Is a seasonally reduced growth potential a convergent strategy to survive drought and frost in plants?

BACKGROUND: Plants have adapted to survive seasonal life-threatening frost and drought. However, the timing and frequency of such events are impacted by climate change, jeopardizing plant survival. Understanding better the strategies of survival to dehydration stress is therefore timely and can be enhanced by the cross-fertilization of research between disciplines (ecology, physiology), models (woody, herbaceous species) and types of stress (drought, frost). SCOPE: We build upon the 'growth-stress survival' trade-off, which underpins the identification of global plant strategies across environments along a 'fast-slow' economics spectrum. Although phenological adaptations such as dormancy are crucial to survive stress, plant global strategies along the fast-slow economic spectrum rarely integrate growth variations across seasons. We argue that the growth-stress survival trade-off can be a useful framework to identify convergent plant ecophysiological strategies to survive both frost and drought. We review evidence that reduced physiological activity, embolism resistance and dehydration tolerance of meristematic tissues are interdependent strategies that determine thresholds of mortality among plants under severe frost and drought. We show that complete dormancy, i.e. programmed growth cessation, before stress occurrence, minimizes water flows and maximizes dehydration tolerance during seasonal life-threatening stresses. We propose that incomplete dormancy, i.e. the programmed reduction of growth potential during the harshest seasons, could be an overlooked but major adaptation across plants. Quantifying stress survival in a range of non-dormant versus winter- or summer-dormant plants, should reveal to what extent incomplete to complete dormancy could represent a proxy for dehydration tolerance and stress survival. CONCLUSIONS: Our review of the strategies involved in dehydration stress survival suggests that winter and summer dormancy are insufficiently acknowledged as plant ecological strategies. Incorporating a seasonal fast-slow economics spectrum into global plant strategies improves our understanding of plant resilience to seasonal stress and refines our prevision of plant adaptation to extreme climatic events.

Coordination of spring vascular and organ phenology in deciduous angiosperms growing in seasonally cold climates.

In seasonally cold climates, many woody plants tolerate chilling and freezing temperatures by ceasing growth, shedding leaves and entering dormancy. At the same time, transport within these plants often decreases as the vascular system exhibits reduced functionality. As spring growth requires water and nutrients, we ask the question: how much does bud, leaf and flower development depend on the vasculature in spring? In this review, we present what is known about leaf, flower and vascular phenology to sort out this question. In early stages of bud development, buds rely on internal resources and do not appear to require vascular support. The situation changes during organ expansion, after leaves and flowers reconnect to the stem vascular system. However, there are major gaps in our understanding of the timing of vascular development, especially regarding the phloem, as well as the synchronization among leaves, flowers, stem and root vasculature. We believe these gaps are mainly the outcome of research completed in silo and urge future work to take a more integrative approach. We highlight current challenges and propose future directions to make rapid progress on this important topic in upcoming years.

Holm oak fecundity does not acclimate to a drier world.

Climate change might impact tree fecundity by altering the relative influences of meteorological and physiological drivers, and by modifying resource investment in reproduction. Using a 13-yr monitoring of Quercus ilex reproduction in a rainfall exclusion experiment, we analysed the interactive effects of long-term increased aridity and other environmental drivers on the inter-annual variation of fecundity (male flower biomass, number of initiated and mature fruits). Summer-autumn water stress was the main driver of fruit abortion during fruit growth. Rainfall exclusion treatment strongly reduced the number of initiated and mature fruits, even in masting years, and did not increase fruit tolerance to severe drought. Conversely, the relative contribution of the meteorological and physiological drivers, and the inter-annual variability of fruit production were not modified by rainfall exclusion. Rather than inducing an acclimation of tree fecundity to water limitation, increased aridity impacted it negatively through both lower fruit initiation due to changes in resource allocation, and more severe water and resource limitations during fruit growth. Long-term increased aridity affected tree reproduction beyond what is expected from the current response to inter-annual drought variations, suggesting that natural regeneration of holm oak forest could be jeopardised in the future.

Flower phenology as a disruptor of the fruiting dynamics in temperate oak species.

Many perennial plants display masting, that is, fruiting with strong interannual variations, irregular and synchronized between trees within the population. Here, we tested the hypothesis that the early flower phenology in temperate oak species promotes stochasticity into their fruiting dynamics, which could play a major role in tree reproductive success. From a large field monitoring network, we compared the pollen phenology between temperate and Mediterranean oak species. Then, focusing on temperate oak species, we explored the influence of the weather around the time of budburst and flowering on seed production, and simulated with a mechanistic model the consequences that an evolutionary shifting of flower phenology would have on fruiting dynamics. Temperate oak species release pollen earlier in the season than do Mediterranean oak species. Such early flowering in temperate oak species results in pollen often being released during unfavorable weather conditions and frequently results in reproductive failure. If pollen release were delayed as a result of natural selection, fruiting dynamics would exhibit much reduced stochastic variation. We propose that early flower phenology might be adaptive by making mast-seeding years rare and unpredictable, which would greatly help in controlling the dynamics of seed consumers.

Resource manipulation through experimental defoliation has legacy effects on allocation to reproductive and vegetative organs in Quercus ilex.

BACKGROUND AND AIMS: In plants, high costs of reproduction during some years can induce trade-offs in resource allocation with other functions such as growth, survival and resistance against herbivores or extreme abiotic conditions, but also with subsequent reproduction. Such trade-offs might also occur following resource shortage at particular moments of the reproductive cycle. Because plants are modular organisms, strategies for resource allocation to reproduction can also vary among hierarchical levels. Using a defoliation experiment, our aim was to test how allocation to reproduction was impacted by resource limitation. METHODS: We applied three levels of defoliation (control, moderate and intense) to branches of eight Quercus ilex trees shortly after fruit initiation and measured the effects of resource limitation induced by leaf removal on fruit development (survival, growth and germination potential) and on the production of vegetative and reproductive organs the year following defoliation. KEY RESULTS: We found that defoliation had little impact on fruit development. Fruit survival was not affected by the intense defoliation treatment, but was reduced by moderate defoliation, and this result could not be explained by an upregulation of photosynthesis. Mature fruit mass was not affected by defoliation, nor was seed germination success. However, in the following spring defoliated branches produced fewer shoots and compensated for leaf loss by overproducing leaves at the expense of flowers. Therefore, resource shortage decreased resource allocation to reproduction the following season but did not affect sex ratio. CONCLUSIONS: Our results support the idea of a regulation of resource allocation to reproduction beyond the shoot scale. Defoliation had larger legacy effects than immediate effects.

A reversal of the shift towards earlier spring phenology in several Mediterranean reptiles and amphibians during the 1998-2013 warming slowdown.

Herps, especially amphibians, are particularly susceptible to climate change, as temperature tightly controls many parameters of their biological cycle-above all, their phenology. The timing of herps' activity or migration period-in particular the dates of their first appearance in spring and first breeding-and the shift to earlier dates in response to warming since the last quarter of the 20th century has often been described up to now as a nearly monotonic trend towards earlier phenological events. In this study, we used citizen science data opportunistically collected on reptiles and amphibians in the northern Mediterranean basin over a period of 32 years to explore temporal variations in herp phenology. For 17 common species, we measured shifts in the date of the species' first spring appearance-which may be the result of current changes in climate-and regressed the first appearance date against temperatures and precipitations. Our results confirmed the expected overall trend towards earlier first spring appearances from 1983 to 1997, and show that the first appearance date of both reptiles and amphibians fits well with the temperature in late winter. However, the trend towards earlier dates was stopped or even reversed in most species between 1998 and 2013. We interpret this reversal as a response to cooling related to the North Atlantic Oscillation (NAO) in the late winter and early spring. During the positive NAO episodes, for certain species only (mainly amphibians), the effect of a warm weather, which tends to advance the phenology, seems to be counterbalanced by the adverse effects of the relative dryness.

Can phenological models predict tree phenology accurately in the future? The unrevealed hurdle of endodormancy break.

The onset of the growing season of trees has been earlier by 2.3 days per decade during the last 40 years in temperate Europe because of global warming. The effect of temperature on plant phenology is, however, not linear because temperature has a dual effect on bud development. On one hand, low temperatures are necessary to break bud endodormancy, and, on the other hand, higher temperatures are necessary to promote bud cell growth afterward. Different process-based models have been developed in the last decades to predict the date of budbreak of woody species. They predict that global warming should delay or compromise endodormancy break at the species equatorward range limits leading to a delay or even impossibility to flower or set new leaves. These models are classically parameterized with flowering or budbreak dates only, with no information on the endodormancy break date because this information is very scarce. Here, we evaluated the efficiency of a set of phenological models to accurately predict the endodormancy break dates of three fruit trees. Our results show that models calibrated solely with budbreak dates usually do not accurately predict the endodormancy break date. Providing endodormancy break date for the model parameterization results in much more accurate prediction of this latter, with, however, a higher error than that on budbreak dates. Most importantly, we show that models not calibrated with endodormancy break dates can generate large discrepancies in forecasted budbreak dates when using climate scenarios as compared to models calibrated with endodormancy break dates. This discrepancy increases with mean annual temperature and is therefore the strongest after 2050 in the southernmost regions. Our results claim for the urgent need of massive measurements of endodormancy break dates in forest and fruit trees to yield more robust projections of phenological changes in a near future.

How climate, migration ability and habitat fragmentation affect the projected future distribution of European beech.

Recent efforts to incorporate migration processes into species distribution models (SDMs) are allowing assessments of whether species are likely to be able to track their future climate optimum and the possible causes of failing to do so. Here, we projected the range shift of European beech over the 21st century using a process-based SDM coupled to a phenomenological migration model accounting for population dynamics, according to two climate change scenarios and one land use change scenario. Our model predicts that the climatically suitable habitat for European beech will shift north-eastward and upward mainly because (i) higher temperature and precipitation, at the northern range margins, will increase survival and fruit maturation success, while (ii) lower precipitations and higher winter temperature, at the southern range margins, will increase drought mortality and prevent bud dormancy breaking. Beech colonization rate of newly climatically suitable habitats in 2100 is projected to be very low (1-2% of the newly suitable habitats colonised). Unexpectedly, the projected realized contraction rate was higher than the projected potential contraction rate. As a result, the realized distribution of beech is projected to strongly contract by 2100 (by 36-61%) mainly due to a substantial increase in climate variability after 2050, which generates local extinctions, even at the core of the distribution, the frequency of which prevents beech recolonization during more favourable years. Although European beech will be able to persist in some parts of the trailing edge of its distribution, the combined effects of climate and land use changes, limited migration ability, and a slow life-history are likely to increase its threat status in the near future.

Phenological plasticity will not help all species adapt to climate change.

Concerns are rising about the capacity of species to adapt quickly enough to climate change. In long-lived organisms such as trees, genetic adaptation is slow, and how much phenotypic plasticity can help them cope with climate change remains largely unknown. Here, we assess whether, where and when phenological plasticity is and will be adaptive in three major European tree species. We use a process-based species distribution model, parameterized with extensive ecological data, and manipulate plasticity to suppress phenological variations due to interannual, geographical and trend climate variability, under current and projected climatic conditions. We show that phenological plasticity is not always adaptive and mostly affects fitness at the margins of the species' distribution and climatic niche. Under current climatic conditions, phenological plasticity constrains the northern range limit of oak and beech and the southern range limit of pine. Under future climatic conditions, phenological plasticity becomes strongly adaptive towards the trailing edges of beech and oak, but severely constrains the range and niche of pine. Our results call for caution when interpreting geographical variation in trait means as adaptive, and strongly point towards species distribution models explicitly taking phenotypic plasticity into account when forecasting species distribution under climate change scenarios.

Changes in the distribution of multispecies pest assemblages affect levels of crop damage in warming tropical Andes.

Climate induced species range shifts might create novel interactions among species that may outweigh direct climatic effects. In an agricultural context, climate change might alter the intensity of competition or facilitation interactions among pests with, potentially, negative consequences on the levels of damage to crop. This could threaten the productivity of agricultural systems and have negative impacts on food security, but has yet been poorly considered in studies. In this contribution, we constructed and evaluated process-based species distribution models for three invasive potato pests in the Tropical Andean Region. These three species have been found to co-occur and interact within the same potato tuber, causing different levels of damage to crop. Our models allowed us to predict the current and future distribution of the species and therefore, to assess how damage to crop might change in the future due to novel interactions. In general, our study revealed the main challenges related to distribution modeling of invasive pests in highly heterogeneous regions. It yielded different results for the three species, both in terms of accuracy and distribution, with one species surviving best at lower altitudes and the other two performing better at higher altitudes. As to future distributions our results suggested that the three species will show different responses to climate change, with one of them expanding to higher altitudes, another contracting its range and the other shifting its distribution to higher altitudes. These changes will result in novel areas of co-occurrence and hence, interactions of the pests, which will cause different levels of damage to crop. Combining population dynamics and species distribution models that incorporate interspecific trade-off relationships in different environments revealed a powerful approach to provide predictions about the response of an assemblage of interacting species to future environmental changes and their impact on process rates.

Stable water isotopes reveal the onset of bud dormancy in temperate trees, whereas water content is a better proxy for dormancy release.

Earlier spring growth onset in temperate forests is a visible effect of global warming that alters global water and carbon cycling. Consequently, it becomes crucial to accurately predict the future spring phenological shifts in vegetation under different climate warming scenarios. However, current phenological models suffer from a lack of physiological insights of tree dormancy and are rarely experimentally validated. Here, we sampled twig cuttings of five deciduous tree species at two climatically different locations (270 and 750 m a.s.l., ~ 2.3 °C difference) throughout the winter of 2019-20. Twig budburst success, thermal time to budburst, bud water content and short-term 2H-labelled water uptake into buds were quantified to link bud dormancy status with vascular water transport efficacy, with the objective of establishing connections between the dormancy status of buds and their effectiveness in vascular water transport. We found large differences in the dormancy status between species throughout the entire investigation period, likely reflecting species-specific environmental requirements to initiate and release dormancy, whereas only small differences in the dormancy status were found between the two studied sites. We found strong 2H-labelled water uptake into buds during leaf senescence, followed by a sharp decrease, which we ascribed to the initiation of endodormancy. However, surprisingly, we did not find a progressive increase in 2H-labelled water uptake into buds as winter advanced. Nonetheless, all examined tree species exhibited a consistent relationship between bud water content and dormancy status. Our results suggest that short-term 2H-labelled water uptake may not be a robust indicator of dormancy release, yet it holds promise as a method for tracking the induction of dormancy in deciduous trees. By contrast, bud water content emerges as a cost-effective and more reliable indicator of dormancy release.

Modeling temperature-dependent survival with small datasets: insights from tropical mountain agricultural pests.

Many regions are increasingly threatened by agricultural pests but suffer from a lack of data that hampers the development of adequate population dynamics models that could contribute to pest management strategies. Here, we present a new model relating pest survival to temperature and compare its performance with two published models. We were particularly interested in their ability to simulate the deleterious effect of extreme temperatures even when adjusted to datasets that did not include extreme temperature conditions. We adjusted the models to survival data of three species of potato tuber moth (PTM), some major pests in the Tropical Andes. To evaluate model performance, we considered both goodness-of-fit and robustness. The latter consisted in evaluating their ability to predict the actual altitudinal limits of the species in the Ecuadorian Andes. We found that even though our model did not always provide the best fit to data, it predicted extreme temperature mortality and altitudinal limits accurately and better than the other two models. Our study shows that the ability to accurately represent the physiological limits of species is important to provide robust predictions of invasive pests' potential distribution, particularly in places where temperatures approach lethal extremes. The value of our model lies in its ability to simulate accurate thermal tolerance curves even with small datasets, which is useful in places where adequate pest management is urgent but data are scarce.

Reproduction alternation in trees: testing the resource depletion hypothesis using experimental fruit removal in Quercus ilex.

The keystones of resource budget models to explain mast seeding are that fruit production depletes tree stored resources, which become subsequently limiting to flower production the following year. These two hypotheses have, however, rarely been tested in forest trees. Using a fruit removal experiment, we tested whether preventing fruit development would increase nutrient and carbohydrates storage and modify allocation to reproduction and vegetative growth the following year. We removed all the fruits from nine adult Quercus ilex L. trees shortly after fruit set and compared, with nine control trees, the concentrations of nitrogen (N), phosphorus (P), zinc (Zn), potassium (K) and starch in leaves, twigs and trunk before, during and after the development of female flowers and fruits. The following year, we measured the production of vegetative and reproductive organs as well as their location on the new spring shoots. Fruit removal prevented the depletion of N and Zn in leaves during fruit growth. It also modified the seasonal dynamics in Zn, K and starch in twigs, but had no effect on reserves stored in the trunk. Fruit removal increased the production of female flowers and leaves the following year, and decreased the production of male flowers. Our results show that resource depletion operates differently for male and female flowering, because the timing of organ formation and the positioning of flowers in shoot architecture differ between male and female flowers. Our results suggest that N and Zn availability constrain flower production in Q. ilex, but also that other regulatory pathways might be involved. They strongly encourage further experiments manipulating fruit development over multiple years to describe the causal relationships between variations in resource storage and/or uptake, and male and female flower production in masting species.

How do genetic correlations affect species range shifts in a changing environment?

Species may be able to respond to changing environments by a combination of adaptation and migration. We study how adaptation affects range shifts when it involves multiple quantitative traits evolving in response to local selection pressures and gene flow. All traits develop clines shifting in space, some of which may be in a direction opposite to univariate predictions, and the species tracks its environmental optimum with a constant lag. We provide analytical expressions for the local density and average trait values. A species can sustain faster environmental shifts, develop a wider range and greater local adaptation when spatial environmental variation is low (generating low migration load) and multitrait adaptive potential is high. These conditions are favoured when nonlinear (stabilising) selection is weak in the phenotypic direction of the change in optimum, and genetic variation is high in the phenotypic direction of the selection gradient.

Climate change impacts on tree ranges: model intercomparison facilitates understanding and quantification of uncertainty.

Model-based projections of shifts in tree species range due to climate change are becoming an important decision support tool for forest management. However, poorly evaluated sources of uncertainty require more scrutiny before relying heavily on models for decision-making. We evaluated uncertainty arising from differences in model formulations of tree response to climate change based on a rigorous intercomparison of projections of tree distributions in France. We compared eight models ranging from niche-based to process-based models. On average, models project large range contractions of temperate tree species in lowlands due to climate change. There was substantial disagreement between models for temperate broadleaf deciduous tree species, but differences in the capacity of models to account for rising CO(2) impacts explained much of the disagreement. There was good quantitative agreement among models concerning the range contractions for Scots pine. For the dominant Mediterranean tree species, Holm oak, all models foresee substantial range expansion.

Changes in leaf phenology of three European oak species in response to experimental climate change.

*Because the phenology of trees is strongly driven by environmental factors such as temperature, climate change has already altered the vegetative and reproductive phenology of many species, especially in the temperate zone. Here, we aimed to determine whether projected levels of warming for the upcoming decades will lead to linear changes in the phenology of trees or to more complex responses. *We report the results of a 3-yr common garden experiment designed to study the phenological response to artificial climate change, obtained through experimental warming and reduced precipitation, of several populations of three European oaks, two deciduous species (Quercus robur, Quercus pubescens) and one evergreen species (Quercus ilex), in a Mediterranean site. *Experimental warming advanced the seedlings' vegetative phenology, causing a longer growing season and higher mortality. However, the rate of advancement of leaf unfolding date was decreased with increasing temperature. Conversely, soil water content did not affect the phenology of the seedlings or their survival. *Our results show that the phenological response of trees to climate change may be nonlinear, and suggest that predictions of phenological changes in the future should not be built on extrapolations of current observed trends.

Historical phenology: grape ripening as a past climate indicator.

French records of grape-harvest dates in Burgundy were used to reconstruct spring-summer temperatures from 1370 to 2003 using a process-based phenology model developed for the Pinot Noir grape. Our results reveal that temperatures as high as those reached in the 1990s have occurred several times in Burgundy since 1370. However, the summer of 2003 appears to have been extraordinary, with temperatures that were probably higher than in any other year since 1370.

Where is the optimum? Predicting the variation of selection along climatic gradients and the adaptive value of plasticity. A case study on tree phenology.

Many theoretical models predict when genetic evolution and phenotypic plasticity allow adaptation to changing environmental conditions. These models generally assume stabilizing selection around some optimal phenotype. We however often ignore how optimal phenotypes change with the environment, which limit our understanding of the adaptive value of phenotypic plasticity. Here, we propose an approach based on our knowledge of the causal relationships between climate, adaptive traits, and fitness to further these questions. This approach relies on a sensitivity analysis of the process-based model phenofit, which mathematically formalizes these causal relationships, to predict fitness landscapes and optimal budburst dates along elevation gradients in three major European tree species. Variation in the overall shape of the fitness landscape and resulting directional selection gradients were found to be mainly driven by temperature variation. The optimal budburst date was delayed with elevation, while the range of dates allowing high fitness narrowed and the maximal fitness at the optimum decreased. We also found that the plasticity of the budburst date should allow tracking the spatial variation in the optimal date, but with variable mismatch depending on the species, ranging from negligible mismatch in fir, moderate in beech, to large in oak. Phenotypic plasticity would therefore be more adaptive in fir and beech than in oak. In all species, we predicted stronger directional selection for earlier budburst date at higher elevation. The weak selection on budburst date in fir should result in the evolution of negligible genetic divergence, while beech and oak would evolve counter-gradient variation, where genetic and environmental effects are in opposite directions. Our study suggests that theoretical models should consider how whole fitness landscapes change with the environment. The approach introduced here has the potential to be developed for other traits and species to explore how populations will adapt to climate change.

Process-based modeling of species' distributions: what limits temperate tree species' range boundaries?

Niche-based models are widely used to understand what environmental factors determine species' distributions, but they do not provide a clear framework to study the processes involved in defining species' ranges. Here we used a process-based model to identify these processes and to assess the potential distribution of 17 North American boreal/temperate tree species. Using input of only climate and soil properties, the model reproduced the 17 species' distributions accurately. Our results allowed us to identify the climatic factors as well as the biological processes involved in limiting species' ranges. The model showed that climatic constraints limit species' distributions mainly through their impact on phenological processes, and secondarily through their impact on drought and frost mortality. The northern limit of species' ranges appears to be caused mainly by the inability to undergo full fruit ripening and/or flowering, while the southern limit is caused by the inability to flower or by frost injury to flowers. These findings about the ecological processes shaping tree species' distribution represent a crucial step toward obtaining a more complete picture of the potential impact of climate on species' ranges.

Variation in cold hardiness and carbohydrate concentration from dormancy induction to bud burst among provenances of three European oak species.

Although cold hardiness is known to be a major determinant of tree species distribution, its dynamics and the factors that regulate it remain poorly understood. Variation in cold hardiness and carbohydrate concentration, from dormancy induction until bud burst, were investigated in populations of two deciduous (Quercus robur L. and Quercus pubescens Willd.) and one evergreen (Quercus ilex L.) European oak. Mean cold hardiness values in January were -56, -45 and -27 degrees C for Q. robur, Q. pubescens and Q. ilex, respectively. Soluble carbohydrate concentrations were closely related to instantaneous cold hardiness, estimated by the electrolyte leakage method, whereas total carbohydrate concentration was related to maximum cold hardiness. Both cold hardiness and carbohydrate concentration showed a close linear relationship with temperatures at the location of the sampled population. Our results show that temporal variation in both the inter- and intraspecific cold hardiness in European oaks can be related to variations in the concentrations of soluble carbohydrates and that these relationships appear to be driven by temperature.