Heikki Hänninen

• PhD in Agriculture and Forestry
• Professor at Zhejiang Agriculture & Forestry University

In this chapter, we provide an overview of plant phenology modeling, focusing on mechanistic phenology models. After a brief history of plant phenology modeling, we present the different models, which have been described in the literature and highlight the main differences between them, i.e. their degree of complexity and the different types of res...

Lammas growth of trees means the additional growth of the shoot after the growth cessation and bud set in late summer. In temperate tree species, lammas growth occurs irregularly and is often regarded as abnormal, disturbed growth. In subtropical tree species, however, lammas growth is a prevalent phenomenon, possibly due to the prolonged occurrenc...

In studies of plant spring phenology, temperature sum models are traditional tools. They are used to quantify plant development in terms of accumulation of temperature-dependent developmental units, such as Growing Degree Hours, GDHs. A key parameter in these models is the threshold (or base) temperature, Tthr, representing the lower thermal limit...

Winter rest and chilling accumulation play a crucial role in regulating the leaf-out and flowering of extratropical woody plants. Still, there is a lack of understanding regarding the potential rest condition of overwintered immature cones of coniferous trees and how the dormancy of different organ types responds to environmental cues. To address t...

Spring phenology is a key indicator of temperate and boreal ecosystems' response to climate change. To date, most phenological studies have analyzed the mean date of budburst in tree populations while overlooking the large variability of budburst among individual trees. The consequences of neglecting the within-population variability (WPV) of budbu...

In autumn, the buds of extratropical trees are in a state of endodormancy, since regardless of the prevailing environmental conditions, growth cannot be activated in these buds because the dormancy is caused by physiological factors in the buds. In natural conditions the growth-arresting physiological factors are removed by prolonged exposure to lo...

Spring phenology is a key indicator of temperate and boreal ecosystems’ response to climate change. To date, most phenological studies have analyzed the mean date of budburst in tree populations while overlooking the large variability of budburst among individual trees. The consequences of neglecting the within-population variability (WPV) of budbu...

Global warming has generally advanced the spring phenology of extratropical trees. In several cases, however, the advancing has levelled off, indicating a declining temperature sensitivity of phenological timing. The potential reasons for the decline have been actively debated, but no direct experimental evidence has been produced to support any of...

Forests are increasingly exposed to extreme global warming-induced climatic events. However, the immediate and carry-over effects of extreme events on forests are still poorly understood. Gross primary productivity (GPP) capacity is regarded as a good proxy of the ecosystem's functional stability, reflecting its physiological response to its surrou...

Climatic warming is currently changing the spring phenology of extratropical trees, and this has several important effects on the trees and ecosystems. The major climatic cues regulating the spring phenology are winter chilling, spring forcing, and photoperiod. The interactions between these three remain largely unstudied because most studies conce...

Bud dormancy and its release are complex physiological phenomena in plants. The molecular mechanisms of bud dormancy in Liriodendron chinense are mainly unknown. Here, we studied bud dormancy and the related physiological and molecular phenomena in Liriodendron under long-day (LD) and short-day (SD). Bud burst was released faster under LD than unde...

Climate warming has significantly altered the phenology of plants in recent decades. However, in contrast to the widely reported warming‐induced extension of vegetative growing season, the response of fruit development period (FDP) from flowering to fruiting remains largely unexplored, particularly for woody plants. Analyzing >560,000 in situ obser...

Key message Autumn phenology and physiology in the subtropical tree speciesTorreya grandisand in a subtropical provenance ofCarya illinoinensisare affected by air temperature rather than photoperiod. Abstract Though leaf phenology is a key tree trait affecting several ecological processes in forested ecosystems, its environmental and genetic regul...

Process-based phenological models are currently used for assessing the effects of climatic warming on the timing of spring phenological events, such as leafout and flowering, in trees. However, the biological realism of the models may be undermined by the practices of often formulating the models solely on the basis of observational records of the...

Pecan (Carya illinoinensis) is an important nut tree species in its native areas in temperate and subtropical North America, and as an introduced crop in subtropical southeastern China as well. We used process-based modeling to assess the effects of climatic warming in southeastern China on the leaf-out phenology of pecan seedlings and the subseque...

• Key message The increase in climate variability is likely to generate an increased occurrence of both frost-induced and drought-induced damages on perennial plants. We examined how these stress factors can potentially interact and would subsequently affect the vulnerability to each other. Furthermore, we discussed how this vulnerability could be...

Endodormancy and the related chilling requirement synchronize the seasonal development of trees from the boreal and temperate regions under the climatic conditions prevailing at their native growing sites. The phenomenon of endodormancy has been known at the whole‐plant level for 100 years, and in the last couple of decades, insights into the physi...

Frost hardiness (FH) is one of the key traits that limits the distribution of tree species in the north. Different species and ecotypes respond differently to the drivers of frost hardening and may therefore have different survival capacities, especially in their northern distribution range. Several southern tree species such as pedunculate oak (Qu...

The environmental regulation of spring phenology in boreal and temperate trees is generally well-understood, but little is known about the regulation in subtropical trees. It has been shown recently that similarly to the more northern trees, subtropical trees also exhibit rest (endodormancy) and chilling requirement of rest break (chilling requirem...

A R T I C L E I N F O Keywords: Bud burst chilling requirement climatic variation endodormancy flowering leafout subtropical trees tree phenology A B S T R A C T Spring phenology is a key phenomenon mediating the effects of climate change on terrestrial plants and ecosystems , but in regard to subtropical trees, the dormancy mechanisms that regulat...

We developed process-based tree phenology models for four subtropical tree species, and for the first time for these trees, we based the model development on explicit experimental work particularly designed to address the processes being modelled. For all the four species, a model of seedling leafout was developed, and for Torreya grandis , a model...

To project the effects of climatic warming on the timing of spring leafout and flowering in trees, process-based tree phenology models are often used nowadays. Unfortunately, the biological realism of the models is often compromised because the model development has often been based on various assumptions and indirect methods. We developed process-...

Leaf‐out and flowering are two key phenological events of plants, denoting the respective onsets of visible vegetative growth and reproduction during the year. For each species, the schedule of vegetative growth and reproduction is crucial to the maximization of its fitness. Warming‐induced advances of leaf‐out and flowering have been reported freq...

Aim Vegetation phenology is highly sensitive to climate change. The timing of spring phenology in temperate grasslands is regulated primarily by temperature and precipitation. The aim of this study was to determine whether the primary factor regulating vegetation phenology has changed under ongoing climate change and the underlying mechanisms. Loc...

In tundra ecosystems, snow cover protects plants from low temperatures in winter and buffers temperature fluctuations in spring. Climate change may lead to reduced snowfall and earlier snowmelt, potentially exposing plants to more frequent and more severe frosts in the future. Frost can cause cell damage and, in combination with high solar irradian...

A warmer world could extend the growing seasons for plants. Changes in spring phenology have been studied, yet autumn phenology remains poorly understood. Using >500,000 phenological records of four temperate tree species between 1951 and 2013 in Europe, we show that leaf senescence in warm autumns exhibits stronger climate responses, with a higher...

Fruits of hickory (Carya cathayensis) are larger and their peel is greener after interspecific pollination by pecan (Carya illinoinensis; later pp fruits) than after intraspecific pollination by hickory (later ph fruits). Previous studies have found little genetic differences between offspring and their maternal parent, indicating that the observed...

Studies addressing endodormancy release in adult trees are usually carried out using twigs detached from the trees in the experiments. Potential problems caused by cutting the root-shoot connection when detaching the twigs can be avoided by using grafts as the experimental material. We studied the effects of chilling on the endodormancy release in...

Spring vegetation phenology is one of the most sensitive bio-indicators of the ongoing climate warming. Climate warming has substantially advanced spring phenological development and increased productivity of terrestrial ecosystems. However, the relative importance of spring phenology and climatic factors on vegetation growth has not yet been thoro...

Bud dormancy of plants has traditionally been explained either by physiological growth arresting conditions in the bud, or by unfavourable environmental conditions, such as non‐growth‐promoting low air temperatures. This conceptual dichotomy has provided the framework also for developing process‐based plant phenology models. Here we propose a novel...

Ppmar1 and Ppmar2 are two active mariner-like elements (MLEs) cloned from moso bamboo (Phyllostachys edulis (Carrière) J. Houz) genome possessing transposases that harbour nuclear export signal (NES) domain, but not any nuclear localization signal (NLS) domain. To understand the functions of NES in transposon activity, we have conducted two experim...

Leaf senescence (LS) affects tree fitness, species distribution and ecosystem structure and functioning. The drivers of LS and the processes underlying it have been studied, but the studies have mainly focused on environmental cues and have mainly been based on statistical analyses using in situ data sets. Experimental investigation and field verif...

Mariner-like elements (MLE) are a super-family of DNA transposons widespread in animal and plant genomes. Based on their transposition characteristics, such as random insertions and high-frequency heterogeneous transpositions, several MLEs have been developed to be used as tools in gene tagging and gene therapy. Two active MLEs, Ppmar1 and Ppmar2,...

Key message Moderate shading is optimal for the growth of Torreya grandis seedlings during drought. Abstract Light and water are two important environmental factors affecting tree seedling traits and regulating seedling survival and growth, but the effects of light on seedlings under drought remain poorly understood. The purpose of the present stu...

BACKGROUND Torreya grandis, a large evergreen coniferous tree with oil‐rich nuts, undergoes a crucial ripening stage after harvest that results in oil accumulation, finally giving rise to the nut that is edible in roasted form. To understand lipid metabolism in T. grandis nuts during the post‐harvest ripening period, the effects of low temperature...

In boreal and temperate trees, air temperature is a major environmental factor regulating the timing of spring phenological events, such as vegetative bud burst, through underlying physiological processes. This has been established by experimental research, and mathematical process-based tree phenology models have been developed based on the result...

Contrary to the generally advanced spring leaf unfolding under global warming, the effects of the climate warming on autumn leaf senescence are highly variable with advanced, delayed, and unchanged patterns being all reported. Using one million records of leaf phenology from four dominant temperate species in Europe, we investigated the temperature...

Frost events during the active growth period of plants can cause extensive frost damage with tremendous economic losses and dramatic ecological consequences. A common assumption is that climate warming may bring along a reduction in the frequency and severity of frost damage to vegetation. On the other hand, it has been argued that rising temperatu...

The occurrence of species-specific phenological timing among populations over broad geographical areas may have converged or diverged with recent climatic warming. The changes in spatial geographical variability of phenological timing may affect the degree of species overlap, and thus have profound ecological consequences in the context of global c...

Climate warming is substantially shifting the leaf phenological events of plants, and thereby impacting on their individual fitness and also on the structure and functioning of ecosystems. Previous studies have largely focused on the climate impact on spring phenology, and to date the processes underlying leaf senescence and their associated enviro...

Key message Transposable elements are abundant in the promoter regions of moso bamboo genome and influence the expression of downstream genes. Abstract As important components of animal and plant genomes, transposable elements (TEs) can shape host genomes and regulate gene expression. In the present study, TEs distributed in the promoter regions o...

Under current global warming, high‐elevation regions are expected to experience faster warming than low‐elevation regions. However, due to the lack of studies based on long‐term large‐scale data, the relationship between tree spring phenology and the elevation‐dependent warming is unclear. Using 652k records of leaf unfolding of five temperate tree...

Background: In tundra ecosystems, the adjustment of phenological events, such as bud burst, to snowmelt timing is crucial to the climatic adaptation of plants. Natural small-scale variations in microclimate potentially enable plant populations to persist in a changing climate. Aims: To assess how plant phenology responds to natural differences in s...

Seed oil content is an important trait of nut seeds, and it is affected by the import of carbon from photosynthetic sources. Although green leaves are the main photosynthetic organs, seed sarcotesta photosynthesis also supplies assimilates to seed development. Understanding the relationship between seed photosynthesis and seed development has theor...

The standard gas chromatogram of the main fatty acids in seeds of Torreya grandis cv. “Merrillii.”

Light responses of net photosynthesis Pn in seeds of Torreya grandis cv. “Merrillii” during seed development; expressed on surface area (A), dry weight (B), and single seed (C) basis. For the Pn values mean ± SD is indicated. Different letters denote significant differences at P ≤ 0.05 level. n = 4. The light responses were measured on eight dates...

The inhibitive effect of different concentrations of DCMU on the ETR of seed in comparison with the control.

Transposable elements (transposons) are fragments of DNA sequences which can move within host genome. Miniature inverted-repeat transposable elements (MITEs) are widespread and high-copy transposable elements in eukaryotic genomes. Tourist-like MITEs are especially abundant in plant kingdom. Earlier genome-wide analysis has shown that MITEs are wid...

Atmospheric nitrogen (N) deposition can increase the susceptibility of vascular plants to other stresses, but the physiological basis of such a response remains poorly understood. This study was designed to clarify the physiological mechanisms and to evaluate bioindicators of N deposition impact on vascular plants. We evaluate multiple physiologica...

Due to infrequent sexual reproduction, moso bamboo breeding by hybridization is extremely technically difficult. Insertional mutagenesis based on endogenous active transposons may thus serve as an alternative method to create new germplasm of moso bamboo. In the present study, using LTR-STRUC, a full-length intact long terminal repeat (LTR) retrotr...

Many different cultivars or forms with diverse phenotypes of moso bamboo have been produced during its long cultivation history. The diverse phenotypes of moso bamboo are mainly reversible and unpredictable during cultivation, which lead to the hypothesis of their epigenetic origin. Earlier studies have shown that transposable elements might be inv...

Torreya grandis, an economically important nut tree in Southeast China, is being subjected to increasing atmospheric nitrogen (N) deposition, and thus far its impact on nut quality remains unknown. Also, studies evaluating nut quality response to biochar application (commonly used as soil amendment) to soils under N deposition conditions are rare....

The hypothetico-deductive modelling framework introduced in Chap. 2 is applied to modelling the annual cycle of frost hardiness in boreal and temperate trees. The concept of frost hardiness is straightforward as such, denoting the threshold temperature that distinguishes between the damaging low-temperature range and the undamaging one. In practice...

The hypothetico-deductive modelling framework introduced in Chap. 2 is applied to the modelling of the annual phenological cycle of boreal and temperate trees. The ecophysiological models of the annual phenological cycle predict the timing of discontinuous developmental events, such as bud burst and height growth cessation. With such events only on...

The hypothetico-deductive modelling framework introduced in Chap. 2 is applied to examining the evolutionary aspects of the annual cycle in boreal and temperate trees. For use of growth resources and competition (capacity adaptation), early onset and late cessation of growth are selected for. However, due to the risk of spring and autumn frost dama...

Upscaling of the models of the annual cycle of boreal and temperate trees to higher levels of organisation is briefly discussed. The models of the annual phenological cycle (Chap. 3), the annual cycle of photosynthesis in evergreen conifers (Chap. 4), and the annual cycle of frost hardiness (Chap. 5) address the modelled phenomena at the level of i...

The hypothetico-deductive modelling framework introduced in Chap. 2 is applied to examining the effects of climatic change on the annual cycle of boreal and temperate trees. Most emphasis is devoted to the paradoxical hypothesis that climatic warming will increase the incidence of frost damage in these trees. According to early computer simulations...

A hypothetico-deductive framework for dynamic ecophysiological modelling of the annual cycle of boreal and temperate trees is described and discussed. In the framework used, the modelling is closely associated with experimental and observational empirical studies, so that inductive (‘empirical’) and deductive (‘theoretical’) phases alternate in the...

Boreal and temperate trees grow under climatic conditions in which the ambient air temperature displays pronounced seasonal variation. Unlike herbs and grasses, trees overwinter without a sheltering snow cover, so that they are exposed to all the harsh climatic conditions. That is why their climatic adaptation is based on their annual cycle of deve...

The hypothetico-deductive modelling framework introduced in Chap. 2 is applied to modelling the annual cycle of photosynthesis in boreal and temperate evergreen conifers. The main emphasis is in the photosynthetic capacity of the needles, i.e., their inherent photosynthesis potential, which is an emergent manifestation of the physiological status o...

The effect of cutting the root connection by detaching the shoot from the root system on dormancy release and vegetative bud burst was examined in 2-year-old seedlings of Norway spruce (Picea abies [L.] Karst.). Seedlings were transferred at 1–4 week intervals between October and January from outdoor conditions to experimental forcing in a heated g...

This book provides an overview of how boreal and temperate tree species have adapted their annual development cycle to the seasonally varying climatic conditions. Therefore, the frost hardy dormant phase, and the susceptible growth phase, are synchronized with the seasonality of the climate. The volume discusses the annual cycle, including various...

Potential for evolutionary responses to climate change - Evidence from tree populations

The perennial herbaceous plant Fragaria vesca produces summer leaves that are shed in autumn and new overwintering leaves in autumn. The aim of this study was to identify the morphological and physiological differences between the two sets of leaves to examine the adaptation of this species to a cold seasonal climate. The winter and summer leaves o...

Snow is known to have a major impact on vegetation in arctic ecosystems, but little is known about how snow affects plants in boreal forests, where the snowpack is uneven due to canopy impact. The responses of two dwarf shrubs, the evergreen Vaccinium vitis-idaea and the deciduous V. myrtillus, to snow conditions were studied in a snow manipulation...

Recent studies have revealed large unexplained variation in heat requirement-based phenology models, resulting in large uncertainty when predicting ecosystem carbon and water balance responses to climate variability. Improving our understanding of the heat requirement for spring phenology is thus urgently needed. In this study, we estimated the spe...

The study addressed the effect of year-to-year variation in air temperature on the early needle frost hardening of first-year Scots pine (Pinus sylvestris L.) seedlings in autumn. To this end a novel method, combining biometeorological and plant ecophysiologal research, was introduced. In the biometeorological part, climatic year-to-year variation...

Evolutionary responses are required for tree populations to be able to track climate change. Results of two hundred years of common garden experiments show that most forest trees have evolved local adaptation, as evidenced by the adaptive differentiation of populations in quantitative traits, reflecting environmental conditions of population origin...

Cells are the basic functional units in forest ecosystems. Plants have strong cell wall, formed by cellulose and lignin. Cell membrane isolates the cell from its surroundings, starch acts as storage and enzymes enable synthesis of new compounds. Membrane pumps allow penetration of cell membrane and pigments capture of light energy. We call enzymes,...

Vegis has put forward the theory that the range of growth-promoting temperatures changes during the induction and the release of dormancy. We have tested the response of buds of Betula pubescens Ehrh. and B. pendula Roth. on temperature during the induction and release of dormancy. Betula seedlings were exposed to dormancy-inducing high-temperature...

The overwintering conditions of northern plants are expected to change substantially due to global warming. For perennial plants, winter warming may increase the risk of frost damage if the plants start dehardening prematurely. On the other hand, evergreen plants may remain photosynthetically active and thereby benefit from milder winters. The posi...

Recent studies suggest that evergreen plants may maintain their photosynthetic capacity through the winter. Since mild winters are predicted to be more frequent in the future, the metabolic activity of plants is also likely to increase. The aim of the present study was to assess how various environmental factors, such as temperature, photoperiod an...

Climate warming has increased researchers' interest in plant phenology and its modelling. Although the main focus is on projections of accelerated springtime phenological events, also a further extension of the growing season by delayed growth cessation is often projected. However, ecophysiological studies indicate that, for boreal and temperate tr...

Preliminary data concerning rest break of buds of 2-year-old seedlings of Pinussylvestris L. and Piceaabies (L.) Karst suggested that (i) an ambient, temperature of 12 °C has a slight rest breaking effect, and (ii) the ability of the rest breaking mechanism to respond to 12 °C is gradually lost when the seedlings are first chilled near 0 °C. This c...

A hypothesis concerning a dynamic temperature response of rate of rest break was tested using a chilling experiment with three northern provenances of 2-year-old seedlings of Norway spruce (Piceaabies (L.) Karst.). According to the hypothesis, (i) within-population variation exists in the higher threshold for the rest-breaking temperature range and...

A framework is presented for modelling bud burst phenology of trees from the cool and temperate regions. Three ecophysiological aspects affecting the timing of bud burst are considered: (i) effects of environmental factors on the rest status of the bud, (ii) effect of rest status on the ability for bud burst, and (iii) direct effect of air temperat...

We investigated sex-related morphological and physiological responses to enhanced UV-B radiation in the dioecious species Populus cathayana Rehd. Cuttings were subjected to two UV-B radiation regimes: ambient (4.5 kJ m⁻² day⁻¹) and enhanced (12.5 kJ m⁻² day⁻¹) biologically effective UV-B radiation for one growing season. Enhanced UV-B radiation was...

Background: The dwarf shrub Vaccinium vitis-idaea has been found to retain its photosynthetic capacity under snow in winter. At snowmelt, the plants are exposed to low temperatures and full light, which may lead to the inhibition of photosynthesis.Aims: To examine the changes in the photosynthesis of V. vitis-idaea at snowmelt and to determine thei...

Seloste artikkelista: Hanninen, H., Luoranen, J., Rikala, R. and Smolander, H. 2009. Late termination of freezer storage increases the risk of autumn frost damage to Norway spruce seedlings. Silva Fennica 43 (5) : 817–830.

Climate change affects both the annual cycle of tree development and the processes related to tree growth. The annual cycle of development manifests as observable phenological events such as leaf unfolding, flowering and leaf fall, but also includes less apparent traits, such as changes in frost hardiness and photosynthetic capacity. Seasonality in...

Automatic continuous monitoring of shoot-level gas exchange and environmental factors in natural conditions provides an efficient but unexploited tool for testing the predictive power of plant photosynthesis models. We used automatically operated measurement chambers to monitor the CO2 exchange of Scots pine (Pinus sylvestris) shoots in Finnish Lap...

Over the last few years it has become increasingly common in artificial forest regeneration to extend the planting period by using freezer-stored seedlings for early summer plantings. Developmentally, however, planted freezer-stored seedlings lag behind seedlings planted earlier in the spring. As freezer-stored seedlings also start hardening later,...

The seasonal changes in two of the photosynthetic parameters of Scots pine (Pinus sylvestris L.), i.e. the light-saturated assimilation rate (Amax) and the apparent quantum yield (α), were compared with the cold hardiness of needles throughout the course of a year. The data for the comparison were obtained from an experiment with close to ambient a...

Bud dormancy in woody plants is released by long-term exposure to non-freezing chilling temperatures, whereas freezing temperatures have been considered to have little or no effect. However, the present results demonstrate that short-term exposure to freezing can release bud dormancy in Betula pubescens (Ehrh.) and B. pendula (Roth). Short-term fre...

Pedunculate oak (Quercus robur L.) grows on the border of its northernmost distribution range in southern Finland. We hypothesised that insufficient cold hardiness (CH) during autumn is a key factor that restricts the northward growth of oak. We tested this hypothesis by monitoring the cold acclimation of oak seedlings growing in central Finland, 3...

The ability to retain their photosynthetic capacity through the winter may be important for plants in boreal conditions, where the growing season is relatively short and winter temperatures fluctuate from severe freezing up to near 0C. The snow cover is an important protector for field-layer plants against both extreme freezing and excessive light,...

In earlier studies the seasonal dynamics of photosynthetic capacity in northern conifers has been explained as a slow response to the ambient temperature. We tested this concept with Scots pine (Pinus sylvestris L.). We analysed the seasonal dynamics of photosynthetic efficiency in Scots pine at the timberline in Finnish Lapland, and in a southern...

Ecophysiological models predicting timing of bud burst were tested with data gathered from 40-year-old Norway spruce (Picea abies (L.) Karst.) trees growing in northern Sweden in whole-tree chambers under climatic conditions predicted to prevail in 2100. Norway spruce trees, with heights between 5 and 7 m, were enclosed in individual chambers that...

Models of the annual development cycle of trees in boreal and temperate regions were reviewed and classified on the basis of their ecophysiological assumptions. In our classification we discern two main categories of tree development: 1) fixed sequence development, which refers to irreversible ontogenetic development leading to visible phenological...