Butia spp. (Arecaceae): An overview

Scientia Horticulturae 179 (2014) 122–131
Contents lists available at ScienceDirect
Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti
Review
Butia spp. (Arecaceae): An overview
Jessica F. Hoffmann a , Rosa L. Barbieri b , Cesar V. Rombaldi a , Fabio C. Chaves a,∗
a
b
Faculdade de Agronomia Eliseu Maciel, Universidade Federal de Pelotas, Caixa Postal 354, CEP 90010-900, Pelotas, RS, Brazil
Embrapa Clima Temperado, Caixa Postal 403, CEP 96001-970, Pelotas, RS, Brazil
a r t i c l e
i n f o
Article history:
Received 2 July 2014
Received in revised form 9 August 2014
Accepted 14 August 2014
Keywords:
Palms
Jelly palm
Pindo palm
Autochtonous fruit
Genetic resources
Underutilized species
a b s t r a c t
Butia is a genus of palms (Arecaceae), autochthonous to South America with great potential for income
generation. In order to better utilize and maintain the currently available genetic resources, it is necessary to pursue studies directed towards the taxonomic and systematic characterization (morphological,
phenotypic, molecular, chemical, and reproductive) and conservation of Butia spp. Despite the long use
of this plant, a limited number of scientific studies and publications are available on Butia spp., with
a significant proportion of the literature written in Portuguese. This review intends to compile all the
available information on the genus, covering several aspects of the plant and its potential applications.
© 2014 Elsevier B.V. All rights reserved.
Contents
1.
2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Occurrence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.
Taxonomy and systematics of the genus Butia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Chemotaxonomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Characterization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1.
Molecular . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.
Phenotypic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.1.
Germination/dormancy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.3.
Pathogens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.4.
Postharvest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.5.
Chemical characteristics of fruits and seeds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.5.1.
Specialized metabolites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.5.2.
Volatile compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.5.3.
Antioxidant potential . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Potential applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction
The health promoting properties and the chemical, morphological, and agronomic characteristics of fruit bearing plants
from Europe and North America have been described in the
∗ Corresponding author. Tel.: +55 53 32757284.
E-mail address: [email protected] (F.C. Chaves).
http://dx.doi.org/10.1016/j.scienta.2014.08.011
0304-4238/© 2014 Elsevier B.V. All rights reserved.
scientific literature, whereas those native to South America have
been substantially less studied (Clerici and Carvalho-Silva, 2011;
Schreckinger et al., 2010). South America possesses a wide diversity of native fruit bearing species consumed regionally that are
slowly gaining popularity for their pleasant sensory attributes such
as flavor and color, but also for their proposed nutritional and
bioactive potential. There has been considerable interest in the
exploration and domestication of alternative species (Clerici and
J.F. Hoffmann et al. / Scientia Horticulturae 179 (2014) 122–131
Fig. 1. Illustrative representation of Butia spp. occurrence in South America
(Adapted from Google maps).
Carvalho-Silva, 2011; Costa et al., 2013; Oliveira et al., 2006; Rufino
et al., 2010).
Fruit of the Arecaceae family, for instance, are attractive for
their organoleptic, nutritional, and functional potential, consumed
fresh or processed as pulp, liquor, sweets, ice creams, preserves,
and other products including oils, waxes, and fibers (Lorenzi et al.,
2006). The genus Butia in particular, native to southern South America (Fig. 1), has great potential for expansion. Eighteen species
occur naturally, predominantly in areas in southern Brazil, eastern
Paraguay, northeastern Argentina, and northwestern and southeastern Uruguay (Lorenzi et al., 2010). Brazil possesses the majority
of the existing species, 18 out of the 20. Their occurrence spans
southeast of Bahia and east of Goias, but the majority of populations is found in southern states, predominating in Rio Grande do
Sul (Marcato, 2004; Müller et al., 2012; Santos et al., 2012; Soares
and Longhi, 2011; Soares et al., 2014).
Butia palms (Fig. 2; also known as jelly palms or pindo palms)
were utilized in Brazil in the 30’s and 50’s for their leaves that
were sun dried, weaved, and used in mattresses, chairs, and sofas
(Tonietto et al., 2009). Currently, Butia fruits are mainly consumed
fresh or processed in pulp, juices, alcoholic beverages, jams, jellies,
and ice creams (Schwartz et al., 2010; Sganzerla, 2010). Butia palms
are also used as ornamentals (Beskow, 2012; Soares and Longhi,
2011) and the dried leaves are still utilized to make hats, brooms,
baskets, and other crafts (Büttow et al., 2009; Sampaio, 2011). In
addition, the oil extracted from seeds of Butia catarinensis has been
used in the making of soaps, and the roots have been described
as having anti-inflammatory potential (Kumagai and Hanazaki,
2013).
There is evidence of use of Butia dating back to ancient periods.
Phytoliths of Butia paraguayenses (Barb. Rodr.) L.H. Bailey and Butia
microspadix Burret were found in Paraná, Brazil (Pereira et al.,
123
2013a,b; Rasbold et al., 2011), and burned palm seeds of Butia
capitata were found at an archeological site in Uruguay (Mazz,
2013). Currently, Butia is typically harvested from wild or naturally occurring populations, with no existing commercial orchards.
Unfortunately the genus is endangered and at a risk of extinction
due to expansion of urban areas, agricultural activities replacing
the natural palm groves, illegal removal and commercialization of
plants, reforestation with other tree species, and limited natural
regeneration due to cattle grazing (Mistura, 2013; Nazareno and
Reis, 2014a; Soares and Witeck, 2009). Butia eriospatha is included
on the Brazilian Endangered Species list (Instrução Normativa 06,
MMA, 2008) and Butia purpuracens Glassman and B. eriospatha
(Martius ex Drude) Beccari appear on the International Union for
Conservation of Nature Red List (IUCN, 2013). In addition, other
species such as Butia campicola, Butia odorata, Butia leiospatha, B.
microspadix, B. purpurascenses, and Butia yatay are on the list of
Brazilian species with limited data/information (Instrução Normativa 06, MMA, 2008).
In order to conserve genetic resources of these species and study
their potential applications, Embrapa Clima Temperado and Universidade Federal de Pelotas maintain active germplasm collections
of Butia and are conducting research on the characterization, propagation, and evaluation of the potential for widespread utilization
of this palm (Barbieri et al., 2014). In addition to these germplasm
collections, natural populations exist in several regions throughout Rio Grande do Sul including Tapes, Santa Vitória do Palmar,
Santa Rosa, and Santa Maria (Ferrão et al., 2013; Nunes et al., 2010;
Schwartz et al., 2010).
Despite the historic use of these palms, a limited number of scientific studies and publications are available on Butia spp., with
a significant proportion of the literature written in Portuguese.
This review intends to compile the available information on the
genus, covering occurrence, taxonomy and systematics, genotypic
and phenotypic characterization, aspects of crop physiology such
as seed germination and dormancy, with emphasis on bioactive
potential of its fruit and potential applications.
2. Occurrence
2.1. Taxonomy and systematics of the genus Butia
Butia Becc. belongs to the Arecales order, Arecaceae (Palmae)
family, Arecoideae subfamily, tribe Cocoeae, subtribe Buttinae (APG
II, 2003; APG III, 2009; Hahn, 2002; Lorenzi et al., 2010;). There
are 20 species of the genus Butia native to South America: Butia
archeri (Glassman) Glassman, B. campicola (Barb. Rodr.) Noblick,
B. capitata (Mart.) Becc., B. catarinensis Noblick and Lorenzi, B.
eriospatha (Mart. ex Drude) Becc., Butia exilata Deble and Marchiori,
Butia exospadix Noblick, Butia lallemantii Deble and Marchiori,
B. leiospatha (Barb. Rodr.) Becc., Butia lepidotispatha Noblick and
Lorenzi, B. leptospatha (Burret) Noblick, Butia marmorii Noblick,
Butia matogrossensis Noblick and Lorenzi, B. microspadix Burret, B.
odorata (Barb. Rodr.) Noblick and Lorenzi, Butia paraguayensis (Barb.
Rodr.) Bailey, Butia pubispatha Noblick and Lorenzi, B. purpurascens
Glassman, Butia witeckii K. Soares and S. Longhi and B. yatay (Mart.)
Becc. (Deble et al., 2011; Leitman et al., 2013; Lorenzi et al., 2010;
Noblick, 2011; Soares and Longhi, 2011).
After a taxonomic revision of the genus Butia (Leitman et al.,
2013; Lorenzi et al., 2010), one of the species occurring in Rio
Grande do Sul previously named B. capitata was renamed B. odorata,
while B. capitata was reorganized to include the species occurring
in the Cerrado biome (center and eastern Brazil). Recently Soares
et al. (2014) described B. catarinensis, B. eriospatha, B. exilata, B. lallemantii, B. odorata, B. paraguayensis, B. witeckii, B. yatay as native to
Rio Grande do Sul and excluded B. microspadix.
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J.F. Hoffmann et al. / Scientia Horticulturae 179 (2014) 122–131
Fig. 2. (a) Butia odorata and (b) basket (made from leaves), fruit, and liquor of Butia yatay (Photos by R.L. Barbieri).
Due to inconsistencies and ambiguities in the identification of
populations of Butia spp., the recently proposed classification by
Lorenzi et al. (2010) and Leitman et al. (2013) was followed for
this report. Therefore, species names were adjusted according to
the location of occurrence as described by the previously referred
authors.
2.2. Chemotaxonomy
Flavonoid sulfates, flavone c-glycosides, tricin, luteolin,
quercetin, and proanthocianidins are distributed in flowers and
fruits in members of the Arecaceae family (Barron et al., 1988;
Harborne et al., 1974; Harborne, 1975; Williams and Harborne,
1973) and were utilized as chemotaxonomic markers for speciation
(Williams et al., 1983). A lipid fraction rich in linear hydrocarbon
waxes has also been utilized as a taxonomic identifier within
the Arecaceae family (García et al., 1995; Paroul et al., 2009). In
both studies, the apolar compounds were extracted from leaves
and analyzed by GC-MS. García et al. (1995) found B. capitata and
Orbignya spp. containing large amounts of ethers, which were
absent from Arecastrum romanzoffianum. Paroul et al. (2009) studied 24 Butia leaf samples and 20 Syagrus leaf samples and found
a high content of linear hydrocarbons, with hentriacontane (C31)
and tritriacontane (C33) being the main constituents responsible
for differentiating both genera.
3. Characterization
3.1. Molecular
The high degree of genotypic diversity in Butia is demonstrated
by the variation in fruit biometric, physicochemical, and sensory
parameters. Recent studies have focused on aspects related to the
biology of the genus Butia. Cytogenetic analyses demonstrated that
Butia species occurring in Rio Grande do Sul, B. eriospatha, B. odorata, B. lallemantii, B. Catarinensis, and B. yatay are diploid (2n = 32)
and possess the same caryotype with 14 metacentric, 12 submetacentric, and 6 acrocentric chromosomes (Corrêa et al., 2009).
In addition to morphological studies, DNA based molecular
markers have been employed to further investigate the diversity
and systematics of the genus Butia. Gene flow in populations of
Butia occurs by seed dispersal by wildlife and pollen dispersal by
insects, leading to high variability within populations common in
outcrossing species (Gaiero et al., 2011; Mistura, 2013).
Inter-simple sequence repeat (ISSR) fingerprinting is a useful
tool for making taxonomic comparisons and determining intrapopulation genetic variability. A study characterizing B. odorata,
B. yatay, B. eriospatha, and B. catarinensis from Rio Grande do Sul
found highly polymorphic bands and high morphological diversity
(Rossato et al., 2007). In another study using ISSR markers, four natural populations of B. lallemantii, one of B. paraguayensis, and three
of B. yatay from different locations in Uruguay were analyzed. The
results showed a high level genetic proximity among the species
(Gaiero et al., 2011).
Random amplified polymorphic DNA (RAPD) markers were used
to determine the genetic diversity among 22 Butia genotypes from
Pelotas, Rio Grande do Sul. 136 fragments were obtained and 77
were polymorphic. A dendrogram based on unweighted pair grouping allowed for separation of the genotypes into two main groups
(Nunes et al., 2008). Additionally, Gavião et al. (2007) found 90% of
genetic variability within populations and 10% among three populations of B. erisphata using RAPDs.
Büttow et al. (2010) investigated the genetic diversity of eight B.
odorata populations from Tapes, Rio Grande, and Santa Vitória do
Palmar in Rio Grande do Sul from a total of 46 plants using amplified fragment length polymorphism (AFLP) markers. On average,
50 polymorphic bands were amplified and the genetic variability
observed did not vary among geographical regions evaluated, with
higher variation was found within populations.
Nazareno et al. (2011) developed microsatellite markers
to investigate genetic diversity, spatial genetic structure, and
mating system in B. eriospatha populations and investigated
J.F. Hoffmann et al. / Scientia Horticulturae 179 (2014) 122–131
transferability of the markers in B. catarinenses. At least 86% of
primers were amplified in B. catarinensis, indicating a high potential for transferring microsatellite markers between species of the
same genus in the Arecaceae family.
Nazareno and Reis (2014b) evaluated the genetic diversity of
a wild population of B. eriospatha and of illegally traded plants
established in urban areas of Santa Catarina state to understand the
genetic diversity of the populations and to try to establish the origin of the illegally traded individuals. Illegally traded individuals
showed higher genetic variability than the wild population suggesting different origins for the individual illegally traded plants
found in the studied urban areas.
Molecular marker studies in Butia reveal a great deal of diversity
within species. Therefore, studies evaluating morphology, chemical composition, and agronomic behavior of Butia populations are
important to complement molecular studies to aid in understanding the taxonomy of the genus. The increased taxonomic knowledge
of Butia and a better understanding of the factors that determine the
actual geographical distribution of species are predominant themes
and have direct implications for the conservation and use of genetic
resources in this genus.
3.2. Phenotypic
Butia spp. occur in an aggregated spacial distribution, sometimes
dense and extensive in palm groves called “butiazais” in Portuguese
and “palmares” in Spanish. Plant height can vary from less than 1 to
12 m tall. The stem is erect or slightly bent and occasionally underground. Leaves are pinned and arched with color varying from
grayish to green, distributed at the top part of the stem in a spiral
fashion, with long, thin, lanceolated and alternate folioles. Leaves
have indistinct sheath and petioles, with margins having flattened
fibers (Lorenzi et al., 2004). Although morphological traits vary significantly among species, bunch length tends to range from 0.22 to
1.18 m, and the number of fruit per bunch may reach 1400, with
an average of 15–56 kg of fruit per plant per year (Azambuja, 2009;
Beskow, 2012; Guilherme and Oliveira, 2011; Nunes et al., 2010;
Rivas and Barilani, 2004; Rosa et al., 1998; Schwartz, 2008; Silva
and Scariot, 2013).
The inflorescence rachilles occur in 13–150 and are 10–100 cm
long (Fonseca et al., 2007; Leitman et al., 2013; Lorenzi et al., 2006;
Reitz, 1974; Sobral et al., 2006). The size of the inflorescence has a
direct relation to the number of flowers (Moura et al., 2007). In B.
eriospatha, the inflorescences are protandrous, where male flowers
reach anthesis before female flowers (Nazareno and Reis, 2012).
In B. paraguayenses, inflorescences are monoecius (SilberbauerGottsberger et al., 2013). In B. odorata, the flowers are distributed
on the bottom side of the rachilles in groups of threes, in which the
side groups are male and the central is female; on the top of the
rachille there are only male flowers (Schwartz, 2008). B. odorata,
B. eriospatha, B. paraguayenses, and B. yatay have microreticulate
pollen grains that are larger than 40 ␮m (Bauermann et al., 2010).
Both male and female flowers have floral nectaries to reward their
pollinators. The rare synchrony between phenophase of male and
female flowers on the same plant can contribute to xenogamy or
cross-pollination in B. capitata (Mercadante-Simões et al., 2006).
Palm trees can take up to 10 years to produce fruit (Büttow et al.,
2009). In the Butia genus, plants flower from September to March
(Rosa et al., 1998). The variation in flowering time influences the
ripening period that can range from as early as October to as late
as May, suggesting that phenological variables are not uniformly
distributed year round for different species of Butia (Nazareno and
Reis, 2012; Reitz, 1974; Rosa et al., 1998; Sampaio, 2011).
During flowering, many insects have been identified visiting the
flowers, including flies, beetles, wasps, and bees (Rosa et al., 1998).
In B. eriospatha, the most frequent visitors belong to Hymenoptera,
125
Diptera, and Coleoptera families. Staminate and pistillate
flowers are most commonly visited by Meliponinae bees, but
also by Halictidae and Apinae, which are considered the most
efficient pollinators of B. eriospatha (Silberbauer-Gottsberger et al.,
2013). The same authors also reported the presence of several fly,
wasp, and ant species visiting the flowers, and considered them
potential pollinators. Additionally, Nazareno and Reis (2012) found
evidence of pollination in the absence of pollinators and when in
isolation in a study of the reproductive biology of B. eriospatha.
3.2.1. Germination/dormancy
Since Butia propagation occurs exclusively by seed, it is necessary to obtain seed of good physiological and sanitary quality
(Magalhães et al., 2008). The dispersal unit consists of a diaspore
composed of an endocarp containing three seeds. The embryo is
generally cylindrical, 1 to 6 mm on average, and immersed in an
endosperm, without a specific location in the seed (basal, lateral or
apical) (Carpenter, 1988; Lorenzi et al., 2006; Reitz, 1974).
The germination of seeds of wild species is generally nonuniform and slow, and may take up to one year to complete,
precluding the production of seedlings on a large scale (Broschat,
1998). Commercial plantings of Butia, its utilization in erosion control, as well as the conservation of established natural populations
will depend on overcoming this limitation (Lopes et al., 2011). The
low germination percentage of Butia is likely to be associated with
dormancy, which can originate from immature embryos, mechanical resistance of the endocarp, gas and/or water impermeability,
presence of chemical inhibitors, and/or the combination of these
factors. Seed dormancy and low germination percentage (below
20%) are major limitations to seedling production and consequently
to conservation and establishment of orchards (Broschat, 1998;
Fernandes, 2008; Lopes et al., 2011; Neves et al., 2010).
Palm diaspores are reported to have various kinds of dormancy
(Baskin and Baskin, 2004, 2014). In Butia, mechanical exogenous
(Fior et al., 2011) and non-deep physiological (Dias et al., 2013;
Magalhães et al., 2013; Schlindwein et al., 2013) dormancy have
been reported. The embryonic structure of B. odorata (genotypes
from Rio Grande do Sul) and B. capitata (genotypes from Minas
Gerais) does not impose limitations on seed germination (Fior et al.,
2011; Magalhães et al., 2013), and dormancy is likely caused by the
inability of the embryo to overcome the resistance of the cell layers of the micropylar endosperm and opercular seed coat (Oliveira
et al., 2013). Extracts of the endocarp and endosperm of B. capitata (Magalhães et al., 2012), as well as extracts of the exocarp,
mesocarp, endocarp, and whole seed of B. capitata did not show
allelopathic effects on lettuce seeds, suggesting absence of chemical
dormancy (Fernandes et al., 2007).
Studies have been performed to reduce dormancy and increase
germination index in Butia seeds. Oliveira et al. (2013) characterized the structures (morphology, physiology, anatomy and
histochemistry) of seeds and seedlings of B. capitata to identify
aspects related to dormancy and determine the processes involved
in reserve mobilization. Endocarp removal is a pre-germination
treatment recommended to accelerate and make germination of
Butia spp. more uniform (Broschat, 1998; Fior et al., 2011; Lopes
et al., 2011). Physical scarification (removing the protective film
from the germ pore) accompanied by gibberellic acid application
(1000 mg L−1 for 24 h) accelerated the germination process, reducing the average time of germination to 51 days (Lopes et al., 2011).
Immersion in gibberellic acid solution (2000 mg L−1 for 24 h) followed by removal of the operculum resulted in 98% germination
in B. capitata (Dias et al., 2013). Seed drying followed by rehydration and exposure to high temperatures also promoted dormancy
alleviation (Schlindwein et al., 2013).
In vitro germination of B. capitata embryos and seedling development are increased with seed maturation (Neves et al., 2010).
126
J.F. Hoffmann et al. / Scientia Horticulturae 179 (2014) 122–131
The cultivation of the zygotic embryo in MS culture media
supplemented with 2,4-D (0.5 mg L−1 ), activated charcoal (0.25%),
and glutamine (0.5 g L−1 ) allowed for a better germination index
and better seedling development (Minardi et al., 2011). Waldow
et al. (2013) found a positive correlation between gibberellic acid
concentration and germination in B. eriospatha. Optimum germination conditions for zygotic embryos were observed in MS or Y3
media containing gibberellic acid (8 mg L−1 ) (Waldow et al., 2013).
Fior et al. (2011) tested the in vitro germination of B. capitata and B. odorata seeds submitted to treatments to overcome
dormancy by operculum withdrawal, by partially and fully opening the embryo cavity. The results indicated that partial openness
increased the germination percentage up to 25% when compared to
non-scarified seeds. Total removal of the operculum of the embryonic cavity increased germination to over 80%. The percentage of
seedling development from this treatment was also high. On average, 92% of the germinated seeds formed complete plantlets, 29
days from sowing.
Ribeiro et al. (2011) evaluated the best conditions in terms of
media composition for the germination of zygotic embryos and
the in vitro development of B. capitata. The authors observed that
lighting conditions did not affect germination, but the absence of
light favored root formation. In media without sucrose, elongation occurred, demonstrating the existence of energy reserves in
embryos.
The emergence of B. odorata seedlings was 72% in 56 days when
scarified by opening the embryonic cavity of the seeds (Fior et al.,
2013). Although this method improved germination percentage
and days to germination, it lacks practical commercial application.
3.3. Pathogens
Thirty records of pathogens were found when searching the
Systematic Mycology and Microbiology Laboratory Literature
Database for the genus Butia (Farr and Rossman, 2014). In Brazil,
Coccostroma palmicola (Coccostromopsis palmicola) (Capted et al.,
2010) and Mycosphaerella advena were found in Butia sp., and Periconia sp. and Trabutia sp. in B. leiospatha. In Florida, United States,
Alternaria sp. (leaf spot), Armillaria tabescens (root rot), Cercospora
sp. (leaf spot), Colletotrichum sp. (leaf spot.), Diplodia sp., Fusarium sp., Graphiola phoenicis (false smut), Graphium sp., Pestalotia
palmarum (leaf spot), Phyllosticta sp. (leaf spot), Phytophthora sp.,
Polyporus lucidus var. zonatus (Ganoderma zonatum) (trunk rot),
Pythium sp. (root rot), Rhizoctonia sp., and Stigmina palmivora (leaf
spot) were reported in B. capitata. In Uruguay, Thielaviopsis paradoxa was found in B. capitata. In Argentina, Berkleasmium corticola,
Cannonia australis, Coccostromopsis palmicola, Cosmospora vilior
(Pseudocosmospora vilior), Dictyosporium cocophylum, and Endocalyx melanoxanthus var. melanoxanthus were found in B. yatay.
Link and Naibo (1995) found the bruchid weevil Butiobruchus
in seeds of B. odorata with no apparent threat of severe damage.
Savaris et al. (2013) reported B. eriospatha as a fruit fly host (presence of Anastrepha fraterculus and Ceratitis capitata). These species
cause significant economic losses in the horticultural sector, and
there is a large investment in measures to control these species
(Zucchi, 2008, 2012).
3.4. Postharvest
Very few reports deal with agronomic aspects of Butia spp.
including yield, productivity, fruit and tree qualitative characteristics, and production cycle. Identifying genotypes with superior
attributes including fruit yield, extractable juice/pulp yield, flavor,
and functional potential will support breeding programs in the
development of commercial cultivars (Beskow, 2012). Jelly palm
fruit are normally hand picked and have a short postharvest life
(Silva and Scariot, 2013). In order to extend shelf life, fruit are
harvested at the greenish-yellow or greenish-red stage and then
immediately stored at 0 ◦ C to maintain texture and prevent decay
(Amarante and Megguer, 2008).
3.5. Chemical characteristics of fruits and seeds
Native fruit species have received more attention recently for
their potential to improve human health. These benefits are usually associated with specialized metabolites, often referred to as
secondary metabolites or natural products, such as carotenoids
and phenolic compounds, which have been reported to slow
down aging symptoms and to prevent chronic diseases such as
cancer, diabetes, and cardiovascular disease (Duyn and Pivonka,
2000; Martínez-Navarrete et al., 2008). Fruit physicochemical characteristics influence shelf life as well as potential application.
Physicochemical characterization of Butia spp. fruit has been performed in order to explore their potential use, improve shelf life,
and aid in species identification (Dal Magro et al., 2006; Nunes et al.,
2010; Pedron et al., 2004; Sganzerla, 2010).
Mature jelly palm fruits when ripe, range from pale yellow
to bright reddish orange in color, with an average diameter of
1.7–4.2 cm. The mesocarp is fleshy, with an endocarp containing
one to three locules with three pores near its middle portion, and a
seed with abundant endosperm (Lorenzi et al., 2004; Moura et al.,
2010; Pedron et al., 2004; Schwartz, 2008). Biometric parameters
are closely associated to yield, and descriptors such as skin, flesh,
and the fruit/seed ratio are good indicators of species and important characteristics for breeding programs (Pedron et al., 2004;
Sganzerla, 2010).
Soluble solids content (SS), pH, and acidity (TA) are relevant
parameters that determine the potential of the fruit for fresh consumption or for processing. The ratio of SS/TA provides a better
evaluation of fruit flavor, being more representative than isolated
measurements of the sugar content or acidity. Table 1 shows the
range of those parameters as observed by several authors for some
Butia species.
The few studies reporting centesimal composition of Butia
spp. fruit showed significant variation and wide range of results
(Table 2). In terms of mineral content, Butia pulp contains Ca, K, P,
Mg, S, Fe, Mn, Na, Al, Cu, and Zn and is also a source of provitamin
A and vitamin C (Faria et al., 2008a,b; Fonseca, 2012).
The fatty acid composition of B. odorata fruit flesh determined by
Ferrão et al. (2013) showed on average 42% saturated fatty acids,
30% monounsaturated fatty acids and 24% polyunsaturated fatty
acids. Lopes et al. (2012) found 63% unsaturated fatty acids and 36%
saturated fatty acids in B. capitata fruit. Both studies reported the
presence of linolenic (omega 3) and linoleic acids (omega 6), which
are considered important from a nutritional standpoint given their
role in cellular membranes and brain function in the transmission
of nerve impulses (Martin et al., 2006).
Butia seeds have a nut that is usually discarded when fruit is
processed for frozen pulp. The nut of B. capitata is rich in fiber
and lipids. The lipid content is predominantly composed of saturated medium chain fatty acids such as lauric (C12:0) and oleic acid
(C18:1). The minerals in greater quantities are potassium, phosphorus, magnesium, and sulfur (Faria et al., 2008a,b). Nuts of B. odorata
and B. eriospatha are rich in phenolic compounds and carotenoids,
which are positively correlated with its high antioxidant capacity (Sganzerla, 2010). The same author extracted oil from the nuts,
obtaining oil content for B. odorata ranging from 29% to 56%, and
for B. eriospatha from 26% to 50%. Regarding the fatty acid profile, lauric, capric, and oleic acid were present in greater quantities.
The high fat, fiber, and mineral content of Butia nuts indicates a
potential for use as an ingredient in the food industry or animal
J.F. Hoffmann et al. / Scientia Horticulturae 179 (2014) 122–131
127
Table 1
Physicochemical characteristics of Butia spp. fruit.
Species
Origin
pH
SS
TA
SS/TA
Reference
B. capitata
B. odorata
B. odorata
B. odorata
B. odorata
B. odorata
B. eriospatha
B. eriospatha
B. eriospatha
B. eriospatha
B. odorata
B. odorata
B. odorata
B. odorata
Unknown
Capão do Leão, RS
Pelotas, RS
Santa Vitória do Palmar, RS
Capão do Leão, RS
Pelotas, RS
São José do Oeste, PR
Faxinal dos Guedes, SC
Pelotas, RS
Guarapuava, PR
Pelotas, RS
Tapes, RS
Santa Rosa̧ RS
Santa Maria, RS
3.01
3.10–3.81
2.87–3.01
2.98–3.09
2.45
–
2.93
3.06
2.36
3.01
2.89–3.12
2.86–3.17
3.35–3.95
3.17–3.88
9.25
12.0–18.0
14.4–15.0
11.0–12.5
11.7
10.3
6.4
7.7
9.0
9.3
12.2–16.0
10.6–14.8
9.5–14.0
10.5–15.2
0.35
1.80–3.90
2.40–2.74
1.96–2.87
2.41
1.38
1.43
1.21
1.88
0.35
1.07–2.25
1.74–3.47
0.69–2.26
0.94–2.17
26.43
3.98–10.0
–
4.17–6.81
–
7.48
–
–
–
Haminiuk et al. (2006)
Nunes et al. (2010)
Krolow et al. (2010)
Schwartz et al. (2010)
Sganzerla (2010)
Pereira et al. (2013a,b)
Dal Magro et al. (2006)
Dal Magro et al. (2006)
Sganzerla (2010)
Rigo et al. (2010)
Beskow (2012)
Fonseca (2012)
Ferrão et al. (2013)
Ferrão et al. (2013)
5.71–14.41
–
4.42–13.67
4.83–14.20
SS—soluble solids content (◦ Brix); TA—titratable acidity (% of citric acid); SS/TA—ratio.
Table 2
Proximate composition of Butia flesh (expressed in %).
Species
Location
Moisture
Ash
Protein
Fiber
Lipids
Carbohydrates
Reference
B. odorata
B. capitata
B. eriospatha
B. odorata
B. odorata
B. odorata
B. odorata
Capão do Leão, RS
Montes Claros, MG
Pelotas, RS
Tapes, RS
Santa Rosa, RS
Santa Maria, RS
Pelotas, RS
84.99
85.40
88.15
79.93–83.61
78.04–84.39
79.47–85.85
87.82
0.63
0.90
0.59
0.99
0.60–0.74
0.47–0.77
0.25
0.94
0.30
1.07
3.24–5.28
0.60–0.93
0.57–0.76
5.79
1.22
–
0.88
1.00–2.10
1.22–2.42
0.84–4.02
4.89
0.11
2.60
0.15
1.40–2.41
0.87–2.27
0.12–1.39
0.61
12.11
10.80
9.16
6.58–11.33
14.84
14.15
10.55
Sganzerla (2010)
Faria et al. (2008a,b)
Sganzerla (2010)
Fonseca (2012)
Ferrão et al. (2013)
Ferrão et al. (2013)
Pereira et al. (2013a,b)
feed, improving the texture and fortifying the products (Faria et al.,
2008a,b; Sganzerla, 2010).
3.5.1. Specialized metabolites
Plants produce an important and diverse array of organic
compounds traditionally referred to as secondary metabolites,
also known as specialized metabolites or natural products, often
distributed among limited taxonomic groups within the plant kingdom (Cheynier et al., 2013). These metabolites play an important
role in plant adaptation and defense under different stress conditions such as drought, UV radiation, and pathogens (Dietrich et al.,
2004; Szajdek and Borowska, 2008).
Species of the Arecaceae family are attractive from a chemical
and pharmacological standpoint (Silveira et al., 2005). Interest in
little explored native species for their potentially bioactive composition of specialized metabolites has increased; however, the genus
Butia has not received much attention. Table 3 shows the bioactive
compounds studied in Butia to date.
Phenolic compounds partially synthesized through the
shiquimic acid pathway are a major group of phytochemicals
that include flavonoids, stilbenes, coumarins, and phenolic acids
(Tulipani et al., 2008). Phenolic compounds can contribute to protection against degenerative diseases, and their effects on health
have been attributed to their antioxidant properties (Seeram,
2008). Pulp of B. odorata and B. eriospatha have been shown to
contain phenolic compounds including gallic acid (85.98 and
51.43 mg 100 g−1 ), p-hydroxybenzoic acid (54.18 and 25.58 mg
100 g−1 ), ferulic acid (0.44 and 0.75 mg 100 g−1 ), epicatechin (9.69
and 8.97 mg 100 g−1 ), and quercetin (1.44 and 1.98 mg 100 g−1 )
(Sganzerla, 2010). Gallic acid is the major phenolic compound in B.
odorata (Beskow et al., 2014). In addition, the colorful anthocyanic
phenolics keracyanin and kuromanin have been found in B. odorata
with a red-pigmented epidermis (Beskow et al., 2014; Sganzerla,
2010).
Carotenoids are the largest group of pigments synthesized by
plants, with more than 600 identified compounds. Their color may
vary from yellow to red, and they have been utilized in foods
as a natural colorant and antioxidant (Rodriguez-Amaya, 2010).
Mostly regarded for their pro-vitamin A activity (␤-ionone ring
containing carotenoids), the range of health promoting potential
of carotenoids includes immuno-enhancement and reduction of
the risk of developing degenerative diseases such as cancer, cardiovascular disease, cataracts, and macular degeneration (Krinsky
and Johnson, 2005). ␤-carotene, ␤-criptoxanthin, lycopene, lutein,
and zeaxanthin have been found in B. odorata and B. eriospatha
(Sganzerla, 2010).
Faria et al. (2011) identified the carotenoids phytoene
(5.7 ␮g g−1 ), phytofluene (4.4 ␮g g−1 ), ␣-carotene (0.1 ␮g g−1 ), ␤carotene (16.1 ␮g g−1 ), ␨-carotene (0.8 ␮g g−1 ), poly-cis-␥-carotene
(4.7 ␮g g−1 ), ␥-carotene (2.9 ␮g g−1 ), ␣-criptoxanthin, or zeinoxanthin (0.8 ␮g g−1 ) in pulp of B. capitata. The ␤-carotene represented
46% of total carotenoids and 92% of the pro-vitamin A activity in
the pulp. Pereira et al. (2013a,b) identified lutein (4.68 ␮g g−1 ),
zeaxanthin (0.099 ␮g g−1 ), 5,6-epoxy-␤-carotene (0.92 ␮g g−1 ),
cryptoxanthin (0.24 ␮g g−1 ), 13-cis-␤-carotene (1.99 ␮g g−1 ), ␤carotene (21.67 ␮g g−1 ), and 9-cis-␤-carotene (10.17 ␮g g−1 ), in
B. odorata. In B. odorata, ␤-criptoxantine was the predominant
carotenoid followed by ␤-carotene (Beskow et al., 2014). Additionally, Sganzerla (2010) found the bioactive lipids ␤, ␥, and
␦-tocopherols, part of the vitamin E complex, in pulp of B. odorata
and B. eriospatha.
L-ascorbic acid content ranged from 38 to 73 mg 100 g−1 in the
pulp of B. capitata (Faria et al., 2008a,b), 3.1 to 39 mg 100 g−1 in B.
odorata (Pereira et al., 2013a,b; Schwartz, 2008; Sganzerla, 2010),
and 21.34 mg 100 g−1 in B. eriospatha (Sganzerla, 2010). The oxalate
content (871 ␮g g−1 ) found in B. capitata and other palms of the
Arecaceae family is considered low and therefore of limited risk for
human health (Broschat and Latham, 1994). Additionally, the leaves
of B. capitata were found to be free of cyanogenic compounds (Lewis
and Zona, 2000).
3.5.2. Volatile compounds
Ferrão (2012) identified and quantified volatile compounds in
the pulp of B. odorata. The pulp presented 77 compounds that
128
J.F. Hoffmann et al. / Scientia Horticulturae 179 (2014) 122–131
Table 3
Bioactive compound content (mg 100 g−1 fw) of Butia fruits.
Compound
B. odorata
B. eriospatha
B. capitata
Reference
Total phenolic
Gallic acid
Hydroxybenzoic acid
Coumaric acid
Ferulic acid
Caffeic acid
(+)-catechin
(−)-epicatechin
Quercetin
Kaempferol
Total anthocyanin
Keracinin
Kuromanin
L-ascorbic acid
636–9062̂60–398
86.0–234
54.0–150
0.44–2.01
0.88–4.12
0.46–4.02
0.84–2.18
9.69–52.0
0.86–4.09
0.83–4.20
1.05–25.13
0.76–19.9
0.06–5.02
23–63
278*
51.0
25.0
–
0.75
–
–
8.97
1.98
–
0.73
–
0.05
21
163–259† ; 78–166‡
–
–
–
–
–
–
–
–
–
–
–
–
38–73
Total carotenoid¶
␤-carotene
2.80–5.5
0.53–2.17
1.73
–
1.10–4.39
0.52–2.28
9-cis-␤-carotene
5,6-epoxy-␤-carotene
13-cis-␤-carotene
␤-criptoxanthine
Lycopene
Zeaxanthine
Phytoene
Phytofluene
␣-carotene
␨-carotene
Poly-cis-␥-carotene
Lutein
Total tocopherol
␦-tocopherol
␥ + ␤-tocopherol
1.02
0.09
0.20
2.07–2.67
0.01–0.10
0.01–0.27
–
–
–
–
–
0.47
0.43
0.07
0.36
–
–
–
–
–
–
–
–
–
–
–
–
0.15
0.05
0.10
–
–
–
–
–
–
0.18–0.86
0.15–0.74
0–0.01
0.02–0.13
0.18–1.01
–
–
–
–
Beskow et al. (2014); Pereira et al. (2013a,b) *
Beskow et al. (2014); Sganzerla (2010)
Beskow et al. (2014); Sganzerla (2010)
Beskow et al. (2014); Sganzerla (2010)
Beskow et al. (2014)
Beskow et al. (2014)
Beskow et al. (2014)
Beskow et al. (2014); Sganzerla (2010)
Beskow et al. (2014); Sganzerla (2010)
Beskow et al. (2014)
Beskow et al. (2014); Fonseca (2012) **
Beskow et al. (2014); Sganzerla (2010)
Beskow et al. (2014); Sganzerla (2010)
Beskow et al. (2014); Pereira et al. (2013a,b);
Sganzerla (2010); Faria et al. (2008a,b) ***
Beskow et al. (2014); Pereira et al. (2013a,b) ****
Beskow et al. (2014); Faria et al. (2011); Pereira
et al. (2013a,b)
Pereira et al. (2013a,b)
Pereira et al. (2013a,b)
Pereira et al. (2013a,b)
Beskow et al. (2014)
Beskow et al. (2014)
Beskow et al. (2014); Pereira et al. (2013a,b)
Faria et al. (2011)
Faria et al. (2011)
Faria et al. (2011)
Faria et al. (2011)
Faria et al. (2011)
Pereira et al. (2013a,b)
Sganzerla (2010)
Sganzerla (2010)
Sganzerla (2010)
m̂g chlorogenic acid equivalents 100 g−1 fw.
mg B-carotene.100 g−1 fw.
†
mg catechin equivalents 100 g−1 fw.
‡
mg tannic acid equivalents 100 g−1 fw.
§
mg galic acid equivalents 100 g−1 fw.
*
Sganzerla (2010); Jacques et al. (2009); Faria et al. (2008a,b); Genovese et al. (2008).
**
Sganzerla (2010).
***
Genovese et al. (2008); Faria et al. (2008a,b).
****
Faria et al. (2011); Jacques et al. (2009).
¶
were identified in seven chemical classes: 34 esters, 14 alcohols, 5
acids, 12 ketones, 9 aldehydes, 3 lactones, and 2 terpenoids. Esters
stood out quantitatively in the volatile composition of pulp and
are likely the main contributors of the characteristic fruity aroma
of the fruit. Ethyl hexanoate, a known low aroma threshold compound, was the major ester in most samples, greatly impacting B.
odorata aroma.
Aguiar et al. (2014) found a decrease in acetic acid, (E)- and
(Z)-hex-2-enal, methoxyphenyloxime, (E)-␤-ocimene, ␣-fenchene,
and ether methyl octyl and an increase in ethyl hexanoate content as B. capitata fruit matured. Ethyl hexanoate (65.9%), ethyl
butanoate (14.5%), and methyl hexanoate (9.64%) were the predominant aroma volatiles of fully ripe fruit.
Sixty compounds were quantified and identified in fermented
fruit of B. odorata, including: 27 esters, 15 alcohols, 11 acids, 2 lactones, 1 aldehyde, 1 ketone, and 1 terpenoid. The compounds with
the largest positive contribution to flavor were ethyl hexanoate
and 3-methyl-1-butanol, while hexanoic acid was identified as a
potential off flavor (Bernardi et al., 2014).
3.5.3. Antioxidant potential
Antioxidant capacity is widely used as a parameter to characterize different substances and food samples with the ability to
scavenge or neutralize free radicals (Brand-Williams et al., 1995;
Pyrzynska and Pekal, 2013). This capacity is related to the presence
of compounds capable of protecting a biological system against
harmful oxidation through one or more mechanisms, such as free
radical inhibition, scavenging of oxygen singlets, energy absorption, and metal complexation (Canuto et al., 2010; Roesler et al.,
2007; Rufino et al., 2009; Yahia, 2010).
There are several methods for the evaluation of antioxidant
efficiency of pure compounds and plant extracts such as ORAC
(oxygen radical absorbance capacity), FRAP (ferric reducing antioxidant power), CUPRAC (cupric reducing antioxidant capacity),
the 2,2-azinobis (3-ethyl-benzothiazoline-6-sulphonate) radical
cation (ABTS) assay, and the 2,2-diphenyl-1-picrylhydrazyl radical (DPPH) assay. The most common assays are those involving
chromogenic radicals, which in the presence of an antioxidant,
are scavenged resulting in a color change. These reactions can be
monitored spectrophotometricly (Pyrzynska and Pekal, 2013).
Sganzerla (2010) evaluated the antioxidant activity of pulp of B.
odorata and B. eriospatha using the DPPH method, reporting values
of 211.92 and 237.22 mg of Trolox equivalent 100 g−1 , respectively. The author found a positive correlation between antioxidant
activity and ascorbic acid content in B. odorata and a positive correlation between antioxidant activity and total phenolic content in B.
eriospatha. Using the same method, Fonseca (2012) found antioxidant activity of B. odorata ranging from 828.27 to 1295.25 mg
equivalent Trolox g−1 fresh fruit.
No data in the literature was found regarding the biological
effects of Butia or the consumption of these fruits on human
health.
J.F. Hoffmann et al. / Scientia Horticulturae 179 (2014) 122–131
4. Potential applications
Uses of Butia date to pre-historic periods. Currently, its utilization remains limited to foraging, with no commercial or extended
production.
Butia fruit jelly is a product with high commercial value, microbiological stability, and requires simple equipment for preparation
(Fonseca, 2012; Krolow et al., 2010; Krumreich et al., 2010). According to Krolow et al. (2010), the major problems for the making
of these fruit jellies are the fruit acidity, low pectin content, and
high fiber content. Studies evaluating the stability of bioactive compounds (total phenolics, vitamin C, and total carotenoids) after
processing and during storage are needed. The processing of fruit
into ice cream also presents an alternative use of the fruits, showing wide acceptance in sensory ratings (Fonseca and Krolow, 2011;
Gegoski et al., 2013). The oil from Butia seeds was tested on dental self-etching adhesives and showed anti-biofouling performance
against aciduric bacteria, lactobacilli, and Streptococcus mutans
(Peralta et al., 2013).
In addition to the use of leaves as incense and to light fires, the
pulp and leaves of B. purpurascences were reported to be used in
the therapeutic treatment of skin diseases and as an antivenom
(Martins et al., 2014).
Despite the limited number of studies on this genus and species,
we foresee great scientific and technological potential of Butia,
leading to similar results obtained with other palms such as açai
(Euterpe oleracea) in Northern Brazil (Gordon et al., 2012; Heinrich
et al., 2011; Kang et al., 2012).
5. Concluding remarks
This review demonstrates the need for further studies of Butia
species, especially regarding their chemical constituents, mechanism of dispersal, germination, and species differentiation.
Compounds in the fruits, in both the pulp and seed, may provide
health benefits such as antioxidant, antiproliferative, and antimicrobial activity, which suggest opportunities for its use in the food
and pharmaceutical industries. It is pertinent to highlight that studies addressing genetic improvement, whether in relation to plant
productivity or fruit quality attributes, should receive more attention.
Acknowledgments
The authors would like to thank SCIT-RS, Fapergs, Capes, and
CNPq for research funding.
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