Warming nondormant tree roots advances aboveground spring phenology in temperate trees.

Climate warming advances the onset of tree growth in spring, but above- and belowground phenology are not always synchronized. These differences in growth responses may result from differences in root and bud dormancy dynamics, but root dormancy is largely unexplored. We measured dormancy in roots and leaf buds of Fagus sylvatica and Populus nigra by quantifying the warming sum required to initiate above- and belowground growth in October, January and February. We furthermore carried out seven experiments, manipulating only the soil and not air temperature before or during tree leaf-out to evaluate the potential of warmer roots to influence budburst timing using seedlings and adult trees of F. sylvatica and seedlings of Betula pendula. Root dormancy was virtually absent in comparison with the much deeper winter bud dormancy. Roots were able to start growing immediately as soils were warmed during the winter. Interestingly, higher soil temperature advanced budburst across all experiments, with soil temperature possibly accounting for c. 44% of the effect of air temperature in advancing aboveground spring phenology per growing degree hour. Therefore, differences in root and bud dormancy dynamics, together with their interaction, likely explain the nonsynchronized above- and belowground plant growth responses to climate warming.

Late to bed, late to rise-Warmer autumn temperatures delay spring phenology by delaying dormancy.

Spring phenology of temperate forest trees has advanced substantially over the last decades due to climate warming, but this advancement is slowing down despite continuous temperature rise. The decline in spring advancement is often attributed to winter warming, which could reduce chilling and thus delay dormancy release. However, mechanistic evidence of a phenological response to warmer winter temperatures is missing. We aimed to understand the contrasting effects of warming on plants leaf phenology and to disentangle temperature effects during different seasons. With a series of monthly experimental warming by ca. 2.4°C from late summer until spring, we quantified phenological responses of forest tree to warming for each month separately, using seedlings of four common European tree species. To reveal the underlying mechanism, we tracked the development of dormancy depth under ambient conditions as well as directly after each experimental warming. In addition, we quantified the temperature response of leaf senescence. As expected, warmer spring temperatures led to earlier leaf-out. The advancing effect of warming started already in January and increased towards the time of flushing, reaching 2.5 days/°C. Most interestingly, however, warming in October had the opposite effect and delayed spring phenology by 2.4 days/°C on average; despite six months between the warming and the flushing. The switch between the delaying and advancing effect occurred already in December. We conclude that not warmer winters but rather the shortening of winter, i.e., warming in autumn, is a major reason for the decline in spring phenology.

Plant responses to climatic extremes: within-species variation equals among-species variation.

Within-species and among-species differences in growth responses to a changing climate have been well documented, yet the relative magnitude of within-species vs. among-species variation has remained largely unexplored. This missing comparison impedes our ability to make general predictions of biodiversity change and to project future species distributions using models. We present a direct comparison of among- versus within-species variation in response to three of the main stresses anticipated with climate change: drought, warming, and frost. Two earlier experiments had experimentally induced (i) summer drought and (ii) spring frost for four common European grass species and their ecotypes from across Europe. To supplement existing data, a third experiment was carried out, to compare variation among species from different functional groups to within-species variation. Here, we simulated (iii) winter warming plus frost for four grasses, two nonleguminous, and two leguminous forbs, in addition to eleven European ecotypes of the widespread grass Arrhenatherum elatius. For each experiment, we measured: (i) C/N ratio and biomass, (ii) chlorophyll content and biomass, and (iii) plant greenness, root (15) N uptake, and live and dead tissue mass. Using coefficients of variation (CVs) for each experiment and response parameter, a total of 156 within- vs. among-species comparisons were conducted, comparing within-species variation in each of four species with among-species variation for each seed origin (five countries). Of the six significant differences, within-species CVs were higher than among-species CVs in four cases. Partitioning of variance within each treatment in two of the three experiments showed that within-species variability (ecotypes) could explain an additional 9% of response variation after accounting for the among-species variation. Our observation that within-species variation was generally as high as among-species variation emphasizes the importance of including both within- and among-species variability in ecological theory (e.g., the insurance hypothesis) and for practical applications (e.g., biodiversity conservation).

Correction: Populations of arable weed species show intra-specific variability in germination base temperature but not in early growth rate.

[This corrects the article DOI: 10.1371/journal.pone.0240538.].

Late autumn warming can both delay and advance spring budburst through contrasting effects on bud dormancy depth in Fagus sylvatica L.

The current state of knowledge on bud dormancy is limited. However, expanding such knowledge is crucial in order to properly model forest responses and feedback to future climate. Recent studies have shown that warming can decrease chilling accumulation and increase dormancy depth, thereby inducing delayed budburst in European beech (Fagus sylvatica L). Whether fall warming can advance spring phenology is unclear. To investigate the effect of warming on endodormancy of deciduous trees, we tested the impact of mild elevated temperature (+2.5-3.5 °C; temperature, on average, kept at 10 °C) in mid and late autumn on the bud dormancy depth and spring phenology of beech. We studied saplings by inducing periods of warming in greenhouses over a 2-year period. Even though warming reduced chilling accumulation in both years, we observed that the response of dormancy depth and spring budburst were year-specific. We found that warming during endodormancy peak could decrease the bud dormancy depth and therefore advance spring budburst. This effect appears to be modulated by factors such as the date of senescence onset and forcing intensity during endodormancy. Results from this study suggest that not only chilling but also forcing controls bud development during endodormancy and that extra forcing in autumn can offset reduced chilling.

Inter-Individual Budburst Variation in Fagus sylvatica Is Driven by Warming Rate.

The onset of the growing season in temperate forests is relevant for forest ecology and biogeochemistry and is known to occur earlier with climate change. Variation in tree phenology among individual trees of the same stand and species, however, is not well understood. Yet, natural selection acts on this inter-individual variation, which consequently affects the adaptive potential to ongoing environmental changes. Budburst dates of 146 mature individuals of Fagus sylvatica, the dominant natural forest tree of central Europe, were recorded over 12 years in one forest stand of 1 ha in the Müritz National Park, Germany. The tree-specific location, topographical differences, as well as social status, were measured to explain the inter-individual variation in budburst. Furthermore, inter-individual differences in bud dormancy were quantified. Additional phenology and weather data across Germany from 405 sites over a 25-year period was used to put the insights from the single stand into perspective. Consistent phenological ranking over the years with respect to early and late flushing trees was observed within the single forest stand, with 23 trees consistently flushing 3-6 days earlier and 22 trees consistently flushing 3-10 days later than the median. Trees flushing consistently early varied most in their spring budburst dates and were less dormant than late-flushing trees already in mid-winter. The higher variation in earlier flushing trees was best explained by a slower warming rate during their budburst period in the observed stand as well as across Germany. Likewise, years with a lower warming rate during the budburst period were more variable in budburst dates. The rate of warming during spring time is crucial to accurately project future within-species variation and the resulting adaptive potential in spring phenology of dominant forest tree species.

Warming Events Advance or Delay Spring Phenology by Affecting Bud Dormancy Depth in Trees.

The frequency of sudden, strong warming events is projected to increase in the future. The effects of such events on spring phenology of trees might depend on their timing because spring warming has generally been shown to advance spring budburst while fall and winter warming have been shown to delay spring phenology. To understand the mechanism behind timing-specific warming effects on spring phenology, I simulated warming events during fall, mid-winter and at the end of winter and quantified their effects on bud dormancy depth and subsequently on spring leaf out. The warming events were carried out in climate chambers on tree seedlings of Betula pendula and Fagus sylvatica in October, January, and February. Control seedlings were kept at photoperiod and temperature matching the daily fluctuating field conditions. Warmed seedlings were kept 10°C warmer than the control seedlings for 10 days during the respective warming periods. Warming in October increased bud dormancy depth and decreased spring leaf-out rate only for F. sylvatica, whereas warming in February reduced bud dormancy depth and advanced spring leaf-out rate only for B. pendula. Neither bud dormancy depth nor spring leaf out rate were affected by January warming. The results indicate that warming-induced changes in bud dormancy depth may explain species- and timing-specific warming effects on spring phenology. The extent to which the timing of bud dormancy phases is species-specific will influence among-species variation in future spring leaf out times.

Populations of arable weed species show intra-specific variability in germination base temperature but not in early growth rate.

Key plant traits affecting growth performance can differ among and within species, influencing competitive plant community dynamics. We determined the intra-specific variability of germination base temperature among 13 arable weed species and the seedlings' early post-emergence relative growth rate among 21 species in climate chamber and green house experiments. Intra-specific variability was quantified with two seed populations (originating from contrasting climate in Germany & France) for the germination base temperature of 6 species and for the early growth rate of 16 species. Inter-specific variability for both traits was always higher than intra-specific variability. Within a given species, we found that germination base temperatures were higher in seeds stemming from colder climate populations. Seedling relative growth rates did not differ between seed populations. Models simulating weed growth should reflect these differences in germination traits among populations, especially when they are used for weed community assembly studies in a local to regional extent.

Differential Thermal Analysis: A Fast Alternative to Frost Tolerance Measurements.

Frost tolerance is an important factor influencing plant growth, plant species distribution and competitive balance among plant species in the face of climate change. Traditional methods for estimating frost tolerance are often time consuming and require a large sample size, limiting the temporal and spatial resolutions. Differential thermal analysis (DTA) can be advantageous compared to other methods used to determine frost tolerance, most importantly by (1) increasing the number of tested species, tissue types and sampling dates, (2) allowing to test frost tolerance in situ, and (3) more realistically testing the influence of freezing rate and duration. Here, we discuss a typical procedure for DTA, compare its use to other frost tolerance methods and point out its limitations.

Community disruption in small biogenic habitats: A coastal invader overcomes habitat complexity to alter community structure.

Non-indigenous species are often identified as threats to native species and communities. Yet, the mechanisms that enable many of these invaders to thrive and alter their newly invaded habitats are still not fully understood. This applies to habitats such as widespread sedimentary shorelines characterized by the presence of scattered biogenic clumps of blue mussels (Mytilus edulis) structurally more complex than bare sediments. In Atlantic Canada, some of these shorelines are numerically dominated by native mud crabs (Dyspanopeus sayi) but have been gradually invaded by the European green crab (Carcinus maenas). This study describes between-habitat (mussel clump vs. bare sediment) differences in density and diversity of invertebrates. It also tests the impact of juvenile green crabs in comparison to native mud crabs using two approaches: First, measuring habitat-related differences in these crabs' feeding rates on a common prey (soft-shell clams, Mya arenaria). Second, measuring their influence on invertebrate communities associated with mussel clumps. The results show that mussel clumps hold higher invertebrate density and diversity than surrounding sedimentary bottoms. In the laboratory, the feeding rates of native mud crabs were dependent on the type of habitat (sand flat > mussel clump), whereas those of green crabs were significantly higher and unrelated to the habitat in which predation occurred. In field experiments, juvenile green crabs were also the only predators that changed community structure in the mussel clump habitat. These results indicate that green crabs can cause a significant impact on native species and communities. Moreover, they suggest that the ability of this species to overcome the refuge provided by complex biogenic habitats for prey may represent an unexplored mechanism to explain this invader's expansion here and elsewhere.

Phenotypic plasticity closely linked to climate at origin and resulting in increased mortality under warming and frost stress in a common grass.

Phenotypic plasticity is important for species responses to global change and species coexistence. Phenotypic plasticity differs among species and traits and changes across environments. Here, we investigated phenotypic plasticity of the widespread grass Arrhenatherum elatius in response to winter warming and frost stress by comparing phenotypic plasticity of 11 geographically and environmentally distinct populations of this species to phenotypic plasticity of populations of different species originating from a single environment. The variation in phenotypic plasticity was similar for populations of a single species from different locations compared to populations of functionally and taxonomically diverse species from one environment for the studied traits (leaf biomass production and root integrity after frost) across three indices of phenotypic plasticity (RDPI, PIN, slope of reaction norm). Phenotypic plasticity was not associated with neutral genetic diversity but closely linked to the climate of the populations' origin. Populations originating from warmer and more variable climates showed higher phenotypic plasticity. This indicates that phenotypic plasticity can itself be considered as a trait subject to local adaptation to climate. Finally, our data emphasize that high phenotypic plasticity is not per se positive for adaptation to climate change, as differences in stress responses are resulting in high phenotypic plasticity as expressed by common plasticity indices, which is likely to be related to increased mortality under stress in more plastic populations.

Winter warming is ecologically more relevant than summer warming in a cool-temperate grassland.

Climate change affects all seasons, but warming is more pronounced in winter than summer at mid- and high latitudes. Winter warming can have profound ecological effects, which are rarely compared to the effects of summer warming, and causal explanations are not well established. We compared mild aboveground infrared warming in winter to warming in summer in a semi-natural, cool-temperate grassland in Germany for four years. Aboveground plant biomass increased following winter warming (+18%) and was unaffected by summer warming. Winter warming affected the composition of the plant community more than summer warming, favoring productive species. Winter warming increased soil respiration more than summer warming. Prolonged growing seasons and changes in plant-community composition accounted for the increased aboveground biomass production. Winter warming stimulated ecological processes, despite causing frost damage to plant roots and microorganisms during an extremely cold period when warming reduced the thermal insulation provided by snow. Future warming beyond such intermittent frosts may therefore further increase the accelerating effects of winter warming on ecological processes.

Intraspecific variation in response to magnitude and frequency of freeze-thaw cycles in a temperate grass.

Winter warming and its accompanying predicted decrease in snow pack for northern temperate regions may increase frost damage to plants induced by an increase in freeze-thaw cycles (FTCs) due to reduced insulation. FTC frequency, minimum temperature during freezing and pre-existing local adaptations potentially all influence site-specific plant responses to future climatic changes. Within a chamber experiment, frost sensitivity towards recurrent FTCs was determined in 12 Dactylis glomerata populations from various European sampling sites differing in temperature and precipitation. After winter hardening, plants were frozen at -4 and -8 °C at frequencies of one, three and seven FTCs within a 1-week treatment phase. The control was kept at 4.5 °C. Plant survival, leaf elongation, chlorophyll content and above-ground net primary productivity (ANPP) decreased with lower minimum temperatures and higher FTC frequencies, while lower freezing temperatures generally proved more influential than increased freezing frequencies. Plant survival rates correlated with the amount of annual precipitation at seed origin, as individuals from comparably drier sites exhibited higher survival rates. This response, however, was limited in its effect to low freezing temperatures (-8 °C) and low and medium freezing frequencies (1 and 3 FTCs). In the set of surviving plants, water availability at seed origin best explained the plants' growth responses to FTC treatment. The observed intraspecific variation emphasizes the ecological importance of potential local adaptations within a more variable future winter climate.

Trait variation in response to varying winter temperatures, diversity patterns and signatures of selection along the latitudinal distribution of the widespread grassland plant Arrhenatherum elatius.

Across Europe, genetic diversity can be expected to decline toward the North because of stochastic and selective effects which may imply diminished phenotypic variation and less potential for future genetic adaptations to environmental change. Understanding such latitudinal patterns can aid provenance selection for breeding or assisted migration approaches. In an experiment simulating different winter temperatures, we assessed quantitative trait variation, genetic diversity, and differentiation for natural populations of the grass Arrhenatherum elatius originating from a large latitudinal gradient. In general, populations from the North grew smaller and had a lower flowering probability. Toward the North, the absolute plastic response to the different winter conditions as well as heritability for biomass production significantly declined. Genetic differentiation in plant height and probability of flowering were very strong and significantly higher than under neutral expectations derived from SNP data, suggesting adaptive differentiation. Differentiation in biomass production did not exceed but mirrored patterns for neutral genetic differentiation, suggesting that migration-related processes caused the observed clinal trait variation. Our results demonstrate that genetic diversity and trait differentiation patterns for A. elatius along a latitudinal gradient are likely shaped by both local selection and genetic drift.

Common garden experiments to characterize cold acclimation responses in plants from different climatic regions.

Cold acclimation is a crucial factor to consider in the context of ongoing climate change. Maladaptation with regard to frost damage and use of the growing season may occur depending on cold acclimation cues. Importance of photoperiod and preceding temperatures as cues needs therefore to be evaluated within (ecotypes) and among species. Common garden designs, in particular the (1) establishment of multiple common gardens along latitudinal/altitudinal gradients, (2) with in situ additional climate manipulations and (3) with manipulations in climate chambers are proposed as tools for the detection of local adaptations and relative importance of temperature and photoperiod as cues for cold adaptation. Here, we discuss issues in species and ecotype selection, establishment of common gardens including manipulations of temperature and photoperiod, and quantification of cold adaptation.