What triggers phenological events in plants under seasonal environments? A study with phylogenetically related plant species in sympatry

Abstract In this study, we evaluated variation in vegetative and reproductive phenological events of four phylogenetically related plant species subjected to a seasonal environment. To this aim, we sampled 15 individuals of each plant species every fortnight for one year, between January and December of 2017. To assess when a given phenophase occurred more intensely in the population, the Fournier intensity index was used and the synchrony of individuals of the sample in a given phenological event was estimated using the activity index. The Rayleigh (Z) test was used to determine whether the phenological events have seasonal distribution. The relationship of abiotic factors (photoperiod, precipitation, relative humidity and temperature) with the intensity of phenophases was evaluated for each plant species using generalized linear models (GLMs). The phenophases of all plants showed a seasonal distribution pattern, as well as variation in synchrony of phenophases and specific sets of abiotic factors significantly influenced their phenophases. New leaves, for example, were produced throughout the seasons, with intense leaf fall in the dry season. Flowering periods, on the other hand, did not overlap. Indeed, species exhibited sequential flowering and asynchronous flowering among individuals. Our results suggest that the phenological patterns of four sympatric plant species are directly linked to climatic variables, but different abiotic factors affected different phenophases.

Resumo Neste estudo, avaliamos a variação nos eventos fenológicos vegetativos e reprodutivos de quatro espécies de plantas filogeneticamente relacionadas submetidas a um ambiente sazonal. Para isso, amostramos 15 indivíduos de cada espécie quinzenalmente, pelo período de um ano, entre janeiro e dezembro de 2017. Para avaliar quando uma determinada fenofase ocorreu de modo mais intenso na população foi utilizado o índice de intensidade de Fournier e a sincronia dos indivíduos da amostra em determinado evento fenológico foi estimada utilizando-se o índice de atividade. O teste de Rayleigh (Z) foi usado para determinar se os eventos fenológicos têm distribuição sazonal. A relação dos fatores abióticos (fotoperíodo, precipitação, temperatura e umidade relativa) com a intensidade das fenofases foi avaliada para cada espécie de planta usando modelos lineares generalizados (GLMs). As fenofases de todas as plantas apresentaram um padrão de distribuição sazonal, bem como variação na sincronia das fenofases e conjuntos específicos de fatores abióticos influenciaram significativamente suas fenofases. Folhas novas, por exemplo, foram produzidas ao longo das estações, com intensa queda de folhas na estação seca. Os períodos de floração, por outro lado, não se sobrepuseram. De fato, as espécies exibiram floração sequencial e floração assíncrona entre os indivíduos. Nossos resultados sugerem que os padrões fenológicos das quatro espécies de plantas simpátricas estão diretamente ligados às variáveis climáticas, mas diferentes fatores abióticos afetaram diferentes fenofases.

What triggers phenological events in plants under seasonal environments? A study with phylogenetically related plant species in sympatry / O que desencadeia eventos fenológicos em plantas em ambientes sazonais? Um estudo com espécies de plantas filogeneticamente relacionadas e em simpatria

In this study, we evaluated variation in vegetative and reproductive phenological events of four phylogenetically related plant species subjected to a seasonal environment. To this aim, we sampled 15 individuals of each plant species every fortnight for one year, between January and December of 2017. To assess when a given phenophase occurred more intensely in the population, the Fournier intensity index was used and the synchrony of individuals of the sample in a given phenological event was estimated using the activity index. The Rayleigh (Z) test was used to determine whether the phenological events have seasonal distribution. The relationship of abiotic factors (photoperiod, precipitation, relative humidity and temperature) with the intensity of phenophases was evaluated for each plant species using generalized linear models (GLMs). The phenophases of all plants showed a seasonal distribution pattern, as well as variation in synchrony of phenophases and specific sets of abiotic factors significantly influenced their phenophases. New leaves, for example, were produced throughout the seasons, with intense leaf fall in the dry season. Flowering periods, on the other hand, did not overlap. Indeed, species exhibited sequential flowering and asynchronous flowering among individuals. Our results suggest that the phenological patterns of four sympatric plant species are directly linked to climatic variables, but different abiotic factors affected different phenophases.

Neste estudo, avaliamos a variação nos eventos fenológicos vegetativos e reprodutivos de quatro espécies de plantas filogeneticamente relacionadas submetidas a um ambiente sazonal. Para isso, amostramos 15 indivíduos de cada espécie quinzenalmente, pelo período de um ano, entre janeiro e dezembro de 2017. Para avaliar quando uma determinada fenofase ocorreu de modo mais intenso na população foi utilizado o índice de intensidade de Fournier e a sincronia dos indivíduos da amostra em determinado evento fenológico foi estimada utilizando-se o índice de atividade. O teste de Rayleigh (Z) foi usado para determinar se os eventos fenológicos têm distribuição sazonal. A relação dos fatores abióticos (fotoperíodo, precipitação, temperatura e umidade relativa) com a intensidade das fenofases foi avaliada para cada espécie de planta usando modelos lineares generalizados (GLMs). As fenofases de todas as plantas apresentaram um padrão de distribuição sazonal, bem como variação na sincronia das fenofases e conjuntos específicos de fatores abióticos influenciaram significativamente suas fenofases. Folhas novas, por exemplo, foram produzidas ao longo das estações, com intensa queda de folhas na estação seca. Os períodos de floração, por outro lado, não se sobrepuseram. De fato, as espécies exibiram floração sequencial e floração assíncrona entre os indivíduos. Nossos resultados sugerem que os padrões fenológicos das quatro espécies de plantas simpátricas estão diretamente ligados às variáveis climáticas, mas diferentes fatores abióticos afetaram diferentes fenofases.

Assessment of the differential trade-off between growth, subsistence, and productivity of two popular Indian hybrid mango varieties under elevated ozone exposure.

The multifunctionality of plants is well known to be compromised in the areas experiencing higher concentrations of tropospheric ozone (O3). Mango (Mangifera indica L.) cultivation is essential to the economy of tropical regions, including India. Mango, widely grown in suburban and rural areas, experiences production loss due to air pollutants. Ozone, the most important phytotoxic gas in mango growing areas, warrants an investigation of its effects. Therefore, we assessed the differential sensitivity of mango saplings (two-year-old hybrid and regular-bearing mango varieties, Amrapali and Mallika) at two levels of O3: ambient and elevated (ambient + 20 ppb) using open-top chambers from September 2020 to July 2022. Under elevated O3, both varieties showed similar seasonal responses (winter and summer) for all the growth parameters but differed in their height-diameter allocation pattern. A decrease in stem diameter and an increase in plant height were observed in Amrapali, whereas Mallika showed a reverse response. Early emergence of phenophases was noticed during the reproductive growth of both varieties under elevated O3 exposure. However, these changes were more pronounced in Amrapali. Stomatal conductance was more negatively affected in Amrapali than in Mallika under elevated O3 during both seasons. Furthermore, leaf morpho-physiological traits (leaf nitrogen concentration, leaf area, leaf mass per area, and photosynthetic nitrogen use efficiency) and inflorescence parameters responded variably in both varieties under elevated O3 stress. A decrease in photosynthetic nitrogen use efficiency, further enhanced yield loss which was more pronounced in Mallika than in Amrapali under elevated O3 exposure. The results of this study could be useful in selecting a better-performing variety based on its productivity, which will be economically more beneficial in achieving the goal of sustainable production at the anticipated high O3 levels under a climate change scenario.

Quantifying the reproductive progression of sunflower using FIJI (Image J).

Sunflower (Helianthus annuus L.) is today the third leading oilseed crop in the world and seed yield is a valuable trait for breeders and researchers. The sunflower capitulum is composed of 700 to 3000 individual flowers on a flattered receptacle. Most reproductive stages (R5 to R6) have at least two disc flower phenophase's coexisting in the same receptacle (E1 to E4). Today, researchers in agroecology and breeders manually quantify the number of disc flowers that achieve the anthesis at different developmental stages of the receptacle. The presented method applies a bioinformatic tool to estimate: (1) the number of disc flowers of each phenophase that are constituting the sunflower´s capitula at different reproductive stages and, (2) the number of developing seeds of each sunflower capitulum. The ImageJ software was used as an image-analysis tool on sunflower capitula photographs. A use case and method validation for each presented protocol is provided. This method will contribute to correlation analysis in agroecological studies and also would be useful for the early prediction of seed yield in breeding programs.•This is a simple method for the estimation of the number of disc flowers at each phenophase in the sunflower receptacle.•It is based on integrating the knowledge of sunflower reproductive development with an open-source image analysis platform applied in single workflows.•This is a precise, non-destructive, rapid, and low-cost method; thus, it has the potential to be adopted as a phenotyping tool for sunflower breeding and research in agroecology.

Comportamiento fenológico ex situ de Lippia integrifolia "incayuyo" (Verbenaceae) de una población de base genética amplia / Ex situ phenological behavior of Lippia integrifolia "incayuyo" (Verbenaceae) from a population with a broad genetic base

Abstract: Lippia integrifolia "incayuyo" is an aromatic, sub - woody shrub used in popular medicine, aperitit drinks and compound herb s. Its choleretic, antispasmodic, biocidal, antibacterial and larvicidal activity has been proven. The objective of the work was to register the phenology of a sample of 70 genotypes from a population with a broad genetic base. The phenophases studied were : vegetative growth, flower bud, flowering and fruiting fortnightly for two years. The initiation, intensity and prolongation of the phenophases were evaluated. The moment of full bloom occurs during the second half of December. Taking this date as a refer ence, a differentiated beginning of flowering was evidenced. The results of two campaigns were compared, observing that 70% of the specimens had a similar behavor, standing out some genotypes for presenting an early flowering and longer duration. The recor ded variability suggests that much of it could be due to intrinsic factors of the plant, and therefore, feasible to be selected .

Resumen: Lippia integrifolia "incayuyo" es un arbusto aromático, subleñoso empleado en la medicina popular, bebidas aperitivas y yerbas compuestas. Se ha comprobado su actividad colerética, antiespasmódica, biocida, antibacteriana y larvicida. El objetivo del trabajo fue registrar la fenología d e una muestra de 70 genotipos de una población de base genética amplia. Las fenofases estudiadas fueron: crecimiento vegetativo, botón floral, floración y fructificación quincenalmente durante dos años. Se evaluó inicio, intensidad y prolongación de las fe nofases. El momento de plena floración ocurre durante la segunda quincena de diciembre. Tomando esta fecha como referencia, se evidenció un inicio de floración diferenciada. Se compararon los resultados de dos campañas, observando que el 70% de los ejempla res tuvo un compartimiento semejante, destacándose algunos genotipos por presentar una floración temprana y de prolongación superior. La variabilidad registrada sugiere que gran parte de ésta podría deberse a factores intrínsecos de la planta, y por ello, factible de ser seleccionados.

Bee phenology is predicted by climatic variation and functional traits.

Climate change is shifting the environmental cues that determine the phenology of interacting species. Plant-pollinator systems may be susceptible to temporal mismatch if bees and flowering plants differ in their phenological responses to warming temperatures. While the cues that trigger flowering are well-understood, little is known about what determines bee phenology. Using generalised additive models, we analyzed time-series data representing 67 bee species collected over 9 years in the Colorado Rocky Mountains to perform the first community-wide quantification of the drivers of bee phenology. Bee emergence was sensitive to climatic variation, advancing with earlier snowmelt timing, whereas later phenophases were best explained by functional traits including overwintering stage and nest location. Comparison of these findings to a long-term flower study showed that bee phenology is less sensitive than flower phenology to climatic variation, indicating potential for reduced synchrony of flowers and pollinators under climate change.

Peanut early flowering stage is beneficial to Metarhizium anisopliae survival and control of white grub larvae.

The study aims to determine the timing of application for high efficacy of Metarhizium anisopliae as a biocontrol agent. A field experiment was undertaken with M. anisopliae applied to the soil at five intervals during the peanut crop lifecycle, at seed germination (day 0) through to pod filling period [75 days after sowing (DAS)], and assessed the change of M. anisopliae density by sampling rhizospheric soil, subsequently at regular intervals and testing counts (CFU/g dry soil) through to harvest. The crop was sown into soil with an established white grub population, with larval density determined at harvest when the trial was concluded. Applications at 0, 15 and 30 days in the crop growth cycle, saw M. anisopliae mean propagule counts drop significantly after 15 days before increasing over the following 15-45 days. We observed an elevated mean increase in counts 30-45 days after application at the early flowering stage (30 DAS). Irrespective of application timing, in general, M. anisopliae densities declined to less than the initial 10% in the late stages of peanut development. At harvest, larval densities in all M. anisopliae treatments were significantly less compared to the control, with the highest mortality (72%) in M. anisopliae treatment applied at early flowering (30 DAS). Relationship analysis showed that white grub density was significantly related to peanut yield. A regression of yield on number of damaged pods also supported that treatment at the early flowering caused the highest impact in terms of reducing damage to pods and improving yield. These results suggest that applying M. anisopliae at the early flowering stage optimizes survival of M. anisopliae in the soil profile, meaning greater probability of larvae contacting the pathogen, leading to greater mortality.

Fenología de Crescentia alata (Bignoniaceae) en Guanacaste, Costa Rica

Los estudios fenológicos generan información que contribuye con el conocimiento de las relaciones entre especies y componentes abióticos de los ecosistemas, disponibilidad de alimento para animales y regeneración de cobertura boscosa. Crescentia alata es una especie arbórea abundante en el bosque tropical seco (BTs); su importancia ecológica, cultural y económica ha sido ampliamente reconocida y por eso existe interés en reproducir esta especie, pero antes es necesario conocer detalladamente su desarrollo fenológico. El objetivo de este estudio fue describir la fenología de C. alata en el BTs de Costa Rica. Se seleccionaron 20 árboles reproductivos en el Parque Nacional Santa Rosa para observar las siguientes fenofases: follaje, floración y fructificación por 14 meses entre 2015 y 2016. Esta especie produjo más follaje en junio, máxima floración en junio y octubre y mayor número de frutos maduros en enero. Los patrones fenológicos en C. alata se relacionaron con factores climáticos comunes, sobre todo precipitación, temperatura y humedad relativa. Los resultados más relevantes de este estudio podrían contribuir a la propagación, el manejo adecuado y la conservación de esta especie.

Phenological studies generate information that contributes knowledge on relationships of species and abiotic components of ecosystems, availability of food for animals and regeneration of forest cover. Crescentia alata is an abundant tree species in tropical dry forests; its ecological, cultural and economic importance has been widely recognized and for this reason there is an interest in reproducing this species, but previously it is necessary to understand its detailed phenological development. The aim of this work was to describe C. alata phenology in dry Costa Rican forests. Twenty reproductive trees were selected at the Santa Rosa National Park to observe phenophases (leaf flushing, flower production, and fructification) during 14 months from 2015 to 2016. Most foliage was observed in June, maximal floration in June and October, and the highest ripe-fruit number in January. Phenological patterns in C. alata were related to common climatic factors as rainfall, temperature, and relative humidity; other factors considered were wind speed, and sun radiation. The most significant phenological data registered for C. alata in this work may contribute to a better management and conservation of this species.

Influence of the growth phenophases on the phenolic composition and anti-oxidant properties of Roscoea procera Wall. in western Himalaya.

Roscoea procera Wall. is one of the important Himalayan medicinal plant used in traditional as well as in modern health care system. The present study aimed to find out the influence of different phenophases on the phenolic compounds and anti-oxidant properties by analysing after every week for over 4 months from shoot bud initiation to the preparation of senescence. Concentration of total phenolic content were found to be about 1.5 times higher in preparation of senescence phase (6.10 mg GAE/g dry weight or dw) as compared to vegetative growth phase. Similarly, total flavonoid concentration ranged from 4.36 to 5.65 mg querectin equivalents/g dw. The concentration of selected phenolic compounds, i.e., gallic acid, catechin and p-coumaric acid was quantified by reverse phase-high performance liquid chromatography and varied significantly among the different phenophases. While, anti-oxidant activity was found 2-3 times higher in preparation of senescence phase as compared to vegetative phase. Thus, these results concluded that in R. procera, November month (preparation of senescence phase) could be recommended for extracting optimum level of total phenolics, flavonoids and anti-oxidant activity. These results will be further helpful for obtaining maximum benefits from the species and to reduce pressure on reproductive phase while ensuring its conservation.

Asymmetric effects of cooler and warmer winters on beech phenology last beyond spring.

In temperate trees, the timings of plant growth onset and cessation affect biogeochemical cycles, water, and energy balance. Currently, phenological studies largely focus on specific phenophases and on their responses to warming. How differently spring phenology responds to the warming and cooling, and affects the subsequent phases, has not been yet investigated in trees. Here, we exposed saplings of Fagus sylvatica L. to warmer and cooler climate during the winter 2013-2014 by conducting a reciprocal transplant experiment between two elevations (1,340 vs. 371 m a.s.l., ca. 6°C difference) in the Swiss Jura mountains. To test the legacy effects of earlier or later budburst on the budset timing, saplings were moved back to their original elevation shortly after the occurrence of budburst in spring 2014. One degree decrease in air temperature in winter/spring resulted in a delay of 10.9 days in budburst dates, whereas one degree of warming advanced the date by 8.8 days. Interestingly, we also found an asymmetric effect of the warmer winter vs. cooler winter on the budset timing in late summer. Budset of saplings that experienced a cooler winter was delayed by 31 days compared to the control, whereas it was delayed by only 10 days in saplings that experienced a warmer winter. Budburst timing in 2015 was not significantly impacted by the artificial advance or delay of the budburst timing in 2014, indicating that the legacy effects of the different phenophases might be reset during each winter. Adapting phenological models to the whole annual phenological cycle, and considering the different response to cooling and warming, would improve predictions of tree phenology under future climate warming conditions.

Fenologia do alecrim-pimenta (Lippia sidoides Cham. ) em área de Cerrado, no norte de Minas Gerais, Brasil / Pepper-rosmarin (Lippia sidoides Cham. ) phenology in a Cerrado area in northern Minas Gerais State, Brazil

Este trabalho teve como objetivo descrever o comportamento fenológico de Lippia sidoides Cham., em área de Cerrado, no norte de Minas Gerais, buscando-se subsidiar o processo de domesticação da espécie, por meio do estudo da ocorrência e duração das fenofases vegetativas e reprodutivas da espécie, bem como avaliar a influência dos fatores climáticos da região em cada fenofase, e ainda verificar a sincronia dessas fenofases entre os indivíduos. Vinte indivíduos foram avaliados mensalmente no período de fevereiro de 2007 a fevereiro de 2009, quanto à intensidade e sincronia das fenofases de brotamento, folhas maduras, senescência foliar, floração, frutificação e queda foliar. Houve acentuada periodicidade na ocorrência dos eventos fenológicos foliares, sendo que essa periodicidade acompanhou a estacionalidade climática da região, evidenciando a forte influência dos fatores abióticos, principalmente da precipitação e umidade relativa do ar. O alecrim-pimenta apresentou comportamento caducifólio, com alta taxa de queda foliar durante grande parte do ano. A floração ocorreu no período de fevereiro a abril, enquanto a frutificação alcançou o pico de intensidade no mês de maio. Todas as fenofases apresentaram altos índices de sincronia, sendo esse um fator facilitador do manejo da espécie.

The aim of this work was to describe the phenological behavior of Lippia sidoides Cham. in a Cerrado area in northern Minas Gerais State, Brazil, in order to contribute to the process of domestication of this species by studying the occurrence and duration of its vegetative and reproductive phenophases, evaluating the influence of local climatic factors on each phenophase and investigating the synchrony of these phenophases among individuals. Twenty specimens were monthly evaluated between February 2007 and February 2009 as to intensity and synchrony of the phenophases sprouting, mature leaves, leaf senescence, flowering, fruiting and leaf abscission. There was great periodicity in the occurrence of leaf phenological events according to the local climatic seasonality, highlighting the strong influence of abiotic factors, especially rainfall and relative air humidity. Pepper-rosmarin showed deciduous behavior, with high leaf abscission rate during a great part of the year. Flowering occurred from February to April, whereas fruiting peaked in May. All phenophases had high levels of synchrony, a facilitating factor for the management of this species.

Fenología reproductiva de las especies arbóreas del bosque tropical de Tenosique, Tabasco, México

Reproductive phenology of tree species in the Tenosique tropical forest, Tabasco, Mexico. Between August 2003 and August 2005 we registered the flowering and fruiting of 75 tree species (341 individual trees) in a tropical rain forest at Tenosique, Tabasco, Mexico. Monthly we checked five transects (500 m long; 5 m wide). To test the homogeneity of flowering and fruiting during the year, and between adjacent months, we applied a X² test. The flowering was bimodal, with a highest peak in March and April, coinciding with the dry season, and a second lower peak in July when precipitation is relatively low. The highest number of fruiting tree species occur between May and July, with its peak in May. Each of the most common botanical families showed a particular phenological pattern. Monthly rainfall and the number of species flowering or fruiting were not significantly correlated. This means that trees are flowering and fruiting all year long, with seasonal increases of both phenological phenomena in the dryer periods. We conclude that phenological patterns vary between individuals and between years and are not seasonally correlated. The data we generated are relevant to program the best periods of seed collections according to individual or groups of species, as part of forest management and conservation practices. Rev. Biol. Trop. 56 (2): 657-673. Epub 2008 June 30.

La fenología de 341 árboles que corresponden a 75 especies fue estudiada en las montañas de Tenosique, Tabasco, entre agosto del 2003 hasta agosto del 2005. Para ello, se establecieron cinco transectos de 500 m de largo por cinco metros de ancho, los cuales se evaluaron mensualmente. Si alguno de los individuos de las especies tenía flores o frutos, la especie como un todo fue considerada en floración o fructificación en ese mes. Se aplicaron pruebas de homogeneidad de ji-cuadrada para evaluar la homogeneidad de la floración y fructificación a lo largo del año y por periodos bimensuales. La floración fue bimodal, con un pico de mayor floración de marzo a abril que corresponde a menor precipitación. En julio se presentó un segundo pico de floración con 21 especies, correspondiendo igualmente a un decremento de la precipitación. El mayor número de especies con fruto se presentó entre mayo y junio, el cual no fue significativo estadísticamente. También se analizan los patrones fenológicos de las familias con mayor número de especies, los cuales difirieron entre sí. No se encontró relación entre el número de especies floreciendo o fructificando y la precipitación promedio mensual. Se encontraron picos fenológicos poco marcados debido a que en la zona de estudio la estacionalidad es poco marcada. Los patrones fenológicos varían dentro de una especie, entre años y entre localidades. Los datos que se aportan en el presente trabajo son relevantes para definir los periodos apropiados de recolecta de semillas para la realización de prácticas de manejo y conservación.