Archivos Latinoamericanos de Producción Animal. 2023. 31 (4)

Soil fertility in silvopastoral systems integrating tree legumes with

signalgrass (Urochloa decumbens Stapf. R. Webster)

Recibido: 20221226. Revisado: 20230822. Aceptado: 20230930

1Corresponding author. Email address: aherrera@unet.edu.ve

2Animal Science Department, Universidade Federal Rural de Pernambuco. CNPq Fellow. Pernambuco, Brazil.

3Associated Professor I, Universidade Estadual do Maranhão. Maranhão, Brazil.

4North Florida Research & Education Center, University of Florida. Florida, United States.

5Animal Science Department. Facultad de Agronomía e Ingeniería Forestal. Pontificia Universidad Católica de Chile. Santiago de Chile. Chile.

6Instituto Agronômico de Pernambuco. Pernambuco, Brazil.

287

Ana María Herrera1

Abstract. Silvopastoral Systems (SPS) can increase overall productivity and income in order to stimulate the

simultaneous growth and development of trees, forage and livestock. Moreover, the SPS with tree legumes would

be important for adding nutrients to the system, mainly N, ensuring soil health and quality. Soil properties were

assessed in two SPS, implanted in 2011, using tree legumes (in double rows) intercropped with Urochloa decumbens

Stapf. R. Webster (Signalgrass). Treatments were Signalgrass + Mimosa caesalpiniifolia Benth (Sabiá) and Signalgrass

+ Gliricidia sepium (Jacq.) Kunth ex Walp. (Gliricidia), and they were allocated in a randomized complete block

design, with three replications. Soil was sampled in 2013, 2017, and 2018, at 0, 4, and 8 m along transects

perpendicular to tree double rows, from 0 to 20 and 20 to 40cm layers. Soil chemical properties evaluated

included pH, P, K+, Ca2+, Mg2+, Al3+, H++Al3+, cation exchange capacity (CEC), and base saturation. In addition,

light fraction of soil organic matter (LFSOM), soil basal respiration (SBR), and natural abundance of 13C of the

respired CO2 (δ13CCO2) were analyzed. Soil pH (5.3, 5.2, 5.1), P (11.3, 7.2, 3.6 mg dm3), and CECeffective (5.8, 5.1, 5.0

cmolc dm3) decreased (P < 0.05) along the years 2013, 2017, and 2018, respectively. In 2018, the LFSOM and δ13C

CO2 were greater in Sabiá (1.1 g kg1 and 16.4 ‰) compared to Gliricidia (0.7 g kg1 and 18.2 ‰). Silvopastoral

systems reduced soil fertility regardless of the tree legume species used as a result of biomass nutrient stock,

without maintenance fertilization. Sabiá had greater deposition of LFSOM, without increasing SBR, providing

potential for microbial C use efficiency. Enriched CCO2 isotope composition had an efficient SOM oxidization in

SPS with Gliricidia or Sabiá. This information can contribute to the assessments related to CO2 balance and C

retention. Both SPS contribute to C sequestration.

Keywords: agroforestry systems; Gliricidia sepium; Mimosa caesalpiniifolia; soil chemical properties; C sequestration.

https://doi.org/10.53588/alpa.310401

Agricultural Research Department, Universidad Nacional Experimental del Táchira. Táchira, Venezuela.

Alexandre Carneiro Leão de Mello2

Fertilidade do solo em sistemas silvipastoris integrando leguminosas arbóreas

com capimbraquiária (Urochloa decumbens Stapf. R. Webster)

Resumo. Os Sistemas Silvipastoris (SSP) podem aumentar a produtividade e gerar renda. Também, os SSP com

leguminosas arbóreas adicionam nutrientes ao sistema, principalmente N, garantindo a saúde e a qualidade do

solo. As propriedades do solo foram avaliadas em dois SSP utilizando leguminosas arbóreas em consorcio com

Urochloa decumbens Stapf. R. Webster (capimbraquiaria). Os tratamentos foram capimbraquiária + Mimosa

caesalpiniifolia Benth (Sabiá) e capimbraquiária + Gliricidia sepium (Jacq.) Kunth ex Walp. (Gliricídia), sendo

distribuídos em delineamento casualizado em blocos (três repetições). As coletas de solo foram realizadas nos anos

2013, 2017 e 2018, a 0, 4 e 8 m ao longo de transectos perpendiculares às fileiras duplas de árvores, nas

profundidades de 020 e 2040 cm. As propriedades químicas do solo avaliadas incluíram pH, P, K+, Ca2+, Mg2+,

Al3+, H++Al3+, capacidade de troca de cátions (CTC) e saturação por bases. Foram analisadas a fração leve da

matéria orgânica (FLMOS), a respiração basal (RBS) e a abundância natural do 13C do CO2 respirado (δ13CCO2). O

pH (5,3; 5,2; 5,1), P (11,3; 7,2; 3,6 mg dm3) e CTCefetiva (5,8; 5,1; 5,0 cmolc dm3) diminuíram (P < 0,05) ao longo dos

anos 2013, 2017 e 2018, respectivamente. Em 2018, a FLMOS e δ13CCO2 foi maior em Sabiá (1,1 g kg1 e 16,4 ‰) em

comparação com Gliricídia (0,7 g kg1 e 18,2 ‰). Os SSP reduziram a fertilidade do solo independentemente das

espécies arbóreas utilizadas em decorrência do estoque de nutrientes da biomassa, sem adubação de manutenção.

Sabiá teve maior deposição de FLMOS, sem aumentar a RBS, proporcionando potencial para a eficiência do uso do

Valéria Xavier de Oliveira Apolinário3José Carlos B. Dubeux Jr4

Robert Emilio MoraLuna5 Erinaldo Viana de Freitas6

288

Introduction

Herrera et al.

Silvopastoral systems (SPS), as an agroforestry

practice, can increase overall productivity and generate

income in order to stimulate the simultaneous growth

and development of trees, forage and livestock (Sarabia

et al., 2019; Watanabe et al., 2016). Moreover, SPS with

tree legumes enhance the delivery of ecosystem

services in livestock system (Dubeux Jr. et al., 2019),

including biological nitrogen fixation, shade and

fodder supply for ruminants, as well as production of

marketable timber, increase in producer income, and

stability of the soilplant system (Apolinário et al., 2015;

Dubeux Jr. et al., 2019). These combinations of SPS

would be important for stabilizing fertilization and

ensuring soil health and quality.

This stability of the soilplant system is possible from

beneficial interactions between biological components

(soil, water, air, plants, and animals) (Sheoran et al., 2017).

Tree legumes, for instance, can increase N input and

nutrient availability in the system, via Nfixation, litter

deposition and decomposition (Sarabia et al., 2019).

However, tree characteristics, such as canopy structure,

leaf deposition, and litter quality, may affect soil

chemical and biological properties (Alfaro et al., 2018).

The soil is considered a complex and fundamental

system for the dynamic of terrestrial ecosystems (Terra

et al., 2019); however, some livestock traditional

activities may contribute to the depletion of soil

productive capacity, leading vast grassland areas to

degradation (Santana et al., 2016). Soil chemical and

physical properties affect water and nutrient

availability for plants and soil microorganisms. The

most common soil properties used to assess nutrient

availability are pH, mineral content, cation exchange

capacity (CEC), soil organic matter (SOM), carbon and

mineralizable nitrogen content (Bünemann et al., 2018).

Regarding biological properties, microbial processes

have fundamental importance for the productivity and

sustainability of systems (Santos et al., 2014), being

C microbiano. A composição enriquecida de isótopos de CCO2 mostraram uma eficiente oxidação da MOS em SSP

com Gliricídia ou Sabiá. Essas informações podem contribuir para as avaliações relacionadas ao balanço de CO2 e

retenção de C. Ambos SSP contribuem para o sequestro de C.

Palavraschave: sistemas agroflorestais; Gliricidia sepium, Mimosa caesalpiniifolia; propriedades químicas do solo;

sequestro de C.

Fertilidad del suelo en sistemas silvopastoriles que integran leguminosas

arbóreas con pasto señal (Urochloa decumbens Stapf. R. Webster)

Resumen. Los Sistemas Silvopastoriles (SSP) pueden aumentar la productividad general y generar ingresos.

Además, los SSP con leguminosas arbóreas adicionan nutrientes al sistema, principalmente N, asegurando la salud

y la calidad del suelo. Propiedades del suelo fueron evaluadas en dos SSP utilizando leguminosas arbóreas en

asociación con Urochloa decumbens Stapf. R. Webster (Barrera). Los tratamientos fueron Barrera + Mimosa

caesalpiniifolia Benth (Sabiá) y Barrera + Gliricidia sepium (Jacq.) Kunth ex Walp. (Gliricidia), distribuidos en un

diseño de bloques aleatorizados (tres repeticiones). Se realizaron colectas de suelo en los años 2013, 2017 y 2018, a 0,

4 y 8 m en transectos perpendiculares a las hileras de árboles, en las profundidades de 020 y 2040 cm. Las

propiedades químicas del suelo evaluadas incluyeron pH, P, K+, Ca2+, Mg2+, Al3+, H++Al3+, capacidad de

intercambio catiónico (CIC) y saturación de bases. Se analizaron la fracción activa de la materia orgánica (FAMOS),

respiración basal (RBS) y abundancia natural de 13C del CO2 respirado (δ13CCO2). El pH (5.3, 5.2, 5.1), P (11.3, 7.2,

3.6 mg dm3) y la CICefectiva (5.8, 5.1, 5.0 cmolc dm3) disminuyeron (P < 0.05) a través de los años 2013, 2017 y 2018,

respectivamente. En 2018, la FAMOS y δ13CCO2 fueron mayores en Sabiá (1,1 g kg1 y 16,4 ‰) comparada con

Gliricidia (0,7 g kg1 y 18,2 ‰). Los SSP redujeron la fertilidad del suelo independientemente de las especies

arbóreas utilizadas como resultado de la reserva de nutrientes de la biomasa, sin fertilización de mantenimiento.

Sabiá tuvo mayor deposición de FAMOS, sin aumentar RBS, favoreciendo potencialmente la eficiencia del uso de C

microbiano. La composición isotópica de CCO2 enriquecida muestra una oxidación eficiente de la MOS en SSP con

Gliricidia o Sabiá. Esta información puede contribuir a las evaluaciones relacionadas con el balance de CO2 y

retención de C. Ambos SSP contribuyen al secuestro de C.

Palabras clave: sistemas agroforestales; Gliricidia sepium; Mimosa caesalpiniifolia; propiedades químicas del suelo;

secuestro de C.

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289

Soil fertility in silvopastoral systems

Location, procedures and experimental design

The research was conducted at the Experimental

Station of the Agronomic Institute of Pernambuco

(IPA), located in Itambé, Pernambuco, Brazil. The

station is located at 7°23’ S and 35°10’ W. Average

annual rainfall is 1253 mm (APAC, 2022), and the

average annual temperature is 25°C (RIMA, 2014), with

KöppenGeiger climate classified as hot and humid

tropical (As). The predominant soil is dystrophic

Ultisol (Silva et al., 2001).

The treatments were defined by two SPS: Gliricidia

+ signalgrass (Gliricidia) and Sabiá + signalgrass

(Sabiá). The experimental area consisted of six

paddocks of 1.0 ha each. Tree legumes were established

in double rows spaced by 15.0 m (between double

rows) x 1.0 m (between rows) x 0.5 m (within rows)

(Fig. 1). Establishment of signalgrass occurred in open

pits (approx. 5 cm deep) and seeds were placed

manually (10 kg of commercial seed ha1 with 40 %

cultural value). Signalgrass was previously established

in one of the blocks since 1969. In the other two blocks

were established along with the tree legumes, between

the double rows. Legume seeds were planted in a

greenhouse and inoculated with specific

Bradyrhizobium strains obtained from the Soil

Microbiology Laboratory at Universidade Federal

Rural de Pernambuco (UFRPE). All paddocks were

fertilized in July 2011 with 44 kg ha1 of P (as single

superphosphate) and 100 kg ha1 of K (as potassium

chloride) on the entire area. Legume seedlings were

transplanted to the field in June 2011 at approximately

30cm height and planted in 20cm deep furrows.

Paddocks were fully established in October 2011.

Material and Methods

highly related to SOM decomposition derived from

plant and animal waste, as well as its recycling. Basal

soil respiration, microbial biomass, and C:N ratio are the

most valuable variables in the interpretation of SOM

dynamics (Alfaro et al., 2018; Santos et al., 2014), as those

are considered indicators of soil organic matter cycling.

Gliricidia sepium (Jacq.) Kunth ex Walp. (Gliricidia)

and Mimosa caesalpiniifolia Benth. (Sabiá) are tree

legumes, introduced and native, respectively, with

potential for use in SPS. These species are drought

tolerant and nitrogen fixers (Apolinário et al., 2015).

Recently, SPS integrating those legumes with the grass

Urochloa decumbens Stapf. R. Webster (signalgrass) have

been evaluated in Northeastern Brazil, in terms of

biomass production, chemical composition, litter

quality, deposition and decomposition, as well as

animal performance (Apolinário et al., 2016, 2015;

Oliveira et al., 2018; Santos et al., 2020). However, there

are few assessments of changes in soil chemical and

biological properties in SPS, including those tree

legumes. The hypothesis of this study was that the

inclusion of those tree legumes in SPS would improve

soil fertility differently with time. The aim of the

experiment was to evaluate the changes along a time

sequence in soil chemical and biological properties in

two SPS, integrating tree legumes, Gliricidia or Sabiá,

with signalgrass.

Fig. 1. Tree spacing in the double row silvopastoral system and soil sampling area. Each oneha plot had 14 double rows.

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Soil chemical properties

Interaction between treatment × distances for H+

+Al3+ (P = 0.04) and TEB (P = 0.02), year × distances for

K+ (P = 0.05) and year × treatment × distances for Mg2+

(P = 0.04) and base saturation (P = 0.004) were

observed. Soil pH, P, CECeffective and CECpotential (Tables

1 and 2) were different (P < 0.05) among years, with no

treatment differences (P > 0.05) in any of the variables

considered in soil chemical properties.

Soil pH significantly reduced from 2013 to 2018

(Table 1), showing increased acidity of soil reflecting

the activity of nitrifying bacteria as they release NO3

and H+ during oxidizing the ammonium NH4+N

(Neina, 2019). Further, this is favored by the presence

of nitrogenfixing species (e.g., Gliricidia and Sabiá)

and nitrate concentrations (Mathesius, 2022).

Moreover, these species deposited Nrich litter that

will further add H+ during nitrification of the

decomposing litter. According to Johan et al. (2021)

soils with elevated acidity, usually have low base

Results and Discussion

290

Initial soil physical characteristics (2011) from 0 to

20cm depth were loamclaysandy texture with

proportions of coarse sand (0.22 mm), fine sand (0.05

0.2 mm), silt (0.0020.05 mm), and clay (< 0.002 mm) of

44, 17, 16, and 22 %, respectively, and soil and particle

density of 1.33 and 2.52 g cm3, respectively. Average

monthly rainfall for the experimental years is shown as

supplementary material.

Each plot had 14 double rows with a tree density of

approximately 2500 plants ha1. Treatments were

allocated in a randomized complete block design, with

three replications. Yearling crossbred Holstein × Zebu

steers, with approximately 200 kg of body weight (BW)

were used as experimental animals, under continuous

stocking with variable stocking rate (Mott and Lucas,

1952). Stocking rate was adjusted every 28 days

following the recommendation of Sollenberger et al.

(2005). The target herbage allowance was 3 kg DM d1

of green herbage mass per kilogram of BW. Water and

a mineral mixture (Ca: 107 g kg1, P: 88 g kg1, S: 12 g

kg1, Na: 126 g kg1, Co: 55 mg kg1, Cu: 1530 mg kg1,

Fe: 1800 mg kg1, I: 75 mg kg1, Mn: 1300 mg kg1, Zn:

3630 mg kg1, F: 880 mg kg1) were offered ad libitum on

each paddock.

Soil chemical properties

Soil chemical properties were evaluated in 2013, 2017

and 2018, at 0 to 20cm depth. Three soil samples

(sampling units) were analyzed per paddock

(experimental unit), at two distances within each

paddock, in between the double rows and at 8 m from

them in a perpendicular transect to the tree row (Fig. 1),

resulting in a composite sample for each distance per

plot. Soil variables included pH, P, K+, Ca2+, Mg2+, Al3+,

and H++Al3+, obtained from the Soil Chemical

Laboratory at UFRPE. Subsequently, the total

exchangeable bases (TEB), effective (TEB + Al3+) and

potential (TEB + H++Al3+) CEC and base saturation

were estimated following EMBRAPA (2017) procedures.

Indicators of soil organic matter cycling

Indicators of soil organic matter cycling were

evaluated for two years (2017 and 2018) at 0 to 20 and

20 to 40cm depth (Fig. 1). The sampling protocol was

similar to the one used for soil chemical properties.

Indicators of soil organic matter cycling included the

light fraction of SOM (LFSOM), soil basal respiration

(SBR), and natural abundance of 13C of the respired

CO2 (δ13CCO2).

The light fraction of SOM was estimated using the

SOM fractionation methodology proposed by Meijboom

et al. (1995) and adapted by Dubeux Jr. et al. (2006). Soil

basal respiration was determined by CO2 emission from

soil samples incubated for 21 d, with soil humidity at

around 60 % of field capacity, without light and

temperature between 25 to 28 °C, quantified and

estimated by titration (Harris et al., 1997; Silva et al.,

2007). After titration, the suspension was processed

following the method of Ramnarine et al. (2012), and

subsequently dried in a forcedair oven (65±2 °C) to

constant weight for storage. Samples were sent to the

University of Florida, to determine the δ13CCO2 using a

CHNS analyzer through the Dumas dry combustion

method (Vario Micro Cube, Elementar) coupled to an

isotope ratio mass spectrometer (IsoPrime 100,

IsoPrime). The δ13CCO2 estimate was performed

according to Unkovich et al. (2008) and Fry (2006).

Statistical analysis

Variance analyses were performed using the PROC

MIXED procedure of the SAS (SAS University Edition

software), using the Tukey test, when the F test was

significant (P < 0.05). For chemical and biological

properties, SPS, distance from the double rows of

legumes, soil depth, and year (as appropriate), were

considered fixed effects, and blocks were the random

effect. The year effect was analyzed using the repeated

measurement procedure.

Herrera et al.

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291

concentration, elevated Al3+ and high P fixation. The

lower soil pH values observed in 2018 compared to

2013 may also be explained by the extractions of

cations by trees and the pasture. This result is probably

associated with decreased P, Mg2+ K2, TEB and

CECeffective over the years (P < 0.05).

Table 1. Soil chemical properties between 0 to 20cm depth in silvopastoral systems intercropped with signalgrass in Itambé,

Pernambuco state, Brazil.

pH P Ca2+ Mg2+ K+ Al3+

Factor (water, 1: 2.5) mg dm3 cmolc dm3

Year (Y)

2013 5.3A 11.3A2.5 2.7A 0.23A0.23A

2017 5.2AB 7.2B3.0 1.1C0.17AB 0.17AB

2018 5.1B 3.6C2.9 1.5B0.12B0.12B

Standard error 0.05 0.07 0.29 0.08 0.06 0.06

Pvalue 0.0061 <0.0001 0.1864 <0.0001 0.0122 0.0122

Treatment (T)

Gliricidia + Signalgrass 5.3 6.1 3.1 1.8 0.21 0.21

Sabiá + Signalgrass 5.1 7.3 2.5 1.6 0.14 0.14

Standard error 0.05 0.07 0.33 0.07 0.06 0.06

Pvalue 0.1239 0.4993 0.3070 0.3514 0.1038 0.1038

Distance (D)

0 m 5.2 6.5 2.7 1.7 0.19 0.19

8 m 5.2 6.8 2.9 1.8 0.15 0.15

Standard error 0.04 0.06 0.26 0.07 0.05 0.05

Pvalue 0.2074 0.8010 0.2563 0.4255 0.1857 0.1857

Y × D

Standard error 0.06 0.08 0.35 0.10 0.09 0,11

Pvalue 0.0974 0.1084 0.8288 0.3055 0.2246 0,0493

Y × T × D

Standard error 0.09 0.11 0.50 0.15 0.13 0.11

Pvalue 0.4229 0.6171 0.4893 0.0017 0.2464 0.3893

P: phosphorus (MehlichI); Ca2+: calcium; Mg2+: magnesium; K+: potassium; Al3+: exchangeable aluminum.

Different uppercase letters in the column, within each factor, differ significantly (P < 0.05). Other interactions were not significant (P > 0.05).

Both legume species, Gliricidia and Sabiá, had an

average biomass accumulation during the initial 5.5

years of approximately 10 Mg ha1 year1 (Apolinário et

al., 2015). Biomass fractions included thin,

intermediate, and thick branches and total leaves (19,

22, 54, and 5 %, respectively). During these years,

nutrient absorption increased exponentially with

growth (mainly due to woody tissue production) until

it reached its maximum growth (between 7 to 10 years,

depending on the species). The order of nutrient

concentrations for all components of the aboveground

biomass, in general, follows this sequence: N> Ca2+>

K+> Mg2+> P (Moura et al., 2006). This could result in

nutrient depletion in the soil over time (Alvarado,

2015), especially when maintenance fertilization is not

considered. Nutrients associated with the residues, as

litter, represent 50 % of total nutrients associated with

aerial biomass, contributing to chemical soil properties

with 40–45 % of the N, 54 % of the K+, 56 % of the Mg2+,

and 28 % of the P (Montagnini, 2000).

Soil P also decreased over the years (P < 0.05), being

considered as medium level in the years 2013 and 2017

and as low in 2018 (Table 1). This decrease may be

associated with the concentration of the element in the

aboveground biomass. For Sabiá with 8 years of

establishment and diameter at breast height (DBH)

between 34 cm, P concentrations of 0.88 g kg DM1

were determined in the aerial biomass (Moura et al.,

2006). Considering the biomass accumulation of 50 Mg

ha1 reported by Apolinário et al. (2015), it is estimated

that approximately 44 kg ha1 of P were stocked in the

arboreal biomass, not to mention the root system.

In Gliricidia, Barreto and Fernandes (2001) reported

P concentrations of 1.7 g kg1 for 4yearold trees,

resulting in an estimated P stock of 85 kg ha1 of P, not

considering the roots. In addition to the element

depletion generated by the absorption of the plant

throughout its growth, according to Larsen (2017) the

total P content of the soils is relatively low (between

500 and 10,000 kg ha1 P up to 50cm deep) and a

portion is usually in forms unavailable for plants

absorption. These assumptions indicate the need to

supply this element. The availability and absorption of

this element stimulate the root growth of crops,

increasing the area of soil explored by vegetation and

greater absorption of other nutrients. Consequently, P

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Soil fertility in silvopastoral systems

Factor H++Al3+ TEB CECeffective CECpotential Base Saturation

cmolc dm3 %

Year (Y)

2013 5.0B5.3A 5.8A10.3B53A

2017 9.6A4.6B 5.1B14.2A32B

2018 9.8A4.6B 5.0B14.4A32B

Standard error 0.4 0.3 0.3 0.5 2.1

Pvalue <0.0001 0.0446 0.0404 <0.0001 <0.0001

Treatment (T)

Gliricidia + Signalgrass 7.5 5.3 5.6 12.7 43

Sabiá + Signalgrass 8.7 4.4 5.0 13.2 35

Standard error 0.6 0.4 0.3 0.6 2.60

Pvalue 0.1842 0.2175 0.2508 0.6464 0.1027

Distance (D)

0 m 8.4A4.7 5.2 13.2 37B

8 m 7.8B5.0 5.4 12.8 41A

Standard error 0.4 0.3 0.3 0.5 2.0

Pvalue 0.0216 0.2904 0.5455 0.3013 0.0440

T × D

Standard error 0.5 0.5 0.4 0.7 2.8

Pvalue 0.0438 0.0240 0.0666 0.8775 0.0008

Y × T × D

Standard error 0.7 0.6 0.4 0.9 3.4

Pvalue 0.0510 0.1975 0.3802 0.5867 0.0039

292

Fig. 2. Interaction between treatment × year × distances for soil Mg2+ (A) and base saturation (B), in silvopastoral systems

intercropped with signalgrass in Itambé, Pernambuco state, Brazil.

The same uppercase letters for treatments and lowercase for distance, across years, do not differ significantly (P > 0.05).

deficiency could affect plant growth, seed formation,

crop maturation, and nitrogenfixing capacity of legume

species (Dubeux Jr et al., 2014; SanzSaez et al., 2017).

In the interaction between treatment × year ×

distances (P < 0.05) for Mg+2, values were greater in

2013 for both SPS and distances (Fig. 2A). This

response is possibly associated with the lower

requirement of trees because of younger age (2 years),

enabling greater Mg2+ concentration from the

deposited arboreal components.

Table 2. Potential acidity, total exchangeable bases, cation exchange capacity and base saturation between 0 to 20cm depth, in

silvopastoral systems intercropped with signalgrass in Itambé, Pernambuco state, Brazil.

H++Al3+: potential acidity; TEB: total exchangeable bases; CEC: cation exchange capacity

Different uppercase letters in the column, within each factor, differ significantly (P < 0.05). Other interactions were not significant (P > 0.05).

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Herrera et al.

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Soil fertility in silvopastoral systems

In 2017 and 2018, the average soil Mg2+ was lower

than in 2013; however, soil Mg2+ concentration was still

adequate for plant growth. According to Karley and

White (2009), Mg2+ concentrations in the soil solution

should be between 0.0125  0.85 cmolc dm3 to support

plant growth. This reduction observed between 2013

and 2017, may be related to the increase in tree nutrient

requirement along 7 years of growth, promoting

depletion of the element into the soil. Barreto and

Fernandes (2001) and Moura et al. (2006), respectively,

reported aboveground biomass Mg2+ concentrations in

Gliricidia (6.6 g kg1) and Sabiá (2.8 g kg1). Considering

these values, and biomass accumulation of 50 Mg ha1

for both species during the initial 5.5 years of tree

development (Apolinário et al., 2015), it is estimated

that approximately 330 and 140 kg ha1 were stocked in

the biomass of Gliricidia and Sabiá, respectively.

Magnesium is often stored in root cells and released to

the xylem if shoots become Mg2+ deficient (Karley and

White, 2009). Furthermore, the pH reduction promotes

the leaching of some elements, including Mg2+ (Neina,

2019).

Interaction (P < 0.05) occurred between distances ×

year for K+ (Fig. 3), with the greatest values in 2013,

regardless of the distances and, in 2017, only between

the double rows of legumes. The decrease in soil K+

from 2013 to 2017 can be associated with tree nutrient

requirements for tree development over time. Greater

removal of K+ and Mg2+ from the soil is a possible

consequence of increased accumulation of these

elements in biomass components, with younger trees

having greater nutrient demand in leaves and branches

(Ali et al., 2017; Dick and Schumacher, 2019). For K+, it

is estimated that approximately 0.8 (16 g kg1) and 0.7

Mg ha1 (14 g kg1) were stocked in the biomass of

Gliricidia and Sabiá, respectively (Apolinário et al.,

2015; Barreto and Fernandes, 2001; Moura et al., 2006).

Similar to N, K+ is the nutrient required in the largest

quantity by plants (5 to 10 times more than P), and the

requirement for optimal plant growth is between 20–50

g kg1 in vegetative parts and fruits (Hawkesford et al.,

2023; Larsen, 2017). Overall reduction in soil K+

concentration was observed in 2018 compared to 2013

(Fig. 3), with no differences between distances. A

gradient with the distance from the trees is not

observed, possibly, because these legumes have a length

and distribution of homogeneous roots up to 8 m from

the crown. Soil K+ declined almost 50 % from the initial

sampling in 2013 until the last sampling in 2018.

Greater soil K+ between legume double rows in 2017

compared to the signalgrass strip (8 m away from

double rows) in the same year is probably associated

with the presence of animals in 2017 (Fig. 3). Before soil

sampling, grazing animals were in continuous stocking

for six months for the year 2017, and for a month prior

to the 2018 sampling (before this, the continuous

stocking was interrupted for four months). K+ is

eliminated in greater proportion by urine (Battisti et al.,

2018) and fecal K+ from grazing livestock may present a

faster release rate into the soil solution during the

decomposition process compared with other elements

(Lima et al., 2018). Furthermore, greater fecal deposition

might occur under the tree canopy because cattle seek

shade during the warmer hours of the day (Dubeux Jr et

al., 2014). The litterfall is another factor that can affect

the concentration of nutrients at different distances from

the double row of legumes, however in both years, the

evaluations were at the end of the rainy season.

Fig. 3. Interaction between year × distances for soil K+ in silvopastoral systems intercropped with signalgrass in Itambé,

Pernambuco state, Brazil.

Same letters, lowercase for year within each distance and uppercase for the distance within each year, do not differ significantly (P > 0.05).

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294

Fig. 4. Interaction between treatment × distances for soil potential acidity and total exchangeable bases in silvopastoral systems intercropped with

signalgrass in Itambé, Pernambuco state, Brazil.

Same letters, lowercase for treatment and uppercase for distance, within each response variable, do not differ significantly (P > 0.05).

Herrera et al.

In the interaction between treatment × sampling

site (P < 0.05) for H++Al3+ and TEB, Gliricidia showed

greater and lower values, respectively, between double

rows, while Sabiá did not show differences between

sampling sites (Fig. 4). This increase is probably

associated with the H+ ions released by the roots, to

balance loads, when the plant absorbs cations products

of litter decomposition (Battisti et al., 2018), since Al3+

remained stable through assessments (Table 2).

Likewise, an increase of ion H+ release is expected to

occur in highly nitrifying systems (Barth et al., 2019),

mainly from the Gliricidia litter, which contains more

N than Sabiá litter (Apolinário et al., 2016). In the

signalgrass strips, 8 m away from the Gliricidia double

row, the release of H+ ions must have occurred at a

lower rate, mainly due to the lower litter

mineralization, especially nitrification, related to the

litter quantity and quality (Barth et al., 2019; Battisti et

al., 2018; Dubeux Jr et al., 2014). Under the Sabiá

canopy, the overall greater litter deposition for Sabiá

(Apolinário et al., 2016) and probably greater tree

development could lead to more root exudation and

litter mineralization. Moreover, the greater nutrient

uptake (mainly K+ and Mg) with immobilization in the

biomass of trees that results in more ion H+ occupying

the base cations sites in the CEC.

The CECeffective decreased (P < 0.05) and the CTCpotential

values (TEB + H++Al+3) increased (P < 0.05) between years

2013 and 2017 (Table 2). Charges on organic colloids

are pHdependent, limiting the benefits in acid soils

since CECeffetive decreases as pH decreases (Gruba and

Mulder, 2015). In this case, the exchangeable base

cations (Ca2+, Mg2+, K+, Na+) occupied less than 37 %

of CECpotential, with elevated H+ ions occupying the

basecations sites, associated probably with an

increase of soil organic matter, as observed by Gruba

and Mulder (2015).

Treatment × year × sampling sites interaction

(P < 0.05) occurred for base saturation (Fig. 2B), with

greater values in 2013, at 8 m away from double

rows of Gliricidia. However, in this site and between

the double rows of Sabiá, the average base saturation

was greater than 50 %. Greater base saturation in

2013, with significant reductions in 2017 and 2018,

must be a consequence of a negative balance

between input and output nutrients 7 years after the

SPS were established. This may result from the

extraction of large amounts of nutrients from the soil

(mainly P, Mg2+ and K+), stored in the tree biomass,

and the absence of nutrient replacement through soil

correction and fertilization. In 2013, as the trees were

still small or medium in size, the extraction of

nutrients from the soil was probably less, increasing

with growth in later years.

Indicator of soil organic matter cycling

Soil basal respiration (SBR) was similar (P > 0.05)

across years and between silvopastoral systems

(Table 3), with lower SBR at the deeper soil layer (20

40 cm), likely related to reduced plant residues and

less microbial activity for SOM decomposition

(Correia et al., 2015). Soil basal respiration decreases

with soil depth and correlates significantly with the

SOM content, concentrating biological activity at the

top 15cm soil layer (RasouliSadaghiani et al., 2018).

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295

Soil fertility in silvopastoral systems

Table 3. Soil biological properties in silvopastoral systems intercropped with signalgrass in Itambé, Pernambuco state, Brazil.

Factor LFSOM SBR δ13CCO2

g kg1 mg CO2 kg solo1 h1 ‰

Year (Y)

2017 1.6 A 0.19 17.0

2018 0.9 B 0.16 17.3

Standard error 0.1 0.01 0.3

Pvalue <0.0001 0.0987 0.6185

Treatment (T)

Gliricidia + Signalgrass 1.1 0.17 17.4

Sabiá + Signalgrass 1.3 0.18 16.9

Standard error 0.08 0.02 0.4

Pvalue 0.2556 0.7310 0.4754

Soil depth (cm)

020 1.5 A 0.21 A 16.9

2040 1.0 B 0.14 B 17.4

Standard error 0.08 0.01 0.4

Pvalue 0.0002 0.0007 0.4005

Distance (m)

0 1.3 0.17 17.4

4 1.1 0.17 16.9

8 1.3 0.19 17.2

Standard error 0.1 0.01 0.5

Pvalue 0.4228 0.7094 0.8274

Y × T

Standard error 0.1 0.01 0.6

Pvalue 0.0128 0.7607 0.0307

There was a treatment × year interaction for the

light fraction of SOM and the δ13CCO2 (Table 3).

For the treatment × year interaction affecting the LF

SOM (Fig. 5), greater values occurred in 2017,

regardless of treatment; however, in 2018 the

consortium with Sabiá presented 63% more of this

fraction in the soil compared with Gliricidia.

The LFSOM in the system indicates recent chan

ges in SOM, related to the amount of litter deposited

in the soil (Alfaro et al., 2018; Lima et al., 2018) and

according to Yang et al. (2019). The LFSOM is an

important C source for soil microorganisms. Lira

Junior et al. (2020) after five years of the silvopastoral

systems establishment, in the same area observed

changes in microbiological attributes and quality of

the soil organic matter on the first 20 cm of soil up,

at the distance of up to 4 m away from the legume

rows. This was observed through average soil C and

N contents increase of 34 and 77 %, respectively.

Apolinário et al. (2016), in an experimental area

similar to the present study, observed greater litter

deposition of Sabiá (5395 kg DM ha1) compared with

Gliricidia (5204 kg DM ha1). However, differences

between species in leaf production along the period

under evaluation could have influenced the leaf

litter fall and, consequently, LFSOM. In 2018, leaf

production of Sabiá was 133 % (5.6 Mg DM ha1)

greater in relation to Gliricidia (2.4 Mg DM ha1), and

61% greater in 2017. Both soil assessments were carried

out at the end of the rainy season when the greatest

litter fall for these species occurs (Apolinário et al.,

2015). Increasing the amount of LFSOM input could

result in a linear increase of CCO2 emission (Rui et al.,

2016). However, the SBR did not show differences

between SPS, probably reflecting the capacity of soil

microorganisms to form new biomass (cell growth)

rather than microbial respiration (Rui et al., 2016) in

SPS with Sabiá.

Interaction between treatment × year occurred

for δ13CCO2 (Fig. 5), because similar values occurred

between treatments in 2017, but lower values were

obtained in 2018 for the SPS with Gliricidia,

indicating depletion of δ13C in this system, likely due

to greater legumeC contribution from Gliricidia.

Greater labile C content can induce greater initial

microbial activity and, over time, its composition

could concentrate more recalcitrant C (Grover et al.,

2015). Thus, in the SPS with Sabiá, recalcitrant

LFSOM: light fraction of SOM; SBR: soil basal respiration; δ13CCO2: natural abundance of 13C of the respired CO2.

Different uppercase letters in the column, within each factor, differ significantly (P < 0.05). Other interactions were not significant (P > 0.05).

ISSNL 10221301. Archivos Latinoamericanos de Producción Animal. 2023. 31 (4): 287  299

296 Herrera et al.

Conclusions

Silvopastoral systems integrating tree legumes in

double rows with signalgrass caused a reduction in

soil fertility regardless of the tree legume species

used, evidenced mainly by soil pH, P, Mg2+ and K+.

This deficiency resulted from the tree growth stage

after 7 years of establishment and biomass nutrient

stock, without maintenance fertilization. Since this

study did not consider the complete development of

the trees, it is necessary to evaluate the input and

output of nutrients from the soil and nutrient stocks

in plants with time, starting from the

implementation of the integrated system. Such

evaluation could increase knowledge on the

dynamics of nutrients and the impact on soil health

of when of legumes such gliricidia and sabia are

incorporated in silvopastoral systems.

Greater litter fall in silvopastoral systems with sabia,

might explain the higher light fraction of SOM

obtained, without increases in soil respiration,

providing potential for enhanced microbial C use

efficiency. Enriched CCO2 isotope composition shows

an efficient SOM oxidize in silvopastoral systems with

Gliricidia or Sabiá. This information can contribute to

the assessments related to CO2 balance and C retention.

Both silvopastoral systems contribute to C

sequestration.

Conflict of interest. The authors declare that they have not any financial and personal relationships with other

people or organizations that could inappropriately influence their work.

Acknowledgements

Science and Technology Support Foundation of

Pernambuco State (FACEPE), Coordination for the

Improvement of Higher Education Personnel (CAPES)

and the Agronomic Institute of Pernambuco (IPA).

Ethics statement: No animals were used.

Fig. 5. Interaction between treatment × years for light fraction of SOM

(LFSOM) and δ13CCO2 in silvopastoral systems intercropped with

signalgrass in Itambé, Pernambuco state, Brazil.

Same letters, lowercase for year within each treatment and uppercase

for treatment within each year, do not differ significantly (P > 0.05).

materials likely limited the decomposition process in

2018, because of greater nonlabile C concentration.

The isotopic measurement of respired CO2 is a useful

method to quantify the abiotic production of CO2

from carbonates due to the signature of δ13C

exclusive of carbonates and SOM (Santos et al., 2014).

According to Mamilov and Dilly (2011), never tilled

soil produced δ13CCO2 during basal metabolism,

which is typical for C3dominated plant community

(−26‰), and organic matter in all tilled soils is

oxidized more efficiently with longterm production

of δ13CCO2 enriched (19‰).

Thus, the δ13CCO2 respired in the soil can be used

for the quantification of labile C (Ramnarine et al.,

2012), identifying the system with the higher

potential to increase the biological C drainage

capacity of atmospheric CO2 (Santos et al., 2014).

Silvopastoral systems soils, implanted with Gliricidia

or Sabiá, could represent a source of CCO2 with

heavier isotope composition (Table 3), information

that can be used for developing strategies to improve

soil quality, reduce CO2 emissions, and verify C

retention efficiency, as observed by Mamilov and

Dilly (2011).

ISSNL 10221301. Archivos Latinoamericanos de Producción Animal. 2023. 31 (4): 287  299

297

296

APAC, 2022. Boletim do Clima. Síntese Climática.

Agência Pernambucana de Águas e Clima 10, 1–30.

EMBRAPA, 2017. Manual de Metodos de Análises de

Solo, 3ra ed, Manual de métodos de análise de solo.

EMBRAPA, Brasília, DF.

Soil fertility in silvopastoral systems

Author contributions

Ana M. Herrera, Alexandre C. L. de Mello, Valéria X.

O. Apolinário, José C. B. Dubeux Jr. and Erinaldo V.

de Freitas, contributed to the study conception and

design. Material preparation, data collection and

analysis were performed by Ana M. Herrera, Valéria

X. O. Apolinário and Robert E. MoraLuna. The first

draft of the manuscript was written by Ana M. Herrera

and Alexandre C. L. de Mello and all authors

commented on previous versions of the manuscript.

All authors read and approved the final manuscript.

Funding: Partial funding was provided by the IPA.

Edited by Julio Galli

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