Morphology, Growth and Yield of Black Oats Cultivated in Agroforestry Systems in Southern Brazil

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Agricultural Systems 184 (2020) 102911

Contents lists available at ScienceDirect

Agricultural Systems
journal homepage: www.elsevier.com/locate/agsy

Morphology, growth and yield of black oats cultivated in agroforestry T


systems in southern Brazil

Jaqueline Sgarbossaa, , Elvis Felipe Ellib, Felipe Schwerzc, Claiton Nardinid, Edinéia de Cristoe,
Davi de Oliveiraf, Braulio Otomar Carone
a
Department of Crop Science, Federal University of Santa Maria, 97105-900 Santa Maria, Rio Grande do Sul, Brazil
b
Department of Biosystems Engineering, “Luiz de Queiroz” College of Agriculture (ESALQ), University of São Paulo (USP), 13418-900 Piracicaba, SP, Brazil
c
Department of Agricultural Engineering, Federal University of Lavras, 37200-000 Lavras, Minas Gerais, Brazil
d
Department of Forest Science, Federal University of Santa Maria, Frederico Westphalen Campus, 98400-000 Frederico Westphalen, Rio Grande do Sul, Brazil
e
Department of Agronomic and Environmental Sciences, Federal University of Santa Maria, Frederico Westphalen Campus, 98400-000 Frederico Westphalen, Rio Grande
do Sul, Brazil
f
Federal University of Santa Maria, Frederico Westphalen Campus, 98400-000 Frederico Westphalen, Rio Grande do Sul, Brazil

A R T I C LE I N FO A B S T R A C T

Keywords: Agroforestry systems have emerged in agriculture as a more sustainable alternative to food and energy pro-
Avena strigosa duction and environment conservation, characterized by the coexistence of two or more species in the same
Forest species cultivation area. Thus, this study aimed to assess the dynamics of solar radiation, radiation use efficiency, growth
Radiation use efficiency and productivity of black oats grown in agroforestry systems and in two crop years. For these ends, the study was
Solar radiation transmissivity
conducted in the field in southern Brazil, in two growing seasons (2017 and 2018). The studied species were:
Sustainability
Schizolobium parahybae, Peltophorum dubium, Parapiptadenia rigida, Eucalyptus urograndis. Samples were collected
at different points in the understory and parameters evaluated were: absolute and relative growth rates, net
assimilation rate, leaf weight ratio, leaf area ratio, specific leaf area, transmissivity of solar radiation, radiation
use efficiency, crude protein content and the productive performance of black oats. The dynamics of solar ra-
diation was modified by the canopy characteristics of the trees, with the highest transmissivity values obtained
in the understory of Parapiptadenia rigida. Higher levels of shading reduced growth and yield, increased the
radiation use efficiency, the number of stomata on the leaf surface and the crude protein content of black oats.
The productive performance of black oats was significantly influenced by the forest species and crop years, with
the highest productivity obtained in the P. rigida understory and in the crop year 2017. Based on the information
generated in this study, the cultivation of black oats under P. rigida is highly recommended.

1. Introduction Cultivation in integrated production systems is a widespread prac-


tice in some regions of the world, such as in sub-Saharan Africa and
Integrated agricultural production systems, such as agroforestry much of Latin America, where these systems are responsible for about
systems (AS), have emerged in agriculture as a sustainable alternative 20% of the world's food supply (Altieri, 2009; Chappell et al., 2013).
to production, characterized by the coexistence of two or more species Studies have identified that the adoption of this cultivation technique
in the same cultivation area (Bi et al., 2019). These systems are char- by farmers is also influenced by factors related to the agricultural
acterized by optimizing land use (Zhang et al., 2019a), improving soil characterization of the region, farm infrastructure, access to technical
structure (Duan et al., 2019) and increasing the organic matter content assistance, institutional support (Dhakal et al., 2012, 2015) and the
(Pardon et al., 2017), biological activity (Rivest et al., 2010) and carbon economic return of the activity (Phimmavong et al., 2019), not only to
sequestration (Sharma et al., 2016). Moreover, AS may favor the in- socio-environmental aspects.
clusion of marginalized areas into the production system, reducing the However, the simultaneous existence of two plant strata (upper -
need to explore new areas, favoring the expansion of agriculture and forest species and lower - annual species) in the same production area
the maintenance of existing biomes. may promote changes in the interaction of the plant community


Corresponding author.
E-mail addresses: sgarbossajs@yahoo.com (J. Sgarbossa), elvisfelipeelli@usp.br (E.F. Elli), felipe_schwerz@hotmail.com (F. Schwerz),
claitonnardini@live.com (C. Nardini), edineia_015@hotmail.com (E. de Cristo), davi2304@gmail.com (D. de Oliveira), otomarcaron@yahoo.com.br (B.O. Caron).

https://doi.org/10.1016/j.agsy.2020.102911
Received 16 March 2020; Received in revised form 15 July 2020; Accepted 20 July 2020
0308-521X/ © 2020 Elsevier Ltd. All rights reserved.
J. Sgarbossa, et al. Agricultural Systems 184 (2020) 102911

Table 1
Chemical composition of the soil of the experimental area in Southern Brazil.
Year pH (H2O) P (mg/L) K (mg/L) Ca (cmol/L) CTC (cmolc/L) V (%) OM (%)

2017 5.2 3.5 87.5 9.0 16.6 71.7 3.3


2018 5.4 6.7 115.5 9.7 19.3 67.9 3.5

(Sgarbossa et al., 2018), modifying the microclimate conditions of the Peltophorum dubium, Parapiptadenia rigida and Eucalyptus urograndis). In
understory. One of the main changes that occur in the AS understory is order to meet this hypothesis, the present study aimed to evaluate the
the reduction in the amounts of solar radiation. When intercepted by dynamics of solar radiation, radiation use efficiency, growth, number of
the canopy of trees, solar radiation may undergo quantitative and stomata, yield and crude protein content of black oats cultivated in
qualitative changes (Caron et al., 2014), depending on the angle of agroforestry systems in two crop years.
incidence of the sun's rays (Righi et al., 2007), canopy size, tree leaf
area index, canopy architecture (Pilau and Angelocci, 2015) and leaf 2. Materials and methods
geometry (Behling et al., 2016).
Some strategies can be used in order to mitigate the effects of the 2.1. Study area and experimental design
canopy of trees on solar radiation, such as the use of forest species with
adapted canopy size, architecture and leaf geometry. Sgarbossa et al. A field experiment was conducted in 2017 (May to September) and
(2018) studying the dynamics of solar radiation in the understory of 2018 (May to October), in the city of Frederico Westphalen, Southern
different forest species, observed a 41.5% superiority in the amounts of Brazil, on geographical coordinates of 27°23′48″ S, 53°25′45″ W and
solar radiation available in the understory of Peltophorum dubium (de- altitude of 490 m. According to the Köppen climate classification, the
ciduous plant) compared to the system cultivated with Eucalyptus region's climate is of the Cfa type, characterized by an average air
grandis. Similarly, Caron et al. (2019) studying the growth and pro- temperature of 19.1 °C, ranging from 0 to 38 °C and an average accu-
ductivity of dual-purpose wheat cultivated in the understory of dif- mulated annual rainfall of 2040 mm (Alvares et al., 2013). The soil in
ferent forest species found higher availability of solar radiation in the the experimental area is classified as Entisol Orthents (da Cunha et al.,
understory of Schizolobium parahyba, Parapiptadenia rigida and Pelto- 2011), with the chemical characteristics shown in Table 1.
phorum dubium (deciduous species) when compared to Eucalyptus The experimental design used was randomized blocks, distributed in
grandis. Thus, new studies must be conducted in order to identify the a 4 × 2 factorial, characterized by four forest species: Schizolobium
most appropriate forest species to compose the agroforestry systems, in parahyba (S. parahyba), Peltophorum dubium (Spr.) Taubert designated
order to generate the balance between the amounts of solar radiation (P. dubium), Parapiptadenia rigida (P. rigida) and Eucalyptus urophylla ST
intercepted by the canopy of the trees and the amounts transmitted to Blake x Eucalyptus grandis Hill ex Maiden (E. urograndis); and two crop
the understory. years 2017 and 2018, with three replications. The trees were dis-
Oats are one of the main winter crops grown in the world. In Brazil, tributed in rows spaced 6 m and 3 m between plants in the planting line
it stands out with the second most important winter crop, showing an (Fig. 1); the black oats were distributed in 25 lines between the tree
increase of 14% in the cultivation area from 2016 to 2017 harvesting rows, with a total of 50 lines per system. In total, 18 trees were dis-
years. In turn, the state of Rio Grande do Sul is responsible for more tributed in the agroforestry system.
than 70% of this production area (Conab, 2017). One of the main fac-
tors that have favored the expansion of the area of cultivation of oats is
2.2. Site history
the possibility of using forage for animal feed (Cassol et al., 2011;
Moreira et al., 2008).
The plant arrangement initially used was 6 × 1.5 m, that is, 6 m of
The insertion of pastures in the integrated production systems,
distance between tree rows and 1.5 m of distance between trees in the
provides forage of better quality and shade for the animals, reducing
planting line. This spacing was chosen based on information on the
stress during grazing (Cubillos et al., 2016). When grown under con-
relief and size of the farms in the region, which are characterized by
ditions of adequate water availability and fertilization, the biomass
more rugged relief and small farms, thus justifying the need for in-
production of the crops is dependent on the amounts of photo-
formation on the use of denser spacing. The forest species were planted
synthetically active radiation absorbed by the leaves and their ability to
manually in September 2007, and the area was previously prepared by
assimilate and convert solar radiation into photoassimilates. Thus,
plowing and harrowing. From the 1st to the 5th year of age of forest
when conducted in shaded environments, plants may show changes in
species, the trees were maintained in consortium with the crop of su-
morphology, growth, radiation use efficiency and consequently in
garcane. In the 6th year of age, the trees were kept in consortium with
productivity.
ryegrass. From the 7th to the 8th age, the trees were conducted in
Studies conducted in shaded environments have confirmed changes
consortium with soybean (summer) and wheat (winter). In the 9th year
in crop characteristics, such as an increase in crude protein content,
of age, a consortium between trees and corn was established (in-season
specific leaf area (Pezzopane et al., 2018), leaf proportion and a re-
and off-season).
duction in the proportion of senescent leaves (Pezzopane et al., 2019b)
In the first years of age, the trees had lower height, smaller diameter
of Urochloa brizantha, reductions in corn yield and forage production of
and smaller canopy size, resulting in less shade in the understory, as
Urochloa brizantha (Pezzopane et al., 2019a), reduced forage yield of
well as less competitive capacity with the intercropping crops.
Lolium multiflorum (Pilau et al., 2015), lower leaf area index and higher
However, with the advancement of age and the increase in the size of its
specific leaf area of Urochloa decumbens (Bosi et al., 2014).
structures, the conditions in the understory became limiting, especially
Little attention has been given in using different forest species in
with regard to the availability of solar radiation. Thus, in 2017, before
agroforestry systems and the impacts on the microclimate conditions of
the sowing of black oats, thinning and pruning of forest species was
the understory, as well as the effects of these changes on the growth and
carried out in order to increase the levels of solar radiation incident in
yield of black oats cultivated in consortium. Thus, the following hy-
the understory.
pothesis was generated: i) The dynamics of solar radiation, growth,
The criteria used for pruning trees were the maintenance of 50% of
morphology, yield and quality of black oats are modified by the shading
the green canopy and the removal of branches below the point where
promoted by different forest species (Schizolobium parahyba,
the tree trunk had a diameter of 6–8 cm (Nicodemo et al., 2016). For

2
J. Sgarbossa, et al. Agricultural Systems 184 (2020) 102911

Fig. 1. A sketch of an experimental unit of the agroforestry systems. Black circles represent the trees, dashed lines indicate where the oats was sowed, the rectangles
in gray represent the sample plots (P1, P2 and P3) and black arrows indicate the spacing used between trees in the planting line (3 m) between the rows of trees (6 m)
and the minimum distance between the first row of black oats and the trees (1 m).

thinning, it was opted to increase the spacing between plants in the axils using a Vertex II Hypsometer. DC and DBH were measured by
planting line from 1.5 m to 3.0 m. Thus, the plant density was reduced using a tape measure. The DBH was measured at 1.30 m from the
from 1111 trees ha−1 to 555 trees ha−1. The realization of these sil- ground level. To determine the average DC, vertical and horizontal
vicultural practices was based on a series of data on transmissivity of measurements were made thereof.
solar radiation and on the understanding that the reduced levels would
restrict the growth and development of annual crops. 2.3. Black oats (Avena strigosa)
During the experimental period, the trees were 10 (2017) and 11
(2018) years old, with the allometric characteristics shown in Table 2. The cultivation system implemented in the experimental area is no-
The height (H), diameter at breast height (DBH), and diameter of the tillage, in which the black oats were inserted in a crop rotation plan
canopy (DC) of the forest (tree) species were evaluated in 2017 and characterized by the cultivation of bean (in-season) and soybean (off-
2018. Tree height was measured from the ground level to the top leaf season) in the summer and black oats in the winter. The black oats were
sown on May 1, 2017 and May 5, 2018, with a spacing of 0.16 m be-
Table 2 tween rows and a population of 450 plants m−2. The cultivar used in
Height, diameter of canopy (DC) and diameter at breast height (DBH) of S. the two crop years was “UPFA 21 - Moreninha”, characterized by an
parahyba, P. dubium, P. rigida and E. urograndis in 2017 and 2018. erect growth habit, showing sharp edges, being moderately resistant to
Species Crop year Height (m) DC(m) DBH (cm) leaf rust, resistant to barley yellow dwarf virus (BYDV), susceptible to
rust and moderately frost-tolerant. The fertilization was performed
S.parahyba 2017 16.24 4.70 20.46 based on soil analysis considering the recommendation for the black
2018 19.38 4.98 22.45
P.dubium 2017 14.02 4.53 11.97
oats (CQFS, 2016).
2018 19.21 4.41 12.86
P.rigida 2017 13.83 5.49 14.11 2.4. Weather conditions
2018 18.48 6.16 14.90
E.grandis 2017 20.81 6.70 30.55
2018 24.98 8.22 34.94 The data of incident global solar radiation, air temperature
(minimum, average and maximum) and accumulated rainfall were

3
J. Sgarbossa, et al. Agricultural Systems 184 (2020) 102911

Fig. 2. Average solar radiation flux (2017 – A and 2018 – B); minimum, average and maximum air temperature (C – 2017 and D – 2018); soil water holding capacity
and rainfall (E – 2017 and F – 2018) (decendial base). Black arrows indicate the data of emergence and harvest of black oats.

obtained from the automatic meteorological station linked to the 15.9 °C, ranging from 0.7 °C to 33.7 °C, an average solar radiation of
National Meteorological Institute (INMET), located approximately 12.31 MJ m−2 day−1, an accumulated rainfall of 640.6 mm and ac-
1500 m from the study. The water balance was performed according to cumulated water deficit of 12.6 mm. Black oats require temperatures
the approach of Thornthwaite and Mather (1955), in an 10-days time between 0 °C and 35 °C (Leite et al., 2012) for some growth and de-
step, from May 2017 to September 2017 and from May 2018 to October velopment to occur. Therefore, during 2017, there were values of ab-
2018, covering the entire period of cultivation of black oats, in the two solute minimum temperature lower than that required by the crop on
crop years and, considering the soil water holding capacity in the the 18th and 19th of July, coinciding with the occurrence of strong
(SWHC) of 80 mm (Doorenbos and Kassam, 1994). The SWHC was frosts. However, no visual damage was observed due to the occurrence
estimated considering the general characteristics of the soil (Alfonsi of these events.
et al., 1990): Average SWHC for clayey soils of 2.0 mm cm−1; and ef-
fective root depth of 40 cm.
2.5. Solar radiation transmissivity
During the cultivation of black oats in 2017, an average air tem-
perature of 17.2 °C was observed, ranging from −1.6 °C to 33.7 °C, an
The incident global solar radiation was measured using a pyr-
average solar radiation flux of 11.8 MJ m−2 day−1, accumulated pre-
anometer (LYCOR PY 32164) coupled with a Datalogger (LICOR 1400).
cipitation of 980.4 mm and accumulated water deficit. 23.6 mm
The incident solar radiation was quantified outside and below the trees
(Fig. 2). For cultivation period in 2018, the average air temperature was
of the agroforestry system (Fig. 1). Measurements were made on June

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J. Sgarbossa, et al. Agricultural Systems 184 (2020) 102911

12, July 12 and August 7 in 2017 and on June 19, July 21 and August “Anati Quanti”.
20 in 2018, at 9, 10, 12, 14 and 15 h. Therefore, at each evaluation
time, four measures were taken. The solar radiation transmissivity was 2.8. Yield variables
calculated by the following equation:
The black oats were harvested on September 14 in 2017 and on
(I)
T= x 100 October 5 in 2018. The yield components were analyzed by collecting 3
(I0 )
lines (samples) of 1 m, which were selected on the day of harvest. The
where, T = transmissivity (%); I = solar radiation incident inside of the number of panicles (NP) per linear meter and the number of grains (NG)
agroforestry system (W m−2); I0 = solar radiation incident outside the per panicle were determined. Panicle length (PL) was measured with
agroforestry system (W m−2). the aid of a graduated ruler. Panicle dry matter (PDM) and 1000-grain
dry matter (GDM) were determined by weighing with the aid of a
2.6. Radiation use efficiency precision scale, the grain moisture was adjusted to 13% and then the
yield value was converted to kg ha−1. The crude protein content (% CP)
The radiation use efficiency (RUE) was calculated based on the was determined by the Kjeldahl method, through the determination of
model proposed by Monteith (1977), in which RUE is a linear function total nitrogen, in acid digestion by sulfuric acid (AOAC, 2005). With the
between the produced dry matter and the intercepted photo- values of the percentage of nitrogen, they were multiplied by the cor-
synthetically active radiation, as follows: rection factor 6.25 according to the methodology of Galvani and
Gaertner (2006).
TDM = RUE∗PARi
where, TDM = total dry matter produced (g m−2); PARi = intercepted 2.9. Statistical analysis
photosynthetically active radiation (MJ m−2).
The photosynthetically active intercepted radiation values were Data were statistically analyzed using software R (R Core Team,
calculated based on the model proposed by Varlet-Grancher et al. 2019). Data were initially examined for variance homogeneity and then
(1989): subjected to analysis of variance (ANOVA) to determine treatment ef-
PARi = 0.95 ∗ (PARinc) ∗ (1 − e(−k ∗ LAI)) fects and possible interactions. Residual normality distribution was
verified by the Shapiro-Wilk test. For the yield and yield components of
where, PARinc = incident photosynthetically active radiation; k = ex- black oats, when significance was verified by the F test (p < .05),
tinction coefficient, determined during the cycle of each crop; means were compared by the Skott Knott test (p < .05).
LAI = leaf area index. The LAI was determined by the relationship
between the leaf area (LA) and the soil area explored by the plant (SA). 3. Results
PARinc values were estimated to be 45% of incident global solar ra-
diation. This fraction represents the average of the values found by de 3.1. Tree characteristics and dynamics of solar radiation
Assis and Mendez (1989) for the studied region.
For all growth variables measured, the highest values were observed
2.7. Plant growth and morphological evaluations for the species E. urograndis. In general, considering the two crop years,
E. urograndis showed higher values for height (36%), canopy diameter
The black oats emerged on May 06 2017, and on May 13, 2018. (49.66%) and diameter at breast height (114%), compared to the other
Growth evaluations were performed fortnightly, starting at 15 days forest species (Table 2). These differences in the growth characteristics
after emergence (DAE). From this, eight growth evaluations were per- of forest species resulted in different amounts of solar radiation incident
formed in 2017 and seven in 2018. In each evaluation period, the plants in the understory. During 2017, the highest values of transmissivity
were collected in the field and taken to the laboratory to separate the were observed for P. rigida (73.71%), being 19.41% higher compared to
different components: leaf, stem, inflorescence, panicles and senescent E. urograndis, 44.30% to P. dubium and 57.03% to S. parahyba. In 2018,
leaves, for subsequent leaf disc preparation and determination of leaf the highest values of transmissivity were also observed for P. rigida
area and LAI, variables used to calculate growth rates and RUE. The (74.21%), which were 6.7% higher compared to P. dubium, 10.48% to
leaves were considered senescent when 50% or more of their leaf area S. parahyba and 44.38% to E. urograndis (Fig. 3).
was dead or compromised. The values obtained for transmissivity resulted in changes in the
After separation, the samples were placed in paper bags and kept in average flux of solar radiation in the understory of forest species. In
a forced air circulation oven at 60 °C until they reached the constant 2017, the highest average solar radiation flux 8.95 MJ m−2 day−1 was
mass. Subsequently, samples were weighed on a precision scale to ob- obtained in the P. rigida understory, followed by E. urograndis
tain the dry matter of each component, which together resulted in the (7.50 MJ m−2 day−1), P. dubium (6.20 MJ m−2 day−1) and S. parahyba
TDM. Based on the dry matter and leaf area results, the crop growth (5.70 MJ m−2 day−1), respectively. Similar responses were observed in
analysis was performed. The calculated variables were: absolute growth 2018, in which the highest average solar radiation flux
rate (AGR), relative growth rate (RGR), net assimilation rate (NAR), 9.14 MJ m−2 day−1 was found in the P. rigida understory, followed by
leaf weight ratio (RWL), leaf area ratio (LAR) and specific leaf area P. dubium (8.56 MJ m−2 day−1), S. parahyba (8.27 MJ m−2 day−1) and
(SLA), according to the methodology proposed by Benincasa (2003). E. urograndis (6.33 MJ m−2 day−1).
Additionally, stomatal evaluations were carried out at the end of the
vegetative period and the beginning of the reproductive period of oat 3.2. Plant growth and morphological characteristics
plants. For these evaluations, the third leaf completely expanded from
the apex to the base was removed. Semi-permanent slides were made Different availability of solar radiation in the understory of each
from the impression of the abaxial and adaxial epidermis of the leaf, forest species, resulted in changes in growth and in the morphological
using cyanoacrylate ester adhesive, a technique such as imprints characteristics of black oat plants. During 2017, the highest LAI values
(Campos et al., 2009; Weyers and Johansen, 1985). The leaves were were found for plants grown in the understory of S. parahyba; 1.94%
pressed for approximately 30 s over the drop of adhesive on the slide, higher compared to P. dubium, 17.23% to P. rigida and 80.73% to E.
allowing the epidermis to remain in print. The slides were viewed under urograndis (Fig. 4A). Similar responses were observed in 2018, i.e., the
an appropriate fotwarer microscope. The stomata were counted using highest LAI values were obtained in the understory of S. parahyba;
the quantitative analysis software axle for studies of plant anatomy 2.05% higher compared to P. dubium, 10.67% to P. rigida and 29.69% E.

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J. Sgarbossa, et al. Agricultural Systems 184 (2020) 102911

crop year. The same was not observed for the leaf weight ratio, with the
lowest values observed for P. dubium (0.4958 g g−1) in 2017 and S.
parahyba in 2018 (0.4819 g g−1).
According to the analysis of variance (ANOVA) there was no crop
year x species interaction, for the total number of stomata, number of
stomata on the leaf's abaxial and adaxial surfaces. When analyzing the
main effects, significance was observed for the crop year factor. Thus,
for all morphological variables analyzed, the highest values were ob-
served in 2017, which were 32.29% higher for the total number of
stomata, 41.08% for the number of stomata on the leaf adaxial surface
and 22.95% for the number of stomata on the leaf's abaxial surface, in
relation to 2018 (Fig. 7).

3.3. Radiation use efficiency

Black oats were more efficient in converting solar radiation into


biomass when conducted under higher levels of shade, regardless of the
crop year. In 2017, the highest value of RUE was obtained in the un-
derstory of S. parahyba (6.53 MJ m−2), being 6.52% higher than that
observed for P. dubium, 49.77% for E. urograndis and 58.49% for P.
Fig. 3. Average transmissivity of solar radiation in the understory of four forest rigida (Fig. 8A). In 2018, the highest RUE was observed in the E. uro-
species (S. parahyba, P. dubium, P. rigida and E. urograndis), during the black grandis understory (6.66 MJ m−2), 20.65% higher than for P. dubium,
oats cultivation period in 2017 and 2018. 22.88% for S. parahyba and 33.47% for P. rigida (Fig. 8B). On the other
hand, in the two crop years, the lowest values of RUE were obtained in
the P. rigida understory (2017 = 4.12 MJ m-2 and 2018 = 4.99 MJ m-
2
), coinciding with the highest transmissivity levels.

3.4. Yield traits

According to ANOVA there was no significant crop year x species


interaction. For the variables NP, PL, PDM, NG and yield, significance
was observed for the crop year factor (Table 3). For the variables PL,
PDM, GDM and yield, significance was verified for the species factor.
When analyzing the productive performance of black oats between crop
years, superiority was found for NP (63.74%) and yield (39.60%) for
2017 compared to 2018. For the other variables, superiority was ver-
ified in 2018 (PL = 15.27%, PDM = 16.90% and NG = 17.23%).
When comparing the productive performance of black oats between
forest species, the highest values of PL (17.981 cm), PDM (0.366 g),
GDM (14.487 g) and productivity (1118.870 kg ha−1) were observed in
the P. rigida understory.

3.5. Crude protein

According to ANOVA, there was a significant crop year x species


interaction for the crude protein (CP) content of black oats grown in
agroforestry systems. The highest CP contents were obtained in 2018,
with an average of 5.14% higher than the 2017 (Fig. 9). In 2017, the
highest CP content was observed in the understory of S. parahyba
(26.01%), 5.01% higher than E. urograndis, 5.23% higher than P. du-
bium and 10.88% higher than P. rigida. In 2018, the highest CP content
was obtained in the E. urograndis understory (28.03%), being 5.26%
higher than S. parahyba, 7.08% higher than P. rigida and 11.39% higher
than P. dubium. It is also interesting to highlight that, regardless of the
crop year, the highest CP levels were observed under the highest levels
Fig. 4. Leaf area index of black oats cultivated in the understory of four forest of shading.
species (S. parahyba, P. dubium, P. rigida and E. urograndis) in 2017 (A) and 2018
(B). 4. Discussion

urograndis. 4.1. Dynamics of solar radiation


The highest values of absolute growth rate, relative growth rate and
net assimilation rate were observed in the understory of P. dubium, for The dynamics of solar radiation varied according to the canopy
2017 and P. rigida for 2018 (Figs. 5 and 6). In general, for the variables characteristics of the trees and the crop year. However, for both crop
leaf area ratio and specific leaf area, the lowest averages were obtained years, the highest values of transmissivity were obtained in the P. rigida
for plants grown in the understory of E. urograndis, regardless of the understory (Fig. 3). These responses can be attributed to the different
growth characteristics of each forest species. P. rigida, for example, is a

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J. Sgarbossa, et al. Agricultural Systems 184 (2020) 102911

Fig. 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 black oats
cultivated in the understory of four forest species (S. parahyba, P. dubium, P. rigida and E. urograndis) in 2017.

deciduous species, which experiences leaf fall in the autumn/winter 4.2. Plant growth and morphological characteristics
period (Carvalho, 2002a), resulting in greater availability of solar ra-
diation in the understory during this period. Although S. parahyba and Variations in the amounts of solar radiation incident inside the
P. dubium also show a deciduous behavior (Carvalho, 2002b; de Souza understory, modified the growth characteristics of black oats. For both
et al., 2003), the process of leaf senescence started later, compared to crop years, the lowest values of LAI, AGR, RGR, NAR, RWL, LAR and
the trees of P. rigida. Caron et al. (2019) studying the growth and yield SLA were obtained under higher levels of shading, especially in the E.
of dual-purpose wheat in the understory of S. parahyba, P. dubium, P. urograndis understory. Generally, when conducted in shaded environ-
rigida and E. grandis point out that at the beginning of the annual crop ments, plants tended to experience increases in leaf proportions and
cycle, deciduous trees had fewer leaves, favoring the transmissivity to dimensions (RWL, LAR and SLA), these strategies are developed in
the understory, however, at the end of the crop cycle, trees already order to intercept and absorb greater amounts of solar radiation, due to
showed the formation of a denser canopy, resulting in lower trans- the increase in leaf surface (Bosi et al., 2014; Schmidt et al., 2017),
missivity values. In addition, it is interesting to highlight that for all however, the same was not observed in the present study (Figs. 4, 5 and
forest species the highest values of transmissivity were obtained in 6). These responses can be attributed to the existing correlation be-
2017, except for E. urograndis. This response can be attributed to the tween the transmissivity of solar radiation and the growth of plants,
thinning and pruning practices carried out before the sowing of black which suggests that in shaded environments and in the absence of water
oats, in 2017, causing less interception of solar radiation by the canopy restriction, reductions of more than 30% in transmissivity can impair
of E. urograndis trees in this period. the growth and development of the culture in understory (Pezzopane
et al., 2019a).

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J. Sgarbossa, et al. Agricultural Systems 184 (2020) 102911

Fig. 6. 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 black oats
cultivated in the understory of four forest species (S. parahyba, P. dubium, P. rigida and E. urograndis) in 2018.

Deiss et al. (2014b) analyzing the growth of oats intercropped with radiation, also reduced the rate of liquid photosynthesis and the dry
Eucalyptus dunni, observed reductions in the relative growth rate of the mass of plants, in addition to competing with agricultural crops for
crop, according to the proximity of the rows of trees and consequently other resources in the environment.
an increase in the intensity of shading. There were also changes in the For the morphological characteristics, the total number of stomata
LAI for dual-purpose wheat (Caron et al., 2019), Urochloa brizantha and the number of stomata on the adaxial and abaxial surfaces of the
(Bosi et al., 2014) and corn (Nardini et al., 2019) and Urochloa brizantha leaf, the largest amounts of stomata were verified in 2017 (Fig. 7),
SLA (Gomes et al., 2019) when grown in agroforestry systems. Simi- coinciding with the period of lower average solar radiation. The in-
larly, Yang et al. (2019) evaluating the growth of wheat in the un- crease in the number of stomata may be related to the need for plants to
derstory of Ziztphus jujuba, found a reduction in the absolute growth capture greater amounts of atmospheric CO2, in order to increase
rate of the crop, due to shading, especially in the positions closest to the photosynthetic efficiency (Castro et al., 2010). Furthermore, the in-
trees. The authors attribute these responses to the limitations imposed crease in stomata quantities is characterized as a strategy developed by
by the forest species, which by reducing the availability of solar plants in order to maintain the CO2 influx necessary for metabolic

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J. Sgarbossa, et al. Agricultural Systems 184 (2020) 102911

higher dry matter. Plants grown under higher intensity of solar radia-
tion (P. rigida), even with lower efficiency in the use of energy units
(MJ m−2), showed higher accumulation of dry matter per unit area.
These responses are related to the greater availability of solar radiation
under the canopy of plants in the understory of P. rigida, which despite
being less efficient in conversion, had greater amounts of this element,
allowing greater accumulation of dry matter.

4.3. Yield traits and crude protein

As well as the growth characteristics and the radiation use effi-


ciency, the productive performance of black oats was influenced by the
forest species and crop years (Table 3). In general, for the variables PL,
PDM and NG the highest values were obtained in 2018. The same was
not observed for NP and grain yield. These results are related to the
greater tillering observed in 2017, which influenced the production of
panicles per linear meter, as well as, contributed significantly to obtain
higher grain yield in this crop, due to persistence of tillers determining
the quantity of panicles to be harvested (Deiss et al., 2014a; Nicodemo
Fig. 7. Total number of stomata and number of stomata on the adaxial and
et al., 2016).
abaxial surface of black oats cultivated in agroforestry in 2017 and 2018.
Another aspect observed about the productive performance of black
oats is that for most of the variables analyzed, the best responses were
activities, preventing that in conditions of less availability of solar ra- obtained in the understory of the forest species P. rigida, coinciding with
diation, such as the 2017, reductions in photosynthesis occur (Batagin the highest levels of solar radiation. Deiss et al. (2016) studying the
et al., 2009). grain yield of oats grown in an agroforestry system with Eucalyptus and
Changes in plant growth and morphological characteristics due to in different points of the understory, found reductions in the number of
reductions in the availability of solar radiation, resulted in differ- spikelets per panicle and grain productivity in the positions closest to
entiated capacities in converting energy units into dry matter, with the the row of trees. Similar results were observed by Nicodemo et al.
highest efficiency values in the use of solar radiation obtained under (2016) that when cultivating oats in consortium with native trees, they
higher levels of shading, regardless of the crop year (Fig. 8). These also verified reductions in dry matter production, number of grains
results corroborate those reported for corn (6.5 g MJ-1 and 3.7 g MJ−1) plant−1, number of grains planicle−1 and dry matter of grains−1, at the
(Nardini et al., 2019) and wheat (6.24 g MJ−1 and 1.12 g MJ−1) (Caron points closest to the rows of trees. Solar radiation is the primary source
et al., 2019), grown in agroforestry systems, in which the highest RUE of energy for the photosynthetic process, so the lower productive per-
values were obtained under lower radiation availability. These re- formance of black oats observed under higher levels of shading may be
sponses can be attributed to the metabolic characteristics (C3) of the related to reductions in photosynthetic rates and CO2 assimilation of
crop, which under the low intensity of solar radiation shows reductions the crop under these conditions (Soares et al., 2016), reflecting less
in the levels of photorespiration, making plants in intercropping more accumulation of photoassimilates and less availability for grain for-
efficient photosynthetically than those conducted under higher in- mation.
tensities of solar radiation (Gao et al., 2010). In addition, some strategies can be adopted in order to increase the
However, it should be noted that the greater efficiency in the use of yield of black oats in agroforestry systems, such as the insertion of the
solar radiation verified under higher levels of shading, is related to the crop in the initial years of agroforestry installation and the use of more
greater efficiency of oat plants when converting a unit of solar radiation widely spaced agroforestry arrangements, which would result in less
into dry matter, in this condition, but not necessarily these plants had competitive capacity of forest species and greater availability of solar

Fig. 8. Radiation use efficiency (RUE = g MJ−1) of black oats cultivated in the understory of four forest species (S. parahyba, P. dubium, P. rigida and E. urograndis) in
2017 (A) and 2018 (B).

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J. Sgarbossa, et al. Agricultural Systems 184 (2020) 102911

Table 3
Productive performance of black oats cultivated in the understory of four forest species (S. parahyba, P. dubium, P. rigida and E. urograndis) in 2017 and 2018.
Study factors Number of panicles Panicle lenght Panicle dry matter Number of grains 1000 - grain dry matter Yield

(linear meters) (cm) (g) (panicle) (g) (kg ha−1)

Forest species
S. parahyba ns 18.960 ± 1.912 a 0.268 ± 0.039 b ns 8.52 ± 1.790 c 632.985 ± 144.157 c
P. dubium ns 18.115 ± 1.828 a 0.303 ± 0.062 b ns 11.340 ± 2.049 b 852.489 ± 182.631 b
P. rigida ns 17.981 ± 1.853 a 0.366 ± 0.056 a ns 14.487 ± 1.486 a 1118.870 ± 312.949 a
E. urograndis ns 15.742 ± 2.144 b 0.269 ± 0.053 b ns 12.366 ± 2.736 b 813.868 ± 177.198 b

Crop years
2017 136.127 ± 12.917 a 16.444 ± 2.093 b 0.278 ± 0.055 b 16.542 ± 2.484 b ns 995.789 ± 262.068 a
2018 83.137 ± 6.062 b 18.955 ± 1.453 a 0.325 ± 0.066 a 19.392 ± 2.705 a ns 713.315 ± 192.310 b

*Means followed by the same letter in the column, do not differ from each other, by the Scott Knott test, at 5% probability of error.
ns Not significant for the F test at 5% probability of error.

withthose observed by Kirchner et al. (2010) evaluating the forage


quality of Avena sativa and Avena strigosa cultivated in consortium with
Pinnus taeda, who found that under transmissivity of solar radiation
below 60%, increases in CP levels of both species occured. In general,
these responses have been related to the delay in the ontogenetic de-
velopment of plants grown under shade, in relation to those grown
without restriction, or under moderate levels of solar radiation
(Tiedemann et al., 1971). However, this delay in development can lead
to confusion in understanding the direct effects of shading on the
quality of the material produced, since with the advance of the crop
cycle, the proportions of non-fibrous carbohydrates, nutrients and
protein levels are changed, silica, lignin and fibers, variables that ef-
fectively determine the nutritional value of forage (Masuda, 1977).
The information generated in this study on growth, morphology,
productivity and quality, allows us to affirm that the cultivation of
black oats in agroforestry systems appears as a promising alternative to
the sustainability of agricultural systems, instigating the development /
disclosure of public policies that encourage this new model production
of black oats, which in addition to favoring the maintenance of existing
Fig. 9. Crude protein content of black oats cultivated in the understory of four biomes, can reduce the exploitation of new areas and enable partial
forest species and (S. parahyba, P. dubium, P. rigida and E. urograndis) in 2017 reforestation of agricultural areas. In this context, the following stand
and 2018. out: Brazilian law No. 12,621, of May 25, 2012, which establishes the
* Means followed by the same letter, lower case comparing forest species and new forest code, allowing small farmers to install agroforestry systems
upper case comparing crop years, do not differ by Skott Knott test at 5% in permanent preservation areas and legal reserves, as long as these
probability of error. systems are subject to the sustainable management plan and the
greenhouse gas emission reduction program. This program provides
radiation within the understory. Caron et al. (2018), Schwerz et al. financial resources for the adoption of sustainable production technol-
(2019) and Elli et al. (2016) observed that the use of more spaced ar- ogies, committed to the reduction of greenhouse gas emissions and
rangements promotes an increase in the availability of solar radiation to greenhouse effect in the Brazilian agricultural sector.
the understory, resulting in increases in crop productivity in con-
sortium. In its turn, Duan et al. (2019), Zhang et al. (2014) and Zhang
5. Conclusions
et al. (2019b) point out that although mutual root competition occurs
between the different plant strata, the competitive capacity of the forest
The dynamics of solar radiation is modified by the canopy char-
species is much higher than that of the agricultural crop, and it tends to
acteristics of the trees, with the highest transmissivity values obtained
increase with the proximity of tree rows and the age of planting.
in the understory of P. rigida. Higher levels of shading reduced growth
Different availability of solar radiation impacted significant varia-
and yield, increased the radiation use efficiency, the number of stomata
tions in CP levels (Fig. 9). When comparing the CP between crop years,
on the leaf surface and the crude protein content of black oats.
the highest values were obtained in 2018. Generally, higher levels of CP
The productive performance of black oats was significantly influ-
observed in agroforestry systems may be associated with the more
enced by the study factors, with the highest yield values obtained in the
significant mineralization of organic matter in the soil, since most of the
P. rigida understory. Based on the information generated in this study,
benefits of systems integrated in the levels of CP are related to the
the cultivation of black oats in the understory of P. rigida is highly re-
improvement of soil fertility (Barro et al., 2008; Paciullo et al., 2007;
commended.
Pandey et al., 2011). This factor, associated with the practice of thin-
This study made it possible to identify positive growth and yield
ning of forest species in the first crop (2017), coincides with the lower
responses of black oats grown in less sparse agroforestry systems
degradation of plant material removed from trees and partially de-
(3 m × 6 m) and intercropped with 10 and 11-year-old trees. Thus, in
posited in the soil, resulting in lower levels of CP in this period. Similar
order to enhance the recommendation of this cultivation model, new
responses were observed by Pezzopane et al. (2019a).
studies should be developed in order to analyze the performance of the
In contrast, higher levels of shading resulted in higher levels of CP,
black oats in the early years of installation of agroforestry (young trees)
regardless of the crop year (Fig. 9). These results are consistent
and the use of wider spacing.

10
J. Sgarbossa, et al. Agricultural Systems 184 (2020) 102911

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