cph001 (to/d) 12/1/04 3:16 pm Page 1 The effect of cork-stripping damage on diameter growth of Quercus suber L. A. COSTA*, H. PEREIRA AND A. OLIVEIRA Instituto Superior de Agronomia, Departamento de Engenharia Florestal, Tapada da Ajuda, 1349-017 Lisboa, Portugal Corresponding author. E-mail: [email protected] Summary The Mediterranean cork oak (Quercus suber L.) agro-forestry system is oriented towards cork production, with cork being extracted from tree stem and branches as planks by cutting with an axe and stripping off. The effect of damage to the tree during cork stripping was studied in cork oaks, weakened by wounding, by following the diameter growth and its seasonality during a 9-year production cycle, and comparing them with healthy cork oaks. Tree wounding decreased diameter growth during the following cycle, e.g. 8.5 mm a–1 and 9.8 mm a–1 for weakened and healthy trees, respectively, mostly in the 2 years immediately following the cork stripping. The beginning of annual growth in spring and the occurrence of the highest increments in June–August were delayed by about 1 month in the weakened trees. The cork produced by weakened trees was reduced by 13 per cent in thickness, with average cork ring widths of 3.3 mm a–1 vs. 3.8 mm a–1 for healthy trees. Introduction The cork oak (Quercus suber L.) is the dominant species of the ‘montado’ agroforestry system prevailing in the south-western part of the Iberian Peninsula (726 000 ha in Portugal and 510 000 ha in Spain). Typically an open forest (50–150 trees ha–1), this complex ecological system is economically sustained by the production of cork. Cork oak sylviculture is oriented towards the periodical removal of the cork. The thick cork layer that covers the tree stem and branches is removed up to a certain level (2–3 m or more, depending on tree size) for the first time when the © Institute of Chartered Foresters, 2004 tree is about 25 years of age (and a circumference over bark at breast height >70 cm), and then subsequently at periodical intervals, usually 9 years. The removal of cork (stripping) is made from May to August, when the physiologically active, swollen and thin phellogen and the newly differentiated cork cells allow an easy rupture and separation of the tissues. The cork is removed as large rectangular planks (1–1.3 m long, 0.4–0.6 m wide) with a special axe by cutting first horizontally around the tree stem and then vertically, and by prying them off with the axe handle. The operation is rather demanding of the skills of the worker: sufficient strength has to be applied to the axe to cut Forestry, Vol. 77, No. 1, 2004 cph001 (to/d) 12/1/04 3:16 pm Page 2 2 F O R E S T RY through the hard phloem tissues that cover externally the cork planks (the cork ‘back’) and the underlying cork layer, but stopping at the phellogen or going only very slightly into the inner bark. In fact, the traumatic phellogen will be regenerated at some depth in the phloem and deep cuts will induce wound responses and a loss of uniformity in the suberous tissue that will be formed subsequently (Graça and Pereira, 2003). The consequence of a cut that penetrates down to the cambium is severe, with loss of cork production in that area for several years until the wound has healed. The effect of cork stripping on tree health and growth has always been a concern for the sustainable management of the system (Natividade, 1938; Correia et al., 1992; Wargo, 1996; Pereira et al., 1999). In addition to the danger of wounding, cork stripping causes a large water loss from the stripped surface (Natividade, 1938; Santos, 1940; Correia et al., 1992) that may induce a decrease in diameter growth (Luque et al., 1999) and enhance additional stresses and susceptibilities (Natividade, 1938; Werner, 1995). In the Mediterranean cork oak forest, susceptibility to attack by fungi (e.g. Hypoxylon mediterraneum) increases when the tree suffers from water stress (Macara, 1974; Luque et al., 1999). These concerns have led to regulation of cork production practices, e.g. in Portugal, stripping height must not exceed three times the stem perimeter at breast height in mature trees and the minimum period between cork extractions must be 9 years. When trees are weak or damaged it is also usual practice to decrease the cork stripping level or to increase the cork production cycle. We studied the effect of tree damage on radial growth by following the diameter growth and its seasonality, during a 9-year production cycle, in cork oaks weakened by wounding during the previous stripping and in healthy cork oaks. The objective was to evaluate the impact of damage caused by cork removal on subsequent tree growth and losses of cork production in the following production cycle. Materials and methods The study was conducted in a typical cork oak stand under cork production with a 9-year cycle, characterized by a density of 67 trees ha–1, 3.2 m2 ha–1 basal area and a mean circumference at breast height of 1.0 m. As regards cork production parameters, maximum height of debarking is on average 1.8 m, total surface of debarking 1.8 m2 tree–1, cork yield 10 kg m–2 of stripped area and annual cork production 900 kg ha–1. A detailed study of this stand is given in Sousa (1997). The study area is located in the south-west of Portugal in the region of Benavente (38° 46′ N, 8° 45′ W) with a Mediterranean-type climate with some Atlantic influence: mean annual temperature 15.5°C, annual precipitation 644 mm and a dry period from May to September. During the study period (1991–2000) the mean temperature was 17.6°C and the average annual precipitation 595 mm with below average rainfall in 1993 and 1995 (575 mm and 550 mm, respectively). After cork stripping in June 1991, a total of 50 healthy cork oak trees were randomly selected in a 7000 m2 plot and manual band dendrometers (model D1; UMS GmbH, Munich, Germany) were installed at breast height (1.30 m above ground) on the debarked stem. During the 9 years of the production cycle (June 1991 to June 2000) monthly measurements were made. This period includes eight complete years of tree growth (1992–1999). Before the cork extraction in June 2000, the tree conditions were evaluated using as analysis parameters crown defoliation and the presence of wounds that could be recognized as having originated from the previous cork stripping and of visible necrosis and deterioration of sapwood tissues. The trees were classified as weakened when they showed 50–75 per cent or more crown transparency and presented wounds, scars or necrosis larger than 15 cm 5 cm (length width) in stem or branches representing >5 per cent of the debarking stem surface. The extent of damage varied from cuts that went deep into the phloem but with limited dimensions (Figure 1a) to large wounds with destruction of the cambium by the removal of the inner bark (Figure 1b). The weakened condition of the trees was confirmed during the cork stripping by the fact that the extraction of the cork planks was more difficult. A total of 10 trees were classified as weak or damaged. cph001 (to/d) 12/1/04 3:16 pm Page 3 EFFECTS OF CORK-STRIPPING DAMAGE ON QUERCUS SUBER a. b. 3 At the previous cork extraction in 1991 and in June 2000, field measurements were made in relation to breast height diameter, total tree height, crown area, stripping height, total stripped surface and cork production. The stripping coefficient was calculated as the ratio of the maximum stripping height and the perimeter at breast height. The cork productivity was calculated per tree as a cork yield produced by unit area of stripped surface (k gm–2). A cork sample with dimensions 20 20 cm2 was taken, during the cork extraction of 2000, at breast height and used to measure cork thickness, ring width for the eight complete years (1992–1999) and porosity. Porosity, a quality parameter of cork, was measured as a porosity coefficient (area of pores as a percentage of total area) using image analysis of the transverse section, as previously described by Pereira et al. (1996). The non-cork growth during the eight complete years of the cork production cycle that includes the wood growth, external phloemic tissues, phelloderm and two mid-years of cork growth, was calculated for each tree based on the difference between the total annual growth (measured with the band dendrometer) and the total cork ring width, measured in the cork sample collected at breast height. For comparison of the diameter growth, a sample of 10 healthy trees with similar dendrometric characteristics in June 1991 to those classified in 2000 as weak or damaged, including their cork stripping parameters was selected (Table 1). Initial differences between weakened trees and healthy trees with respect to diameter over and under cork, cork stripping coefficient and cork stripping height were compared using a t test. Differences of total and annual diameter increases between weakened and healthy trees were statistically assessed using t tests. In addition, an analysis of variance was made for the annual diameter increase using a KruskalWallis one-way analysis of variance on ranks. Results Figure 1. Some examples of wounds, scars and necrosis caused by cork stripping in the stem and branches of weakened trees. Initial condition In 1991, there were no significant differences (P = 0.05) between the 10 trees classified in 2000 cph001 (to/d) 12/1/04 3:16 pm Page 4 4 F O R E S T RY Table 1: Characterization of the weakened and healthy cork oak trees in relation to tree and cork parameters (1991 and June 2000) Parameters Weakened trees Healthy trees 49.0 ± 12.9 43.3 ± 12.4 48.9 ± 12.9 45.1 ± 12.0 11.2 ± 2.0 2.1 ± 0.4 97.3 ± 55.4 2.7 ± 0.8 1.8 ± 0.4 4.6 ± 2.3 53.1 ± 10.1 42.6 ± 10.5 50.6 ± 11.4 44.2 ± 10.5 10.9 ± 2.8 2.9 ± 1.1 89.9 ± 45.0 3.0 ± 0.7 1.9 ± 0.4 5.2 ± 1.9 1991 over cork d.b.h. (cm) 1991 under cork d.b.h. (cm) 2000 over cork d.b.h. (cm) 2000 under cork d.b.h. (cm) Total height (m) Stem height (m) Crown area (m2) Cork stripping height (m) Cork stripping coefficient Total cork stripping surface (m2) Values are mean of 10 trees and standard deviation. Table 2: Annual diameter increase (cm) for the eight complete years of growth in the cork production cycle for weakened and healthy cork oak trees Years Weakened trees Healthy trees 1.09 ± 0.30 0.70 ± 0.27 1.26 ± 0.32 0.60 ± 0.32 1.01 ± 0.20 1.00 ± 0.23 0.78 ± 0.32 0.36 ± 0.24 6.78 ± 1.25 0.85 ± 0.16 1.52 ± 0.27 0.96 ± 0.20 1.30 ± 0.31 0.71 ± 0.22 1.09 ± 0.20 0.96 ± 0.23 0.81 ± 0.23 0.52 ± 0.19 7.86 ± 1.19 0.98 ± 0.15 1992 1993 1994 1995 1996 1997 1998 1999 1992–1999 Annual average Values are mean of 10 trees and standard deviation. as healthy and those classified as weak or damaged in breast height diameter, cork production and stripping height. Diameter growth In the 9-year production cycle, both weakened and healthy trees showed positive annual growth increments in diameter but the total diameter growth was smaller for the weakened trees than for healthy trees (6.96 1.27 cm and 8.08 1.23 cm, respectively). However, between-tree variability was large and the difference was not statistically significant (P > 0.06). Considering only the eight years with complete growth (Table 2), the diameter increase was also smaller for the weakened trees than the healthy trees (6.78 1.25 cm and 7.86 1.19 cm, respectively). Along the production cycle the diameter growth showed a decreasing trend that was very similar in all trees (Table 2), with smaller increments in the final years. In 1993 and 1995 the diameter increase was exceptionally low. The average annual diameter increment in the eight years of complete growth that are included in the cork production cycle was 9.8 1.5 mm a–1 for healthy trees and 8.5 1.6 mm a–1 for weakened trees (Table 2). The annual growth of healthy trees was higher than the growth of weakened trees for all years with the exception of 1997 with a similar value for the two groups. Only the difference in growth for the first two cph001 (to/d) 12/1/04 3:16 pm Page 5 EFFECTS OF CORK-STRIPPING DAMAGE ON QUERCUS SUBER 5 Table 3: Characterization of cork production of weakened and healthy cork oak trees Parameters Weakened trees Healthy trees 48.7 ± 26.6 28.2 ± 4.4 10.4 ± 5.3 9.9 ± 1.9 59.2 ± 24.2 33.5 ± 5.2 9.9 ± 4.5 11.5 ± 2.0 Cork green weight (kg tree–1) Thickness (mm) Porosity (%) Cork yield (kg m–2) Values are mean of 10 trees and standard deviation. years in the cycle (1992 and 1993) was larger and statistically significant (P = 0.003 and P = 0.042, respectively). Cork production Cork production was on average lower in the weakened trees in comparison with the healthy trees but the between-tree variation is high with coefficients of variation of the mean of 34 per cent and 55 per cent, respectively, for healthy and for weakened trees, and the difference was not statistically significant (P = 0.373). The cork yield, measured as the cork weight per unit debarked surface, was on average 14 per cent lower in the weakened trees (9.9 1.9 kg m–2 as compared with 11.5 2.0 kg m–2 for healthy trees) but the difference was not statistically significant. The total thickness of cork obtained from the weakened trees was reduced in comparison to healthy trees on average by 16 per cent and this difference was statistically significant (P = 0.017). The quality of cork, measured as its porosity, was similar for both groups of cork oaks (Table 3). Cork and ‘wood’ growth The growth of cork is the main component in the total diameter increase of cork oaks representing on average 77.3 per cent and 78.9 per cent, respectively, in weakened and healthy trees. The inter-annual variation of cork ring width showed a pattern similar to the radial growth, with an overall decreasing trend (Figure 2). On average for the 8-year cycle, the cork ring width was smaller in the weakened trees than in the healthy trees (3.3 0.5 mm a–1 and 3.8 ± 0.4 mm a–1, respectively) but between-tree variability was important and the difference was not statistically significant. Annually, the growth of cork was higher in the healthy trees during the first 5 years of the cycle, e.g. in the first and second years (1992 and 1993) cork increased 4.8 mm and 3.9 mm in healthy trees and 3.5 mm and 2.9 mm in the weakened trees, and remained practically the same in the last 3 years of the cycle (Figure 2). The average non-cork growth (or ‘wood’ growth) of weakened and healthy trees (Figure 2) was similar in most of the years and the small differences found for 1992, 1994 and 1995 were not statistically different (P < 0.05). Seasonal pattern of diameter growth The diameter growth showed a seasonal pattern for all trees in the eight years of the cycle with a clearly marked growth period followed by a period without diameter increments. Growth begins in March and extends to October with the highest increments in June–August (Figure 3). However, the beginning of annual growth and the occurrence of the highest increments were not simultaneous in healthy and weakened trees. The onset of growth was delayed by ~1 month in the weakened trees while maintaining the same pattern of radial increments subsequently (Figure 3), thereby also delaying the growth peaks by approximately the same time period. A comparison made between the growth patterns of the weakened trees showed that those with a higher extent of damage more clearly expressed the later growth onset (Figure 4). Discussion The cork oaks that were classified as weakened after one cork production cycle showed a 12/1/04 3:16 pm Page 6 6 F O R E S T RY 8.0 7.0 Weakened (cork) Healthy (cork) Weakened (wood) Healthy (wood) Annual growth (mm) 6.0 5.0 4.0 3.0 2.0 1.0 0.0 1992 1993 1994 1995 1996 1997 1998 1999 Figure 2. Cork ring width (mm) and annual growth of ‘wood’ (mm) during eight complete years of the cork production cycle for weakened and healthy cork oak trees. Mean of 10 trees and half of standard deviation. 4.5 Monthly diameter increments (mm) 4.0 Healthy trees increment 3.5 Weakened trees increment 3.0 2.5 2.0 1.5 1.0 0.5 Nov-99 May-99 Nov-98 May-98 Nov-97 May-97 Nov-96 May-96 Nov-95 May-95 Nov-94 May-94 Nov-93 May-93 Nov-92 May-92 0.0 Nov-91 cph001 (to/d) Figure 3. Average monthly diameter increments (mm) for healthy and weakened trees for the period of eight complete years of the cork production cycle. diameter growth that followed the previously reported pattern for mature cork oaks, namely a decreasing trend along the cycle (Costa et al., 2001). In addition, the below average rainfall in the previous winter 1992/1993 and 1994/1995 reduced the cork growth in 1993 and 1995 (Caritat et al., 2000; Costa et al., 2001). The empirical arguments that cork oak radial growth decreases in trees weakened from a bad stripping (Natividade, 1950; Correia et al., 1992) were confirmed by the results obtained, the increase in diameter after one production cycle was smaller (by 14 per cent) than in the healthy cork oaks used for comparison, although the cph001 (to/d) 12/1/04 3:16 pm Page 7 EFFECTS OF CORK-STRIPPING DAMAGE ON QUERCUS SUBER 7 Monthly diameter increments (cm) 0.50 Heavy damaged Lightly damaged 0.40 0.30 0.20 0.10 0.00 Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Month Figure 4. Monthly diameter increments (cm) for the year 1992–1993 of six weakened cork oaks with two different degrees of damage. difference was in the range of between-tree variation and therefore not statistically significant. If the annual growth increments are compared (Table 2), it can be seen that they were reduced in the weakened trees, mainly in the first two years of the production cycle, which showed a statistically significant reduction in growth of ~30 per cent. It seems therefore that the influence of the cork stripping damage on radial growth is immediate in the two subsequent years. Since damage extent was highly variable, as shown in Figure 1, it would be expected to have different reaction intensities from individual trees. This was the case and the between-tree growth variability was higher in the weakened trees than in the healthy trees, i.e. the coefficient of variation of the mean annual growth in the first and second years of the cycle was 28 per cent and 39 per cent for weakened trees and 18 per cent and 21 per cent for healthy trees. The main component of diameter growth refers to the increase in cork thickness, which is known to represent ~80 per cent of total diameter increments (Costa et al., 2001). Therefore, in agreement with the differences in total diameter increase between weakened and healthy trees, the cork thickness obtained from weakened trees was 16 per cent less. However, this reduction in cork growth was not uniform along the cork cycle, and it could be observed that the cork rings were smaller in the weakened trees only in the first half of the cycle and similar in the second half (Figure 2). The activity of the newly formed traumatic phellogen after the cork stripping was thereby reduced as a tree response to wounding. It is known that traumatic phellogens have an enhanced meristematic activity in the years immediately following their formation, thereby originating wider cork rings in the first years of the production cycle (Pereira et al., 1992; Ferreira et al., 2000). Tree wounding seemed therefore to reduce this increased activity of the phellogen in its first years of age. In agreement, the increment of the non-cork component of diameter growth (of wood, if the formation of phloem and pheloderm is disregarded) did not show a consistent decrease in the weakened trees, except for the first year after the cork stripping (Figure 2). The seasonality of radial increase was also influenced by the cork stripping damage, with weakened trees showing about 1 month delay in the onset of spring growth and the occurrence of increment peaks (Figure 3), the effect being higher for the more extensive damage (Figure 4). This response of cork oaks to stress was previously reported regarding the influence of adverse environmental factors on the timing of cph001 (to/d) 12/1/04 8 3:16 pm Page 8 F O R E S T RY phenological events (Pereira et al., 1987; Oliveira et al., 1994; Oliveira, 1995) as well as of cork stripping on bud burst and radial increments (Fialho et al., 2001). Of the initial sample of 50 healthy cork oak trees in 1991, 20 per cent were classified as weakened due to stem wounding after one cork production cycle. Although the experiment was not designed ab initio to study the incidence of decline diseases with time and no conclusions are to be drawn on this matter, it is nevertheless noteworthy that a significant number of trees showed consequences of the previous cork stripping. This calls attention to the need of careful cork extraction procedures as frequently stressed in the past by different authors (Natividade, 1950; Pereira et al., 1999). In conclusion, the operation of cork stripping could represent a potential danger of tree wounding that will reduce tree diameter and cork growth, especially in the years immediately following the injury. Although cork oaks survive many years despite suffering continuous harm by stripping and consequent biotic attacks (Natividade, 1950), their longevity as productive trees will depend on the protection mechanisms they develop. Expertise and careful cutting procedures in cork stripping are therefore essential elements to guarantee the sustainable management of cork oaks in cork production. References Caritat, A., Gutierrez, E. and Molinas, M. 2000 Influence of weather on cork-ring width. Tree Physiol. 20, 893–900. Correia, O., Oliveira, G., Martins-Loução, M. and Catarino, F. 1992 Effects of bark-stripping on the water relations of Quercus suber L. Scient. Gerundensis 18, 195–204. 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