Phenology in a warming world: differences between native and non‐native plant species

Phenology is a harbinger of climate change, with many species advancing flowering in response to rising temperatures. However, there is tremendous variation among species in phenological response to warming, and any phenological differences between native and non‐native species may influence invasion outcomes under global warming. We simulated global warming in the field and found that non‐native species flowered earlier and were more phenologically plastic to temperature than natives, which did not accelerate flowering in response to warming. Non‐native species' flowering also became more synchronous with other community members under warming. Earlier flowering was associated with greater geographic spread of non‐native species, implicating phenology as a potential trait associated with the successful establishment of non‐native species across large geographic regions. Such phenological differences in both timing and plasticity between native and non‐natives are hypothesised to promote invasion success and population persistence, potentially benefiting non‐native over native species under climate change.     

Genetic variation in flowering phenology and reproductive performance in a Mediterranean high‐mountain specialist,Armeria caespitosa (Plumbaginaceae)

Adaptive responses to past climate change may play an important role in the persistence of high‐mountain plants, which are vulnerable to global warming. Armeria caespitosa is a high‐mountain plant, endemic to the Iberian Central Range. Differences in abiotic environment along the elevational gradient impose two opposing stress gradients (i.e. water stress and duration of the growth season) on the species. Furthermore, the species is found in two interspersed, contrasting microhabitats (rocky outcrops and dry cryophilic grasslands) that have different effects on plants depending of the elevation. As a result of this, the species shows great among‐population variation in many reproductive and vegetative traits. We used a common garden approach to determine whether this phenotypic variation has a genetic basis or is the result of plastic responses shaped by heterogeneous environmental conditions. Plants from the high‐elevation edge and dry cryophilic grasslands flowered earlier and produced more viable fruits but were smaller. These results confirm that among‐population variation in flowering phenology and reproductive performance traits in A. caespitosa is partially genetically based. The results also show that the stronger selection response in favour of early‐flowering individuals in populations at the low‐elevation edge did not correspond with the greater proportion of early‐flowering individuals. Genetic variability associated with flowering onset may be relevant in coping with the impacts of ongoing global warming. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 176 , 384–395.     

Selection on flowering time in Mediterranean high-mountain plants under global warming

Under climate warming, plants will undergo novel selective pressures to adjust reproductive timing. Adjustment between reproductive phenology and environment is expected to be higher in arctic and alpine habitats because the growing season is considerably short. As early- and late-flowering species reproduce under very different environmental conditions, selective pressures on flowering phenology and potential effects of climate change are likely to differ between them. However, there is no agreement on the magnitude of the benefits and costs of early- vs. late-flowering species under a global warming scenario. In spite of its relevance, phenotypic selection on flowering phenology has rarely been explored in alpine plants and never in Mediterranean high mountain species, where selective pressures are very different due to the summer drought imposed over the short growth season. We hypothesized that late-flowering plants in Mediterranean mountains should present stronger selective pressures towards early onset of reproduction than early-flowering species, because less water is available in the soil as growing season progresses. We performed selection analyses on flowering onset and duration in two high mountain species of contrasting phenology. Since phenotypic selection can be highly context-dependent, we studied several populations of each species for 2 years, covering their local altitudinal ranges and their different microhabitats. Surrogates of biotic selective agents, like fruitset for pollinators and flower and fruit loss for flower and seed predators, were included in the analysis. Differences between the early- and the late-flowering species were less than expected. A consistent negative correlational selection of flowering onset and duration was found affecting plant fitness, i.e., plants that bloomed earlier flowered for longer periods improving plant fitness. Nevertheless, the late-flowering species may experience higher risks under climate warming because in extremely warm and dry years the earlier season does not bring about a longer flowering duration due to summer drought.     

The jasmonic acid‐signalling and abscisic acid‐signalling pathways cross talk during one,but not repeated,dehydration stress: a non‐specific ‘panicky’ or a meaningful response?

Experiencing diverse and recurring biotic and abiotic stresses throughout life, plants have evolved mechanisms to respond, survive and, eventually, adapt to changing habitats. The initial response to drought involves a large number of genes that are involved also in response to other stresses. According to current models, this initial response is non‐specific, becoming stress‐specific only at later time points. The question, then, is whether non‐specific activation of various stress‐signalling systems leading to the expression of numerous stress‐regulated genes is a false‐alarm (panicky) response or whether it has biologically relevant consequences for the plant. Here, it is argued that the initial activation of genes associated other stresses reflects an important event during which stress‐specific mechanisms are generated to prevent subsequent activation of non‐drought signalling pathways. How plants discriminate between a first and a repeated dehydration stress and how repression of non‐drought specific genes is achieved will be discussed on the example of jasmonic acid‐associated Arabidopsis genes activated by a first, but not subsequent, dehydration stresses. Revealing how expression of various biotic/abiotic stress responding genes is prevented under recurring drought spells may be critical for our understanding of how plants respond to dynamically changing environments.     

Community-level flowering phenology and fruit set: Comparative study of 25 woody species in a secondary forest in Japan

We investigated the flowering phenology, pollinator visitation, and fruit set of 25 animal-pollinated woody species in a warm temperate secondary forest in Japan. Various species flowered sequentially from February to October. The principal pollinators were bumblebees, honey-bees, flies and/or beetles and birds; bumblebees and flies/beetles pollinated most trees. The duration of flowering was shorter for species that bloomed in the middle of the season than it was for species that bloomed earlier or later in the season. The timing of flowering was more synchronous within species that had a shorter flowering duration; this was also detected when phylogenetically independent contrasts were calculated. This could be important for the effective pollination of species with a short flowering duration because such species bloom sequentially over a short period of less than 1month around May. Fruit set was related not to pollinator type, sex expression, flowering sequence (in order of the date of peak flowering) or flowering duration, but to the relative abundance of the species in the forest. This correlation was detected for fly- and beetle-pollinated species but not for bumblebee-pollinated species. Thus, relatively rare plant species with opportunistic pollinators might experience limited fruit set because of insufficient pollinator services. Bagging experiments conducted on eight hermaphrodite species revealed that the fruit set of bagged flowers was nearly zero, lower than that of control flowers. These results indicate the importance of pollinators for successful reproduction and thus for the coexistence of plants in this secondary forest.     

Species-specific flowering phenology responses to experimental warming and drought alter herbaceous plant species overlap in a temperate–boreal forest community

Background and AimsWarmer temperatures and altered precipitation patterns are expected to continue to occur as the climate changes. How these changes will impact the flowering phenology of herbaceous perennials in northern forests is poorly understood but could have consequences for forest functioning and species interactions. Here, we examine the flowering phenology responses of five herbaceous perennials to experimental warming and reduced summer rainfall over 3 years.MethodsThis study is part of the B4WarmED experiment located at two sites in northern Minnesota, USA. Three levels of warming (ambient, +1.6 °C and +3.1 °C) were crossed with two rainfall manipulations (ambient and 27 % reduced growing season rainfall).Key ResultsWe observed species-specific responses to the experimental treatments. Warming alone advanced flowering for four species. Most notably, the two autumn blooming species showed the strongest advance of flowering to warming. Reduced rainfall alone advanced flowering for one autumn blooming species and delayed flowering for the other, with no significant impact on the three early blooming species. Only one species, Solidago spp., showed an interactive response to warming and rainfall manipulation by advancing in +1.6 °C warming (regardless of rainfall manipulation) but not advancing in the warmest, driest treatment. Species-specific responses led to changes in temporal overlap between species. Most notably, the two autumn blooming species diverged significantly in their flowering timing. In ambient conditions, these two species flowered within the same week. In the warmest, driest treatment, flowering occurred over a month apart.ConclusionsHerbaceous species may differ in how they respond to future climate conditions. Changes to phenology may lead to fewer resources for insects or a mismatch between plants and pollinators.     

REPRODUCTIVE PHENOLOGIES IN LOBELIA INFLATA (LOBELIACEAE) AND THEIR ENVIRONMENTAL CONTROL

Flowering and fruiting phenologies of individual plants and flowers of Lobelia inflata, a North American summer annual, were studied in the field and greenhouse to determine whether onset of flowering and fruit maturation were correlated, and the degree to which these reproductive phenologies were influenced by the environment. Within each of two field populations, larger plants flowered earlier and produced more flowers than smaller plants. Onset of flowering was positively correlated with onset of fruit maturation but not perfectly so. Two factors decreased the intensity of this correlation. First, at the flower level, the earlier a flower bloomed, the longer the resulting fruit took to develop. Second, fruit development times varied significantly among individual plants. In the greenhouse, individuals watered more frequently attained greater size and flowered earlier than individuals watered less frequently. Nutrient additions did not affect plant size or onset of flowering. These results indicate that for the summer annual Lobelia inflata, reproductive phenologies are phenotypically correlated, and that timing of reproduction is resource and size dependent, as it is for other monocarpic plant species.     

THE FLORAL ECOLOGY OF PLATANTHERA BLEPHARIGLOTTIS

The floral ecology of a central Maine population of Platanthera blephariglottis was studied during the 1979–1981 flowering seasons. Although this species possesses characteristics typical of moth-pollinated plants, only diurnal pollinators were documented, primarily Hesperiidae, Pieridae, and Apidae. Pollinators were scarce throughout the study, yet bagging experiments indicated vectors were necessary for successful capsule set. The average capsule set per plant was lowest (32.2%) in 1979 when 362 plants bloomed and highest in 1980 (80.2%) when 202 plants flowered. Capsule set was found to be limited by pollinator activity. The adaptations of P. blephariglottis, including sequential flowering, length of receptivity, nectar production and inflorescence size, enable consistently successful reproduction regardless of microhabitat. This species is well-adapted to reproduce in environments experiencing periods of unfavorable weather and low pollinator abundance.     

A natural heating experiment: Phenotypic and genotypic responses of plant phenology to geothermal soil warming

Under global warming, the survival of many populations of sedentary organisms in seasonal environments will largely depend on their ability to cope with warming in situ by means of phenotypic plasticity or adaptive evolution. This is particularly true in high‐latitude environments, where current growing seasons are short, and expected temperature increases large. In such short‐growing season environments, the timing of growth and reproduction is critical to survival. Here, we use the unique setting provided by a natural geothermal soil warming gradient (Hengill geothermal area, Iceland) to study the response of Cerastium fontanum flowering phenology to temperature. We hypothesized that trait expression and phenotypic selection on flowering phenology are related to soil temperature, and tested the hypothesis that temperature‐driven differences in selection on phenology have resulted in genetic differentiation using a common garden experiment. In the field, phenology was related to soil temperature, with plants in warmer microsites flowering earlier than plants at colder microsites. In the common garden, plants responded to spring warming in a counter‐gradient fashion; plants originating from warmer microsites flowered relatively later than those originating from colder microsites. A likely explanation for this pattern is that plants from colder microsites have been selected to compensate for the shorter growing season by starting development at lower temperatures. However, in our study we did not find evidence of variation in phenotypic selection on phenology in relation to temperature, but selection consistently favoured early flowering. Our results show that soil temperature influences trait expression and suggest the existence of genetically based variation in flowering phenology leading to counter‐gradient local adaptation along a gradient of soil temperatures. An important implication of our results is that observed phenotypic responses of phenology to global warming might often be a combination of short‐term plastic responses and long‐term evolutionary responses, acting in different directions.     

Photographs and herbarium specimens as tools to document phenological changes in response to global warming

Global warming is affecting natural systems across the world. Of the biological responses to warming, changes in the timing of phenological events such as flowering are among the most sensitive. Despite the recognized importance of phenological changes, the limited number of long-term records of phenological events has restricted research on the topic in most areas of the world. In a previous study in Boston (American Journal of Botany 91: 1260-1264), we used herbarium specimens and one season of field observations to show that plants flowered earlier as the climate warmed over the past 100 yr. In our new study, we found that two extra years of data did not strengthen the explanatory power of the analysis. Analysis of herbarium specimens without any field data yielded results similar to analyses that included field observations. In addition, we found that photographs of cultivated and wild plants in Massachusetts, data similar to that contained in herbarium specimens, show changes in flowering times that closely match independent data on the same species in the same locations. Dated photographs of plants in flower represent a new resource to extend the range of species and localities addressed in global-warming research.     

Gene expression profiles during short‐term heat stress in the red sea coral Stylophora pistillata

During the past several decades, corals worldwide have been affected by severe bleaching events leading to wide‐spread coral mortality triggered by global warming. The symbiotic Red Sea coral Stylophora pistillata from the Gulf of Eilat is considered an opportunistic ‘r’ strategist. It can thrive in relatively unstable environments and is considered a stress‐tolerant species. Here, we used a S. pistillata custom microarray to examine gene expression patterns and cellular pathways during short‐term (13‐day) heat stress. The results allowed us to identify a two‐step reaction to heat stress, which intensified significantly as the temperature was raised to a 32 °C threshold, beyond which, coping strategies failed at 34 °C. We identified potential ‘early warning genes’ and ‘severe heat‐related genes’. Our findings suggest that during short‐term heat stress, S. pistillata may divert cellular energy into mechanisms such as the ER‐unfolded protein response (UPR) and ER‐associated degradation (ERAD) at the expense of growth and biomineralization processes in an effort to survive and subsequently recover from the stress. We suggest a mechanistic theory for the heat stress responses that may explain the success of some species which can thrive under a wider range of temperatures relative to others.     

Flowering range changes across an elevation gradient in response to warming summer temperatures

Many studies have demonstrated plant response to warming temperatures, both as advancement in the timing of phenological events and in range shifts. Mountain gradients are ideal laboratories for studying species range changes. In this study of 363 plant species in bloom collected in five segments across a 1200 m (4158 ft) elevation gradient, we look for changes in species flowering ranges over a 20-year period. Ninety-three species (25.6%) exhibited a significant change in the elevation at which they flowered from the first half to the second half of the record, with many of these changes occurring at higher elevations. Most of the species exhibiting the changes were perennial plants. Interestingly, though many changes in flowering range were specific to higher elevations, range changes occurred all across the gradient. The changes reported in this study are concurrent with significant increases in summer temperatures across the region and are consistent with observed changes around the globe.     

植物有性生殖对温度胁迫反应的研究进展

开花植物的有性生殖阶段对温度胁迫高度敏感,高温热害和低温冷害都会对这一过程造成严重影响。本文全面总结了温度胁迫对作物有性生殖的影响,明确花粉发育过程是有性生殖过程中对温度胁迫最敏感的时期;转录组和蛋白质组的研究结果表明,蛋白激酶、热激转录因子、热休克蛋白等可能参与花粉发育期对热胁迫的信号转导。理解植物在有性生殖发育阶段如何适应温度胁迫的机理,为遗传育种实践中筛选对温度耐受的作物品种提供指导,也为基因工程选育对温度耐受的品种提供可能。     

Obligatory short‐day plant,Perilla frutescens var. crispa can flower in response to low‐intensity light stress under long‐day conditions

An obligatory short‐day plant, Perilla frutescens var. crispa was induced to flower under long‐day conditions when grown under low‐intensity light (30 µmol m^?2 s^?1). Plant size was smaller under lower light intensity, indicating that the low‐intensity light acted as a stress factor. The phenomenon is categorized as stress‐induced flowering. Low‐intensity light treatment for 4 weeks induced 100% flowering. The plants responded to low‐intensity light immediately after the cotyledons expanded, and the flowering response decreased with increasing plant age. The induced plants produced fertile seeds, and the progeny developed normally. The plants that flowered under low‐intensity light had greener leaves. This greening was because of the decrease in anthocyanin content, and there was a negative correlation between the anthocyanin content and percent flowering. Treatment with L‐2‐aminooxy‐3‐phenylpropionic acid, an inhibitor of phenylalanine ammonia‐lyase (PAL), did not induce flowering under non‐inductive light conditions and inhibited flowering under inductive low‐intensity light conditions. The metabolic pathway regulated by PAL may be involved in the flowering induced by low‐intensity light.     

Conservation,propagation, and redistribution (CPR) of Hill’s thistle: paradigm for plant species at risk

Cryopreservation is a valuable tool that could potentially create an alternate plant preservation strategy for species at risk such as Hill’s thistle. The present study is focused on a successful paradigm involving conservation, propagation and redistribution (CPR), emaphasizing the usefulness of cryopreservation techniques for plant conservation using Hill’s thistle (Cirsium hillii. (Canby) Fernald). A cryopreservation protocol was established using the droplet-vitrification method for 5-week-old shoot tips of in vitro grown cultures. More than 90% of shoot tips showed regrowth and nearly all regenerated plants were able to survive in the greenhouse. The survival, growth, and development of plants from cryopreserved shoot buds and their performance in field conditions were all comparable or better than the plants from non-cryopreserved buds. Reintroduced plants flowered following overwintering and the magnitude of flowering was site dependent with ca. 80% flowering observed in one site. The site dependent flowering patterns were assessed using phytohormone profiling and compared to herbivory, a common biotic stressor of these plants. Lower tryptophan concentrations led to higher flowering except in alvars, where the limestone resisted root penetration resulting in poor flowering. The presence of tryptamine in the greenhouse acclimatized or alvar field leaves suggested the preparedness of the plants for herbivory/grazing. Serotonin and melatonin concentrations were lower in flowering plants and in sites where the biotic/abiotic stress was minimal. This study provides evidence of the effectiveness of the CPR model in species recovery programs for endangered species. Physiological characterization of plants developed from cryopreserved tissues can be useful for fundamental and applied research in stress adaptation and reproductive biology of plants.

     

Sensitivity of flowering plant gametophytes to temperature fluctuations

Research on plant responses to temperature stress is receiving increased interest due to the growing awareness about global warming. High and low temperature stresses help establish the narrow geographic distribution of some cultivated plants, the limited geographic extension of some other economically nutritionally important species, and also induce irregular bearing for some species. However, the understanding of plant responses to temperature stress lags behind other biotic and abiotic stresses probably due to the complex response at the molecular, cellular, and organismal level. Temperature stress affects, indeed, many developmental processes during the plant's life cycle. However, the reproductive stage, the outcome of which represents the economic value for many cultivated plants, is especially vulnerable. Here the effect of low and high temperature stresses during the flowering phase is reviewed in flowering plants in an attempt to unravel sensitive stages that are behind irregular cropping. The review presents detailed findings from 33 previously published reports spanning 19 different flowering plant species. Both the male and female organs of the flower are especially sensitive to temperature fluctuations both during their development before pollination and during the post-pollination stage. The effect of temperature stress is, however, obscured by the complex male–female interaction superimposed on the individual behavior of each organ. Interestingly, a review of the literature on this topic shows that genetic variation does exist in reproductive behavior under temperature fluctuations. This genetic diversity must be preserved and characterized in further detail to understand how plants naturally cope with changing environmental conditions, which will, undoubtedly, help us to design better strategies to face current and future challenging temperature fluctuations.     

Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades

Recent changes in climate have led to significant shifts in phenology, with many studies demonstrating advanced phenology in response to warming temperatures. The rate of temperature change is especially high in the Arctic, but this is also where we have relatively little data on phenological changes and the processes driving these changes. In order to understand how Arctic plant species are likely to respond to future changes in climate, we monitored flowering phenology in response to both experimental and ambient warming for four widespread species in two habitat types over 21 years. We additionally used long‐term environmental records to disentangle the effects of temperature increase and changes in snowmelt date on phenological patterns. While flowering occurred earlier in response to experimental warming, plants in unmanipulated plots showed no change or a delay in flowering over the 21‐year period, despite more than 1 °C of ambient warming during that time. This counterintuitive result was likely due to significantly delayed snowmelt over the study period (0.05–0.2 days/yr) due to increased winter snowfall. The timing of snowmelt was a strong driver of flowering phenology for all species – especially for early‐flowering species – while spring temperature was significantly related to flowering time only for later‐flowering species. Despite significantly delayed flowering phenology, the timing of seed maturation showed no significant change over time, suggesting that warmer temperatures may promote more rapid seed development. The results of this study highlight the importance of understanding the specific environmental cues that drive species’ phenological responses as well as the complex interactions between temperature and precipitation when forecasting phenology over the coming decades. As demonstrated here, the effects of altered snowmelt patterns can counter the effects of warmer temperatures, even to the point of generating phenological responses opposite to those predicted by warming alone.