PHENOLOGICAL SYNCHRONICITY OF Byrsonima pachyphylla A. Juss. AND B. verbascifolia (L.) DC. (MALPIGHIACEAE) AND ITS RELATION WITH CLIMATE SEASONALITY

ABSTRACT Phenology is defined as the study of the timing of biological events and the biotic and abiotic factors that trigger them. This study reports a description of the phenology of Byrsonima pachyphylla and B. verbascifolia in an ecotonal area between the Cerrado and Amazonia biomes in the Brazilian state of Tocantins, to contribute to a better understanding of their autoecology in this region. Two populations of 15 adult individuals of each species, randomly selected in a Cerrado area in Porto Nacional, Tocantins, were surveyed for 12 months. Percentages were estimated of leaf flush, young, mature, and senescent leaves (vegetative phenology), flower buds, open flowers, green and ripe fruits (reproductive phenology) present in the canopy, as well as the synchrony of the reproductive phenophases. The vegetative and reproductive phenological events were seasonal and occurred mainly at the end of the dry season and during the transition from the dry to the rainy season. Considering the vegetative and reproductive phenology, B. pachyphylla was classified as “evergreen with continuous growth” and as a late-flowering species, whereas B. verbascifolia was classified as “evergreen with seasonal growth” and as an early-flowering species. The reproductive phenological activity of the species exhibited high synchrony. The results suggest that the vegetative and reproductive events are peculiar to each species and represent effective strategies for their survival in the Cerrado, which is markedly seasonal.


INTRODUCTION
Phenology is defi ned as the study of the timing of biological events, and what stimulates them, in relation to biotic and abiotic factors, as well as the interrelationship of the phenophases characterized by these events in the same and in diff erent species (Lieth, 1974;Grossman, 2023).There are still few works published on plant phenology for the state of Tocantins, so this article is of great importance for understanding the autoecological strategies of Byrsonima pachyphylla and B. verbascifolia in this ecotonal region between the Cerrado and Amazon biomes.
The main events considered in most studies of plant phenology are leaf sprouting, leaf fall, fl owering and fruiting (Lenza and Klink, 2006;Sivéro and Lenza, 2010;Shi et al., 2015;Urbaez et al., 2015;Santos et al., 2022).Based on this information, it is possible to make predictions about the phenological strategies of the species regarding the reproductive period, deciduousness and vegetative growth cycle of the species (Grossman, 2023).
Leaf renewal in the Cerrado normally occurs in the dry season (Oliveira and Gibbs, 2000), but it can also happen in response to other environmental conditions, such as variations in relative humidity and temperature, so it can refl ect the phenotypic plasticity of species.The temporal distribution of fl owering and fruiting is strongly linked to the incidence of appropriate environmental conditions for fl ower pollination and seed dispersal, which aff ect the reproductive success of the species.In this context, several studies have documented fl owering and fruiting patterns in diff erent plant communities and analyzed their correlation with biotic and abiotic factors (Rathcke and Lacey, 1985).
In the case of seasonal ecosystems, there is evidence that abiotic factors have an important infl uence on phenological variables (Tooke and Battey, 2010).For this reason, the seasonal response of phenophases has been related to diff erent exogenous factors, such as temperature, evaporation, radiation (Ranieri et al., 2012), photoperiod (Morellato et al., 2000) and precipitation (Belo et al., 2013).
The vast majority of studies carried out in the Cerrado have investigated the behavior of vegetation at the community level (Lenza and Klink, 2006;Silvério and Lenza, 2010).A recurrent criticism of phenological studies at this level is that these studies can fail to note the diversity of seasonal responses of phenophases at the species level (Singh and Kushwaha, 2005).For this reason, an alternative method of dealing with this problem is to divide community patterns into subsets of species that are internally homogeneous in terms of sharing common life histories (Marquet et al., 2004;Azeria et al., 2011).Malpighiaceae, the family to which the species examined in this study belong, is monophyletic and comprises approximately 77 genera and 1,300 species, distributed in the tropics (Davis and Anderson, 2010), of which 85% are restricted to the Neotropical region (Davis et al., 2001).In Brazil, at least 150 species of the genus Byrsonima Rich have been found (Cronquist, 1991).
Byrsonima fruits are popularly called murici and are important as foods.They can be consumed in natura or used as a basis for the production of beverages (Aniceto et al., 2021;Souza et al., 2020), sweets (Neri-Numa et al., 2018) and cereal bars (Vinhal et al., 2022).Murici extracts are also used in the manufacture of pharmaceutical products such as medicines and cosmetics (Neri-Numa et al., 2018;Saldanha et al., 2016).
B. pachyphylla A. Juss.and B. verbascifolia (L.) DC., both popularly known as murici, are species native to Brazil and have life forms that vary from bushes to trees (Mamede and Francener, 2016).
Our objective is to describe the vegetative and reproductive phenology of B. pachyphylla and B. verbascifolia in order to generate information about the behavior of these two species occurring in an area of Cerrado stricto sensu in the municipality of Porto Nacional, Tocantins, thus contributing to a better understanding of their autoecology.

Study area
The study was carried out at the São Judas Tadeu farm, located in an area of Cerrado stricto sensu in the municipality of Porto Nacional, Tocantins,Brazil (10º 48'31''S and 48º 26'52''W).The soil in this area is classifi ed as Red-Yellow Latosol, with the presence of rocky fragments.The region's climate is classifi ed as Aw according to the Köppen scale (1928), with hot and rainy summers and cooler dry winters.The average annual rainfall in the last nine years was approximately 1,800 mm, concentrated between November and April (INMET, 2015).

Description of the studied species
Byrsonima pachyphylla is an arboreal species that has a trunk covered with thick and broken bark, peeling off in irregular plates.The leaves are single, opposed, crossed, narrow-obovate to lanceolate, leathery and/or glossy and have trichomes on the underside (Silva-Junior, 2005;Hughes, 2021).
B. verbascifolia is a shrub whose trunk is crooked, covered with thick, rough bark.The leaves are single, concentrated towards the end of the branches, shortpetiolate with a tomentose-villous surface on both sides (Lorenzi, 1998).
The infl orescences of both species are composed of simple terminal racemes, with hermaphrodite fl owers having fi ve pairs of elaiophores.The color of the petals varies from yellow at the beginning of anthesis to reddish brown in the senescence period.Its fruits are of the globose drupe type, having a fl eshy mesocarp with juicy and sweet pulp (Lorenzi, 1998;Lorenzi, 2006).
The species were identifi ed in the fi eld with the help of specialized taxonomists.Samples of botanical materials of B. pachyphylla and B. verbascifolia were deposited in the Tocantins Herbarium (HTO) of Federal University of Tocantins, under registration numbers 10,947 and 10,948, respectively.

Phenological studies
Two populations of 15 adult individuals of each species (in the reproductive phase), approximately 1.5 km apart, were studied.Individuals were marked with aluminum tags numbered from 1 to 30.Field expeditions for phenological observations were carried out at intervals of 15 days, from May 2014 to April 2015.
The presence or absence of phenophasesvegetative (budding, young, adult and senescent leaves); reproductive (fl owering -presence of fl ower buds at any stage of development and fl owers in anthesis); and fruiting (green and ripe fruits)were recorded in fi eld worksheets.The percentage of each phenophase in the canopy was visually estimated based on Fournier (1974) through the intensity index using a semi-quantitative scale from 0 to 4 with 25% intervals, where 0 represents total absence of the phenophase.
The species were classifi ed into vegetative phenological groups according to Sarmiento and Monastério (1983), as modifi ed by Lenza and Klink (2006).These are based on temporal aspects of occurrence of the phenophases of leaf fall and production, as well as the degree of deciduousness of individuals.Reproductive phenological groups were also established according to the period of the year in which fl owering occurred (Sarmiento and Monastério, 1983).Classifi cation of fl owering type was performed according to Gentry (1974).

Data analysis
The phenological events were evaluated by means of circular histograms containing the percentage of individuals of each species in each month, showing the vegetative and reproductive phenophases.Using the Activity Index proposed by Bencke and Morellato (2002), the synchrony of the reproductive phenological events was estimated.Less than 20% of the individuals in the phenophase were asynchronous, 20% to 60% of the individuals were synchronous and more than 60% of the individuals were highly synchronous.
Analyses of circular distributions were performed for the phenological events in order to determine the average angle of occurrence of these events and the measures of dispersion around this angle.The average angle corresponds to the average date of occurrence of the events.The concentration (r) of the event around this date ranged from 0 to 1, related to the length of the mean vector.The uniformity of the circular distribution of events throughout the year was evaluated using the Rayleigh (Z) test (Zar, 1999).
The Shapiro-Wilk test was performed to verify the normality of the data, and since the data had nonparametric distribution, Spearman correlations were calculated between the phenophases and the climatic variables rainfall (mm), average monthly temperature (°C), relative air humidity (%) and pitch evaporation (mm).Meteorological records were provided by the National Meteorology Institute (INMET, 2015) (Figure 1).Circular distribution analyses were performed using the demo version of the Oriana 2.0 program.The Shapiro-Wilk test and Spearman correlation test were performed using the R version 3.0.2software.

Reproductive and vegetative phenology
Byrsonima pachyphylla showed the phenophases of budding and young leaves almost throughout the year, with peaks in September and October.The average dates of occurrence of these phenophases were October 4th and 15th, respectively (Figures 2   A and B, Table 1).The presence of adult leaves was verifi ed throughout the year in all individuals, with crowns being in category 4, that is, from 76 to 100% adult leaves.The average date of occurrence of this phenophase was January 30th (Figure 2 C).Senescent leaves were also observed throughout the year, with the highest amounts recorded in June.The average date of occurrence of this phenophase was August 10th (Figure 2 D).This species was classifi ed as "evergreen with continuous growth" (Sarmiento and Monastério, 1983;Lenza and Klink, 2006), since it did not present evident deciduousness and the production of leaves occurred for a prolonged period.Of the vegetative   1, Table 2).
The emission of fl oral buds and fl owers by B. pachyphylla plants occurred between May and November, with peak in July (Figures 2 E and F).The presence of unripe fruits was verifi ed between July and December, with higher production in September (Figure 2 G).Ripe fruits were recorded between October and December (Figure 2H).The average dates of occurrence of the reproductive phenophases were July 8th and 20th for fl oral buds and open fl owers, respectively, August 24th for unripe fruits and November 17th for ripe fruits.The fl owering and fruiting pattern was annual.The synchrony between the reproductive phenophases was high, since 90% of the individuals presented the occurrence of fl owering and 86.6% of the individuals exhibited fruiting in the peak season.B. pachyphylla was considered a late fl owering species, fl owering mainly in the dry period.In addition, its fl owering was classifi ed as the "big bang" type, with a single peak of short duration  and high synchrony between individuals (Gentry, 1974).Among the reproductive phenophases of B. pachyphylla, fl ower buds, open fl owers and unripe fruits correlated positively with evaporation and negatively with relative humidity.
In Byrsonima verbascifolia, the phenophases of budding and young leaves occurred between August and April, with peaks being recorded on November 30th and December 7th, respectively (Figures 3 A  and B). Adult and senescent leaves were observed throughout the year, without defi ned peaks (Figures 3 C and D).This species was classifi ed as "evergreen with seasonal growth" (Sarmiento and Monastério, 1983;Lenza and Klink, 2006), since it showed evident leaf deciduousness and leaf production coincided with the climatic seasonality of the study area.The average dates of occurrence of these phenophases were May 11th and September 17th, respectively.Of the vegetative phenophases, only young leaves showed a positive correlation with precipitation, while senescent leaves had negative correlation with temperature.
The presence of fl ower buds in B. verbascifolia was observed between August and November, with a peak in October (Figure 3 E).Flowers were recorded between the months of July and November, with greater production in October and November (Figure 3 F).The presence of green fruits was verifi ed between August and April, with greatest production in January (Figure 3 G).Ripe fruits were recorded from December to April (Figure 3H).The average dates of occurrence of the reproductive phenophases were October 20th and 23rd for fl oral buds and open fl owers, respectively, January 1st for unripe fruits and February 7th for mature fruits.
The fl owering and fruiting pattern of B. verbascifolia was annual.The synchrony of the reproductive phenophases was also considered high, with 90% of the individuals presenting fl owering and 80% of the individuals exhibiting the fruiting phenophase.The production of fl owers occurred in the transition between the dry and rainy seasons, so the plants were considered to have a kind of early fl owering.These plants also presented a single peak of short duration and high synchrony between individuals, and thus their fl owering was also classifi ed as "big bang" (Gentry, 1974).The phenophase of fl ower buds of B. verbascifolia correlated positively with evaporation and negatively with precipitation and relative humidity; unripe and ripe fruits showed positive correlations with precipitation and relative humidity and negative correlation with evaporation.

DISCUSSION
The synchronicity and seasonality of the vegetative phenophases were in accordance with the tendency found in some Cerrado species to lose leaves in the dry period and later to start issuing leaf shoots (Alberton et al., 2014;Souza et al., 2015).Similar results were also recorded in phenological studies of Byrsonima crassifolia and B. coccolobifolia (Barbosa et al., 2012), B. intermedia and B. pachyphylla (Boas et al., 2013), and even B. verbascifolia (Araújo et al., 2014).
The presence of adult leaves recorded in both species throughout the study period is common in evergreen species (Franco et al., 2005), and is considered a strategy extensively used by species to combat various environmental constraints (Lenza and Klink, 2006) that can be caused by the climatic seasonality of the Cerrado biome.
Leaf senescence, followed by abscission in the dry period, recorded in the species studied, can be considered an adaptation to the decrease in water availability, as a mechanism for saving and effi ciently using water by plants to increase their survival during these unfavorable periods (Lenza and Klink, 2006;Grossman, 2023).There may also be translocation of nutrients during the senescence period or even a reduction in transpiration caused by leaf abscission (Mantovani and Martins, 1988).
Cerrado species have shown variations in their vegetative phenological behavior depending on the region studied (Franco et al., 2005;Lenza and Klink, 2006).When studying the phenology of B. pachyphylla in a Cerrado area in the state of Mato Grosso, Silvério and Lenza (2010) classifi ed this species as "always green with seasonal growth", characterized by leaf fall and budding at the end of the dry period and beginning of the rainy season, a result diff erent from that observed by us.Lenza and Klink (2006), investigating the vegetative phenological behavior of B. verbascifolia in the Federal District, classifi ed the species as "brevideciduous", also diff ering from our observation.
The most striking characteristics observed by these authors were the complete replacement of the crown during the dry period and the fact that during this period the plants had only a few leaves in the process of formation and senescence.These diff erences may be related to the strong phenotypic plasticity of Cerrado species resulting from the diversity of biotic and abiotic factors found in this biome.
Regarding the reproductive dynamics, marked seasonality was also verifi ed in both species studied (fl owering in periods of greater evaporation and temperature [dry season] and fruiting in periods of greater relative humidity and precipitation [rainy season]).This is in accordance with the behavior recorded in other studies for several other Cerrado species (Lenza and Klink, 2006;Silvério and Lenza, 2010;Araújo et al., 2014).
Peak fl owering in the dry season and fruiting in the wet season by B. pachyphylla have also been recorded in other studies in Cerrado areas, namely in Nova Xavantina, Mato Grosso (Silvério and Lenza, 2010), and in Campo Grande, Mato Grosso do Sul (Boas et al., 2013).The reproductive phenology of B. verbascifolia observed in the present study was similar to that recorded in a Cerrado area in Brasília, Federal District (Lenza and Klink, 2006) and in an area of Tabuleiro in Maceió, Alagoas (Araújo et al., 2014).This seasonality was found in other species of the genus studied in Cerrado areas: B. coccolobaefolia, B. sericea and B. verbascifolia in the Araripe National Forest in the municipality of Barbalha, Ceará (Costa et al., 2004); B. rotunda in Urbano Santos, Maranhão (Mendes et al., 2011) and also in B. crassifolia (L.) and B. coccolobifolia in Boa Vista, Roraima (Barbosa et al., 2012).
The high synchrony of the fl owering phenophase registered in the studied species can be considered a strategy to guarantee reproductive success.This pattern is common in entomophilous species (Primack, 1980), and may increase the attraction of pollinating agents that promote cross-pollination, thus contributing to increased gene fl ow between diff erent individuals, and consequently ensuring greater fruit production.
The occurrence of fl owering in the dry season observed in the studied species has advantages, such as coincidence with the period of greatest activity of pollinators and the decrease in fl orivory (Rathcke and Lacey, 1985), in addition to the reduction of mechanical damage to fl owers that can be caused by rain (Fernandes et al., 2012).
The ripening of zoochoric fruits during the rainy season (as observed in the studied species) is important for the maintenance of these fruits, as their attractiveness can remain for a longer period, thus increasing the chances of dispersion (Mantovani and Martins, 1988;Batalha and Mantovani, 2000;Grossman, 2023).This seasonal fruiting pattern was recorded in other studies with diff erent woody species in Cerrado areas (Batalha and Mantovani, 2000).

CONCLUSION
The vegetative and reproductive phenological events of Byrsonima pachyphylla and B. verbascifolia are peculiar to each of these species, which makes them strategically synchronic and effi cient for their survival in the ecotone between the Cerrado and Amazon biomes, which is markedly seasonal.In addition, there was no overlap between the peaks of the reproductive phenophases of the species, a possible way to avoid the sharing of pollinators and seed dispersers at the interspecifi c level, thus increasing the reproductive success and consequently the maintenance of the species.

AUTHOR CONTRIBUTIONS
Andressa Cavalcante Meireles wrote the paper obtained and discussed the statistical, experimental, and estimated data.Ageu da Silva Monteiro Freire, Wagner de Melo Ferreira and Rodney Haulien Oliveira Viana supported the writing of the paper.

ACKNOWLEDGMENTS
Federal University of Tocantins (UFT) provided logistical support.The fi rst author received a master's grant from the Offi ce to Coordinate Improvement of Higher Education Personnel (CAPES).
We dedicate this work with all our love to Wagner de Melo Ferreira ✝ , who will be forever in our hearts.

Figure 2 -
Figure 2 -Histograms of the circular distribution of vegetative and reproductive phenology of Byrsonima pachyphylla.A) budding; B) young leaves; C) adult leaves; D) senescent leaves; E) fl ower buds; F) open fl owers; G) green fruits and H) ripe fruits from May 2014 to April 2015 in an area of Cerrado stricto sensu, Porto Nacional, Tocantins, Brazil.The vector indicates the average date of the event and the average phenological event concentration around this time.Figura 2 -Histogramas das distribuições circulares da fenologia vegetativa e reprodutiva de Byrsonima pachyphylla.A) brotação; B) folhas jovens; C) folhas adultas; D) folhas senescentes; E) botões fl orais; F) fl ores abertas; G) frutos verdes e H) frutos maduros no período de maio/2014 a abril/ 2015 em uma área de Cerrado stricto sensu, Porto Nacional, Tocantins, Brasil.O vetor indica a data média do evento fenológico e a concentração média do evento em torno desta data.

Figure 3 -
Figure 3 -Histograms of the circular distribution of vegetative and reproductive phenology of Byrsonima verbascifolia.A) budding; B) young leaves; C) adult leaves; D) senescent leaves; E) fl ower buds; F) open fl owers; G) green fruits and H) ripe fruit from May 2014 to April 2015 in an area of Cerrado stricto sensu, Porto Nacional, Tocantins, Brazil.The vector indicates the average date of the event and the average phenological event concentration around this time.Figura 3 -Histogramas das distribuições circulares da fenologia vegetativa e reprodutiva de Byrsonima verbascifolia.A) brotação; B) folhas jovens; C) folhas adultas; D) folhas senescentes; E) botões fl orais; F) fl ores abertas; G) frutos verdes e H) frutos maduros no período de maio/2014 a abril/2015 em uma área de Cerrado stricto sensu, Porto Nacional, Tocantins, Brasil.O vetor indica a data média do evento fenológico e a concentração média do evento em torno desta data.