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Soil recovery of alluvial gold mine spoils in the Peruvian Amazon using
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DOI: 10.1002/ldr.4118

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Received: 25 April 2021 Revised: 17 September 2021 Accepted: 1 October 2021
DOI: 10.1002/ldr.4118

REVIEW ARTICLE

Soil recovery of alluvial gold mine spoils in the Peruvian

Amazon using Stylosanthes guianensis, a promising cover crop

Manuel Gabriel Velásquez Ramírez1 | Dennis del Castillo Torres2 |

3 2
Juan Antonio Guerrero Barrantes | Joel Vásquez Bardales | Evert Thomas4 |
Edgar Cusi Auca1 | Midori Chinen Gushiken1 | Betzy Muñoz Diaz1 |
Ricardo Russo5 | Ronald Corvera Gomringer1

1
Instituto de Investigaciones de la Amazonía
Peruana (IIAP), Puerto Maldonado, Peru Abstract
2
Instituto de Investigaciones de la Amazonía The Amazon is an important reservoir of biodiversity and carbon but it is under pres-
Peruana (IIAP), Iquitos, Peru
sure by multiple threats such as artisanal and small-scale gold mining (ASGM). In Peru
3
Universidad Nacional Agraria La Molina
(UNALM), Lima, Peru ASGM has degraded 90,000 ha of old-growth forest since the eighties, leaving vast
4
Bioversity International, Lima, Peru areas as wastelands. As most ASGM in the region is illegal, efforts to recover
5
Universidad La Salle (ULASALLE), San José, degraded areas have been scant. Here we assessed the potential of Stylosanthes
Costa Rica
guianensis to recover soil health as a first step in the restoration of gold mine spoils in
Correspondence a Native community and a mining concession in Madre de Dios, Peru. We evaluated
Manuel Gabriel Velásquez Ramírez, Instituto
de Investigaciones de la Amazonía Peruana
plant growth and analyzed changes in physical, chemical, and biological soil parame-
(IIAP), Jr. Ica N
1162, Apartado postal 17001, ters. After 470 days from sowing, the average plant height was 46.7 cm with a sur-
Puerto Maldonado, Peru.
Email: mvelasquez@iiap.gob.pe
vival rate >50% and yields of 23.9 t ha1 and 450 kg ha1 of dry biomass and
nitrogen, respectively. Multiple soil parameters increased significantly, including cat-
Funding information
Consejo Nacional de Ciencia, Tecnología e
ionic exchange capacity (3.3 to 4.0 cmol [+] kg1), soil organic matter (0.03% to

n Tecnolo
Innovacio
gica (CONCYTEC); 0.39%), soil respiration (0.02 to 0.06 mg CO2 g1 d1) and biomass (0.03 to
PROCIENCIA
0.15 mg C g1). Soil macrofauna increased from 2 to 11 taxonomic groups, including
ants, considered as soil engineers. Furthermore, S. guianensis increased soil carbon
sequestration of impacted areas from 0.004 t C ha1 by more than 1650%, up to
0.07 t C ha1. These promising findings clearly illustrate S. guianensis potential to
kick-start natural succession of Amazonian forests after degradation by ASGM and
hence help to achieve the Sustainable Development Goals.

KEYWORDS
Amazon, degradation, forest, gold mining, restoration

1 | I N T RO DU CT I O N Monitoring Institute of the Andean Amazon Project (MAAP), by 2018

The Amazon is a reservoir of biodiversity and carbon storage of global
importance (Gosling & Holden, 2011; Myers et al., 2000; Olson
et al., 2001; Poorter et al., 2015), but it is increasingly threatened by
deforestation and Carbon (C) loss due to illegal logging, slash-and-
burn agriculture, and artisanal and small scale gold mining (ASGM),
among other activities (Finer & Mamani, 2017). According to the
the loss of forest cover reached almost 1 million ha in Western Ama-
zonia (Ecuador, Bolivia, Peru, Colombia, and Brazil), of which more
than 200,000 ha corresponded to Peru (Finer & Mamani, 2019).
ASGM is an increasingly important driver of deforestation. A
recent analysis reported that in Latin America went from
52,974 mining areas in 2012 to 58,432 in 2020, representing an
increase of 10%. In territorial terms, this period saw a reduction of

Land Degrad Dev. 2021;1–11. wileyonlinelibrary.com/journal/ldr © 2021 John Wiley & Sons, Ltd. 1
2

306,250 km² of Amazonia occupied by mining activity, from
1,628,850 in 2012 to 1,322,600 km² in 2020. (De Almeida, 2019).
ASGM involves logging and burning forest, excavation, removal and
washing of sediments, amalgamation of mercury with gold followed
by burning to isolate the gold with concomitant volatilization of mer-
cury in the environment (Salinas, 2007; Velásquez Ramírez
et al., 2021). Consequently, it brings about: (i) health risks due to
exposure to contaminants (mercury, solid waste, fuels, and lubricants),
(ii) loss of soil organic matter; (iii) increased water and wind erosion,
(iv) leaching of sediments to lower areas and water bodies, (v) soil
compaction due to the transit of machinery and (vi) loss of ecological


connectivity (Alvarez et al., 2011; Esdaile & Chalker, 2018; Mosquera
et al., 2009).
The Madre de Dios region in the Peruvian Amazon is designated
as the national ‘Capital of Biodiversity’. It is part of the Tropical Andes
Biodiversity Hotspot (Myers et al., 2000) and its vegetation cover
stores more than 6.9 billion tons of C (Asner et al., 2014). However,
ASGM in Madre de Dios has already resulted in the deforestation and
severe degradation of 95,750 ha of old-growth forests (Caballero
Espejo et al., 2018), at an average rate of 6000 ha per year (Asner
et al., 2013). Gold mine spoils are dominated by sandy soils, inter-
spersed with mounds of stones and pebbles, characterized by very
low fertility and potential mercury pollution (Román-Dañobeytia
et al., 2020; Velásquez Ramírez et al., 2020).
To recover degraded areas and achieve land degradation neutral-
ity by 2030 (UNCCD, 2019), it is urgent to implement integrated solu-
tions based on a socio-economical-ecological systems analysis, using
concepts such as nature-based solutions and connectivity (Keesstra
et al., 2018). In these processes, healthy soils and healthy land are
essential to achieving many of the societal goals in the framework of
the Sustainable Development Goals (SDGs) (Keesstra et al., 2016;
Keesstra et al., 2018).
The use of cover crops is ideal to improve soil health. They
increase soil fertility, structure, water retention, groundwater recov-
ery, pest control, soil productivity and environmental quality, and help
reducing soil erosion and nutrient loss (Adetunji et al., 2020; Bren-
nan & Acosta-Martinez, 2019; Fageria et al., 2005). Moreover, its
usage as green manure increases microbial carbon biomass and soil
respiration (Tejada et al., 2008a, 2008b). The selection of suitable spe-
cies is a critical step to achieve the recovery of mine spoils (Citadini-
Zanette et al., 2018; Román-Dañobeytia et al., 2020), by
reestablishing ecological cycles, facilitating natural succession while at
the same time increasing the capacity of the soil to sustain a new for-
est and capture C (Sabine et al., 2004). Particularly pioneer species in
the legume family (Fabaceae) are of interest for their ability to fix
nitrogen from N2 to NH3, thus increasing soil fertility and lowering
fertilizer costs (García et al., 2002; Thomas, 2014).
Stylosanthes guianensis is a native Latin American tropical legume.
It is an erect, short-lived perennial shrub that shows optimal produc-
tion levels at low altitudes (< 850 msnm), high levels of sand (18–
56%), low soil organic matter (<3.4%), and low pH (<5.0) (Amezquita
et al., 1991). Based on initial tests in 32 areas across Latin American
(International Tropical Pastures Evaluation Network 1 in 1984), It is
VELASQUEZ RAMÍREZ ET AL.
considered a suitable plant for use in tropical savannas and the humid
tropics (Amezquita et al., 1991; CIAT, 1984). Here we hypothesized
that the use of S. guianensis as a cover crop can help to significantly
recover soils health and kickstart the restoration of ASGM mine spoils
in Madre de Dios. We particularly focused on S. guianensis adaptation,
the contribution of biomass accumulation, ability to improve soil fertil-
ity and potential carbon sequestration.
2 | M A T E R I A L S A N D M ET H O D S
2.1 | Assessment area description
We carried out research in an area degraded by ASGM, located in the
Native Community of San Jacinto and the mining concession of the
Mining Association “Los Rebeldes de Madre de Dios”, in the Peruvian
Amazon of Madre de Dios (Figure 1). The study area is located on a
low terrace of recent quaternary alluvial deposits, with slopes <2%
and climax vegetation of subtropical humid forest. An assessment of
the area prior to the start of the experiment, found that the concen-
tration of mercury in the soil was 0.04 ± 0.05 mg kg1 DM
(Becerra, 2019), which is below the Peruvian Soil Quality Standard
(MINAM, 2017) and Soil Canadian Environmental Quality Guidelines
(CCME, 2007) of 6.6 mg kg1 DM.
2.2 | Experimental design and data collection
We established Stylosanthes guianensis (Aubl.) Sw. cv 'Pucallpa' (CIAT
184) in three plots on land previously degraded by alluvial ASGM.
Before planting the experimental areas had been abandoned for 1.5 yr
and was devoid of vegetation. Each plot was sown manually on
15 January 2018 along rows spaced by 25 cm over a total area of
3540 m2 (1080 m2 - plot 1, 840 m2 - plot 2 and 1620 m2 - plot 3).
The plots were adjusted to the erratic form of mine spoils.
The survival, height, and plant cover of S. guianensis were evalu-
ated throughout the experiment up to 470 days after sowing (DAS).
We measured plant cover every 15 days in three small subplots of
4 m2 per plot, and took pictures for analysis with the software, CobCal
v. 1.0.
The ability of S. guianensis to improve soil conditions of recently
abandoned mine spoils was assessed over a period of 470 DAS
(2018–2019). The physical and chemical characteristics of the soil
were evaluated from three composite samples per plot at the begin-
ning and the end of the experiment (470 DAS), through the following
variables: pH (1: 1 ratio), electrical conductivity (EC), soil organic mat-
ter (SOM) (Walkley and Black method), nitrogen (N) (Kjeldahl method),
available phosphorus (P) (Bray II method), available potassium (K), tex-
ture (Bouyucos method), cation exchange capacity (CEC) (saturation
with ammonium acetate at pH 7 method) and gravimetric humidity.
We measured also the biological characteristics of the soil using
the same composite samples per each plot at the beginning and the
end of the experiment (470 DAS). More specifically, we assessed soil


VELASQUEZ RAMÍREZ ET AL.
F I G U R E 1 Study area located at mining spoils characterized by minimally mechanized mining technology in the Peruvian Amazon region of
Madre de Dios [Colour figure can be viewed at wileyonlinelibrary.com]
respiration (capture in alkali method), microbial biomass (fumigation
with chloroform method), bacteria, fungi, and actinomycetes colony
forming units (CFU) (sequential series of dilutions method), free-living
nitrifying bacteria, and nitrifying bacteria (culture and most probable
number method). In addition, we sampled soil macrofauna in three
subplots of 25 cm2  10 cm separated from each other by 7 m at the
beginning and the end of the research, collecting arthropods based on
the TSBF (Tropical Soil Biology and Fertility) method (Anderson &
Ingram, 1993), using a metal rear frame. We collected arthropod and
soil samples in: (i) the litter layer, (ii) at 0–10 cm, and (iii) 10–20 cm soil
depths. We conserved all macrofauna present in small containers with
96% alcohol for later taxonomic classification in the lab.
At the end of the experiment, we measured the potential carbon
sequestration of S. guianensis according to Global Soil Partnership
(GSP) Secretariat and the Intergovernmental Technical Panel on Soils
(ITPS) (GSP, 2016), formula 1:
SOC stock ¼ d  BD  ðCtot – Cmin Þ  CFst  0:58 ð1Þ
Where, SOC = soil organic carbon stock (kg m2).
1
Ctot and Cmin = total and mineral (or inorganic) carbon content (g g ).
d = depth of horizon/depth class (m).
3
BD = bulk density (kg m ).
CFst = correction factor for stoniness (1 - % stones) 1001).
We consider 0% stoniness. 0.58 = Assuming 58% SOC in SOM (Van
Bemmelen, 1980).
3
For reference purposes, we also collected soil samples in non-
impacted old-growth forest at the beginning of the experiment. Sam-
ples were located 3 km from the mine spoils and characterized
according to the same parameters described above.
2.3 | Statistical analysis
Data were analyzed using Kruskal Wallis with Wilcoxon as post hoc
test, considering a significance threshold of 0.05. Residual normality
and homogeneity of variance were evaluated with the Shapiro–Wilk
and Bartlett tests, respectively. Statistical analysis was performed in R
statistical program v 3.2.2 (R Core Team, 2017).
3 | RE SU LT S
At 470 DAS the average height of S. guianensis plants was 46.7 cm
with a survival rate of 45.9%. Close to full soil coverage was reached
at 290 DAS (Table 1). Average humid biomass at 470 DAS was
77.1 t ha1, corresponding with 3.0, 60.8, and 13.2 t ha1 for roots,
stems, and leaves, respectively. Average dry biomass was 23.3 t ha1,
corresponding with 1.2, 19.4 and 3.1 t ha1 for roots, stems, and
leaves, respectively (Figure 2). The contribution of nitrogen to the soil
was 23.2, 376.9, and 63.3 kg ha1 for the roots, stems, and leaves,
respectively (Figure 3).
4

VELASQUEZ RAMÍREZ ET AL.

TABLE 1 Biometry of S. guianensis at 470 DAS

S. guianensis Samples (n) Mean ± standard deviation Coefficient of variance

Height (cm) 64 plants/plot 46.7 ± 5.7 0.1
Cover of plant (%) 9 plots 92.6 ± 6.0a 0.1
Survival (%) 9 plots 45.9 ± 14.1 0.3
Humid biomass (kg ha1) Root 3 plots 3,088.2 ± 728.6 0.1
Stem 3 plots 60,846.0 ± 22,043.5 0.4
Leaf 3 plots 13,200.6 ± 7,627.9 0.6
Total 3 plots 77,125.0 ± 25,370.3 0.3
Dry biomass (kg ha1) Root 3 plots 1,262.1 ± 185.6 0.1
Stem 3 plots 19,470.7 ± 7,053.9 0.4
Leaf 3 plots 3,168.2 ± 1,830.7 0.6
Total 3 plots 23,901.0 ± 3,012.9 0.3
Nitrogen (%) Root 3 plots 1.7 ± 0.4 0.2
Stem 3 plots 1.8 ± 0.2 0.3
Leaf 3 plots 2.0 ± 0.1 0.1
Nitrogen (kg ha1) Root 3 plots 23.2 ± 5.3 0.2
Stem 3 plots 376.9 ± 143.1 0.3
Leaf 3 plots 63.3 ± 36.6 0.6
a
We got almost 100% of cover of plant at 290 DAS

F I G U R E 2 Biomass of
S. guianensis (kg ha1) at 470 DAS
[Colour figure can be viewed at
wileyonlinelibrary.com]

low cation exchange capacity (3.3 cmol [+] kg1). In contrast, at

F I G U R E 3 Nitrogen in plant organs S. guianensis (kg ha1) at
470 DAS [Colour figure can be viewed at wileyonlinelibrary.com]
Before the establishment of S. guianensis, soils at the experimen-
tal plots presented low fertility with moderate to slightly acidic pH
(5.4), low SOM (0.03%), low P (4.4 ppm), low K (37.0 ppm), and very
470 DAS S. guianensis soils showed significant increases in SOM
(0.39%) and CEC [4.0 cmol (+) kg1] as well as a decrease in pH (4.8);
K and P content tended to increase, although not significantly. The
soil of reference forest (without human intervention) presented a
strongly acid pH (4.5), with higher content of SOM (3.1%) and P
(8.6 ppm), low K (105.2 ppm), and medium CEC [13.1 cmol (+) kg1].
The biological fertility of the soil in the experimental plots
increased considerably at 470 DAS (Table 2). There was significantly
higher gravimetric humidity in the soil (13.56%) than the impacted soil
before planting (8.27%). Also, bacterial (from 1.36  106 CFU g1 of
dry soil to 2.72  107 CFU g1 dry soil), and fungal (from 1.13  104
CFU g1 of dry soil to 4.22  105 CFU g1 dry soil) biomass
increased substantially in the plots after planting S guianensis. By con-
trast, we did not detect any significant changes in Actinomycetes,
free-living nitrogen-fixing bacteria, and nitrifying bacteria, although
there was a tendency for these to increase. Furthermore,


VELASQUEZ RAMÍREZ ET AL. 5

microorganism respiration and biomass significantly increased by

a 5.55  104 ± 2.50  104

a 1.00  105 ± 1.30  105

300% and 500%, respectively. Soil characterization showed that

(organisms g1 dry soil)

S. guianensis influences the path of improvement of biological soil

Nitrifying bacteria
fertility.
Prior to the establishment of S. guianensis, the impacted soil pres-
ented only 11 individuals of arthropods m2 pertaining to 2 taxonomic

0.05
No
groups (Table 3). By contrast, at 470DAS we found 887 individuals of
arthropods m2 pertaining to 11 taxonomic groups. The vertical distri-
a 2.53  103 ± 1.29  103

a 1.00  104 ± 1.30  104

Free living nitrogen fixing

bution of arthropods in the litter layer and at 0–10 cm and 10–20 cm

bacteria (organisms g1

soil depths prior to planting S. guianensis was 0%, 67%, and 33% and
470 DAS 16%, 82%, and 2%, respectively (Table 4).
According to formula 1 the potential carbon sequestration of the
dry soil)

impacted soil before planting S. guianensis, at 470 DAS, and in refer-

0.05 ence forest were 0.004, 0.07, and 0.43 t C ha1, respectively
No

(Table 5).
b 0.03 ± 0.01

a 0.15 ± 0.09
Biomass (mg

dry soil)
C g 1

0.03

4 | DI SCU SSION
Yes
b 0.02 ± 0.01

a 0.06 ± 0.02
(mg CO2 g1

4.1 | Biomass yield

dry soil d1)
Respiration

0.03
Microbiological characteristics of the soils before and after the establishment of S. guianensis at 470 DAS

The average height of S. guianensis observed in the present study was

Yes

within the range reported by other studies (Amezquita et al., 1991;

b 1.13  104 ± 2.50  103

a 4.22  105 ± 1.85  105

Fungi (UFC g1 of dry soil)

Caruzo et al., 2004) (Table 6). In spite of the initial degraded soil con-
ditions, we obtained 100% coverage as of 290 DAS, which was faster
than the 63% after 360 DAS reported by Caruzo et al. (2004), but
slower than observed in the study of Amezquita et al. (1991) who
reported 100% coverage in 150 DAS. The contribution to dry matter
formation in the present study (Table 1 and Figure 2) was comparable
0.01
Yes

to yields reported by Amezquita et al. (1991) and Caruzo et al. (2004).

b 2.38  105 ± 1.44  105

b 1.76  105 ± 8.57  104

By contrast Ciotti et al. (2003) obtained much higher yields

Actinomycetes (UFC g1

(7220 kg ha1) after the use of P fertilization, thus indicating the

importance of P fertilization for the increase of biomass to boost the
recovery of degraded areas, especially in soils that have low
of dry soil)

available P, such in our case (Table 7). When S. guianensis grows in

unfertile soils P concentrations in tissue are 0.06%, but when fertilized
0.05
No

this can increase to more than 0.30% of the dry matter (T'Mannetje &
Jones, 1992). Nitrogen fixation from the atmosphere also depends on
b 1.36  106 ± 1.90  106

a 2.72  107 ± 1.60  107

the availability of P in the soil (Kennedy & Cocking, 1997). Long

Bacteria (UFC g1 of

et al. (2017) showed that S. guianensis consumed P from the soil

together with nitrogen from atmospheric fixation during growth,
reducing the total and available P in the soil (Table 8). The roots of
dry soil)

S. guianensis are highly efficient in obtaining soil P (Probert, 1984),

0.01
Yes

although the underlying mechanisms remain unclear.

While we obtained similar levels of S. guianensis dry biomass as
b 8.28 ± 2.97

a 13.56 ± 3.07
humidity (%)
Gravimetric

those reported by previous studies, the N yield was considerably

lower (440.29 kg ha1 N) in the present study compared to the
0.03
Yes

837 kg ha1 N reported by Phengsavanh and Frankow-

Lindberg (2013). This might indicate N yield limitation of S. guianensis
experiment)

Differences (p
Impacted soil

in the infertile soils of ASGM areas (Table 1 and Table 6), at least dur-
S. guianensis

470DAS
plots at
TABLE 2

value)

ing the initial phase of the soil recovery process.

(start
Area

In sum, our findings suggest that the planting of S. guianensis is an

excellent way to quickly increase aerial and soil biomass in alluvial
6

VELASQUEZ RAMÍREZ ET AL.

TABLE 3 Population density (individual m2) of the most representative taxonomic groups based on the type of vegetation

Type of vegetation

Brachiaria Leucaena
Impacted soil (start Impacted area S. Arachis pintoi brizantha leucocephala Solanum rugosum
Soil
experiment in this guianensis (this (Velásquez (Velásquez (Velásquez (Velásquez
macrofauna
research) research) et al., 2012) et al., 2012) et al., 2012) et al., 2012)
taxonomic
groups Population density (individual m2)
Isoptera 0 0 1,194 3605 978 120
Formicidae 9 683 990 24 28 24
Oligochetos 0 0 253 116 217 270
Coleoptera 0 124 37 37 14 53
(adult)
Coleoptera 0 37 5 11 5 21
(larva)
Thysanoptera 2 0 0 0 0 0

T A B L E 4 Vertical distribution (%) of soil macrofauna in plots the start of the experiments. From this perspective of SOM dynamics,
planted with S. guianensis the diversity of soil organisms is very important, as both macro fauna

Impacted soil Impacted area like beetles and earthworms and microbiota like fungi and bacteria,
Sol (start experiment S. guianensis can increase the stabilization of SOM as well as speed up its decom-
depth (cm) in this research) (this research) position (Jackson et al., 2017).
Litter 0 16 While cover crops in dry and semiarid climate can decrease the
0–10 67 82 soil water content in the first soil layers due to the increase of transpi-
10–20 33 2 ration, they can at the same time improve water storage due to
increased soil permeability and porosity and reduced soil and water
losses (Celano et al., 2011; Novara et al., 2021). In contrast, under our
gold mine spoils. According to García et al. (2002) a good green tropical conditions we found higher gravimetric humidity in oils
manure is characterized by providing a dry matter content of 10 to planted with S. guianensis (13.56%) than the bare impacted soil before
15%, which in our case was 30.9% (Table 1 and Figure 2). The greater planting (8.27%).
the flow of organic matter in the soil, the greater the degree of aggre- Yu et al. (2016) demonstrated that legume species with coarse
gation and the better the performance of functions that depend on it, root axes created substantially more macropores compared to fine-
such as aeration, drainage, and rooting (Mielniczuck et al., 2003). rooted species, thus enhancing soil hydraulic conductivity and effec-
tively reducing surface runoff. Furthermore, plant stems reduce the
runoff velocity and this results in an increase in infiltration due to the
4.2 | Improving chemical and physical soil fertility pond pressure (Novara et al., 2021; Pan & Shangguan, 2006).

Our results reconfirm the infertile soil conditions created by ASGM

operations in Madre de Dios. Mine spoils are characterized by surficial
sandy soils due to the transport of old sediment from the bottom to
the top (Esdaile & Chalker, 2018), lower capacity to adsorb and pro-
vide nutrient to plants (Table 1 and Table 7), and higher pH caused by
lower SOM compared to reference forest. S. guianensis promoted soil
recovery at 470 DAS by increasing SOM by 1200% and CEC by 23%,
accompanied by a slightly soil acidification. Changes in P and K levels
tended to increase but not in a significant manner.
Long et al. (2017) who grew S. guianensis in a sandy loam soil in a
dry and hot Asian valley (Table 8), did report substantial increases in
available P (up to 52%), and available K (up to 31%) at 420 DAS. On
the other hand, Long et al. (2017) reported increases of SOM (150%)
far lower than those we observed. Possibly this is related to differ-
ences in the soil characteristics and initial degradation state prior to
4.3 | Improving biological soil fertility
We found larger bacteria and fungi populations, as well as higher bio-
mass and respiration rates at 470 DAS of S. guianensis which is a good
soil quality indicator. Free-living nitrogen-fixing bacteria and nitrifying
bacteria tended to increase at 470 DAS but not in a significant man-
ner (Table 2). This may be because the duration of the experiment
was too short to detect significant changes. Adequate nodulation in
the rhizosphere is conditional on favorable edaphic conditions, such
as sufficient concentrations of calcium (more required by the roots
than the shoots of the host plant) and a not too acidic pH (above 5 to
5.5). Furthermore, an increase in soil P can have a positive effect on
nodulation in Stylosanthes (Lopes et al., 2011). Da Silva Chaves et al.
(2016), isolated nodular bacteria in plants of the Stylosanthes genus


VELASQUEZ RAMÍREZ ET AL. 7

TABLE 5 Carbon sequestration in soils from reference forest, impacted areas and S. guianensi

Bulk density SOM (%) Correction factor Van Bemmelen SOC stock
Area (t m3) BD Ctot – Cmin for stoniness CFst factor (t ha2)
Impacted soil (start experiment) ab 1.40 ± 0.16 c 0.03 ± 0.0 0.01 0.58 c 0.004 ± 0.002
S. guianensis plots at 470 DAS a 1.60 ± 0.10 b 0.39 ± 0.1 0.01 0.58 b 0.07 ± 0.01
Reference forest b 1.19 ± 0.05 a 3.1 ± 0.9 0.01 0.58 a 0.43 ± 0.11
Kruskal wallis differences (p value) Yes Yes - - Yes
0.04 0.02 0.02

TABLE 6 Comparison of the biometry of S. guianensis observed in the present study in comparison with findings from other publications

This research biometric at Amezquita et al. (1991) Caruzo et al. (2004) Ciotti et al. (2003)
470 DAS biometric at 360 DAS biometric at 150 DAS biometric at 180 DAS

S. guianensis parameter Measurement CV Measurement CV Measurement CV Measurement CV

Height (cm) 46.70 ± 5.70 0.1 39.5 ± 17.1 0.4 68.0 0.2 - -
Coverage (%) 99.6 ± 6.0 (290 DAS) 0.1 63.0 ± 31.6 0.5 100.0 0.1 - -
Survival (%) 49.6 ± 12.6 0.2 - - 40.0 0.4 74.0c -
45.0d
Total dry mass (kg ha1) 23.901.0 ± 3.012.9 0.3 4,376.0 ± 2,347.0a 0.5 4,032.0 0.2 4,000.0c -
4,070.0 ± 3,825.8b 0.9 7,220.0d
a
Yield at maximum rainfall (kg ha112 weeks1)
b
Yield with minimal rainfall (kg ha112 weeks1)
c
Treatment without fertilization with PP
d
Treatment with PP fertilization at 11 kg ha1

TABLE 7 Characteristics and physical and chemical properties of the soil samples before and after the establishment of S. guianensis at
470 DAS

Bulk density CEC (cmol

Area (g cm3) Sand (%) Silt (%) Clay (%) Texture [+] kg1) K (ppm) SOM (%) P (ppm) pH

Impacted soil (start ab 1.40 ± 0.16 a 93.6 ± 2.3 b 3.3 ± 2.3 b 4.0 ± 0.0 Sand c 3.3 ± 0.2 b 37.0 ± 8.5 c 0.03 ± 0.0 b 4.4 ± 0.2 a 5.4 ± 0.2
of experimen)

S. guianensis. plots a 1.60 ± 0.10 a 93.6 ± 2.3 b 2.6 ± 3.7 b 3.6 ± 0.6 Sand b 4.0 ± 0.3 b 53.3 b 0.39 ± 0.1 b 4.5 ± 1.1 b 4.8 ± 0.2
at 470 DAS ± 14.5

Reference forest b 1.19 ± 0.05 b 13.9 ± 0.0 a 57.8 a 27.9 Silty a 13.1 a 105.15 a 3.1 ± 0.9 a 8.6 ± 2.5 c 4.5 ± 0.2
± 4.0 ± 4.0 loam ± 1.6 ± 0.8

Kruskal wallis Yes Yes Yes Yes - Yes Yes Yes Yes No
differences (p 0.04 0.01 0.01 0.02 0.01 0.01 0.02 0.04 0.05
value)

growing in clayey and sandy latosols with 5.4–6.8 pH and 22.84–
4.42 ppm P, indicating that Stylosanthes should be able to develop
nodules under the conditions at our experimental sites (Table 7).
Hence, the appearance of significant increases nitrifying bacteria
populations might be a matter of time.
S. guianensis positively influenced arthropod populations
(increases up to 7983% at 470 DAS) and distributions across the soil
profile. Similar soil recovery effects were reported by Tapia-Coral,
Pashanasi (2006) and García-Villacorta et al. (2006) for white sand pri-
mary forests and by Villalobos et al. (2000) for maize crop fields. In
2
addition, the arthropod density we found (887 m population den-
sity) is higher than reported by Villalobos et al. (2000) in a Zea maiz
crop (246 m2 population density) (Table 9). We particularly found a
higher population density of Formicidae in our plots at 470 DAS
(683 individuals m2) than reported for Brachiaria brizantha, Leucaena
leucocephala, and Solanum rugosum but it was slightly lower than
reported for Arachis pintoi (Velásquez et al., 2012) (Table 3).
Formicidae play a key role in recovering soil structure due to their role
as one of the most important soil engineers. Overall, these findings
suggest that even in intensive degraded soils S. guianensis effectively
promotes the recolonization and establishment of a variety of soil
arthropods, possibly through plant productivity and the accumulation
of soil organic matter which is generally positively correlated to
arthropod abundance and diversity (Flores-Rios et al., 2020). In turn,
soil macrofauna are a good indicator of soil development because
these organisms decompose organic matter, release nutrients,
8

VELASQUEZ RAMÍREZ ET AL.

TABLE 8 Characteristics and physical and chemical properties of the soil samples before and after the establishment of cover crops

This research characteristics of the

soil before and after the 470 DAS
of S. guianensis Long et al. (2017) Characteristics of the soil before and after 420 DAS of S. guianensis

Zone impacted by mining Ground soil Flatland soil Hill soil

Impacted soil Before Before Before S.

Parameter (start experiment) S. guianensis sowing S. guianensis sowing S. guianensis sowing guianensis
K (ppm) a 37.0 ± 8.5 a 53.3 ± 14.5 a 36.2 ± 36.0 a 45.8 ± 54.3 b 92.5 ± 12.7 a 63.8 ± 14.5 a 44.4 ± 11.5 a 6.4 ± 13.8
SOM (%) b 0.03 ± 0.1 a 0.39 ± 0.1 b 4.2 ± 5.2 a 6.3 ± 5.9 a 5.4 ± 0.9 a 6.4 ± 0.6 a 6.8 ± 3.6 a 8.2 ± 1.6
P (ppm) a 4.4 ± 0.2 a 4.5 ± 1.1 b 2.1 ± 2.6 a 3.2 ± 4.4 a 2.4 ± 2.2 a 1.9 ± 1.1 a 1.4 ± 1.1 a 1.9 ± 1.5
pH a 5.4 ± 0.2 a 4.8 ± 0.2 a 6.3 ± 6.3 a 5.9 ± 6.3 a 6.3 ± 0.1 a 6.4 ± 0.1 b 5.6 ± 1.6 a 6.3 ± 0.1

TABLE 9 Taxonomic groups and population density of soil macrofauna in different ecosystems

Taxonomic Population density

Type of vegetation Location groups (n
) (individuals m2)
Impacted soil (start of experiment) San Jacinto Native Community (Madre de Dios-Perú) 2 11
Impacted area S. guianensis (This research) San Jacinto Native Community (Madre de Dios-Perú) 11 887
Varillal natural forest (Tapia-coral & Natural Protected Area “Reserva Nacional Allpahuayo 15 768
Pashanasi, 2006) Mishana” (Loreto-Perú)
Varillal natural forest (Tapia-coral & Jenaro Herrera (Loreto-Perú) 12 1,611
Pashanasi, 2006)
Chamizal natural forest (Tapia-Coral & Jenaro Herrera (Loreto-Perú) 12 1,728
Pashanasi, 2006)
Chamizal natural forest (Tapia-coral & Natural Protected Area “Reserva Nacional Allpahuayo 10 1,179
Pashanasi, 2006) Mishana” (Loreto-Perú)
Zea maiz crop (Villalobos et al., 2000) La Mancha (Veracruz, México) 10 246
Arachis pintoi crop (Velásquez et al., 2012) Benfica settlement (Pará State -Brazil) 10 2,633
Brachiaria brizantha (Velásquez et al., 2012) Benfica settlement (Pará State -Brazil) 8 3,808
Leucaena leucocephala (Velásquez et al., 2012) Benfica settlement (Pará State -Brazil) 10 1,386
Solanum rugosum (Velásquez et al., 2012) Benfica settlement (Pará State -Brazil) 9 541

enhance the mineralization and humification process, transport
organic material to deeper soil layers and improve soil chemistry by
increasing nitrogen and phosphorous stocks that benefit plants,
microorganisms and other soil organisms (Amador & Görres, 2007;
Frouz & Ilková, 2008; Lavelle et al., 2006; Lavelle, 2002).
4.4 | Carbon sequestration and land degradation
neutrality
We found that alluvial gold mining reduced the soil carbon sequestra-
tion capacity of forest soils by 99.9%, from 0.43 ± 0.11 in mature for-
est to 0.004 ± 0.0028 t C ha1 in ASGM. However, already at
470 DAS S. guianensis increased soil carbon sequestration of impacted
areas by more than 1650%, from 0.004 t C ha1 in, up to
0.07 t C ha1. Soil carbon is relevant to land-based efforts to hold off
carbon emissions, discharge atmospheric carbon dioxide, and carry
ecosystem services in addition to climate mitigation (Bossio
et al., 2020; Duarte-Guardia et al., 2020). SOC will increase up to the
point at which a new SOC equilibrium (balance between organic mat-
ter inputs and SOM turnover) is reached (Lal, 2003).
To achieve land degradation neutrality (UNCCD, 2019) and other
environmental initiatives such as Nationally Appropriate Mitigation
and Adaptation Actions (NAMAs) in tropical alluvial gold mining areas,
six main issues have to be considered: soil fertility and the role of soils
for food security, soil and public health, soil water, mitigation of cli-
mate change on soils and opportunities for mitigation, functions of
soil Biodiversity and the challenge to implement effective soil conser-
vation. Applied to S. guianensis, its establishment significantly
improves soil fertility, helps recovering soil C stock, increases soil
water retention, promotes soil biodiversity, and hence seems like a
promising method to restore degraded ASGM areas (Keesstra
et al., 2016). Together, these benefits are essential to achieving many
of the societal goals in the framework of the Sustainable Develop-
ment Goals (SDGS 1,2 3, 6, 7, 8, 9, 11, 12, 13, and 15) (Keesstra
et al., 2016; Keesstra et al., 2018).
5 | CONC LU SIONS
S. guianensis var CIAT 184 turned out to be a pioneer species with
large potential to kick-start the recovery of soils in areas degraded by


VELASQUEZ RAMÍREZ ET AL. 9

ASGM. The species successfully establishes under conditions of infer- RE FE RE NCE S

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How to cite this article: Velásquez Ramírez, M. G., del Castillo
Torres, D., Guerrero Barrantes, J. A., Vásquez Bardales, J.,
Thomas, E., Cusi Auca, E., Chinen Gushiken, M., Muñoz Diaz,
B., Russo, R., & Corvera Gomringer, R. (2021). Soil recovery of
alluvial gold mine spoils in the Peruvian Amazon using
Stylosanthes guianensis, a promising cover crop. Land
Degradation & Development, 1–11. https://doi.org/10.1002/
ldr.4118