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Tree Vitality and Forest Health: Can Tree-Ring Stable Isotopes Be Used as Indicators?

Tree Vitality and Forest Health: Can Tree-Ring Stable Isotopes Be Used as Indicators? Purpose of Review Society is concerned about the long-term condition of the forests. Although a clear definition of forest health is still missing, to evaluate forest health, monitoring efforts in the past 40 years have concentrated on the assessment of tree vitality, trying to estimate tree photosynthesis rates and productivity. Used in monitoring forest decline in Central Europe since the 1980s, crown foliage transparency has been commonly believed to be the best indicator of tree condition in relation to air pollution, although annual variations appear more closely related to water stress. Although crown transparency is not a good indicator of tree photosynthesis rates, defoliation is still one of the most used indicators of tree vitality. Tree rings have been often used as indicators of past productivity. However, long-term tree growth trends are difficult to interpret because of sampling bias, and ring width patterns do not provide any information about tree physiological processes. Recent Findings In the past two decades, tree-ring stable isotopes have been used not only to reconstruct the impact of past climatic events, such as drought, but also in the study of forest decline induced by air pollution episodes, and other natural disturbances and environmental stress, such as pest outbreaks and wildfires. They have proven to be useful tools for understand- ing physiological processes and tree response to such stress factors. Summary Tree-ring stable isotopes integrate crown transpiration rates and photosynthesis rates and may enhance our under- standing of tree vitality. They are promising indicators of tree vitality. We call for the use of tree-ring stable isotopes in future monitoring programmes. . . . . . Keywords Dendroecology Forest health Forest decline Tree vitality Tree rings Stable isotopes Introduction This article is part of the Topical Collection on Physiological Processes Scientific Hypothesis and Rationale * Paolo Cherubini paolo.cherubini@wsl.ch Despite the efforts to monitor forest health that have been ongoing for almost 50 years, there is still no clear and univer- Giovanna Battipaglia giovanna.battipaglia@unicampania.it sally agreed concept of the vitality of individual trees or the broader concept of forest health. The reason for this lack of John L. Innes definition is the poor understanding of the physiological john.innes@ubc.ca mechanisms underlying tree mortality and forest dieback ep- WSL, Swiss Federal Institute for Forest, Snow and Landscape, isodes. Recently, there has been some level of agreement that Zürcherstrasse 111, CH-8903 Birmensdorf, Switzerland tree mortality processes involve the storage and transport sys- Department of Forest and Conservation Sciences, Faculty of tems of water and photosynthate. Extreme drought events in- Forestry, University of British Columbia, Vancouver, BC V6T 1Z4, duce runaway xylem embolism and eventually the loss of Canada xylem hydraulic conductivity, causing tree death. Department of Environmental, Biological and Pharmaceutical Stable isotope analysis of tree rings provides a powerful Sciences and Technologies, University of Campania “L. Vanvitelli”, method to assess physiological processes in trees retrospec- Via Vivaldi 43, I-81100 Caserta, Italy tively and to understand the role played by drought in forest Departme nt of Forest Resources Management, Faculty of Forestry, decline episodes. We postulate that the recent forest dieback University of British Columbia, Vancouver, BC V6T 1Z4, Canada 70 Curr Forestry Rep (2021) 7:69–80 episodes that have been observed were induced by drought. cause of the decline remains unclear [4], although droughts We further propose that some of the episodes of mortality and seem to have at least triggered some of the declines in health. dieback observed during the 1970s and 1980s were also In Central Europe, particularly in German-speaking countries caused by drought. If this is the case, then stable isotopes, where forests are considered a symbolic part of the cultural which integrate information about stomatal activity and pho- identity [5], citizens were shocked and in some cases there tosynthesis, should be a much better indicator of tree vitality was even panic, incited by environmentalist movements sup- than more commonly used indicators such as tree-ring width ported by poor or nonexistent science. Governments were and crown transparency. induced to adopt measures to reduce pollution emissions and to invest public money in forest health research and monitor- Forest Health ing programmes. Questions about the causes of the decline have never really been resolved and remain controversial Forests are important to society because they provide multiple [6], although it is notable that the symptoms that were ob- goods and services, including the maintenance of biodiversity, served in the late 1970s (foliage reductions and discoloration) production of timber, protection against natural hazards, and after the severe drought of 1976 were again repeated follow- provision of cultural and recreational benefits. Poor forest ing droughts in the 1990s and 2000s [7]. Nonetheless, emis- health is associated with the loss of some of these goods and sions, particularly of sulfurs and heavy metals, dropped sig- services. As a result, society is increasingly concerned about nificantly over the past 30 years as a result of the Waldsterben the long-term condition of the forests. Questions about the fear. At the same time, air quality improved, as did our under- state of the forests often arise when and where there are no standing of forest ecology and ecosystem processes. Ongoing other major upheavals and woes, such as wars, famines, waves research associated with the ensuing monitoring efforts has of poverty, or pandemics. The importance of healthy forests shown how complex ecosystem processes are [8] and how typically becomes a topic of discussion when natural hazards difficult it is to define forest health, which we need to do if such as wildfires, avalanches, and landslides occur, or when we want to be able to assess it [9]. dramatic forest declines are observed. In such cases, it be- Defining forest health is as difficult as defining the health comes clear how important it is to be able to assess forest of human populations. What indicators should be used to as- health, as well as how deep our ignorance is of baseline sess the health of a forest stand? Amongst the different possi- conditions. ble indicators, which are most meaningful? Is it the mean, or Scientists, when asked about the state of the forests, often perhaps the median, tree life expectancy? And, if it is, how can provide controversial answers, evidence that a clear consen- we know how life expectancy compares to life expectancy in sual definition of forest health is still missing. When forest the past? How should we assess the health of trees that are attacked by non-lethal fungal pathologies and other diseases declines occur, forest health becomes a matter of public debate and political discussion, with news cycles strongly influencing and pests? And what mortality rates characterize a healthy public opinion. Depending on what else is in the headlines, forest versus a declining one? It is evident that in order to small events may garner much attention, whereas larger, more answer all these questions, a definition of forest health is nec- diffuse events may occur without even a passing mention. As essary. However, as noted 15 years ago [10], a clear definition a result, many people lack not only a baseline understanding of forest health has been lacking. Our literature search showed of forest health but also the ability to gauge the relative sever- that the development of a concept of forest health has been ity of any particular event. A lack of knowledge tends to make completely neglected for the past twenty years; indeed, no people more inclined to trust “experts”, particularly those who notable advances have been made at all in this regard. offer reassuring theories. Studies of forest health have been limited to the assessment Waldsterben, the forest decline that occurred in Central of the condition of single forest stands, mainly those declining Europe during the last century, is a good example of sudden, as a result of drought [11]. And again, a considered commu- uninformed public interest in forest health. In the 1970s, a nication between science and society has been lacking. decline in silver fir (Abies alba Mill.) stands was observed in Announcements of global forest health decline have appeared Germany, the so-called Tannensterben or fir dieback [1]. in scientific journals and been broadcast by mass media, caus- Some of the declines were localised around point sources of ing significant public concern. However, a meaningful defini- air pollution, such as in the Black Triangle, i.e., at the borders tion of forest health is still missing, making it difficult for between Germany, the Czech Republic, and Poland, and were anyone, expert or lay, to gauge the relative severity of the evidently caused by local emissions of pollutants [2]. Later, reported declines and respond accordingly. when a more diffuse and widespread decline of other tree Although it may be questioned whether a universal defini- species was observed in European forests (called tion of forest health is even possible, it seems unreasonable to Waldsterben or forest dieback [3]), mass media jumped on base this only on the observations of the appearance of trees. the news and provoked significant alarm. To this day, the This is a legacy of the past emphasis on production forestry, Curr Forestry Rep (2021) 7:69–80 71 where unhealthy trees were seen as a potential loss of stand clear border between life and death for trees. For example, is a yield. Today, with multi-objective forestry, the presence of tree dead as soon as it is felled, even if the crown foliage is still dead and dying trees is seen as an essential part of the main- green and actively photosynthesising? Many trees can be tenance of biodiversity. Trees and forest stands are only a part grown from cuttings, so clearly a shoot can survive been ex- of the much larger ecosystem, and their interactions with the cised from a tree, at least for a short time. Are cambial cells other components of the ecosystem have to be considered. In dead if they are still being fed carbohydrates by the foliage? Or Central European forest ecosystems, for example, forest con- is a stump dead if it is still growing thanks to carbohydrates dition is influenced by soil acidification, extreme climatic provided by neighbouring trees through root anastomoses? events such as drought or frost, pest outbreaks, interactions The stumps of many broad-leaved trees can resprout, so clear- between primary, secondary, and saprophytic fungal diseases, ly they are not dead. Our understanding of tree-longevity and many other factors. The complex synergies amongst all mechanisms [16] and prior-to-death physiological processes these factors determine tree death and forest stand dieback. is still poor. Tree senescence, including the role of telomeres This is why atmospheric, soil, and hydrological processes in ageing processes [17], is still not fully understood [18� ]. should all be taken into consideration when assessing forest In conclusion, although tree death processes are not yet health [12, 13]. However, a distinction between the various fully understood, tree mortality rates may be used as indicators factors leading to forest decline is seldom made in the public of tree vitality within a forest stand. However, although discourse [14, 15� ]. Once again, the discussion is misleading counting dead trees in a forest is certainly feasible, analysing and public opinion confounded. and interpreting tree mortality rates are difficult [19–21]. Tree mortality rates in natural conditions are completely unknown, Tree Health, Condition, and Vitality and they vary strongly depending on species and site condi- tions. Moreover, data about mortality rates in the past are not Tree vitality is one of the most important indicators of forest available and are difficult to estimate due to logging and the condition. Tree vitality, or tree condition, describes the gener- removal of deadwood by humans. Even in unmanaged forests, al outer appearance of an individual tree. In contrast, tree it may be difficult to determine when any dead trees actually health reflects the pathological state of a tree [9]. As vitality died, making calculation of mortality rates extremely difficult. cannot be measured directly, various indicators can be used to Large (50 ha), long-term monitoring plots where every tree is describe it. If tree vitality is used as an indicator of forest tagged and repeatedly assessed are beginning to shed light on condition during forest surveys, it is clear that field-practical, this important question, and the information will steadily im- low-cost methods are needed. Although vitality is a theoretical prove as long as the monitoring is maintained [22]. Without a concept and defined differently in a range of studies, it always comparison in space or time, tree mortality rates are difficult to interpret as indicators of forest health. includes the power to live, grow, and develop [10]. Therefore, indicators of tree life, growth, and development have to be used. Here, we review the literature dealing with indicators Tree Physiological Processes of tree health, together with their main advantages and limitations. Tree vitality includes the power of the tree to live and grow. Photosynthesis, which is the process by which trees synthesize carbohydrates from carbon dioxide and water using sun ener- Indicators for Assessing Tree and Forest gy, is theoretically the most appropriate indicator of tree pro- Vitality ductivity and vitality. However, data on photosynthesis rates require precision measurements and expensive equipment that Tree Death and Mortality Rates are difficult to use in the forest. As a result, photosynthesis is seldom considered in long-term forest monitoring Like all living organisms, trees die. Tree death is the ultimate programmes. Likewise, other indicators of tree biochemical indicator of zero tree vitality. Because the definition of tree and physiological processes, such as phytohormones or en- vitality includes the capacity of a tree to live, one good indi- zymes, luminescence, needle emissions, cambial electrical re- cator of tree vitality is tree survival after stress. Predisposing, sistance, and electronic potential [23] cannotbeconsideredin inciting, and contributing stress factors lead to tree decline. forest surveys because of the costs involved in their analysis During or after stress, the tree reacts immediately, then usually and the practical difficulties encountered when trying to take recovers. Trees usually reallocate carbon to overcome stress; measurements in the forest. if stress continues, the ability of a tree to overcome stress Data acquisition of physiological processes using remote diminishes until tree death occurs. sensing techniques can cost less than data acquired during However, at what point is a tree actually dead, and how ground-based fieldwork. However, fieldwork is essential for does one know? As with humans, it can be difficult to define a ground validation of remote sensing data and is indispensable 72 Curr Forestry Rep (2021) 7:69–80 when indicators cannot be observed through remote sensing once they are exposed to more light. Moreover, trees may technology within an acceptable range of accuracy. As a con- enhance their growth in response to disruptions in the forest sequence, forest health assessments are commonly undertaken ecosystem cycle, such as increased nitrogen availability in- by relating field observations (e.g., defoliation or discolor- duced by atmospheric deposition. Even if such trees are eval- ation) to remotely sensed measures. uated as being in good health, their growth rates are not good Remote sensing techniques for monitoring forest health indicators of the overall health of the forest. Nonetheless, tree include airborne imaging spectroscopy to derive vegetation productivity is commonly used as an indicator of tree health in indices, airborne laser scanning penetration variables, and surveys performed throughout the world, especially within the spectral mixture analysis [24, 25]. The most important photo- context of production forestry. synthesis indicator used in the assessment of tree vitality is To assess tree productivity, the carbohydrates being pro- chlorophyll fluorescence, which is assessed using spectrome- duced, i.e., the carbon fixed through photosynthesis, should be try [26]. Chlorophyll fluorescence is useful for assessing the measured. As it is difficult to measure carbohydrate produc- overall ability of trees to produce carbohydrates and has also tion in the field, tree biomass, as derived from tree volume, is been suggested as a way to diagnose plant stress caused by used. Thus, tree volume is often taken as an indicator of tree environmental factors [27]. However, this method has been vitality. However, tree volume itself is difficult to assess, as it more widely applied in urban tree-monitoring programmes includes foliage, branches, and roots. Indeed, the root system than in forest health surveys. is thought to be of considerable volume, but is almost impos- In conclusion, remote sensing can be used to assess tree sible to measure. Even if the root system were to be extracted vitality, but the data obtained through remote sensing must be from the soil, the volume would be underestimated, as it validated with ground data. It is perhaps for this reason that would exclude the fine roots, which seem to be a conspicuous remote sensing has seldom been used in forest surveys to part of the root system. For this reason, tree stem volume alone assess vitality. However, recent advances in remote sensing is used to assess tree productivity and therefore vitality. make the development of methods to assess photosynthetic Tree stem volume should be measured using Archimedes’ rates easier and more promising for forest-scale studies [28]. principle, but because this is impractical in a forest setting, it is usually calculated from basal area and tree height. The tree Crown Transparency taper, i.e., the degree to which a tree stem decreases in diam- eter as a function of height above ground, should be taken into Since the first observations of forest decline during the 1970s account. In practice, stem volume is calculated from measure- in Central Europe, crown foliage transparency has been com- ments of tree diameter at breast height (1.3 m height) and monly believed to be the best indicator of tree condition in overall tree height. A good example of assessing tree productivity, i.e., car- relation to air pollution. For this reason, it has been widely adopted as the most important indicator of tree vitality. bon (C) content, is offered by Bascietto et al. [34]. The re- Although crown transparency assessment has been criticized sults of their study showed that ring width and stem analyses vehemently because it is highly subjective and not cause- maybe usedtoreconstruct treestem volumeandcarbon specific [29], European forest health has been assessed for production. the past 30 years using this indicator [12]. This wealth of data Tree productivity, biomass, and volume are certainly indi- has shown that most of the variability associated with crown cators of tree growth, but they are difficult and time- transparency assessments is the result of methodological dif- consuming to estimate, and strongly affected by errors and ferences, differences in tree age, and some climatic factors, approximations. mainly drought [30], rather than air pollution [8]. Crown transparency is therefore not a good indicator of tree vitality, although it continues to be recommended as an indicator when Basal Area Increment used in association with other indices of crown condition [31–33]. Basal area increment may be used as a proxy for volume [35]. The advantage of using basal area instead of ring width is that Tree Productivity, Biomass, and Volume no data standardization is needed to remove the geometrical age trend, i.e., the decreasing trend in ring width due to the Tree productivity is often considered to be an expression of increasing stem circumference with tree age, preserving all tree vitality. However, its use is questionable because the most other long-term trends [36]. To obtain accurate results, stem productive trees are not always in good health. For example, disks are needed because extrapolating basal area increment tree growth may increase as a reaction to fungal attacks or using tree cores often introduces mistakes that compromise injury. Trees may also grow very slowly in the shade of other the results. However, the use of stem disks requires that the trees for hundreds of years, only becoming truly productive tree be felled. Curr Forestry Rep (2021) 7:69–80 73 Tree-Ring Growth although recent studies have shown that different sampling strategies achieve different results [46]. Given the difficulties in calculating tree stem volume, and the The weakness of ring width as an indicator is also shown uncertainty of tree volume estimates, tree-ring measurements by tree-ring studies of trees grouped into vitality classes to test have often been preferred to stem volume assessments in for- growth differences between the classes [47]. While many of est health surveys. Particularly when assessing forest health these studies show decreased growth and higher crown trans- over large areas, dendrochronological studies provide infor- parency, others show no such relation [48], or no relationship mation about the growth of a large number of trees without the at low to moderate levels of transparency [49]. Although it has need to fell them. Tree-ring studies also allow for the recon- been demonstrated that crown transparency correlates with struction of past tree growth over time. Therefore, tree-ring subsequent tree mortality in some cases [50], an unambiguous width, as an indicator of tree volume growth, is a widely used relationship between crown transparency and tree growth can- indicator of tree vitality. not be demonstrated. Similarly, attempts to relate the results In temperate climates, the cambial activity of trees and obtained from dendrometer bands to crown transparency have shrubs stops during the cold season, resulting in the formation yielded few significant relationships. of annual growth rings. Tree rings have been used for In conclusion, tree-ring widths have frequently been used reconstructing past climatic conditions and events. More as indicators of tree vitality in forest stands suffering environ- broadly, tree rings can be used as indicators of the environ- mental stress. However, the majority of such studies are af- mental conditions (not only climatic) in which trees have been fected by potential sampling bias, and by uncertainty related to growing because their chemical and physical characteristics whether growth changes are the result of stand dynamics or an depend on the environmental conditions in which they grew. independent change in tree vitality. Tree-ring analysis has contributed significantly to the discus- sion about the impact of environmental changes on tree growth and tree vitality. However, many different factors Tree-Ring Stable Isotopes as Integrative can have the same effect on tree growth, making it difficult Physiological Indicators of Tree Vitality to disentangle the effects of different factors. In studies of the impact of air pollution on forests, Tree-Ring Stable Isotopes dendroecological methods have been used to identify anoma- lous growth trends. However, unlike the effects of point Stable isotopes are important tools for evaluating the impact of sources [37], the large-scale diffuse impacts of air pollution biotic (e.g., pest outbreaks and fungal diseases) and abiotic on forests are still unclear [4, 38]. In Central Europe, for ex- (e.g., extreme climatic events, fire, air pollution, direct dam- ample, abrupt growth decreases were detected during the age due to management operations) factors on forest health 1980s [39, 40]. Some pioneering studies around pollution and vitality. If the stress conditions are not so harsh as to point sources, such as smelters, have documented a decrease prevent tree growth, i.e., allowing tree-ring formation, tree- in tree growth as a consequence of water, air, and soil pollut- ring stable isotopes can be used to assess retrospectively the ants [41]. Studies of the impact of air pollution at a regional impact of environmental disturbances on tree vitality. scalehavebeenmorecontroversial[42]. Stand dynamics However, it is extremely difficult to disentangle the role of seem to have strongly affected the results of many of these the different disturbances in forest decline episodes [51, 52]. studies [43]. Tree-ring studies provide information about past growth Carbon Stable Isotopes rates, but the interpretation of long-term growth trends is dif- ficult. Many dendroecological studies of long-term growth Tree-ring carbon stable isotope ratios (δ C) are powerful trends are affected by sampling bias because of the influence proxies used in climate reconstructions [53] and are increas- of stand dynamics (e.g., mortality, competition, disturbance). ingly used to help unravel tree physiological processes [54]. In particular, the restriction of sampling to a few of the largest- Tree-ring carbon stable isotope ratios can be considered an diameter trees within a stand may have a marked influence on integrated indicator of tree vitality over time. Plants discrimi- the ensuing results [44]. When assessing long-term growth nate against the heavier carbon isotope C; as a result, plant trends, most investigators sample the largest-diameter trees material is depleted in C relative to air CO . A negative sign 13 12 in a stand. This strategy has arisen from the desire to sample indicates that the plant sample has a lower C/ C ratio than the oldest trees in a stand, which are often incorrectly assumed the standard (PDB), and a lower discrimination is indicated by to be the largest. However, tree-ring patterns and the sizes of a higher, i.e., less negative, δ C. In C plants, the discrimina- trees are strongly affected by forest management and natural tion is driven by two fractionation processes: (a) diffusion of disturbances [45]. The effects of restricting sampling to the CO through stomata, reducing δ C by 4.4‰, and (b) the largest trees have never been adequately documented, enzymatic process of carboxylation, which further reduces 74 Curr Forestry Rep (2021) 7:69–80 13 13 13 δ Cby 27‰. The carbon isotope ratio (δ C) is therefore δ C, but is unaffected by changes in net photosynthetic ac- affected by both changes in atmospheric CO concentrations tivity (A) [65]. (c ) and by changes in the substomatic chamber or intercellu- lar (c)CO concentrations. The CO input rate (g ) of the Using Carbon and Oxygen Stable Isotopes to Study i 2 2 s substomatic chamber is regulated by the stomata; the output Air Pollution rate is regulated by CO assimilation (A). These processes are strongly influenced by environmental variables such as light, Variations in atmospheric gas concentrations, such as the in- temperature, and water and nutrient availability, which are creases in CO concentrations, air pollution, and acidic pre- then reflected in tree-ring stable isotopes [55]. cipitation due to fossil fuel combustion, affect forest ecosys- In general, C discrimination declines under stress condi- tems at individual tree and canopy levels. Stable isotopes have tions, such as water shortage. This may be attributed to partial largely been applied to assess the physiological mechanisms or complete stomatal closure in the case of water stress, which induced by those factors and to better understand their impli- causes limited diffusion of both CO and H O and thus less cations for the global carbon, water, and nitrogen cycles (see 2 2 carbon isotope discrimination [47]. However, stomatal conduc- Table 1 Supplementary Material). For example, in several tance responds not only to water availability but also to water forests, elevated CO concentrations, temperature, and demand. This means that other variables such as air relative drought increase seem to promote an increase in plant water humidity, vapour pressure deficit, and potential evapotranspira- use efficiency with an enhancement of photosynthesis and a tion also affect discrimination [56]. Furthermore, other stress generally modest reduction in stomatal conductance [66]. The conditions induced by changes in temperature, light, CO con- influence of each factor is still under debate and difficult to centrations, or nutrient availability [57] could influence stoma- disentangle [67]. Tree-ring δ C samples from around the tal conductance and lead to increases in the CO assimilation globe show an increase in WUE since pre-industrial times 2 i rate via Rubisco. This increase leads to a corresponding de- [68, 69]. Exposure to SO and O has been reported to inhibit 2 3 crease in c /c and causes plants to discriminate less against photosynthesis by inducing stomatal closure [70, 71]. i a C. Furthermore, through its relationship with the ratio be- Meanwhile, elevated NO concentrations may increase pho- tween the intercellular and the atmospheric CO partial pres- tosynthetic rates by activating carboxylation enzymes due to sures, tree-ring δ C has been widely used to study intrinsic the “N fertilization effect” during short-term exposure [72]or water use efficiency in plants ( WUE) [55, 58]. in the long-term trend [73]. However, long-term exposure is In tree-ring cellulose, the δ C incorporates additional believed to cause forest decline. The general isotopic response sources of variation unrelated to environmental factors, such to air pollution is a reduced discrimination against Cdue to as fractionation processes taking place during the mobilization stomatal closure, which creates higher δ C values in tree of photosynthetic assimilates from the leaf to tree-ring produc- rings and leaf tissues. Such studies reported that the increase tion [59]. For instance, the tree may use remobilized stored in δ C in plant tissues is mainly due to [1]stimulated activ- carbohydrates (primarily starch) for the construction of new ities of PEP carboxylase, [2]change in cell metabolism, [3] wood cells. This is the so-called memory effect [60, 61]. As a decline in carboxylation efficiency due to collapse of meso- consequence, the tree ring might have the signal of the year in phyll cells, or [4] higher rates of dark respiration, with no which the starch was produced, which may differ from the significant changes in the stomata aperture (Table 1 year in which it is incorporated into the tree ring by many Supplementary Material). The majority of the studies around months or even years [62]. point-source pollution under real field conditions showed an increase of tree-ring δ Cvalues [74, 75]. Oxygen Stable Isotopes Using Nitrogen Stable Isotopes to Study Air Pollution Oxygen stable isotopes (δ O) are another important source of environmental information that can be extracted from trees Besides δ C, most of the studies on the effects of air pollution 18 15 [63]. Tree δ O includes three variable components beyond on tree growth and physiology are based on δ N that can source water variability: (1) the leaf water enrichment, modi- provide indications of changes in ecosystem N cycling in re- fied by the Péclet effect and the dampening of δ Oat evap- sponse to the different pollution sources [76]. oration sites due to leaf water heterogeneity, (2) the biochem- Studies of nitrogen stable isotopes in tree rings started some ical fractionation between carbonyl oxygen and water during decades ago. Poulson et al. [76] measurednitrogenisotopesin cellulose synthesis, and (3) the δ O of water vapor outside two individuals of Tsuga canadensis to study the effect of the leaf, mostly influenced by relative humidity [64]. atmospheric N deposition on a forest in NH, USA. Both trees 18 15 Furthermore, tree δ O can be used to discriminate between showed a decreasing trend in δ N from the 1960s to the biochemical and stomatal limitations to photosynthesis, since 1990s and an increasing nitrogen concentration. The authors it shares a dependence on stomatal conductance (g )withplant attributed this result to the increasing emission of NOx in the s Curr Forestry Rep (2021) 7:69–80 75 USA, which leads to increasing atmospheric deposition of infestation of piercing–sucking insects in AZ (USA). A simi- isotopically light nitrate and ammonium in acid rain. The an- lar lack of response was observed by Haavik et al. [84]ina thropogenic impact on natural nitrogen isotope variation was study of growth patterns of Quercus rubra during and after a also studied in a polluted area of Germany by Jung et al. [77]. pest infestation in the late 1990s. The authors found that Pinus sylvestris needles and tree rings In contrast, Simard et al. [85]reported Cenrichment in were more depleted in δ N and had lower N concentrations at Abies balsamea and Picea mariana following defoliation by sites further from the industrial agglomeration. Ammann et al. the spruce budworm Choristoneura fumiferana in boreal for- 115 18 [78]investigated δ Nin Picea abies needles in a forest in the est of Quebec. However, they found no differences in δ O Swiss Central Plateau, near a highway. They found the highest values during and after the outbreak and concluded that the values in plots closest to vehicular traffic and estimated that observed C enrichment could be explained by both an in- vehicular emissions contributed about 25% of the N nutrition crease in photosynthetic rate and the remobilisation of starch of the needles. At the same site, Saurer et al. [75]studied a reserves during severe defoliation. Kress et al. [86]inferred transect of Picea abies perpendicular to the highway, to deter- that larch budmoth (LBM) did not impact the carbon and mine the effect of NOx from car exhaust on tree growth. They oxygen tree-ring isotope signatures of Larix decidua trees on found that the trees growing nearest the highway exhibited a European Alps. Similarly, Weidner et al. [87]observed that disturbance in nitrogen concentration and a dramatic increase the loss of needles due to LBM outbreaks did not significantly in tree-ring δ N signal starting when the highway was built. influence the tree-ring carbon isotope signature. In contrast to This study confirmed that tree rings can be an environmental carbon isotopes, however, they found that oxygen isotopes monitoring tool and that the isotopic signal of N sources can seemed to react much more sensitively to strong LBM infes- be stored in them. However, Battipaglia et al. [79] could not tations. This could be because during the main defoliation find any clear δ N signal in tree rings close to a traffic pol- event, photosynthesis does not take place due to either a lack lution source, showing that radiocarbon is a much better indi- of needles or desiccated or dysfunctional (brown) needles. cator of changes in air quality due to fossil fuel combustion. Accordingly, very few photosynthates are produced. They Burning fossil fuel introduces CO that has no C into the therefore suggested that tree-ring cellulose formed during atmosphere, which influences the global atmospheric LBM outbreak years is built with carbohydrates formed either CO - Csignal,i.e., the Suess effect [80]. Several other pa- before the heavy feeding occurs or shortly thereafter, i.e., 15 18 13 pers have coupled δ N with δ Oand δ C to monitor plant when new foliage emerges 3–4 weeks after defoliation. exposure to elevated oxidant pollutants such as ozone, sulfur Simard et al. [88] (2012) investigated the potential use of dioxide, and NOx using different temporal and spatial per- tree-ring isotope composition to identify different degrees of spectives [81]. However, both the magnitude and the direction past spruce budworm defoliation episodes in seedlings of of the reported isotope effects have varied as a result of the Abies balsamea grown in a controlled experiment. They re- 13 13 opposing effects of fossil fuel CO dilution and the effects of ported an enrichment of C in moderately to heavily secondary combustion products on tree physiology. Thus, it defoliated seedlings, probably due to the remobilization of can be difficult to extract general trends from these data. stored carbohydrates enriched in C. They did not observe any variation in carbon composition in seedlings that experi- Pest Outbreaks enced less severe defoliation. Few studies have examined the effects of insect outbreak Other Disturbances events on tree-ring stable isotope composition, and the results of those that exist are rather controversial. Although it is well Natural forest disturbances, such as fires, windstorms, or known that host plants can change their physiology by altering flooding, are expected to increase in both severity and fre- their water relations and their modifying photosynthate allo- quency under global warming and to seriously affect forest cation and photosynthetic capacity as a consequence of insect health and ecosystem services. Stable isotopes in tree rings defoliation, the isotope signals do not always reveal changes have the potential to provide information about the frequency in discrimination rate. Leavitt and Long [82] compared tree- and severity of extreme events in the past, thereby aiding with ring carbon stable isotopes of two host species (Abies extreme-hazard assessments. concolor and Pseudotsuga menziesii) during a western spruce To aid with the understanding of the physiological responses budworm outbreak in the USA. Although they observed an of trees to wildfire in southern Europe, the dual-isotope ap- 13 13 18 increase in δ C when compared to a non-host species (Pinus proach [89], which combines the analysis of δ Cand δ O, ponderosa), they did not record any change in discrimination has been used to discriminate between biochemical and stoma- in the host species due to the pest outbreak. Likewise, tal limitation to photosynthesis [90–98]. Indeed, fire can dam- Ellsworth et al. [83] did not observe any variation in δ Cor age the crown, reducing leaf surface and altering the plant’s WUE in the leaves remaining on deciduous trees after an photosynthetic rates and, being the plant δ O related to i 76 Curr Forestry Rep (2021) 7:69–80 stomatal conductance (gs) but unaffected by photosynthesis strong coherence amongst species and strong correlations with (A), it can help separate the independent effects of A and gs climatic indices, including growing season, temperature, and on δ C. drought. In particular, stable isotopic ratios can provide infor- Other studies demonstrated physiological consequences of mation about the water use efficiency, i.e., the amount of fire deficits in forests of the western United States [99]and in carbon assimilated as biomass per unit of water used by the trees growing on permafrost in boreal ecosystems [100]. All of tree. A growing body of evidence shows that plants can close these studies demonstrated that the responses of the trees, and their stomata during drought events to avoid unnecessary wa- thus of the stable isotope signature, depend on fire severity. ter loss. Consequently, stomatal conductance to CO de- Severe wildfires that result in partial or complete crown defoli- creases and Rubisco fixes a higher-than-usual proportion of 13 18 13 12 ation lead to a simultaneous enrichment of δ Cand δ Oin Ccompared to C. As a result, rings are formed in which tree rings. This is because trees close their stomata and decrease the cellulose is enriched in the heavier isotope, which trans- their photosynthetic activity [92, 98, 99]. Medium and low lates as less negative isotopic signatures and those large anom- 13 13 severity fires produce little to no change in δ C, no change alies in their δ C can be indicators of forest health [106–109]. in δ O, and a partial reduction in tree growth due to the lower Other studies of co-occurring healthy and dead trees found a photosynthetic capacity of the burned trees [79]. lower WUE in dead trees, suggesting either a reduction in photosynthesis rates or, more probably, a poor regulation of stomatal conductance [110–112]. The higher WUE observed Tree Response to Drought in surviving trees suggests higher photosynthesis rates or more conservative water use strategies during drought [111]. Over the past decades, there has been a worldwide increase in Stable isotopes are a key to understanding physiological reports of drought-related forest declines [11, 101]. The de- processes related to tree vitality, and to understanding how clines are seemingly triggered by multiple, interacting factors, forest declines are linked to drought events. A good example ranging from drought to insect pests and diseases and to af- is given by Gessler et al. [113� ], who developed a conceptual 13 18 forestation with poorly adapted non-native species. This model based on tree-ring δ Cand δ O isotopes. Their model makes it difficult, if not impossible, to disentangle the drivers suggests that when dead trees have long-lasting gas exchange of forest declines. Abiotic stress factors can induce forest and growth declines, in comparison with healthy trees, mor- health problems and extreme climate events, particularly tality is induced principally by carbon starvation, whereas drought, are thought to be a primary factor triggering many rapid or no decline of both stomatal conductance and growth extensive forest pest outbreaks and fungal diseases [102]. prior to death is indicative of hydraulic failure [99]. There are two main physiological processes involved dur- ing tree mortality: Conclusions 1. Hydraulic failure processes, induced by reduced soil wa- ter supply coupled with high evaporative demand. This A clear definition of forest health is still missing and little causes xylem conduits and the rhizosphere to cavitate, progress had been made toward the developing the theoretical stopping the flow of water and desiccating plant tissues framework around the concept of forest health. This lack of [103, 104]. definition is caused by the poor understanding of the physio- 2. Carbon starvation processes, induced by stomatal closure. logical mechanisms underlying tree mortality and forest die- Although designed to prevent water loss, stomatal closure back episodes. To evaluate forest health, monitoring efforts leads to a decrease in carbon uptake and photosynthetic have concentrated on the assessment of tree vitality, trying to activity, which causes the plant to starve as a result of its estimate photosynthesis rates and productivity. In order to continued metabolic demand for carbohydrates. extend such estimates back in time, tree rings have been used as indicators of past productivity. In particular, tree-ring width Researchers have debated the roles of these two co- measurements have been widely used to provide information occurring processes. Adams et al. [105]stated that in most about past climatic events, such as drought and frost, and cases, both processes occur together, even if hydraulic failure trends and the response of trees to them. However, ring width can occur alone without any carbon starvation, whereas car- patterns are prone to misinterpretation and do not provide any bon starvation only occurs in conjunction with hydraulic fail- information about tree physiological processes other than ure. The majority of studies assessing hydraulic failure have those directly related to tree growth. looked at the percentage of loss of xylem conductivity (PLC), In the past two decades, it has become clear that tree mor- while carbon starvation was assessed via changes in tissue tality processes involve the storage and transport systems of non-structural carbohydrate (NSC) concentrations [103]. water and photosynthate. Extreme drought events induce the Some studies of tree-ring stable isotopic composition show a loss of xylem hydraulic conductivity, causing tree death. Tree- Curr Forestry Rep (2021) 7:69–80 77 credit line to the material. If material is not included in the article's ring stable isotopes have been increasingly used in the study Creative Commons licence and your intended use is not permitted by of drought-induced forest decline and have proven to be use- statutory regulation or exceeds the permitted use, you will need to obtain ful tools for understanding physiological processes in the past. permission directly from the copyright holder. To view a copy of this Although they have yet to be used to assess tree vitality rather licence, visit http://creativecommons.org/licenses/by/4.0/. than to study tree response to environmental stress, tree-ring stable isotopes integrate crown transpiration rates and photo- References synthesis rates. When analysed together with ring widths, tree- ring stable isotopes may enhance our understanding of tree Papers of particular interest, published recently, have been vitality. They are promising indicators of tree vitality and also highlighted as: allow for retrospective studies of tree physiological response � Of importance to past abiotic and biotic disturbance events and trends. �� Of major importance Here, we have reviewed the existing literature on forest health and tree vitality indicators. We postulate that the forest 1. Schütt P. Der Stand unseres Wissens über eine aktuelle und gefährliche Komplexkrankheit der Weißtanne (Abies alba Mill.). dieback episodes that have been recently observed were in- Forstw Cbl. 1977;96:177–86. duced by drought. We propose that some of the episodes of 2. Ulrich B, Pankrath J. Effects of accumulation of air pollutants in mortality and dieback observed during the 1970s and 1980s forest ecosystems. Dordrecht: De Reidel Publ. 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Tree Vitality and Forest Health: Can Tree-Ring Stable Isotopes Be Used as Indicators?

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10.1007/s40725-021-00137-8
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Abstract

Purpose of Review Society is concerned about the long-term condition of the forests. Although a clear definition of forest health is still missing, to evaluate forest health, monitoring efforts in the past 40 years have concentrated on the assessment of tree vitality, trying to estimate tree photosynthesis rates and productivity. Used in monitoring forest decline in Central Europe since the 1980s, crown foliage transparency has been commonly believed to be the best indicator of tree condition in relation to air pollution, although annual variations appear more closely related to water stress. Although crown transparency is not a good indicator of tree photosynthesis rates, defoliation is still one of the most used indicators of tree vitality. Tree rings have been often used as indicators of past productivity. However, long-term tree growth trends are difficult to interpret because of sampling bias, and ring width patterns do not provide any information about tree physiological processes. Recent Findings In the past two decades, tree-ring stable isotopes have been used not only to reconstruct the impact of past climatic events, such as drought, but also in the study of forest decline induced by air pollution episodes, and other natural disturbances and environmental stress, such as pest outbreaks and wildfires. They have proven to be useful tools for understand- ing physiological processes and tree response to such stress factors. Summary Tree-ring stable isotopes integrate crown transpiration rates and photosynthesis rates and may enhance our under- standing of tree vitality. They are promising indicators of tree vitality. We call for the use of tree-ring stable isotopes in future monitoring programmes. . . . . . Keywords Dendroecology Forest health Forest decline Tree vitality Tree rings Stable isotopes Introduction This article is part of the Topical Collection on Physiological Processes Scientific Hypothesis and Rationale * Paolo Cherubini paolo.cherubini@wsl.ch Despite the efforts to monitor forest health that have been ongoing for almost 50 years, there is still no clear and univer- Giovanna Battipaglia giovanna.battipaglia@unicampania.it sally agreed concept of the vitality of individual trees or the broader concept of forest health. The reason for this lack of John L. Innes definition is the poor understanding of the physiological john.innes@ubc.ca mechanisms underlying tree mortality and forest dieback ep- WSL, Swiss Federal Institute for Forest, Snow and Landscape, isodes. Recently, there has been some level of agreement that Zürcherstrasse 111, CH-8903 Birmensdorf, Switzerland tree mortality processes involve the storage and transport sys- Department of Forest and Conservation Sciences, Faculty of tems of water and photosynthate. Extreme drought events in- Forestry, University of British Columbia, Vancouver, BC V6T 1Z4, duce runaway xylem embolism and eventually the loss of Canada xylem hydraulic conductivity, causing tree death. Department of Environmental, Biological and Pharmaceutical Stable isotope analysis of tree rings provides a powerful Sciences and Technologies, University of Campania “L. Vanvitelli”, method to assess physiological processes in trees retrospec- Via Vivaldi 43, I-81100 Caserta, Italy tively and to understand the role played by drought in forest Departme nt of Forest Resources Management, Faculty of Forestry, decline episodes. We postulate that the recent forest dieback University of British Columbia, Vancouver, BC V6T 1Z4, Canada 70 Curr Forestry Rep (2021) 7:69–80 episodes that have been observed were induced by drought. cause of the decline remains unclear [4], although droughts We further propose that some of the episodes of mortality and seem to have at least triggered some of the declines in health. dieback observed during the 1970s and 1980s were also In Central Europe, particularly in German-speaking countries caused by drought. If this is the case, then stable isotopes, where forests are considered a symbolic part of the cultural which integrate information about stomatal activity and pho- identity [5], citizens were shocked and in some cases there tosynthesis, should be a much better indicator of tree vitality was even panic, incited by environmentalist movements sup- than more commonly used indicators such as tree-ring width ported by poor or nonexistent science. Governments were and crown transparency. induced to adopt measures to reduce pollution emissions and to invest public money in forest health research and monitor- Forest Health ing programmes. Questions about the causes of the decline have never really been resolved and remain controversial Forests are important to society because they provide multiple [6], although it is notable that the symptoms that were ob- goods and services, including the maintenance of biodiversity, served in the late 1970s (foliage reductions and discoloration) production of timber, protection against natural hazards, and after the severe drought of 1976 were again repeated follow- provision of cultural and recreational benefits. Poor forest ing droughts in the 1990s and 2000s [7]. Nonetheless, emis- health is associated with the loss of some of these goods and sions, particularly of sulfurs and heavy metals, dropped sig- services. As a result, society is increasingly concerned about nificantly over the past 30 years as a result of the Waldsterben the long-term condition of the forests. Questions about the fear. At the same time, air quality improved, as did our under- state of the forests often arise when and where there are no standing of forest ecology and ecosystem processes. Ongoing other major upheavals and woes, such as wars, famines, waves research associated with the ensuing monitoring efforts has of poverty, or pandemics. The importance of healthy forests shown how complex ecosystem processes are [8] and how typically becomes a topic of discussion when natural hazards difficult it is to define forest health, which we need to do if such as wildfires, avalanches, and landslides occur, or when we want to be able to assess it [9]. dramatic forest declines are observed. In such cases, it be- Defining forest health is as difficult as defining the health comes clear how important it is to be able to assess forest of human populations. What indicators should be used to as- health, as well as how deep our ignorance is of baseline sess the health of a forest stand? Amongst the different possi- conditions. ble indicators, which are most meaningful? Is it the mean, or Scientists, when asked about the state of the forests, often perhaps the median, tree life expectancy? And, if it is, how can provide controversial answers, evidence that a clear consen- we know how life expectancy compares to life expectancy in sual definition of forest health is still missing. When forest the past? How should we assess the health of trees that are attacked by non-lethal fungal pathologies and other diseases declines occur, forest health becomes a matter of public debate and political discussion, with news cycles strongly influencing and pests? And what mortality rates characterize a healthy public opinion. Depending on what else is in the headlines, forest versus a declining one? It is evident that in order to small events may garner much attention, whereas larger, more answer all these questions, a definition of forest health is nec- diffuse events may occur without even a passing mention. As essary. However, as noted 15 years ago [10], a clear definition a result, many people lack not only a baseline understanding of forest health has been lacking. Our literature search showed of forest health but also the ability to gauge the relative sever- that the development of a concept of forest health has been ity of any particular event. A lack of knowledge tends to make completely neglected for the past twenty years; indeed, no people more inclined to trust “experts”, particularly those who notable advances have been made at all in this regard. offer reassuring theories. Studies of forest health have been limited to the assessment Waldsterben, the forest decline that occurred in Central of the condition of single forest stands, mainly those declining Europe during the last century, is a good example of sudden, as a result of drought [11]. And again, a considered commu- uninformed public interest in forest health. In the 1970s, a nication between science and society has been lacking. decline in silver fir (Abies alba Mill.) stands was observed in Announcements of global forest health decline have appeared Germany, the so-called Tannensterben or fir dieback [1]. in scientific journals and been broadcast by mass media, caus- Some of the declines were localised around point sources of ing significant public concern. However, a meaningful defini- air pollution, such as in the Black Triangle, i.e., at the borders tion of forest health is still missing, making it difficult for between Germany, the Czech Republic, and Poland, and were anyone, expert or lay, to gauge the relative severity of the evidently caused by local emissions of pollutants [2]. Later, reported declines and respond accordingly. when a more diffuse and widespread decline of other tree Although it may be questioned whether a universal defini- species was observed in European forests (called tion of forest health is even possible, it seems unreasonable to Waldsterben or forest dieback [3]), mass media jumped on base this only on the observations of the appearance of trees. the news and provoked significant alarm. To this day, the This is a legacy of the past emphasis on production forestry, Curr Forestry Rep (2021) 7:69–80 71 where unhealthy trees were seen as a potential loss of stand clear border between life and death for trees. For example, is a yield. Today, with multi-objective forestry, the presence of tree dead as soon as it is felled, even if the crown foliage is still dead and dying trees is seen as an essential part of the main- green and actively photosynthesising? Many trees can be tenance of biodiversity. Trees and forest stands are only a part grown from cuttings, so clearly a shoot can survive been ex- of the much larger ecosystem, and their interactions with the cised from a tree, at least for a short time. Are cambial cells other components of the ecosystem have to be considered. In dead if they are still being fed carbohydrates by the foliage? Or Central European forest ecosystems, for example, forest con- is a stump dead if it is still growing thanks to carbohydrates dition is influenced by soil acidification, extreme climatic provided by neighbouring trees through root anastomoses? events such as drought or frost, pest outbreaks, interactions The stumps of many broad-leaved trees can resprout, so clear- between primary, secondary, and saprophytic fungal diseases, ly they are not dead. Our understanding of tree-longevity and many other factors. The complex synergies amongst all mechanisms [16] and prior-to-death physiological processes these factors determine tree death and forest stand dieback. is still poor. Tree senescence, including the role of telomeres This is why atmospheric, soil, and hydrological processes in ageing processes [17], is still not fully understood [18� ]. should all be taken into consideration when assessing forest In conclusion, although tree death processes are not yet health [12, 13]. However, a distinction between the various fully understood, tree mortality rates may be used as indicators factors leading to forest decline is seldom made in the public of tree vitality within a forest stand. However, although discourse [14, 15� ]. Once again, the discussion is misleading counting dead trees in a forest is certainly feasible, analysing and public opinion confounded. and interpreting tree mortality rates are difficult [19–21]. Tree mortality rates in natural conditions are completely unknown, Tree Health, Condition, and Vitality and they vary strongly depending on species and site condi- tions. Moreover, data about mortality rates in the past are not Tree vitality is one of the most important indicators of forest available and are difficult to estimate due to logging and the condition. Tree vitality, or tree condition, describes the gener- removal of deadwood by humans. Even in unmanaged forests, al outer appearance of an individual tree. In contrast, tree it may be difficult to determine when any dead trees actually health reflects the pathological state of a tree [9]. As vitality died, making calculation of mortality rates extremely difficult. cannot be measured directly, various indicators can be used to Large (50 ha), long-term monitoring plots where every tree is describe it. If tree vitality is used as an indicator of forest tagged and repeatedly assessed are beginning to shed light on condition during forest surveys, it is clear that field-practical, this important question, and the information will steadily im- low-cost methods are needed. Although vitality is a theoretical prove as long as the monitoring is maintained [22]. Without a concept and defined differently in a range of studies, it always comparison in space or time, tree mortality rates are difficult to interpret as indicators of forest health. includes the power to live, grow, and develop [10]. Therefore, indicators of tree life, growth, and development have to be used. Here, we review the literature dealing with indicators Tree Physiological Processes of tree health, together with their main advantages and limitations. Tree vitality includes the power of the tree to live and grow. Photosynthesis, which is the process by which trees synthesize carbohydrates from carbon dioxide and water using sun ener- Indicators for Assessing Tree and Forest gy, is theoretically the most appropriate indicator of tree pro- Vitality ductivity and vitality. However, data on photosynthesis rates require precision measurements and expensive equipment that Tree Death and Mortality Rates are difficult to use in the forest. As a result, photosynthesis is seldom considered in long-term forest monitoring Like all living organisms, trees die. Tree death is the ultimate programmes. Likewise, other indicators of tree biochemical indicator of zero tree vitality. Because the definition of tree and physiological processes, such as phytohormones or en- vitality includes the capacity of a tree to live, one good indi- zymes, luminescence, needle emissions, cambial electrical re- cator of tree vitality is tree survival after stress. Predisposing, sistance, and electronic potential [23] cannotbeconsideredin inciting, and contributing stress factors lead to tree decline. forest surveys because of the costs involved in their analysis During or after stress, the tree reacts immediately, then usually and the practical difficulties encountered when trying to take recovers. Trees usually reallocate carbon to overcome stress; measurements in the forest. if stress continues, the ability of a tree to overcome stress Data acquisition of physiological processes using remote diminishes until tree death occurs. sensing techniques can cost less than data acquired during However, at what point is a tree actually dead, and how ground-based fieldwork. However, fieldwork is essential for does one know? As with humans, it can be difficult to define a ground validation of remote sensing data and is indispensable 72 Curr Forestry Rep (2021) 7:69–80 when indicators cannot be observed through remote sensing once they are exposed to more light. Moreover, trees may technology within an acceptable range of accuracy. As a con- enhance their growth in response to disruptions in the forest sequence, forest health assessments are commonly undertaken ecosystem cycle, such as increased nitrogen availability in- by relating field observations (e.g., defoliation or discolor- duced by atmospheric deposition. Even if such trees are eval- ation) to remotely sensed measures. uated as being in good health, their growth rates are not good Remote sensing techniques for monitoring forest health indicators of the overall health of the forest. Nonetheless, tree include airborne imaging spectroscopy to derive vegetation productivity is commonly used as an indicator of tree health in indices, airborne laser scanning penetration variables, and surveys performed throughout the world, especially within the spectral mixture analysis [24, 25]. The most important photo- context of production forestry. synthesis indicator used in the assessment of tree vitality is To assess tree productivity, the carbohydrates being pro- chlorophyll fluorescence, which is assessed using spectrome- duced, i.e., the carbon fixed through photosynthesis, should be try [26]. Chlorophyll fluorescence is useful for assessing the measured. As it is difficult to measure carbohydrate produc- overall ability of trees to produce carbohydrates and has also tion in the field, tree biomass, as derived from tree volume, is been suggested as a way to diagnose plant stress caused by used. Thus, tree volume is often taken as an indicator of tree environmental factors [27]. However, this method has been vitality. However, tree volume itself is difficult to assess, as it more widely applied in urban tree-monitoring programmes includes foliage, branches, and roots. Indeed, the root system than in forest health surveys. is thought to be of considerable volume, but is almost impos- In conclusion, remote sensing can be used to assess tree sible to measure. Even if the root system were to be extracted vitality, but the data obtained through remote sensing must be from the soil, the volume would be underestimated, as it validated with ground data. It is perhaps for this reason that would exclude the fine roots, which seem to be a conspicuous remote sensing has seldom been used in forest surveys to part of the root system. For this reason, tree stem volume alone assess vitality. However, recent advances in remote sensing is used to assess tree productivity and therefore vitality. make the development of methods to assess photosynthetic Tree stem volume should be measured using Archimedes’ rates easier and more promising for forest-scale studies [28]. principle, but because this is impractical in a forest setting, it is usually calculated from basal area and tree height. The tree Crown Transparency taper, i.e., the degree to which a tree stem decreases in diam- eter as a function of height above ground, should be taken into Since the first observations of forest decline during the 1970s account. In practice, stem volume is calculated from measure- in Central Europe, crown foliage transparency has been com- ments of tree diameter at breast height (1.3 m height) and monly believed to be the best indicator of tree condition in overall tree height. A good example of assessing tree productivity, i.e., car- relation to air pollution. For this reason, it has been widely adopted as the most important indicator of tree vitality. bon (C) content, is offered by Bascietto et al. [34]. The re- Although crown transparency assessment has been criticized sults of their study showed that ring width and stem analyses vehemently because it is highly subjective and not cause- maybe usedtoreconstruct treestem volumeandcarbon specific [29], European forest health has been assessed for production. the past 30 years using this indicator [12]. This wealth of data Tree productivity, biomass, and volume are certainly indi- has shown that most of the variability associated with crown cators of tree growth, but they are difficult and time- transparency assessments is the result of methodological dif- consuming to estimate, and strongly affected by errors and ferences, differences in tree age, and some climatic factors, approximations. mainly drought [30], rather than air pollution [8]. Crown transparency is therefore not a good indicator of tree vitality, although it continues to be recommended as an indicator when Basal Area Increment used in association with other indices of crown condition [31–33]. Basal area increment may be used as a proxy for volume [35]. The advantage of using basal area instead of ring width is that Tree Productivity, Biomass, and Volume no data standardization is needed to remove the geometrical age trend, i.e., the decreasing trend in ring width due to the Tree productivity is often considered to be an expression of increasing stem circumference with tree age, preserving all tree vitality. However, its use is questionable because the most other long-term trends [36]. To obtain accurate results, stem productive trees are not always in good health. For example, disks are needed because extrapolating basal area increment tree growth may increase as a reaction to fungal attacks or using tree cores often introduces mistakes that compromise injury. Trees may also grow very slowly in the shade of other the results. However, the use of stem disks requires that the trees for hundreds of years, only becoming truly productive tree be felled. Curr Forestry Rep (2021) 7:69–80 73 Tree-Ring Growth although recent studies have shown that different sampling strategies achieve different results [46]. Given the difficulties in calculating tree stem volume, and the The weakness of ring width as an indicator is also shown uncertainty of tree volume estimates, tree-ring measurements by tree-ring studies of trees grouped into vitality classes to test have often been preferred to stem volume assessments in for- growth differences between the classes [47]. While many of est health surveys. Particularly when assessing forest health these studies show decreased growth and higher crown trans- over large areas, dendrochronological studies provide infor- parency, others show no such relation [48], or no relationship mation about the growth of a large number of trees without the at low to moderate levels of transparency [49]. Although it has need to fell them. Tree-ring studies also allow for the recon- been demonstrated that crown transparency correlates with struction of past tree growth over time. Therefore, tree-ring subsequent tree mortality in some cases [50], an unambiguous width, as an indicator of tree volume growth, is a widely used relationship between crown transparency and tree growth can- indicator of tree vitality. not be demonstrated. Similarly, attempts to relate the results In temperate climates, the cambial activity of trees and obtained from dendrometer bands to crown transparency have shrubs stops during the cold season, resulting in the formation yielded few significant relationships. of annual growth rings. Tree rings have been used for In conclusion, tree-ring widths have frequently been used reconstructing past climatic conditions and events. More as indicators of tree vitality in forest stands suffering environ- broadly, tree rings can be used as indicators of the environ- mental stress. However, the majority of such studies are af- mental conditions (not only climatic) in which trees have been fected by potential sampling bias, and by uncertainty related to growing because their chemical and physical characteristics whether growth changes are the result of stand dynamics or an depend on the environmental conditions in which they grew. independent change in tree vitality. Tree-ring analysis has contributed significantly to the discus- sion about the impact of environmental changes on tree growth and tree vitality. However, many different factors Tree-Ring Stable Isotopes as Integrative can have the same effect on tree growth, making it difficult Physiological Indicators of Tree Vitality to disentangle the effects of different factors. In studies of the impact of air pollution on forests, Tree-Ring Stable Isotopes dendroecological methods have been used to identify anoma- lous growth trends. However, unlike the effects of point Stable isotopes are important tools for evaluating the impact of sources [37], the large-scale diffuse impacts of air pollution biotic (e.g., pest outbreaks and fungal diseases) and abiotic on forests are still unclear [4, 38]. In Central Europe, for ex- (e.g., extreme climatic events, fire, air pollution, direct dam- ample, abrupt growth decreases were detected during the age due to management operations) factors on forest health 1980s [39, 40]. Some pioneering studies around pollution and vitality. If the stress conditions are not so harsh as to point sources, such as smelters, have documented a decrease prevent tree growth, i.e., allowing tree-ring formation, tree- in tree growth as a consequence of water, air, and soil pollut- ring stable isotopes can be used to assess retrospectively the ants [41]. Studies of the impact of air pollution at a regional impact of environmental disturbances on tree vitality. scalehavebeenmorecontroversial[42]. Stand dynamics However, it is extremely difficult to disentangle the role of seem to have strongly affected the results of many of these the different disturbances in forest decline episodes [51, 52]. studies [43]. Tree-ring studies provide information about past growth Carbon Stable Isotopes rates, but the interpretation of long-term growth trends is dif- ficult. Many dendroecological studies of long-term growth Tree-ring carbon stable isotope ratios (δ C) are powerful trends are affected by sampling bias because of the influence proxies used in climate reconstructions [53] and are increas- of stand dynamics (e.g., mortality, competition, disturbance). ingly used to help unravel tree physiological processes [54]. In particular, the restriction of sampling to a few of the largest- Tree-ring carbon stable isotope ratios can be considered an diameter trees within a stand may have a marked influence on integrated indicator of tree vitality over time. Plants discrimi- the ensuing results [44]. When assessing long-term growth nate against the heavier carbon isotope C; as a result, plant trends, most investigators sample the largest-diameter trees material is depleted in C relative to air CO . A negative sign 13 12 in a stand. This strategy has arisen from the desire to sample indicates that the plant sample has a lower C/ C ratio than the oldest trees in a stand, which are often incorrectly assumed the standard (PDB), and a lower discrimination is indicated by to be the largest. However, tree-ring patterns and the sizes of a higher, i.e., less negative, δ C. In C plants, the discrimina- trees are strongly affected by forest management and natural tion is driven by two fractionation processes: (a) diffusion of disturbances [45]. The effects of restricting sampling to the CO through stomata, reducing δ C by 4.4‰, and (b) the largest trees have never been adequately documented, enzymatic process of carboxylation, which further reduces 74 Curr Forestry Rep (2021) 7:69–80 13 13 13 δ Cby 27‰. The carbon isotope ratio (δ C) is therefore δ C, but is unaffected by changes in net photosynthetic ac- affected by both changes in atmospheric CO concentrations tivity (A) [65]. (c ) and by changes in the substomatic chamber or intercellu- lar (c)CO concentrations. The CO input rate (g ) of the Using Carbon and Oxygen Stable Isotopes to Study i 2 2 s substomatic chamber is regulated by the stomata; the output Air Pollution rate is regulated by CO assimilation (A). These processes are strongly influenced by environmental variables such as light, Variations in atmospheric gas concentrations, such as the in- temperature, and water and nutrient availability, which are creases in CO concentrations, air pollution, and acidic pre- then reflected in tree-ring stable isotopes [55]. cipitation due to fossil fuel combustion, affect forest ecosys- In general, C discrimination declines under stress condi- tems at individual tree and canopy levels. Stable isotopes have tions, such as water shortage. This may be attributed to partial largely been applied to assess the physiological mechanisms or complete stomatal closure in the case of water stress, which induced by those factors and to better understand their impli- causes limited diffusion of both CO and H O and thus less cations for the global carbon, water, and nitrogen cycles (see 2 2 carbon isotope discrimination [47]. However, stomatal conduc- Table 1 Supplementary Material). For example, in several tance responds not only to water availability but also to water forests, elevated CO concentrations, temperature, and demand. This means that other variables such as air relative drought increase seem to promote an increase in plant water humidity, vapour pressure deficit, and potential evapotranspira- use efficiency with an enhancement of photosynthesis and a tion also affect discrimination [56]. Furthermore, other stress generally modest reduction in stomatal conductance [66]. The conditions induced by changes in temperature, light, CO con- influence of each factor is still under debate and difficult to centrations, or nutrient availability [57] could influence stoma- disentangle [67]. Tree-ring δ C samples from around the tal conductance and lead to increases in the CO assimilation globe show an increase in WUE since pre-industrial times 2 i rate via Rubisco. This increase leads to a corresponding de- [68, 69]. Exposure to SO and O has been reported to inhibit 2 3 crease in c /c and causes plants to discriminate less against photosynthesis by inducing stomatal closure [70, 71]. i a C. Furthermore, through its relationship with the ratio be- Meanwhile, elevated NO concentrations may increase pho- tween the intercellular and the atmospheric CO partial pres- tosynthetic rates by activating carboxylation enzymes due to sures, tree-ring δ C has been widely used to study intrinsic the “N fertilization effect” during short-term exposure [72]or water use efficiency in plants ( WUE) [55, 58]. in the long-term trend [73]. However, long-term exposure is In tree-ring cellulose, the δ C incorporates additional believed to cause forest decline. The general isotopic response sources of variation unrelated to environmental factors, such to air pollution is a reduced discrimination against Cdue to as fractionation processes taking place during the mobilization stomatal closure, which creates higher δ C values in tree of photosynthetic assimilates from the leaf to tree-ring produc- rings and leaf tissues. Such studies reported that the increase tion [59]. For instance, the tree may use remobilized stored in δ C in plant tissues is mainly due to [1]stimulated activ- carbohydrates (primarily starch) for the construction of new ities of PEP carboxylase, [2]change in cell metabolism, [3] wood cells. This is the so-called memory effect [60, 61]. As a decline in carboxylation efficiency due to collapse of meso- consequence, the tree ring might have the signal of the year in phyll cells, or [4] higher rates of dark respiration, with no which the starch was produced, which may differ from the significant changes in the stomata aperture (Table 1 year in which it is incorporated into the tree ring by many Supplementary Material). The majority of the studies around months or even years [62]. point-source pollution under real field conditions showed an increase of tree-ring δ Cvalues [74, 75]. Oxygen Stable Isotopes Using Nitrogen Stable Isotopes to Study Air Pollution Oxygen stable isotopes (δ O) are another important source of environmental information that can be extracted from trees Besides δ C, most of the studies on the effects of air pollution 18 15 [63]. Tree δ O includes three variable components beyond on tree growth and physiology are based on δ N that can source water variability: (1) the leaf water enrichment, modi- provide indications of changes in ecosystem N cycling in re- fied by the Péclet effect and the dampening of δ Oat evap- sponse to the different pollution sources [76]. oration sites due to leaf water heterogeneity, (2) the biochem- Studies of nitrogen stable isotopes in tree rings started some ical fractionation between carbonyl oxygen and water during decades ago. Poulson et al. [76] measurednitrogenisotopesin cellulose synthesis, and (3) the δ O of water vapor outside two individuals of Tsuga canadensis to study the effect of the leaf, mostly influenced by relative humidity [64]. atmospheric N deposition on a forest in NH, USA. Both trees 18 15 Furthermore, tree δ O can be used to discriminate between showed a decreasing trend in δ N from the 1960s to the biochemical and stomatal limitations to photosynthesis, since 1990s and an increasing nitrogen concentration. The authors it shares a dependence on stomatal conductance (g )withplant attributed this result to the increasing emission of NOx in the s Curr Forestry Rep (2021) 7:69–80 75 USA, which leads to increasing atmospheric deposition of infestation of piercing–sucking insects in AZ (USA). A simi- isotopically light nitrate and ammonium in acid rain. The an- lar lack of response was observed by Haavik et al. [84]ina thropogenic impact on natural nitrogen isotope variation was study of growth patterns of Quercus rubra during and after a also studied in a polluted area of Germany by Jung et al. [77]. pest infestation in the late 1990s. The authors found that Pinus sylvestris needles and tree rings In contrast, Simard et al. [85]reported Cenrichment in were more depleted in δ N and had lower N concentrations at Abies balsamea and Picea mariana following defoliation by sites further from the industrial agglomeration. Ammann et al. the spruce budworm Choristoneura fumiferana in boreal for- 115 18 [78]investigated δ Nin Picea abies needles in a forest in the est of Quebec. However, they found no differences in δ O Swiss Central Plateau, near a highway. They found the highest values during and after the outbreak and concluded that the values in plots closest to vehicular traffic and estimated that observed C enrichment could be explained by both an in- vehicular emissions contributed about 25% of the N nutrition crease in photosynthetic rate and the remobilisation of starch of the needles. At the same site, Saurer et al. [75]studied a reserves during severe defoliation. Kress et al. [86]inferred transect of Picea abies perpendicular to the highway, to deter- that larch budmoth (LBM) did not impact the carbon and mine the effect of NOx from car exhaust on tree growth. They oxygen tree-ring isotope signatures of Larix decidua trees on found that the trees growing nearest the highway exhibited a European Alps. Similarly, Weidner et al. [87]observed that disturbance in nitrogen concentration and a dramatic increase the loss of needles due to LBM outbreaks did not significantly in tree-ring δ N signal starting when the highway was built. influence the tree-ring carbon isotope signature. In contrast to This study confirmed that tree rings can be an environmental carbon isotopes, however, they found that oxygen isotopes monitoring tool and that the isotopic signal of N sources can seemed to react much more sensitively to strong LBM infes- be stored in them. However, Battipaglia et al. [79] could not tations. This could be because during the main defoliation find any clear δ N signal in tree rings close to a traffic pol- event, photosynthesis does not take place due to either a lack lution source, showing that radiocarbon is a much better indi- of needles or desiccated or dysfunctional (brown) needles. cator of changes in air quality due to fossil fuel combustion. Accordingly, very few photosynthates are produced. They Burning fossil fuel introduces CO that has no C into the therefore suggested that tree-ring cellulose formed during atmosphere, which influences the global atmospheric LBM outbreak years is built with carbohydrates formed either CO - Csignal,i.e., the Suess effect [80]. Several other pa- before the heavy feeding occurs or shortly thereafter, i.e., 15 18 13 pers have coupled δ N with δ Oand δ C to monitor plant when new foliage emerges 3–4 weeks after defoliation. exposure to elevated oxidant pollutants such as ozone, sulfur Simard et al. [88] (2012) investigated the potential use of dioxide, and NOx using different temporal and spatial per- tree-ring isotope composition to identify different degrees of spectives [81]. However, both the magnitude and the direction past spruce budworm defoliation episodes in seedlings of of the reported isotope effects have varied as a result of the Abies balsamea grown in a controlled experiment. They re- 13 13 opposing effects of fossil fuel CO dilution and the effects of ported an enrichment of C in moderately to heavily secondary combustion products on tree physiology. Thus, it defoliated seedlings, probably due to the remobilization of can be difficult to extract general trends from these data. stored carbohydrates enriched in C. They did not observe any variation in carbon composition in seedlings that experi- Pest Outbreaks enced less severe defoliation. Few studies have examined the effects of insect outbreak Other Disturbances events on tree-ring stable isotope composition, and the results of those that exist are rather controversial. Although it is well Natural forest disturbances, such as fires, windstorms, or known that host plants can change their physiology by altering flooding, are expected to increase in both severity and fre- their water relations and their modifying photosynthate allo- quency under global warming and to seriously affect forest cation and photosynthetic capacity as a consequence of insect health and ecosystem services. Stable isotopes in tree rings defoliation, the isotope signals do not always reveal changes have the potential to provide information about the frequency in discrimination rate. Leavitt and Long [82] compared tree- and severity of extreme events in the past, thereby aiding with ring carbon stable isotopes of two host species (Abies extreme-hazard assessments. concolor and Pseudotsuga menziesii) during a western spruce To aid with the understanding of the physiological responses budworm outbreak in the USA. Although they observed an of trees to wildfire in southern Europe, the dual-isotope ap- 13 13 18 increase in δ C when compared to a non-host species (Pinus proach [89], which combines the analysis of δ Cand δ O, ponderosa), they did not record any change in discrimination has been used to discriminate between biochemical and stoma- in the host species due to the pest outbreak. Likewise, tal limitation to photosynthesis [90–98]. Indeed, fire can dam- Ellsworth et al. [83] did not observe any variation in δ Cor age the crown, reducing leaf surface and altering the plant’s WUE in the leaves remaining on deciduous trees after an photosynthetic rates and, being the plant δ O related to i 76 Curr Forestry Rep (2021) 7:69–80 stomatal conductance (gs) but unaffected by photosynthesis strong coherence amongst species and strong correlations with (A), it can help separate the independent effects of A and gs climatic indices, including growing season, temperature, and on δ C. drought. In particular, stable isotopic ratios can provide infor- Other studies demonstrated physiological consequences of mation about the water use efficiency, i.e., the amount of fire deficits in forests of the western United States [99]and in carbon assimilated as biomass per unit of water used by the trees growing on permafrost in boreal ecosystems [100]. All of tree. A growing body of evidence shows that plants can close these studies demonstrated that the responses of the trees, and their stomata during drought events to avoid unnecessary wa- thus of the stable isotope signature, depend on fire severity. ter loss. Consequently, stomatal conductance to CO de- Severe wildfires that result in partial or complete crown defoli- creases and Rubisco fixes a higher-than-usual proportion of 13 18 13 12 ation lead to a simultaneous enrichment of δ Cand δ Oin Ccompared to C. As a result, rings are formed in which tree rings. This is because trees close their stomata and decrease the cellulose is enriched in the heavier isotope, which trans- their photosynthetic activity [92, 98, 99]. Medium and low lates as less negative isotopic signatures and those large anom- 13 13 severity fires produce little to no change in δ C, no change alies in their δ C can be indicators of forest health [106–109]. in δ O, and a partial reduction in tree growth due to the lower Other studies of co-occurring healthy and dead trees found a photosynthetic capacity of the burned trees [79]. lower WUE in dead trees, suggesting either a reduction in photosynthesis rates or, more probably, a poor regulation of stomatal conductance [110–112]. The higher WUE observed Tree Response to Drought in surviving trees suggests higher photosynthesis rates or more conservative water use strategies during drought [111]. Over the past decades, there has been a worldwide increase in Stable isotopes are a key to understanding physiological reports of drought-related forest declines [11, 101]. The de- processes related to tree vitality, and to understanding how clines are seemingly triggered by multiple, interacting factors, forest declines are linked to drought events. A good example ranging from drought to insect pests and diseases and to af- is given by Gessler et al. [113� ], who developed a conceptual 13 18 forestation with poorly adapted non-native species. This model based on tree-ring δ Cand δ O isotopes. Their model makes it difficult, if not impossible, to disentangle the drivers suggests that when dead trees have long-lasting gas exchange of forest declines. Abiotic stress factors can induce forest and growth declines, in comparison with healthy trees, mor- health problems and extreme climate events, particularly tality is induced principally by carbon starvation, whereas drought, are thought to be a primary factor triggering many rapid or no decline of both stomatal conductance and growth extensive forest pest outbreaks and fungal diseases [102]. prior to death is indicative of hydraulic failure [99]. There are two main physiological processes involved dur- ing tree mortality: Conclusions 1. Hydraulic failure processes, induced by reduced soil wa- ter supply coupled with high evaporative demand. This A clear definition of forest health is still missing and little causes xylem conduits and the rhizosphere to cavitate, progress had been made toward the developing the theoretical stopping the flow of water and desiccating plant tissues framework around the concept of forest health. This lack of [103, 104]. definition is caused by the poor understanding of the physio- 2. Carbon starvation processes, induced by stomatal closure. logical mechanisms underlying tree mortality and forest die- Although designed to prevent water loss, stomatal closure back episodes. To evaluate forest health, monitoring efforts leads to a decrease in carbon uptake and photosynthetic have concentrated on the assessment of tree vitality, trying to activity, which causes the plant to starve as a result of its estimate photosynthesis rates and productivity. In order to continued metabolic demand for carbohydrates. extend such estimates back in time, tree rings have been used as indicators of past productivity. In particular, tree-ring width Researchers have debated the roles of these two co- measurements have been widely used to provide information occurring processes. Adams et al. [105]stated that in most about past climatic events, such as drought and frost, and cases, both processes occur together, even if hydraulic failure trends and the response of trees to them. However, ring width can occur alone without any carbon starvation, whereas car- patterns are prone to misinterpretation and do not provide any bon starvation only occurs in conjunction with hydraulic fail- information about tree physiological processes other than ure. The majority of studies assessing hydraulic failure have those directly related to tree growth. looked at the percentage of loss of xylem conductivity (PLC), In the past two decades, it has become clear that tree mor- while carbon starvation was assessed via changes in tissue tality processes involve the storage and transport systems of non-structural carbohydrate (NSC) concentrations [103]. water and photosynthate. Extreme drought events induce the Some studies of tree-ring stable isotopic composition show a loss of xylem hydraulic conductivity, causing tree death. Tree- Curr Forestry Rep (2021) 7:69–80 77 credit line to the material. If material is not included in the article's ring stable isotopes have been increasingly used in the study Creative Commons licence and your intended use is not permitted by of drought-induced forest decline and have proven to be use- statutory regulation or exceeds the permitted use, you will need to obtain ful tools for understanding physiological processes in the past. permission directly from the copyright holder. To view a copy of this Although they have yet to be used to assess tree vitality rather licence, visit http://creativecommons.org/licenses/by/4.0/. than to study tree response to environmental stress, tree-ring stable isotopes integrate crown transpiration rates and photo- References synthesis rates. When analysed together with ring widths, tree- ring stable isotopes may enhance our understanding of tree Papers of particular interest, published recently, have been vitality. They are promising indicators of tree vitality and also highlighted as: allow for retrospective studies of tree physiological response � Of importance to past abiotic and biotic disturbance events and trends. �� Of major importance Here, we have reviewed the existing literature on forest health and tree vitality indicators. We postulate that the forest 1. Schütt P. Der Stand unseres Wissens über eine aktuelle und gefährliche Komplexkrankheit der Weißtanne (Abies alba Mill.). dieback episodes that have been recently observed were in- Forstw Cbl. 1977;96:177–86. duced by drought. We propose that some of the episodes of 2. Ulrich B, Pankrath J. Effects of accumulation of air pollutants in mortality and dieback observed during the 1970s and 1980s forest ecosystems. Dordrecht: De Reidel Publ. 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