Forestry Advance Access originally published online on April 11, 2006
Forestry 2006 79(4):425-437; doi:10.1093/forestry/cpl009
| ||||||||||||||||||||||||||||||||||||||||||||||||||||
Bud development types as a new macroscopic marker of Norway spruce decline and recovery processes along a mountainous pollution gradient
1 Department of Plant Physiology, Faculty of Science, Charles University, Vini
ná 5, CZ-128 44, Prague 2, Czech Republic
2 Institute of Botany, Academy of Sciences of the Czech Republic, CZ-252 43 Pruhonice, Czech Republic
3 Complex Systems Research Center, University of New Hampshire, Morse Hall, Durham, NH 03824-3525, USA
*Corresponding author. E-mail: albrecht{at}natur.cuni.cz
 |
Summary |
|---|
 Top Summary IntroductionMaterials and methodsResultsDiscussionConclusionsAcknowledgementsReferences |
|---|
A new macroscopic marker of decline and recovery processes in Norway spruce (Picea abies) based on proportions of bud development types was evaluated in 315 mature trees in two mountainous regions of the Czech Republic. This study was conducted in 1998 at 63 sites located in the Krusne hory Mts, which exhibited a wide range of damage corresponding to a gradient of increasing air pollution load (mainly SO2 and NOx) and the Sumava Mts, a relatively unpolluted area. Proportions of bud development types (regular buds, buds with growth potential and aborted buds) were found to reflect the current intensity of primary shoot formation in crowns as well as a capability to replace needle loss by formation of secondary shoots via differentiation of buds with growth potential. Using cluster analysis, the trees were classified according to the proportion of individual bud development types into one of three shoot growth categories: accelerated, stabilized or decreased shoot growth. Trees with accelerated shoot growth are characterized by intense production of assimilative organs and a small pool of viable buds with growth potential. Trees with stabilized shoot growth have high potential for crown recovery via activation of abundant buds with growth potential, and trees with decreased shoot growth have high rates of aborted buds, slow primary shoot formation and small pools of buds with growth potential. This new marker reflects well the forest recovery observed in areas with recent decreases in pollution loads. The results indicate that traditional macroscopic markers such as crown defoliation are less sensitive to the current status of tree crowns when compared with the proportion of individual bud development types. The potential of this new marker for forestry practice and tree physiology is discussed.
|
Introduction |
|---|
|
TopSummaryIntroductionMaterials and methodsResultsDiscussionConclusionsAcknowledgementsReferences |
|---|
Traditional macroscopic markers of tree crown status are crown defoliation and needle discoloration. Defoliation as a valid indicator of tree crown status has been questioned (Salemaa and Jukola-Sulonen, 1990
; Klap et al., 2000) since trees with little foliage are known to survive on extreme sites for many years (Pfanz et al., 1994) or even compensate needle losses by formation of new secondary shoots and to recover (Cudlín et al., 2001). The processes leading to crown recovery promote tree resistance to defoliation (Chen et al., 2001) since they enable replacement of needles shed as the result of either normal senescence or the impact of stress factors such as air pollution. Therefore, improved assessment methods and understanding of the recovery processes could be an important tool for forestry management for employing timely measures and for the detection of resistant or susceptible individuals to a range of environmental factors.
Symptoms of tree damage due to stress impact can be identified at the macroscopic level and also at previsual microscopic and metabolic levels. These approaches differ in the timing of detection of the initial signs of the tree damage. The markers of tree damage are first detectable at metabolic and microscopic levels when the initial stress impact occurs. Studies focused on metabolic markers of damage conducted on spruce needles include chlorophyll degradation (Moss et al., 1998; Soukupová et al., 2000), accumulation of phenolic compounds (Vogelmann and Rock, 1988) and changes in cell lignification and in synthesis of peroxidases in the needles (Pfanz and Oppmann, 1991; Soukupová et al., 2000) and at the microscopic level e.g. epicuticular wax degradation (Viskari, 2000), changes in anatomical structure of needles (Vogelmann and Rock, 1988; Moss et al., 1998; Soukupová et al., 2000) and chloroplast ultrastructure (e.g. Fink, 1999; Lepedu
et al., 2001).
Fewer studies have focused on the investigation of Norway spruce buds and their physiological state. The markers of tree damage at the microscopic level include e.g. increase in number of living bud scales, decrease in number of leaf primordia and decrease of flatness of bud apical meristems (Soukupová et al., 2002) and at the metabolic level e.g. enhanced accumulation of phenolic compounds, increased activity of non-specific esterase (Soukupová et al., 2002) and changes in contents of non-structural carbohydrates (Svobodová et al., 2000). A study of metabolic and microscopic markers of tree damage usually requires extensive laboratory work, both expensive and time consuming. Therefore, macroscopic markers which are less affected by seasonal fluctuations of environmental conditions and less laborious are potentially very useful tools for studying forest decline.
The proportion of individual bud development types has been suggested as a new and potentially effective macroscopic marker of tree crown status for forestry management (Albrechtová, 1997; Polák et al., 2004) because the state of apical meristems (the buds) determines regenerative processes in the crown. Any disruption of bud development reduces the biomass and/or quality of foliage produced in the following year (Straw et al., 2000). The development of vegetative buds of Picea abies was first described by Hejnowicz and Obarska (1995) and in more detail by Soukupová et al. (2002). Kozlowski (1971) classified buds as active, producing primary shoots by regular growth (regular buds), and inactive buds. Regular buds periodically complete the annual growth cycle. In the beginning of the vegetative season resting, dormant buds break dormancy and a new primary shoot is flushed and elongated. New buds are set and differentiated during the second half of the vegetative season. Some buds do not complete the annual growth cycle and stay inactive during the entire vegetative season (Kozlowski, 1971). Inactive buds can develop in two alternative ways depending on a combination of external and internal factors. Meristematic tissues of the first group remain viable at least until the following season. For the purpose of this study, we designate this type of inactive buds as ‘buds with growth potential’, independent of their inner structure, i.e. if they are dormant or latent (Albrechtová, 1997). Buds with growth potential are prepared for activation during subsequent seasons and form secondary shoots out of normal phyllotaxy (Gruber, 1994). Buds with growth potential may resume development depending on their development program or in response to environmental cues (Kozlowski, 1971; Shimizu-Sato and Mori, 2001). Secondary shoots are not normally initiated until the trees are stressed by insect feeding (Powell, 1974), defoliation (Halle et al., 1978) or pruning (Ishii et al., 2000). Meristematic regions of the second group of inactive buds are dead or lost, i.e. aborted, which means they do not have any potential to be differentiated into a shoot in the future. Based on a detailed anatomical study, macroscopic criterion was developed for the classification of individual vegetative bud development types, including regular buds, aborted buds and buds with growth potential (Albrechtová, 1997).
Proposing any new biomarker of tree crown status requires sampling a range of trees damaged by different stress impacts. During the 1970s and 1980s, air pollution loading was the most harmful stress factor affecting endangered mountain forest ecosystems in Central Europe. Since the 1990s, environmental conditions in the Czech Republic have greatly improved; however, it is apparent that pollution-induced adverse soil conditions will persist much longer following the improvement of air quality. Even though emission levels have decreased dramatically, e.g. SO2 emission decreased from 2161 ktons year–1 in 1985 to 443 ktons in 1998 (data from the Czech Hydrometeorological Institute: http://www.chmi.cz/), the emission levels still remain relatively high with a low probability of further decreases and may contribute further to forest decline in the future (Klap et al., 2000).
This study was conducted in two regions of the Czech Republic exposed to different levels of stress factors, where differences in air pollution load played the most significant role. The south-western part of the Czech Republic, where the Sumava Mts are located, belonged to the least polluted area in the Czech Republic (data from the Czech Hydrometeorological Institute). In contrast, the most heavily polluted area was north-western Bohemia, where the Krusne hory Mts are located (Figure 1, Table 1). The latter region was part of the so-called ‘Black Triangle’ and exhibited a strong gradient of acidic pollution loads in the past with the eastern and central parts of the Krusne hory more heavily polluted than the western part (Figure 1, Table 1).
|
|
The individual goals of the study were to (1) evaluate the current state of buds according to their activity for trees from different areas using macroscopic criterion for classification of bud development types, (2) propose new categories of shoot growth of mature Norway spruce trees reflecting the ongoing decline or recovery processes taking place in crowns using criterion for classification of bud development types, (3) evaluate the relationship between the newly proposed shoot growth categories and crown defoliation and (4) compare newly proposed categories of shoot growth in two different mountainous areas characterized by a gradient of pollution loads.
|
Materials and methods |
|---|
|
TopSummaryIntroductionMaterials and methodsResultsDiscussionConclusionsAcknowledgementsReferences |
|---|
Research areas, tree sampling and standard forestry measurements
A total of 63 plots of 30 x 30 m each located in homogeneous mature (60 years or older) Norway spruce forests were selected for the present study. Study sites were selected in the Sumava Mts (area 1) and three areas from the western (area 2) to central (areas 3 and 4) Krusne hory Mts (Figure 1). The sites had minimal differences in slope, climate and altitude (800–1150 m), but differed greatly in the amount of acidic deposition and air pollution loading in the past, especially during the 1980s and in the beginning of the 1990s: the Sumava had relatively low levels of pollution, while area 2 had medium and areas 3 and 4 high pollution levels (Table 1).
Five representative trees at each site were selected to reflect the variability of crown defoliation. One sunlit branch was systematically collected for analysis, using pruning poles, from the middle third of the production portion of a crown from trees at all sites (315 trees).
Standard forestry measurements included crown defoliation using the classification table for individual spruce phenotypes (Müller and Stierlin, 1990), needle discoloration and needle retention. Tree damage class (TDC) was determined according to crown defoliation and needle discoloration (0–9 per cent defoliation, TDC 0; 10–29 per cent, TDC 1; 30–49 per cent, TDC 2; 50–69 per cent, TDC 3, and 70–99 per cent, TDC 4). In the case of needle discoloration, the TDC was set one level higher. We did not find any Norway spruce with TDC 4 at the selected sites. Needle discoloration, including yellowing and browning, was assessed as a binary variable (1, present; 0, no discoloration) for individual trees and a mean proportional value for each area was recorded.
Classification of bud development types
Due to the periodic growth of a shoot unit which leaves a scar between annual shoots, it is possible to determine the year of a shoot's origin and to count the number of regular and inactive buds occurring on the branch (Figure 2a,b). By longitudinal cutting of an inactive bud into two halves (Figure 2c), the difference between a bud with growth potential and an aborted bud can be distinguished. The bud with growth potential is characterized by green meristematic tissue (Figure 2d), while the aborted bud is characterized by dead, brown meristematic tissue (Figure 2e). The green colour of viable dormant buds is due to chloroplasts contained in needle primordia (e.g. Lepedu et al., 2001) and these buds might form secondary shoots during subsequent seasons, i.e they have growth potential. The brown colour of the meristematic region of an aborted bud is due to dead tissue containing no chlorophyll and a lot of lignin and other phenolics.
|
To determine the current status of Norway spruce buds in a crown, only the buds (either terminal or lateral) which appeared on 1-year-old shoots were analysed (red lines, Figure 2a). These are the youngest shoots on which regular buds can be reliably identified as those giving origin to current-year primary shoots. During sampling in August 1998, we analysed the buds formed on 1997 shoots. At least 70 buds per distal segment of a branch were classified into one of the three categories: regular (Figure 2b), aborted buds (Figure 2e) or buds with growth potential (Figure 2d).
Statistical analysis
The shoot growth categories were set according to cluster analysis using quadratic Euclidean distance and the Ward criterion (Brosius, 1989) to address the following question: How can the 315 Norway spruce trees measured be grouped into clusters in which the intensity of shoot growth is described by a proportion of individual bud development types? The relationship among discrete variables, including shoot growth categories, TDC and tree location (area), were studied by loglinear models. To study the influence of locality (area) and TDC on response variables (ratio of regular to aborted buds and proportion of buds with growth potential), a Hierarchical-Classification Design of anaylsis of variance (ANOVA) has been used. Area and TDC were designated as fixed factors, while site was used as a nested factor inside an area. We were interested in the contribution of the factors ‘area’ and ‘TDC’ and their interaction to the whole model. One-way ANOVA was used to detect differences between individual areas and the Tukey–Kramer test was used as a Multiple Comparison test. The data were normally distributed and the tests were based on a 0.05 significance level. Statistical analyses were performed using NCSS 2001 software (Hintze, 2001).
|
Results |
|---|
|
TopSummaryIntroductionMaterials and methodsResultsDiscussionConclusionsAcknowledgementsReferences |
|---|
Bud development types
Two variables were used to interpret the results of the macroscopic classification of bud development types: the ratio of regular to aborted buds and the proportion of buds with growth potential. The higher the ratio of regular to aborted buds, the more intensive the primary shoot formation. Low values of the ratio correspond to a high rate of bud mortality, a low proportion of regular buds and, thus, a low intensity of the primary shoot formation. The higher the proportion of buds with growth potential, the higher the tree's capability to replace actual or potential needle loss in the future by formation of new secondary shoots under stress conditions.
The results of the Hierarchical-Classification Design of ANOVA revealed that both variables – the ratio of regular to aborted buds and the proportion of buds with growth potential – were significantly affected by TDC (P = 0.0007 and P = 0.0012, respectively), but not by area location (P = 0.3067 and P = 0.1274, respectively). The intensity of primary shoot formation was about two times higher for heavily defoliated trees (TDC = 2, 3) than for healthy, less defoliated trees (TDC = 0, 1) independent of the area of tree location (Figure 3a). Whereas the mean values of proportion of buds with growth potential for areas 1–4 varied between 20 and 32 per cent for healthy trees, it reached only 10 per cent for the most defoliated trees (Figure 3b). Non-significant interaction of both factors leads to a generalized pattern in which the intensity of primary shoot formation increased and the growth potential to form secondary shoots decreased with higher TDC, regardless of the timing of levels of air pollution loading for all areas under study.
|
= 0.05.Shoot growth categories
A total of 315 Norway spruce trees were grouped by cluster analysis by the proportion of individual bud development types falling into the three categories. Since the categories reflect shoot growth accomplished via bud meristems, in principle, they correspond to accelerated shoot growth, stabilized shoot growth or decreased shoot growth. A tree with accelerated shoot growth is defined by a high ratio of regular to aborted buds (>7) and a low proportion of buds with growth potential (
20 per cent), which indicates intensive formation of primary shoots and a low pool of reserve meristems in buds with growth potential capable of forming secondary shoots under unfavourable stress conditions. A tree with stabilized shoot growth is defined by a high proportion of buds with growth potential (>20 per cent) and therefore by a high potential to replace needle loss by the activation of secondary shoots. Intensity of shoot growth (the ratio of regular to aborted buds) is not a determining factor for this category. A tree with decreased shoot growth is characterized by a low proportion of buds with growth potential (20 per cent) and low regular to aborted buds ratio (7). The primary shoot formation of these trees is slow and a pool of viable meristems in buds with growth potential is low.
Shoot growth categories and TDC
Tree damage class, derived from crown visual estimates of defoliation and needle discoloration, is determined by ongoing degradative and regenerative processes in the crown. The newly defined shoot growth categories are measures of recovery processes taking place in a tree crown; therefore, some trade-offs might be expected between shoot growth categories and TDC. Loglinear models revealed a significant relationship between shoot growth categories and TDC as well as between shoot growth categories and tree location (both P < 0.0001). Figure 4a indicates that 60–65 per cent of healthy to mildly defoliated trees (TDC = 0, 1; defoliation < 30 per cent) revealed stabilized shoot growth, whereas it occurred in only 13 per cent of heavily defoliated trees (TDC = 3). The majority of heavily defoliated trees (77 per cent of TDC = 3) exhibited accelerated shoot growth, compared with 42 per cent for moderately defoliated trees (TDC = 2) and only 12 per cent for mildly defoliated trees with TDC = 0, 1.
|
Shoot growth categories and tree location
The study sites were selected in areas with comparable environmental conditions but with very different pollution loading. In 1998, the standard forestry measurements reflecting foliage biomass (needle retention and TDC assessed on the basis of visual crown defoliation) and physiological status of assimilative organs (needle discoloration) revealed the best crown status of trees from the area 1 (Sumava Mts) and from the area 2 (the western part of Krusne hory) (Figure 5a–c). This trend corresponded very well with the lowest air pollution load (SO2 and NOx emissions) in these areas (Table 1). Figure 4b represents the classification of trees according to their location and shoot growth category. Stabilized shoot growth characterized the trees from relatively healthy areas 1 (77 per cent of all trees) and 2 (45 per cent). The highest proportion of trees with decreased shoot growth characterized the relatively healthy area 2 (40 per cent) in comparison with 2 per cent of trees with decreased shoot growth from area 1. This may have indicated a previsual worsening of a crown status, which was recorded on a visible level in this area during the following season (1999) as a massive needle yellowing. In 1998, standard forestry measurements, such as TDC, defoliation or needle retention, did not reflect those initial previsual changes.
|
The highest levels of pollutants (frequently more than double of those measured in area 2 and three to five times of those measured in area 1) were recorded prior to the present study in areas 3 and 4 located in the central part of the Krusne hory Mts (Table 1). Spruce forests in both areas 3 and 4 were heavily damaged in the past and found to be seriously defoliated in 1998 (Figure 5a). The proportion of chlorotic trees was higher than 60 per cent and needle retention was low, indicating a high intensity of degradative processes in the crown (Figure 5b,c). The proportion of trees which revealed accelerated shoot growth was high in comparison with areas 1 and 2 and reached 40 and 50 per cent, respectively (Figure 4b). This indicated a massive forest recovery in the region of central Krusne hory (areas 3 and 4) which had been heavily damaged by air pollution in the past.
|
Discussion |
|---|
|
TopSummaryIntroductionMaterials and methodsResultsDiscussionConclusionsAcknowledgementsReferences |
|---|
Bud development types – a new marker of tree damage/recovery
Crown defoliation as a macroscopic stress indicator is a projection of the tree crown status from past years of growth, corresponding to needle retention, although this can be misleading when attempting to evaluate current crown development (Salemaa and Jukola-Sulonen, 1990; Dobbertin and Brang, 2001). Often, particularly in very stressed environments such as long-term exposure to air pollution, defoliation determined as very high may not account for recent recovery processes. Therefore, the use of bud condition now allows the analysis of current regenerative processes, and could be a useful tool in forestry management practises. In addition, the determination of tree decline and recovery processes can be used for selection of either resistant trees for propagation or trees susceptible to stress for removal.
The proportion of bud development types determined in young shoot-age classes reflects the potential for crown recovery by secondary shoot formation and corresponds to the current intensity of primary shoot formation (Polák et al., 2004). According to this criterion, we have separated three categories of shoot growth corresponding to the intensity and potential of recovery processes. Both accelerated and decreased shoot growth categories are characterized by low regenerative growth potential for secondary shoot formation. However, they differ in the intensity of primary shoot formation, which is higher for trees with accelerated shoot growth, and in the proportion of aborted buds, which is higher for trees with decreased shoot growth. Trees with stabilized shoot growth are characterized by a high growth capability to replace potential foliage loss in the future by differention of secondary shoots.
Physiological processes of shoot differentiation
Trees with low biomass of assimilative organs and occurrence of needle chlorosis are unable to produce sufficient amounts of carbohydrates to supply all tree sinks. When we consider the assumption of sink/source hypothesis, our finding, that 77 per cent of heavily defoliated Norway spruce trees (crown defoliation 50–69 per cent) exhibited accelerated shoot growth, can be expected since the amount of carbohydrates available for allocation is limited and shoot growth is the primary sink for assimilates (Cline and Deppong, 1999; Schreuder and Brewer, 2001). The buds containing apical meristems belong to the most important primary plant sinks (e.g. Svobodová et al., 2000) and highly defoliated trees cannot afford buds to be unused for a shoot growth. Allocation to ‘low priority’ carbon sinks would depend on what is remaining from the shoot growth processes (Herms and Mattson, 1992; McKinnon and Quiring, 1998). For highly defoliated trees, the allocation to defence compounds, wood production (Solberg and Moshaug, 1999; Blundell and Peart, 2001) and production of reproductive structures (Kaitaniemi et al., 1999) is reduced. As noted in Results, non-significant interaction of factors TDC and area suggests that the intensity of primary shoot formation increased and the potential to form secondary shoots decreased with higher tree damage, regardless of the area of location and the corresponding air pollution load. Therefore, the conclusion can be drawn that the above statement seems to be a general pattern of tree response to high crown defoliation.
The heavily defoliated trees with accelerated shoot growth belong to resilient trees, which are defined by Begon et al. (1990) as organisms that are able to survive damage in disrupted environment. The heavily defoliated trees with decreased shoot growth are susceptible to environmental factors since they have poor primary shoot production and low capability to form secondary shoots and may not be able to replace needle loss. The most sustainable strategy for mature trees seems to be stabilized shoot growth, which may optimize resource-use efficiency and other attributes associated with long-term survival, wood production and reproductive success. Simultaneously, the trees with stabilized shoot growth maintain a high capability of tree recovery via crown regeneration from secondary shoots.
Zvereva and Kozlov (2001) found that crown recovery through differentiation of both primary and secondary shoots was a common compensatory response to high defoliation in unpolluted sites but not in polluted sites that the authors explained as weakened apical dominance. According to our results, trees in heavily polluted areas 3 and 4 did not exhibit lowered intensity of primary shoot growth and/or decreased growth potential to form secondary shoots. However, our findings are not necessarily in disagreement with the findings of Zvereva and Kozlov (2001). Physiological mechanisms underlying weakened apical dominance caused by higher pollution load may result from the higher activity of soluble peroxidases which may be involved in the oxidation of indoleacetic acid (Whitmore, 1976), a main growth hormone involved in apical dominance. In our case, the activity of soluble peroxidases was found to be significantly higher in needles from polluted sites located in areas 3 and 4 (Soukupová et al., 2000), and thus may have reduced auxin concentrations in plant tissues. Another reason could be that at the time of observation (1998) the pollution load was much lower than during the peak loads in the 1980s and it could have been too low to weaken apical dominance and therefore did not result in lower intensity of primary shoot formation. We also found that the rate of bud abortions was very low for trees in polluted areas 3 and 4 which is another explanation for the observed high shoot growth intensity in those areas. The other explanation is through reduced competition for light in polluted sites (Cline, 1991), caused by higher defoliation and tree mortality.
Spruce decline and recovery processes along the gradient of air pollution load
Stabilized shoot growth was typical for healthy to mildly defoliated trees from the low polluted, relatively undisturbed area 1 (Sumava Mts). Only 2 per cent of trees from area 1 revealed decreased shoot growth. Generally, low TDC and needle discoloration values and high needle retention in this area indicated a relatively healthy forest ecosystem in 1998. In contrast, 40 per cent of trees revealed decreased shoot growth for area 2 from the western Krusne hory Mts with equal and/or lower TDC values, needle discoloration and needle retention compared with trees from area 1. In contrast to the stands from areas 3 and 4, the stands from area 2 did not exhibit forest dieback back in times of peak air pollution loads. Trees with decreased shoot growth are characterized by high bud abortion and a low proportion of viable buds with growth potential. The poor physiological state of bud meristems observed in 1998 might have been a preliminary symptom of the worsening of the physiological state of trees, expressed on the macroscopic level as massive needle yellowing, which appeared in this area during the following spring (1999). This symptom of needle yellowing was later identified as due to a chronic impact of stress factors (e.g. 
rámek et al., 2003). The accumulation of pollutants, exhaustion of the self-regulation capacity of older trees and destabilization of sensitive spruce monoculture ecosystems were the causes which led to exceeding the threshold value of stresses. The negative role of environmental stress factors in the physiological state of bud meristems might consist of damage-induced changes in the ability of meristems to compete for resources (Honkanen and Haukioja, 1994). Buds containing apical meristems belong to the most important plant sinks and acidic pollution was found to affect many physiological processes of Norway spruce buds, e.g. changes in contents of non-structural saccharides (Svobodová et al., 2000) and increased activity of non-specific esterase (Soukupová et al., 2002). Damage expressed by altered physiological processes may modify sink strengths either by directly disturbing them or by disturbances to source leaves during sink formation (Honkanen and Haukioja, 1994; Honkanen et al., 1999).
During the 1970s and 1980s, a massive forest dieback was observed in the region of areas 3 and 4 from the central Krusne hory Mts (Pfanz et al., 1994). The stress impact (mainly acidic air pollution) of that region was too high and forest decline leading to forest dieback was observed. No recovery processes in crowns were reported during that time. Since 1995, a strong forest recovery of spruce monocultures has been reported to take place in this region (rámek et al., 2003) following a remarkably sharp decrease in pollution exposure beginning in the early 1990s (http://www.chmi.cz). In 1998, the majority of highly defoliated trees that survived the high stress impact in this heavily polluted region revealed accelerated shoot growth and thus belonged to resilient trees. The recovery processes taking place in crowns were described using bud developmental types, which denoted the majority of trees from areas 3 and 4 to the category of accelerated shoot growth reflecting massive forest recovery (rámek et al., 2003). The standard forestry markers, such as crown defoliation, needle retention and needle discoloration of the trees, still had values typical for previously heavily damaged trees and did not reflect the very recent recovery processes.
The new marker of bud development types described here enabled us to analyse regenerative and degradative processes in crowns. It is a useful tool for forestry management practise and can be used as a prognosis of further development of trees assuming that the current stress impact will not significantly change in the near future. It should be mentioned that such a prognosis would not work well under unexpected extreme stress events. The prognosis for area 2 from the western Krusne hory Mts could be that a continual impact of stress factors will increase crown defoliation. When a loss of assimilative organs exceeds a certain threshold value, the tree usually responds by accelerated shoot growth. Based on our analysis, exceedance of crown defoliation above 30 per cent is the point which corresponds to an increase in primary shoot formation as indicated by the regular to aborted bud ratio and decrease in proportion of buds with growth potential. According to our observations (Polák et al., 2003) and the findings of other authors (Modrzy
ski, 2003; rámek et al., 2003), the defoliation of stands in area 2 has been progressing dramatically since 1998. In the years following 1998, higher defoliation of the trees at this site was followed by more intensive primary shoot formation (Polák et al., 2003). The prognosis for areas 3 and 4 could be that these heavily defoliated trees will continue in accelerated shoot growth, leading either to total tree recovery or to energetic exhaustion and tree death. Our ongoing measurements in 1999–2002 showed that the foliage mass of trees from areas 3 and 4 increased significantly as a result of accelerated shoot growth and improved pollution and climatic conditions (Polák et al., 2003).
|
Conclusions |
|---|
|
TopSummaryIntroductionMaterials and methodsResultsDiscussionConclusionsAcknowledgementsReferences |
|---|
Crown defoliation allows the classification of previous proportional foliage loss in relation to an optimal presence of foliage, but it does not reflect current trends in tree decline and recovery. The proportion of bud development types reacts more quickly to changes in environmental conditions and reliably reflects the ratio of ongoing regenerative or degradative processes in a tree crown. Using the ratio of regular to aborted buds and the percentage of buds with growth potential on 1-year-old shoots allows one to differentiate categories of trees with accelerated, stabilized and decreased shoot growth.
The new macroscopic classification of bud development types, in combination with traditional macroscopic markers of the tree crown status, provides a very promising tool for estimating current growth trends of decline and recovery events of Norway spruce. Because of the simplicity of this method, easily applied under field conditions, it has good practical potential for large-scale monitoring of Norway spruce decline and recovery events.
The crown status of spruce trees in area 1, the Sumava Mts., assessed by shoot growth categories, indicated a healthy forest ecosystem in 1998. The highest proportion of trees with decreased shoot growth was present in area 2, the western Krusne hory Mts., up to this time a relatively healthy area, where tree crown status and physiological state of trees has significantly declined since 1998. Due to a dramatic decrease in air pollution load during the 1990s, heavily defoliated trees in the most polluted areas (3 and 4) from the central part of Krusne hory Mts have started to recover intensively, i.e. to produce new shoots and, thus, they were assigned a category of accelerated shoot growth. Continuing recovery was observed during 1999–2002 in the central Krusne hory (Polák et al., 2003). However, due to changes in soil chemistry and adverse soil conditions induced by some of the highest long-term acidic deposition in the world, it can be expected that stress conditions are going to persist much longer there even though the air pollution load has already decreased remarkably. The local surviving spruce forests are still on or behind the border of ecological stability.
|
Acknowledgements |
|---|
|
TopSummaryIntroductionMaterials and methodsResultsDiscussionConclusionsAcknowledgementsReferences |
|---|
The present research was supported by Grant Agency of the Academy of Science of The Czech Republic (KJB6111307), Grant Agency of the Czech Republic (206/03/H137) and National Aeronautics and Space Administration (NASA) grant (NAG5-5192). Participation of the last two authors during the final paper preparation was covered by a joint U.S.–Czech project (National Science Foundation NSF 108385) and Ministry of Education (ME 658). We also thank Dr Petya Entcheva-Campbell, Shannon Spencer, Ryan Huntley and Sarah Pope formerly from the University of New Hampshire, USA; Dr Jitka Soukupová, Dr Blanka
olcová, Dr Ale Soukup and Dr Radka Malcová formerly students from Charles University, CZ, and other students who participated in the 1998 field research. |
References |
|---|
|
TopSummaryIntroductionMaterials and methodsResultsDiscussionConclusionsAcknowledgementsReferences |
|---|
Albrechtová J. (1997) Development and growth of vegetative buds of Norway spruce (Picea abies /L./Karst.): the effect of acid rain. (Summary of Ph.D. thesis, Charles University in Prague, Czech Republic, (http://www.natur.cuni.cz/
albrecht/)).Begon M, Harper JL, Townsend CR. (1990) Ecology: Individuals, Populations and Communities (Blackwell Scientific Publications, Oxford).
Blundell AG and Peart DR. (2001) Growth strategies of a shade-tolerant tropical tree: the interactive effects of canopy gaps and simulated herbivory. J. Ecol. 89:608–615.[CrossRef]
Brosius G. (1989) SPSS/PC+ Advanced Statistics und Tables-Einführung und praktische Beispiele (McGraw-Hill, London).
Chen Z, Kolb TE, Clancy KM. (2001) Mechanisms of Douglas-fir resistance to western spruce budworm defoliation: bud burst phenology, photosynthetic compensation and growth rate. Tree Physiol. 21:1159–1169.
Cline MG. (1991) Apical dominance. Bot. Rev. 57:318–358.
Cline MG and Deppong DO. (1999) The role of apical dominance in paradormancy of temperate woody plants: a reappraisal. J. Plant Phys. 155:350–356.[Web of Science]
Cudlín P, Novotn
R, Moravec I, Chmelíková E. (2001) Retrospective evaluation of the response of montane forest ecosystems to multiple stress. Ekologia (Bratisl) 20:108–124.
Dobbertin M and Brang P. (2001) Crown defoliation improves tree mortality models. For. Ecol. Manage. 141:271–284.[CrossRef]
Fink S. (1999) Pathological and Regenerative Plant Anatomy. (Borntraeger, Berlin).
Gruber F. (1994) Morphology of coniferous trees: possible effects of soil acidification on the morphology of Norway spruce and Silver fir. In Godbold D and Hüttermann A (Eds.). Effects of Acid Rain On Forest Processes (Wiley-Liss, New York) pp. 265–324.
Halle F, Oldeman RAA, Tomlinson PB. (1978) Tropical Trees and Forests. An Architectural Analysis. (Springer-Verlag, Berlin).
Hejnowicz A and Obarska E. (1995) Structure and development of vegetative buds, from the lower crown of Picea abies. Ann. Sci. For. 52:433–447.
Herms DA and Mattson WJ. (1992) The dilemma of plants: to grow or defend. Q. Rev. Biol. 67:283–335.[CrossRef]
Hintze J. (2001) NCSS and PASS. Number Cruncher Statistical Systems , Kaysville, Utah (http://www.ncss.com).
Honkanen T and Haukioja E. (1994) Why does a branch suffer more after branch-wide than after tree-wide defoliation? . Oikos 71:441–450.[CrossRef][Web of Science]
Honkanen T, Haukioja E, Kitunen V. (1999) Responses of Pinus sylvestris branches to simulated herbivory are modified by tree sink/source dynamics and by external resources. Funct. Ecol. 13:126–140.[CrossRef]
Ishii H, Clement JP, Shaw DC. (2000) Branch growth and crown form in old coastal Douglas-fir. For. Ecol. Manage. 131:81–91.[CrossRef]
Kaitaniemi P, Neuvonen S, Nyyssonen T. (1999) Effects of cumulative defoliations on growth, reproduction, and insect resistance in mountain birch. Ecology 80:524–532.[CrossRef][Web of Science]
Klap JM, Voshaar JHO, De Vries W, Erisman JW. (2000) Effects of environmental stress on forest crown condition in Europe. Part IV: statistical analysis of relationships. Water Air Soil Pollut. 119:387–420.[CrossRef]
Kozlowski TT. (1971) Growth and Development of Trees (Academic Press, New York) pp. 443.
Lepedu H, Cesar V, Ljubeic N. (2001) Chloroplast ultrastructure and chlorophyll levels in vegetative buds and needles of Norway spruce (Picea abies L. Karst.). Period. Biol. 103:61–65.
McKinnon ML and Quiring DT. (1998) Influence of resource availability on growth and foliar chemistry within and among young white spruce trees. Ecoscience 5:295–305.
Müller E and Stierlin H. (1990) Sanasilva Kronnenbilder mit Nedel-und Blattverlustprozenten (Swiss Federal Institute for Forest, Snow and Landscape Research, Birmensdorf).
Modrzyski J. (2003) Defoliation of older Norway spruce (Picea abies /L./ Karst.) stands in the Polish Sudety and Carpathian mountains. For. Ecol. Manage. 181:289–299.[CrossRef]
Moss DM, Rock BN, Bogle AL, Bilkova J. (1998) Anatomical evidence of the development of damage symptoms across a growing season in needles of red spruce from central New Hampshire. Environ. Exp. Bot. 39:247–262.[CrossRef][Web of Science]
Pfanz H and Oppmann B. (1991) The possible role of apoplastic peroxidases in detoxifying the air pollutant sulphur dioxide. In Lobarzewski J, Greppin H, Penel C, Gaspar TG (Eds.). Biochemical, Molecular and Physiological Aspects of Plant Peroxidases (University of Geneva, Geneva, Switzerland) pp. 401–417.
Pfanz H, Vollrath B, Lomsk B, Oppmann B, Hynek V, Beyschlag W, et al. (1994) Life expectancy of spruce needles under extremely high air-pollution stress – performance of trees in the Ore Mountains. Trees 8:213–222.
Polák T, Albrechtová J, Rock BN. (2003) Development of macroscopic markers of Norway spruce damage in the Krusne hory between 1998 and 2000. Ekologia (Bratisl) 22:Suppl 1, 284–287.
Polák T, Albrechtová J, Cudlín P, Moravec I. (2004) Proportion of bud development types – new indicator of current tree health status? Ekologia (Bratisl) 23:Suppl 2, 113–123.
Powell GR. (1974) Initiation and development of lateral buds in Abies balsamea. Can. J. For. Res. 4:458–469.
Salemaa M and Jukola-Sulonen EL. (1990) Vitality rating of Picea abies by defoliation class and other vigour indicators. Scand. J. For. Res. 5:413–426.
Schreuder MDJ and Brewer CA. (2001) Persistent effects of short-term, high exposure to chlorine gas on physiology and growth of Pinus ponderosa and Pseudotsuga menziesii. Ann. Bot. 88:197–206.
Shimizu-Sato S and Mori H. (2001) Control of outgrowth and dormancy in axillary buds. Plant Physiol. 127:1405–1413.
Solberg S and Moshaug E. (1999) Crown condition of Norway spruce: within-stand relationships and competition. Forestry 72:329–336.
Soukupová J, Cvikrová M, Albrechtová J, Rock BN, Eder J. (2000) Histochemical and biochemical approaches to the study of phenolic compounds and peroxidases in needles of Norway spruce (Picea abies). New Phytol. 146:403–414.[CrossRef]
Soukupová J, Albrechtová J, Svobodová H, Opatrná J. (2002) Anatomical and histochemical changes of Norway spruce buds induced by simulated acid rain. Biol. Plant. 45:77–84.
Straw NA, Fielding NJ, Green G, Price J. (2000) The impact of green spruce aphid, Elatobium abietinum (Walker), and root aphids on the growth of young Sitka spruce in Hafren Forest, Wales: effects on height, diameter and volume. For. Ecol. Manage. 134:97–109.[CrossRef]
rámek V, Fadrhonsová V, Lomsk B. (2003) Liming and fertilizing of forest ecosystem in Czech Republic during 2000–2004. Lesnická práce 4:184–186 [In Czech].
Svobodová H, Lipavská H, Albrechtová J. (2000) Non-structural carbohydrate status in Norway spruce buds in the context of annual bud structural development as affected by acidic pollution. Environ. Exp. Bot. 43:253–265.[CrossRef][Web of Science][Medline]
Viskari EL. (2000) Epicuticular wax of Norway spruce needles as indicator of traffic pollutant deposition. Water Air Soil Pollut. 121:327–337.
Vogelmann AF and Rock BN. (1988) Anatomy of Red spruce needles from forest decline sites in Vermont. Environ. Exp. Bot. 28:19–26.[CrossRef][Web of Science]
Whitmore FW. (1976) Binding of ferulic acid to cell walls by peroxidases of Pinus elliottii. Phytochemistry 15:375–378.[CrossRef]
Zvereva EL and Kozlov MV. (2001) Effects of pollution-induced habitat disturbance on the response of willows to simulated herbivory. J. Ecol. 89:21–30.
Received 1 April 2005.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||