ISSN 0100-2945 DOI: http://dx.doi.org /10.

1590/0100-29452020628

Economy

Leaf area estimation of ​​Anacardium humile

Francielly Rodrigues Gomes1, Danielle Fabíola Pereira da Silva²,
Angelita Lorrayne Soares Lima Ragagnin3, Pedro Henrique Magalhães de Souza4,
Simério Carlos Silva Cruz5

Abstract - The Anacardium humile A. St.- Hil. fruit tree has productive potential, being their
fruits appreciated in the Cerrado region for having characteristic flavor, however, this species is
still exploited in an extractive way, being necessary studies for its domestication. The aim of this
work was to estimate the leaf area of ​​Anacardium humile. One hundred leaves were collected in the
biological collection from a genetic resources field and evaluated for length, width and fresh weight,
and scanned at resolution of 300 dpi to determine the leaf area with the aid of the ImageJ image
analysis program. Subsequently, a leaf disc with a diameter of 22.27 mm was detached at the basal
portion of each leaf, in which the fresh weight of the discs was obtained. Data were submitted to
descriptive analysis and the relationship among the features explained by Pearson’s correlation with
the software Rbio. The data were also subjected to regression analysis to explain the relationship
between leaf area and measurements of width, length and leaf weight, and to fit the proper statistical
model with the software Origin. It was concluded that leaf area can be determined by image analysis
software and linear measurements are correlated to leaf area.
Index terms: Cajuzinho-do-cerrado, native fruits, species conservation.

Estimativa da área foliar de Anacardium humile

Resumo – As plantas de Anacardium humile A. St.- Hil. (cajuzinho-do-cerrado) possuem potencial
produtivo, sendo seus frutos apreciados na região do Cerrado por apresentarem sabor característico;
no entanto, esta espécie ainda é explorada de forma extrativista, fazendo com que sejam necessários
estudos que objetivem sua domesticação. O objetivo do presente trabalho foi estimar a área foliar
de plantas de Anacardium humile. As folhas foram coletadas na coleção biológica de um campo de
recursos genéticos e avaliadas quanto ao comprimento, largura e massa fresca, e foram escaneadas na
resolução de 300 dpi para determinar da área foliar com auxílio do programa de análise de imagens
Corresponding author: ImageJ. Posteriormente, foi destacado um disco foliar na porção basal de cada folha com o auxílio de
fram_rodgomes@hotmail.com um vazador de 22,27 mm, no qual se obteve a massa fresca dos discos. Os dados foram submetidos

Received: April 03, 2020

à análise descritiva, e a relação entre as características, explicadas pela correlação de Pearson no
Accepted: June 19, 2020 programa Rbio. Os dados foram ainda submetidos a analises de regressão para explicar a relação
entre a área foliar e as medidas de comprimento, largura e peso das folhas, e para ajustar o modelo
Copyright: All the contents
of this journal, except where matemático adequado com o software Origin. Concluiu-se que a área foliar pode ser determinada
otherwise noted, is licensed por programas de análises de imagens e que as medidas lineares se relacionam com a área foliar.
under a Creative Commons
Attribution License.
Termos para indexação: Cajuzinho-do-cerrado, Fruteiras nativas, conservação das espécies.

1
Agronomist, master in Agronomy, Universidade Federal de Jataí, Jataí – GO, Brazil. E-mail: fram_rodgomes@hotmail.com(ORCID 0000-0001-

7282-0719)
2
Agronomist, PhD in Plant Science, professor at Universidade Federal de Jataí, Academic department of agrarian sciences, Jataí – GO, Brazil.
E-mail: daniellefpsilva@ufg.br(ORCID 0000-0001-7366-5650)- Productivity scholarship of CNPq
3
Agronomist, master’s degree student at Programa de Pós-graduação em Agronomia, Universidade Federal de Jataí, Jataí – GO, Brazil. E-mail:
angelitaragagnin@gmail.com (scholarship of CNPq)(ORCID 0000-0002-5115-2704)
4
Agronomist, master’s degree student at Programa de Pós-graduação em Agronomia, Universidade Federal de Jataí, Jataí – GO, Brazil. E-mail:
pedrrromagalhaes@gmail.com (scholarship of CAPES) (ORCID 0000-0002-4824-0738)
5
Agronomist, PhD in Agronomy, professor at Universidade Federal de Jataí, Academic department of agrarian sciences, Jataí – GO, Brazil.
E-mail: simerio_cruz@yahoo.com.br(ORCID 0000-0002-6327-8590)
1
2 F. R. Gomes et al.

Introduction It is known that the leaf is the main organ responsible

for water loss and gas exchange between the plant and
The Cerrado is the second largest Brazilian biome, the environment, also, is where the photosynthetic
standing out as one of the richest in the world for having process occurs, which depends on the absorption of
species with pharmaceutical and food potential (LIMA; light energy and its conversion to chemical energy. The
PORTARI, 2019). It can be found in Goiás, Mato Grosso, knowledge about plants metabolism and growth can be
Tocantins, Mato Grosso do Sul, Minas Gerais, Rondônia, obtained through leaf area analysis (MORGADO et al.,
São Paulo, Distrito Federal and some parts of Piauí, Bahia 2013; PADRÓN et al., 2016), which can assist cultural
and Maranhão (REIS; SCHIMIELE, 2019), with area of treatments such as pruning, fertilization and planting
approximately 2 million km², which represents almost 25% density (TOEBE et al., 2019).
of the national territory (DURIGAN; RATTER, 2016). Evaluation by leaf dimension is one of the most
This biome presents predominantly seasonal tropical used techniques because it has low cost, requiring only
climatic conditions with rainfall of approximately 1500 the use of a graduated ruler or similar, and because it
mm, which is favorable for the development of attractive has good accuracy (SILVA et al., 2015). Another viable
species for exploitation, research and marketing, and these alternative is the use of digitalized images in software
species are characterized by having high nutritional value, capable of processing the images and calculating the leaf
characteristic flavor and aroma, and healthy appeal (REIS; area (LUCENA et al., 2011).
SCHMIELE, 2019). According to Lima et al. (2019), Anacardium
Among these species there is the A. humile, species are rustic and widely adapted to the climatic
which is widely distributed, especially in the Brazilian conditions of Brazil, especially the northeast region,
Midwest region, and produces fruits that are used in however, they present significant losses caused by
extractive way by the regional population and employed diseases. The occurrence of diseases leads to reduction
in the manufacture of food, juices, medicines and of leaf area, which affects photosynthetic efficiency and
cosmetics (RESSEL et al., 2015). These fruits have great photosynthesis accumulation (FIALLOS; FORCELINI,
acceptance by the local population, because they have 2011).
peculiar organoleptic characteristics and high potential Since the study of leaf area is essential to the
for sustainable production (CARVALHO et al., 2012). knowledge of species propagation and management
The literature reports many works with the genus techniques, being essential to evaluate vegetative growth
Anacardium, but fewer referring to the A. humile. Due to and development (RIBEIRO et al., 2018) and the A. humile
this lack of studies, there are many possibilities for the has high nutritional and productive potential, but consists
beginning of research on the development of the species, in of an undomesticated species due to the lack of studies
order to plan future strategies for this species preservation on it (RESSEL et al., 2015), the aim of this work was to
and use. Studies with wild species are an important estimate the leaf area of A. humile by image analysis.
alternative for incorporating them into the commercial
chain (CARVALHO et al., 2005; ATAÍDE et al., 2012). Material and Methods
Besides the great potential of this fruit species due
to its high vitamin C content, the leaves are also widely The work was carried out on summer in a region
used in common medicine as expectorant (FERREIRA et classified as tropical rainy (Aw) according to the Köppen’s
al., 2012; PEREIRA et al., 2019; MUIANGA et al., 2016). classification, with an average annual temperature from
It has been reported that these leaves have insecticidal, 18 to 32 °C and average annual rainfall of 1700 mm.
anti-inflammatory, antimicrobial and antioxidant The A. humile leaves evaluated were selected in the
properties (ANDRADE FILHO et al., 2010). collection of the field of genetic resources with 542 plants
Also known popularly as “Cajuzinho-do-cerrado”, cultivated from seeds, which were obtained in fourteen
this species is a hermaphroditic subshrub with flowering municipalities.
from June to November and fruiting from October to Within the plants located in the biological
November, the peduncle is very appreciated in Cerrado collection, one hundred leaves were harvested from the
regions and it can be consumed fresh or processed median portion of the plants, following the methodology
(SANTOS; SANTOS JUNIOR, 2015). The A. humile tree adopted by Lemos et al. (2010). These leaves were placed
is a perennial species, which has a small plant with leathery into plastic bags and sent to laboratory where they were
leaves and terminal inflorescence (LORENZI, 2006; evaluated for length and width with the aid of a digital
SILVA-LUZ; PIRANI, 2010). Its leaves are alternate, the caliper, which the results were given in mm, and leaf
adaxial face presents flat and glabrous surface, while the weight obtained in a weighing machine with results given
abaxial face presents glabrous to glabrescent surface with in grams.
prominent nerve (RESSEL et al., 2015).

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 Leaf area estimation of ​​Anacardium humile 3

After the evaluation of measurements and weight, results were given in cm² (Figure 1). Posteriorly, discs
the one hundred leaves were scanned individually at with 22.27 mm were detached from the base of each leaf.
resolution of 300 dpi and processed aiming determinate All discs were evaluated for the weight with the aid of a
leaf area with the aid of image analysis software, and these weighing machine and the results were expressed in grams.

Figure 1. Scanned leaf of A. humile for the processing in ImageJ (A and B), black and white leaf surface for contrast
(C), drawing of the leaf surface (D) and the leaf area in cm² (E).

The data were treated as completely randomized Results and Discussion

design, submitted to descriptive analysis and in order to
determine the relationship among the features of length, The leaves of the A. humile had average leaf area
width, weight of discs and leaves and leaf area, was of 66.68 cm², and it is possible to observe that there was
performed the Pearson’s correlation at significance level great variation among the leaves, with leaf area varying
of 1 and 5%. The data were also subjected to regression approximately between 24 and 127 cm² (Table 1). Due to
analysis to explain the relationship between leaf area and the genetic variability that occurs in A. humile, plants are
measurements of length, width and leaf weight and to fit highly divergent from the fruits to the size of the plants
the proper statistical model. Data of length, width, fresh (SANTOS et al., 2020), which leads to variation in the
weight and leaf area were analyzed using Rbio statistical size of their leaves.
software (BHERING, 2017), the adjustment of the models
and the graphics were plotted in Origin 8.5.1 SR1, and
leaf area was determined by imageJ software.

Table 1. Descriptive analysis of features from one hundred leaves of A. humile

LA/1 (cm²) W (mm) L (mm) LW (g) DW (g)
Average 66.68 60.31 145.85 1.86 0.10
Minimum 24.94 36.54 84.46 0.72 0.01
Maximum 127.5 104.97 204.80 4.08 0.18
Standard deviation 22.04 13.72 24.28 0.72 0.03
CV (%) 33.05 22.74 16.65 38.68 33.60

/1
LA: Leaf Area, W: Width, L: Length, LW: Leaf weight, DW: Disc weight.

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4 F. R. Gomes et al.

Knowledge of leaf area is important, regardless with reduced leaf area and shady plants develop higher
of culture, because this characteristic represents the vegetative growth as a strategy to absorb more light
light interception by the photosynthetic apparatus and is energy.
widely used to determine vegetative growth (SANTOS et An efficient way to evaluate vegetative growth
al., 2014; FERREIRA et al., 2017). The maximum light is by the length and width variables. The use of linear
interception through the leaf area varies for each crop; leaf measurements allows the monitoring of leaf
however, a larger leaf area will cause greater shading of development in the field without the need to collect the
the lower plants and a lower photosynthetic rate of plants leaf, implying a simple and less costly procedure, and
(OLIVEIRA FILHO et al., 2018). these two characteristics are efficient in estimating leaf
The processing by softwares helps to obtain images area (OLIVEIRA et al., 2016). According to Sachet et al.
information for latter interpretations. Image analysis is (2015), the joint analysis of these two variables allows
efficient to determine shapes and sizes from the objects obtaining better coefficients of determination when
of interest and can be used in a quickly and simple way, compared with other methods.
discarding the need to use expensive devices (VIEIRA Several studies have been conducted regarding
JUNIOR et al., 2006; MATOS et al., 2019). According the influence of fresh weight on leaf area estimation,
to Shi et al. (2019), the leaf surface of a plant is the basis however, according to Cunha et al. (2010) few studies
of the potential yield of the crop and knowledge of the use the fresh leaf weight in the estimation, because it is
leaf area of the plant allows the estimation of water loss, not possible to establish a direct relationship between
since the leaves are the main organs that participate in the the weight and the leaf area. Estimation by fresh weight
transpiration process, responsible for gas exchange with of leaf discs may yield results with good accuracy in
the environment. some crops or low coefficient of determination and be
The width of the leaves the average was 60.31 mm inefficient for other crops, as it is variable according to
and for the length was 145.85 mm, regarding the leaf species, one should always compare with another method
weight, it was observed that they had an average weight and take consideration of the characteristics of the species
of 1.86 g and the leaf discs had a weight of approximately (LUCENA et al., 2011).
0.10 g (Table 1). Toebe et al. (2012), report that the leaf disc method
According to Faleiro and Saiki (2007), larger leaves was inadequate to determine the snap bean leaf area, as it
have high evapotranspiration, but with high photosynthetic was underestimated and the image analysis method was
efficiency. According to these authors, in regions like the efficient because it evaluates the leaf as a whole, regardless
Cerrado, there is a tendency for the leaves to be small, of the weight difference between the areas.
being considered an adaptive advantage of the species to By Pearson’s correlation coefficients between
avoid water loss through evapotranspiration the features of the leaves of A. humile, it is possible to
Similar behavior was observed by Moraes et al. observe that width, leaf area, length and leaf weight
(2013), in five native Cerrado species, where plants in presented significant correlation with each other (Table 2),
shaded environments presented greater length and width indicating that the leaf linear measurements are directly
than plants in environments with a high incidence of solar related to the leaf area, this behavior allows to evaluate
radiation, such effect can be explained by the fact that the vegetative growth, biomass accumulation and the final
plants in sunny locations have more active metabolism plant productivity (PEZZINI et al., 2018).

Table 2. Pearson’s correlation coefficients between features from one hundred leaves of A. humile
LA/¹ W L LW
W 0.88 **

L 0.73** 0.45**
LW 0.87** 0.73** 0.71**
DW 0.06 NS
-0.005 NS
0.04NS 0.25*
NS
Not significant; * Significant at 5% probability; ** Significant at 1% probability.
/¹ LA: Leaf Area, W: Width, L: Length, LW: Leaf weight, DW: Disc weight.

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 Leaf area estimation of ​​Anacardium humile 5

The leaf area of A. humile has a positive and Leaf length, width and weight are strongly
significant correlation with length and width (0.73 and correlated with leaf area. It is known that the leaf is
0.88), as well as length positively correlates with width the organ responsible for the production of lipids,
(0.45). It can be observed that the width has a negative and carbohydrates and proteins, being the knowledge of linear
non-significant correlation with the disc weight (-0.005), measurements and leaf area very important to understand
as well as the length and leaf area (0.04 and 0.06) and that the processes of plant development, photosynthetic
the leaf weight has a positive and significant correlation potential, nutritional and water requirement (ZEIST et
with the weight of the discs (0.25) (Table 2). al., 2014).
According to Kozak (2009), values below 0.2 are The simple linear regression model was the most
not significantly correlated, while values between 0.2 and accurate to explain the relationship of the leaf area
0.5 are poorly correlated, likewise values between 0.5 with width, length and leaf weight, and showed a high
and 0.7 or above 0.7 constitute a strong and very strong coefficient of determination (R²) for the relationships
correlation, with positive variables moving together and between leaf area x width, and leaf area x leaf weight
negative variables in opposite directions. In the present (Figure 2). The higher is the R² values and the lower is the
experiment, the leaf area showed a strong correlation with standard error of the estimate (SEE) values, the greater will
length and width, indicating that as one trait increases the be the accuracy of the model (MORGADO et al., 2013).
others increase. The prediction of models can be influenced by leaves
shape and their variations along the growth, which can
be decisive for the development of high precision models
(HARA et al., 2019).

Figure 2. Relationship between leaf area and width (A); leaf area and length (B); and leaf area and leaf weight (C) of
A. humile using linear regression models.

The relationship between the leaf area and the there was an increase in SEE and a reduction in R² (Table
length, width and leaf weight adjusted to linear statistical 3). The increase in R² values is related to the reduction
model. The relationship of the leaf area x leaf weight of the standard error of the estimate, which occurs due to
showed low SEE and high R², while to leaf area x width the increase in F-calc and to the reduction of sum of the
squares of the residues (FIALHO et al., 2011).

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6 F. R. Gomes et al.

Table 3. Statistical models, regression parameters, Standard error of estimate (SEE), Determination coefficients adjusted
for degrees of freedom (R2), F-Calculated (F-calc) and leaf area estimate (LA) as a function of linear dimensions
(Width (W), Length (L)) and leaf weight (LW) of one hundred A. humile leaves
Model Parameters SEE R2 F-calc LA estimate
β0= -19.4152 *
LAw= β0+ β1X 4.6065 0.7872 367.22* LAw= -19.4152+ 1.4274W
β1= 1.4274*
β0= -30.8220*
LAl= β0+ β1X 9.1704 0.5300 116.15* LAl= -30.8220 + 0.6684L
β1= 0.6684*
β0= 16.8361*
LAlw= β0+ β1X 2.9884 0.7628 319.42* LAlw= 16.8361+ 26.7284LW
β1= 26.7284*
*
Significant at 5% level.

Conclusions CARVALHO, R.S.; PINTO, J.F.N.; REIS, E.F.; SANTOS,

S.C.; DIAS, L.A.S. Variabilidade genética de cajuzinho-
The leaf area can be determined by scanning images do-cerrado (Anacardium humile ST. Hill.) por meio de
and further processing in the image analysis software. The marcadores RAPD. Revista Brasileira de Fruticultura,
leaf area can be related to linear measurements. Jaboticabal, v.34, n.1, p.227-233, 2012.

CUNHA, J.L.X.L.; NASCIMENTO, P.G.M.L.;

MESQUITA, H.C.; SILVA, M.G.O.; DOMBROSKI,
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