Potential of slash-and-mulch system with legumes to conserve soil attributes and macrofauna diversity in Eastern Amazon

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Pedobiologia - Journal of Soil Ecology 95 (2022) 150840
Available online 16 September 2022
0031-4056/© 2022 Elsevier GmbH. All rights reserved.
Potential of slash-and-mulch system with legumes to conserve soil 
attributes and macrofauna diversity in Eastern Amazon 
Guillaume Rousseau a,*, Jesús Burgos-Guerrero a, Luis Hernández-García a, 
Ernesto Gómez-Cardozo a, Stefania Triana a, Julio Medina a, Kellen da Silva b, 
Danielle Celentano a 
a Programa de pós-graduação em Agroecologia, Universidade Estadual do Maranhão (UEMA), Av. Lourenço Vieira da Silva 1000, Jardim São Cristovão, 65055-310 São 
Luís, MA, Brazil 
b Soil Biology Laboratory (LABS), UEMA, Av. Lourenço Vieira da Silva 1000, Jardim São Cristovão, 65055-310 São Luís, MA, Brazil 
A R T I C L E I N F O 
Keywords: 
Amazon 
Fire 
Smallholder agriculture 
Secondary forest 
Soil biodiversity 
Co-inertia 
A B S T R A C T 
Slash-and-burn agriculture has been practiced for thousands of years in the tropics and is sustainable in con-
ditions of low population density, and long fallow. However, the population increase leads to intensification, and 
consequently the reduction of fallow, productivity, and sustainability. Then, public and private institutions with 
farmers, are seeking alternatives to replace this farming system. The slash-and-mulch technique for smallholder 
farmers is widespread in Central America and has the potential to be transferred to other regions. Nonetheless, 
little information is available about its potential for the eastern Amazon. The soil macrofauna is associated with 
soil quality and agricultural sustainability as it plays a key role in the provision of ecosystem services. Higher 
taxa of this fauna are often used to evaluate soil management, given that they are influenced by land-use and 
produce a fast response. Therefore, this study evaluates the short-term effects of the slash-and-burn or the slash- 
and-mulch system, after different durations of fallow on the composition, density, and diversity of the soil 
macrofauna higher taxa and selected physical and chemical attributes. Results are compared to old-growth forest 
and secondary forest fragments. The slash-and-mulch fields had soil fertility attributes similar to slash-and-burn 
and macrofauna diversity and composition were similar to forests. In particular, functional groups like ecosystem 
engineers or predators augmented with slash-and-mulch and were efficient indicators of land-use change. Despite 
its scarcity and their very high fragmentation, old-growth forest small remnants do conserve a more diverse and 
abundant soil invertebrates community of saprophages and predators, therefore their conservation is of utmost 
importance. This is the first study to show the potential of the slash-and-mulch system in this region to enhance 
the resilience of the smallholders’ landscapes. Nonetheless, soil quality needs to be monitored to confirm the 
effective restoration of soil functionality and agriculture productivity. 
1. Introduction 
Slash-and-burn agriculture or shifting cultivation has been practiced 
for thousands of years in the tropics (Pedroso et al., 2008). This cropping 
system consists in cut down all the forest vegetation that is allowed to 
dry and is burned just before the staple crops sowing. Thereafter, the 
area is left to regrow and fallow vegetation restores the soil fertility. It is 
considered a sustainable agricultural method in conditions of low pop-
ulation density, high land availability, and long fallow periods (Pedroso 
et al., 2008; Padoch and Pinedo-Vasquez, 2010; Lawrence et al., 2010). 
However, the population growth and its demand for land have led to 
agriculture intensification (Van Vliet et al., 2012), and caused the 
reduction of fallow periods thus making those systems increasingly less 
productive and sustainable (Ayarza et al., 2010; Loch et al., 2021). 
Indeed slash-and-burn agriculture is often associated with deforestation, 
global warming, soil degradation, and biodiversity loss (Pedroso et al., 
2008). In Alcântara and Eastern Amazon, the cropping cycle only lasts 
one year and fallow less than 10 years (Loch et al., 2021). Globally, 
* Corresponding author. 
E-mail addresses: guillaumerousseau@professor.uema.br (G. Rousseau), jeburgos551@gmail.com (J. Burgos-Guerrero), hglm72@gmail.com (L. Hernández- 
García), egomezca@hotmail.com (E. Gómez-Cardozo), stefaniapt@gmail.com (S. Triana), julius0076@hotmail.com (J. Medina), kellen_ruth@hotmail.com (K. da 
Silva), danicelentano@yahoo.com.br (D. Celentano). 
Contents lists available at ScienceDirect 
Pedobiologia - Journal of Soil Ecology 
journal homepage: www.elsevier.com/locate/pedobi 
https://doi.org/10.1016/j.pedobi.2022.150840 
Received 10 March 2022; Received in revised form 11 August 2022; Accepted 14 September 2022 
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slash-and-burn agriculture is expected to drastically decline and prob-
ably disappear by 2090 due to the competition with industrial agricul-
ture, tree plantations, urban expansion, and forest protection and 
restoration (Heinimann et al., 2017). This poses serious threats to the 
livelihood of the small farmers that currently practice this kind of 
agriculture. For these reasons, academic institutions, governments, and 
non-governmental organizations, together with farmers, are seeking 
alternatives to replace this farming system (Padoch and Pinedo-Vasquez, 
2010). 
Proposed alternative systems have included alley cropping (Moura 
et al., 2009), chop-and-mulch (Vielhauer et al., 2004), slash-and-mulch 
(Erenstein, 2003), no-tillage (Baretta et al., 2014), and agroforestry 
systems (Pinho et al., 2012), including the Quesungual agroforestry 
system (CIAT, 2009). This system consists of cutting and pruning the 
natural vegetation to provide permanent soil cover and permit trees and 
shrubs to regenerate within the crop field. Quesungual adoption is 
widespread in Honduras and Nicaragua (Rousseau et al., 2013) and the 
system has the potential to be transferred to other regions. In this study, 
we propose to explore the effects of an adaptation of the Quesungual 
system by Alcântara farmers on soil macrofauna and selected soil 
fertility attributes. 
The effects of slash-and-burn vs. slash-and-mulch systems on soil 
macrofauna and soil fertility, especially in the long term, are poorly 
documented in the literature with some exceptions. We found no report 
on the use of the slash-and-mulch practice in the Amazon region of 
Maranhão. The only results referred to the SHIFT program (Studies of 
Human Impact on Forests and Floodplains in the Tropics) and Tipitamba 
project developed by Embrapa in the neighboring Bragantina region of 
Pará State which promoted chop-and-mulch i.e. the mechanized version 
of slash-and-mulch (Vielhauer et al., 2004; Rousseau et al., 2010). 
Repeated burning cycles are generally acknowledged to reduce soil 
fertility (Sommer et al., 2004), biomass accumulation in subsequent 
cycles (Lawrence et al., 2010), and soil macrofauna (Rossi et al., 2010; 
Rousseau et al., 2014). According to Rousseau et al. (2010), more 
earthworms were present in chop-and-mulch than in slash-and-burn or a 
40 years secondary forest in the Bragantina region of Pará State. No 
differences were reported for ant abundance while other invertebrates 
were also much more abundant in chop-and-mulch than inslash-and-burn or a 40 years secondary forest. For total richness, no 
differences were found for earthworms and ants between 
chop-and-mulch and slash-and-burn. In Quesungual agroforestry sys-
tems from Western Honduras, Fonte et al. (2010) found more earthworm 
biomass than in slash-and-burn systems. In a review from Africa, Hauser 
et al. (2012) reported that burning greatly reduced cast deposition by 
worms compared with mulching on the Ultisols included in the review. 
The soil macrofauna community is directly and indirectly associated 
with soil quality and agricultural sustainability (Brussaard et al., 2007). 
These invertebrates play a key role in the provision of soil ecosystem 
services as their density and diversity are associated with better soil 
functioning (Lavelle et al., 2006; Rousseau et al., 2014). Broad taxo-
nomic groups of soil macrofauna (class, order, or family) are often used 
to evaluate soil management strategies and the restoration process 
(Vasconcellos et al., 2013; Rousseau et al., 2013), given that they are 
strongly influenced by land-use systems and produce a fast response 
(Barros et al., 2002; Lavelle et al., 2006; Marichal et al., 2014; Moura 
et al., 2015). In the eastern Amazon, Rousseau et al. (2014) studied the 
composition and diversity of the soil macrofauna higher taxa in a 
chronosequence of fallow and forests and found long-lasting impacts of 
soil degradation on macrofauna and associated soil ecological functions. 
In Central America, Rousseau et al. (2012) found that the abundance of 
macrofauna groups was a good indicator of soil quality in agroforestry 
systems compared to mature forests. Nonetheless, literature on the 
whole soil macrofauna community (class, order, or family) is scarce in 
the Amazon with a total of eighteen articles (search keys: "soil macro-
fauna" OR "soil invertebrates" OR "soil fauna" OR "soil macro-
invertebrates" OR "edaphic macrofauna" AND Amazon; 17 databases). 
Six articles focused on agroforestry systems (Barros et al., 2003; Laossi 
et al., 2008; Moura et al., 2015; Suárez Salazar et al., 2015; Durán 
Bautista et al., 2018; Suárez et al., 2018), four on diverse land-uses 
(Barros et al., 2002; Mathieu et al., 2005; Marichal et al., 2014; Rous-
seau et al., 2014), four on pastures (Barros et al., 2004; Decaëns et al., 
2004; Mathieu et al., 2004, 2009; Feigl et al., 2006) and three on forest 
(Römbke et al., 2006; Santos et al., 2008; Tapia-Coral et al., 2019). As a 
consequence, there is an urgent need to study the effects of land-use 
change and agricultural systems on soil macrofauna in the region. 
This study evaluates the short-term effects of the slash-and-burn or 
the slash-and-mulch system, after different durations of fallow on the 
composition, density and diversity of the soil macrofauna higher taxa 
and selected physical and chemical attributes. Results are compared to 
mature forest, and secondary forest fragments present in the landscape. 
We hypothesize that the macrofauna community of the slash-and-mulch 
system will be more similar to the fallows than to the slash-and-burn and 
that the old-growth forest fragments will conserve a more diverse 
macrofauna community. 
2. Materials and methods 
2.1. Study area 
The study was conducted in five villages in the municipality of 
Alcântara, northern Maranhão state, Brazil (02º19’17’’ - 02º24’05’’ S 
and 44º25’42’’- 44º28’49’’ W) (Fig. 1). This region is part of the Eastern 
Amazon biome (IBGE, 2002). The climate is tropical with dry summer As 
type, according to the classification system of Köppen (Alvares et al., 
2013), with two well-defined seasons: a rainy season from January to 
June and a dry season from July to December. The average annual 
precipitation varies between 1000 and 1800 mm, with an average 
temperature of 25 ◦C (Brito and Rego, 2001). The soil is classified as 
Plinthosol (Anjos et al., 1995) characterized by low fertility and prone to 
cohesion (Moura et al., 2009). The landscape is dominated by young 
secondary forests, some old forest fragments (Zelarayán et al., 2015), 
and areas with slash-and-burn agriculture. The population is very poor 
(IDHM=0.573; PNUD, 2013) and relies on slash-and-burn agriculture 
for subsistence (Celentano et al., 2014). The average fallow duration is 
6.6 years with only one crop cycle dominated by Zea mays, Manihot 
esculenta, Citrullus lanatus, Cucumis anguria, and Oryza sativa (Loch et al., 
2021). 
2.2. Experimental design 
The experimental design comprised of four land-uses and two age 
classes organized in an unbalanced completely randomized design 
(Table 1, Fig. 1). Land-uses were: OF - Old-growth forest (> 120 yr old, 
with selective logging, n = 5); SF secondary forests (3–30 yr old, 
n = 12); SB - slash-and-burn from 3 to 10 yr old secondary forests 
(n = 8); SM - slash-and-mulch from 3 to 8 yr old secondary forests 
(n = 8). For slash-and-burn and slash-and-mulch Young (Y) slashed 
secondary forests were 3–5 yr old (n = 4) and Intermediate (I) were 
7–8 yr old (n = 4). For secondary forests Y were 3–10 yr old (n = 6) and 
I were 11–30 yr old (n = 6)(Table 1, Fig. 2). These differences were 
caused by the lack of secondary forest older than 8 yr old available for 
the farmers to cultivate due to land tenure issues. Forest ages (time since 
last slash-and-burn) were reported by each landowner (Table 1). The 
slash-and-mulch and slash-and-burn systems were implemented in 
40×50 m plots (0.2 ha) in October 2014 and 2015. To prepare the slash- 
and-burn plots, all vegetation inside the plots was cut, evenly distrib-
uted, and burned (after two months when it was completely dry). Cas-
sava (Manihot esculenta Crantz) and maize (Zea mays) were planted at 
the beginning of the rainy season (March 2015 and February 2016). The 
slash-and-burn system was implemented exactly as the farmers tradi-
tionally do in this region. To prepare the slash-and-mulch plots, trees 
were pruned to 1.5 m of height, and those of interest (fruit and timber) 
G. Rousseau et al. 
Pedobiologia - Journal of Soil Ecology 95 (2022) 150840
3
were left standing, then the material (leaves and branches) were placed 
as mulching throughout the plot (FAO, 2005)(Fig. B.1). In March 2015 
and February 2016, we planted cassava, maize, pigeon peas (Cajanus 
cajan), and jack beans (Canavalia ensiformis) as green manure (Fig. 2: 
YSM and ISM). Before the sowing, the plots were manured with lime-
stone (2 Mg ha− 1) and rock phosphate (0.34 Mg ha− 1). Maize received 
additional urea (100 Kg ha− 1) at the 8 leaves stage. The slash-and-mulch 
system is an adaptation of the Quesungual system (FAO, 2005) where 
green manure, limestone, and rock phosphate aim to compensate for the 
lack of nutrients from ash and build more durable soil fertility according 
to Moura et al. (2009, 2015). Canopy cover was estimated after land 
preparation with a spherical convex densiometer and four separate 
readings were taken in each plot and averaged. 
2.3. Soil macrofauna sampling 
Sampling was carried out in May 2015 and June 2016 (end of the 
rainy season), six and seven months after land preparation respectively. 
Half of the plots per land-use were sampled in 2015 and half in 2016 
(Table 1). Macrofauna was collected according to the modified Tropical 
Soil Biology and Fertility method (TSBF, Anderson and Ingram, 1993). 
Five soil monoliths of 0.25×0.25 m and 0.10 m soil depth were 
extracted in a cruciform shape from each plot, with one central monolith 
and one 20 m apart in each direction (North, South, East, and West). The 
macrofauna (soil invertebrates with 2 mm<body diameter<20 mm) 
were hand-sorted from litter and soil separately, preserved in 99% 
alcohol, and identified to large taxa (class, order, or family).Taxa were 
thereafter classified according to their function in the soil (Moço et al., 
2010; Potapov et al., 2022)(Table 2). The specimens captured were 
deposited in the Soil Invertebrates Collection of the Maranhão State 
University. 
2.4. Soil analysis 
Five soil samples were sampled in each plot (next to each monolith) 
from 0 to 10 cm depth, with volumetric rings of 282.6 cm3 volume. The 
soil was weighed wet and divided into sub-samples according to the type 
of analysis. For determination of moisture content and bulk density, a 
40 g soil sub-sample was oven-dried at constant temperature (105 ◦C for 
48 h) and the moisture percentage and the bulk density were calculated. 
The remaining soil was air-dried and passed through a 2 mm sieve. The 
textural composition was determined according to the pipette method 
(Embrapa, 1997). For chemical analysis, we followed the procedures of 
the Agronomic Institute of Campinas (van Raij et al., 2001) to determine 
the pH (0.01 M suspension in Calcium Dichloride, CaCl2), total organic 
carbon content (by Loss On Ignition at 360◦C in a muffle furnace), resin 
exchangeable Phosphorus, (P) Potassium (K), Calcium (Ca), Magnesium 
(Mg), Sodium (Na) and Potential Acidity as Hydrogen+Aluminum 
(H+Al)(Shoemaker-McLean-Pratt method). We also calculated the 
Effective Cation Exchange Capacity (ECEC) as K+Ca+Mg+Al, the 
Cation Exchange Capacity (CEC) as ECEC+H, the sum of bases (SB) as 
K+Ca+Mg, and the Base Saturation (Sat) as 100 x SB/CEC (van Raij 
et al., 2001)(Table 3). 
Fig. 1. Location of study areas in Alcântara, Maranhão, Brazil. Land-uses: OF: Old-growth Forest; YSF: Young Secondary Forest; ISF: Intermediate Secondary Forest; 
YSM: Slash-and-Mulch field from YSF; ISM: Slash-and-Mulch field from ISF; YSB: Slash-and-Burn field from YSF; ISB: Slash-and-Burn field from ISF. 
G. Rousseau et al. 
Pedobiologia - Journal of Soil Ecology 95 (2022) 150840
4
2.5. Statistical analysis 
2.5.1. Univariate analysis and rarefaction curves 
The density of each macrofauna taxon was calculated as the mean 
individual density per square meter (ind⋅m− 2) in the plot (mean of five 
monoliths). The total density of soil macrofauna was calculated as the 
sum of mean density per square meter (ind⋅m− 2) across taxa and di-
versity was assessed through total richness (S), Margalef richness (d), 
Shannon-Wiener (H), and Pielou (J) indices at plot level (adapted from 
Bandeira et al., 2013). To determine the effect of land-use on the mac-
rofauna (density and diversity) and environmental (canopy and soil) 
variables, we performed one-way ANOVA on the four land-uses in an 
unbalanced completely randomized design: OF= 5 repetitions, SF= 12, 
SM= 8, and SB= 8 (Table 1). To assess the effect of fallow age and age x 
land-use interaction we performed a two-way ANOVA on the three 
land-uses (SF, SB, SM) with two age classes (Y, I) in an unbalanced 
completely randomized design. Each combination of land-use × age 
class had four to six repetitions (Table 1). Homoscedasticity was checked 
through the Levene test. Variables were ln(x + 1) transformed when 
required. After transformation, only Neuroptera did not present homo-
scedasticity. Means were compared according to Tukeýs HSD test, with a 
significance level of p ≤ 0.05. All statistical analyses were performed 
with the software R (R Core Team, 2020). The packages lattice (Sarkar 
and Sarkar, 2007), car (Fox et al., 2013), and agricolae (De Mendiburu, 
2009) were used for ANOVA and related tests. Rarefaction curves were 
performed for each land-use using the package BiodiversityR (Kindt and 
Kindt, 2019). 
2.5.2. Principal component and between-class analysis 
The matrix composed of total density and diversity indices was 
considered to represent the “community structure” while the matrix 
composed of the density of all macrofauna taxa is considered as “com-
munity composition”. The Principal Component Analysis (PCA) was 
performed on ln(x + 1) transformed data to explore the correlations 
between the macrofauna variables and represent the position of land- 
uses plots in the macrofauna space. To assess the multivariate effects 
of land-uses and fallow age on the macrofauna community structure and 
composition, Between-Class Analysis (BCA) was performed on ln(x + 1) 
transformed data. The BCA is a canonical extension of PCA where the 
contributions of the land-use and age classes to the species matrix are 
estimated and tested. The class effect was assessed through a Monte 
Carlo test with 999 permutations (Chessel et al., 2004). Classes were set 
according to the four land-uses (OF, SF, SB, SM) to test for land-use effect 
and three age classes Mature (M), Intermediate (I), Young (Y) to test for 
age effect. To test for the land-use x age class interaction, the classes 
were Mature Forest (OF), Intermediate Secondary Forest (ISF), Young 
Secondary Forest (YSF), Intermediate Slash-and-Burn (ISB), Young 
Slash-and-Burn (YSB), Intermediate Slash-and-Mulch (ISM) and Young 
Slash-and-Mulch (YSM) (Dolédec and Chessel, 1987; Chessel et al., 
2004). The same procedure was repeated for the canopy and 
physical-chemical attributes of the soil that were significantly affected 
by land-uses (Table 3). The BCA was performed with the ade4 package 
(Dray et al., 2003). 
2.5.3. Co-inertia analysis 
To verify if the effects of land-use or fallow age on the macrofauna 
community structure and composition could be explained by changes in 
the canopy and soil physical-chemical attributes, a co-inertia analysis 
(CIA) was performed. The co-inertia seeks a common structure between 
the matrices, in this case, it coupled the PCA performed on macrofauna 
matrices with the PCA performed on the canopy and physical-chemical 
matrix. The co-structure between the couples of matrices is estimated by 
the Rv coefficient (Dray et al., 2003). The co-inertia analysis was per-
formed with the ade4 package. 
Table 1 
Description of plots and land uses in Alcântara Municipality, Maranhão State, Brazil. 
Land use Abbreviation Years of succession Abbreviation Village Coordinates S-W Sampling year 
Slash-and-Burn (n = 8) SB 4 YSB Cajueiro 02º22’24’’ 44º27’45’’ 2015 
3 Espera 02º22’13’’ 44º26’42’’ 
4 Espera 02º22’08’’ 44º26’44’’ 2016 
5 Espera 02º22’04’’ 44º26’19’’ 
8 ISB Só assim 02º21’26’’ 44º28’40’’ 2015 
7 Espera 02º21’55’’ 44º27’14’’ 
7 Só assim 02º21’28’’ 44º28’49’’ 2016 
7 Espera 02º21’53’’ 44º27’15’’ 
Slash-and-Mulch (n = 8) SM 4 YSM Cajueiro 02º22’24’’ 44º27’42’’ 2015 
3 Espera 02º22’09’’ 44º26’42’’ 
3 Espera 02º22’09’’ 44º26’42’’ 2016 
3 Espera 02º22’04’’ 44º26’18’’ 
8 ISM Só Assim 02º21’27’’ 44º28’40’’ 2015 
7 Espera 02º21’54’’ 44º27’14’’ 
7 Espera 02º21’54’’ 44º27’13’’ 2016 
7 Só Assim 02º21’27’’ 44º28’40’’ 
Secondary forest (n = 12) SF 5 YSF Espera 02º22’13’’ 44º26’40’’ 2015 
4 Cajueiro 02º22’26’’ 44º27’43’’ 
4 Espera 02º22’02’’ 44º26’23’’ 2016 
5 Espera 02º22’03’’ 44º26’42’’ 
7 Espera 02º21’52’’ 44º27’14’’ 2015 
8 Só Assim 02º21’29’’ 44º28’39’’ 
10 Só Assim 02º21’21’’ 44º28’44’’ 2016 
10 Espera 02º21’51’’ 44º27’16’’ 
20 ISF Espera 02º21’56’’ 44º27’10’’ 2015 
30 Maruda 02º19’17’’ 44º28’28’’ 
30 Old Pepital 02º21’02’’ 44º25’48’’ 2016 
30 Old Pepital 02º20′57′’ 44º25′42′’ 
Old-growth forest (n = 5) OF > 120 Espera 02º21’58’’ 44º27’16’’ 2015 
> 120 Cajueiro 02º24’02’’ 44º27’40’’ 
> 120 Espera 02º21’57’’ 44º27’16’’ 2016 
> 120 Cajueiro 02º24’05’’ 44º27’33’’ 
> 120 Cajueiro 02º24’06’’ 44º27’44’’ 
G. Rousseau et al. 
Pedobiologia - Journal of Soil Ecology 95 (2022) 150840
5
3. Results3.1. Summary data 
A total of 6121 individuals were counted and classified into 26 
taxonomic groups, of which the most abundant were Isoptera (33.1%), 
Formicidae (28.8%), Oligochaeta (16.9%), Coleoptera (4.6%), Chilo-
poda (3.7%), Araneae (3.6%), Diplura (1.4%), Gastropoda (1.2%), and 
Pseudoscorpiones (1.1%). The other groups represented less than 1% of 
the total abundance. Mature Forest (OF) was the only land-use with the 
presence of all 26 taxa found in the study. Auchenorrhyncha and 
Scorpiones were represented by one single individual in the OF. Ac-
cording to the rarefaction curve, all land-uses were saturated or close to 
saturation (Fig. B.2). 
3.2. Soil macrofauna composition 
Twenty-one taxa were found in all land-use systems (Araneae, Blat-
todea, Chilopoda, Coleoptera adult and larva, Diplopoda, Diplura, 
Diptera adult and larva, Formicidae, Gastropoda, Heteroptera, Hyme-
noptera, Isopoda, Isoptera, Ixodidae, Lepidoptera larva, Oligochaeta, 
Opiliones, Orthoptera, and Pseudoscorpiones), whereas two taxa 
Fig. 2. View of the land-uses evaluated in Alcântara, Maranhão, Brazil. Land uses: OF: Old-growth Forest; YSF: Young Secondary Forest; ISF: Intermediate Secondary 
Forest; YSM: Slash-and-Mulch field from YSF; ISM: Slash-and-Mulch field from ISF; YSB: Slash-and-Burn field from YSF; ISB: Slash-and-Burn field from ISF. 
G. Rousseau et al. 
Pedobiologia - Journal of Soil Ecology 95 (2022) 150840
6
(Auchenorryncha and Scorpiones) were exclusive in OF. Thirteen taxa 
had densities that differed significantly between the land-uses (Table 2). 
Among ecosystem engineers, Formicidae had significantly higher den-
sity in OF and SM than in SB, while Oligochaeta density was high (>109 
Ind⋅m− 2) in all land-uses except SB (42 Ind⋅m− 2). Isoptera was not 
affected by land-use. Among predators, five taxa had significantly higher 
densities in OF, while densities in SM and SF were not significantly 
different from OF. Nonetheless, only Chilopoda and Pseudoscorpiones 
had densities significantly higher in SM than SB (Table 2). Among sap-
rophages, Blattodea had the highest densities in SM and OF, while 
Table 2 
Soil macrofauna taxa (mean±SD) in four land uses of Alcântara, Eastern Amazon, in 2015–2016. 
Macrofauna taxa (ind⋅m− 2)/Functional group Land uses 
Old-growth Forest Secondary Forest Slash-Mulch Slash-Burn F P 
Ecosystem engineer 
Formicidae (omnivore) 320.6 ± 179.3aa 134.4 ± 177.6ab 281.2 ± 151.3a 80.0 ± 76.8b 6.17 0.0021 
Isoptera (saprophage) 307.2 ± 163.6 260.2 ± 494.6 128.8 ± 115.4 154.8 ± 164.2 1.25 0.31 
Oligochaeta (saprophage) 181.8 ± 105.9a 112.2 ± 85.2a 109.6 ± 76.6a 42.4 ± 48.1b 3.26 0.0352 
Predator 
Araneae 49.3 ± 23.8a 14.0 ± 9.8b 29.2 ± 15.3ab 15.2 ± 9.0b 9.39 0.0001 
Chilopoda 60.2 ± 21.1a 18.5 ± 12b 31.2 ± 28.4ab 4.8 ± 4.2c 12.18 0.0001 
Diplura 19.2 ± 15.8a 12.1 ± 8.1a 8.4 ± 13.9ab 1.2 ± 2.4b 7.04 0.001 
Neuroptera larvab 1.9 ± 2.9 0.2 ± 0.9 0.0 ± 0.0 0.0 ± 0.0 3.25 0.0354 
Hymenoptera (not Formicidae) 0.6 ± 1.4 2.2 ± 6.2 0.8 ± 1.5 0.8 ± 1.5 0.07 0.97 
Opiliones 31.4 ± 39.7a 3.9 ± 6.7ab 2.8 ± 6.7ab 0.4 ± 1.1b 3.80 0.0202 
Pseudoscorpiones 12.2 ± 10.0a 5.2 ± 5.6ab 11.6 ± 8.4a 1.2 ± 2.4b 4.96 0.0065 
Saprophage 
Blattodea 4.5 ± 4.3ab 1.47 ± 3.1b 9.2 ± 13.5a 0.4 ± 1.1b 5.48 0.004 
Diplopoda 12.8 ± 10.6a 2.0 ± 3.1b 2.4 ± 3.7b 6.0 ± 8.4ab 4.14 0.0144 
Isopoda 14.0 ± 15.8a 1.2 ± 2.1b 2.4 ± 5.6b 1.2 ± 2.4b 6.67 0.0014 
Herbivore 
Embioptera (phycophage) 1.9 ± 2.9ab 2.2 ± 2.4ab 3.6 ± 3.2a 0.0 ± 0.0b 3.87 0.0188 
Heteroptera 5.1 ± 3.6 2.0 ± 2.8 4.8 ± 9.8 1.2 ± 1.6 1.35 0.28 
Lepidoptera larva 3.8 ± 5.2 1.2 ± 2.1 2.8 ± 3.6 1.6 ± 1.7 0.73 0.54 
Orthoptera 4.5 ± 3.6 1.7 ± 3.1 4.4 ± 5.1 1.2 ± 2.4 2.56 0.0736 
Omnivore 
Coleoptera adult 35.2 ± 12.8 16.5 ± 10.3 22 ± 10.9 16.8 ± 20.6 2.47 0.08 
Coleoptera larva 12.8 ± 6.8 9.3 ± 8.4 8.4 ± 6.4 6.4 ± 5.7 1.13 0.35 
Dermaptera 1.3 ± 1.7 0.7 ± 1.9 1.6 ± 4.5 0.0 ± 0.0 0.78 0.51 
Diptera adult 0.6 ± 1.4 1.0 ± 2.7 1.2 ± 1.6 0.8 ± 1.5 0.22 0.88 
Diptera larva 3.2 ± 4.5 2.0 ± 2.1 2.0 ± 2.9 0.4 ± 1.1 1.1 0.36 
Ixodidae 1.3 ± 1.7 2.2 ± 3.5 0.4 ± 1.1 0.4 ± 1.1 1.18 0.33 
Gastropoda (microbivore) 6.4 ± 4.5ab 6.4 ± 10.3ab 13.2 ± 20.8a 2.4 ± 5.6b 3.13 0.0401 
Not Identified 3.2 ± 3.9 2.7 ± 3.4 4.0 ± 8.1 1.6 ± 1.7 0.16 0.92 
a Lowercase letters indicate significant differences between land uses according to Tukey test (P < 0.05). 
b Heteroscedasticity according to Levene test. 
Table 3 
Canopy cover and soil attributes (mean±SD) in four land uses of Alcântara, Eastern Amazon, in 2015–2016. 
Land uses 
Units Mature Forest Secondary Forest Slash-Mulch Slash-Burn F P 
Canopy cover % 88.2 ± 0.4aa 82.5 ± 6.4a 10.4 ± 3.9b 2.0 ± 2.9c 778.3 0.0001 
Physical attributes 
Water content % 9.1 ± 4.1 11.8 ± 3.5 11.6 ± 3.6 10.2 ± 4.2 0.79 0.51 
Bulk density g.cm− 3 1.27 ± 0.09 1.29 ± 0.11 1.39 ± 0.18 1.39 ± 0.11 1.89 0.15 
Water-filled pore space % 23.2 ± 14.5 30.7 ± 12.0 35.4 ± 16.1 30.2 ± 14.0 0.80 0.50 
Coarse sand % 18.1 ± 3.4 16.6 ± 4.0 17.7 ± 8.9 17.3 ± 4.0 0.12 0.95 
Fine sand % 60.5 ± 4.5 62.3 ± 3.7 60.8 ± 8.7 60.8 ± 4.9 0.22 0.88 
Silt % 5.1 ± 0.9 5.7 ± 1.3 5.3 ± 0.8 5.6 ± 1.0 0.50 0.69 
Clay % 16.2 ± 1.6 15.3 ± 2.6 16.1 ± 1.9 16.2 ± 5.0 0.20 0.89 
Chemical attributes 
pH – 4.1 ± 0.4d 4.2 ± 0.4c 5.3 ± 0.4a 4.7 ± 0.4b 12.9 0.0001 
Organic carbon Mg.ha− 1 21.7 ± 3.0 26.3 ± 18.9 21.8 ± 6.1 19.6 ± 4.1 0.55 0.65 
Phosphorus Mg.ha− 1 0.04 ± 0.02 0.04 ± 0.01 0.09 ± 0.10 0.05 ± 0.02 2.23 0.11 
Potassium Mg.ha− 1 0.06 ± 0.01 0.08 ± 0.04 0.09 ± 0.02 0.09 ± 0.02 1.22 0.32 
Calcium Mg.ha− 1 0.36 ± 0.28ab 0.33 ± 0.25b 0.63 ± 0.17a 0.46 ± 0.19ab 3.07 0.04 
Magnesium Mg.ha− 1 0.13 ± 0.05ab 0.12 ± 0.06b 0.41 ± 0.51a 0.17 ± 0.09ab 3.11 0.04 
Sodium Mg.ha− 1 0.06 ± 0.01 0.10 ± 0.04 0.11 ± 0.03 0.10 ± 0.04 2.04 0.13 
Aluminum Mg.ha− 1 0.18 ± 0.17ab 0.21 ± 0.17a 0.03 ± 0.07b 0.04 ± 0.04b 4.62 0.0089 
Hydrogen Mg.ha− 1 0.65 ± 0.15ab 0.73 ± 0.19a 0.42 ± 0.16b 0.47 ± 0.24b 5.26 0.0049 
Acidity Mg.ha− 1 0.83 ± 0.29ab 0.94 ± 0.31a 0.46 ± 0.22b 0.52 ± 0.25b 6.65 0.0014 
Sum of bases Mg.ha− 1 0.55 ± 0.32ab 0.54 ± 0.31b 1.13 ± 0.58a 0.73 ± 0.28ab 4.27 0.0126 
E.CEC mmolc.dm− 3 29.2 ± 11.1 28.4 ± 9.5 50.9 ± 32.7 30.6 ± 13.8 2.78 0.0584 
CEC mmolc.dm− 3 80.1 ± 10.4 84.5 ± 15.9 81.2 ± 34.7 64.5 ± 22.2 1.38 0.27 
Saturation % 29.8 ± 15.5 BCE 26.7 ± 14.2c 58.6 ± 16.4a 45.5 ± 14.9ab 8.54 0.0003 
a Lowercase letters indicate significant differences between land uses according to Tukey test (P < 0.05). 
G. Rousseau et al. 
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Diplopoda and Isopoda had significantly highest densities in OF. Among 
omnivores, Gastropoda were more abundant in SM than SB, SF and OF 
had intermediate densities. Other omnivores were not affected by land- 
use (Table 2). The age of the land-use system had a significant positive 
effect only on Isopoda and did not present interaction with land-use 
(Table A.2). 
The Principal Component Analysis (PCA) on community composition 
represented 39% of total variation on the first two components. All taxa 
but Hymenoptera were negatively correlated to the first component 
(PC1 =24.8%) which means this axis separates plots depending on their 
fauna density (Fig. 3a). Land-uses separated along with this component: 
SM and OF had higher density for most taxa while SB had higher 
Hymenoptera density (Fig. 3b). The 2nd component (PC2 =14.2%) 
separated different sub-communities of invertebrates: Oligochaeta, Not 
Identified taxa, Diptera adults, Dermaptera, and Lepidoptera larvae 
were negatively correlated,and Ixodidae, Isoptera, and Orthoptera 
positively correlated to PC2. All other taxa were more correlated to PC1 
than PC2 (Fig. 3a). Land-uses poorly separated along PC2 nonetheless, 
plots inside land-uses clouds were strongly dispersed along PC2, espe-
cially in OF and SF (Fig. 3b). 
The Between-Class Analysis (BCA) on community composition with 
land-uses as classes explained 21.9% of total inertia (P = 0.0001) 
(Table 4) with 67.4% of inertia on BC1 and 17.4% on BC2. The BC1 axis 
was similar to PC1 but BC2 better-separated land-uses with the two sub- 
Fig. 3. The Principal Component Analysis (PCA) on macrofauna community in Alcântara, Maranhão, Brazil: a) correlation circle for macrofauna taxa; b) variability 
of scores among land uses with boxes placed at the centroid of land uses, and 95% confidence ellipse; c) correlation circle for macrofauna structure variables; d) 
variability of scores among land uses with boxes placed at the centroid of land uses, and 95% confidence ellipse. See Tables 1 and 2 for abbreviations. 
G. Rousseau et al. 
Pedobiologia - Journal of Soil Ecology 95 (2022) 150840
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communities associated with OF and SM revealed in PCA. The BCA with 
the interaction land-use x age explained 30.5% of total inertia (P =
0.0003) with 57.7% on BC1 and 14.4% on BC2. The land-use effect is the 
main source of data variability, and the age effect the second, with a 
clear separation of OF from the others, and the segregation of the oldest 
classes inside both secondary forests and agricultural systems (Fig. B.4). 
3.3. Soil macrofauna density and diversity 
Total macrofauna density (D) was significantly higher in OF with 
1113 Ind⋅m− 2 than in Slash-and-burn (SB) with 344, while Secondary 
Forest (SF) and Slash-and-mulch (SM) were not significantly different 
from both OF and SB. Richness (S) was significantly higher in OF (19) 
than in any other land-use. The Richness in SF and SM was not signifi-
cantly different (14, 15) but, was significantly higher than in SB (10). 
Margalef was significantly lower in SB (1.6) than in any other land-use 
(>2.2). Shannon-Wiener was significantly higher in OF (1.9) than in any 
other land-use. Pieloús evenness was not significantly different between 
land-uses (Table 5). The age effect was significant for D and S where 
older systems had higher density and richness than younger ones 
(Table A.1). There was no significant interaction between land-use and 
age class. 
The PCA on community structure represented 93.2% of total varia-
tion on the first two components. The PC1 (52%) separated plots ac-
cording to their richness (Margalef and Richness) (Fig. 3c). The land- 
uses separated mainly along with PC1: OF was the richest land-use 
and SB the poorest, SM and SF had intermediate richness (Fig. 3d). 
The PC2 (41.2%) separated plots according to Pieloús evenness (J) and 
total Density (D) (Fig. 3c). The land-uses were less separated along PC2 
but OF had the highest densities and SB the lowest while SM and SF had 
intermediate densities (Fig. 3d). 
3.4. Canopy and soil attributes 
Canopy cover was well developed in forests and was not significantly 
different between OF and SF (88% and 82%). Despite the suppression of 
the secondary vegetation during slash-and-mulch land preparation, this 
system retained a significantly higher canopy cover (10%) than slash- 
and-burn (2%) (Table 3). Soil physical attributes were not affected by 
land-use. Among the fourteen soil chemical attributes, eight were 
significantly affected by land use with the greatest differences between 
SM and SF. The pH and bases-related variables (K, Ca, Mg, Sum of Bases, 
ECEC, CEC, Base Saturation) were the highest under SM and the lowest 
in forests (OF, and/or SF), while acidity-related variables (Al, H, Acid-
ity) were the lowest in SM and the highest in SF (Table 3). There was no 
age effect nor interaction between land-uses and age classes on soil 
physical and chemical attributes nonetheless, there was an interaction 
for canopy: ISB conserved 4% of canopy cover while YSB has 0% canopy 
cover (Table A.3). 
The PCA on canopy and soil physical-chemical attributes represented 
83% of total variation on the first two components. The PC1 (62.5%) 
separated plots according to acidity-related variables vs. pH and bases- 
related variables. Forests strongly correlated to acidity and agriculture 
to bases along this axis. The PC2 (21.2%) separated plots according to 
CEC and bases concentrations; SB was negatively correlated to CEC but 
positively to bases while SM was positively correlated to bases and 
slightly correlated to CEC (Fig. B.3). 
The BCA on canopy and soil physical-chemical attributes explained 
39.6% of total inertia (P = 0.0001)(Table 5) with 86.5% on BC1 and 
12.8% on BC2. Both BCA axes are similar to PCA and confirm the 
chemical shift realized in both agricultural systems to attend crop de-
mand (Fig. B.5). The BCA with age as classes explained 5.2% of total 
inertia (P = 0.49). 
3.5. Macrofauna composition, canopy and soil attributes 
The co-inertia (CIA) is a versatile multivariate analysis that seeks for 
co-structure between two tables and allows the representation of the 
plots in the two spaces (Dray et al., 2003). It indicated no co-structure 
between soil macrofauna composition and soil physical-chemical attri-
butes plus canopy (Rv=0.13, P = 0.44) (Table 4) i.e. the effects of 
land-uses on the macrofauna community are poorly explained by the 
differences in the canopy and soil physical-chemical identified between 
land-uses (Table 3). The co-inertia axis 1 (CIA1) represented 63.2% of 
total inertia and separated forests from agriculture plots with 16 taxa 
positively correlated to forest and 9 to agriculture. All predator taxa but 
Araneae were positively correlated with forests (Fig. 4a and c). The CIA2 
(20.6% of inertia) separated OF from SB plots, with 18 taxa positively 
correlated to OF and 7 to SB (Fig. 4a and c). The CIA1 is positively 
correlated to acidity-related variables (forests) and therefore negatively 
correlated to bases-related variables (agriculture). The CIA2 is nega-
tively correlated to CEC and Canopy (OF)(Fig. 4b and c). 
Table 4 
Principal Component and Co-inertia analysis between soil macrofauna community composition (structure) and soil physical-chemical attributes (plus canopy) of slash- 
and-mulch, slash-and-burn, secondary forest and forest of Alcântara, Eastern Amazon, in 2015–2016. 
Total inertia First eigenvalue Inertia ratio (%) P 
PCA Fauna community composition 25 6.2 
BCA Composition x Land use 5.5 3.7 21.9 0.0001 
PCA Fauna community structure 5 2.6 
BCA Structure x Land use 1.43 1.39 28.5 0.0006 
PCA Canopy and soil attributes 9 6 
BCA Canopy and soil attributes x Land use 3.96 3.42 39.6 0.0001 
CIA Fauna x Canopy and soil attributes 7.5 4.8 13.5 0.44 
Table 5 
Soil macrofauna community structure (mean±SD) in four land uses of Alcântara, Eastern Amazon, in 2015–2016. 
Land uses 
Macrofauna indices Mature Forest Secondary Forest Slash-Mulch Slash-Burn F P 
Density (total ind.m− 2) 1113 ± 206aa 626 ± 597ab 690 ± 321ab 344 ± 197b 3.38 0.03 
Richness 19 ± 2a 14 ± 2b 15 ± 2b 10 ± 3c 17.27 0.0001 
Margalef 2.6 ± 0.2a 2.2 ± 0.3a 2.2 ± 0.2a 1.6 ± 0.5b 11.03 0.0001 
Shannon-Wiener 1.9 ± 0.2a 1.8 ± 0.4b 1.7 ± 0.2b 1.4 ± 0.3b 3.23 0.04 
Pielou 0.64 ± 0.06 0.67 ± 0.16 0.63 ± 0.08 0.62 ± 0.17 0.21 0.89 
a Lowercase letters indicate significant differences between land uses according to Tukey test (P < 0.05). 
G. Rousseau et al. 
Pedobiologia- Journal of Soil Ecology 95 (2022) 150840
9
Fig. 4. The Co-Inertia Analysis (CIA) on macrofauna 
composition and canopy more soil physical and 
chemical attributes in Alcântara, Maranhão, Brazil: a) 
correlation circle for macrofauna taxa; b) correlation 
circle for canopy plus physical and chemical attri-
butes; c) Factor map of land uses, the boxes placed at 
the centroid of land uses, and lines connect the plots to 
the centroids. The color indicates land uses in the 
macrofauna space and the greyscale indicates land 
uses in the canopy plus physical and chemical space. 
See Tables 1 and 2 for abbreviations. 
G. Rousseau et al. 
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4. Discussion 
4.1. The higher taxa approach 
The higher taxa approach is commonly used to assess land-use effects 
on soil invertebrates and related ecosystem functions (Rodriguez et al., 
2021), nonetheless, they are probably not a good proxy for in-
vertebrates’ species diversity. Indeed, Neeson et al. (2013) reported low 
performance of surrogate taxa when mean and variance of species 
number per higher taxa is high, which is the case for many invertebrates, 
including this study (Table 2). This confirmed a review by Lewandowski 
et al. (2010) that compared surrogate effectiveness where higher taxa of 
arthropods performed less than herpetofauna, plants, mammals, and 
birds. Despite these results, we found no references that focused spe-
cifically on soil macrofauna higher taxa as a surrogate for species di-
versity. We therefore based our interpretations on the well accepted 
sensitivity of soil macrofauna higher taxa to land-use change (Durán 
Bautista et al., 2018; Lavelle et al., 2016; Marichal et al., 2014; Rodri-
guez et al., 2021) and their known relationships with soil functions 
(Jouquet et al., 2014; Lavelle et al., 2016, 2020; Potapov et al., 2022; 
Rodriguez et al., 2021). Additionally, surveying higher taxa saves 
important resources and time with species identification and still pro-
vides valuable information for inference on biodiversity recovery 
(Mathieu et al., 2005; Yoshima et al., 2013; Cabrera-Dávila et al., 2017). 
Given the urgency to understand the potential of alternative farming 
systems to conserve biodiversity and ecosystem services, rapid survey 
assessments of biodiversity may be necessary to inform immediate 
conservation actions (Lewandowski et al., 2010). 
4.2. Soil macrofauna composition 
The fact that two taxa were present only in OF and Diplopoda and 
Isopoda had up to 6 times higher abundance in these fragments indicates 
they conserve habitats absent from the other land uses in the landscape. 
Diplopoda and Isopoda were proposed as indicators of ecosystem func-
tioning and restoration as they need leaf litter and promote its decom-
position and nutrient cycling (Snyder and Hendrix, 2008). Nakamura 
et al. (2003) found that the frequency of Diplopoda and Isopoda (along 
with Chilopoda, Amphipoda, and Formicidae) identified at this level, 
better-discriminated forest remnants from restoration sites (1–12 years) 
and pastures. Soil Auchenorrhyncha, represented mainly by large soil 
borers Cicadidae larvae, are mentioned in numerous studies (Pauli et al., 
2011, 2015) and are not rare in old-growth and secondary forests in 
Amazon (Rousseau et al., 2014). The singleton sampled in Alcântara 
old-growth forest suggests this group may be at risk locally. 
The soil macrofauna composition in the slash-and-mulch system is 
more similar to the secondary or old-growth forest than to the slash-and- 
burn system, despite a high variability within classes as indicated by the 
standard deviation in Table 2 or the cloud dispersion in factor maps 
(Figs. 3 and 4). Such variability is common for soil invertebrates and 
may limit their use as indicators (Rousseau et al., 2012) or surrogate 
taxa as discussed earlier (Neeson et al., 2013). Nonetheless, for most of 
the groups, SM had no effect or a positive effect compared to the other 
land-uses and particularly forests (Table 2). It seems that the thick mulch 
layer produced by the slash-and-mulch of the young forests can effi-
ciently buffer the effects of vegetation suppression. Mulch biomass was 
not estimated in this study, nonetheless, previous work in Alcântara 
estimated that early-succession forests (vegetation height <7 m and 
canopy opening 53%) stock between 5 and 17 Mg⋅Ha− 1 of aboveground 
biomass (Zelarayán et al., 2015) which represents, once mulched, a 
considerable improvement of habitat for litter-dwelling animals 
compared to the nearly bare soil of slash-and-burn (Fig. B.1). Indeed, 
typic litter dwellers like Blattaria, Embioptera, and Gastropoda had their 
highest abundance in SM, while Chilopoda, Araneae, Pseu-
doescorpiones, and Formicidae had their second-highest abundance in 
SM. In a Quesungual agroforestry system of Honduras, Pauli et al. 
(2011) also reported a similar macrofauna composition between the 
slash-and-mulch system and secondary forests in the short (2 years) and 
medium-term (10 years). This supports the potential to transfer the 
system in the region and the need to monitor the installed systems in the 
long term. 
4.3. Soil macrofauna density and diversity 
Despite represented by very small (2–10 Ha) and degraded frag-
ments, old-growth forests still present the highest diversity and abun-
dance for most macrofauna groups and therefore act as refuges for a 
significant fraction of this important soil biota. Indeed, old-growth forest 
fragments, even degraded, conserve a much more complex structure 
(Cardozo et al., 2022) and diversified necromass than young or inter-
mediate secondary forests (Zelarayán et al., 2015) and, therefore, pro-
vide more potential habitats for edaphic macrofauna. In a pioneer work 
in the same Pepital watershed as this study, Triana et al. (2015) reported 
the same trend in a gradient of riparian forest succession, with the 
higher diversity of soil macrofauna taxa in the late-successional stages 
(>15 years and >40 Years-old). A coarse level of identification may be 
suitable to monitor the evolution of soil quality and function in alter-
native farming systems like slash-and-mulch if we consider forest rem-
nants as the reference and the relatively low cost of these methods. 
Nonetheless, the literature available on soil fauna in forest fragments is 
still scarce, and degradation may paradoxically have a positive impact 
on soil macrofauna as conserved mature forests are known to present 
nutrients immobilization, in particular phosphorus, that limits de-
composers’ (saprophages, phycophages, omnivores) development and 
therefore affects all the food web (Doblas-Miranda et al., 2008). 
Degradation by selective logging or moderate fires may accelerate 
nutrient turnover and positively impact the food web (Azevedo-Ramos 
et al., 2006). As acknowledged by Costa et al. (2015), small forest 
fragments are more suitable to conserve small animals like invertebrates 
and less large fauna, and even an increase in species number was re-
ported for leaf-litter invertebrates, compared to the continuous forest 
(Didham, 1997). As conservation policies are based on better docu-
mented large fauna studies, small fragments are generally neglected 
unless they are crucial for small biota conservation (Ribas et al., 2005) 
and the essential ecosystem services they provide (Rodriguez et al., 
2021). Indeed, mature riparian secondary forests in the Pepital water-
shed were reported to host 63 ant species (Triana et al., 2019) when 
undisturbed old-growth forests in Paragominas (at the Maranhão-Pará 
State frontier) host about 65 species for the same number of samples (4 
transects)(Solar et al., 2016). Nonetheless, the conservation valueof 
forest fragments varies from one group to another and a conservative 
approach suggests a forest area of 500–1000 ha to conserve all the 
invertebrate fauna of a locality within the Amazon biome (Didham, 
1997). Therefore, the high potential of swidden agriculture landscape to 
conserve forest diversity (Padoch and Pinedo-Vasquez, 2010) is prob-
ably severely threatened in Eastern Amazon by the reduction of 
old-growth forest fragments and the associated reduction of the fallow 
period (Denich et al., 2005). This emphasizes the need for cropping 
systems that reduce the pressure on the forest while ensuring better 
productivity along with higher diversity. 
For the first time the SM system potential to conserve soil macro-
fauna diversity in the region is reported (Table 5). In Central America, 
where the slash-and-mulch Quesungual system is well developed, 
notably different results were presented: Rousseau et al. (2013) found no 
significant difference in macrofauna richness between Quesungual and 
secondary forests, silvopastoral or traditional slash-and-burn systems. 
Nonetheless, Quesungual had higher macrofauna abundance. Pauli et al. 
(2011) found no difference in diversity but in composition between 
Quesungual and other local land-uses. None of these studies had 
old-growth forests as a reference and slash-and-mulch differences with 
other land-uses were less marked than in this study. In the Amazon, the 
only study that compared slash-and-mulch with slash-and-burn system 
G. Rousseau et al. 
Pedobiologia - Journal of Soil Ecology 95 (2022) 150840
11
and secondary forests (Rousseau et al., 2010), reported results similar to 
this study with a higher richness of macrofauna higher taxa in 
slash-and-mulch and 40 years-old secondary forest. On the contrary, ant 
and earthworm genus richness showed different patterns: land-uses 
were not significantly different, except the 40 years-old secondary for-
est with much higher ant richness than any other land-use. Thus, 
different levels of identification show different and complementary re-
sponses to land-use effects. 
Older systems always had more total density and richness than 
younger ones, even in the case of SB (Table A.1; Fig. B.4). The reduction 
of the fallow period is the main issue in the crisis of shifting agriculture 
and the main cause of associated forest and soil degradation (Lawrence 
et al., 2010; Villa et al., 2020). In the Amazon, even if macrofauna re-
covers similar richness to mature forests after twenty years, a large gap 
exists, which does not allow to generalize these results (Serra et al., 
2021). As a consequence, we dońt know yet if 10 years of fallow is 
enough to recover soil macrofauna and associated soil functions in the 
SB context. This is reinforced by the fact that the age effect detected in 
the whole community is significant only for Isopoda when groups are 
tested individually (Table A.2). 
4.4. Canopy and soil attributes 
The slash-and-mulch land preparation promoted better soil chemical 
fertility according to agriculture needs with the highest pH and lower 
acidity, similar to the traditional slash-and-burn. These results are 
attributed to liming that is already recommended to enhance the 
chemical attributes of the hard setting soils of the region (Moura et al., 
2009). As acknowledged by these authors, the combination of liming (as 
a source of Ca) and high biomass mulch cover are practices proved to be 
able to substitute the use of fire and restore the fertility of the region 
fragile soils (Moura et al., 2015, 2016). Contrary to Moura et al., soil 
physical attributes were not affected by land-uses and there was espe-
cially no difference between fire and no-fire farming systems. This can 
be attributed to the fact that our system is at the implementation phase 
while the previous studies reported results of at least 10 years-old ex-
periments with mulching. Nonetheless, it is important to monitor soil 
physical attributes as they are more critical than chemical ones to 
restore the fertility of the local soils (Moura et al., 2009). Indeed, soil 
chemistry can be relatively easily corrected with lime or fertilization at 
reasonable costs while the texture, characterized by very low clay and 
high fine sand content, cannot. Farmers rely mainly on rich and abun-
dant soil macrofauna to maintain an ephemeral structure in constant 
renovation (Moura et al., 2015). In terms of soil chemical fertility, the 
two agricultural systems provide the adequate bases and pH sought for 
the production of local staple crops, either by biomass burning or liming, 
while the forests conserve the natural attributes of local soil, low pH and 
base availability. As a consequence, forests are probably not the 
adequate land-use reference for soil chemical attributes if agriculture 
productivity is the focus (Rousseau et al., 2012). These positive results 
on soil chemical fertility, are probably more susceptible to advocate for 
the slash-and-mulch system with the farmers than the less known soil 
fauna but, this need to be investigated as farmer ecological knowledge 
influences the adoption of new practices or systems (Pauli et al., 2012; 
Celentano et al., 2014). 
4.5. Macrofauna composition, canopy and soil attributes 
According to the Co-Inertia analysis, all land-uses but SB are sepa-
rated in the two spaces (mainly along CIA1) which reflects the low 
correlation between macrofauna and soil attributes. In particular, SM 
and SF have a very similar position on both axis in macrofauna space 
(close to origin) but, in soil attributes space they strongly separate along 
the “acidity-saturation” gradient with SF on the “forests side” and SM on 
the “agriculture side” (Fig. 5). This is probably related to the short time 
elapsed between land preparation and macrofauna sampling. 
Nonetheless, measuring direct relationships between soil attributes and 
macrofauna is not straightforward as most of them are indirect (Moço 
et al., 2010) and, when direct relationships are identified, correlation 
coefficients are low (Rousseau et al., 2013; Durán Bautista et al., 2018). 
Co-inertia summarizes what we were expecting from the 
slash-and-mulch system: conserve the macrofauna community from the 
secondary forest and provide the bases necessary for crop production. It 
remains to monitor if the macrofauna community persists stable and can 
sustain its functions in the soil, in particular, structure maintenance 
(Moura et al., 2015; Rodriguez et al., 2021). 
From the functional groups’ perspective, the slash-and-mulch system 
is also much more favorable than the slash-and-burn. Ants have 3.5 
times higher density in SM than SB and earthworms 2.6, densities not 
different from forests (Table 2). It indicated a positive prognostic for soil 
structure maintenance, even if no effect was detected yet (Moura et al., 
2015; Jouquet et al., 2014; Lavelle et al., 2020). Three taxa associated 
with litter had their highest densities in SM (up to 23 times SB density; 
Table 2), likely a response to the massive fresh litter entry. Embioptera 
are classified as phycophages (feed on algae, lichens and detritus), 
Gastropoda as omnivores (mainly microbivores but also herbivores, 
carnivores and detritivores) and Blattodea as saprophages and therefore 
act as detritivores and decomposers (Potapov et al., 2022). The 
Embioptera are rarely mentioned in the soil macrofauna literature even 
if they are widely distributed and often associated with litter (Potapov 
et al., 2022). Nonetheless, a high proportion of detritivores to 
non-decomposers was considered a good soil quality indicator by Cab-
rera-Dávila et al. (2017) while, Blattodea and Gastropoda are commonly 
associated with litter quantity, quality (Mouraet al., 2015), and forest 
ecosystems (Marichal et al., 2014; Rousseau et al., 2014; Suárez et al., 
2018). The predators were also significant contributors to the between 
land-uses variation, particularly abundant in the old-growth forest 
fragments but also secondary forest and slash-and-mulch. Two out of 
seven groups that significantly differentiated slash-and-burn from 
slash-and-mulch were predators (Table 2). They are reliable indicators 
of the macrofauna community functionality in these systems as their 
abundance is naturally correlated to their prey abundance and proper 
energy flow (Chen and Wise, 1999; Hunt and Wall, 2002). Predators are 
associated with forest and old succession sites (Mathieu et al., 2005; 
Vasconcellos et al., 2013; Marichal et al., 2014; Suárez et al., 2018), 
more complex trophic structures (Amazonas et al., 2018), and 
mentioned in about half of the studies on soil macrofauna and land-use 
in the tropics but, their potential as soil quality indicators is rarely dis-
cussed (Moço et al., 2010; Rousseau et al., 2012, 2014; Triana et al., 
2015). Additionally, they are not included in the current approaches of 
soil health assessment (Rinot et al., 2019). We suggest that the potential 
of predators, even higher taxa, as soil quality indicator is 
underexploited. 
Land preparation without fire provides similar (or better) soil 
fertility conditions to slash-and-burn given proper liming and fertiliza-
tion are applied. Additionally, the slash-and-mulch fields had a very 
similar macrofauna community to secondary forest suggesting, for the 
first time in this region, that this system better conciliate food produc-
tion and soil macrofauna diversity conservation than the slash-and-burn 
system. In particular, functional groups like ecosystem engineers or 
predators were raised with slash-and-mulch and were efficient in-
dicators of land-use change. Despite its scarcity in the landscape and 
their very high fragmentation, old-growth forest small remnants do 
conserve a more diverse and abundant soil invertebrates’ community. 
This study is the first to report that the integration of the slash-and- 
mulch system in this swidden agriculture landscape has the potential 
to enhance its resilience. Nonetheless, soil quality needs to be monitored 
to confirm the effective restoration of soil full functionality and agri-
culture productivity. 
G. Rousseau et al. 
Pedobiologia - Journal of Soil Ecology 95 (2022) 150840
12
Declaration of Competing Interest 
The authors declare that they have no known competing financial 
interests or personal relationships that could have appeared to influence 
the work reported in this paper. 
Acknowledgements 
We thank the Alcântara communities for their collaboration with 
plots establishment, management and sampling. We thank the 
Maranhão State Foundation for Research Development (FAPEMA) 
(grant 05114/17), the Brazilian Council for Higher Education (CAPES) 
(grant 3281/2013), the Brazil National Research Counsil – CNPq (grant 
402707/2017-6) and UEMA (Productivity grant) for the financial 
support. 
Appendix A. Supporting information 
Supplementary data associated with this article can be found in the 
online version at doi:10.1016/j.pedobi.2022.150840. 
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