Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

Flowering time and harvest on floral morphology and production

of hermaphrodite flowers in the cashew tree Anacardium occidentale

(Anacardiaceae)

Jéssica Soares Pereira¹*; https://orcid.org/0000-0002-1662-7591

Júlio César DoVale¹; https://orcid.org/0000-0002-3497-9793

Ingrid Pinheiro Machado¹; https://orcid.org/0000-0001-7486-1063

José Wagner Silva Melo¹; https://orcid.org/0000-0003-1056-8129

Francisco das Chagas Vidal Neto2; https://orcid.org/0000-0001-9412-6955

Dheyne Silva Melo2; https://orcid.org/0000-0001-9961-7286

Levi de Moura Barros2; https://orcid.org/0000-0002-0379-9685

1. Departamento de Fitotecnia, Universidade Federal do Ceará, Campus do Pici–Blocos 805 e 806, 60356-000, Fortaleza,

Ceará, Brasil; jessicasoaresp99@gmail.com (*Correspondence), juliodovale@ufc.br, ingridpin03@hotmail.com,

wagnermelo@ufc.br

2. Embrapa Agroindústria Tropical, Rua Dra. Sara Mesquita, 2270, Pici, 60511-110, Fortaleza, Ceará, Brasil; vidal.

neto@embrapa.br, dheyne.melo@embrapa.br, levi.barros@embrapa.br

Received 09-VIII-2022. Corrected 14-XI-2022. Accepted 27-I-2023.

ABSTRACT

Introduction: Morphological parameters of flowering are fundamental in the reproductive process of plants, but

this subject is poorly explored in the cashew tree Anacardium occidentale.

Objective: To determine the influence of the flowering and harvest period on floral parameters, and to identify

association with hermaphrodite flowers in the dwarf cashew.

Methods: For the 2018 and 2019 harvests in 120 samples we measured number of male/hermaphrodite/abnor-

mal flowers; panicle biomass, length, maximum width, and ramifications at 30, 45 and 60 days for 360 samples

in total.

Results: The harvest effect was not significant. Panicle length and width (at 30 days), had the greatest contribu-

tions to the production of hermaphrodite flowers. The presence of male flowers (at 45 days), and the panicle

length and number of primary branches (at 60 days) were the main factors at their respective periods.

Conclusions: The emission of hermaphrodite flowers responds negatively to male flowers. Variations in flower-

ing compromise the production of hermaphrodite flowers and the flowering structure.

Key words: Anacardium occidentale; floral biology; panicle length; flowering times; flowering; panicle width.

RESUMEN

Período de floración y cosecha en la morfología floral y producción de flores hermafroditas

en el árbol de marañón, Anacardium occidentale (Anacardiaceae)

Introducción: Parámetros morfológicos de la floración son fundamentales en el proceso reproductivo de las

plantas, sin embargo, el tema es poco explorado en el árbol de marañón Anacardium occidentale.

https://doi.org/10.15517/rev.biol.trop..v71i1.52092

BOTANY AND MYCOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

INTRODUCTION

Flowering in plants indues a succession

of subsequent events, including anthesis, fruc-

tification, development, and fruit maturation,

which determine the propagation of species and

can contribute to crop improvement via genetic

recombination (Bhagwan & Reddy, 2014). In

fruit trees, flowering is an important reproduc-

tive phenomenon that marks the commence-

ment of fruit production (Olubode et al., 2018).

It typically progresses in four stages: floral

induction, floral initiation, floral differentia-

tion, and flowering. The length of the flower-

ing phase is dependent on both genotype and

environmental conditions (Saroj et al., 2014).

In cashew, flower production is a gradual pro-

cess that can be influenced by morphological

mechanisms in the panicles, interfering in the

final proportion of male and hermaphrodite

flowers that remain until the final development

of the fruits in the crop.

The plant family Anacardiaceae comprises

more than 700 species (Barros, 1988; Naka-

sone & Paul, 1998). Prominent among these

is the cashew tree Anacardium occidentale

Linnaeus, a species native to Northeastern

Brazil (Barros et al., 2002), although is now

cultivated in more than 30 countries worldwide

(FAOSTAT, 2021). Classified as an andromo-

noic species, the cashew tree has both male and

hermaphroditic flowers (Barros & Crisóstomo,

1995). The inflorescence of A. occidentale is a

panicle, with variable shapes, sizes, quantities,

and proportions of male and hermaphrodite

flowers (Adiga et al., 2019; Sousa et al., 2007).

Flowering in cashew is directly associated

with vegetative growth fluxes, both of which

occur concomitantly during certain periods

and with different intensities. The period of

maximum floral differentiation and flowering

occurs mainly during the dry season (Frota &

Parente, 1995; Wunnachit & Sedgley, 1992)

and can extend to up to 7 months (Sousa et al.,

2007) due to the heterogeneity of the orchards,

which undergo variations in the length of the

flowering period (Barros, 1988). Under suit-

able growing conditions with well-distributed

rainfall, cashew trees can flower more than

once a year (Nambiar, 1979; Ohler, 1979; Wait

& Jamieson, 1986), with flowering and fruiting

during the dry season conferring the distinct

advantage of a lower incidence of pests and

diseases, thereby reducing potential damage

during these vulnerable phenological phases

(Wunnachit & Sedgley, 1992). However, low

levels of relative humidity during flowering and

fruiting can reduce not only stigma receptivity

but also pollen viability (Sturtz, 1981), and

increase the likelihood of the abortion of devel-

oping fruits (Wunnachit & Sedgley, 1992).

Cashew flowering normally begins at the

end of the rainy season, after the emergence

of a new growth stream, although its onset and

duration are strongly dependent on external

environmental factors, including temperature,

Objetivo: Determinar la influencia de la floración y periodos de cosecha sobre parámetros florales, e identificar

asociaciones con flores hermafroditas en el marañón enano.

Métodos: Para las cosechas de 2018 y 2019 en 120 muestras, medimos el número de flores masculinas/herma-

froditas/anormales; biomasa de panícula, largo, ancho máximo, y ramificaciones a los 30, 45 y 60 días, un total

de 360 muestras.

Resultados: El efecto de la cosecha fue insignificante. Longitud y ancho de la panícula (a los 30 días), tuvo la

mayor contribución a la producción de flores hermafroditas. La presencia de flores masculinas (a los 45 días), y

el largo de panícula y número de ramas primarias (a los 60 días) fueron los principales factores en sus periodos

respectivos.

Conclusiones: La emisión de flores hermafroditas responde negativamente a flores masculinas. Variaciones en

la floración afecta la producción de flores hermafroditas y estructura de floración.

Palabras clave: Anacardium occidentale; biología floral; longitud de panícula; tiempos de floración; floración;

ancho de panícula.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

radiation and precipitation, which occur in the

planting area during the period. of flowering

(Saroj et al., 2014). Such factors can compro-

mise the structural aspects of flowering, inter-

fering with the sexual expression of flowers

(Sousa et al., 2007), promoting the develop-

ment of panicles that present a large number of

male flowers and low emission of hermaphro-

dite flowers, negatively influencing production

(Madail et al., 2012).

Although cashew trees produce an abun-

dance of flowers, less than 10 % of these are

hermaphroditic and, among these, approxi-

mately 85 % are fertilized. Of these fertilized

flowers, however, only 4 % to 6 % will subse-

quently undergo development to maturity and

bear fruit, with the remainder being eliminated

at different stages of production (Mog et al.,

2018). Accordingly, the characteristics of flow-

ers and flowering affect not only those of the

fruits, but also their production. Nevertheless,

despite the important practical implications of

floral biology, this is an aspect that has hardly

been investigated in A. occidentale. In this

study, we tried for the first time to answer some

behaviors. How can the association between

the expression of hermaphrodite flowers and

other morphological parameters of panicles in

dwarf cashew trees be explained? Furthermore,

from an evolutionary point of view, how is the

influence of the evaluation period of flowering

and harvests established on the floral param-

eters of the culture? These parameters are

important, because the time of flowering evalu-

ation is important to explain the production

of hermaphrodite and male flowers during the

different flowering periods of the species, and

they can also exhibit different behaviors under

the influence of the crops and their respective

environmental characteristics.

MATERIALS AND METHODS

Experimental area: Data were col-

lected from dwarf-type cashew plants that

were vegetatively propagated and cultivated

under rain-fed conditions in an experimental

field of Embrapa Agroindústria Tropical, in

the municipality of Pacajus in Ceará, Brazil

(4º10’21” S & 38°27’50” W). The predominant

climate of the region is humid hot tropical (Aw,

in the Köppen Geiger climate classification),

with an average annual temperature of 26 °C

and an average annual rainfall of 1 020 mm

(Kottek et al., 2006). The meteorological data

recorded in the experimental area in 2018 and

2019 are presented in Fig. 1.

Genetic material: Ten clones of the dwarf

cashew tree were selected in progeny experi-

ments based on phenotypic evaluations of their

suitability to edaphoclimatic conditions in the

state of Ceará (Table 1). The selected clones

differed with respect to several characteristics,

including chestnut and peduncle productiv-

ity, average weight of chestnut and peduncle,

peduncle color and shape, plant size, early

flowering, fruiting, and the duration of these

productive periods and almond yield.

TABLE 1

Identification of dwarf cashew clones

and their referred origins

Clones Origins

END II 6-9 Dwarf x Dwarf hybrid

PRO 555/2 Free-pollinated progeny

PRO 553/2 Free-pollinated progeny

A + A 134/1 Dwarf x Dwarf hybrid

HB 116/4 Dwarf x Dwarf hybrid

HB 33 Dwarf x Dwarf hybrid

PRO 740/4 Free-pollinated progeny

PRO 106/2 Free-pollinated progeny

CCP 76 Commercial Clone

BRS 226 Commercial Clone

Experimental design: Experiments

were performed based on a randomized block

design, with 10 treatments (genotypes), three

replications, and four plants per plot. One plant

in each plot was selected for examination. The

block structure and the genotype factor were

not considered in the analysis, thereby enabling

extrapolation of results for the dwarf cashew

tree. In this way, each plant represented a rep-

etition (30 repetitions). The five-year-old plants

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

were spaced in rows of 8 m × 6 m, and all cul-

tural management practices, including pruning,

fertilization, weed control, and pest and disease

control, were carried out in accordance with

the recommendation for commercial cashew

cultivation under rain-fed conditions (Serrano

& Oliveira, 2013).

Evaluations: For the morphological char-

acterization of panicles, we took into con-

sideration the period of maximum floral

differentiation and full flowering that occurred

in the 2018 and 2019 growth seasons. As a ref-

erence point, for the purposes of evaluations,

we defined the commencement of the repro-

ductive period of each genotype as day 30 after

marking panicles in the field.

For each of the focal plants, three panicles

were selected and marked at each of the

cardinal points (North, South, East, and West)

of the tree, one for each flowering time assess-

ment (30, 45, and 60 days after the beginning of

flowering), totaling 12 panicles per plant.

During each of the two flowering seasons,

four panicles (one from each quadrant of the

plant) were detached from the plants, packed

in labeled plastic bags to prevent dehydration,

and placed in plastic boxes. After which they

were transported to the evaluation room at the

Laboratory of Plant Genetics and Breeding of

Embrapa Agroindústria Tropical, for morpho-

logical characterization of the floral structures.

According to Violle et al. (2007), the

functional traits of plants can be defined as the

morphological, physiological and phenological

characteristics that directly impact the perfor-

mance reproduction of individuals, thus influ-

encing their aptitude for a given environmental

Fig. 1. Meteorological information from the experimental area in the two crops evaluated for the years A. 2018. B. 2019 in

the municipality of Pacajus–CE, Brazil, 2021.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

condition. Based on its attributes, which repre-

sent the different values that a given functional

trait can assume (Appendix), the characteriza-

tion of the floral structures of A. occidentale L.

(Fig. 2) was carried out through the evaluation

and classification of panicles, according to the

following parameters: Number of male flow-

ers: counting the number of male flowers with

approximately 10 stamens (male organ of the

flower), with one stamen being more developed

than the others. Number of hermaphrodite flow-

ers: counting the number of hermaphrodite

flowers with small stamens and a pistil, the

latter of which is generally longer than the

most developed stamen and is attached to the

ovary. Number of abnormal flowers: counting

the number of flowers with an arrangement

similar to that of male or hermaphrodite flow-

ers, but with no pistil or larger stamen. Panicle

biomass: determined by weighing the panicles.

Panicle length: the distance from the first node

to the apex. Maximum panicle width: the maxi-

mum distance between the ends of the panicle

branches. Number of panicle branches: count-

ing the number of branches originating from

the main axis of the panicle (primary branches)

and from the branches that develop from the

primary branches (secondary branches).

Variation in floral parameters as a func-

tion of time-point and harvest: Variations in

floral parameters with respect to the effect of

time (time-point of flowering evaluation) and

harvest were determined by analysis of vari-

ances, followed by Tukey’s HSD and Fisher’s

exact tests (F test), respectively. Analyses of

variance were conducted using the following

genetic-statistical model:

Eq. (1): Yijk = m + di + sj + dsij + eijk,

Fig. 2. Classification, floral structures and evaluations performed on dwarf cashew plants in the 2018 and 2019 harvests

in the experimental area of the municipality of Pacajus, Ceará, Brazil. A. Male flowers on panicles. B. Floral details and

structures of male flowers. C. Hermaphrodite flowers in panicles. D. Floral details and structures of hermaphrodite flowers.

E. Flowers classified as abnormal for presenting malformation, absence, or duplication of floral structures. F. Biomass. G.

length. H. width evaluations of panicles. I. General structure of panicles. J. Branches classified as primary. K. Branches

classified as secondary. An = Anther; St = Stamen; Pt = Petals; Sg = Stigma; Sl = Style; Pb = Primary branches; Sb =

Secondary branches.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

where Yijk is the observation referring to the i-th

flowering time-point, in the j-th harvest, in the

k-th replication (block); m is the general mean;

di is the effect of the i-th season (i = 30, 45, or

60 days after flowering), considered as fixed;

sj is the effect of the j-th harvest (j = 2018 and

2019), considered as random, where sj~NID (0,

σ2); dsij is the effect of the interaction between

the i-th flowering season in the j-th crop, con-

sidered as random, where dsij~NID (0, σ2) and

eijk is the random experimental error associated

with the Yijk observation.

The period effect was considered as fixed

in view of the particularities of each flowering

period in the crop, specifically to enable con-

clusions to be drawn regarding panicle behavior

in each of the three evaluation periods. The har-

vest effect was considered as random, with the

aim of reaching broader conclusions regarding

the responses of the cashew tree flowering,

regardless of the agricultural year (harvest)

considered. Block structure and the genotype

factor were not considered in the analysis, to

enable extrapolation of the results for the dwarf

cashew tree. Thus, influences associated with

flowering times of the two evaluated crops

could be extrapolated to the whole, as time

× harvest interactions have a random effect

(Resende, 2005).

The relationships between floral param-

eters and the expression of hermaphrodite

flowers: The data obtained for panicle morpho-

logical parameters were subjected to correlation

analysis using linear regression, implemented

with SAS® statistical software (SAS, 2002).

Given that we detected minimal seasonal varia-

tion in these morphological parameters (7 of

the 8 floral parameters showed no significant

differences), they were grouped in order to con-

struct more robust statistical models. Data were

subjected to multiple regression analyses using

the proc reg procedure, selection=stepwise,

with hermaphrodite flowers as the dependent

variable (y), and the numbers of male and

abnormal flowers; the inflorescence biomass;

the length and width of the inflorescence; and

the numbers of primary and secondary branch-

es as independent variables.

Initially, all eight floral morphological

parameters were included, adjusted by stepwise

regressions, to explain the dependent variable

(number of hermaphrodite flowers). Using the

statistically significant model, the parameters

were selected according to the flowering season

and higher coefficient values in the regression

analysis, and thereafter, the data obtained for

the parameters selected by stepwise regression

were plotted as a function of the hermaphrodite

flower number.

RESULTS

Variation of floral parameters depend-

ing on the time-point and harvest: With

the exception of panicle biomass, significant

effects of the time-point (T) (P < 0.05 and P

< 0.01) were observed for all other assessed

floral parameters, whereas in contrast, with

the exception of the number of secondary

branches, no significant effects were detected

with regards to harvest. However, period of

evaluation × harvest interactive effects were

found to be significant for most of the assessed

parameters (Table 2). These significant interac-

tive effects can be attributed to the variation in

all floral parameters in the year 2018 and an

absence of variation in almost all parameters in

2019 (Fig. 3).

During the 2018 harvest, the number of

hermaphrodite and male flowers, panicle fresh

biomass, and length and width of panicles

showed similar trends, with higher mean values

observed at 30 days after the commencement of

flowering and lower mean values at 45 and 60

days after the initiation of flowering (Fig. 3A,

Fig. 3B, Fig. 3D, Fig. 3E and Fig. 3F). With

regards to the number of abnormal flowers, we

observed mean values higher than 30 and 45

days and lower than 60 days after the onset of

flowering (Fig .3 C).

The number of primary branches showed

lower mean values at 30 days after the com-

mencement of flowering and higher mean

values at 45 and 60 days (Fig. 3G). Compared

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

TABLE 2

P-values for the effects of season, crop and interaction (season x crop) of floral morphology characters of dwarf cashew tree,

evaluated in two years of cultivation, in the municipality of Pacajus, CE, 2021

Effects GL P-values

FH FM FA BP CP LP RP RS

Season (S) 2< 0.0001 < 0.0001 < 0.0001 0.0846 0.0003 < 0.0001 0.0084 < 0.0001

Harvest (H) 1 0.5739 0.8867 0.0534 0.6036 0.1374 0.2878 0.0965 0.0225

S x H 2< 0.0001 < 0.0001 0.0004 0.0913 < 0.0001 0.0042 0.0076 0.4999

Values in bold are significant (P < 0.05) or (P < 0.01) by the F test. FH–hermaphrodite flowers; FM–male flowers; FA–abnormal

flowers; BP–panicle biomass; CP–panicle length; LP–panicle width; RP–primary branches; RS–secondary branches.

Fig. 3. Dwarf cashew plants showed higher flower production at the beginning of the flowering season. Boxplots of panicle

floral morphology characters. A. Hermaphroditic flowers. B. Male flowers. C. Abnormal flowers. D. Panicle biomass. E.

Panicle length; F. Panicle width; G. Primary branches. H.* Secondary branches) of dwarf cashew, analyzed in two harvests

(2018 and 2019), in the municipality of Pacajus-CE, for the three periods after the beginning of flowering (30, 45 and 60

days). Only significant differences are shown. Different letters indicate significant differences between seasons for the same

season by the Tukey test (P < 0.05). (*) indicates that there was a significant effect of crops (isolated effect).

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

with 30 days after the initiation of flowering,

mean values of number of secondary branches

were higher at 45 days and lower at 60 days

(Fig. 3H). With respect to the 2019 harvest,

we detected significant variations only for the

number of male flowers, with lower mean val-

ues at 30 days and higher mean values at 45 and

60 days after the beginning of flowering.

The effect of harvest was detected only

with respect to the number of secondary

branches (Fig. 3H), with the average number of

secondary branches in the 2019 harvest being

higher than that observed in the 2018 harvest.

The relationship between floral param-

eters and the expression of hermaphrodite

flowers: Different models were obtained to

explain the expression of hermaphrodite flow-

ers at the three evaluation times (30, 45, and

60 days after the commencement of flowering)

(Table 3). For the 30-day evaluation, the param-

eters contributing most to an explanation for

hermaphrodite flower expression were panicle

length and width, which together accounted

for 47 % (R² = 0.47) of the numerical varia-

tions in hermaphrodite flowers. For the 60-day

evaluation, panicle length and the number of

primary branches were found to make the high-

est contribution, collectively explaining 37 %

(R² = 0.37) of the numerical variation in her-

maphrodite flowers. We were, however, unable

to obtain a significant model for the 45-day

evaluation period. Interestingly, although nei-

ther significant nor marginally significant (P =

0.102), the floral parameter that appeared to be

the most important at this time-point was the

number of male flowers.

In terms of the accumulation of hermaph-

rodite flowers, a contrasting result was obtained

with respect to panicle dimensions (length and

width) during the first flowering season (30

days after the commencement of flowering),

with the number of hermaphrodite flowers

being positively correlated with panicle width.

However, we detected a negative correlation

with panicle length (Fig. 4A, Fig. 4B).

Furthermore, there was a negative correla-

tion between male and hermaphrodite flowers

at 45 days after the onset of flowering (Fig.

4C). This negative effect of an increase in

the production of male flowers suppresses

the development of hermaphrodite flowers,

the production of which was observed to be

inversely proportional to the increase in the

number of male flowers in panicles.

When evaluated after 60 days of flowering,

it was found that the greater the panicle length,

the higher the number of hermaphroditic flow-

ers per panicle (Fig. 4D). At this time-point, we

also detected an inverse correlation between

number of primary branches and number of

hermaphrodite flowers produced in inflores-

cences (Fig. 4E).

DISCUSSION

The findings of this study revealed that

with the exception of panicle biomass, all

assessed morphological parameters of cashew

panicles showed significant effects with respect

TABLE 3

Contributions of dwarf cashew panicles morphological characters in the dynamics of explaining the emission of

hermaphrodite flowers collected in two harvests, in the municipality of Pacajus, CE

Flowering season Characters R² (partial) Estimated R² (model) F Test P

Panicle length (1) 0.2621 -6.3992 - - -

Panicle width (2) 0.2089 6.6411 - - -

(1)*(2) - - 0.4710 25.37 < 0.001

45 Male flowers (1) 0.0454 -0.0354 0.0454 2.76 0.102

Panicle length (1) 0.3449 1.0027 - - -

Primary Branches (2) 0.0333 -1.0174 - - -

(1)*(2)* - - 0.3782 17.34 < 0.001

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

to evaluation time-point. Contrastingly, for

most parameters, we were unable to detect any

significant differences between the two harvest

seasons, which can be explained by the fact that

the annual variations in abiotic factors were not

pronounced enough to promote quantitative

changes among the panicle parameters. The

number of hermaphrodite flowers produced

by cashew trees is dependent on parameters

associated with the vegetative structures of

panicles. The contribution of this factor to the

expression of these flowers was found to differ

Fig. 4. Different floral morphological attributes explained the emission of hermaphrodite flowers in panicles. Stepwise

regression analysis correlating morphological characters and the production of hermaphrodite flowers in dwarf cashew

panicles in 2018 and 2019 crops, in the municipality of Pacajus, CE. Assessments performed at 30 days. A. Panicle length

x hermaphrodite flowers, y = -1.6892x + 63.3501, R2 = 0.0267. B. Panicle width x hermaphrodite flowers, y = 3.7713x –

39.2612, R2 = 0.2095; P = <0.001), 45 days. C. Male flowers x hermaphrodite flowers, y = -0.0356x + 14.4965, R2 = 0.0460;

P = 0.102), and 60 days. D. Panicle length x hermaphrodite flowers, y = 0.8702x -11.0664, R2= 0.3445. E. Primary branches

x hermaphrodite flowers, y = 0.4163x + 1.4416, R2 = 0.0068; P = <0.001) after flowering starts.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

when evaluated at three different time-points

during the flowering period.

The cashew tree growth pattern alternates

between vegetative and reproductive phases,

whose onset and duration differ according to

the genotype, as these phases are regulated by

genetic and environmental factors (Saroj et

al., 2014). Among the environmental factors,

those that have the most pronounced effects on

cashew growth are the amount of solar radia-

tion and the availability of water, as they play

a particularly important role in the opening of

flower buds, triggered by the hormonal activity

expressed in the plants (Saroj et al., 2014).

The higher rate of flower production

observed at the beginning of the flowering

season in the 2018 crop, with similar trends in

the first evaluation period at 30 days, is consis-

tent with corroborates the results of research

carried out by Sharma (2009), who claimed to

have reported a greater production of male and

female flowers (hermaphrodites) in early flow-

ering. Similarly, Wunnachit and Sedgley (1992)

found that the majority of hermaphrodite flow-

ers were produced during the first 21 days of

the flowering period.

According to Parente et al. (1991), in the

semi-arid regions of the tropics, dwarf cashew

trees are known to display peak flowering in

August, with greater flowering intensities at

the beginning of the reproductive period. This

behavior among panicles can be explained by

the occurrence of higher temperatures during

this period of the season. Our failure to detect

any significant differences among the three

periods evaluated in 2019 can be ascribed to the

fact that transitions in the phases of the plant

life cycle are regulated by genetic development

programs, modulated by environmental and

endogenous stimuli (Ravindra, 2014). Thus, we

suspect that the environmental stimuli experi-

enced by cashews during the 2019 season were

not strong enough to promote any pronounced

differences among parameters.

According to the meteorological data

obtained for the experimental area during

the 2018 and 2019 harvests, the period from

August to November corresponds to the period

with the lowest relative humidity, high average

temperatures (close to 30 °C), and high solar

radiation levels. These factors predictably con-

tribute to greater variation in the floral biology

of plants, affecting the emission of hermaphro-

dite flowers during the typical period of flower-

ing of the crop (Fig. 1). In 2018, low amounts

of rainfall were recorded during the months of

August and December, which, together with the

low relative humidity and high average tem-

peratures, probably altered the microclimate

of the area, thereby influencing the pattern of

flowering. The occurrence of high temperatures

during this period, along with the differences

in humidity and solar radiation, enabled the

cashew trees to channel larger amounts of pho-

toassimilates to the formation of new branches,

thus providing a physical structure of healthy

branches for the support and favorable distribu-

tion of inflorescences.

At the onset of the flowering cycle, pan-

icles assign a large proportion of the energy

contained in photoassimilates to the growth of

the main stem and the production of primary

branches, which serve as a structural basis for

the development of secondary branches. This

development of secondary branches becomes

more pronounced after 45 and 60 days of flow-

ering, when there is a greater incidence of solar

radiation and higher temperatures together with

greater panicle growth. In this regard, sev-

eral species exhibit gradual phenotypic changes

during the flowering period, corresponding to

variations determined by meteorological vari-

ables (Wadgymar et al., 2015). Changes in tem-

perature during the dry season, together with a

reduction in the length of the photoperiod, are

considered factors most conducive to the pro-

motion of flowering (Silvério & Lenza, 2010).

The production of flowers during periods of

lower rainfall is assumed to be a survival strat-

egy, which, in addition to avoiding damage to

the flowers from heavy rainfall (Janzen, 1967;

Sousa & Cunha, 2018), makes the flowers more

conspicuous to potential pollinators, thereby

enhancing pollination.

In the present study, we found that the

emission of hermaphroditic flowers was

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

associated with the characteristics of other

structural parameters of panicle morphology,

which influenced the proportions of these

flowers throughout the three evaluation peri-

ods. Structural parameters of panicle length

and width, primary/secondary branches, and

production of male flowers in panicles were

identified as the most important determinants.

In this sense, several studies have evaluated the

influence of panicle structure on fruit produc-

tion and quality, which are directly dependent

on the density of fertile flowers suitable for pol-

lination. Vidal-Neto et al. (2013) reported that

panicle structure is an important factor, as it

directly or indirectly influences the production

of hermaphroditic flowers. Thus, the oscillation

of climatic variables, mainly temperature, solar

radiation, and humidity, between the evalu-

ation periods, contributed to changes in the

development pattern of hermaphrodite flowers

in the panicles, reflecting changes in the avail-

able amounts of nutrients and photosyntates in

the plants directed to the formation of flowers

(Olsen & Martin, 1980).

We identified associations between differ-

ent floral components and the emission of her-

maphrodite flowers throughout the evaluation

period. At 30 days after the onset of flowering,

the length and width of the panicle were found

to affect the number of hermaphroditic flowers,

which to a large extent was expected, given

that an increase in panicle dimensions provides

mechanical support for better distribution of

branches in the inner structure of the inflo-

rescence. The flowering process is affected by

the structural characteristics of the aerial parts

(Ravishankar, 2014), with the composition

of floral buds being altered by the degree of

branch extension. Although this direct growth

relationship is clear in cashew, the panicle does

not grow in width and length simultaneously,

which is taken to be a strategy of the plant to

evenly distribute the photoassimilates among

panicle, as the larger the panicle, the greater the

potential number of hermaphroditic flowers.

An increase in the width of the inflores-

cences promotes a greater allocation of pho-

tosynthetic resources to the panicle structure,

thereby initiating a greater expansion in the

primary and secondary branches, the structures

of which are essential for the effective distribu-

tion of new flowers. This broad inflorescence

structure contributes to enhancing the pollina-

tion and fertilization of hermaphrodite flowers,

which develop throughout the period of bloom-

ing. Conversely, the development of narrower

panicles would limit the access of pollinators

to flower buds, thereby leading to pollination

deficits, and thus potentially compromising

the desired productivity (Freitas, 2014). A

further characteristic that tends to preclude

the production of hermaphrodite flowers is the

development of male flowers. Male flowers,

when present in larger quantities in these inflo-

rescences, can interfere with the proportion of

hermaphrodite flowers exposed to pollinators.

With the progression of flowering time,

we found that after 45 days, there was a direct

relationship between the emission of hermaph-

rodite flowers and the trend in male flower

production. During this period, there was peak

in male flower production, which accordingly

represents greater competition for photoassimi-

lates. Flowers are normally supplied via the

formation of new buds, which serve as a

depot for carbohydrates in the subterranean

and aerial organs of the plants (Baptist et al.,

2009). Therefore, if the production of flowers

is sustained by the provision of photoassimi-

lates, large amounts of which are consumed in

the production of male flowers, there will be a

reduction in the availability of these resources

for the production of hermaphrodite flowers.

Another important feature to be highlighted in

this context is that flowers of the cashew tree

abort during flowering. Consequently, floral

parameters that might initially contribute to

flower development may no longer make a

prominent contribution when evaluated later

during the flowering period, as the number of

hermaphrodites tends to decline as a conse-

quence of abortion.

The production of large numbers of male

flowers consumes large amounts of energy, the

expenditure of which results in a reduction in

production efficiency (Araújo, 2013; Pinheiro

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

et al., 1993). In this regard, anacardiaceous

species are typically characterized by prolific

flower abortion and, accordingly, it can be con-

jectured that over time, the length and width

of panicles might no longer explain the num-

ber of hermaphroditic flowers present. At 60

days into the flowering period, it is likely that

the composition of the continually developing

inflorescences comprise not only hermaph-

roditic, but also male and abnormal flowers.

During this period, increases in the length and

width of panicles occur as a consequence of the

sustained input of photoassimilates throughout

the flowering phase, which enables the different

cashew genotypes to maintain the growth of

vegetative structures. This is consistent with the

findings of Saroj et al. (2014), who observed

that the proportion and emission of hermaph-

rodite flowers differed significantly from the

development of new branches, due to the veg-

etative growth of the species.

In the present study, we detected positive

and negative linear correlations between the

morphological attributes of panicles and the

emission of hermaphrodite flowers, reinforcing

the fact that cashew flowers show associations

with the morphological structure of panicles,

irrespective of the evaluation period. Positive

linear correlations with structural components

at the beginning of the reproductive period

indicate that during this period, plants require

a sufficient quantity of photoassimilates to

strengthen development of the panicle struc-

ture, contributing to an increase in panicle

width. Furthermore, the negative linear corre-

lation between panicle length and the produc-

tion of hermaphroditic flowers indicates that

the greater the extension in panicle length, the

lower the production of hermaphrodite flowers.

In our evaluation of flowering at day

45, we detected a negative linear correlation

between the number of male and hermaphro-

dite flowers, indicating that a higher density

of male flowers tends to suppress the produc-

tion of hermaphrodite flowers, and vice versa,

due to competition for plant photoassimilates.

Evaluations performed at day 60 revealed posi-

tive linear correlations between the length and

number of primary branches, and the produc-

tion of hermaphrodite flowers in the panicles.

On the basis of these findings, we can deduce

that as flowering progresses, there is a conver-

sion of energy to promote an increase in the

growth of the panicle main axis, thereby posi-

tively influencing the production of hermaph-

rodite flowers in the branches. This, in turn, can

probably be attributable to the fact that a larger

panicle area is conducive to increased photo-

synthesis, thereby channeling larger amounts of

photosynthates for flower production.

With the advance of flowering, floral struc-

tures show significant development, concomi-

tant with a gain in fresh plant biomass and an

increase in branch expansion. Given their influ-

ence on the structure of panicles, the primary

branches of panicle have a notable influence

on the proportion of hermaphrodite flowers,

with the number of these branches showing a

positive correlation with the number of her-

maphrodite flowers. The greater the number of

primary branches, the greater the support base

for the development of new secondary branch-

es, which in turn facilitates the development of

new floral apices.

The flowering distribution in cashew was

found to be strongly dependent on the develop-

ment of the morphological parameters of pani-

cles, which changed over time. These alterations

promoted changes in the vegetative structures

of the species associated with an elongation of

the internodes, which subsequently developed

into productive branches, with the produc-

tion of an inflorescence in the terminal part

of the newly formed bud. Thus, the emission

of hermaphrodite flowers was altered due to

characteristic variations in the floral and repro-

ductive morphology of the crop, consequently

determining the potential production.

Collectively, our findings thus indicate

that changes in the vegetative structure at dif-

ferent time-points in the flowering period and

the variation between different harvest seasons

lead to differences in the parameters of panicle

floral morphology. Another important finding

is that the numbers of hermaphrodite flowers

were mainly influenced by panicle length and

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

width, the presence of primary branches, and

the production of male flowers in panicles. A

greater number of hermaphrodite flowers in the

panicles is fundamental in the selection of early

dwarf cashew tree clones.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is

no conflict of interest of any kind; and that

we followed all pertinent ethical and legal

procedures and requirements. All financial

sources are fully and clearly stated in the

acknowledgements section. A signed document

has been filed in the journal archives.

ACKNOWLEDGMENTS

The authors are grateful to Empresa

Brasileira de Agropecuária (EMBRAPA), to

Coordination for the Improvement of Higher

Education Personnel–Brazil (CAPES), and

Postgraduate Program in Agronomy/Plant Sci-

ence of the Federal University of Ceará for

conducting this research.

APPENDIX

Morphological characters of panicles and their relevance to the fitness of Anacardium occidentale

Morphological Characters Relevance to plant fitness

Number of male flowers Pollen grain production. The formation of the pollen grain plays a role in fertilization and

fruit production. A greater energy expenditure of the plant for the production of pollen,

results in a low productive efficiency.

Number of hermaphrodite

flowers

Fruit production. In addition to the male gamete (pollen grain), which serves as food for

visiting insects, this type of flower also has the female gamete (egg), located inside the

ovary. Therefore, these flowers result in the production of fruits.

Number of abnormal flowers They have a stamen arrangement similar to that of staminate and hermaphrodite flowers;

however, they do not present the most developed stamen or the pistil, being, therefore,

denominated as anomalous. They affect the concentration of fertile flowers that are suitable

for pollination. Differences related to floral structures contribute to variability in flower

quality, pollination efficiency, and uneven production.

Panicle biomass Allocation of photosynthetic resources that are directed to production of new floral gems.

The panicle area favors the increase of photosynthesis, energy conversion and the targeting

of photosyntates for the production of flowers.

Panicle length Panicle length extension. The expansion of the forming panicle affects the number of

flowers on the lateral and sublateral branches.

Maximum panicle width Greater dimensioning of photosynthetic resources in the partitioning of the panicle

structure, promoting greater expansion of primary and secondary branches, whose

structure is essential for the distribution of new flowers.

Number of panicle branches Physical structure of healthy branches for the support and distribution of inflorescences.

They serve as a structural basis for the development of primary and secondary branches,

which will support the development of flower buds.

REFERENCES

Adiga, J. D., Muralidhara, B. M., Preethi, P., & Savadi, S.

(2019). Phenological growth stages of the cashew

tree (Anacardium occidentale L.) according to the

extended BBCH scale. Annals of Applied Biology,

175(2), 246–252.

Araújo, J. P. P. (2013). Agronegócio do caju: práticas e

inovações. Embrapa.

Baptist, F., Tcherkez, G., Aubert, S., Pontailler, J. Y., Cho-

ler, P., & Nogués, S. (2009). 13C and 15N allocations

of two alpine from early and late snowmelt reflect

their different growth strategies. Journal of Experi-

mental Botany, 60(9), 2725–2735.

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

Barros, L. M. (1988). Biologia floral, colheita e rendimen-

to. In V. P. M. S. Lima (Eds.), A cultura do cajueiro no

Nordeste do Brasil (pp. 301–319). Escritório Técnico

de Estudos Econômicos do Nordeste.

Barros, L. M., & Crisóstomo, J. R. (1995). Melhoramento

genético do cajueiro. In J. P. P. Araújo, & V. V. Silva

(Eds.), Cajucultura: modernas técnicas de produção

(pp. 73–93). Embrapa Agroindústria Tropical.

Barros, L. M., Crisóstomo, J. R., Paiva, J. R., Cavalcanti,

J. J. V., & Araújo, J. P. P. (2002). Cajueiro. In C. H.

Bruckner (Eds.), Melhoramento de fruteiras tropicais

(pp. 159–176). Visoça.

Bhagwan, A., & Reddy, Y. N. (2014). Induction of flowe-

ring in fruit crops–Physiological and plant architectu-

ral implications. In H. Ravishankar, V. K. Singh, A. K.

Misra, & M. Mishra (Eds.), Physiology of Flowering

in Perennial Fruit Crops (pp. 24–47). Central Institu-

te for Subtropical Horticulture (ICAR).

FAOSTAT (Base de Datos Estadísticos Corporativos de la

Organización para la Agricultura y la Alimentación).

(2021). Crops Production Cashew nuts, with shell.

http://www.fao.org/faostat/en/#search/cashew.

Freitas, B. M. (2014). Plano de manejo para polinização da

cultura do cajueiro: conservação e manejo de polini-

zadores para agricultura sustentável, através de uma

abordagem ecossistêmica. Funbio.

Frota, P. C. E., & Parente, J. I. G. (1995). Clima e

fenologia do cajueiro. In J. P. P. Araújo, & V. V.

Silva (Eds.), Cajucultura: modernas técnicas de pro-

dução (pp. 43–54). Empresa Brasileira de Pesquisa

Agropecuária.

Janzen, D. H. (1967). Syncronization of sexual reproduc-

tion of trees within the dry season in Central América.

Evolution, 21(3), 620–637.

Kottek, M., Grieser, J., Beck, C., Rudolf, B., & Rubel, F.

(2006). World map of the Köppen-Geiger climate

classification updated. Meteorologische Zeitschrift,

15(3), 259–263.

Madail, R. H., Herter, F. G., & Leite, G. B. (2012). Influen-

ce of floral structure and flower bud quality on pro-

ductivity and fruit shape in different apple cultivars.

Revista Brasileira de Fruticultura, 34(3), 686–694.

Mog, B., Adiga, D., & Nayak, M. G. (2018). Role of

plant growth hormones in cashew: Key strategy for

modifying crop performance. International Journal

Current Microbiology and Applied Sciences, 7(7),

1470–1484.

Nakasone, H. Y., & Paull, R. E. (1998). Tropical Fruits.

CAB International.

Nambiar, M. C. (1979). Cashew. In P. T. Alvim, & T. T.

Kozlowski (Eds.), Ecophysiology of tropical crops

(pp. 461–85). Academic Press.

Ohler, J. G. (1979). Cashew. Koninklijk Instituut voor de

Tropen.

Olsen, K. L., & Martin, G. C. (1980). Influence of apple

bloom date on maturity and storage quality of ‘star-

king delicious’ apples. American Society for Horticul-

tural Science,105(2), 183–186.

Olubode, O. O., Joseph-Adekunle, T. T., Hammed, L. A.,

& Olaiya, A. O. (2018). Evaluation of production

practices and yield enhancing techniques on produc-

tivity of cashew (Anacardium occidentale L.). Fruits,

73(2), 75–100.

Parente, J., Frota, P., Melo, F., & Costa, J. (1991). Com-

portamento de crescimento e desenvolvimento de

cajueiros precoce e comum no litoral do Ceará.

Revista Brasileira de Fruticultura, Jaboticabal, 13(2),

107–111.

Pinheiro, F. F. M., Crisóstomo, J. R., Parente, J. I. G.,

Melo, F. I. O., & Almeida, J. I. L. (1993). Desenvol-

vimento de caracteres da panícula e frutificação de

duas populações de cajueiros comum e anão precoce

(Anacardium occidentale). Boletim de Pesquisa (N°

8, 1993, 1–24).

Ravindra, V. (2014). Physiological signals, environmental

cues and their interactions for induction of flowering

in perennials–lessons for mango. In H. Ravishankar,

V. K. Singh, & A. K. Misra, M. Mishra (Eds.), Phy-

siology of flowering in perennial fruit crops (pp.

59–73). Central Institute for Subtropical Horticulture

(ICAR).

Ravishankar, H. (2014). Assimilate partitioning and trans-

formations in some perennial fruit crops with due

focus on mango (Mangifera indica L.): dynamics of

shoot-root communication in reproductive phenolo-

gy-an appraisal. In H. Ravishankar, V. K. Singh, A. K.

Mistra, & M. Mishra (Eds.), Physiology of flowering

in perennial fruit crops (pp. 3–23). Central Institute

for Subtropical Horticulture (ICAR).

Resende, M. D. V. (2005). Métodos estatísticos ótimos na

análise de experimentos de campo, Colombo. Embra-

pa Florestas.

Saroj, P. L., Nayak, M. G., & Meena, R. K. (2014). Phy-

siology of flowering, fruit and nut development in

cashew. In H. Ravishankar, V. K. Singh, A. K. Misra,

& M. Mishra (Eds.), Physiology of Flowering in

Perennial Fruit Crops (pp. 105–114). Central Institu-

te for Subtropical Horticulture (ICAR).

SAS. (2002). Institute SAS/STAT User’s guide. (Version

8.02). SAS Institute Inc., North Carolina, USA.

Serrano, L. A. L., & Oliveira, V. H. (2013). Aspectos botâ-

nicos, fenologia e manejo da cultura do cajueiro. In J.

P. P. Araújo (Eds.), Agronegócio do caju: práticas e

inovações (pp. 77–165). Embrapa.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52092, enero-diciembre 2023 (Publicado Mar. 02, 2023)

Sharma, D. (2009). Distribution of staminate and herma-

phrodite flowers and fruit-set in the canopy of cashew

genotypes. Journal of Horticultural Sciences, 4(1),

45–49.

Silvério, D. V., & Lenza, E. (2010). Fenologia de espécies

lenhosas em um cerrado típico no Parque Municipal

do Bacaba, Nova Xavantina, Mato Grosso, Brasil.

Biota Neotropica, 10, 205–216.

Sousa, D. G. D., & Cunha, H. F. D. (2018). Population

structure, spatial distribution and phenology of Ana-

cardium humile A. St.-Hil. (Anacardiaceae) in cerra-

do stricto sensu. Hoehnea, 45(3), 450–467.

Sousa, L. B. D., Feitoza, L. D. L., Gomes, R. L. F., Lopes,

Â. C. D. A., Soares, E. B., & Silva, E. M. P. D. (2007).

Aspectos de biologia floral de cajueiros anão precoce

e comum. Ciência Rural, 37(3), 882–885.

Sturtz, J. D. (1981). Cashew. In P. E. Page (Eds.), Tropical

tree fruits for Australia (pp. 53–9). Department of

Primary Industries Conference and Workshop Series.

Vidal-Neto, F. C., Barros, L. M., Cavalcanti, J. J. V., &

Melo, D. S. (2013). Melhoramento genético e cultiva-

res de cajueiro. In J. P. P. Araújo (Eds.), Agronegócio

caju: práticas e inovações (pp. 481–505). Embrapa.

Violle, C., Navas, M. L., Vile, D., Kazakou, E., Fortunel,

C., Hummel, I., & Garnier, E. (2007). Let the concept

of trait be functional! Oikos, 116(5), 882–892.

Wadgymar, S. M., Cumming, M. N., & Weis, A. E. (2015).

The success of assisted colonization and assisted gene

flow depends on phenology. Global Change Biology,

21(10), 3786–3799.

Wait, A. J., & Jamieson, G. I. (1986). The cashew:

its botany and cultivation. Queensland Agricultural

Journal, 112(5), 253–257.

Wunnachit, W., & Sedgley, M. (1992). Floral structure and

phenology of cashew in relation to yield. Journal of

Horticultural Science, 67(6), 769–777.