptera 2.17 ± 0.91 0.97 ± 0.57 ns
Coleoptera 18.32 ± 2.61 70.67 ± 11.84 ***
Hemiptera 7.50 ± 3.17 3.15 ± 0.83 ns
Formicidae 69.50 ± 12.92 166 ± 36.09 **
Homoptera 1.58 ± 0.56 0.73 ± 0.53 ns
Isoptera 34.15 ± 10.43 276.60 ± 81.62 ***
Coleoptera 53.30 ± 6.88 52.57 ± 6.18 ns
Orthoptera 1.19 ± 0.29 1.38 ± 0.73 ns Formicidae 400.30 ± 161.11 395.60 ± 167.44 ns
Lepidoptera (larvae) 1.50 ± 0.40 3.16 ± 2.22 ns Isoptera 309.30 ± 111.15 209.60 ± 70.73 ns
Diptera 0.67 ± 0.27 9.87 ± 6.03 ***
Orthoptera 1.58 ± 0.48 0.97 ± 0.44 ns
Blattaria 3.47 ± 0.61 1.97 ± 0.71 ns Lepidoptera (larvae) 1.97 ± 0.65 0.73 ± 0.40 ns
Araneae 10.04 ± 1.67 8.09 ± 1.96 ns Diptera (larvae) 9.67 ± 2.51 10.42 ± 2.33 ns
Opiliones 0.10 ± 0.07 0.00 ± 0.00 ns Blattaria 3.75 ± 0.84 4.36 ± 1.43 ns
Isopoda 2.64 ± 1.03 2.17 ± 0.59 *
Araneae 21.71 ± 5.34 21.08 ± 3.57 ns
Native earthworms 25.62 ± 3.66 28.62 ± 7.37 ns Opiliones 0.59 ± 0.33 0.97 ± 0.45 ns
P. corethrurus 102.30 ± 13.13 32.57 ± 10.63 *
Isopoda 10.07 ± 4.97 6.06 ± 2.44 ns
Chilopoda 0.93 ± 0.35 20.33 ± 5.15 ***
Native earthworms 40.67 ± 2.44 27.13 ± 4.97 ns
Diplopoda 4.61 ± 1.96 16.58 ± 4.97 ***
P. corethrurus 11.84 ± 3.24 7.75 ± 2.92 ns
Gastropoda 0.98 ± 0.50 4.54 ± 1.01 ***
Chilopoda 35.34 ± 6.87 37.31 ± 6.50 ns
Diplopoda 41.65 ± 10.89 20.35 ± 4.88 *
ns: p > 0.05.
*
Gastropoda 12.44 ± 3.44 7.99 ± 4.78 ns
p < 0.05.
** ns: p > 0.05.
p < 0.01.
*** *
p < 0.001. p < 0.05.
 R. Marichal et al. / Applied Soil Ecology 83 (2014) 177–185 183

Fig. 3. Results of co-inertia analysis between soil macrofauna and landscape metrics at the point level (radius of 50 m). (a) Contribution of soil macrofauna taxa densities
(identified by their positions on the first two co-inertia axes) to the correlation with landscape metrics. Homo: Homoptera, Col: Coleoptera, Isopt: Isoptera, Ara: Araneae, Orth:
Orthoptera, Lepi: Lepidoptera, N.earth: native earthworms, Derm: Dermaptera, Diplo: Diplopoda, Blat: Blattaria, Chilo: Chilopoda, Gast: Gastropoda, For: Formicidae, Isopo:
Isopoda, Dip: Diptera, Hemi: Hemiptera, Opi: Opiliones. (b) Contribution of landscape metrics (identified by their positions on the first two co-inertia axes) to the correlation
with macrofauna taxa densities. PR: patch richness, Ltypo: landscape dynamic typology, landscape composition (% of land use): P1: pasture, P2: pasture with babaçu, P3:
pasture with trees, P4: pasture with scattered trees, C: crops, O: orchard, CP: cocoa plantation, AP: açaï plantation, PP: African palm-tree plantation, AP: agroforestry plantation,
SP: fodder shrub plantation, YFP: young fallow after pasture, OFP: old fallow after pasture, YFC: young fallow after crop, OFC: old fallow after crop, B: babaçus, F3: burned
forest, F2: exploited forest, F1: forest, LF: lowland forest, LP: lowland pasture, LB: lowland bush, BS: bare soil, R: river or pond. RV = 0.30, p < 0.01.

generally start 2–3 years after deforestation, have greater macro-
fauna density and diversity than fallows after pastures (Mathieu
et al., 2005).
Fallows after crops had similar macrofauna diversity and density
as forests, which confirms that they may contribute significantly
to the conservation of soil macrofauna (Mathieu et al., 2005) and
aboveground biodiversity (Barlow et al., 2007).
Percentages of pasture, old fallows after pasture and fodder
shrub plantations were associated with low soil fauna density and
diversity. Our results indicated that land-use composition (mea-
sured by patch richness and percentages of land use types within a
100 m radius around the sampling point) is an important determi-
nant of macrofauna communities. For example, pasture points with
forest within 100 m had higher macrofauna densities and diversity
than pasture points with no forest within 100 m. Most macroinver-
tebrate taxa followed this pattern, showing that nearby forest can
be a “source” of forest fauna in a pasture (Dias, 1996; Pulliam, 1988)
or can increase the suitability of environmental conditions for soil
fauna by affecting a pasture’s microclimate. An exception was P.
corethrurus, which had higher densities in pastures with no forest
within 100 m than in pastures with forest within 100 m. Diversity
of soil macrofauna and Diplopoda densities at forest points with
pasture within 100 m were lower than at forest points with only
forest within 100 m. This pattern could be a consequence of the
“edge effect” associated with fragmentation (Gascon et al., 2000;
Laurance et al., 2001), since wind and light penetrating deeply into
a forest can change its animal and plant communities (Didham et al.,
1998).
Time since deforestation of the original forest ecosystem and
rate of deforestation (expressed in the landscape integrity param-
eter) was the most important factor determining diversity and
densities of soil macrofauna communities, followed by the relative
percentage of forest cover. This result emphasizes the importance
of time since deforestation, regardless of land use (Mathieu et al.,
2005).
4.2. Macroinvertebrates and soil ecosystem services
Soil invertebrates are both actors and indicators of soil services.
Soil invertebrates, mainly earthworms, are known to consider-
ably influence types and rates of soil services in diverse ways
(Blouin et al., 2013; Lavelle et al., 2006). An increase in their
densities is thus expected to increase the provision of services
(an effect mechanism). This type of relation may also result from
community responses to increases in services caused by other fac-
tors (a response mechanism), such as organic matter storage or
nutrient accumulation in clayey soils (Lavelle and Spain, 2001).
Invasion by P. corethrurus results in a significant increase in soil
macroaggregation due to the high production of solid casts in the
soil (Lavelle et al., 1994). Significant covariation observed between
184 R. Marichal et al. / Applied Soil Ecology 83 (2014) 177–185

Fig. 4. Results of co-inertia analysis between soil macrofauna and indicators of ecosystem services. (a) Contribution of soil macrofauna taxa densities (identified by their
positions on the first two co-inertia axes) to the correlation with ecosystem service indicators. Homo: Homoptera, Col: Coleoptera, Isopt: Isoptera, Ara: Araneae, Orth:
Orthoptera, Lepi: Lepidoptera, N. earth: native earthworms, Derm: Dermaptera, Diplo: Diplopoda, Dip: Diptera, Chilo: Chilopoda, Gast: Gastropoda, For: Formicidae, Isopo:
Isopoda, Blat: Blattaria, Hemi: Hemiptera, Opi: Opiliones. (b) Contribution of soil ecosystem services (identified by their positions on the first two co-inertia axes) to the
correlation with macrofauna taxa densities. BCStree: tree and shrub carbon biomass; Physical, morphological, chemical, organic: indicators of soil physical, morphological,
chemical and organic quality, respectively; SCS030: soil carbon stock (0–30 cm deep), AW010: plant-available soil water (0–10 cm deep), INFIL: water infiltration into the
soil Macro010: soil macroporosity (0–10 cm deep), INFIL: water infiltration into the soil. RV = 0.35, p < 0.01.

native earthworm density and macroporosity is consistent with the Acknowledgements

known effects of earthworm burrowing and bioturbation activities
on these indicators of soil services (Blouin et al., 2013). However,
mesocosm experiments have shown that effects of earthworms
on soil functioning depend on land use (Hedde et al., 2013); this
aspect requires further investigation in the Amazonian context.
Soil macrofauna influences several soil properties, but the distri-
bution of species can be influenced by soil properties (Marichal
et al., 2012; Vasconcellos et al., 2013). Covariation with carbon in
aboveground plant biomass, in contrast, simply reflects the fact that
native earthworm density is higher in forests than in other land uses
(Fragoso et al., 1997; Marichal et al., 2010; Rombke and Verhaagh,
1992). Significant covariations of Formicidae and Isoptera densi-
ties with plant-available soil water and macroporosity also suggest
that these taxa influence the ecosystem services indicated by these
properties (Cowan et al., 1985; Lockaby and Adams, 1985). These
soil ecosystem engineers can dig networks of galleries and cham-
bers, with known effects on macroporosity, aeration and infiltration
(Folgarait, 1998; Lobry de Bruyn and Conacher, 1990; Mando et al.,
1996). This is not the case for Chilopoda or Diplopoda, which take
advantage of existing forest conditions; these taxa are thus more
indicators of than actors on soil services.
5. Conclusion
Soil macrofauna communities respond to land use, landscape
dynamics and composition, and their links to soil services makes
them good indicators of soil ecosystem services. Therefore, the
potential of using soil invertebrates to assess soil ecosystem ser-
vices is confirmed by our study. Further studies are needed,
however, to directly quantify effects of soil macrofauna on soil
services and link them to biological “effect” traits (Lavorel and
Garnier, 2002) involved in supplying services. This next step would
lead to the development of soil-service indicators calculated from
percentages or frequencies of biological traits.
This work was a part of the AMAZ project (ANR-06-PADD-
001-011 and ANR 06 BIODIV 009-01, coordinator: Patrick Lavelle)
supported by the ANR (Agence Nationale de la Recherche, France)
and CNPq (Conselho Nacional de Desenvolvimento Científico e Tec-
nológico) and jointly implemented by IRD (Institut de Recherche pour
le Développement), UFPA (Universidade Federal do Pará), UFRA (Uni-
versidade Federal Rural da Amazônia), MPEG (Museu Paraense Emílio
Goeldi), UTP (Universidad Tecnológica de Pereira–Colombia), and
CIAT (Colombia). We thank Andres F. Carvajal for helping to sample
and separate macrofauna, Edward Guevara for landscape metrics,
Max Sarrazin for soil analysis, and all those who participated in
field and laboratory activities (students, technicians, farmers, field
workers). We also thank ECOS Colombia (AMAZ AGREG project,
ECOS6 Nord/COLCIENCIAS//ICETEX).
References
Anderson, J.L., Ingram, J.S.I., 1993. Tropical Soil Biology and Fertility. A Handbook of
Methods, 2nd ed, Wallingford, UK.
Barlow, J., Gardner, T.A., Araujo, I.S., Avila-Pires, T.C., Bonaldo, A.B., Costa, J.E., Espos-
ito, M.C., Ferreira, L.V., Hawes, J., Hernandez, M.I.M., Hoogmoed, M.S., Leite, R.N.,
Lo-Man-Hung, N.F., Malcolm, J.R., Martins, M.B., Mestre, L.A.M., Miranda-Santos,
R., Nunes-Gutjahr, A.L., Overal, W.L., Parry, L., Peters, S.L., Ribeiro-Junior, M.A.,
da Silva, M.N.F., da Silva Motta, C., Peres, C.A., 2007. Quantifying the biodi-
versity value of tropical primary, secondary, and plantation forests. PNAS 104,
18555–18560.
Barros, E., Grimaldi, M., Sarrazin, M., Chauvel, A., Mitja, D., Desjardins, T., Lavelle,
P., 2003. Soil physical degradation and changes in macrofaunal communities in
Central Amazon. Appl. Soil Ecol. 26, 157–168.
Barros, E., Pashanasi, B., Constantino, R., Lavelle, P., 2002. Effects of land-use sys-
tem on the soil macrofauna in western Brazilian Amazonia. Biol. Fertil. Soils 35,
338–347.
Blouin, M., Hodson, M.E., Delgado, E.A., Baker, G., Brussaard, L., Butt, K.R., Dai, J.,
Dendooven, L., Peres, G., Tondoh, J.E., Cluzeau, D., Brun, J.J., 2013. A review of
earthworm impact on soil function and ecosystem services. Eur. J. Soil Sci. 64,
161–182.
Brussaard, L., de Ruiter, P.C., Brown, G.G., 2007. Soil biodiversity for agricultural
sustainability. Agric. Ecosyst. Environ. 121, 233–244.
 R. Marichal et al. / Applied Soil Ecology 83 (2014) 177–185
Carvalho, K.S., Vasconcelos, H.L., 1999. Forest fragmentation in central Amazonia
and its effects on litter-dwelling ants. Biol. Conserv. 91, 151–157.
Chessel, D., Dufour, A.B., Thioulouse, J., 2004. The ade4 package-I-One-table meth-
ods. R News 4, 5–10.
Cowan, J.A., Humphreys, G.S., Mitchell, P.B., Murphy, C.L., 1985. An assessment of
pedoturbation by two species of mound-building ants, Camponotus intrepidus
(Kirby) and Iridomyrmex purpureus (F. Smith). Aust. J. Soil Res. 22, 95–107.
Decaëns, T., 2010. Macroecological patterns in soil communities. Global. Ecol. Bio-
geogr. 19, 287–302.
Decaens, T., Jimenez, J.J., Barros, E., Chauvel, A., Blanchart, E., Fragoso, C., Lavelle,
P., 2004. Soil macrofaunal communities in permanent pastures derived from
tropical forest or savanna. Agric. Ecosyst. Environ. 103, 301–312.
Desjardins, T., Lavelle, P., Barros, E., Brossard, M., Chapuis-Lardy, L., Chauvel, A.,
Grimaldi, M., Guimaraes, F., Martins, P., Mitja, D., Muller, M., Sarrazin, M., Tavares
Fiho, J., Topall, O., 2000. Dégradation des pâturâges amazoniens. Description d’un
syndrome et de ses déterminants. Etude et gestion des sols 7, 353–378.
Dias, C.D., 1996. Sources and sinks in population biology. Trends Ecol. Evol. 11,
326–330.
Didham, R.K., Hammond, P.M., Lawton, J.H., Eggleton, P., Stork, N.E., 1998. Beetle
species respond to tropical forest fragmentation. Ecol. Monogr. 68, 295–323.
Doledec, S., Chessel, D., 1994. Co-inertia analysis: an alternative method for studying
species-environment relationships. Freshw. Biol. 31, 277–294.
Dray, S., Chessel, D., Thioulouse, J., 2003. Co-inertia analysis and the linking of eco-
logical tables. Ecology 84, 3078–3089.
Dray, S., Dufour, A.B., 2007. The ade4 package: implementing the duality diagram
for ecologists. J. Stat. Softw. 22, 1–20.
Dray, S., Dufour, A.B., Chessel, D., 2007. The ade4 package-II: two-table and K-table
methods. R News 7, 47–52.
Ferraz, S.F.D., Vettorazzi, C.A., Theobald, D.M., Ballester, M.V.R., 2005. Landscape
dynamics of Amazonian deforestation between 1984 and 2002 in central Ron-
donia, Brazil: assessment and future scenarios. For. Ecol. Manag. 204, 67–83.
Folgarait, P.J., 1998. Ant biodiversity and its relationship to ecosystem functioning:
a review. Biodivers. Conserv. 7, 1221–1244.
Fragoso, C., Brown, G.G., Patron, J.C., Blanchart, E., Lavelle, P., Pashanasi, B., Senapati,
B., Kumar, T., 1997. Agricultural intensification, soil biodiversity and agroecosys-
tem function in the tropics: the role of earthworms. Appl. Soil Ecol. 6, 17–35.
Gascon, C., Williamson, G.B., da Fonseca, G.A.B., 2000. Receding forest edges and
vanishing reserves. Science 288, 1356–1358.
Hedde, M., Bureau, F., Delporte, P., Cecillon, L., Decaens, T., 2013. The effects of earth-
worm species on soil behaviour depend on land use. Soil Biol. Biochem. 65,
264–273.
Hollander, M., Wollfe, D.A., 1973. Non-parametric statistical methods. John Wiley &
Sons, New York.
Ihaka, R., Gentleman, R., 1996. R: a language for data analysis and graphics. Comput.
Graph. Stat. 5, 299–314.
INPE-PRODES, 2010. Monitoramento da floresta amazônica brasileira por satélite.
www.obt.inpe.br/prodes
Kruskal, W.H., Wallis, W.A., 1952. Use of ranks in one-criterion variance analysis. J.
Am. Stat. Assoc. 47, 583–621.
Lassabatere, L., Angulo-Jaramillo, R., Ugalde, J.M.S., Cuenca, R., Braud, I., Haverkamp,
R., 2006. Beerkan estimation of soil transfer parameters through infiltration
experiments – BEST. Soil Sci. Soc. Am. J. 70, 521–532.
Laurance, W.F., Lovejoy, T.E., Vasconcelos, H.L., Bruna, E.M., Didham, R.K., Stouffer,
P.C., Gascon, C., Bierregaard, R.O., Laurance, S.G., Sampaio, E., 2001. Ecosystem
decay of Amazonian forest fragments: a 22-year investigation. Conserv. Biol. 16,
605–618.
Lausch, A., Herzog, F., 2002. Applicability of landscape metrics for the monitoring of
landscape change: issues of scale, resolution and interpretability. Ecol. Indic. 2,
3–15.
Lavelle, P., 2002. Functional domains in soils. Ecol. Res. 17, 441–450.
Lavelle, P., Barois, I., Cruz, I., Fragoso, C., Hernandez, A., Pineda, A., Rangel, P., 1987.
Adaptative strategies of Pontoscolex corethrurus (Glossoscolecidae, Oligochaete),
a peregrine geophageous earthworm of the humid tropics. Biol. Fertil. Soils 5,
188–194.
Lavelle, P., Bignell, D., Lepage, M., Wolters, V., Roger, P., Ineson, P., Heal, O.W., Dhillion,
S., 1997. Soil function in a changing world: the role of invertebrate ecosystem
engineers. Eur. J. Soil Biol. 33, 159–193.
Lavelle, P., Dangerfield, M., Fragoso, C., Eschenbrenner, V., Lopez-Hernandez, D.,
Pashanasi, B., Brussaard, L., 1994. The relationship between soil macrofauna and
tropical soil fertility. In: Swift, M.J., Woomer, P. (Eds.), Tropical Soil Biology and
Fertility. John Wiley-Sayce, New York, pp. 137–169.
Lavelle, P., Decaen, T., Aubert, M., Barot, S., Blouin, M., Bureau, F., Margerie, P., Mora,
P., Rossi, J.-P., 2006. Soil invertebrates and ecosystem services. Eur. J. Soil Biol.
42, S3–S15.
Lavelle, P., Pashanasi, B., 1989. Soil macrofauna and land management in Peruvian
Amazonia (Yurimaguas, Loreto). Pedobiologia 33, 283–291.
Lavelle, P., Spain, A.V., 2001. Soil ecology. Kluwer Scientific Publications, Amsterdam.
Lavorel, S., Garnier, E., 2002. Predicting changes in community composition and
ecosystem functioning from plant traits: revisiting the Holy Grail. Funct. Ecol.
16, 545–556.
Lavit, C., Escoufier, Y., Sabatier, R., Traissac, P., 1994. The act (statis method). Comput.
Stat. Data Anal. 18, 97–119.
Le Tourneau, J.-F., 2004. Jusqu’au bout de la forêt? Causes et mécanismes de la
déforestation en Amazonie brésilienne, M@ppemonde 75.
Lobry de Bruyn, L.A., Conacher, A.J., 1990. The role of termites and ants in soil mod-
ification: a review. Aust. J. Soil Res. 28, 88–93.
185
Lockaby, B.G., Adams, J.C., 1985. Pedoturbation of a forest soil by fire ants. Soil Sci.
Soc. Am. J. 49, 220–223.
Louzada, J., Lima, A.P., Matavelli, R., Zambaldi, L., Barlow, J., 2010. Community struc-
ture of dung beetles in Amazonian savannas: role of fire disturbance, vegetation
and landscape structure. Landsc. Ecol. 25, 631–641.
Mando, A., Stroosnijder, L., Brussaard, L., 1996. Effects of termites on infiltration into
crusted soil. Geoderma 74, 107–113.
Manly, B.F.J., 1991. Randomization and Monte Carlo Methods in Biology. Chapman
and Hall, London.
Marichal, R., Feijoo, M.A., Praxedes, C., Ruiz, D., Carjaval, A.F., Oszwald, J., del Pilar
Hurtado, M., Brown, G.G., Grimaldi, M., Desjardins, T., Sarrazin, M., Decaens, T.,
Velasquez, E., Lavelle, P., 2010. Invasion of Pontoscolex corethrurus (Glossoscole-
cidae, Oligochaeta) in landscapes of the Amazonian deforestation arc. Appl. Soil
Ecol. 46, 443–449.
Marichal, R., Grimaldi, M., Mathieu, J., Brown, G.G., Desjardins, T., da Silva, M.L.,
Praxedes, C., Martins, M.B., Velasquez, E., Lavelle, P., 2012. Is invasion of defor-
ested Amazonia by the earthworm Pontoscolex corethrurus driven by soil texture
and chemical properties? Pedobiologia 55, 233–240.
Mathieu, J., Grimaldi, M., Jouquet, P., Rouland, C., Lavelle, P., Desjardins, T., Rossi,
J.P., 2009. Spatial patterns of grasses influence soil macrofauna biodiversity in
Amazonian pastures. Soil Biol. Biochem. 41, 586–593.
Mathieu, J., Rossi, J.-P., Grimaldi, M., Mora, P., Lavelle, P., Rouland, C., 2004. A multi-
scale study of soil macrofauna biodiversity in Amazonian pastures. Biol. Fertil.
Soils 40, 300–305.
Mathieu, J., Rossi, J.-P., Mora, P., Lavelle, P., Martins, P.F.D.S., Rouland, C., Grimaldi, M.,
2005. Recovery of soil macrofauna communities after forest clearance in Eastern
Amazonia, Brazil. Conserv. Biol. 19, 1598–1605.
McGarigal, K., Cushman, S.A., Neel, M.C., Ene, E., 2002. FRAGSTATS: Spatial Pattern
Analysis Program for Categorical Maps. Computer Software Program Produced
by the Authors at the University of Massachusetts, Amherst, USA, Available at
http://www.umass.edu/landeco/research/fragstats/fragstats.html
Millennium Ecosystem Assessment, www.millenniumassessment.org
Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Simpson, G.L., Stevens, M.H.A., Wagner,
H., 2008. vegan: Community Ecology Package.
Oszwald, J., Gond, V., Doledec, S., Lavelle, P., 2011. Identification d’indicateurs de
changement d’occupation du sol pour le suivi des mosaïques paysagères. Bois
et Forêts des Tropiques 307, 7–21.
Pansu, M., Gautheyrou, J., 2006. Handbook of Soil Analysis: Mineralogical, Organic
and Inorganic Methods. Springer.
Pulliam, H.R., 1988. Sources, sinks, and population regulation. Am. Nat. 132,
652–661.
R-Development-Core-Team, 2009. R: A Language and Environment for Statistical
Computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-
900051-07-0, Available at http://www.R-project.org
Righi, G., 1984. Pontoscolex (Oligochaeta, Glossoscolecidae), a new evaluation. Stud.
Neotrop. Fauna Environ. 19, 159–177.
Rombke, J., Verhaagh, M., 1992. About earthworm communities in a rain forest and
an adjacent pasture in Peru. Amazoniana XII, 29–49.
Rossi, J.-P., Celini, L., Mora, P., Mathieu, J., Lapied, E., Nahmani, J., Ponge, J.F., Lavelle,
P., 2010. Decreasing fallow duration in tropical slash-and-burn agriculture alters
soil macroinvertebrate diversity: a case study in southern French Guiana. Agric.
Ecosyst. Environ. 135, 148–154.
Rousseau, G.X., Deheuvels, O., Arias, I.R., Somarriba, E., 2012. Indicating soil quality
in cacao-based agroforestry systems and old-growth forests: the potential of
soil macrofauna assemblage. Ecol. Indic. 23, 535–543.
Rousseau, G.X., Silva, P.R.d.S., de Carvalho, C.J.R., 2010. Earthworms, ants
and other arthropods as soil health indicators in traditional and no-fire
agro-ecosystems from Eastern Brazilian Amazonia. Acta Zool. Mex. 26,
117–134.
Ruiz-Camacho, N., Velasquez, E., Pando, A., Decaens, T., Dubs, F., Lavelle, P.,
2009. Indicateurs synthétiques de la qualité du sol. Etude et gestion des sols
16.
Sanchez-de Leon, Y., Zou, X., Borges, S., Ruan, H., 2004. Recovery of native earth-
worms in abandoned tropical pastures. Conserv. Biol. 17, 999–1006.
Siegel, S., Castellan, N.J., 1988. Non Parametric Statistics for the Behavioural Sciences.
MacGraw Hill Int., New York.
Silva Costa, L.G., Miranda, I.S., Grimaldi, M., Silva, M.L., Mitja, D., Lima, T.T.S., 2012.
Biomass in different types of land use in the Brazil’s ‘arc of deforestation’. For.
Ecol. Manage. 278, 101–109.
Turbe, A., De Toni, A., Benito, P., Lavelle, P., Lavelle, P., Ruiz, N., Van der Putten, W.H.,
Labouze, E., Mugdal, S., 2010. Soil biodiversity: functions, threats and tools for
policy makers. Bio Intelligence Services, IRD and NIOO. Report for European
Commission (DG Environment)., pp. 250.
van Eekeren, N., de Boer, H., Hanegraaf, M., Bokhorst, J., Nierop, D., Bloem, J.,
Schouten, T., de Goede, R., Brussaard, L., 2010. Ecosystem services in grass-
land associated with biotic and abiotic soil parameters. Soil Biol. Biochem. 42,
1491–1504.
Vasconcellos, R.L.F., Segat, J.C., Bonfim, J.A., Baretta, D., Cardoso, E.J.B.N., 2013. Soil
macrofauna as an indicator of soil quality in an undisturbed riparian forest and
recovering sites of different ages. Eur. J. Soil Biol. 58, 105–112.
Velasquez, E., Lavelle, P., Andrade, M., 2007a. GISQ, a multifunctional indicator of
soil quality. Soil Biol. Biochem. 39, 3066–3080.
Velasquez, E., Pelosi, C., Brunet, D., Grimaldi, M., Martins, M., Rendeiro, A.C., Barrios,
E., Lavelle, P., 2007b. This ped is my ped: visual separation and near infrared
spectra allow determination of the origins of soil macroaggregates. Pedobiologia
51, 75–87.