Effects of plant size and weather on the flowering phenology of the organ pipe cactus (Stenocereus thurberi)

Background and Aims

Flowering phenology is a critical life-history trait that influences reproductive success. It has been shown that genetic, climatic and other factors such as plant size affect the timing of flowering and its duration. The spatial and temporal variation in the reproductive phenology of the columnar cactus Stenocereus thurberi and its association with plant size and environmental cues was studied.

Methods

Flowering was monitored during 3 years in three populations of S. thurberi along a latitudinal gradient. Plant size was related to phenological parameters. The actual and past weather were used for each site and year to investigate the environmental correlates of flowering.

Key Results

There was significant variation in the timing of flowering within and among populations. Flowering lasted 4 months in the southern population and only 2 months in the northern population. A single flowering peak was evident in each population, but ocurred at different times. Large plants produced more flowers, and bloomed earlier and for a longer period than small plants. Population synchrony increased as the mean duration of flowering per individual decreased. The onset of flowering is primarily related to the variance in winter minimum temperatures and the duration to the autumn–winter mean maximum temperature, whereas spring mean maximum temperature is best correlated with synchrony.

Conclusions

Plant size affects individual plant fecundity as well as flowering time. Thus the population structure strongly affects flowering phenology. Indications of clinal variation in the timing of flowering and reproductive effort suggest selection pressures related to the arrival of migrating pollinators, climate and resource economy in a desert environment. These pressures are likely to be relaxed in populations where individual plants can attain large sizes.Key words: Flowering phenology, optimal timing, plant size, Sonoran Desert, Stenocereus thurberi, temperature     

Vulnerability and determinants of reproductive success in the narrow endemic Antirrhinum microphyllum (Scrophulariaceae)

The breeding system and flowering phenology of the narrow endemic Antirrhinum microphyllum (Scrophulariaceae) were studied in order to assess the main factors affecting female reproductive success and to identify existing or potential threats to the viability of its populations. Hand-pollination experiments showed that A. microphyllum is an allogamous self-incompatible species. In both populations studied, the flowering season was 4 mo long and mean flowering duration per plant was about 1 mo. Peak flower production took place between mid-April and mid-May and overlapped with the period of activity of the main pollinator, Rhodanthidium sticticum (Megachilidae). Estimated mean number of seeds produced per plant was 9391, showing that population viability is not presently limited by seed output. The study of the direct and indirect effects of plant size, phenological traits (first flowering date, flowering duration, and flowering synchrony), and distance to neighbor plants on reproductive success was performed using structural equation modeling (SEM). In both populations, number of flowers and plant size were the main factors that determined the total number of fruits produced by a plant. First flowering date and flowering synchrony also affected fruit production. Multisample comparison of path coefficients for the two populations rejected the possibility that reproductive patterns could be described by one single model.     

Herbarium records identify sensitivity of flowering phenology of eucalypts to climate: Implications for species response to climate change

Flowering phenology is very sensitive to climate and with increasing global warming the flowering time of plants is shifting to earlier or later dates. Changes in flowering times may affect species reproductive success, associated phenological events, species synchrony, and community composition. Long‐term data on phenological events can provide key insights into the impacts of climate on phenology. For Australia, however, limited data availability restricts our ability to assess the impacts of climate change on plant phenology. To address this limitation other data sources must be explored such as the use of herbarium specimens to conduct studies on flowering phenology. This study uses herbarium specimens for investigating the flowering phenology of five dominant and commercially important Eucalyptus species of south‐eastern Australia and the consequences of climate variability and change on flowering phenology. Relative to precipitation and air humidity, mean temperature of the preceding 3 months was the most influential factor on the flowering time for all species. In response to a temperature increment of 1°C, a shift in the timing of flowering of 14.1–14.9 days was predicted for E. microcarpa and E. tricarpa while delays in flowering of 11.3–15.5 days were found for E. obliqua, E. radiata and E. polyanthemos. Eucalyptus polyanthemos exhibited the greatest sensitivity to climatic variables. The study demonstrates that herbarium data can be used to detect climatic signals on flowering phenology for species with a long flowering duration, such as eucalypts. The robust relationship identified between temperature and flowering phenology indicates that shifts in flowering times will occur under predicted climate change which may affect reproductive success, fitness, plant communities and ecosystems.     

Climate changes affecting biotic interactions,phenology, and reproductive success in a savanna community over a 10-year period

Climatic parameters are able to influence the timing of phenological events affecting the degree of synchrony among plant species, their interactions, and reproductive success. Shrubs of Malpighiaceae family in the Brazilian Tropical Savanna present sequential flowering phenology. We verified variations in climatic factors (temperature and precipitation) over a period of 10 years (2005–2014) and correlated them with the onset of flowering of four of these Malpighiaceae species. Furthermore, we tested whether the phenological synchronization among species has changed over time affecting the herbivory and fruit set. Herbivory and fruit production were recorded during three reproductive seasons (2008/2009, 2011/2012, 2013/2014). We developed a mathematical model to estimate the flower and fruit production in response to phenological changes for the next 5 years. Results show that climatic factors changed, influencing the onset of species flowering. The degree of overlap among species also changed and the effects on species interactions were species specific. The mathematical model successfully presented a tendency on flower and fruit production contributing to the predictions of the outcomes in response to phenological changes. We confirm the effects of climate changes on plant phenological events and the importance of feature plasticity for better performance of species.     

Plant size,flowering synchrony and edge effects: What,how and where they affect the reproductive success of a Neotropical tree species

Plant reproductive success is supposedly influenced by phenology and individual size, which may be modified under edge effects. We tested if reproductive success, estimated by fruit set, in Senefeldera verticillata (Euphorbiaceae) is related to flowering synchrony and tree size, including plant height and circumference at breast height. The study was carried out in the interior and in edges of clearings for gas pipelines and electric lines of a lowland rainforest in south‐eastern Brazil. Monthly observations were performed during one reproductive season, of 19 individuals that grew at edges of electric lines and gas pipelines and at forest interior. Reproductive success was significantly higher at forest interior than at gas pipeline area; there was no significant difference between gas pipeline and electric line areas or between forest interior and electric line area. In the forest edges, only plant height was positively related to plant reproductive success. This is probably related to crown exposure to sunlight, which enhances flower production. At forest interior, reproductive success was positively influenced by the synchrony of flowering activity among neighbouring individuals. In contrast, flowering synchrony based on phenophase intensity negatively impacted reproductive success. Senefeldera verticillata shows temporal dioecy and is mainly pollinated by small social bees, and the high degree of flowering synchrony at low intensity may increase the number of mating partners and therefore enhance its reproductive success. Inside the forest fragments, individuals with thicker trunks showed lower reproductive success, which may be related to a loss of reproductive capacity of older individuals. Our results evidenced the complexity of responses experienced by tropical plants subjected to forest fragmentation because of linear clearings.     

Relationships between flowering phenology,plant size and reproductive success in shape Lotus corniculatus (Fabaceae)

Over three years the flowering phenology of individuals of Lotus corniculatus has been studied in relation to fruit set and seed predation to determine the relationships between four components of flowering time, plant size and reproductive success. Timings of first and peak flowering, and duration and synchrony of flowering differed between individuals in the same years. Between years, timing of first flowering was highly correlated for the same individuals, and was closely correlated with plant size and duration of flowering–larger plants flowered earlier and for a longer period. Peak flowering and synchrony were not correlated between-years for individuals.Fruit production and seed predation were correlated with some of the components of flowering phenology in some years, but not in others. The inconstancy of these relationships suggests that directional or stabilising selection is not acting consistently on the aspects of reproductive success studied in this work. The inconstancy of selection may result in the rather asynchronous flowering phenologies of individuals of L. corniculatus observed.We emphasize the importance of studying different components of flowering phenology in relation to individual plant size over several seasons. This work has shown that plant size not only has a direct effect on individual plant fecundity but also can influence flowering time and hence indirectly affect reproductive output.     

Consequences of variation in flowering phenology for seed head herbivory and reproductive success in Erigeron glaucus (Compositae)

Summary We examined the relationship between flowering phenology, reproductive success (seed production only), and seed head herbivory for 20 similarly sized clones of Erigeron glaucus growing at Bodega Bay Reserve, northern California, USA. Although clones tended to reach peak flowering on the same date, they differed in the proportion of their total flowers produced around that date (flowering synchrony). Clones also differed in the number and density of flower heads presented at any one time to pollinators and herbivores (floral display). Both of these characteristics had consequences for herbivory and plant reproductive success. The proportion of flower heads damaged by insect herbivores was greater for clones that concentrated flowering activity during the main flowering period for the population as a whole (high synchrony) compared to clones that spread flowering out temporally. The primary reason for this result was that clones with low flowering synchrony produced a significant proportion of their flower heads during the fall and therefore, escaped attack by the tephritid fly, Tephritis ovatipennis. Clones with intermediate synchrony had lower seed success (total number of viable seeds produced over the year) than clones with either low or high synchrony. The proportion of flower heads damaged by insect herbivores and number of tephritid flies reared from flower heads were both negatively correlated to floral display while seed head mass and germination rates were positively related to display. Thus, clones which produced dense floral displays were favored both in terms of reduced herbivory and increased successful seed production.     

Reproductive phenology in three Genisteae (Fabaceae) shrub species of the W Mediterranean Region

We studied the flower duration, the phenology of flowering and fruiting, and flower, fruit, and seed production in three Genisteae shrub species of the W Mediterranean Region: Cytisus multiflorus, C. striatus , and Retama sphaerocarpa . Flower duration was negatively correlated with temperature, and in the case of C. striatus it was also influenced by pollination. In Cytisus multiflorus , which flowers during winter in the population studied, two floral morphs were recognized differentiated by flower size, phenological pattern, and production of the reproductive organs: morph LF (large flowers) and morph SF (small flowers). The former is earlier in phenology but its reproductive success is less than the second since it not only produces significantly fewer flowers/plant, but also a smaller crop of fruit and seeds. The flowering of the LF morph lasted some three months and of the SF morph 11 weeks. The winter-spring flowering C. striatus , with a four month duration of flowering time, is sympatric with C. multiflorus and their flowering periods overlap, but the former is more successful reproductively. Retama sphaerocarpa is clearly spring flowering, with an extremely short duration of flowering (c. 6.5 weeks), but, unlike the other two species which disperse their seeds in the same season in which they are produced, it staggers the dispersal of its diaspores over more than one year. Despite the great flower per plant production, especially in Retama sphaerocarpa , and of the number of fruit initiated, the final crop of fruit and seed/plant is low in the three species (C. multiflorus : fruit 8.40% and seeds 1.96%; C. striatus : fruit 13.09% and seeds 4.12%; Retama sphaerocarpa : fruit 5.65% and seeds 1.33%).     

Dissecting components of flowering pattern: size effects on female fitness

Flowering synchrony is essential for plant reproductive success, especially in the case of small‐sized populations of self‐incompatible species. Closely related to synchrony, flowering intensity influences pollinator attraction and pollinator movements. Thus, a high flowering intensity may increase pollinator attraction but, at the same time, may also increase the probability of geitonogamous pollinations. Depending on the mating system, the female fitness of plants in small populations may be affected by both the positive effects of higher flowering synchrony and pollinator attraction and the negative effects of geitonogamous pollinations induced by a high flowering intensity. It was hypothesized that different‐sized plants in a population would show contrasting flowering patterns, resulting in differences in pollinator behaviour. These influences could result in differences in mating and female reproductive success. This hypothesis was tested by studying the flowering pattern of Erodium paularense (Geraniaceae), a rare and endangered endemic of central Spain. The temporal distribution of flower production was explored throughout the reproductive season, and the probability of xenogamy and geitonogamy and their relationship to plant size and fitness components were calculated. The analysis of this partially self‐compatible species showed diverse flowering patterns related to different plant sizes. Small plants produced a larger number of seeds per fruit in spite of having lower values of flowering synchrony. By contrast, large plants produced a larger number of seeds from geitonogamous pollinations. The effect of different flower displays and outcrossing rates on seed set varied throughout the season in the different groups. Our findings highlight the relevance of individual plant size‐dependent phenology on female reproductive success and, in particular, on the relationship between flowering synchrony and fitness. © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society, 2008, 156 , 227–236.     

准噶尔无叶豆的开花物候与生殖特征

 为了研究沙漠稀有植物准噶尔无叶豆(Eremosparton songoricum)的开花物候特征及其对生殖成功的影响, 2005和2006年连续两年对其自然种群的开花物候和开花过程中的花部表型变化进行了观察, 并运用相对开花振幅、开花强度和开花同步性等开花物候指数研究了开花物候特征。结果表明: 准噶尔无叶豆在5月下旬至6月中下旬开花, 其种群、个体、花序和单花的花期分别历时26~29 d、8~10 d、5~7 d和2~3 d。单花开花进程依其形态和散粉特征可分为散粉前期、散粉初期、散粉盛期和凋谢期4个时期。其个体水平的开花物候进程(开花振幅曲线)呈渐进式单峰曲线, 具有很高的开花同步指数, 表现出一种集中开花的模式。开花物候指数与座果数之间的相关分析结果表明, 始花日期与花期持续时间存在负相关关系, 而与开花数和座果数存在正相关关系; 花期持续时间与开花数和座果数存在显著正相关关系。准噶尔无叶豆个体开花物候在很大程度上是由其遗传因子决定的, 而开花物候在年度间的变异, 可能是由于荒漠气候的差异(主要是水分和温度的差异)所引起的。作为沙漠窄域分布特有种, 准噶尔无叶豆在环境和人为干扰的双重选择压力下, 为了吸引更多的传粉者访问而达到生殖成功, 形成了大量集中开花的模式。     

Are mismatches the norm? Timing of flowering,fruiting, dispersal and germination and their fitness effects in Frangula alnus (Rhamnaceae)

The close morphological and temporal links between phases of plant growth and reproduction call for integrated studies incorporating several reproductive phases from flowering to recruitment, and associated plant‐animal interactions. Phenological strategies, as well as plastic phenological response to climate change, incorporate complex interactions between developmental constraints, pollination and seed dispersal. Relationships between reproductive phenology and components of fitness were studied for two years in the north‐temperate, self‐incompatible, insect‐pollinated, and bird‐dispersed shrub Frangula alnus (Rhamnaceae). Fruit set, dispersal, germination and juvenile survival, as well as seed mass and juvenile size were measured in relation to flowering, fruiting and germination time. The results suggest that effects of flowering and fruiting time prevailed in subsequent phases, to some extent as far as to the juvenile phase, but effects of timing were complex and had partly opposing effects on different fitness components. Early flowers had higher fruit‐set and experiments indicated that synchronous peak flowering increased fruit‐set, but later flowers had higher seed mass. Peak fruiting was not associated with peak dispersal. Late fruits derived from late flowers promoted dispersal. Juvenile recruitment was enhanced by increasing seed size. We conclude that the phenology of flowering and fruiting in F. alnus comprises several features, each with different and sometimes counteracting effects on fitness components. From a general perspective, this result implies that we should not expect to find finely tuned matches in timing specifically between flowering and pollinators, and fruiting and seed dispersing birds.     

西双版纳地区鞘花的繁殖物候特征及影响因素

桑寄生植物作为关键种和关键性食物资源在生态系统中扮演着重要角色,其鞘花的繁殖物候特征不仅会影响自身的繁殖适合度而且还会影响依赖于其获取食物资源的动物。为了解鞘花的繁殖物候特征及其影响因素,探究其与寄主植物和种子散布者之间的相互作用关系。该研究以西双版纳地区分布的鞘花为对象,通过定期观测鞘花和其寄主植物木荷的繁殖物候,测量它们的生物学特性和温湿度等环境因子,并分析鞘花在个体水平和种群水平上的繁殖物候特征以及寄主植物和温湿度对其繁殖物候的影响。结果表明:(1)鞘花的开花物候属于集中大量开花模式,整个种群的花期和果期的持续时间分别约为20 d和72 d,花期和果期的同步性指数都较高,6月中旬鞘花果实被取食的数量和速率最大,之后逐渐降低。(2)鞘花的始花期与木荷的始花期相关性较高,花期和果期与木荷的繁殖物候基本重叠。(3)每月开花和果熟的个体数量与同期和前一个月的平均温度和相对湿度的相关关系均不显著。总之,桑寄生植物的繁殖物候特征可能受到较多因素的影响,若想全面了解半寄生植物的繁殖物候特征,就要综合考虑生物和非生物等多种因子的共同作用。     

Inter and intraspecific variation on reproductive phenology of the Brazilian Atlantic forest Rubiaceae: ecology and phylogenetic constraints

The reproductive phenology of seven species of Rubiaceae from the Brazilian Atlantic rain forest was compared to evaluate the occurrence of phylogenetic constraints on flowering and fruiting phenologies. Since phenological patterns can be affected by phylogenetic constraints, we expected that reproductive phenology would be similar among plants within a family or genus, occurring during the same time (or season) of the year. Observations on flowering and fruiting phenology were carried out monthly, from December 1996 to January 1998, at Núcleo Picinguaba, Parque Estadual da Serra do Mar, Ubatuba, S?o Paulo State, Brazil. Nine phenological variables were calculated to characterize, quantify and compare the reproductive phenology of the Rubiaceae species. The flowering patterns were different among the seven species studied, and the Kruskal-Wallis test indicated significant differences in flowering duration first flowering, peak flowering and flowering synchrony. The peaks and patterns of fruiting intensity were different among the Rubiaceae species studied and they differed significantly from conspecifics in the phenological variables fruiting duration, fruiting peak date, and fruiting synchrony (Kruskal-Wallis test). Therefore, we found no evidence supporting the phylogenetic hypotheses, and climate does not seem to constrain flowering and fruiting patterns of the Rubiaceae species in the understory of the Atlantic forest.     

Phylogenetic conservatism and climate factors shape flowering phenology in alpine meadows

The study of phylogenetic conservatism in alpine plant phenology is critical for predicting climate change impacts; currently we have a poor understanding of how phylogeny and climate factors interactively influence plant phenology. Therefore, we explored the influence of phylogeny and climate factors on flowering phenology in alpine meadows. For two different types of alpine plant communities, we recorded phenological data, including flowering peak, first flower budding, first flowering, first fruiting and the flowering end for 62 species over the course of 5 years (2008–2012). From sequences in two plastid regions, we constructed phylogenetic trees. We used Blomberg’s K and Pagel’s lambda to assess the phylogenetic signal in phenological traits and species’ phenological responses to climate factors. We found a significant phylogenetic signal in the date of all reproductive phenological events and in species’ phenological responses to weekly day length and temperature. The number of species in flower was strongly associated with the weekly day lengths and followed by the weekly temperature prior to phenological activity. Based on phylogenetic eigenvector regression (PVR) analysis, we found a highly shared influence of phylogeny and climate factors on alpine species flowering phenology. Our results suggest the phylogenetic conservatism in both flowering and fruiting phenology may depend on the similarity of responses to external environmental cues among close relatives.     

The strength of assortative mating for flowering date and its basis in individual variation in flowering schedule

Although it has been widely asserted that plants mate assortatively by flowering time, there is virtually no published information on the strength or causes of phenological assortment in natural populations. When strong, assortative mating can accelerate the evolution of plant reproductive phenology through its inflationary effect on genetic variance. We estimated potential assortative mating for flowering date in 31 old‐field species in Ontario, Canada. For each species, we constructed a matrix of pairwise mating probabilities from the individual flowering schedules, that is the number of flower deployed on successive dates. The matrix was used to estimate the phenotypic correlation between mates, ρ, for flowering date. We also developed a measure of flowering synchrony within species, S, based upon the eigenstructure of the mating matrix. The mean correlation between pollen recipients and potential donors for flowering date was  = 0.31 (range: 0.05–0.63). A strong potential for assortative mating was found among species with high variance in flowering date, flowering schedules of short duration and skew towards early flower deployment. Flowering synchrony, S, was negatively correlated with potential assortment (r = ?0.49), but we go on to show that although low synchrony is a necessary condition for phenological assortative mating, it may not be sufficient to induce assortment for a given phenological trait. The potential correlation between mates showed no seasonal trend; thus, as climate change imposes selection on phenology through longer growing seasons, spring‐flowering species are no more likely to experience an accelerated evolutionary response than summer species.     

Gender specialization and factors affecting fruit set of the wind-pollinated heterodichogamous Juglans regia

Gender expression, flowering phenology, reproductive performance and factors affecting fruit set (i.e., flowering synchrony, size and distance to the nearest pollen donor) were investigated in a cultivated population of a wind-pollinated self-compatible heterodichogamous Juglans regia (Juglandaceae). Four flowering morphs, (i.e., protandrous, protogynous, male and female) were observed. The sexual functions of the protandrous and protogynous morphs were almost synchronous; however, they were not reciprocal, and the separation of male and female flowering within most monoecious individuals was not complete. Thus, within-morph mating and geitonogamous pollination may be common. The ratio of protandrous versus protogynous morphs was biased towards the protandrous morph, but the fruit set did not differ between the morphs, suggesting that the fruit set of the protandrous morph could be partly compensated by within-morph pollination. The ratio of the female flower number or fruit number to the total male catkin length was higher in the protogynous morph than in the protandrous morph and did not vary with plant size, suggesting that gender variation was not size dependent and that the sexual function of protandrous morphs was more male biased. Fruit set depended on plant size only for protandrous morphs. The fruit set of individual plants decreased with increasing distance to the nearest pollen donor regardless of morph, possibly because of pollen limitation. The fruit set of individual plants increased with flowering synchrony, indicating that flowering synchrony could affect reproductive success.     

Aphid–willow interactions in a high Arctic ecosystem: responses to raised temperature and goose disturbance

Recently, there have been several studies using open top chambers (OTCs) or cloches to examine the response of Arctic plant communities to artificially elevated temperatures. Few, however, have investigated multitrophic systems, or the effects of both temperature and vertebrate grazing treatments on invertebrates. This study investigated trophic interactions between an herbivorous insect (Sitobion calvulum, Aphididae), a woody perennial host plant (Salix polaris) and a selective vertebrate grazer (barnacle geese, Branta leucopsis). In a factorial experiment, the responses of the insect and its host to elevated temperatures using open top chambers (OTCs) and to three levels of goose grazing pressure were assessed over two summer growing seasons (2004 and 2005). OTCs significantly enhanced the leaf phenology of Salix in both years and there was a significant OTC by goose presence interaction in 2004. Salix leaf number was unaffected by treatments in both years, but OTCs increased leaf size and mass in 2005. Salix reproduction and the phenology of flowers were unaffected by both treatments. Aphid densities were increased by OTCs but unaffected by goose presence in both years. While goose presence had little effect on aphid density or host plant phenology in this system, the OTC effects provide interesting insights into the possibility of phenological synchrony disruption. The advanced phenology of Salix effectively lengthens the growing season for the plant, but despite a close association with leaf maturity, the population dynamics of the aphid appeared to lack a similar phenological response, except for the increased population observed.     

Reproductive phenology of coastal plain Atlantic forest vegetation: comparisons from seashore to foothills

The diversity of tropical forest plant phenology has called the attention of researchers for a long time. We continue investigating the factors that drive phenological diversity on a wide scale, but we are unaware of the variation of plant reproductive phenology at a fine spatial scale despite the high spatial variation in species composition and abundance in tropical rainforests. We addressed fine scale variability by investigating the reproductive phenology of three contiguous vegetations across the Atlantic rainforest coastal plain in Southeastern Brazil. We asked whether the vegetations differed in composition and abundance of species, the microenvironmental conditions and the reproductive phenology, and how their phenology is related to regional and local microenvironmental factors. The study was conducted from September 2007 to August 2009 at three contiguous sites: (1) seashore dominated by scrub vegetation, (2) intermediary covered by restinga forest and (3) foothills covered by restinga pre-montane transitional forest. We conducted the microenvironmental, plant and phenological survey within 30 transects of 25 m × 4 m (10 per site). We detected significant differences in floristic, microenvironment and reproductive phenology among the three vegetations. The microenvironment determines the spatial diversity observed in the structure and composition of the flora, which in turn determines the distinctive flowering and fruiting peaks of each vegetation (phenological diversity). There was an exchange of species providing flowers and fruits across the vegetation complex. We conclude that plant reproductive patterns as described in most phenological studies (without concern about the microenvironmental variation) may conceal the fine scale temporal phenological diversity of highly diverse tropical vegetation. This phenological diversity should be taken into account when generating sensor-derived phenologies and when trying to understand tropical vegetation responses to environmental changes.