Ecological Indicators 27 (2013) 71–82

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Soil macrofauna as indicators of soil quality and land use impacts in smallholder
agroecosystems of western Nicaragua
Laurent Rousseau a , Steven J. Fonte b,∗ , Orlando Téllez c , Rein van der Hoek c , Patrick Lavelle a,b
a
Institut de Recherche pour le Développement (IRD), 93143 Bondy Cedex, France
b
Centro Internacional de Agricultura Tropical (CIAT), Tropical Soil Biology and Fertility Program, Latin American and Caribbean Region, Cali, Colombia
c
Centro Internacional de Agricultura Tropical (CIAT), Tropical Forages Program, Managua, Nicaragua

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

Article history: The tropical dry forest region along the western slope of Central America represents a biodiverse and
Received 11 July 2012 fragile area that is under increasing pressure from agricultural production, thus threatening the provi-
Received in revised form sion of ecosystem services, the integrity of these landscapes, and the rural communities who depend on
26 November 2012
them. To address this issue, we evaluated the influence of common agricultural management practices
Accepted 29 November 2012
(cropping and livestock systems) vs. the Quesungual slash-and-mulch agroforestry system (QSMAS) on
diverse parameters of soil quality and function. We then used this information to identify soil inver-
Keywords:
tebrate bioindicators that represent key aspects of soil quality (chemical fertility, physical properties,
Bioindicators
Forest conversion
aggregate morphology, and biological functioning). In February of 2011 soil sampling was conducted on
Indicator Value Index six hillside farms near the town of Somotillo in western Nicaragua to assess soil properties and the abun-
Quesungual slash-and-mulch agroforestry dance and diversity of soil macrofauna within four management systems: (1) QSMAS, based on maize
system production, (2) traditional maize cropping system with few trees (TC), (3) silvopastoral system with low
Soil ecosystem services tree density (SP), and (4) secondary forest (SF), used as a reference. The conversion of forest to agriculture
Soil invertebrates demonstrated the greatest impact of management in this study. For example, SF presented significantly
higher diversity of soil invertebrate taxonomic groups than either TC or SP (P < 0.03), and demonstrated
the lowest level of soil compaction, significantly less than SP (P < 0.05). Additionally, SF demonstrated
the highest value of soil quality according to a synthetic indicator that integrates chemical, physical and
biological aspects of soil quality. Although overall soil quality under QSMAS was lower than SF, this sys-
tem demonstrated the highest abundance (number of individuals) of soil macrofauna, and appeared to
at least partially mitigate the negative consequences of forest conversion on soil functioning. Using the
Indicator Value Index, which ranks species according to their specificity and fidelity across sites, along
with farmer consultation we found seven indicator taxa of soil quality that could greatly facilitate future
evaluation of land management impacts by farmers and technicians in the region. We suggest that the
methodology applied is robust and adaptable to diverse agroecological contexts and would allow for
more rapid responses to evolving land use issues as they arise.
© 2012 Elsevier Ltd. All rights reserved.

1. Introduction
Overuse of land and poor management practices have led to
extensive degradation of biodiversity and ecosystem services glob-
ally (Foley et al., 2005; Giller et al., 1997). This trend is particularly
concerning in smallholder agroecosystems of Central America that
are often located on highly susceptible hillside soils and dominated
by biologically diverse tropical dry forests. Traditional management
in this region (including slash and burn) typically eliminates soil
cover and organic matter inputs prior to planting, thus leaving soils
∗ Corresponding author at: CIAT, A.A. Postal 6713, Cali, Colombia.
Tel.: +57 2 445 0100x3517; fax: +57 2 445 0073.
E-mail address: s.fonte@cgiar.org (S.J. Fonte).
exposed to erosion and soil organic matter (SOM) loss. Under such
conditions crop yields can decrease considerably after only a few
years. Production plots must then be abandoned and left to fal-
low for long intervals to allow adequate soil regeneration (Szott
et al., 1999). A growing trend of shortening fallows along with
increased grazing pressure in these systems inhibits the recovery
of soils and forests (Lopez Hernandez et al., 1997; Netuzhilin et al.,
1999) and thus, severely threatens long-term agricultural produc-
tivity, food security, and the provision of ecosystem services in the
region.
In addressing this threat, farmers, researchers and technicians
must find adequate ecologically-based management alternatives to
control soil erosion, maintain soil functioning, and enhance agroe-
cosystem resilience and biodiversity (Perfecto and Vandermeer,
2008). The Quesungual slash-and-mulch agroforestry system

1470-160X/$ – see front matter © 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ecolind.2012.11.020
72 L. Rousseau et al. / Ecological Indicators 27 (2013) 71–82
(QSMAS), originating in south-western Honduras (Lempira Dept.),
represents such a management alternative that holds great promise
for hillside farmers throughout the region. This system relies upon a
diverse assemblage of native tree species interspersed with annual
crops (corn, beans and sorghum) to stabilize hillsides, promote soil
fertility, and conserve vital soil moisture (Hellin et al., 1999). Rather
than clearing or burning, trees are pruned annually and the residues
left on the soil surface as mulch to promote soil biological activity
and SOM accumulation (Fonte and Six, 2010). In addition to greatly
extending the productive phase of these agroecosystems (from 1 to
3 years under slash-and-burn to more than 7 years under QSMAS),
the Quesungual system has shown remarkable resilience in the face
of hurricanes and drought, thus facilitating its adoption and adap-
tation throughout similar climate zones of Mesoamerica (Ayarza
and Welchez, 2004).
While the existence and successful dissemination of systems
such as QSMAS is encouraging, much work remains in under-
standing the biophysical drivers of ecosystem degradation and the
effectiveness of alternative management practices to mitigate these
impacts under diverse socioeconomic and environmental condi-
tions. In addition, simple monitoring tools are needed to quickly
and inexpensively evaluate key ecosystem parameters and func-
tions (Dale and Beyeler, 2001). Bioindicators (species or taxa used
for monitoring ecosystem health or function) offer a promising
means for scientists, technicians and farmers to quickly gauge
the effectiveness of new alternative land management strate-
gies and allow for a better informed response in addressing new
issues as they arise (Lobry de Bruyn, 1997; McGeoch, 1998).
Much of the past research on identifying bioindicator species has
focused on characterizing particular habitats or land use condi-
tions (Cristofoli et al., 2010; Dufrêne and Legendre, 1997; Ruiz
et al., 2011). Substantially less effort has sought to link indicator
taxa with targeted ecosystem functions and services. We address
this issue by relating invertebrate taxa to synthetic indicators
of soil quality that combine a suite of statistically selected soil
attributes that embody key soil functions (e.g., chemical fertility,
hydrologic services). We then validate these bioindicators against
local knowledge of these species and their role in agroecosys-
tems.
In this study, we focus on soil macrofauna for evaluating impacts
of agroecosystem management and in their use as potential biolog-
ical indicators of soil quality. The emphasis on soil macrofauna is
based on several criteria. First, this group is sensitive to changes
in their environment and shifts in their community structure offer
an integrative assessment (i.e., combining changes in multiple soil
properties into a single measure) of ecosystem impacts over time
(Lobry de Bruyn, 1997; Mathieu et al., 2005; Paoletti, 1999). Sec-
ond, soil macrofauna, particularly ecosystem engineers (e.g. ants,
earthworms), can have significant influences on soil and ecosystem
functioning and thus their populations reflect key ecological pro-
cesses within agroecosystems (Lavelle et al., 2006). Finally, large
soil invertebrates are relatively simple to measure, ubiquitous, and
familiar to farmers, as they are frequently encountered during soil
preparation and field maintenance.
The research presented here sought to address two main objec-
tives. First, we sought to examine the impacts of traditional land
management on soil quality and functioning and to better under-
stand the potential of the Quesungual agroforestry system to
ameliorate the deleterious impact of agriculture in this region on
soil-based ecosystem services and biodiversity. Second, we sought
to associate soil macrofauna taxa, indentified using the Indicator
Value Index method (IndVal; Dufrêne and Legendre, 1997), with
different states of soil biological, chemical and physical quality
(Velasquez et al., 2007a) and then to validate these bioindicators
with local land managers for potential use in monitoring changes
in soil quality and function.
2. Materials and methods
2.1. Sites description and experimental design
The study was conducted in the community of La Danta, located
in western Nicaragua, near Somotillo, in the Chinandega Depart-
ment (13◦ 09 09 N, 86◦ 51 32 W). Classified as a tropical dry forest
zone according to Holdridge (1947), rainfall varies between 700 and
1500 mm year−1 and occurs largely between May and October, with
a pronounced dry season from November to April. Average temper-
atures range from 24 ◦ C in the wet season to 35 ◦ C in the dry season.
The topography is hilly with elevations ranging from 200 to 350 m.
The landscape is comprised of approximately 25% forested areas,
30% crops (including agroforestry components) and 45% pastures
(INTA, 2005). Soils are mainly sandy-textured with a high stone
content and are represented by a mix of alfisols (28%), entisols
(23%), molisols (44%), inceptisols/vertisols (5%) (Calero Calderón,
2008).
Six replicate farms were chosen for the study, each contain-
ing four common types of land use management (treatments)
in the region: (1) traditional cropping system (TS) – with few
trees and low organic matter inputs, (2) silvopastoral system
(SP) – with naturalized pastures, low densities of native trees
and shrubs and frequent livestock entry, (3) Quesungual slash-
and-mulch agroforestry system (QSMAS) and (4) secondary forest
(SF), as a reference system. Within each replicate farm, four plots
representing the above management types (roughly 1 ha each)
were selected for all measurements. In the two cropping sys-
tems (TS and QSMAS), maize (Zea mays) is typically sown in
early May and common bean (Phaseolus vulgaris) in August with
harvest of both crops in late November. Both cropping systems
also receive moderate amounts of fertilizer (average 70 kg NPK
and 70 kg urea ha−1 year−1 ) and pesticides (typically Glyphosate at
maize planting and insecticides as needed), while SP only receives
herbicides prior to seeding.
The majority of the soil sampling was conducted over a two
week period in February of 2011, during the dry season. Soil
samples were taken at three equally-spaced points along a 30 m
transect cutting diagonally through the middle of each plot. In total,
72 points were sampled in 24 plots within the landscape. A second
partial sampling was undertaken at the start of the wet season to
better evaluate key soil physical properties (penetration resistance
and shear strength).
2.2. Soil macrofauna abundance and biodiversity
In February 2011, sampling of soil macroinvertebrates (>2 mm
in size; Lavelle and Spain, 2001) was carried out using the TSBF
method (Tropical Soil Biology and Fertility; Anderson and Ingram,
1993). In brief, a pit (25 cm × 25 cm × 30 cm deep) was excavated
and soil macrofauna were collected by hand from the litter layer
and 3 soils depths (0–10 cm, 10–20 cm and 20–30 cm), placed
in 70% alcohol (or 4% formalin for earthworms) and taken to
the lab for identification. Given the low occurrence below 10 cm,
we report only the sum of macrofauna encountered in all soil-
litter layers. Additionally, pitfall traps were used to collect and
determine the relative abundance of macroinvertebrates mov-
ing on the soil surface. These traps consisted of buried plastic
cups (dia. 10 cm) with the upper rim of the cup level with the
soil surface. Three traps were placed around each TSBF sam-
pling point and partially filled with a mixture of water, detergent
and table salt (Souza et al., 2012). After one week, specimens
were collected from each cup and taken to the lab for iden-
tification. Macrofauna from both collection methods (TSBF and
pitfall traps) were counted and identified at the order, genus
and species level (when possible). Diversity was assessed using
 L. Rousseau et al. / Ecological Indicators 27 (2013) 71–82
both specific richness (S – the number of species and/or taxo-
nomic groups distinguished) and the Shannon index (H; Shannon,
1948).
2.3. Soil morphology
Adjacent to each macrofauna pit, a soil monolith
(10 cm × 10 cm × 10 cm) was removed using a square metal
frame, while ensuring to keep the soil structure intact during
transfer to the lab for morphological separation (Velasquez et al.,
2007b). This monolith was used for estimation of bulk density
(BD) and the contents were separated visually into 6 categories
(according to Velasquez et al., 2007b): (1) physicogenic macroag-
gregates – formed by physico-chemical or bacterial processes and
comprised of rather brittle and geometric shapes, (2) biogenic
macroaggregates – formed by the soil invertebrates, dense and
more rounded shapes with clear evidence of biological activity,
(3) root-associated macroaggregates – those adhering to the roots
after gentle shaking, (4) organic debris – course decaying remains
of plants and other organisms, (5) aggregates and non-aggregated
soil smaller than 4 mm, and (6) stones with range between 0.5
and 10 cm. The fractions were air-dried and weighed to deter-
mine the proportion of whole soil in each and stone weight per
monolith.
2.4. Soil chemical and physical properties
At each point, soil samples (0–15 cm) were air-dried for analy-
sis of pH, organic matter, and plant available nutrients. Soil organic
matter (SOM) content was determined with the Walkley–Black
method, pH by potentiometric method in water, total nitrogen
concentration (TN) by the Kjeladhl method, available phosphorus
(Pavail ) by Olsen method, calcium (Ca), potassium (K) and magne-
sium (Mg) contents (mg 100 g−1 of dry soil) by atomic absorption
spectrometry (Perkin Elmer, Model 3100). These samples were
also used to determine soil texture according to the Bouyoucos
method and relative soil humidity (RH) (Houba et al., 1989; USDA,
2004).
Penetration resistance (PR) and shear strength (SS) were mea-
sured at each point with a cone penetrometer and a hand
torcometer in May 2011 (once the first rains had thoroughly wet-
ted the soil). At each point soil compaction (with bulk density) was
evaluated averaging three subsamples (Velasquez et al., 2007a).
2.5. Indicators of soil quality
To provide an integrated assessment of the effects of the differ-
ent management systems on soil health and functioning, data were
summarized in one general indicator of soil quality (GISQ), by using
methods adapted from Velasquez et al. (2007a). In brief, the indi-
cator was calculated by first conducting a principal components
analysis (PCA) individually for the four data sets of soil variables
(macrofauna, aggregate morphology, chemical fertility and soil
physical properties) to identify the soil parameters that best differ-
entiate treatments and explain the overall variability within each
data set. Variables with significant contribution (>50% of the max-
imum value) to either of the first two principal component axes
were selected. For each selected variables, its contribution to axes
1 and 2 were multiplied by the overall variability explained by
each principal component axis in order to generate a weight fac-
tor for each variable. Values for each variable were then multiplied
by their corresponding weight factor and summed to generate a
raw sub-indicator value. This value was then scaled to a num-
ber ranging from 0.1 to 1.0 by a homothetic transformation, for
comparability across sub-indicators. This procedure was conducted
for each of the four sets of soil variables, thus resulting in: (1)
73
a biological sub-indicator, (2) a morphological sub-indicator, (3)
a chemical sub-indicator, and (4) a physical sub-indicator. These
four sub-indicators were then combined to generate the over-
all GISQ by submitting them to the same process as described
above, whereby the sub-indicator values were examined with PCA,
weighted according to their contribution to the first 2 PCA axes,
and then combined by summing these contributions. Soil macro-
fauna collected in pitfall traps were not included in this calculation
so as to maintain consistency with prior application of the GISQ
(Velasquez et al., 2007a) and to avoid redundancy in the biologi-
cal aspects of soil health. For subsequent analyses with the IndVal
method (see below) each sampling point was ranked among the
four sub-indicators and the GISQ such that values between 0.1
and 0.4 were considered to represent low quality, 0.4–0.7 medium
quality, and 0.7–1.0 high soil quality for each indicator consid-
ered.
2.6. Indicator species via the IndVal method
In order to find representative species or taxonomic groups of
the different soil conditions, we applied the Indicator Value Index
method (IndVal; Dufrêne and Legendre, 1997) which quantifies the
extent to which each species meets the criteria of specificity (pres-
ence of a species in the samples of a particular category) and fidelity
(frequency of this species in these samples). We considered each
species as a bioindicator of low, medium or high quality within the
four sub-indicators and the overall GISQ described above. A species
or taxonomic group is a bioindicator if it is typical of a group of sam-
ples (and therefore absent from the other groups of samples) and
also present in all samples of this group. IndVal is calculated as
follows:
N.ind (ij)
Specificity = Aij =
N.ind (i)
N.samples (ij)
Fidelity = Bij =
N.samples (j)
IndValij = Aij × Bij
where Aij represents specificity, N.ind (ij) is the mean number of
individuals of species (i) across sample group (j) and N.ind (i) is
the sum of the mean numbers of individuals of species (i) over all
sample groups in the data set. Fidelity is represented by Bij , where
N.samples (ij) is the number of samples in group (j) where species
(i) is present and N.samples (j) is the total number of samples in
that group. Aij is at a maximum when a species is present in only
one group of samples and Bij is at a maximum when this species is
present in all samples of this group. IndVal Index is the product of
these two terms and its value is between 0 and 1. Finally, a permu-
tation test is performed (random-test of Monte Carlo; McGeoch and
Chown, 1998) to test if a species is significantly associated with a
group of samples (P < 0.05). Each selected indicator species (or tax-
onomic group) is then presented as an indicator of quality (low,
medium or high) relevant to each soil sub-indicator and/or the
GISQ. Both the macrofauna collected from the TSBF method and
pitfall traps were used in the calculation of indicator species.
In May 2011, a workshop was held with local farmers to present
the results of this research and evaluate the applicability of the
indicator species determined by the IndVal method. Fresh samples
were excavated in the field together with farmers, while preserved
specimens were used to support field identification or for indica-
tor taxa not encountered in the field on the day of the workshop.
For each taxa identified by the IndVal method, farmers were asked
if they recognized the species, what perceptions they held about
it and in which management systems and conditions they were
74 L. Rousseau et al. / Ecological Indicators 27 (2013) 71–82

Table 1
Mean abundance and diversity of soil macrofauna according to the TSBF method in four management systems in farmers’ fields near Somotillo, Nicaragua, sampled in February
of 2011. Standard errors are included below each value in italics and the P-value to the right of each row. Values with different letters indicate statistically significant differences
between treatments according to Tukey’s test.

Macrofauna group or variable SFa (ind. m−2 ) SP (ind. m−2 ) QSMAS (ind. m−2 ) TS (ind. m−2 ) P-valueb

254.2 240.0 296.0 104.9 ns

Hymenoptera
120.6 151.6 116.5 57.5
20.4a 3.6b 11.6ab 3.6b 0.016
Arachnida
3.8 1.1 5 1.1
6.2 0.9 6.2 3.6 ns
Diplopoda
8.5 2.2 4.0 4.4
8.0 0 4.4 2.7 ns
Chilopoda
3.3 0 2.5 1.2
43.6 20.4 25.8 21.3 ns
Coleoptera
6.5 3.8 11 6.2
4.4 0.9 4.4 1.8 ns
Lepidoptera
2.1 0.9 1.6 1.1
10.7 5.3 2.7 5.3 ns
Hemiptera
5.2 2.8 1.8 1.9
0 2.7 0.9 0 ns
Diptera
0 1.8 0.9 0
2.7 0.9 0 0 ns
Orthoptera
2.7 0.9 0 0
133.3 17.8 304.0 33.8 ns
Isoptera
81.1 5.8 144.3 26.8
488.0ab 293.3ab 656.9a 176.9b 0.012
Total abundance
113.5 153 153.5 83.6
8.0a 4.1b 5.5ab 3.4b 0.003
Specific richness (S)
2.0 0.7 2.7 0.6
1.5a 1.0ab 1.0ab 0.9b 0.026
Shannon index (H)
0.2 0.1 0.1 0.1
a
SF, secondary forest; SP, silvopastoral system; QSMAS, Quesungual slash-and-mulch agroforestry system; TS, traditional cropping system.
b
ns = not significant (P > 0.05).

encountered. The information gathered from this workshop was 3. Results

also supplemented by semi-structured interviews, similar to those
outlined by Pauli et al. (2012). 3.1. Management system impacts on macrofauna

Sixty one species and taxonomic groups were identified from

2.7. Comparison of management systems and covariation
between data sets
Soil biological, morphological, chemical and physical properties
and associated sub-indicators were compared between manage-
ment systems using the average value of the three transect points
in each plot, for a total of 24 independent samples. One-way ANOVA
and a multiple comparison test (Tukey’s Honestly Significant Dif-
ference) were used to examine differences between the four land
use systems. Natural log transformations were applied to meet the
assumptions of ANOVA (normality, homoscedasticity) when neces-
sary. When these assumptions could not be met, a non-parametric
Kruskal–Wallis test was used to compare land-use systems in the
case of non-normal distributions, while a Welch’s ANOVA was used
to compare non-equal variances.
Principal component analyses were also performed to explore
relationships between variables within each data set (macrofauna,
morphology, chemical and physical properties). Additionally,
between-class PCA was used to examine multivariate differences
between management systems via permutation tests, comparing
the observed test statistic with a distribution obtained by a random
permutation of the data (Random Monte-Carlo test; Zerbino, 2010).
Co-inertia analyses were then conducted using the above PCA data
to examine covariation and similarities in data structure among
the different data sets with the matrix coefficient of covariation
(Rv; Dray et al., 2003).
All statistical analyses were carried out using the software R (R
Development Core Team, 2010). The IndVal method was conducted
using specific packages (labdsv, Akima, MASS, vegan and mgcv),
while PCA and co-inertia analyses were conducted using the ade4
package (Dray et al., 2003; Thioulouse et al., 1997).
the excavation of soil monoliths using the TSBF method, includ-
ing 11 species of ants, two termite species and 16 species of the
order Coleoptera. Overall, the samples were dominated by ants and
termites, comprising over 85% of the macrofauna collected. Only
five earthworms were found during sampling (in QSMAS and TS)
and not considered in the statistical analysis. Between manage-
ment systems the most pronounced differences were observed for
the order Arachnida, SF containing nearly six times higher abun-
dance than TS or SP (P = 0.016; Table 1), with QSMAS in between.
Total abundance of macrofauna was highest under QSMAS, with
657 ind. m−2 and significantly higher than TS or SP (P = 0.012). Spe-
cific richness (S) was significantly higher in SF than in TS or SP
(P = 0.003), and similarly the Shannon index of diversity (H) was
significantly higher in SF than in TS (P = 0.026), with QSMAS in
between.
Pitfall traps captured 83 species and taxonomic groups includ-
ing 12 species of ants (Hymenoptera), two species of termites
(Isoptera) and 14 species of Coleoptera. Ants alone comprised over
85% of the macrofauna collected in the pitfall traps and were
found to be highest under SP, with significantly more Hymenoptera
(P = 0.011), as well as total macrofauna (P = 0.029) in SP than in
SF (Table 2). Blattaria (cockroaches) were also found to be sig-
nificantly higher under SF than in SP or TS (P = 0.019), while
Chilopoda (centipedes) was only observed in pitfall traps in SF.
There were no significant management effects on species richness
(S) for macrofauna collected in pitfall traps, but the Shannon Index
was significantly higher under SF than for SP (P = 0.017). Total rel-
ative abundance of macrofauna collected in these samples was
highest under SP (153.6 ind. per trap), followed by QSMAS, and
was significantly higher than observed for SF (71 ind. per trap;
P = 0.029).
 L. Rousseau et al. / Ecological Indicators 27 (2013) 71–82 75

Table 2
Mean abundance and diversity of soil macrofauna abundance according to the pitfall traps method in four management systems in farmers’ fields near Somotillo, Nicaragua,
sampled during one week in February of 2011. Standard errors are included below each value in italics and the P-value to the right of each row. Values with different letters
indicate statistically significant differences between treatments according to Tukey’s test.

Macrofauna group or variable SFa (ind. per trap) SP (ind. per trap) QSMAS (ind. per trap) TS (ind. per trap) P-valueb

50.5a 138.1b 93.9ab 62.8ab 0.011

Hymenoptera
11.4 20.8 27.8 10.8
4.3 3.2 6.5 2.6 ns
Arachnida
0.6 0.8 1.4 0.4
0.1 0 0 0 ns
Chilopoda
0.1 0 0 0
2.1 0.5 0.4 0.4 ns
Coleoptera
0.8 0.2 0.2 0.2
0.4 0.2 0.1 0.2 ns
Lepidoptera
0.2 0.1 0.1 0.2
4.1 5.2 1.8 1.7 ns
Hemiptera
2.3 2.5 0.7 0.8
0.3 0.9 0.1 0.7 ns
Diptera
0.2 0.8 0.1 0.4
5.8 2.0 1.8 2.3 ns
Orthoptera
2.3 0.9 0.4 0.9
0.5 0.3 0.3 0.4 ns
Trichoptera
0.2 0.2 0.1 0.3
2.6a 0.3b 1.7ab 0.9b 0.019
Blattaria
0.8 0.1 0.5 0.8
0.3 2.9 1.8 0.1 ns
Isoptera
0.1 1.8 1.0 0.1
71a 153.6b 108.3ab 72.2ab 0.029
Total abundance
14.5 20.2 28.8 12.2
15.2 13.1 13.9 11.3 ns
Specific richness (S)
1.1 0.6 1.4 1.4
2.1a 1.6b 1.8ab 1.7ab 0.017
Shannon index (H)
0.1 0.1 0.1 0.1
a
SF, secondary forest; SP, silvopastoral system; QSMAS, Quesungual slash-and-mulch agroforestry system; TS, traditional cropping system.
b
ns = not significant (P > 0.05).

3.2. Impacts on soil physical, chemical and morphological
variables
Of the soil physical variables measured (Table 3), penetration
resistance (PR) and shear strength (SS) demonstrated the greatest
impacts of management, such that shear strength was significantly
higher under SP than SF or QSMAS (P = 0.001) and penetration resis-
tance (PR) significantly higher under SP than under SF or QSMAS
(P = 0.04). No other soil physical variables demonstrated a signifi-
cant (P > 0.05) management effect. Soil morphology was impacted
to the extent that the proportion of physicogenic macroaggregates
was significantly higher under SP and TS than under SF and QSMAS
(P = 0.001; Table 3). While no significant impacts of management
were observed for the soil chemical variables measured, SF tended
to show higher contents of SOM and Ca (Table 3).
3.3. Synthetic indicators of soil quality
Comparison of land management systems according to the GISQ
and the four sub-indicators revealed relatively small, but important
differences between systems. For example, the biological sub-
indicator was significantly higher under SF than TS (P = 0.042), with
QSMAS and SP having intermediate values. While not significantly
different from the other systems, SF suggested a trend of higher soil
quality for the chemical, physical and morphological sub-indicators
(Table 4). These trends are reflected in the overall GISQ, where SF
was found to have soils of significantly higher overall quality than
either SP or TS (P = 0.002), with QSMAS intermediate in value.
3.4. Multivariate system differences and co-inertia between data
sets
Permutation tests demonstrated significant multivariate sepa-
ration between management systems for all five of the soil data
sets (Figs. 1 and 2; results not shown for all data sets). Manage-
ment systems were clearly differentiated by the between-class
PCA of macrofauna data sets associated with both TSBF and pit-
fall traps (PT) methods (P < 0.001). For macrofauna assessed by the
TSBF method (Fig. 1), systems were best separated along the first
axis which explains variability associated with species richness and
abundance of Arachnida. The second axis was largely associated
with total macrofauna abundance, which was largely driven by the
abundance of ants (Hymenoptera) and termites (Isoptera; Fig. 1).
Very similar trends were found for macrofauna collected in pitfall
traps (data not shown).
System differentiation by soil physical and morphological vari-
ables using between-class PCA was also significant (P < 0.001). For
physical soil variables, axis 1 was largely associated with tex-
ture, while axis 2 was related to soil compaction, with penetration
resistance exerting the largest influence (Fig. 2). Although the soil
chemical data was also able to significantly differentiate the man-
agement systems (P = 0.04), differences were small and explanation
for these patterns was less clear (data not shown). Management
system differences highlighted by morphological variables appear
to be driven largely by the second PCA axis that is associated
with physicogenic aggregates and organic debris (data not shown).
In accordance with the above PCA results, key parameters were
identified within each data set and used to generate the four sub-
indicators as well as the overall GISQ (Table 5). For example, the
physical sub-indicator was largely determined by soil textural com-
ponents, penetration resistance and the stone content of the soil,
while the biological sub-indicator was formulated based on total
abundance, elements of taxonomic diversity, and the abundance of
Coleoptera.
Coinertia analyses revealed significant covariation between all
data sets except between the soil macrofauna from TSBF method
and soil morphological data tables (Fig. 3). For example, signifi-
cant covariation between macrofauna and soil physical variables
76 L. Rousseau et al. / Ecological Indicators 27 (2013) 71–82

Table 3
Mean of soil physical and chemical properties and morphological variables under four management systems in farmers’ fields near Somotillo, Nicaragua, sampled in February
and May of 2011. Standard errors are included below each value in italics and the P-value to the right of each row. Values with different letters indicate statistically significant
differences between treatments according to Tukey’s test.

Variableb SFa SP QSMAS TS P-valuec

1.1 1.2 1.1 1.1 ns

BD (g cm−3 )
0.1 0 0 0.07
RH (% of dry 8.2 6.4 6.4 4.7 ns
weight) 1.2 1.1 0.7 0.6
69.7a 93.3b 71.9a 87.4ab 0.040
PR (kPa)
9.9 7.1 4.9 5.9
45.1a 85.6b 51.3a 56.0a 0.001
SS (kPa)
5.2 8.9 6.4 5.8
31 29 29 32 ns
Clay (%)
3 2 1 3
33 33 34 34 ns
Silt (%)
3 1 2 3
36 38 37 34 ns
Sand (%)
6 2 2 3
181.6 185.2 198.5 190.4 ns
Stone (g/soil monolith)
49.9 68.5 56.9 34.6
6.1 5.9 6.1 6.0 ns
pH
0.1 0.1 0.2 0.1
4.5 3.3 3.1 3.6 ns
SOM (% of dry soil)
0.7 0.3 0.3 0.7
0.2 0.2 0.2 0.2 ns
TN (% of dry soil)
0 0 0 0
2.5 2.7 2.5 5.5 ns
Pavail (ppm)
0.7 0.6 0.4 2.8
0.3 0.3 0.3 0.3 ns
K (mg/100 g)
0.1 0 0.1 0.1
11.5 8.5 9.9 9.3 ns
Ca (mg/100 g)
1.4 1.1 2.2 0.9
2.3 1.7 2 1.9 ns
Mg (mg/100 g)
0.6 0.3 0.5 0.3
41 39 43 42 ns
BIO (%)
5 4 5 6
2a 12b 2a 9b 0.001
PHYS (%)
1 2 1 2
5 5 3 3 ns
ROOT (%)
1 1 1 1
50 44 52 45 ns
NA (%)
6 4 5 5
1 1 1 1 ns
OD (%)
0 0 0 0
a
SF, secondary forest; SP, silvopastoral system; QSMAS, Quesungual slash-and-mulch agroforestry system; TS, traditional cropping system.
b
BD, bulk density; RH, relative humidity; PR, penetration resistance; SS, shear strength; SOM, soil organic matter; TN, total nitrogen; Pavail , phosphorus available; BIO,
biogenic macroaggregates; PHYS, physical macroaggregates; ROOT, root-associated macroaggregates; NA, non-macroaggregated soil; OD, fragments of organic debris.
c
ns = not significant (P > 0.05).

suggests that total macrofauna abundance and diversity (richness Table 4

and Shannon index) are negatively associated with soil compaction,
particularly penetration resistance (Figs. 1 and 2).
3.5. Determination of indicator species and farmer validation
Mean values for sub-indicators and overall general indicator of soil quality with
four management systems in farmers’ fields near Somotillo, Nicaragua, sampled
in February and May of 2011. Standard errors are included below each value in
italics and the P-value to the right of each row. Values with different letters indicate
statistically significant differences between treatments according to Tukey’s test.

Variable SFb SP QSMAS TS P-valuec

Applying the IndVal method to the soil macrofauna data col-
0.37a 0.24ab 0.31ab 0.23b 0.042
lected via the TSBF sampling, twelve species (or taxonomic groups) BSIa
0.04 0.04 0.05 0.06
were identified as bioindicators of soil quality (Table 6). For exam- 0.58a 0.54a 0.52a 0.56a ns
CSI
ple, six taxa were found to indicate high biological quality of soils, 0.09 0.04 0.06 0.06
0.61a 0.53a 0.56a 0.54a ns
including three species of Coleoptera, and one each of Arachnida, MSI
0.05 0.05 0.03 0.05
Hymenoptera and Isoptera. Other species were found to indicate 0.73a 0.63a 0.71a 0.71a ns
high quality in terms of the chemical and morphological soil qual- PSI
0.10 0.05 0.06 0.04
ity sub-indicators. Two macrofauna taxa recovered by the TSBF GISQ
0.66a 0.52b 0.58ab 0.56b 0.002
method were found to indicate low soil quality, Coproporus sp. (low 0.06 0.02 0.03 0.05

CSI) and Tribolium castaneum (bioindicator of low GISQ). a

BSI, biological subindicator (based on soil macrofauna from TSBF method); CSI,
Macrofauna collected in pitfall traps yielded 26 indicator taxa chemical subindicator; PSI, physical subindicator; MSI, morphological subindicator;
GISQ, general indicator of soil quality.
(Table 7). Nine taxa were found to indicate high biological quality, b
SF, secondary forest; SP, silvopastoral system; TS, traditional system; QSMAS,
including five taxa of Hymenoptera, two Coleoptera, one Arachnida, Quesungual slash-and-mulch agroforestry system.
and one Hemiptera. At the same time, six taxa were found to be c
ns = not significant (P > 0.05).
bioindicators of low chemical quality, including two species of
Hymenoptera, two Arachnida and three Hemiptera. Three taxa were
found to be bioindicators of the GISQ, with Pardosa sp. (Arachnida)
 L. Rousseau et al. / Ecological Indicators 27 (2013) 71–82 77

Table 5
Variables used to construct the sub-indicators and the overall GISQ and their associated weight factor in the calculation.

Indicatora BSI CSI PSI MSI GISQ

Coleoptera 4.65 pH 8.73 PR −9.92 BIO 17.36 PSI 18.39

S 7.72 SOM 13.06 Clay 8.46 PHYS −7.85 CSI 17.30
H −5.30 NT 13.02 Silt 7.34 ROOT 7.69 BSI 14.07
Variables
Total Abun. 6.60 K 4.94 Sand −12.25 NA −19.44 MSI 12.15
Ca −12.21 Stone −6.97 OD 12.45
Mg −11.73
a
BSI, biological subindicator (based on soil macrofauna from TSBF method); CSI, chemical subindicator; PSI, physical subindicator; MSI, morphological subindicator; GISQ,
general indicator of soil quality; S, specific richness; H, Shannon index; SOM, soil organic matter; TN, total nitrogen; PR, penetration resistance; BIO, biogenic macroaggregates;
PHYS, physical macroaggregates; ROOT, root-associated macroaggregates; NA, non-macroaggregate soil; OD, organic debris.

and Gryllus sp. (Orthoptera) indicating high soil quality and the leaf-
cutter ant, Atta cephalotes, indicating low GISQ.
During the sampling campaign, farmers’ perspectives were dis-
cussed regarding soil quality, the Quesungual system, and the role
of invertebrates for indicating quality of their soils (Barrera-Bassols
and Zinck, 2003; Tselouiko, 2010). This process began during the
field separation of macrofauna in February 2011 (often with farmer
assistance) and at a preliminary meeting to present our study
objectives. We returned in May 2011 to present the results and dis-
cuss the indicator species identified with farmers, so as to develop
participatory bioindicators of soil quality (Doran and Zeiss, 2000;
Tselouiko, 2010). Larger taxa (>5 mm) appeared to be more readily
identified by farmers than smaller ones. We discussed with farmers
their familiarity with each taxa and what the presence and/or abun-
dance of these species indicate to them with regards to soil quality
or fertility on their farms. In total, three species from the TSBF
method and four from the pitfall traps method were selected based
on farmer recognition and classification. These taxa are Cylindroiu-
lus sp. (Diplopoda Judidae), Nasutitermes sp. (Isoptera Termitidae) and
Atta sp. (Hymenoptera Formicidae) for the TSBF method (Table 6)
and Polistes sp. (Hymenoptera Vespidae), Phrurolithus sp. (Arachnida
Corinnidae), A. cephalotes and larva of Elateridae (Coleoptera) for
macrofauna collected within pitfall traps (Table 7). For example,
both our findings and farmers agree that the ant A. cephalotes is a
sign of low soil quality, while Cylindroiulus sp. (Diplopoda Judidae)
indicates a high soil chemical fertility.
4. Discussion
4.1. Management system impacts
Of the management effects observed in this study, the con-
version of forest to agriculture demonstrated the greatest impact
on soil quality parameters. This was perhaps most evident for
soil macrofauna communities. Although SF did not present the
greatest abundance, macrofauna collected from both the TSBF and
pitfall trap methods demonstrated the highest diversity (S and H;
Tables 1 and 2), and this diversity likely contributes to improving
overall biological functioning in these soils (Brussaard et al., 2007).
For example, spiders collected via the TSBF method were most
abundant under SF (Table 1), and as top predators likely contribute
to pest control services and indicate an enhanced food-web struc-
ture (Ferris et al., 2001; Marc et al., 1999; Rousseau et al., 2012).
We also note that SF demonstrated the highest value for the bio-
logical sub-indicator (Table 4), suggesting benefits of forest cover
to macrofauna communities as a whole. Along with impacts on soil

Table 6
Indicator species (or taxa) of soil macrofauna determined using the IndVal method (P < 0.05), for specimens collected near the community of La Danta, in northern Nicaragua
in February 2011, using the TSBF sampling technique. Each species is classified as an indicator of high, medium, or low soil quality according to five indices of soil quality.
Order of each species and the IndVal value are located below each species/taxa name.

Quality group BSIa CSI PSI MSI GISQ

Hypoponera sp. Cylindroiulus sp. Atta sp.

(Hymenoptera) (Diplopoda)b (Hymenoptera)b
0.636 0.175 0.219
High
Costabrimma sp. Pselaphochernes sp.
(Arachnida) (Arachnida)
0.500 0.195
Anthicus sp. – –
(Coleoptera)
0.434
Coproporus sp. –
(Coleoptera)
0.496
Blapstinus sp. –
(Coleoptera)
0.496
Nasutitermes sp.
(Isoptera)b
0.816

Medium Larva Elateridae sp. – – – –

(Coleoptera)
0.541

Low – Coproporus sp. – – Tribolium

(Coleoptera) castaneum
0.182 (Coleoptera)
0.399
a
BSI, biological subindicator (based on soil macrofauna from TSBF method); CSI, chemical subindicator; PSI, physical subindicator; MSI, morphological subindicator; GISQ,
general indicator of soil quality.
b
Farmer-validated indicator species/taxa.
78 L. Rousseau et al. / Ecological Indicators 27 (2013) 71–82

Table 7
Indicator species (or taxa) of soil macrofauna determined using the IndVal method (P < 0.05), for specimens collected near the community of La Danta, in northern Nicaragua
in February 2011, using the pitfall traps sampling technique. Each species is classified as an indicator of high or low soil quality according to five indices of soil quality (no
indicators of medium soil quality were identified for this dataset). Order of each species and the IndVal value are located below each species/taxa name.

Quality group BSIa CSI PSI MSI GISQ

Crematogaster sp. Pardosa sp. Gryllus sp. Pardosa sp.

(Hymenoptera) (Arachnida) (Orthoptera) (Arachnida)
0.753 0.425 0.352 0.522
Stenopolybia sp. Gryllus sp. Gryllus sp.
High (Hymenoptera) (Orthoptera) (Orthoptera)
0.775 0.440 0.512
Polistes sp.
(Hymenoptera)b
0.670
Augochlora sp.
(Hymenoptera)
0.823
Anoplius sp. – –
(Hymenoptera)
0.844
Phrurolithus sp. – –
(Arachnida)
0.880
Larva Elateridae
(Coleoptera)b
IV = 0.500
Blapstinus sp.
(Coleoptera)
IV = 0.815
Heterogaster sp.
IV = 0.551

– Crematogaster sp. Atta cephalotes Larva Tenebrionidae Atta cephalotes

(Hymenoptera) (Hymenoptera)b (Coleoptera) (Hymenoptera)b
0.255 0.719 0.181 IV = 0.801
Low Augochlora sp. Eleodes sp.
(Hymenoptera) (Coleoptera).
0.367 IV = 0.432
Phrurolithus sp. Larva Diptera
(Arachnida)b (Diptera)
0.206 0.194
Didymocentrus sp.
(Scorpionida)
0.312
Augocoris gonesii – –
(Heteroptera)
IV = 0.243
Madura sp. –
(Heteroptera)
0.269
Chariesterus sp.
(Heteroptera)
0.269
a
BSI, biological subindicator (based on soil macrofauna from TSBF method); CSI, chemical subindicator; PSI, physical subindicator; MSI, morphological subindicator; GISQ,
general indicator of soil quality.
b
Farmer-validated indicator species/taxa.

biological parameters, SF had the lowest levels of soil compaction
and suggested marginally higher (P < 0.1) levels of humidity, SOM
and key nutrients such as Ca and Mg (Table 3). The overall benefits
of forest cover are reflected in the GISQ, where SF had significantly
higher values than both SP and TS (Table 4). These findings are con-
sistent with past research suggesting a negative impact of forest
conversion on soil compaction and SOM dynamics within tropi-
cal hillside agroecosystems (Fonte et al., 2010a; McDonald et al.,
2002; Rivera Peña, 2008). These studies indicate that degradation
is largely driven by a decrease in organic inputs and a loss of top
soil due to erosion.
While the three production systems generally exhibited lower
soil quality than SF, important differences exist between these
systems. In particular, QSMAS appeared to support improved soil
functioning in several aspects. For example, QSMAS demonstrated
the highest overall abundance of soil macrofauna collected using
the TSBF method (Table 1). While not significantly different from
the other systems (P > 0.05), we note that the abundance of key
taxonomic groups (i.e., top predators Arachnida and Chilopoda) as
well as overall species richness were consistently higher for QMSAS
than for SP and TS (Netuzhilin et al., 1999). These results cor-
roborate past findings suggesting a higher presence of predators
(Arachnida and Chilopoda) and overall macrofauna abundance in
QMSAS as compared to other management systems at a similar
site in Honduras (Pauli et al., 2011). Improved soil quality under
QSMAS is also apparent for measures of soil compaction (penetra-
tion resistance and shear strength), where QSMAS was significantly
less compacted than SP and generally intermediate between SF
and TS (Table 3). We note that the higher compaction under SP
is most likely associated with the greater presence of livestock,
which can be particularly detrimental to the hillside soils in the
region (Sepúlveda and Nieuwenhuyse, 2011). In agreement with
the benefits for soil physical properties, QSMAS had a significantly
lower proportion of physicogenic aggregates and tended towards
more biogenic aggregates than in other systems, which is reflected
by the higher populations of earthworms that have been observed
 L. Rousseau et al. / Ecological Indicators 27 (2013) 71–82
Fig. 1. (a) PCA biplot of TSBF macrofauna orders, total abundance, and diversity
variables (S, specific richness; H, Shannon index). (b) Plot based on PCA analysis rep-
resenting separation of points (P = 0.001 by permutation test) according to the land
use systems (SF, secondary forest; SP, silvopastoral system; QSMAS, Quesungual
slash-and-mulch agroforestry system; TS, traditional cropping system).
under QSMAS at other sites during the wet season (Fonte et al.,
2010a; Pauli et al., 2011). Finally, benefits of QSMAS are apparent
from the overall GISQ, with a value between those of SF and the
two other management systems.
A number of factors may be responsible for improved soil condi-
tions under SF and QMSAS. Past research has shown that both dense
tree cover and a developed mulch layer, common features of SF and
QSMAS, can benefit soil macrofauna populations (Martius et al.,
2001; Oritz-Ceballos and Fragoso, 2004; Sileshi and Mafongoya,
2007). Trees and the associated litter layer, likely provide increased
habitat complexity, which supports overall taxonomic diversity
(and higher biological quality), while reduced disturbance in the
forest allows for better representation of taxa within higher trophic
levels that often exhibit slower growth and reproduction rates
(Ferris et al., 2001; Landis et al., 2000). We note that reduced soil
compaction may be associated with microbially-mediated aggre-
gation that often results from higher organic residue inputs (Kong
et al., 2005), as well as generally lower livestock densities in these
systems. Additionally, organic inputs provide a food source for soil
macrofauna, suggesting that decompaction of soil under SF and
QSMAS may be associated with the activities of soil ecosystem engi-
neers, particularly earthworms (Ampoorter et al., 2011; Fonte et al.,
2010b; Velasquez et al., 2012). This idea is further supported by the
significant covariation observed between the macrofauna and soil
physical variables. The overall better soil quality observed under
forest, compared to the TS or SP, appears to be driven by the higher
biological quality, but also by more subtle trends observed in the
other soil data sets. While not significantly different from the other
management systems, the morphological, chemical and physical
sub-indicators were all consistently higher under SF than the other
79
Fig. 2. (a) PCA biplot of the soil physical variables (BD, bulk density; RH, relative
humidity; PR, penetration resistance; SS, shear strength). (b) Plot based on PCA
analysis representing separation of points (P = 0.001 by permutation test) accord-
ing to the land use systems (SF, secondary forest; SP, silvopastoral system; QSMAS,
Quesungual slash-and-mulch agroforestry system; TS, traditional cropping system).
management systems (Table 4) and the cumulative effect of this
trend led to a significantly higher GISQ under SF.
Whereas the overall differences between QSMAS and the other
management systems are subtle, they are important nonetheless.
We suggest that differences might have been greater if this study
had been conducted during the rainy season, when earthworms
are more active and differences in soil structure are likely to be
more pronounced (Fonte et al., 2010a). Additionally, technological
‘drift’ may be an important factor. Farmers in the community of La
Danta began to adopt Quesungual practices in 2006 and abandoned
burning altogether over the next few years. Based on the obvious
success of QSMAS, farmers began incorporating QSMAS principles
into other forms of land management, like more actively promoting
trees within SP and TS (personal observation). Such ‘drift’ likely
resulted in a homogenization of management practices and may
have led to less striking differences between land use systems than
might have been observed only five years earlier when burning
and extensive tree removal were prevalent in traditional crop and
livestock systems.
4.2. Developing general indicators of soil quality
In designing indicators of soil quality several key criteria need to
be met. Useful indicators should be sensitive to management alter-
ations, well-correlated with relevant ecosystem functions, easy to
understand, and inexpensive to measure (Doran and Zeiss, 2000).
The strategy for developing the sub-indicators and overall GISQ
employed in this study provides a relatively flexible and unbiased
means to identify relevant indicators of soil quality, while tak-
ing the above factors into consideration (Velasquez et al., 2007a).
80 L. Rousseau et al. / Ecological Indicators 27 (2013) 71–82
Fig. 3. Schematic summary of the co-inertia analyses between 4 data tables, with the Rv (matrix coefficient of covariation) and levels of significance (P-value) for each pair
of data sets.
The approach first seeks to summarize the overall variability for
each data table by identifying a subset of variables within each
table that best explain patterns in the data. This information is
then combined with practical knowledge of laboratory tests and
ecosystem functioning to determine indicators that are sensitive
and easy to measure by local land managers and technicians. For
example, sand content and soil penetration resistance offer rela-
tively easy to measure and influential determinants of the physical
sub-indicator. Thus, future assessments which focus solely on these
two parameters would likely be adequate for evaluating impacts
of management and/or environmental conditions on soil physi-
cal quality in the study region. Similarly, SOM (reflected by total
C and N) appears to be the most important variable in calculat-
ing the chemical sub-indicator, while Ca also plays an important
role (Table 5). Measurement of these specific variables must be
done in a laboratory or with technical field equipment and thus
cannot be carried out directly by farmers. This knowledge is, how-
ever, still valuable since it can greatly reduce the resources required
to assess soil chemical fertility. The morphological sub-indicator
is driven largely by the biogenic and non-macroaggregated mor-
phological fractions, while the biological sub-indicator reflects
taxonomic richness and total abundance of macrofauna to a large
extent (Table 5). These variables do not necessarily require labo-
ratory facilities, but still demand a fair level of technical capacity.
Overall, we note that the GISQ was more strongly influenced by
soil physical and chemical parameters and less by macrofauna and
morphology (Table 5).
While the biological sub-indicator may have contributed rela-
tively less to the calculation of the GISQ, we note that this was the
only sub-indicator to demonstrate significant differences between
land use types (Table 4), and that the management impacts were
generally more pronounced for macrofauna than for other soil
parameters. Thus, soil invertebrates appear to offer an early and
sensitive indicator of management impacts on soil quality (Barros
et al., 2002) and could provide information about the trajectory
of soil quality changes, while soil chemical and physical parame-
ters better reflect changes that have already occurred. The use of
macrofauna as an early indicator is in agreement with a number
of other studies suggesting their use as means to assess short-term
management impacts on soil function and ecosystem health (Lobry
de Bruyn, 1997; Paoletti, 1999). For example, Mathieu et al. (2005)
found soil invertebrates to quickly respond to forest clearance and
regrowth in the Brazilian Amazon. Similarly, Blanchart et al. (2007)
examined the recovery of soil C stocks and biological communi-
ties following conversion of conventionally tilled systems to no-till
agriculture in Brazil, and found soil macrofauna to increase signif-
icantly in the first year of no-till, while measurable differences in
soil C did not appear until much later (>5 years). Velasquez et al.
(2007a) also observed macrofauna to be highly sensitive to land
use change in a more humid region of Nicaragua, and found signifi-
cant covariation between biological and soil physical, chemical and
morphological attributes. This is not the case here and this is likely
due to the considerable influence of earthworms on the biogenic
aggregate soil fraction, and the near absence of earthworm activity
and presence in the dry season. The high abundance of macrofauna
collected here and assessment of seasonal macrofauna dynamics
from similar conditions in Honduras (Pauli et al., 2011) suggest
that, in contrast to earthworms, a number of soil taxa remain active
throughout the dry season. While many of these organisms may not
be as important as earthworms in terms of their ecosystem engi-
neering activities (Lavelle et al., 1997), they nonetheless respond to
changes in the soil environment and can provide valuable informa-
tion about management impacts at a time when farmer labor and
time constraints are less restrictive to soil quality evaluation.
4.3. Participatory identification of bioindicator species
The efforts to identify indicators of soil quality discussed above
are relevant, particularly when technical assistance is available
locally to facilitate access to standardized soil analyses and help
with interpretation of the results. Apart from this, it is also neces-
sary to identify simple soil bioindicators that farmers can measure
and evaluate independently, as technical support is not always
available at times when information is most needed (Tselouiko,
2010). In our study, we combined a rigorous statistical selection of
indicator taxa (using the IndVal method) together with a participa-
tory process involving farmer knowledge and local experience, in
order to determine relevant bioindicator species of distinct phys-
ical, chemical and biological soil states. While others have used
similar approaches to identify indicator species for differentiating
land use types (McGeoch, 1998; Ruiz et al., 2011) and assessing
ecosystem degradation or restoration (Nahmani et al., 2006; Rossi
 L. Rousseau et al. / Ecological Indicators 27 (2013) 71–82
et al., 2010), our study is unique in linking specific indicator taxa
with synthetic indicators of soil quality. In relating specific taxa to
a range of soil properties that best explain local variability in soil
functions and represent distinct aspects of soil quality, this research
intends to provide farmers and local land managers with simple
and powerful tools for evaluation of land management impacts on
specific components of soil function. For example, stink beetles of
the genus Eleodes, collected from pitfall traps were found to be a
bioindicator of poor soil physical quality (Table 7). Thus, a farmer
who encounters this insect on particular plot of land will know that
there is a high probability that the soil is compacted in this part
of his/her farm and that corrective actions should be taken (e.g.,
reduced grazing, addition of organic residues to attract decompact-
ing fauna such as earthworms). Similarly, a farmer who encounters
spiders within the genus Pardosa may conclude that soil in that area
possesses relatively good chemical fertility (high in SOM and key
macronutrients) and overall soil quality (Table 7), thus indicating
that the need for fertilizer input may be lower than elsewhere on
his/her farm.
The bioindicators presented here offer a robust preliminary set
of taxa for evaluating the impacts of land management on soil qual-
ity; however, we urge several points of caution at this stage. While
the methodology employed is applicable across a broad array of sit-
uations and agricultural landscapes, the bioindicators developed
here are currently useful only at the local scale in this study and
are likely to be most accurate during the dry season. Inter-seasonal
and inter-annual variability as well as differences among sites are
among factors suggested by McGeoch and Chown (1998) that war-
rant further testing of indicators in subsequent years and across
different sites to fully understand their potential value. Addition-
ally, while our indicator taxa were discussed and validated by local
farmers, we note that this activity was rather informal and included
a relatively small number of farmers (<10). Thus, further develop-
ment of these indicators should attempt to encompass a broader
temporal and spatial diversity, and to better integrate the perspec-
tives of a greater number of farmers with more diverse knowledge
on land management issues and local bioindicators of soil quality.
5. Conclusions
The findings presented here help to elucidate our understand-
ing of how agricultural expansion and common land management
practices contribute to the degradation of soil resources in the trop-
ical dry forest region of Central America. We found conversion
of forest to traditional agricultural systems to reduce biodiversity
and increase compaction of hillside soils of the region. Inclusion
of native trees, active pruning and mulch management, and abol-
ishment of burning associated with the Quesungual agroforestry
system appear to mitigate some of the deleterious impacts of
agriculture, as this system was shown to improve macrofauna
abundance and diversity as well as reduce compaction relative
to traditional cropping and pasture systems. The calculation of
synthetic indicators of soil quality provided a robust and inte-
grative assessment land management impacts and indentified key
parameters of soil variability for reducing future investment in soil
quality evaluation. Of these parameters, soil macrofauna appeared
to provide a sensitive and early indicator or land use impacts on
soil quality. Drawing upon these synthetic indicators, we indenti-
fied bioindicator species that were validated by farmers to offer a
simple and powerful tool for local land managers to quickly assess
and react to land management impacts in the region. While our
findings remain preliminary and are not immediately applicable to
other regions, we provide a basic methodology that is broadly appli-
cable for developing bioindicators for diverse socio-environmental
contexts.
81
Acknowledgments
We thank all the people that participated in field and labora-
tory operations, especially the farmers and their families in the
community of La Danta. We also greatly appreciate the support of
Aracely Castro, Juan-Carlos Mercado, and other CIAT staff for their
collaboration and assistance with technical and logistical issues.
Additionally, we thank Eva Gutiérrez for assistance with equip-
ment, Mirna Ortiz for help with macrofauna identification, and
Leonardo Garcia Centero for support with soil analyses at UNA-
Managua. This work was part of the project “Eco-efficient crop and
livestock production for the poor farmers in the sub-humid hill-
side areas of Nicaragua” coordinated by the International Center
for Tropical Agriculture (CIAT) in collaboration with University of
Natural Resources and Applied Life Sciences (BOKU – Austria), Insti-
tuto Nicaragüense de Tecnología Agropecuario (INTA – Nicaragua),
Universidad Nacional Agraria (UNA – Nicaragua), Consorcio para el
Manejo Integrado de Suelos (MIS – Nicaragua) and funded in part by
the Federal Ministry of Finance (BMF) of the Republic of Austria and
the Austrian Development Agency (ADA). Additional funding sup-
port was provided by the INDICS project from the French Fondation
pour la Recherche sur la Biodiversité.
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