Received: 19 April 2020 | Revised: 24 August 2020 | Accepted: 27 August 2020

DOI: 10.1111/jac.12450

MISCELLANEOUS

Bean–soybean succession under full sun and in agroforestry

systems: Impacts on radiation use efficiency, growth and yield

Jaqueline Sgarbossa1 | Elvis Felipe Elli2 | Felipe Schwerz3 | Claiton Nardini4 |

Fábio Miguel Knapp5 | Denise Schmidt6 | Alessandro Dal’Col Lúcio1 |
Braulio Otomar Caron6

1
Department of Crop Science, Federal
University of Santa Maria, Santa Maria, Abstract
Brazil Simultaneous cultivation of agricultural and forest species may result in changes in
2
Department of Biosystems Engineering,
plant community interactions, generating microclimatic changes within the under-
College of Agriculture, University of São
Paulo, Piracicaba, Brazil story and then modifying growth and yield characteristics of the intercropping sys-
3
Department of Agricultural Engineering, tems. Thus, this study aimed to assess the radiation use efficiency, growth and yield
Federal University of Lavras, Lavras, Brazil
4
of bean and soybean cultivated in succession under two arrangements of agrofor-
Department of Forest Science, Federal
University of Santa Maria, Frederico estry and full sun. To these ends, two field experiments were conducted in Southern
Westphalen, Brazil Brazil: bean in-season and soybean off-season. Absolute and relative growth rates,
5
Department of Biosystems Engineering,
net assimilation rate, leaf weight ratio, leaf area ratio, specific leaf area, radiation use
Federal University of Goiás, Goiânia, Brazil
6
Department of Agronomic and efficiency and yield of bean and soybean were assessed. The solar radiation flux was
Environmental Sciences, Federal University modified by plant arrangement and tree canopy characteristics. Shading affected
of Santa Maria, Frederico Westphalen, Brazil
growth and yield characteristics and the radiation use efficiency of the studied crops.
Correspondence From the results obtained in this study, it is possible to recommend crop bean cul-
Jaqueline Sgarbossa, Department of Crop
Science, Federal University of Santa Maria, tivation in agroforestry systems. However, for soybean, due to the reduced yields
97105-900, Santa Maria, Rio Grande do Sul, obtained in agroforestry systems, further research should be conducted in order to
Brazil.
Email: sgarbossajs@yahoo.com study more spaced arrangements and crop insertion in the early years of agrofor-
estry, in order to enable its insertion in agroforestry systems in Southern Brazil.
Funding information
National Council for Scientific and
KEYWORDS
Technological Development
annual crops, forest species, plant arrangement, shading, solar radiation transmissivity,
sustainability

1 | I NTRO D U C TI O N
Agroforestry systems are alternative agricultural production sys-
tems where agricultural and forest species are grown simultane-
ously (Benbi, Brar, Toor, Singh, & Singh, 2011; Sharma, Chauhan,
& Tripathi, 2016). These systems may optimize land use (Zhang
et al., 2019), improve soil structure (Benlhabib, Yazar, Qadir, Lourenço,
& Jacobsen, 2014; Duan et al., 2019) and increase organic matter
contents (Pardon et al., 2017), microbial activity (Rivest, Cogliastro,
Bradley, & Olivier, 2010) and carbon sequestration (Carvalho &
Lourenço, 2014; Sharma et al., 2016). Furthermore, agroforestry
systems may optimize the use of marginalized areas with sustainable
agricultural systems, reducing the need for exploration of new areas
and then favouring the maintenance of existing biomes.
However, the simultaneous cultivation of agricultural and forest
species in the same production area may result in alterations in plant
community interactions (Sgarbossa et al., 2018), affecting microcli-
mate within the understory. These changes often present positive
aspects, but when improperly planned, they may present negative
aspects (Bosi, Pezzopane, & Sentelhas, 2019). One of the main
changes caused by crop cultivation in the understory of agroforestry
systems is the reduction of solar radiation incidence within the un-
derstory. When intercepted by the tree canopy, solar radiation un-
dergoes quantitative and qualitative changes and can be reflected,

J Agro Crop Sci. 2020;00:1–16. wileyonlinelibrary.com/journal/jac© 2020 Wiley-VCH GmbH | 1

2 |
absorbed or transmitted (Caron et al., 2014), depending on the angle
of incidence of the sun's rays (Righi et al., 2007), canopy size, leaf
area index, canopy architecture (Pilau & Angelocci, 2015) and tree
leaf geometry (Behling et al., 2016).
Numerous strategies can be used to mitigate the effects of the
tree canopy on solar radiation, such as the use of different forest
arrangements and species. Caron et al. (2018) studying the dy-
namics of solar radiation in different agroforestry arrangements
(6 m × 1.5 m and 12 m × 3 m) found 82.58% superiority in the
amounts available to the understory in more spaced arrange-
ments. Similarly, Sgarbossa et al. (2018) evaluating the dynamics
of solar radiation in the understory of different forest species,
found a superiority of 41.58% in the solar radiation available in the
understory of Peltophorum dubium (deciduous plant) compared to
the system cultivated with Eucalyptus urograndis. In this context,
further studies should be conducted in order to identify the most
appropriate arrangement and forest species to compose the sys-
tem in order to generate the balance between the amounts of ra-
diation intercepted by the tree canopy and the amounts available
to the understory.
In addition, consideration should be given to the use of crops
widespread in agriculture, such as bean (Phaseolus vulgaris) and
soybean (Glycine max), sources of protein and oil for human and
animal consumption. Bean is grown in approximately 100 coun-
tries, with a wide range of species and varieties. Brazil stands out
as the world's third-largest bean producer (Conab, 2018), with pro-
duction for the 2019/2020 harvest of 3.05 million tons of grains,
with a planted area of 2.92 million hectares (ha) and average yield
of 1,047 kg/ha (Conab, 2020). Soybean is the main oilseed grown
in the world, with about 122.7 million hectares cultivated, produc-
tion of 341.4 million tons of grain and average yield of 2,784 kg/
ha (Fiesp, 2019). Brazil, the second-largest producer of this crop in
the world, presented in the 2019/2020 a harvested area of 36.80
million ha, production of 123.24 million tons and average yield of
3,349 kg/ha (Conab, 2020).
In recent years, Brazilian agriculture has been characterized by
the search for increases in grain production, which has favoured a
second crop (Nóia Júnior & Sentelhas, 2019), especially those sys-
tems in succession. The cultivation of beans in-season is a wide-
spread practice, as it enables the conduction of another crop of
economic importance in succession. In Brazil, bean sowing in
August-November (in-season) corresponds to 31.3% of the total area
planted with the crop (Conab, 2019). In addition, favourable mar-
keting conditions, coupled with the high technological input, have
prompted the sowing of off-season soybean (January-February), in
order to increase production as well as expand soybean cultivation
area (Embrapa, 2014).
On the other hand, intensification of the production system,
through the successive cultivation of agricultural species, especially
those with similar characteristics such as bean and soybean, can
trigger the depletion of natural resources, decreasing the accumu-
lation of organic matter and the cycling of nutrients, as well as fa-
vouring pest and disease pressure. Thus, the association of these
SGARBOSSA et al.
practices with cultivation in agroforestry systems can mitigate these
undesirable effects. In the literature, there are still incipient stud-
ies that consider the insertion of bean (Righi & Bernardes, 2008)
and soybean in agroforestry systems (Caron et al., 2018; Sgarbossa
et al., 2018; Werner, Balbinot Junior, Franchini, Ferreira, & Silva,
2017), especially in a succession system.
When grown under conditions of good water supply and fer-
tilization, biomass production of these crops is dependent on the
amounts of photosynthetically active radiation absorbed by the
leaves, and their efficiency in assimilating and converting solar
radiation by the photosynthesis (Heerden, Donaldson, Watt, &
Singels, 2010; Monteith, 1977). According to Zhu, Long, and Ort
(2008), agricultural crops with C3 metabolism have the maximum
capacity to convert only 4.6% of the intercepted photosynthetic
radiation into produced biomass. Bean and soybean are C3 metabo-
lism species and, due to their metabolic characteristics, have lower
efficiency in the conversion of solar radiation into photoassimilates
compared to C4 species. Thus, when conducted in agroforestry sys-
tems can present modifications in growth, radiation use efficiency
and consequently, yield.
Studies conducted in agroforestry systems have confirmed
changes in crop characteristics, such as the absolute growth rate and
net assimilation rate in sugarcane (Schwerz et al., 2018), leaf area
index, absolute growth rate (Yang et al., 2019) and yield of wheat
(Duan et al., 2019), biomass production and protein content of piatã
palisadegrass and corn (Pezzopane et al., 2019). Duan et al. (2019)
studied the responses of wheat grown in agroforestry systems with
walnut trees and found a reduction in grain yield (annual crop) and
fruit yield (forest species) when grown in a consortium. However,
they verified increases in land-use efficiency and total yield
(grains + fruits) of 62% compared to single cultivation of annual spe-
cies and forest species.
Little attention has been given to the use of different arrange-
ments and forest species in agroforestry systems and the impacts
on understory microclimate conditions, as well as the effect of these
changes on the growth and yield of intercropping species. Thus, the
following hypothesis was generated: (a) radiation use efficiency,
growth and yield of bean and soybean grown in succession are mod-
ified by shading of different forest species (Peltophorum dubim and
Eucalyptus urograndis) and arrangements (6 m × 3 m and 12 m × 3 m)
in agroforestry systems. In order to meet this hypothesis, the present
study aimed to assess the radiation use efficiency, growth and yield
of bean and soybean grown in succession in the P. dubium and E. uro-
grandis understory in two arrangements of agroforestry and full sun.
2 | M ATE R I A L A N D M E TH O DS
2.1 | Study area and experimental design
Two field experiments were conducted in the 2017/2018 crop year,
bean in-season (September to January) and soybean off-season
(January to April) in the city of Frederico Westphalen, Southern
SGARBOSSA et al.
Brazil, under geographic coordinates of 27º23'48” S, 53º25'45” W
and altitude of 490 m above sea level. According to the Köppen cli-
mate classification system, the region's climate is Cfa, that is humid
subtropical, with an average annual temperature of 19.1ºC, ranging
between 0 and 38°C and a cumulative annual rainfall of 2,040 mm
(Alvares, Stape, Sentelhas, Gonçalves, & Sparovek, 2013). The soil of
the experimental area is classified as typical Entisol Orthents (Cunha
et al., 2011), with a pH in water of 5.2, 3.7 mg/kg of P (Mehlich),
93.7 mg/kg of K, 8.7 cmol/kg Ca, cation exchange capacity (CEC)
-1
of 16.8 cmolc kg , base saturation of 69.4% (V) and 3.3% organic
matter (OM). The soil was fertilized based on soil analysis and crop
recommendations for the studied region (CQFS, 2016).
The experimental design was a randomized complete block, ar-
ranged in a 2 × 2 factorial scheme with additional treatment, charac-
terized by two arrangements: Intercrop I and Intercrop II; two forest
species: Peltophorum dubium (Spr.) Taubert designated (P. dubium),
and Eucalyptus urophylla ST Blake × Eucalyptus grandis Hill ex Maiden
designated (E. urograndis); and full sun, with three repetitions. In
Intercrop I, the trees were distributed in rows spaced at 6 m and 3 m
between plants in the planting lines (Figure 1); bean and soybean
were distributed in 8 rows and arranged between tree rows, with
a total of 16 rows within the system. In Intercrop II, the trees were
spaced 12 m and 3 m between the plants; bean and soybean were
distributed in 30 rows arranged within the tree rows. In total, 18
trees were distributed in Intercrop I and 12 trees in Intercrop II for
each experimental unit.
Forest species seedlings were manually planted in September
2007, where the area was previously prepared by plowing and har-
rowing. During the experimental period, the trees were 11-year-old,
with the allometric characteristics shown in Table 1. Tree height
(H) was measured from the ground level to the top leaf axils using
F I G U R E 1 A sketch of an experimental
unit of the agroforestry systems (Intercrop
I and Intercrop II) and the full sun
system. Black circles represent the trees,
continuous lines indicate rows where the
annual crops (bean and soybean) were
sowed, the rectangles represent the
sample plots (P1, P2 and P3), black braces
indicate the spacing used between trees
in the planting line (3 m) and between the
rows of trees (6 m—Intercrop I and 12 m—
Intercrop II) and black arrows indicate the
minimum distance between the first row
of annual crops and the trees (1 m)
| 3
a Vertex II Hypsometer. Diameter of the canopy (DC) and diameter
at breast height (DBH) were measured by using a tape measure. The
DBH was measured at 1.30 m from the ground level. To determine
the average DC, vertical and horizontal measurements were made
thereof.
The bean in-season was sowed on 21 September 2017, with spac-
ing of 0.45 m between rows and population of 28.88 plants/m2. The
cultivar used was IPR Uirapuru, characterized by its undetermined
growth habit, erect gait, short guides and possibility of mechanical
harvesting. Soybean off-season was sowed on 3 January 2018, with
spacing of 0.45 m between rows and population of 15.55 plants/m2.
The cultivar used was TMG 7,062, characterized by its semi-deter-
mined growth habit, average gait and belonging to maturity group
6.2. Additionally, it should be noted that a plant population of 40%
lower than that recommended for cultivation was used. This decision
was based on preliminary studies conducted with soybean under ar-
tificial shading, in which the highest yields were obtained using 60%
of the recommended plant population (unpublished data).
2.2 | Meteorological conditions
Incoming solar radiation, air temperature (minimum, average and
maximum) and rainfall were obtained from an automatic meteoro-
logical station of the Brazilian Institute of Meteorology (INMET),
located approximately 1,500 m from the study site. Water balance
was run according to Thornthwaite and Mather (1955) approach at
a 10-day time step from September 2017 to April 2018, covering
the whole period for bean and soybean cultivation, considering a
soil water holding capacity (SWHC) of 80 mm. The SWHC was es-
timated considering the general soil characteristics (Doorenbos &
4 | SGARBOSSA et al.

TA B L E 1 Height (H), mean diameter of canopy (DC) and Where T = transmissivity rate (%); I = solar radiation incident
diameter at breast height (DBH) of Eucalyptus urograndis and inside of the agroforestry system (W/m2); and I 0 = solar radiation
Peltophorum dubium trees in two agroforestry systems (Intercrop I
incident outside the agroforestry system (W/m2). To estimate the
and Intercrop II) tested during the experimental period
transmissivity of the day, the average of the values obtained at each
DC DBH evaluation time was generated.
Species System H (m) (m) (cm)

E. urograndis Intercrop I 25.45 7.28 34.94

E. urograndis Intercrop II 28.16 8.96 38.34
P. dubium Intercrop I 19.20 4.38 12.86
P. dubium Intercrop II 20.60 5.30 15.72
Kassam, 1979): average SWHC for clayey soils of 2.0 mm/cm and
average values of effective depth of the crop root system (Alfonsi
et al., 1990) of 40 cm.
The bean cultivation period presented average air tempera-
ture of 20.8°C, ranging from 9.3°C to 34.6°C, average solar radia-
2 -1
tion flux of 20.8MJ/m day , accumulated rainfall of 649.4 mm and
accumulated water deficit of 10.4 mm (Figure 2). For the soybean
cultivation period, the average air temperature was 22.2°C, rang-
ing from 10.8°C to 33.2°C, average solar radiation flux of 19.2MJ/
2 -1
m day , accumulated rainfall of 578 mm and an accumulated water
deficit of 27.1 mm. Bean requires air temperatures between 10°C
and 35°C (Embrapa, 2012) and accumulated rainfall of 300–400 mm
(Embrapa, 2011), while soybean crop requires air temperatures be-
tween 20°C and 30°C and accumulated rainfall of 450–800 mm
(Embrapa, 2013). The water deficit observed in the bean cycle co-
incided with the physiological maturation period, not affecting the
growth, development, and yield of the crop. For soybean cultivation,
two periods with water deficit were observed, in the initial stages of
establishment of the crop and in the physiological maturation.
2.3 | Solar radiation transmissivity
The incident global solar radiation was measured using a pyranom-
eter (LYCOR PY 32,164) coupled with a Datalogger (LICOR 1,400).
The incident solar radiation was quantified outside and below the
trees of the agroforestry system, and measurements at 9, 10, 12, 14,
15 and 16 hr were collected at each evaluation point. The evalua-
tion points were selected in order to quantify the uneven incidence
of solar radiation in the understory of forest species, as follows:
1.45 m (P1), 2.35 m (P2) and 1.90 m (P3) away from the tree rows for
Intercrop I and 1.45 m (P1), 4.15 m (P2) and 2.80 m (P3) away from
the tree rows for Intercrop II. Therefore, at each evaluation time,
four measures were taken at each evaluation point. Measurements
were made on 10 October 2017 and 11 November 2017 for bean
and 15 February 2018 and 23 April 2018 for soybean, on typical
days for agrometerology. The transmissivity was calculated by the
following equation:
(I)
T= x100.
(I0)
2.4 | Radiation use efficiency
The radiation use efficiency (RUE) was calculated based on the
model proposed by Monteith (1977), in which RUE is a linear func-
tion between the produced dry matter and the intercepted photo-
synthetically active radiation, as follows:
TDM = RUE ∗ PARi
Where TDM = total dry matter produced (g/m2); PARi = intercepted
photosynthetically active radiation (MJ/m2).
The photosynthetically active intercepted radiation values
were calculated based on the model proposed by Varlet-Grancher
et al. (1989):
PARi = 0.95 ∗ (PAR) ∗ (1 − e( − k ∗ LAI)).
Where PAR = incident photosynthetically active radiation;
k = extinction coefficient, determined during the cycle of each crop;
and LAI = leaf area index. The LAI was determined by the relation-
ship between the leaf area (LA) and the soil area explored by the
plant (SA). PAR values were estimated to be 45% of incident global
solar radiation. This fraction represents the average of the values
found by Assis and Mendez (1989) for the studied region. To esti-
mate the global solar radiation incident on the understory of each
forest species and agroforestry arrangement, we considered cor-
rection factors for solar radiation transmissivity, as follows: 69.23%
(P. dubium Intercrop I), 79.19% (P. dubium Intercrop II), 57.94% (E. uro-
grandis Intercrop I) and 77.20% (E. urograndis Intercrop II) for bean
and 61.35% (P. dubium Intercrop I), 71.03% (P. dubium Intercrop II),
60.52% (E. urograndis Intercrop I) and 76.85% (E. urograndis Intercrop
II) for soybean.
2.5 | Plant growth evaluations
The bean emerged on 21 September 2017 and soybean on 9 January
2018. Growth evaluations were performed fortnightly, starting at
15 days after emergence (DAE). In this context, five growth evalua-
tions were performed during bean cultivation and six during soybean
cultivation. In each evaluation period, six plants were collected in
areas near the tree rows, in the north and south directions, as well
as in the centre of the alley. Afterwards, the samples collected in the
field were taken to the laboratory to separate the different compo-
nents: leaf, stem, branches, flowers, pods and senescent leaves, for
subsequent leaf disc preparation and determination of leaf area and
SGARBOSSA et al.
F I G U R E 2 Incoming solar radiation
(a), minimum, average and maximum air
temperature (b) and soil water holding
capacity and rainfall (c) (decendial base)
LAI, variables used to calculate growth rates and RUE. The leaves
were considered senescent when 50% or more of their leaf area was
dead or compromised.
After separation, the samples were placed in paper bags and kept
in a forced air circulation oven at 60°C until they reached the constant
mass. Subsequently, samples were weighed on a precision scale to
| 5
obtain the dry matter of each component, which together resulted in
the TDM. Based on the dry matter and leaf area results, the crop growth
analysis was performed. The calculated variables were as follows: abso-
lute growth rate (AGR), relative growth rate (RGR), net assimilation rate
(NAR), leaf weight ratio (RLW), leaf area ratio (LAR) and specific leaf area
(SLA), according to the methodology proposed by Benincasa (2003).
6 |
2.6 | Yield components
Bean harvest was performed on 19 December 2017, and soybean
harvest on 1 May 2018. Yield components were analysed by collect-
ing 10 plants randomly from each plot, selected on harvest day. The
criterion used for the selection of the sample plots was that they
should reliably represent the growth and development character-
istics of the total plants in the understory. Thus, these plots were
located near the tree rows in the north direction; centre of the alley;
and located near the tree rows in the south direction. The number of
pods per plant (NPP) and the number of grains per plant (NGP) were
determinated by counting. The grain weight per plant (GW) was eval-
uated by weighing on a precision scale. In order to evaluate the yield,
the total grains obtained in each evaluation plot were weighed by a
precision scale, the grain moisture was adjusted to 13%, and then,
the yield value was converted to kg/ha. When converting the yield
to kg/ha, the area occupied by the forest species was discounted,
being 33.33% of the area occupied by trees in Intercrop I and 15.67%
in Intercrop II. The relative yield was calculated by the ratio between
full sun yield and yield in each agroforestry arrangement and forest
species, according to the equation:
YAS
RY =
YM
Where RY = relative yield; YM = full sun yield; and YAS = agroforestry
yield for each agroforestry arrangement and forest species.
2.7 | Statistical analysis
Data were statistically analysed using software R (R Core Team, 2019)
and Statistical Analysis System (SAS, 2003). Data were initially ex-
amined for variance homogeneity and then subjected to analysis of
variance (ANOVA) to determine treatment effects and possible inter-
actions. Residues normality distribution was verified by the Shapiro–
Wilk test. For the yield and yield components of annual crops, when
significance was verified by the F test (p < .05), we compared the
means by the Tukey test (p < .05). These analyses were performed
SGARBOSSA et al.
F I G U R E 3 Average solar radiation
flux in the understory of two forest
species (E. urograndis and P. dubium) in
two agroforestry arrangements (Intercrop
I and Intercrop II) and in full sun, during
bean (a) and soybean (b) cultivation
(September-May)
using ExpDes (Ferreira, Cavalcanti, & Nogueira, 2018) package R soft-
ware (R Core Team, 2019). To analyse the yield of annual crops grown
in agroforestry systems in relation to full sun, we compared the means
by Dunnett's test (p < .05), in the SAS software (SAS, 2003).
In order to obtain an integrated analysis of the cultivation sys-
tems, the growth variables, productive performance and average
solar radiation flux were subjected to a multivariate approach, using
a principal component analysis (PCA). PCA was performed using
the means of the variables in each culture system and the tidyverse
(Wickham et al., 2019), factoextra (Kassambara & Mundt, 2020),
dplyr (Wickham, François, Henry, & Müller, 2020) and metan
(Olivoto & Lúcio, 2020) packages R software (R Core Team, 2019).
The PCA method reduces the dimensionality of the data with a large
number of measured variables, transforming them into a consider-
ably smaller new data set that has zero averages and one variance
at the beginning of the analysis, designated of principal components
(PCs). Each annual crop underwent a PCA.
The variables used in the PCA analysis were as follows: average
solar radiation flux (Flux), radiation use efficiency (RUE), absolute
growth rate (AGR), relative growth rate (RGR), net assimilation rate
(NAR), leaf weight ratio (RLW), leaf area ratio (LAR), specific leaf
area (SLA), number of pods plant-1 (NPP), number of grains plant-1
(NGP) and yield. Two PCs were selected considering all variables,
and two-dimensional (with two main components) ordering graphs
were made, in which the axes were designated as main component 1
(PC1) and main component 2 (PC2).
3 | R E S U LT S
3.1 | Dynamics of solar radiation
During the bean cultivation period, the highest values of average
solar radiation flux in agroforestry systems were obtained in the
P. dubium Intercrop II understory, followed by E. urograndis Intercrop
II, P. dubium Intercrop I and E. urograndis Intercrop I, respectively
(Figure 3a). Different responses were observed for the soybean cul-
tivation period, in which the highest values of average solar radiation
SGARBOSSA et al.
flux were found in the E. urograndis Intercrop II understory, followed
by P. dubium Intercrop II, P. dubium Intercrop I and E. urograndis
Intercrop I (Figure 3b).
3.2 | Plant growth
Similar patterns for absolute growth rate (AGR), relative growth rate
(RGR) and net assimilation rate (NAR) were observed in plant growth
up to 45 days after emergence, regardless of the cropping system,
coinciding with the end of the vegetative period and beginning of
the reproductive period of bean (Figure 4a–c). In general, the highest
values for AGR, RGR and NAR were verified for full sun and P. du-
bium Intercrop II. Analysing plant growth between agroforestry ar-
rangements, we observed superiorities in the average values of AGR
(33.05%), RGR (7.75%) and NAR (3.61%) for Intercrop II compared to
Intercrop I. Comparing the growth of bean plants in the understory of
the different forest species, higher average values of AGR (47.98%),
RGR (11.02%) and NAR (15.50%) were obtained for P. dubium.
Similar patterns were found for soybean cultivation (Figure 5a–
c). Higher values of AGR (141.83%), RGR (15.79%) and NAR (3.83%)
were observed for Intercrop II compared to Intercrop I. Comparing
the different forest species, higher AGR (41.01%), RGR (2.47%)
and NAR (2.49%) values were found in the understory of P. dubium
F I G U R E 4 Absolute growth rate (a),
relative growth rate (b), net assimilation
rate (c), leaf weight ratio (d), leaf area
ratio (e) and specific leaf area (f) of bean
cultivated in agroforestry systems and
under full sun
| 7
compared to E. urograndis. Leaf weight ratio (RLW), leaf area ratio
(LAR) and specific leaf area (SLA) decreased with increasing crop
age, regardless of the crop (Figures 4 and 5). The lowest values
were observed under full sun (RLW = 0.470 g/g and 0.467 g/g;
LAR = 0.018 m2/g and 0.013 m2/g; SLA = 0.036 m2/g and
0.026 m2/g, for bean and soybean, respectively), compared to the
average values found in the understory of agroforestry systems.
3.3 | Radiation use efficiency
The bean crop when conducted under full sun showed higher effi-
ciency in converting solar radiation to biomass (Figure 6a). Regarding
the different agroforestry arrangements and forest species, higher
RUE was observed in the understory of E. urograndis, Intercrop I.
During soybean cultivation, the highest radiation use efficiency was
also obtained under full sun (Figure 6b). When comparing agrofor-
estry systems, soybean plants conducted under Intercrop II arrange-
ment and the forest species E. urograndis presented the higher RUE.
It should also be noted that, regardless of the agroforestry arrange-
ment or forest species, when cultivated in an agroforestry system,
bean demonstrate greater stability and less variation for RUE val-
ues, with different levels of radiation. The same is not observed for
soybean.
8 |
3.4 | Yield traits
According to the analysis of variance (ANOVA), no significant ar-
rangement x species interaction was observed (Table 2). No signifi-
cant effect of arrangement and species for the variables number of
pods plant-1, number of grains plant-1 grain weight plant-1 were found
for bean crop. For the variables yield and relative yield, significance
was observed for the arrangement factor. When grown in agrofor-
estry systems, bean presented average number of pods plant-1 of 7.3,
-1 -1
average number of grains plant of 28.9 average grain weight plant
of 4.7 g (Figure 7).
SGARBOSSA et al.
F I G U R E 5 Absolute growth rate (a),
relative growth rate (b), net assimilation
rate (c), leaf weight ratio (d), leaf area ratio
(e) and specific leaf area (f) of soybean
cultivated in agroforestry systems and
under full sun
F I G U R E 6 Radiation use efficiency (g/
MJ) of bean (a) and soybean (b) cultivated
in agroforestry systems and under full
sun. RUE = radiation use efficiency,
PARai = accumulated intercepted
photosynthetically active radiation and
TDM = total dry matter produced
The highest values for yield and relative yield were observed in
Intercrop II, 40% higher than Intercrop I (Figure 8a,b). The ANOVA
showed significance for the yield of bean cultivated under full sun in
relation to agroforestry systems (Figure 8c), and the highest values
obtained under full sun. In general, bean grain yield in agroforestry
systems was 58.5% lower than full sun.
An interaction between arrangement x species for yield com-
ponents and yield of soybean was found. For the variables num-
ber of pods plant-1 and number of grains plant-1 , yield and relative
yield the lowest values were obtained for Intercrop I, when the
forest species E. urograndis was used (Figure 9). A similar trend
SGARBOSSA et al. | 9

TA B L E 2 Analysis of variance and

Relative
significance of the mean squares of the
Source of variation Yield Yield GW NGP NPP
sources of variation and coefficient of
variation (CV), of the yield traits of the Bean
bean and soybean Arrangements 348,253* 0.007* 0.883 92.593 0.0023
Species 40,679 0.008 1.502 39.725 1.687
* *
Arrangements*Species 70,145 0.014 0.8 35.021 2.224
Residuals 16,176 0.003 1.585 17.089 1.916
CV (%) 13.83 13.89 13.01 14.65 18.77
Soybean
Arrangements 188,797* 0.023* 6.193* 211.82* 66.898*
Species 1,270 0.0002 0.3815 7.389 0.926
* * * *
Arrangements*Species 102,284 0.013 7.896 228.959 52.780*
Residuals 13,097 0.001 0.761 34.428 45.698
CV (%) 29.81 30.06 27.18 31.21 26.53

Note: Traits: Yield (kg/ha); Relative Yield; GW: grain weight per plant (g); NGP: number of grains per
plant; and NPP: number of pods per plant.
*Significant effect by F test at 5% probability level.

F I G U R E 7 Yield components of bean

cultivated in agroforestry systems: (a)
number of pods per plant, (b) number of
grains per plant, (c) grain weight per plant.
ns
Not significant, based on F test (p < .05)

was observed for the grain weight plant-1 , in which the lowest systems was obtained in the E. urograndis understory under
were obtained for the Intercrop I arrangement and the forest Intercrop II, that is 38.40% higher than the P. dubium Intercrop
species E. urograndis. In general, the highest yield in agroforestry I understory, 63.78% higher than the P. dubium Intercrop II
10 | SGARBOSSA et al.
understory and 279.44% higher than the E. urograndis Intercrop
I understory.
The ANOVA also showed a significance for soybean yield under
full sun in relation to agroforestry systems (Table 2), and the high-
est averages were found under full sun (Figure 10). In general, the
yield values obtained for the E. urograndis Intercrop II, P. dubium
Intercrop I and P. dubium Intercrop II understory corresponded to
15.53% of the yield observed in full sun. The yield observed in the
E. urograndis Intercrop I understory corresponded to only 5.26%
of full sun.
3.5 | Principal component analysis
PCA analysis for bean showed that the primary and secondary
components accounted for, respectively, 73.4% and 18.6% of the
cumulative variation among all variables and cultivation systems
studied (Figure 11a). For soybean, we observed that the primary
and secondary components accounted for, respectively, 76.9% and
17.0% (Figure 11b). In this context, the PCA allowed an explanation
of more than 90% of the accumulated variance for both bean and
soybean crop systems. For bean crop, the PCA showed an inverse
relationship between the variables AGR, RGR, NAR and average
solar radiation flux with RLW, LAR and SLA, suggesting that shad-
ing tends to promote higher leaf production. Similarly, for soybean
crop, an inverse relationship was observed between the variables
F I G U R E 8 Yield (a) and relative
yield (b) of bean cultivated in different
agroforestry arrangements and yield
of bean cultivated in different cropping
systems (c). *Means followed by the
same letter do not differ by Tukey's test
(p < .05) (panel a and panel b). **Means
followed by the same letter do not differ
by Dunnett's test (p < .05) (panel c)
NAR, AGR and RUE with RLW. Regardless of the crop, the yield var-
iables were associated with greater availability of solar radiation.
4 | D I S CU S S I O N
4.1 | Dynamics of solar radiation
The greater interception of solar radiation by E. urograndis is ex-
plained by its larger canopy size compared to P. dubium. Besides
that, P. dubium trees have a deciduous behaviour (Carvalho, 2002).
During the bean cultivation period (especially at the beginning of the
cycle), P. dubium trees were still emitting new leaves, not reaching
maximum canopy density, promoting lower interception of radiation
by the tree canopy and justifying the greater solar radiation flux in
the understory compared to those values obtained in the understory
of E. urograndis (Figure 3a). However, during the conduction of soy-
bean, P. dubium trees presented higher canopy density and then in-
tercepted greater amounts of solar radiation similar to those levels
intercepted by E. urograndis trees (Figure 3b). The higher solar radia-
tion flux observed for Intercrop II is related to the greater distance
between the tree rows. Our results are in agreement with those
found by Caron et al. (2018), who studied the dynamics of solar ra-
diation in different arrangements (1.5 m × 6 m and 3 m × 12 m) of
agroforestry systems, and found that incident solar radiation was
82% higher for more open arrangements (3 m × 12 m).
SGARBOSSA et al.
F I G U R E 9 Yield components of
soybean cultivated in agroforestry
systems: number of pods per plant (a),
number of grains per plant (b), grain
weight plant-1 (c), relative yield (d) and
yield (e). *Means followed by the same
letter, lower case comparing arrangement
and upper case comparing species, do not
differ by Tukey's test (p < .05)
4.2 | Plant growth and solar radiation use efficiency
Reductions in absolute growth rates, relative growth rate and net
assimilation rate from 45 days after emergence are associated with
plant self-shading because the maximum leaf area index has been
reached (Figure 4 and Figure 5). On the other hand, from this pe-
riod there is the appearance of senescent leaves that contribute to
the reduction in rates, and consequently variations between the dif-
ferent cultivation environments. Similar results were observed by
Schwerz et al. (2018) who analysed sugarcane growth in different
agroforestry arrangements and full sun, and found that shading af-
fected the absolute growth rate and net assimilation rate of the crop.
Similarly, Yang et al. (2019) evaluating wheat growth in the Zizyphus
jujuba understory and under full sun, found a reduction in the abso-
lute growth rate of the crop due to shading, especially in the posi-
tions closest to the trees. The authors attribute these responses to
the reduced availability of solar radiation.
The lowest values of leaf weight ratio, leaf area ratio and specific
leaf area were observed for plants under full sun, especially from
| 11
45 days after emergence. Studies have shown that reductions in the
availability of solar radiation can lead to increases in leaf propor-
tions and dimensions of understory plants. These strategies are de-
veloped by plants to intercept and absorb more solar radiation due
to the increase in surface leaf (Bosi, Pezzopane, Sentelhas, Santos,
& Nicodemo, 2014; Schmidt, Caron, Pilau, Nardino, & Elli, 2017).
Changes in leaf size and plant growth due to reductions in solar
radiation availability resulted in different capacities to convert en-
ergy units into dry matter. Nassiri Mahallati, Koocheki, Mondani,
Feizi, and Amirmoradi (2015) analysing the radiation use efficiency
of bean cultivated in consortium with corn found values for RUE of
1.03 g/MJ and 0.86 g/MJ for the consortium and 0.95 g/MJ and
0.73 g/MJ for single cultivation. Similar responses were observed
for soybean grown in intercropping with corn, where values of RUE
1.65 g/MJ and 1.63 g/MJ were obtained for intercropping and of
1.55 g/MJ for single cultivation (Gao et al., 2010).
These responses were attributed to the metabolic character-
istics (C3) of bean and soybean which, under low solar radiation
intensity, showed reductions in photorespiration levels, making
12 | SGARBOSSA et al.

intercropping plants more photosynthetically efficient than those

conducted under high solar radiation intensity. However, the same
cannot be applied to the present study, since the radiation use ef-
ficiency was higher when the plants were cultivated under full sun.
(Figure 6). These results may be related to the reduced availability of
solar radiation in the understory of agroforestry systems, condition-
ing annual crops to light stress and thus limiting the ability of plants
to convert energy to dry matter.
Additionally, it should be considered that each plant has a min-
imum energy demand (solar radiation) to produce enough photoas-
similates to at least maintain the plant structures already formed,
called as trophic limit. On average the trophic limit of agricultural
crops is around 8.4 MJ/day (Fagan et al., 2010). Of the total pho-
toassimilates produced by the photosynthetic process, a fraction is
used as a substrate in the process of maintaining cell integrity, and
the excess is used for synthesis of specific components and their
incorporation into cell structures, resulting in biomass increment
(McCree, 1974; Thornley, 1970). Thus, the increase in plant bio-
mass is dependent on the amount of photoassimilates produced,
the amount of substrate used in the maintenance processes and the
efficiency with which the remaining substrate is converted to bio- F I G U R E 1 0 Yield of soybean cultivated in agroforestry systems
and under full sun. *Means followed by the same letter do not
mass (Machado & Pereira, 1990). Based on this information, it can be
differ by Dunnett's test (p < .05)
inferred that the average radiation flux in agroforestry systems was
very close to the trophic limit of the crops, which may have reduced
the metabolic activity of the crops and thus determined the reduc- systems, and obtained the lowest yield levels in a less spaced ar-
tions in RUE, mainly for soybean. rangement (6 m × 1.5 m) and under consortium with Eucalyptus.
Werner et al. (2017) studying the performance of four cultivars of
soybean intercropped with E. grandis and in different positions in the
4.3 | Yield responses understory, found reductions in the number of pods per plant, grain
weight and crop yield according to the proximity to the tree row.
According to ANOVA, bean yield was significantly influenced by the Another aspect that may have compromised soybean yield per-
arrangement used (Table 2). Shading significantly reduced crop yield, formance, especially when grown in the less spaced arrangements,
with values found in agroforestry systems corresponding to 41.5% was the competition imposed by tree roots for water and nutrients.
of full sun (Figure 8). Similar responses were obtained by Righi and Studies conducted with wheat (Wang et al., 2014; Zhang et al., 2013,
Bernardes (2008) who analysed the bean yield cultivated in the un- 2016), cotton (Zhang et al., 2019) and corn (Gao et al., 2017) iden-
derstory of rubber trees and found yield reductions for the plants tified reductions in root growth and spatial distribution due to
cultivated closer to the trees. On the other hand, Hadi, Ghassemi- intercropping. Duan et al. (2019), Zhang et al. (2014) and Zhang
Golezani, Khoei, Valizadeh, and Shakiba (2006) evaluating the re- et al. (2019) point out that although mutual root competition occurs
sponse of bean to different levels of artificial shading did not find between the different plant strata, the competitive capacity of the
a reduction in crop yield. Thus, it is possible to associate the yield forest species is much higher than that of the agricultural crop, and
values obtained in agroforestry systems, not only to the reduction it tends to increase with the proximity of tree rows and the age of
in solar radiation availability due to the intercropping but also to the planting.
spatiotemporal competition imposed by tree roots for water and nu- When analysing soybean yield in different cropping systems, the
trients. Despite the low yield, the value found in the present study highest averages were obtained in full sun (Figure 10). Sgarbossa
for bean cultivated in Intercrop II (1,090 kg/ha) was similar to the et al. (2018) evaluating the productive characteristics of soybean
average Brazilian yield during the first crop (2019/2020), which is grown in-season and in consortium with forest species and in a less
1,174 kg/ha (Conab, 2020), which makes the bean a potential alter- spaced arrangement (6 m × 1.5 m), also obtained the best responses
native of cultivation in agroforestry systems. under full sun. Studies carried out with wheat (Duan et al., 2019; Yang
The lowest values for number of pods plant-1, number of grains et al., 2019) and cotton (Zhang et al., 2019) have confirmed the re-
plant-1, grain weight plants-1, relative yield and yield for soybean duction in grain yield of agricultural crops as well as fruit production
(Figure 9) were obtained from E. urograndis Intercrop I understory. of forest species when grown in a consortium. However, the same
Similar responses were observed by Caron et al. (2018), which eval- authors observed increases in land-use efficiency (ratio between
uated the yield of soybean (in-season) cultivated in agroforestry the area needed to obtain in intercropping the same yield verified
SGARBOSSA et al. | 13

F I G U R E 1 1 Principal component
analysis of bean (a) and soybean (b)
cultivated in agroforestry systems and
under full sun. Black circles indicate the
cropping systems: P. dubium Intercrop
I (PI), P. dubium Intercrop II (PII), E.
urograndis Intercrop I (EI), E. urograndis
Intercrop II (EII) and full sun (FS). Brown
arrows indicate growth variables, blue
arrows indicate yield components, yield
(Y) and relative yield (RY), and black arrow
indicates mean solar radiation flux (Flux)

in an area in sole cropping) and total yield (grain + fruit) of 62% for
wheat + Juglans regia (Duan et al., 2019), 5% for wheat + Zizyphus
jujuba (Yang et al., 2019) and 25% for cotton + Zizyphus jujuba (Zhang
et al., 2019), thus demonstrating the productive viability of alterna-
tive cropping systems.
4.4 | Principal component analysis
The results presented in this study indicate that solar radiation flux,
growth characteristics, radiation use efficiency, and yields of annual
crop varied among cropping systems, particularly for soybean crop
(Figure 11a,b). In general, the principal component analysis showed
that the growth variables that consider the increase of plant dry mat-
ter over time, productive performance and radiation use efficiency
correlated positively to the environments with higher solar radiation
flux and less interspecific competition (Intercrop II).
The results found in this study are similar to those observed by
Pezzopane et al. (2020), who performed a multivariate PCA approach
of the growth characteristics, nutritional value and forage yield of
Urochloa brizantha at different positions in the Eucalyptus urograndis
understory, and found that increasing shading (positions closer to
the tree rows) promoted a reduction in forage production. Similarly,
Pezzopane et al. (2019) found that dry matter production of corn
grown in integrated systems was associated with greater availabil-
ity of solar radiation. PCA analysis also confirmed the occurrence
14 | SGARBOSSA et al.
of positive shading associations with leaf dimensions (LAR, SLA,
and RWL). When grown in agroforestry systems, the plants need to
develop acclimatization strategies to the environmental conditions.
Among these strategies, increases in leaf proportions and dimen-
sions are fundamental because they are intended to increase leaf
surface area and thus promote greater interception of solar radia-
tion, a limiting factor in these systems (Bosi et al., 2014; Schmidt
et al., 2017).
5 | CO N C LU S I O N S
Bean and soybean cultivation in agroforestry systems presented
reduced plant growth (AGR, RGR and NAR) and efficiency in con-
verting solar radiation to dry matter. When cultivated in shaded
environments, the crops developed morphological modifications in
order to acclimate the conditions of the environment, reflecting in-
creased leaf proportions and dimensions (RLW, LAR and SLA).
The yield of bean (in-season) crop was significantly influenced
by plant arrangement, and the highest yield was obtained under full
sun. However, because the average yield obtained in the Intercrop II
arrangement is similar to the average Brazilian bean yield under full
sun, bean cultivation in agroforestry systems can be recommended
for cultivation.
The productive performance of soybean (off-season) was sig-
nificantly influenced by the study factors (arrangements and for-
est species), and the lowest yield was obtained for Intercrop I and
E. urograndis species. However, due to the reduced yields obtained
in agroforestry systems, mainly due to the limitation by solar ra-
diation, further research should be conducted in order to study
more spaced arrangements and crop insertion in the early years
of agroforestry, in order to enable soybean cultivation in agrofor-
estry systems.
AC K N OW L E D G E M E N T S
The authors are grateful to the National Council for Scientific and
Technological Development (CNPq-Brazil), for the productivity
scholarship of the co-authors Braulio Otomar Caron (1D) and Denise
Schmidt (PQ2) and the Coordenation for Improvement of Higher
Education Personnel (Capes-Brazil) for their financial support of the
author Jaqueline Sgarbossa. Also, I would like to thank the members
of the Agrometeorology laboratory for the help in this project.
ORCID
Jaqueline Sgarbossa https://orcid.org/0000-0001-7541-090X
Elvis Felipe Elli https://orcid.org/0000-0001-9247-4956
Felipe Schwerz https://orcid.org/0000-0001-5266-4309
Claiton Nardini https://orcid.org/0000-0001-5791-6720
Fábio Miguel Knapp https://orcid.org/0000-0002-9964-1101
Denise Schmidt https://orcid.org/0000-0001-7228-7424
Alessandro Dal’Col Lúcio https://orcid.
org/0000-0003-0761-4200
Braulio Otomar Caron https://orcid.org/0000-0002-6557-3294
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How to cite this article: Sgarbossa J, Elli EF, Schwerz F, et al.
Bean–soybean succession under full sun and in agroforestry
systems: Impacts on radiation use efficiency, growth and
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