Exploring the causes of variation in phenology and morphology in Mediterranean geophytes: a genus-wide study of Cyclamen

The phenology and morphology of Mediterranean plants are constrained by drought in summer and cold temperatures in winter. In this study we examine how climatic factors and phylogenetic constraints have shaped variation in the phenology and morphology of 17 species of the genus Cyclamen cultivated in uniform garden conditions. We quantify the extent to which traits differ among subgenera and thus represent conserved traits within evolutionary lineages. We also explore whether leaf, flowering and seed-release phenology are correlated among species, and thus whether variation in flowering phenology results from selection on dispersal phenology. Our results show a significant influence of subgenus membership on leaf and flowering phenology but not on morphological traits or the timing of seed release. Among-species variation in foliage height, leaf size and seed mass (but not in floral traits) is correlated with chromosome number. Leaf traits show that species with a shorter vegetative period have a higher capacity for resource acquisition. Major phenological shifts, i.e. spring vs. autumn flowering and a decoupling of leaf and flower phenology in autumnal flowering species, thus occurred prior to the diversification of species in each subgenus and not as a response to selection on dispersal timing. Leaf and flowering phenology illustrate a gradient of strategies from autumn flowering in the absence of leaves (hysteranthous species) to spring flowering with fully developed foliage (synanthous species). In the former, flowering is uncoupled from resource acquisition by simultaneous photosynthesis, indicative that hysteranthy is a response to temporal unpredictability in the onset of rain after the summer drought. Our results support the idea that whereas leaf development is controlled primarily by moisture availability and secondarily by temperature, flowering is temperature dependent, above a minimum moisture threshold. © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 145 , 469–484.     

Phenology and floral synchrony of Rhizophora mangle along a natural salinity gradient

Rhizophora mangle is the most common species of mangrove within its range and a major component of coastal ecosystems in the tropics and subtropics. Its phenology is affected by seasonal variations in temperature, salinity, and precipitation, all of which may be altered by impending climate change. In this work, the monthly leaf, flower, and fruit phenology of R. mangle was assessed at three sites, along a natural salinity gradient for 12 months. We assessed phenological states using litter traps installed in mangrove stands, and by direct observation of leaf production at two sites, and flower, and fruit production at a single site. Phenological events were compared with seasonal climatic variations (in wind, rain, and temperature) to explore potential abiotic controls on the phenology of this species. Leaf shedding was lowest at the low salinity site. Leaf and stipule production showed a seasonal trend, decreasing during the cool and dry winter months. Flowering was highly seasonal and synchronous and peaked during the rainy season. Flowering was correlated with average temperature (r = 0.82; p < 0.05) at all three study sites, but was not correlated with precipitation. At the high‐salinity site, flowering was restricted to the rainy season. Fruit abortion was associated with wind speed (r = 0.79; p < 0.05). Flowering of R. mangle is induced by increasing temperatures and the onset of rains. Rising temperatures, drier summers, and more frequent and intense storms, due to climate change, may influence mangrove productivity, population dynamics, and floral synchrony.     

Latitudinal cline of flowering and fruiting phenology in Fagaceae in Asia

The seasonal timing of flowering and fruiting is crucial for the reproductive success of plants and for resource availability to animals. Although plants synchronize their reproductive timing to coincide with appropriate seasons by responding to environmental cues, seasonal variations in temperature and precipitation vary minimally in very wet tropical environments. To explore the latitudinal cline in the reproductive phenology of the Fagaceae in Asia, we analyzed phenology data for a total of 94, 121, and 219 species from Thailand, Malesia, and China, respectively, in the three genera of Fagaceae, Quercus, Castanopsis, and Lithocarpus. We found that Quercus and Castanopsis showed flowering peaks in April in China. In Thailand, the peak shifted to an earlier month, and the peak disappeared in Malesia. The flowering period lengthened with decreasing latitude in the animal-pollinated genera Castanopsis and Lithocarpus. However, this was not the case for the wind-pollinated genus Quercus. The fruiting period lengthened with decreasing latitude in all three genera. We examined the relationship between reproductive phenology and climatic factors. The combination of monthly temperature and precipitation best explained the monthly change in the proportion of flowering and fruiting species in China in all three genera. However, climatic factors had almost no impact on the predictive ability of the model in Malesia. Our results on phenological shifts in the family Fagaceae, from the temperate climates and seasonal tropics to the humid tropics, provide valuable information for predicting phenological changes in future climate change.     

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.     

Reproductive phenology of two Mimusops species in relation to climate,tree diameter and canopy position in Benin (West Africa)

Assessing species phenology provides useful understanding about their autecology, to contribute to management strategies. We monitored reproductive phenology of Mimusops andongensis and Mimusops kummel, and its relationship with climate, tree diameter and canopy position. We sampled trees in six diameter classes and noted their canopy position. For both species flowering began in the dry season through to the rainy season, but peaked in the dry season, whilst fruiting occurred in the rainy season and peaked during the most humid period. Flowering was positively correlated with temperature. Conversely, fruiting was negatively correlated with temperature and positively with rainfall, only in the Guineo‐Sudanian zone. For M. andongensis, flowering and fruiting prevalences were positively linked to stem diameter, while only flowering was significantly related to canopy position. For M. kummel, the relationship with stem diameter was significant for flowering prevalence only and in the Guineo‐Sudanian zone. Results suggest that phylogenetic membership is an important factor restricting Mimusops species phenology. Flowering and fruiting of both species are influenced by climate, and consequently climate change might shift their phenological patterns. Long‐term investigations, considering flowering and fruiting abortion, will help to better understand the species phenology and perhaps predict demographic dynamics.     

Escape from floral herbivory by early flowering in Arabidopsis halleri subsp. gemmifera

Natural selection on flowering phenology has been studied primarily in terms of plant–pollinator interactions and effects of abiotic conditions. Little is known, however, about geographic variation in other biotic factors such as herbivores and its consequence for differential selection on flowering phenology among populations. Here, we examine selection by floral herbivores on the flowering phenology of Arabidopsis halleri subsp. gemmifera using two adjacent populations with contrasting herbivory regimes. Intensive floral herbivory by the leaf beetle Phaedon brassicae occurs in one population, while the beetle is absent in another population. We tested the hypothesis that the two populations experience differential selection on flowering time that is attributable to the presence or absence of floral herbivory. A two-year field study showed that early flowering was favoured in the population under intensive floral herbivory, whereas selection for early flowering was not found in one year in the population where floral herbivory was absent. Selection for early flowering disappeared when the abundance of floral herbivores was artificially decreased in a field experiment. Thus, the heterogeneous distribution of P. brassicae was a major agent for differential selection on flowering time. However, flowering time did not differ between the two populations when plants were grown in the laboratory. The lack of genetic differentiation in flowering time may be explained by ongoing gene flow or recent invasion of P. brassicae. This study illustrates that the role of floral herbivory in shaping geographic variation in selection on flowering phenology may be more important than previously thought.     

气候变化背景下青藏高原东部猪毛蒿物候的变化规律和影响因素

近几十年来青藏高原正经历着广泛而深远的气候变化,这种变化对当地物种的物候及分布格局产生了显著影响。猪毛蒿作为干旱半干旱地区的优势物种和影响群落稳定性的关键物种,青藏高原东缘是其重要的分布区域之一,然而其物候将如何应对气候变化目前我们尚不清楚。为此,基于青海省东部连续20年的气象数据和原位物候观测实验,探讨猪毛蒿物候的变化规律及量化不同气候因子的相对贡献率。结果表明：1)过去20年间年均温和年均每日日照时长分别呈现出显著的上升和下降趋势,而年降水和年均每日最大风速没有显著的变化;2)20年间猪毛蒿返青-开花的时间间隔和开花-结果的时间间隔并未表现出显著的变化趋势,结果-枯黄的时间间隔显著缩短;3)所有气候因子均对猪毛蒿不同物候的时间间隔有显著影响,其中最大风速是影响猪毛蒿物候时间间隔最重要的气候因子。这一研究发现可以为气候变化情景下青藏高原高寒植物的保护和利用提供理论依据。     

Species‐specific responses to combined water stress and increasing temperatures in two bee‐pollinated congeners (Echium,Boraginaceae)

1. Water stress and increasing temperatures are two main constraints faced by plants in the context of climate change. These constraints affect plant physiology and morphology, including phenology, floral traits, and nectar rewards, thus altering plant–pollinator interactions.
2. We compared the abiotic stress responses of two bee‐pollinated Boraginaceae species, Echium plantagineum, an annual, and Echium vulgare, a biennial. Plants were grown for 5 weeks during their flowering period under two watering regimes (well‐watered and water‐stressed) and three temperature regimes (21, 24, 27°C).
3. We measured physiological traits linked to photosynthesis (chlorophyll content, stomatal conductance, and water use efficiency), and vegetative (leaf number and growth rate) and floral (e.g., flower number, phenology, floral morphology, and nectar production) traits.
4. The physiological and morphological traits of both species were affected by the water and temperature stresses, although the effects were greater for the annual species. Both stresses negatively affected floral traits, accelerating flower phenology, decreasing flower size, and, for the annual species, decreasing nectar rewards. In both species, the number of flowers was reduced by 22%–45% under water stress, limiting the total amount of floral rewards.
5. Under water stress and increasing temperatures, which mimic the effects of climate change, floral traits and resources of bee‐pollinated species are affected and can lead to disruptions of pollination and reproductive success.

     

Variation in the phenology and abundance of flowering by native and exotic plants in subalpine meadows

The timing and abundance of flower production is important to the reproductive success of angiosperms as well as pollinators and floral and seed herbivores. Exotic plants often compete with native plants for space and limiting resources, potentially altering community floral dynamics. We used observations and a biomass-removal experiment to explore the effects of an invasive exotic flowering plant, Linaria vulgaris, on community and individual species flowering phenology and abundance in subalpine meadows in Colorado, USA. Invasion by L. vulgaris was associated with a shift in both the timing and abundance of community flowering. Invaded plant communities exhibited depressed flowering by 67% early in the season relative to uninvaded communities, but invaded sites produced 7.6 times more flowers than uninvaded sites once L. vulgaris began flowering. This increase in flowers at the end of the season was driven primarily by prolific flowering of L. vulgaris. We also found lower richness and evenness of resident flowering species in invaded plots during the period of L. vulgaris flowering. At the species level, a common native species (Potentilla pulcherrima) produced 71% fewer flowers in invaded relative to uninvaded plots, and the species had reduced duration of flowering in invaded relative to uninvaded sites. This result suggests that L. vulgaris does not simply alter the flowering of subordinate species but also the flowering of an individual common species in the plant community. We then used observational data to explore the relationship between L. vulgaris density and resident floral production but found only partial evidence that higher densities of L. vulgaris were associated with stronger effects on resident floral production. Taken together, results suggest that a dominant invasive plant can affect community and individual-species flowering.     

Divergent selection on flowering phenology but not on floral morphology between two closely related orchids

Closely related species often differ in traits that influence reproductive success, suggesting that divergent selection on such traits contribute to the maintenance of species boundaries. Gymnadenia conopsea ss. and Gymnadenia densiflora are two closely related, perennial orchid species that differ in (a) floral traits important for pollination, including flowering phenology, floral display, and spur length, and (b) dominant pollinators. If plant–pollinator interactions contribute to the maintenance of trait differences between these two taxa, we expect current divergent selection on flowering phenology and floral morphology between the two species. We quantified phenotypic selection via female fitness in one year on flowering start, three floral display traits (plant height, number of flowers, and corolla size) and spur length, in six populations of G. conopsea s.s. and in four populations of G. densiflora. There was indication of divergent selection on flowering start in the expected direction, with selection for earlier flowering in two populations of the early‐flowering G. conopsea s.s. and for later flowering in one population of the late‐flowering G. densiflora. No divergent selection on floral morphology was detected, and there was no significant stabilizing selection on any trait in the two species. The results suggest ongoing adaptive differentiation of flowering phenology, strengthening this premating reproductive barrier between the two species. Synthesis: This study is among the first to test whether divergent selection on floral traits contribute to the maintenance of species differences between closely related plants. Phenological isolation confers a substantial potential for reproductive isolation, and divergent selection on flowering time can thus greatly influence reproductive isolation and adaptive differentiation.     

Adaptation to climate through flowering phenology: a case study in Medicago truncatula

Local climatic conditions likely constitute an important selective pressure on genes underlying important fitness‐related traits such as flowering time, and in many species, flowering phenology and climatic gradients strongly covary. To test whether climate shapes the genetic variation on flowering time genes and to identify candidate flowering genes involved in the adaptation to environmental heterogeneity, we used a large Medicago truncatula core collection to examine the association between nucleotide polymorphisms at 224 candidate genes and both climate variables and flowering phenotypes. Unlike genome‐wide studies, candidate gene approaches are expected to enrich for the number of meaningful trait associations because they specifically target genes that are known to affect the trait of interest. We found that flowering time mediates adaptation to climatic conditions mainly by variation at genes located upstream in the flowering pathways, close to the environmental stimuli. Variables related to the annual precipitation regime reflected selective constraints on flowering time genes better than the other variables tested (temperature, altitude, latitude or longitude). By comparing phenotype and climate associations, we identified 12 flowering genes as the most promising candidates responsible for phenological adaptation to climate. Four of these genes were located in the known flowering time QTL region on chromosome 7. However, climate and flowering associations also highlighted largely distinct gene sets, suggesting different genetic architectures for adaptation to climate and flowering onset.     

Divergence on floral traits and vertebrate pollinators of two endemic Encholirium bromeliads

Shifts in pollen vectors favour diversification of floral traits, and differences in pollination strategies between congeneric sympatric species can contribute to reproductive isolation. Divergence in flowering phenology and selfing could also reduce interspecific crossing between self‐compatible species. We investigated floral traits and visitation rates of pollinators of two sympatric Encholirium species on rocky outcrops to evaluate whether prior knowledge of floral characters could indicate actual pollinators. Data on flowering phenology, visitation rates and breeding system were used to evaluate reproductive isolation. Flowering phenology overlapped between species, but there were differences in floral characters, nectar volume and concentration. Several hummingbird species visited flowers of both Encholirium spp., but the endemic bat Lonchophylla bokermanni and an unidentified sphingid only visited E. vogelii. Pollination treatments demonstrated that E. heloisae and E. vogelii were partially self‐compatible, with weak pollen limitation to seed set. Herbivores feeding on inflorescences decreased reproductive output of both species, but for E. vogelii the damage was higher. Our results indicate that actual pollinators can be known beforehand through floral traits, in agreement with pollination syndromes stating that a set of floral traits can be associated with the attraction of specific groups of pollinators. Divergence on floral traits and pollinator assemblage indicate that shifts in pollination strategies contribute to reproductive isolation between these Encholirium species, not divergence on flowering phenology or selfing. We suggest that hummingbird pollination might be the ancestral condition in Encholirium and that evolution of bat pollination made a substantial contribution to the diversification of this clade.     

Flowering phenology change and climate warming in southwestern Ohio

Global surface temperature has increased markedly over the last 100 years. This increase has a variety of implications for human societies, and for ecological systems. One of the most obvious ways ecosystems are affected by global climate change is through alteration of organisms’ developmental timing (phenology). We used annual botanical surveys that documented the first flowering for an array of species from 1976 to 2003 to examine the potential implications of climate change for plant development. The overall trend for these species was a progressively earlier flowering time. The two earliest flowering taxa (Galanthus and Crocus) also exhibited the strongest shift in first flowering. We detected a significant trend in climate suggesting higher temperatures in winter and spring over the sampling interval and found a significant relationship between warming temperatures and first flowering time for some species. Although 60% of the species in our study flowered earlier over the sampling interval, the remaining species exhibited no statistically detectable change. This variation in response is ostensibly associated with among-species variation in the role of climate cues in plant development. Future work is needed to isolate specific climate cues, and to link plant phenology to the physiological processes that trigger plant development.     

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.     

Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes

Warmer temperatures are accelerating the phenology of organisms around the world. Temperature sensitivity of phenology might be greater in colder, higher latitude sites than in warmer regions, in part because small changes in temperature constitute greater relative changes in thermal balance at colder sites. To test this hypothesis, we examined up to 20 years of phenology data for 47 tundra plant species at 18 high‐latitude sites along a climatic gradient. Across all species, the timing of leaf emergence and flowering was more sensitive to a given increase in summer temperature at colder than warmer high‐latitude locations. A similar pattern was seen over time for the flowering phenology of a widespread species, Cassiope tetragona. These are among the first results highlighting differential phenological responses of plants across a climatic gradient and suggest the possibility of convergence in flowering times and therefore an increase in gene flow across latitudes as the climate warms.