From observations to experiments in phenology research: investigating climate change impacts on trees and shrubs using dormant twigs

Background and Aims Climate change is advancing the leaf-out times of many plant species and mostly extending the growing season in temperate ecosystems. Laboratory experiments using twig cuttings from woody plant species present an affordable, easily replicated approach to investigate the relative importance of factors such as winter chilling, photoperiod, spring warming and frost tolerance on the leafing-out times of plant communities. This Viewpoint article demonstrates how the results of these experiments deepen our understanding beyond what is possible via analyses of remote sensing and field observation data, and can be used to improve climate change forecasts of shifts in phenology, ecosystem processes and ecological interactions.Scope The twig method involves cutting dormant twigs from trees, shrubs and vines on a single date or at intervals over the course of the winter and early spring, placing them in containers of water in controlled environments, and regularly recording leaf-out, flowering or other phenomena. Prior to or following leaf-out or flowering, twigs may be assigned to treatment groups for experiments involving temperature, photoperiod, frost, humidity and more. Recent studies using these methods have shown that winter chilling requirements and spring warming strongly affect leaf-out and flowering times of temperate trees and shrubs, whereas photoperiod requirements are less important than previously thought for most species. Invasive plant species have weaker winter chilling requirements than native species in temperate ecosystems, and species that leaf-out early in the season have greater frost tolerance than later leafing species.Conclusions This methodology could be extended to investigate additional drivers of leaf-out phenology, leaf senescence in the autumn, and other phenomena, and could be a useful tool for education and outreach. Additional ecosystems, such as boreal, southern hemisphere and sub-tropical forests, could also be investigated using dormant twigs to determine the drivers of leaf-out times and how these ecosystems will be affected by climate change.     

Substantial variation in leaf senescence times among 1360 temperate woody plant species: implications for phenology and ecosystem processes

Background and Aims Autumn leaf senescence marks the end of the growing season in temperate ecosystems. Its timing influences a number of ecosystem processes, including carbon, water and nutrient cycling. Climate change is altering leaf senescence phenology and, as those changes continue, it will affect individual woody plants, species and ecosystems. In contrast to spring leaf out times, however, leaf senescence times remain relatively understudied. Variation in the phenology of leaf senescence among species and locations is still poorly understood.Methods Leaf senescence phenology of 1360 deciduous plant species at six temperate botanical gardens in Asia, North America and Europe was recorded in 2012 and 2013. This large data set was used to explore ecological and phylogenetic factors associated with variation in leaf senescence.Key Results Leaf senescence dates among species varied by 3 months on average across the six locations. Plant species tended to undergo leaf senescence in the same order in the autumns of both years at each location, but the order of senescence was only weakly correlated across sites. Leaf senescence times were not related to spring leaf out times, were not evolutionarily conserved and were only minimally influenced by growth habit, wood anatomy and percentage colour change or leaf drop. These weak patterns of leaf senescence timing contrast with much stronger leaf out patterns from a previous study.Conclusions The results suggest that, in contrast to the broader temperature effects that determine leaf out times, leaf senescence times are probably determined by a larger or different suite of local environmental effects, including temperature, soil moisture, frost and wind. Determining the importance of these factors for a wide range of species represents the next challenge for understanding how climate change is affecting the end of the growing season and associated ecosystem processes.     

Spatial and temporal variations in photosynthetic capacity of a temperate deciduous-evergreen forest

Key message

The understory evergreen trees showed maximal photosynthetic capacity in winter, while the overstory deciduous trees showed this capacity in spring. The time lag in productive ecophysiologically active periods between deciduous overstory and evergreen understory trees in a common temperate forest was clearly related to the amount of overstory foliage.

Abstract

In temperate forests, where deciduous canopy trees and evergreen understory trees coexist, understory trees experience great variation in incident radiation corresponding to canopy dynamics represented by leaf-fall and leaf-out. It is generally thought that changes in the light environment affect understory plants’ ecophysiological traits. Thus, to project and estimate annual energy, water, and carbon exchange between forests and the atmosphere, it is necessary to investigate seasonal variation in the ecophysiological activities of both evergreen trees in the understory and deciduous trees that make up the canopy/overstory. We conducted leaf-scale gas-exchange measurements and nitrogen content analyses for six tree species along their heights throughout a complete year. Photosynthetic capacity as represented by the maximum carboxylation rate (V _cmax25) and photosynthetic nitrogen use efficiency (PNUE) of deciduous canopy trees peaked immediately after leaf-out in late May, declined and stabilised during the mid-growing season, and drastically decreased just before leaf-fall. On the other hand, the timing of lowest V _cmax25 and PNUE for evergreen understory trees coincided with that of the highest values for canopy trees. Furthermore, understory trees’ highest values appeared just before canopy tree leaf-out, when incident radiation in the understory was highest. This implies that failing to consider seasonal variation in leaf ecophysiological traits for both canopy and understory trees could lead to serious errors in estimating ecosystem productivity and energy balance for temperate forests.

     

Divergent phenological response to hydroclimate variability in forested mountain watersheds

Mountain watersheds are primary sources of freshwater, carbon sequestration, and other ecosystem services. There is significant interest in the effects of climate change and variability on these processes over short to long time scales. Much of the impact of hydroclimate variability in forest ecosystems is manifested in vegetation dynamics in space and time. In steep terrain, leaf phenology responds to topoclimate in complex ways, and can produce specific and measurable shifts in landscape forest patterns. The onset of spring is usually delayed at a specific rate with increasing elevation (often called Hopkins' Law; Hopkins, 1918), reflecting the dominant controls of temperature on greenup timing. Contrary with greenup, leaf senescence shows inconsistent trends along elevation gradients. Here, we present mechanisms and an explanation for this variability and its significance for ecosystem patterns and services in response to climate. We use moderate‐resolution imaging spectro‐radiometer (MODIS) Normalized Difference Vegetation Index (NDVI) data to derive landscape‐induced phenological patterns over topoclimate gradients in a humid temperate broadleaf forest in southern Appalachians. These phenological patterns are validated with different sets of field observations. Our data demonstrate that divergent behavior of leaf senescence with elevation is closely related to late growing season hydroclimate variability in temperature and water balance patterns. Specifically, a drier late growing season is associated with earlier leaf senescence at low elevation than at middle elevation. The effect of drought stress on vegetation senescence timing also leads to tighter coupling between growing season length and ecosystem water use estimated from observed precipitation and runoff generation. This study indicates increased late growing season drought may be leading to divergent ecosystem response between high and low elevation forests. Landscape‐induced phenological patterns are easily observed over wide areas and may be used as a unique diagnostic for sources of ecosystem vulnerability and sensitivity to hydroclimate change.     

Deciduousness in a seasonal tropical forest in western Thailand: interannual and intraspecific variation in timing, duration and environmental cues

Seasonal tropical forests exhibit a great diversity of leaf exchange patterns. Within these forests variation in the timing and intensity of leaf exchange may occur within and among individual trees and species, as well as from year to year. Understanding what generates this diversity of phenological behaviour requires a mechanistic model that incorporates rate-limiting physiological conditions, environmental cues, and their interactions. In this study we examined long-term patterns of leaf flushing for a large proportion of the hundreds of tree species that co-occur in a seasonal tropical forest community in western Thailand. We used the data to examine community-wide variation in deciduousness and tested competing hypotheses regarding the timing and triggers of leaf flushing in seasonal tropical forests. We developed metrics to quantify the nature of deciduousness (its magnitude, timing and duration) and its variability among survey years and across a range of taxonomic levels. Tree species varied widely in the magnitude, duration, and variability of leaf loss within species and across years. The magnitude of deciduousness ranged from complete crown loss to no crown loss. Among species that lost most of their crown, the duration of deciduousness ranged from 2 to 21 weeks. The duration of deciduousness in the majority of species was considerably shorter than in neotropical forests with similar rainfall periodicity. While the timing of leaf flushing varied among species, most (∼70%) flushed during the dry season. Leaf flushing was associated with changes in photoperiod in some species and the timing of rainfall in other species. However, more than a third of species showed no clear association with either photoperiod or rainfall, despite the considerable length and depth of the dataset. Further progress in resolving the underlying internal and external mechanisms controlling leaf exchange will require targeting these species for detailed physiological and microclimatic studies.     

Divergent carbon cycle response of forest and grass‐dominated northern temperate ecosystems to record winter warming

Northern temperate ecosystems are experiencing warmer and more variable winters, trends that are expected to continue into the foreseeable future. Despite this, most studies have focused on climate change impacts during the growing season, particularly when comparing responses across different vegetation cover types. Here we examined how a perennial grassland and adjacent mixed forest ecosystem in New Hampshire, United States, responded to a period of highly variable winters from 2014 through 2017 that included the warmest winter on record to date. In the grassland, record‐breaking temperatures in the winter of 2015/2016 led to a February onset of plant growth and the ecosystem became a sustained carbon sink well before winter ended, taking up roughly 90 g/m² more carbon during the winter to spring transition than in other recorded years. The forest was an unusually large carbon source during the same period. While forest photosynthesis was restricted by leaf‐out phenology, warm winter temperatures caused large pulses of ecosystem respiration that released nearly 230 g C/m² from February through April, more than double the carbon losses during that period in cooler years. These findings suggest that, as winters continue to warm, increases in ecosystem respiration outside the growing season could outpace increases in carbon uptake during a longer growing season, particularly in forests that depend on leaf‐out timing to initiate carbon uptake. In ecosystems with a perennial leaf habit, warming winter temperatures are more likely to increase ecosystem carbon uptake through extension of the active growing season. Our results highlight the importance of understanding relationships among antecedent winter conditions and carbon exchange across land‐cover types to understand how landscape carbon exchange will change under projected climate warming.     

Spring leaf phenology and the diurnal temperature range in a temperate maple forest

Spring leaf phenology in temperate climates is intricately related to numerous aspects of the lower atmosphere [e.g., surface energy balance, carbon flux, humidity, the diurnal temperature range (DTR)]. To further develop and improve the accuracy of ecosystem and climate models, additional investigations of the specific nature of the relationships between spring leaf phenology and various ecosystem and climate processes are required in different environments. This study used visual observations of maple leaf phenology, below-canopy light intensities, and micrometeorological data collected during the spring seasons of 2008, 2009, and 2010 to examine the potential influence of leaf phenology on a seasonal transition in the trend of the DTR. The timing of a reversal in the DTR trend occurred near the time when the leaves were unfolding and expanding. The results suggest that the spring decline in the DTR can be attributed primarily to the effect of canopy closure on daily maximum temperature. These findings improve our understanding of the relationship between leaf phenology and the diurnal temperature range in temperate maple forests during the spring. They also demonstrate the necessity of incorporating accurate phenological data into ecosystem and climate models and warrant a careful examination of the extent to which canopy phenology is currently incorporated into existing models.     

Field evidence for earlier leaf-out dates in alpine grassland on the eastern Tibetan Plateau from 1990 to 2006

Worldwide, many plant species are experiencing an earlier onset of spring phenophases due to climate warming. Rapid recent temperature increases on the Tibetan Plateau (TP) have triggered changes in the spring phenology of the local vegetation. However, remote sensing studies of the land surface phenology have reached conflicting interpretations about green-up patterns observed on the TP since the mid-1990s. We investigated this issue using field phenological observations from 1990 to 2006, for 11 dominant plants on the TP at the levels of species, families (Gramineae—grasses and Cyperaceae—sedges) and vegetation communities (alpine meadow and alpine steppe). We found a significant trend of earlier leaf-out dates for one species (Koeleria cristata). The leaf-out dates of both Gramineae and Cyperaceae had advanced (the latter significantly, starting an average of 9 days later per year than the former), but the correlation between them was significant. The leaf-out dates of both vegetation communities also advanced, but the pattern was only significant in the alpine meadow. This study provides the first field evidence of advancement in spring leaf phenology on the TP and suggests that the phenology of the alpine steppe can differ from that of the alpine meadow. These findings will be useful for understanding ecosystem responses to climate change and for grassland management on the TP.     

Interactive climate factors restrict future increases in spring productivity of temperate and boreal trees

Climate warming is currently advancing spring leaf‐out of temperate and boreal trees, enhancing net primary productivity (NPP) of forests. However, it remains unclear whether this trend will continue, preventing for accurate projections of ecosystem functioning and climate feedbacks. Several ecophysiological mechanisms have been proposed to regulate the timing of leaf emergence in response to changing environmental cues, but the relative importance of those mechanisms remains unclear. Here, we use 727,401 direct phenological observations of common European forest trees to examine the dominant controls on leaf‐out. Using the emerging mechanisms, we forecast future trajectories of spring arrival and evaluate the consequences for forest carbon dynamics. By representing hypothesized relationships with autumn temperature, winter chilling, and the timing of spring onset, we accurately predicted reductions in the advance of leaf‐out. There was a strong consensus between our empirical model and existing process‐based models, revealing that the advance in leaf‐out will not exceed 2 weeks over the rest of the century. We further estimate that, under a ‘business‐as‐usual’ climate scenario, earlier spring arrival will enhance NPP of temperate and boreal forests by ~0.2 Gt per year at the end of the century. In contrast, previous estimates based on a simple degree‐day model range around 0.8 Gt. As such, the expected NPP is drastically reduced in our updated model relative to previous estimates—by a total of ~25 Gt over the rest of the century. These findings reveal important environmental constraints on the productivity of broad‐leaved deciduous trees and highlight that shifting spring phenology is unlikely to slow the rate of warming by offsetting anthropogenic carbon emissions.     

Inter-annual variation in the response of leaf-out onset to soil moisture increase in a teak plantation in northern Thailand

To understand the impact of inter-annual climate change on vegetation-atmosphere mass and energy exchanges, it has become necessary to explore changes in leaf-out onset in response to climatic fluctuations. We examined the response of leaf-out and transpiration onset dates to soil moisture in a teak plantation in northern Thailand based on a 12-year leaf area index and sap flow measurements. The date of leaf-out and transpiration onset varied between years by up to 40 days, and depended on the initial date when the relative extractable water in a soil layer of 0–0.6 m (Θ) was greater than 0.2 being consistent with our previous results. Our new finding is that the delay in leaf-out and transpiration onset relative to the initial date when Θ?>?0.2 increases linearly as the initial date on which Θ?>?0.2 becomes earlier. The delay spans about 20 days in years when Θ?>?0.2 occurs in March (the late dry season)—much earlier than usual because of heavy pre-monsoon rainfalls—while there is little delay in years when Θ?>?0.2 occurs in May. This delay indicates the influence of additional factors on leaf-out onset, which controls the delay in the response of leaf-out to soil moisture increase. The results increased our knowledge about the pattern and extent of the changes in leaf phenology that occur in response to the inter-annual climate variation in tropical regions, where, in particular, such research is needed.     

Ecosystem Consequences of Exotic Earthworm Invasion of North Temperate Forests

The invasion of north temperate forests by exotic species of earthworms is an important issue that has been overlooked in the study and management of these forests. We initiated research to address the hypothesis that earthworm invasion will have large consequences for nutrient retention and uptake in these ecosystems. In this special feature of Ecosystems, we present five papers describing results from our experiment. In this paper, we (a) introduce our experimental approach and conceptual model of how earthworms influence forest ecosystem processes, (b) describe the characteristics of the study areas and earthworm communities at our two study locations, and (c) provide a brief overview and synthesis of the main findings. The most dramatic effect of earthworm invasion was the loss of the forest floor at an undisturbed forest site, which altered the location and nature of nutrient cycling activity in the soil profile. Invasion changed soil total carbon (C) and phosphorus (P) pools, carbon–nitrogen (C:N) ratios, the loss and distribution of different soil P fractions, and the distribution and function of roots and microbes. Response to invasion varied with site characteristics and earthworm species. Our results suggest that exotic earthworm invasion is a significant factor that will influence the structure and function of northern temperate forest ecosystems over the next few decades. Regional evaluations of these forests will need to consider the presence or absence of earthworms along with other important ecosystem drivers, such as pollution, climate, and underlying soil characteristics.     

Multiscale modeling of spring phenology across Deciduous Forests in the Eastern United States

Phenological events, such as bud burst, are strongly linked to ecosystem processes in temperate deciduous forests. However, the exact nature and magnitude of how seasonal and interannual variation in air temperatures influence phenology is poorly understood, and model‐based phenology representations fail to capture local‐ to regional‐scale variability arising from differences in species composition. In this paper, we use a combination of surface meteorological data, species composition maps, remote sensing, and ground‐based observations to estimate models that better represent how community‐level species composition affects the phenological response of deciduous broadleaf forests to climate forcing at spatial scales that are typically used in ecosystem models. Using time series of canopy greenness from repeat digital photography, citizen science data from the USA National Phenology Network, and satellite remote sensing‐based observations of phenology, we estimated and tested models that predict the timing of spring leaf emergence across five different deciduous broadleaf forest types in the eastern United States. Specifically, we evaluated two different approaches: (i) using species‐specific models in combination with species composition information to ‘upscale’ model predictions and (ii) using repeat digital photography of forest canopies that observe and integrate the phenological behavior of multiple representative species at each camera site to calibrate a single model for all deciduous broadleaf forests. Our results demonstrate variability in cumulative forcing requirements and photoperiod cues across species and forest types, and show how community composition influences phenological dynamics over large areas. At the same time, the response of different species to spatial and interannual variation in weather is, under the current climate regime, sufficiently similar that the generic deciduous forest model based on repeat digital photography performed comparably to the upscaled species‐specific models. More generally, results from this analysis demonstrate how in situ observation networks and remote sensing data can be used to synergistically calibrate and assess regional parameterizations of phenology in models.     

Drought-deciduous behavior reduces nutrient losses from temperate deciduous trees under severe drought

Nutrient resorption from senescing leaves is an important mechanism of nutrient conservation in temperate deciduous forests. Resorption, however, may be curtailed by climatic events that cause rapid leaf death, such as severe drought, which has been projected to double by the year 2100 in the eastern United States. During a record drought in the southeastern US, we studied 18 common temperate winter-deciduous trees and shrubs to understand how extreme drought affects nutrient resorption of the macronutrients N, P, K, and Ca. Four species exhibited drought-induced leaf senescence and maintained higher leaf water potentials than the remaining 14 species (here called drought-evergreen species). This strategy prevented extensive leaf desiccation during the drought and successfully averted large nutrient losses caused by leaf desiccation. These four drought-deciduous species were also able to resorb N, P, and K from drought-senesced leaves, whereas drought-evergreen species did not resorb any nutrients from leaves lost to desiccation during the drought. For Oxydendrum arboreum, the species most severely affected by the drought, our results indicate that trees lost 50% more N and P due to desiccation than would have been lost from fall senescence alone. For all drought-deciduous species, resorption of N and P in fall-senesced leaves was highly proficient, whereas resorption was incomplete for drought-evergreen species. The lower seasonal nutrient losses of drought-deciduous species may give them a competitive advantage over drought-evergreen species in the years following the drought, thereby impacting species composition in temperate deciduous forests in the future.     

Estimating Daytime Ecosystem Respiration to Improve Estimates of Gross Primary Production of a Temperate Forest

Leaf respiration is an important component of carbon exchange in terrestrial ecosystems, and estimates of leaf respiration directly affect the accuracy of ecosystem carbon budgets. Leaf respiration is inhibited by light; therefore, gross primary production (GPP) will be overestimated if the reduction in leaf respiration by light is ignored. However, few studies have quantified GPP overestimation with respect to the degree of light inhibition in forest ecosystems. To determine the effect of light inhibition of leaf respiration on GPP estimation, we assessed the variation in leaf respiration of seedlings of the dominant tree species in an old mixed temperate forest with different photosynthetically active radiation levels using the Laisk method. Canopy respiration was estimated by combining the effect of light inhibition on leaf respiration of these species with within-canopy radiation. Leaf respiration decreased exponentially with an increase in light intensity. Canopy respiration and GPP were overestimated by approximately 20.4% and 4.6%, respectively, when leaf respiration reduction in light was ignored compared with the values obtained when light inhibition of leaf respiration was considered. This study indicates that accurate estimates of daytime ecosystem respiration are needed for the accurate evaluation of carbon budgets in temperate forests. In addition, this study provides a valuable approach to accurately estimate GPP by considering leaf respiration reduction in light in other ecosystems.     

暖温带落叶阔叶林碳循环的初步估算

 森林生态系统碳循环过程与大气中二氧化碳含量有密切的关系,直接影响着大气成分的组成,进而对全球气候变化有重要影响。以我国暖温带落叶阔叶林生态系统近10年的定位研究为基础,初步建立了该类生态系统碳循环数值模式。结果表明：暖温带落叶阔叶林典型生态系统每年从外界主要是大气中吸收的碳是10.3 t·hm-2·a-1,植物呼吸释放到大气中的碳通量为5.5 t·hm-2·a-1。森林植物干物质积存的碳量为4.8 t·hm-2·a-1,通过凋落物分解释放到大气中的碳通量为2.46 t·hm-2·a-1。森林同化的碳绝大部分以活生物呼吸和凋落物分解的形式释放到大气中去了,存留在活生物体和凋落物中的很少。通过对碳现存量的研究发现,所研究的森林生态系统碳现存量为165.05 t·hm-2,其中活生物体碳现存量为61.2 t·hm-2,死生物体碳现存量为104.05 t·hm-2 (包括土壤中碳),土壤碳现存量为96 t·hm-2。土壤碳储量占总碳储量的58%,土壤是该地区森林生态系统主要的碳库,森林生态系统土壤中碳储量的变化必然引起整个区域碳储量整体动态的变化。     

南京地区落叶栎林木本植物叶物候研究

叶物候参数长期以来被认为与植物的碳获取的最大化有关,能反映物种的资源利用策略。温带地区因为寒冷冬天的限制,延长叶寿命成为一些物种进行生长发育和繁衍的基础。为探讨叶寿命延长的可能途径(早出叶、晚落叶,或两者兼有),该研究以南京地区两个落叶栎(Quercus spp.)林为研究对象,观测了其中木本植物的出叶物候、落叶物候,并分析了它们与叶寿命之间的关系。结果发现:1)不同物种的出叶开始时间相差较大,出叶早的物种早结束出叶过程;2)不同物种的落叶开始时间相差较大,早开始落叶的物种,落叶持续时间较长,落叶结束时间则相对集中。3)相关分析和回归分析都表明,叶寿命与出叶时间和落叶时间显著关联,但早出叶对叶寿命的延长可能更为重要,因为早出叶相对于晚落叶在物种资源利用上比较具有优势。4)不同物种的出叶时间和落叶时间没有显著相关,可能因为出叶过程和落叶过程是由不同的启动因子引起。这说明延长叶寿命不一定同时通过早出叶和晚落叶来达到。     

Tree leaf out response to temperature: comparing field observations,remote sensing,and a warming experiment

Leaf out time is a widely used indicator of climate change and represents a critical transition point of annual seasonality in most temperate ecosystems. We compared three sources of data to determine the effect of spring temperature on tree leaf out: field observations, remotely sensed satellite data, and experimental warming. All three methods recorded earlier leaf out with warmer spring temperatures. However, leaf out timing was more than twice as sensitive to temperature in the field study (advancing at a rate of 6.1 days/°C), as under experimental warming (2.1 days/°C), with remote sensing intermediate (3.7 days/°C). Researchers need to be aware of the currently unexplained differences among methodologies when using phenological data to parameterize or benchmark models that represent ecosystem processes. The mechanisms behind these discrepancies must be better understood if we are to confidently predict responses of leaf out timing to future climates.     

中国温带和亚热带8个树种叶和吸收根协同分解

叶和细根(2mm)是森林生态系统的分解主体,二者是否协同分解,将极大影响所属植物在生态系统碳(C)循环中的物种效应。已有研究显示,叶和细根的分解关系具有极大的不确定性,认为很大程度上归因于细根内部具有高度的异质性,导致叶和细根在功能上不相似。为此,使用末梢1级根和细根根枝作为研究对象,它们在功能上同叶类似,称为吸收根。通过分解包法,分别在黑龙江帽儿山和广东鹤山,研究了2个阔叶树种和2个针叶树种(共8个树种)的叶和吸收根持续2a多的分解。结果发现,分解速率k(a~(-1),负指数模型)在8个树种整体分析时具有正相关关系(P0.05),在相同气候带或植物生活型水平上是否相关,受叶的分解环境及吸收根类型的影响;N剩余量整体上并不相关,亚热带树种的叶和细根根枝的N剩余量在分解1a后高度显著正相关,温带树种的叶和1级根的N剩余量在分解2a后显著高度正相关。本研究中,根-叶分解过程是否受控于相同或相关的凋落物性质是决定根-叶分解是否相关的重要原因,其中分解速率与酸溶组分正相关、与酸不溶组分负相关。比较已有研究,总结发现,根-叶分解关系受物种影响较大,暗示气候变化导致物种组成的改变将极大影响地上-地下关系,也因此影响生态系统C循环。     

A parameterization of leaf phenology for the terrestrial ecosystem component of climate models

Leaf phenology remains one of the most difficult processes to parameterize in terrestrial ecosystem models because our understanding of the physical processes that initiate leaf onset and senescence is incomplete. While progress has been made at the molecular level, for example by identifying genes that are associated with senescence and flowering for selected plant species, a picture of the processes controlling leaf phenology is only beginning to emerge. A variety of empirical formulations have been used with varying degrees of success in terrestrial ecosystem models for both extratropical and tropical biomes. For instance, the use of growing degree‐days (GDDs) to initiate leaf onset has received considerable recognition and this approach is used in a number of models. There are, however, limitations when using GDDs and other empirically based formulations in global transient climate change simulations. The phenology scheme developed for the Canadian Terrestrial Ecosystem Model (CTEM), designed for inclusion in the Canadian Centre for Climate Modelling and Analysis coupled general circulation model, is described. The representation of leaf phenology is general enough to be applied over the globe and sufficiently robust for use in transient climate change simulations. Leaf phenology is functionally related to the (possibly changing) climate state and to atmospheric composition rather than to geographical boundaries or controls implicitly based on current climate. In this approach, phenology is controlled by environmental conditions as they affect the carbon balance. A carbon‐gain‐based scheme initiates leaf onset when it is beneficial for the plant, in carbon terms, to produce new leaves. Leaf offset is initiated by unfavourable environmental conditions that incur carbon losses and these include shorter day length, cooler temperatures, and dry soil moisture conditions. The comparison of simulated leaf onset and offset times with observation‐based estimates for temperate and boreal deciduous, tropical evergreen, and tropical deciduous plant functional types at selected locations indicates that the phenology scheme performs satisfactorily. Model simulated leaf area index and stem and root biomass are also compared with observational estimates to illustrate the performance of CTEM.     

Fruiting and flushing phenology in Asian tropical and temperate forests: implications for primate ecology

In order to understand the ecological adaptations of primates to survive in temperate forests, we need to know the general patterns of plant phenology in temperate and tropical forests. Comparative analyses have been employed to investigate general trends in the seasonality and abundance of fruit and young leaves in tropical and temperate forests. Previous studies have shown that (1) fruit fall biomass in temperate forest is lower than in tropical forest, (2) non-fleshy species, in particular acorns, comprise the majority of the fruit biomass in temperate forest, (3) the duration of the fruiting season is shorter in temperate forest, and (4) the fruiting peak occurs in autumn in most temperate forests. Through our comparative analyses of the fruiting and flushing phenology between Asian temperate and tropical forests, we revealed that (1) fruiting is more annually periodic (the pattern in one year is similar to that seen in the next year) in temperate forest in terms of the number of fruiting species or trees, (2) there is no consistent difference in interannual variations in fruiting between temperate and tropical forests, although some oak-dominated temperate forests exhibit extremely large interannual variations in fruiting, (3) the timing of the flushing peak is predictable (in spring and early summer), and (4) the duration of the flushing season is shorter. The flushing season in temperate forests (17–28 % of that in tropical forests) was quite limited, even compared to the fruiting season (68 %). These results imply that temperate primates need to survive a long period of scarcity of young leaves and fruits, but the timing is predictable. Therefore, a dependence on low-quality foods, such as mature leaves, buds, bark, and lichens, would be indispensable for temperate primates. Due to the high predictability of the timing of fruiting and flushing in temperate forests, fat accumulation during the fruit-abundant period and fat metabolization during the subsequent fruit-scarce period can be an effective strategy to survive the lean period (winter).