- Email: [email protected]
Dead wood creation and restoration burning: Implications for bark beetles and beetle induced tree deaths
Forest Ecology and Management 231 (2006) 205–213 www.elsevier.com/locate/foreco
Dead wood creation and restoration burning: Implications for bark beetles and beetle induced tree deaths Miikka Eriksson a,b,*, Saara Lilja c, Heikki Roininen a a
University of Joensuu, Department of Biology, P.O. Box 111, FIN-80101 Joensuu, Finland b Finnish Forest Research Institute, P.O. Box 68, FIN-80101 Joensuu, Finland c University of Helsinki, Faculty of Agriculture and Forestry, Department of Forest Ecology, P.O. Box 27, 00014, Finland Received 13 February 2006; received in revised form 4 May 2006; accepted 17 May 2006
Abstract Dead wood creation is an important tool for restoring the natural characteristics of boreal managed forests, where the amount of dead wood has seriously declined as a result of forest management practices. Although many forest species would benefit from restoration, foresters are concerned about the increased risk of bark beetle attacks on surrounding managed forests. In our study, we investigated whether the number or size of dead wood created affects the number of bark beetles (Ips typographus and Pityogenes chalcographus) colonizing the felled trees and whether the amount of dead wood and burning treatment after colonization has an effect on I. typographus breeding success and consequential tree deaths in forest borders surrounding restoration areas. The experimental restoration of Norway spruce dominated stands included partial cuttings with three levels of down wood retention (DWR) (5, 30, and 60 m3 ha1) and a burn/non-burn treatment (3 2 factorial) with three replicates of each treatment combination. An increase in the total number of down wood retention spruces (DWRS) decreased the proportion of trees colonized by I. typographus, but increased the total number of colonized trees. P. chalcographus colonized almost 100% of felled spruces. The total number of I. typographus egg galleries was best explained by the interaction of the number and mean diameter of DWRS. According to the models constructed the experimental areas with great numbers of large spruces harbor the most I. typographus egg galleries, while stands with the same number of smaller trees almost totally lack egg galleries. The number of P. chalcographus mating chambers increased along with an increase in the number of DWRS. Burning treatment diminished the breeding success of I. typographus, especially at the highest DWR level, where the intensity of fire was also the highest. Instead of relatively extensive colonization by I. typographus and P. chalcographus, numbers of tree deaths at forest edges surrounding restoration areas were overall very low, and therefore no significant predictors were found. This study shows that the number and size of damaged trees affects the number of bark beetles colonizing the restoration area. However, in Finland the risks of restoration projects of this magnitude, at least when I. typographus populations are at endemic levels, are rather low. # 2006 Elsevier B.V. All rights reserved. Keywords: Bark beetles; Ips typographus; Picea abies; Restoration; Dead wood; Burning
1. Introduction Artificial dead wood creation is in many respects comparable to leaving wind-damaged trees in forests and involves its own risks as regard to forest health in nearby areas. The increasing number of wind-felled spruces has been shown to attract more colonizing individuals of the European spruce bark beetle (Ips typographus L.) (Coleoptera: Scolytidae), which is practically the only significant bark beetle pest affecting mature
* Corresponding author. Tel.: +358 10 211 3269; fax: +358 10 211 3251. E-mail address: [email protected] (M. Eriksson). 0378-1127/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2006.05.050
Norway spruce (Picea abies (L.) Karst.) in Finland, into the damage area (Eriksson et al., 2005) and to correlate positively with the number of living trees killed in windthrow areas (Schroeder and Lindelo¨w, 2002). Even though I. typographus is a serious forest pest it also creates new breeding material for a variety of insect species. Dead and decaying wood, including trees killed by I. typographus, constitute a habitat for a large number of harmless species (Esseen et al., 1997; Jonsell et al., 1998; Siitonen, 2001). Unfortunately, partly due the fear of I. typographus attacks and the consequent high standards of forest hygiene, the amount of dead wood in managed forests has been seriously reduced (Fridman and Walheim, 2000; Siitonen, 2001). At
206
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
present, the average volume of dead wood in the managed forests of southern Finland is from 1.2 to 2.9 m3 ha1 (Tomppo et al., 1999) while natural forest in the same areas have on average 60–90 m3 ha1 of coarse woody debris (Siitonen, 2001). However, the volume of dead wood in natural stands could be even higher after stand-replacing disturbance or when the fire return interval is very long (Siitonen et al., 2000). Consequently, the creation of dead wood in managed forests is an essential tool for forest restoration, in order to rehabilitate important stand structures, processes, and species composition in ecosystems altered by human action (Bradshaw, 1997; Anon, 2003; Kuuluvainen et al., 2005). In Finland the goal during the years 2003–2012 is to restore about 33,000 ha of state owned land (Anon, 2002). In forest areas this includes artificial creation of dead wood (10,430 ha), small gap creation (5210 ha) and burning of 160 tracts of forest (960 ha). Although the total area of forest restoration operations per year is fairly low, each restoration treatment has its own effect on the surrounding managed forests, and this should be taken into account before operations are started. However, there are no studies on the effects of down wood retention level, with more than five cut trees (Hedgren et al., 2003), on bark beetles or on surrounding forests. Neither have the effects of fire on I. typographus breeding or consequential tree deaths been studied earlier. Therefore, there is a need for experimental studies that consider the insect induced risks involved in forest restoration projects. I. typographus breeds commonly in wind-felled trees, large diameter logging waste, and sometimes also in solitary living trees, which they may kill on the edges of clear-cut areas (Peltonen, 1999; Hedgren et al., 2003). For successful breeding in living trees, a high number of colonizing beetles is needed to overcome the defensive systems of the trees (e.g. Mulock and Christiansen, 1986). Such an increase in population levels is possible, for example, after heavy windstorms, when there is a surplus of breeding material with low or no resistance at all. Thus, extensive storm damage may lead to I. typographus outbreaks and consequential damages to living trees (e.g. Saalas, 1949; Lekander, 1972; Schroeder, 2001). Damaged spruces also provide a suitable breeding ground for Pityogenes chalcographus (L.), which alone does not seem to impose a risk for healthy spruces (Hedgren, 2004). P. chalcographus may, however, affect I. typographus populations by utilizing partly the same resources as I. typographus. In this study, the risks of restoration operations were investigated. Restoration included partial cuttings with three levels of down wood retention (DWR = trees felled and left on the stand) and a burn/non-burn treatment. A constant volume (50 m3 ha1) of standing retention trees was left in the stands. The main objective of this study was to answer to the following questions: (1) Does the increase in the amount of DWR trees affect the proportion of DWR spruces colonized by bark beetles or the number of egg galleries or breeding chambers in DWR spruces? (2) Does burning treatment, after the colonization of felled spruces, and the increase in the amount of DWR trees affect the breeding success of I. typographus and the number of tree deaths on forest edges surrounding restoration areas?
2. Methods 2.1. Study area and experimental design The study area is located in the southern boreal zone (Ahti et al., 1968) in southern Finland (latitude 618120 –618250 N, longitude 258000 –258150 E). The experimental stands were searched from the data bases of several landowners using the following criteria: mature managed P. abies-dominated stand, area of 1–3 ha, and Vaccinium myrtillus forest type (Cajander, 1926). The stands were selected iteratively by visiting them in the field and accepting them if they fulfilled the criteria. The selected stands were clustered within an area of 26 km 12 km (Fig. 1). Altogether, 18 stands were selected for the experiment. The average age of the stands was 80 years (from 60 to 100 years). All of the stands were managed. Most of the stands fulfilled the criteria for V. myrtillus forest type (MT), but three stands also had some characteristics of the Oxalis Myrtillus forest type (OMT) (Cajander, 1926). The stands were of mixed tree species composition, including Betula pendula Roth, B. pubescens Ehrhart, Populus tremula L., and Pinus sylvestris L. In addition, Sorbus aucuparia L. and Juniperus communis L. occurred in the shrub layer. Although each stand was classified under one forest type for forestry purposes, there was clear small-scale within-stand variation. Accordingly, each stand included an upland and a paludified biotope. The upland biotopes were typically dominant, while paludified biotopes covered smaller patches. Experimental treatments were randomized among the stands. The treatments consisted of three levels of down wood retention (DWR) = trees, including all tree species, felled and left in the stand) and burning treatment (burn/non-burn) (3 2 factorial). Each treatment combination was repeated three times (3 6 = 18). A constant volume of 50 m3 ha1 of standing dispersed retention trees (all tree species included) was left on all the stands, meaning that some of the felled trees
Fig. 1. Locations of experimental stands within the study area.
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
were transported out of the stand. The three levels of DWR were 5, 30, and 60 m3 ha1. The harvestings were carried out using conventional forestry machinery which cut the branches from the stem and spread the logging residues evenly on the forest floor. However, branches from the stems of DWR spruces (DWRS = spruces felled and left in the stand) were left untouched. The restorative cuttings were conducted in February and March 2002 and the burnings during June–August 2002. The burnings were carried out using the traditional Finnish prescribed burning technique (Lemberg and Puttonen, 2003). With this method, ignition lines form a circle around the stand and the burning front advances partly against the wind, which decreases the risk of escape. In addition, extra ignition lines were lit inside the circle. For a detailed description of the experimental stands and the methods used in restoration, see Lilja et al. (2005). 2.2. Insect sampling In July 2003, DWRS were inspected for bark beetle galleries. Although half of the stands were burned after the main swarming period of I. typographus and P. chalcographus, the galleries of both species were visible and countable in most of the inspected spruces. In most DWRS, on burned stands, the bark was only slightly charred and branches were burned. Some of the DWRS were not burned at all. Only a few trees were not qualified for inspection because of burning. A sample of 6–41 DWRS per restoration area (Table 1) was inspected, depending on the amount of available DWRS outside the sample plots (two 30 m 50 m plots on each stand), which were reserved for other uses. Pieces of bark (15 cm 60 cm) were removed and egg galleries and exit holes of I. typographus were counted at
207
1.3 and 4 m, and at intervals of 4 m until the diameter of tree trunk decreased to less than 10 cm. P. chalcographus mating chambers were counted at the same heights from a smaller area (15 cm 15 cm). DWRS were counted in each stand and the inspected spruces were measured for diameter at breast height (1.3 m above the cut point) and at the last inspection height. New dead standing spruces with I. typographus damages on forest edges (0–20 m from the forest edge) directly surrounding experimental stands were counted each autumn in the years 2003–2005. 2.3. Calculations The DWR level, including volumes of Pinus, Picea, and Betula spp., was assessed using the volume equations of Laasasenaho (1982) based on tree diameter at breast height (D1.3) and tree height. The volume of all other deciduous trees was estimated using the equations for Betula. The volumes of DWRS were assessed using the equations based on tree diameter (Laasasenaho, 1982) and cylinder formulae were used to compute the bark area of the inspected trees. For calculating the total number of egg galleries and mating chambers per experimental stand, sampled trunks were divided into sections so that each insect sample represented a section of the tree trunk (sample from 1.3 m represented stem section from 0 to 2.00 m, sample from 4 m represented stem section from 2.01 to 6.00 m, sample from 8 m represented stem section from 6.01 to 10.00 m and so on). Total number of galleries and chambers per tree were obtained by first calculating the number of galleries and chambers per m2, then multiplying the result with the area of the corresponding trunk section and finally summing the
Table 1 Experimental stands, DWR level, stand area, number of inspected DWRS, DWRS characteristics (total number, total volume, and mean D1.3), proportion of colonized trees, the total number of I. typographus (I.t.) egg galleries and P. chalcographus (P.c.) mating chambers, and the number of dead spruces in forest edges Experimental DWR-level Area Inspected DWRS stand (m3 ha1) (ha) DWRS
230 291 552 168 271 496 37 196 617 165B 250B 301B 41B 85B 203B 55B 205B 327B
5 5 5 30 30 30 60 60 60 5 5 5 30 30 30 60 60 60
2.66 1.30 2.16 2.10 1.08 1.31 1.36 2.86 1.09 1.06 1.57 0.78 2.55 0.86 2.15 2.56 3.37 1.65
19 16 13 29 12 41 25 26 22 6 19 16 34 10 25 29 40 28
Proportion Number of of DWRS colonized by
Dead spruces in forest edges
Number Volume (m3) Mean D1.3 (cm) I.t
P.c.
I.t. egg galleries P.c. mating chambers
40 23 15 126 24 162 125 104 53 9 22 16 210 25 75 140 206 147
1.00 0.94 1.00 1.00 1.00 1.00 0.96 0.96 0.95 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00
4050 1765 4674 1133 11303 2096 15001 9821 5234 9442 4856 4931 1426 4074 3208 28296 1278 15539
10.6 6.2 8.3 28.7 10.4 27.4 42.2 44.0 29.4 6.5 5.1 6.0 34.3 13.8 35.0 56.6 38.1 43.1
B after the stand number indicates the burning treatment.
19.7 19.5 26.0 18.8 24.8 16.9 21.9 24.4 25.8 30.2 18.6 23.0 16.3 26.8 25.2 23.3 17.1 20.1
0.37 0.63 0.62 0.24 0.92 0.17 0.80 0.58 0.55 1.00 0.53 1.00 0.09 0.80 0.40 0.55 0.13 0.36
85253 44526 46757 240876 66478 237505 169314 133331 93319 17370 37837 30375 315280 63233 168413 189926 338053 264473
2 0 4 0 5 3 4 0 1 1 0 0 0 0 8 1 0 0
208
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
number of galleries or chambers in each section. The average of the number of egg galleries or mating chambers in sample trees in each experimental stand was taken and multiplied with the total number of DWRS’s to obtain the total number of egg galleries or mating chambers per each experimental stand. The number of egg galleries or mating chambers per hectare was obtained by dividing the total number of galleries or chambers with the size (ha) of the experimental stand. The breeding success (female offspring per mother beetle) of I. typographus was calculated: 0.5 (the number off exit holes/the number of egg galleries). It was assumed that one beetle had left through each exit hole. The data for felled spruces (DWRS) were collected during insect sampling, but the data on other species and standing trees is based on the data collected from the sample plots in each restoration area (see Lilja et al., 2005). 2.4. Statistical analysis The effects of DWR level and burning treatment on the colonization of DWRS and tree deaths on the restoration area forest border were tested. Response variables included the proportion of DWRS colonized (both beetle species separately), the estimated number of I. typographus egg galleries ha1, the estimated number of P. chalcographus mating chambers ha1, the reproductive success of I. typographus and tree deaths on the restoration area forest border. Since burning treatments were carried out after the main swarming period of both bark beetle species, it did not influence (tested as nonsignificant predictor in models concerned with colonization) the colonization of DWRS. Non-burned and burned stands were therefore combined for analyzing the proportions of colonized DWRS and the numbers of egg galleries and mating chambers. Alternative models with more specific continuous predictors were constructed on account of the large variation in the mean D1.3 of DWRS and the size of the restoration areas (Table 1), which meant that DWR level did not give much information about the total number or the size of DWRS. Response variables in these alternative models included the proportion of colonized DWRS (for both beetle species separately), the total number of egg galleries, mating chambers, and tree deaths per restoration area. Predictors included the number of DWRS, the mean diameter (D1.3) of DWRS and the size of the restoration stand (Table 2). Furthermore, the total number of colonized DWRS (I.
typographus) and insect gallery or chamber numbers per stand were included in the alternative analysis of tree deaths (Table 2). Generalized linear models (GLM) were used for the analyses. The proportion of colonized DWRS was analyzed by weighted regression, using the individual sample sizes as weights (Crawley, 2003: p. 513–536). In the model handling the proportion of DWRS colonized by I. typographus, overdispersion was taken into account by using a quasibinomial family with logit link function. Counts of both species on felled spruces had a highly skewed distribution. For this reason quasilikelihood, introduced by Wedderburn in 1974, which uses only the variance–mean relationship of the response variable, was utilized. The link function ‘‘log’’ was used to linearize the response, and the variance function was specified as ‘‘m2’’ (‘‘m’’ as the mean of the distribution) to take into account the increase in variance with the square of the mean (Crawley, 2003: p. 544). Minimal models (i.e. final models with only statistically significant predictors left) were determined by assessing the increase in deviance (the measure of discrepancy in a GLM used to assess the goodness of fit of the model to the data) attributable to the removal of individual predictors through F goodness-of-fit tests comparing the deviance of the models with and without the particular term included (Crawley, 2003). Only the analysis of I. typographus breeding success was conducted using a square root transformed response variable and two-way analysis of variance. Predictors were deemed significant at the P < 0.05 probability level. The analyses were carried out in R (R Development Core Team, 2005). 3. Results The total volume of DWRS per experimental area varied somewhat even within the same DWR-level because of the variation in both the size of the areas and the amount of other tree species. The total number and volume of DWRS per experimental area varied from 9 to 210 and from 5 to 57 m3, respectively (Table 1). There was also variation in the size of DWRS as the mean D1.3 of felled spruces varied from 16.3 to 30.2 cm. Large variation, between areas, was also found in total I. typographus egg gallery and P. chalcographus mating chamber numbers (from 1133 to 28,296 and from 17,370 to 338,053,
Table 2 Predictors (with mean and SD) used in alternative models
Stand area (ha) No. DWRS Mean D1.3 of DWRS No. DWRS colonized No. egg galleries No. mating chambers
Mean
S.D.
1.80 84.56 22.13 31.55 7118 141240
0.77 68.78 3.95 25.09 6951 103207
Stand area, no. DWRS and mean D1.3 were used in all five models. No. DWRS colonized by I. typographus, no. egg galleries (I. typographus), and no. mating chambers (P. chalcographus) were used only in the model concerning tree deaths in forest edges.
Fig. 2. Tree deaths on forest edges surrounding experimental areas in 2003– 2005. Burned stands are marked with the letter B after the site number.
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
Fig. 3. The proportion (S.E.) of DWRS colonized by I. typographus and P. chalcographus at three DWR levels.
respectively) (Table 1). The mean I. typographus egg gallery density per m2 of colonized bark was overall rather low, varying from 18.1 to 96.0 (mean 50.9 4.8) and correlated negatively with the number of DWRS (Pearson, r = 0.55, P = 0.02). The breeding success of I. typographus varied from 3.5 to 11.5 (mean 6.1 0.9) female offspring per egg gallery in sites with no burning and from 0.3 to 3.0 (mean 1.7 0.3) in sites with burning treatment. Numbers of dead spruces on forest edges surrounding the experimental areas were low during the first 3 years after the experimental treatments, varying from 0 to 8 per restoration area (Fig. 2). There were altogether 19 (mean 2.1 0.7) dead standing spruces, with I. typographus, on forest edges surrounding stands with no burning and 10 (mean 1.1 0.9) dead spruces on forest edges surrounding stands with burning treatment. The number of tree deaths among the three DWR levels, 5, 30, and 60 m3 ha1, were 6 (mean 1 0.6), 16 (mean 2.7 1.4), 7 (mean 1.2 0.7), respectively. DWR-level did not affect the proportion of colonized DWRS of either I. typographus or P. chalcographus (Fig. 3). Also there were no differences between DWR levels concerning the number
209
Fig. 5. The effect of DWR level and burning on I. typographus breeding success (number of female offspring per egg gallery) (S.E.). The two lowest levels of DWR are combined.
of I. typographus egg galleries per hectare (Fig. 4a). On the other hand the number of P. chalcographus mating chambers per hectare was higher at the two highest DWR levels when compared to the lowest level (Fig. 4b). When the two lowest levels of DWR were combined, to save an extra degree of freedom by reducing factor levels, burning treatment significantly decreased the breeding success of I. typographus (Fig. 5, Table 3). DWR level alone did not have an effect on breeding success but the interaction between DWR level and burning treatment was significant (Table 3). The effect of burning on decreasing breeding success was clearly stronger in experimental areas with a high DWR level (60 m3 ha1). The number of tree deaths on forest edges surrounding experimental areas was not affected by the DWR level or by the burning treatment. The use of alternative models for estimating the proportion of colonized trees, the total numbers of egg galleries and breeding chambers all explained a larger proportion of the deviance than did models using only DWR level (Table 4). The proportion of trees colonized by I. typographus decreased as the total number
Fig. 4. The number (S.E.) of I. typographus egg galleries ha1 (a) and P. chalcographus mating chambers ha1 (b) at three DWR levels.
210
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
Table 3 Deviance table of the effects of DWRS characteristics and DWR level on the proportion of colonized DWRS, the number of I. typographus egg galleries and the number of P. chalcographus mating chambers
Proportion of DWRS colonized by I. typographus Intercept Number of DWRS Mean D1.3 of DWRS
Deviance (residual)
Deviance (null model)
47.29
135.30
Number of I. typographus egg galleries Intercept Number of DWRS D1.3 of DWRS Number of DWRS D1.3 of DWRS
6.13
Number of P. chalcographus mating chambers ha1 Intercept DWRL 30/60
2.23
Total number of P. chalcographus mating chambers Intercept Number of DWRS
1.94
Coefficient
S.E.
Change in deviance
P
2.775 0.009 0.163
1.668 0.004 0.068
16.32 16.78
0.030 0.028
7.348 0.039 0.039 0.002
1.483 0.013 0.062 0.001
3.30 0.18 4.35
0.011 NS 0.005
10.238 1.295
0.151 0.185
5.57
<0.001
10.622 0.011
0.126 0.001
9.53
<0.001
14.41
7.79
11.47
Only models with significant predictors are included.
Fig. 6. The predicted proportion (a) and number (b) of DWRS colonized by I. typographus in relation to the total number and mean D1.3 of DWRS.
of DWRS increased (Fig. 6a). Increasing tree size (D1.3) increased the proportion of DWRS colonized by I. typographus (Fig. 6a). As P. chalcographus colonized almost 100% of DWRS in all areas, there were obviously no significant predictors. The total number and the mean D1.3 of DWRS and their interaction were included in the final model predicting the total number of I. typographus egg galleries. The model predicts an increase in egg gallery numbers along with the increase in mean D1.3 (Fig. 7). In stands with DWRS of small mean D1.3, the number of egg galleries slightly decreases as the number of DWRS increases. However, as the mean D1.3 increases the effect of increasing
numbers of DWRS also has a positive effect on the number of egg galleries. The total number of DWRS was the only significant predictor included in the model predicting the number of P. chalcographus mating chambers. An increase in this predictor also increases the number of mating chambers (Fig. 8).
Table 4 Factorial ANOVA table of the effects of DWR level and burning treatment on I. typographus breeding success
DWRL Burning treatment DWRL Burning treatment
Sum of squares
Mean squares
F
P
0.227 6.367 0.931
0.227 6.367 0.931
1.491 41.831 6.115
NS <0.001 0.027
Fig. 7. The predicted number of I. typographus egg galleries in relation to the total number and D1.3 of DWRS.
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
Fig. 8. The predicted number of P. chalcographus mating chambers in relation to the total number of DWRS.
4. Discussion 4.1. Colonization of felled spruces These together with our previous (Eriksson et al., 2005) results support the idea that larger amounts of damaged spruces attract more colonizing bark beetles into restoration or windthrow areas. Although the proportion of DWRS colonized by I. typographus decreased as the number of DWRS increased (Fig. 6a), the number of colonized DWRS still increased (Fig. 6b). The same trend in the number of colonized DWRS also applies to P. chalcographus, with the exception that this species colonized almost every DWRS at all DWR levels. However, when we compared the models estimating the number of colonizing beetles, the differences in host preferences become clear. Where there were numerous large felled spruces large quantities of I. typographus egg galleries harbored, while the same numbers of smaller trees almost totally lacked egg galleries (Fig. 7). This is understandable, as I. typographus is known to prefer host trees of large diameter (Butovitsch, 1938; Butovitsch, 1971; Go¨thlin et al., 2000) or stands with wind-felled spruces of large mean D1.3 (Eriksson et al., 2005). On the other hand, the number of P. chalcographus mating chambers was significantly affected only by the number of DWRS (Fig. 8). The observed difference between species is best explained by the ability of P. chalcographus to exploit trees of all sizes and even small diameter logging waste. To our knowledge this is the first study that experimentally attempts to estimate the significance of the amount of felled retention trees on the number of colonizing bark beetles. However, there are a few studies of the colonization of windfelled spruces in northern Europe (e.g. Butovitsch, 1938; Annila and Peta¨isto¨, 1978; Go¨thlin et al., 2000). These nonexperimental studies included only a few windthrow areas. Therefore, they do not give much information about the effect of the amount of damaged trees on the magnitude of colonization. The present and our earlier study on wind-felled spruces in 65 stands (Eriksson et al., 2005) do indicate that there
211
is a connection between the amount of damaged trees and the number of colonizing beetles. One possible link between the amount of damaged trees and the attractiveness of a stand is the amount of volatiles emitted from damaged spruces. These volatiles, mainly ethanol and acetaldehyde, are known to attract I. typographus (Lindelo¨w and Risberg, 1992). If the amount of volatiles emitted increases along with an increase in the amount of damaged spruces, large amounts of felled spruces should be very attractive for I. typographus. Earlier studies also show that the host volatiles emitted by damaged spruces strengthen the impact of the aggregation pheromones of I. typographus (Austara˚ et al., 1986; Franklin et al., 2000). The possible interaction of these two factors might further increase the attractiveness of large amounts of damaged spruces. The minimal model using stand or tree characteristics as predictors for estimating the number of I. typographus egg galleries in this study explained 57% of the null model’s deviance. The comparable model in our earlier study (Eriksson et al., 2005), with wind-felled spruces, explained 51%. The models used in both studies include the number of wind-felled or man-felled spruces per stand and the mean D1.3 of felled spruces. Furthermore, the model in the earlier study included the basal area of recently dead spruces, which was not included in this study, since all the experimental stands were managed and hence had only a very low number of dead trees. The slightly better fit of the model in this study is probably due the uniformity of the experimental stands and the smaller geographic area they represent (26 km 12 km versus 200 km 200 km). Furthermore, as cut trees have no resistance at all, the colonization of felled spruces is more predictable than the colonization of wind-felled spruces, which have varying degree of root connection and resistance. 4.2. I. typographus breeding success Breeding success in non-burned stands was significantly higher than in areas which had undergone burning treatment (Fig. 5). It also seems that burning treatment had a more devastating effect on offspring survival in areas with a high DWR level (60 m3) than at the two lowest levels. Actually, studies by Lilja et al. (2005) in the same experimental areas show that the living tree mortality, inside experimental areas was highest with a high DWR level, because the flames climbed up to the canopy, using down retention trees as a ‘‘ladder’’. Thus, the low breeding success at the highest level of DWR with burning treatment was attributable to the intensity of the fire. 4.3. Tree killing The number of trees killed, with I. typographus, in forest edges surrounding experimental stands during the three summers following the year when the treatments were applied, was overall very low (Fig. 2). The treatments, DWR level or burning, or the other predictors had no significant effect on tree deaths. Similar results have been obtained when using not more than five cut spruces (Hedgren et al., 2003) or when using
212
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
wind-felled trees (Peltonen, 1999) on clear-cut forest edges. In both studies the number of dead standing spruces attacked by I. typographus did not depend on the amount of cut trees or windthrows at the same site. In another study, where the amount of wind-felled spruces per windthrow area is more comparable with that of our study, Schroeder and Lindelo¨w (2002) reported an almost perfect linear relationship between the number of wind-felled spruces colonized by I. typographus and the number of trees killed in the 4 years following the storm felling. Naturally our experimental stands differ from windthrow areas since the trees were cut down leaving no root contact left, which lead to rapid desiccation of the felled trees. While I. typographus can successfully breed in 2 year old wind-felled spruces (Butovitsch, 1971; Annila and Peta¨isto¨, 1978; Go¨thlin et al., 2000; Eriksson et al., 2005) the rapid desiccation of cut trees means that successful breeding is possible only during the first summer after cutting. Since there were altogether 19 dead spruces in forest edges surrounding stands that had not been burned and 10 where surrounding stands had been burned, the results do suggest that, with a larger sample size, burning might have had a considerable effect on tree deaths in surrounding forest edges. This would be understandable, because most of the bark beetles breeding in felled spruces were scorched alive in stands with burning treatment. Burning treatment might also be the source of some of the unexplained variation in the model, as in all our burning treatments patches were left unburned, and paludified biotopes contributed most to the stand heterogeneity of the burning mosaic (Lilja et al., 2005). Standing retention spruces that are not killed but slightly weakened might be very attractive for I. typographus in the years following the burning treatment. However, data based on window trappings (trunk window-traps) by Toivanen et al. (in prep.), in the same experimental areas, suggest that I. typographus colonized fire damaged spruces at a much lower intensity than they did girdled trees in non-burnt areas. Further studies concerning I. typographus are, however, needed to find out whether burning increases the attraction range of a stand with damaged trees. Another point requiring clarification concerns the potential of spruces damaged and weakened by fire to sustain or even increase I. typographus populations.
by the amount and quality of suitable breeding material. If the damaged trees are of very small diameter, for example, under 15 cm (D1.3), then the probability of attacks on nearby standing trees might increase. Logging residues probably have the same effect. It is, however, unlikely that restoration operations of this magnitude would have any long-distance effects as earlier studies indicate that only years of large windfall episodes have a significant effect on the population level of I. typographus (Økland and Bjørnstad, 2003; Økland and Berryman, 2004). To minimize the risks of restoration, restorative operations should be avoided in the same area in consecutive years or after severe storms with windthrows, or at least considered thoroughly. Although no significant effects of burning treatment on tree deaths were found, it seems that burning after bark beetle colonization decreases the risks of restoration. This hypothesis is supported by our results, which showed a significant decrease in the breeding success of I. typographus. On the other hand, trees only mildly damaged by fire might become very susceptible to insect attacks in the years following the burning treatment and thereby increase the risk of further damage on nearby forest edges.
5. Conclusions
References
The risks involved in restoration, in terms of tree deaths seem to be minor, at least when populations of I. typographus are at endemic levels. However, large amounts of damaged trees seem to attract more beetles than smaller amounts. Beetles probably use the volatiles from injured or decaying trees (Lindelo¨w and Risberg, 1992) as a cue when seeking out suitable host trees. Obviously I. typographus cannot discriminate between suitable (large enough) and unsuitable spruces simply on the basis of host volatiles. Thus, the number of beetles, arriving in stand with damaged trees is probably the result of interaction between the amount of host volatiles, the local bark beetle population levels and weather conditions. Furthermore, the number of colonizing beetles is also affected
Acknowledgements We would like to thank all those who participated in the burning activities and field inventory work, especially Liina Kjellberg, Tero Toivanen, and Veli Liikanen for their assistance in insect inventories, Seppo Neuvonen for his valuable comments on the manuscript, and Rosemary Mackenzie for checking the English. The Ha¨me Polytechnic, the Finnish Forest and Park Service, UPM-Kymmene Ltd., the City of Ha¨meenlinna and the Finnish Forest Research Institute provided the stands for the study and implemented the treatments. This study was funded by the Finnish Ministry of Agriculture and Forestry and the Graduate School in Forest Sciences. The study is part of the FIRE-project in the Sustainable use of Natural Resources (SUNARE) 2001–2004 program financed by the Academy of Finland and part of the EU-project forest fire spread prevention and mitigation (SPREAD).
Ahti, T., Ha¨met-Ahti, L., Jalas, J., 1968. Vegetation zones and their sections in northwestern Europe. Ann. Bot. Fenn. 5, 169–211. Annila, E., Peta¨isto¨, R.-L., 1978. Insect attack on windthrown trees after the december 1975 storm in western Finland. Commun. Inst. For. Fenn. 94, 1– 24. Anon, 2002. Etela¨-Suomen, Oulun la¨a¨nin la¨nsiosan ja Lapin la¨a¨nin lounaisosan metsien monimuotoisuuden turvaamisen toimintaohjelma. Ehdotus Etela¨Suomen, Oulun la¨a¨nin la¨nsiosan ja Lounais-Lapin metsien suojelun tavoite, rahoitus-, ja toimintaohjelmaksi. Etela¨-Suomen metsien suojelutoimikunta (Metso) (in Finnish). Anon, 2003. Restoration in protected areas, report by the working group on restoration 2003. The Finnish Environment. 618, 1–220 (in Finnish with Abstract in English). Austara˚, O., Bakke, A., Midtgaard, F., 1986. Response in Ips typographus to logging waste odours and synthetic pheromones. J. Appl. Ent. 101, 194– 198.
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213 Bradshaw, A.D., 1997. What do we mean by restoration? In: Urbanska, K.M., Webb, N.R., Edwards, P.J. (Eds.), Restoration ecology and sustainable development. Cambridge University Press, Cambridge, U.K., pp. 8–14. Butovitsch, V., 1938. Om granbarkborrens massfo¨ro¨kning i so¨dra Dalarna. Norrl. Skogsv. Fo¨rb. Tidskr. Ha¨fte 2, 1–36 (in Swedish with abstract in German). Butovitsch, V., 1971. Underso¨kningar o¨ver skadeinsekternas upptra¨dande i de stormha¨rjade skogarna i mellersta Norrlands kustland a˚ren 1967–1969. Inst. Skogszool. Rapp. Upps. 8, 1–204 (in Swedish). Cajander, A.K., 1926. The theory of forest types. Acta Forestalia. Fennica. 29, 1–108. Crawley, M.J., 2003. Statistical Computing. John Wiley & Sons Ltd., Wiltshire. Eriksson, M., Pouttu, A., Roininen, H., 2005. The influence of windthrow area and timber characteristics on colonization of wind-felled spruces by Ips typographus (L.). For. Ecol. Manage. 216, 105–116. Esseen, P.A., Ehnstro¨m, B., Ericson, L., Sjo¨berg, K., 1997. Boreal forests. Ecol. Bull. 46, 16–47. Franklin, A.J., Debruyne, C., Gre´goire, J.-C., 2000. Recapture of Ips typographus L. (Col., Scolytidae) with attractants of low release rates, localized dispersion and environmental influences. Agric. For. Entomol. 2, 259–270. Fridman, J., Walheim, M., 2000. Amount, structure and dynamics of dead wood on managed forestland in Sweden. For. Ecol. Manage. 31, 23–26. ˚ ., 2000. Attacks by Ips typographus Go¨thlin, E., Schroeder, L.M., Lindelo¨w, A and Pityogenes chalcographus on windthrown spruces (Picea abies) during the two years following a storm felling. Scand. J. Forest Res. 15, 542–549. Hedgren, P.O., 2004. The bark beetle Pityogenes chalcographus (L.) (Scolytidae) in living trees, reproductive success, tree mortality and interaction with Ips typographus. J. Appl. Ent. 128, 161–166. Hedgren, P.O., Schroeder, L.M., Weslien, J., 2003. Tree killing by Ips typographus (Coleoptera: Scolytidae) at stand edges with and without colonized felled spruce trees. Agric. For. Entomol. 5, 67–74. Jonsell, M., Weslien, J., Ehnstro¨m, B., 1998. Subtrate requirements of red-listed saproxylic invertebrates in Sweden. Biodiver. Conserv. 7, 749–764. Kuuluvainen, T., Tukia, H., Aapala, K., 2005. Ecological restoration of forested ecosystems in Finland. in: Stanturf, J.A., Madsen, P. (Eds.), Restoration of boreal and temperate forests. pp. 285–298, ISBN 1-56670-635-1. Laasasenaho, J., 1982. Taper curve and volume functions for pine, spruce and birch. Comm. Inst. For. Fenn. 108, 1–74. Lekander, B., 1972. A mass outbreak of Ips typographus in Ga¨strikland, Central Sweden, in 1945–1952. Department of Forest Zoology, Research notes, 10. Royal College of Forestry, Stockholm (in Swedish with English summary). Lemberg, T., Puttonen, P., 2003. Kulottajan ka¨sikirja. Metsa¨lehti kustannus, Vammalan kirjapaino Oy. pp. 113. ISBN 952-5118-41-X (in Finnish).
213
Lilja, S., de Chantal, M., Kuuluvainen, T., Vanha-Majamaa, I., Puttonen, P., 2005. Restoring natural characteristics in boreal Norway spruce (Picea abies L. Karst) stands with partial cutting, dead wood creation and fire, immediate treatment effects. Scan. J. For. Res. 20 (Suppl. 6), 68– 78. ˚ ., Risberg, B., 1992. Attraction during flight of scolytids and other Lindelo¨w, A bark- and wood-dwelling beetles to volatiles from fresh and stored spruce wood. Can. J. For. Res. 22, 224–228. Mulock, P., Christiansen, E., 1986. The threshold of successful attack by Ips typographus on Picea abies, a field experiment. For. Ecol. Manage. 14, 125– 132. Økland, B., Bjørnstad, O.N., 2003. Synchrony and geographical variation of the spruce bark beetle (Ips typographus) during a non-epidemic period. Population Ecol. 45, 213–219. Økland, B., Berryman, A., 2004. Resource dynamic plays a key role in regional fluctuations of the spruce bark beetles Ips typographus. Agr. For. Entom. 6, 141–146. Peltonen, M., 1999. Windthrows and dead-standing trees as bark beetle breeding material at forest-clearcut edge. Scand. J. Forest Res. 14, 505–511. R Development Core Team, 2005. R, A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org. Saalas, U., 1949. Suomen metsa¨hyo¨nteiset. Werner So¨derstro¨m Oy, Porvoo, Helsinki (in Finnish). Schroeder, L.M., 2001. Tree mortality by the bark beetle Ips typographus (L.) in storm-disturbed stands. Int. Pest Manage. Rev. 6, 169–175. ˚ ., 2002. Attacks on living spruce trees by the bark Schroeder, L.M., Lindelo¨w, A beetle Ips typographus (Col. Scolytidae) following a storm felling, a comparison between stands with and without removal of wind felled trees. Agr. For. Entom. 4, 47–56. Siitonen, J., 2001. Forest management, coarse woody debris and saproxylic organisms. Fennoscandian boreal forests as an example. Ecol. Bull. 49, 11– 39. Siitonen, J., Martikainen, P., Punttila, P., Rauh, J., 2000. Coarse woody debris and stand characteristics in mature managed and old-growth boreal mesic forests in southern Finland. For. Ecol. Manage. 128, 211–225. Tomppo, E., Henttonen, H., Korhonen, K., Aarnio, A., Ahola, A., Ihalainen, A., Heikkinen, J., Tuomainen, T., 1999. Keski-Suomen metsa¨keskuksen alueen metsa¨varat ja niiden kehitys 1967–1996. Metsa¨tieteen aikakausikirja 2B/ 1999, 309–387 (in Finnish). Wedderburn, 1974. Quasi-likelihood functions, generalized linear models, and the Gauss–Newton method. Biometrika 61, 439–447.
Dead wood creation and restoration burning: Implications for bark beetles and beetle induced tree deaths Miikka Eriksson a,b,*, Saara Lilja c, Heikki Roininen a a
University of Joensuu, Department of Biology, P.O. Box 111, FIN-80101 Joensuu, Finland b Finnish Forest Research Institute, P.O. Box 68, FIN-80101 Joensuu, Finland c University of Helsinki, Faculty of Agriculture and Forestry, Department of Forest Ecology, P.O. Box 27, 00014, Finland Received 13 February 2006; received in revised form 4 May 2006; accepted 17 May 2006
Abstract Dead wood creation is an important tool for restoring the natural characteristics of boreal managed forests, where the amount of dead wood has seriously declined as a result of forest management practices. Although many forest species would benefit from restoration, foresters are concerned about the increased risk of bark beetle attacks on surrounding managed forests. In our study, we investigated whether the number or size of dead wood created affects the number of bark beetles (Ips typographus and Pityogenes chalcographus) colonizing the felled trees and whether the amount of dead wood and burning treatment after colonization has an effect on I. typographus breeding success and consequential tree deaths in forest borders surrounding restoration areas. The experimental restoration of Norway spruce dominated stands included partial cuttings with three levels of down wood retention (DWR) (5, 30, and 60 m3 ha1) and a burn/non-burn treatment (3 2 factorial) with three replicates of each treatment combination. An increase in the total number of down wood retention spruces (DWRS) decreased the proportion of trees colonized by I. typographus, but increased the total number of colonized trees. P. chalcographus colonized almost 100% of felled spruces. The total number of I. typographus egg galleries was best explained by the interaction of the number and mean diameter of DWRS. According to the models constructed the experimental areas with great numbers of large spruces harbor the most I. typographus egg galleries, while stands with the same number of smaller trees almost totally lack egg galleries. The number of P. chalcographus mating chambers increased along with an increase in the number of DWRS. Burning treatment diminished the breeding success of I. typographus, especially at the highest DWR level, where the intensity of fire was also the highest. Instead of relatively extensive colonization by I. typographus and P. chalcographus, numbers of tree deaths at forest edges surrounding restoration areas were overall very low, and therefore no significant predictors were found. This study shows that the number and size of damaged trees affects the number of bark beetles colonizing the restoration area. However, in Finland the risks of restoration projects of this magnitude, at least when I. typographus populations are at endemic levels, are rather low. # 2006 Elsevier B.V. All rights reserved. Keywords: Bark beetles; Ips typographus; Picea abies; Restoration; Dead wood; Burning
1. Introduction Artificial dead wood creation is in many respects comparable to leaving wind-damaged trees in forests and involves its own risks as regard to forest health in nearby areas. The increasing number of wind-felled spruces has been shown to attract more colonizing individuals of the European spruce bark beetle (Ips typographus L.) (Coleoptera: Scolytidae), which is practically the only significant bark beetle pest affecting mature
* Corresponding author. Tel.: +358 10 211 3269; fax: +358 10 211 3251. E-mail address: [email protected] (M. Eriksson). 0378-1127/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2006.05.050
Norway spruce (Picea abies (L.) Karst.) in Finland, into the damage area (Eriksson et al., 2005) and to correlate positively with the number of living trees killed in windthrow areas (Schroeder and Lindelo¨w, 2002). Even though I. typographus is a serious forest pest it also creates new breeding material for a variety of insect species. Dead and decaying wood, including trees killed by I. typographus, constitute a habitat for a large number of harmless species (Esseen et al., 1997; Jonsell et al., 1998; Siitonen, 2001). Unfortunately, partly due the fear of I. typographus attacks and the consequent high standards of forest hygiene, the amount of dead wood in managed forests has been seriously reduced (Fridman and Walheim, 2000; Siitonen, 2001). At
206
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
present, the average volume of dead wood in the managed forests of southern Finland is from 1.2 to 2.9 m3 ha1 (Tomppo et al., 1999) while natural forest in the same areas have on average 60–90 m3 ha1 of coarse woody debris (Siitonen, 2001). However, the volume of dead wood in natural stands could be even higher after stand-replacing disturbance or when the fire return interval is very long (Siitonen et al., 2000). Consequently, the creation of dead wood in managed forests is an essential tool for forest restoration, in order to rehabilitate important stand structures, processes, and species composition in ecosystems altered by human action (Bradshaw, 1997; Anon, 2003; Kuuluvainen et al., 2005). In Finland the goal during the years 2003–2012 is to restore about 33,000 ha of state owned land (Anon, 2002). In forest areas this includes artificial creation of dead wood (10,430 ha), small gap creation (5210 ha) and burning of 160 tracts of forest (960 ha). Although the total area of forest restoration operations per year is fairly low, each restoration treatment has its own effect on the surrounding managed forests, and this should be taken into account before operations are started. However, there are no studies on the effects of down wood retention level, with more than five cut trees (Hedgren et al., 2003), on bark beetles or on surrounding forests. Neither have the effects of fire on I. typographus breeding or consequential tree deaths been studied earlier. Therefore, there is a need for experimental studies that consider the insect induced risks involved in forest restoration projects. I. typographus breeds commonly in wind-felled trees, large diameter logging waste, and sometimes also in solitary living trees, which they may kill on the edges of clear-cut areas (Peltonen, 1999; Hedgren et al., 2003). For successful breeding in living trees, a high number of colonizing beetles is needed to overcome the defensive systems of the trees (e.g. Mulock and Christiansen, 1986). Such an increase in population levels is possible, for example, after heavy windstorms, when there is a surplus of breeding material with low or no resistance at all. Thus, extensive storm damage may lead to I. typographus outbreaks and consequential damages to living trees (e.g. Saalas, 1949; Lekander, 1972; Schroeder, 2001). Damaged spruces also provide a suitable breeding ground for Pityogenes chalcographus (L.), which alone does not seem to impose a risk for healthy spruces (Hedgren, 2004). P. chalcographus may, however, affect I. typographus populations by utilizing partly the same resources as I. typographus. In this study, the risks of restoration operations were investigated. Restoration included partial cuttings with three levels of down wood retention (DWR = trees felled and left on the stand) and a burn/non-burn treatment. A constant volume (50 m3 ha1) of standing retention trees was left in the stands. The main objective of this study was to answer to the following questions: (1) Does the increase in the amount of DWR trees affect the proportion of DWR spruces colonized by bark beetles or the number of egg galleries or breeding chambers in DWR spruces? (2) Does burning treatment, after the colonization of felled spruces, and the increase in the amount of DWR trees affect the breeding success of I. typographus and the number of tree deaths on forest edges surrounding restoration areas?
2. Methods 2.1. Study area and experimental design The study area is located in the southern boreal zone (Ahti et al., 1968) in southern Finland (latitude 618120 –618250 N, longitude 258000 –258150 E). The experimental stands were searched from the data bases of several landowners using the following criteria: mature managed P. abies-dominated stand, area of 1–3 ha, and Vaccinium myrtillus forest type (Cajander, 1926). The stands were selected iteratively by visiting them in the field and accepting them if they fulfilled the criteria. The selected stands were clustered within an area of 26 km 12 km (Fig. 1). Altogether, 18 stands were selected for the experiment. The average age of the stands was 80 years (from 60 to 100 years). All of the stands were managed. Most of the stands fulfilled the criteria for V. myrtillus forest type (MT), but three stands also had some characteristics of the Oxalis Myrtillus forest type (OMT) (Cajander, 1926). The stands were of mixed tree species composition, including Betula pendula Roth, B. pubescens Ehrhart, Populus tremula L., and Pinus sylvestris L. In addition, Sorbus aucuparia L. and Juniperus communis L. occurred in the shrub layer. Although each stand was classified under one forest type for forestry purposes, there was clear small-scale within-stand variation. Accordingly, each stand included an upland and a paludified biotope. The upland biotopes were typically dominant, while paludified biotopes covered smaller patches. Experimental treatments were randomized among the stands. The treatments consisted of three levels of down wood retention (DWR) = trees, including all tree species, felled and left in the stand) and burning treatment (burn/non-burn) (3 2 factorial). Each treatment combination was repeated three times (3 6 = 18). A constant volume of 50 m3 ha1 of standing dispersed retention trees (all tree species included) was left on all the stands, meaning that some of the felled trees
Fig. 1. Locations of experimental stands within the study area.
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
were transported out of the stand. The three levels of DWR were 5, 30, and 60 m3 ha1. The harvestings were carried out using conventional forestry machinery which cut the branches from the stem and spread the logging residues evenly on the forest floor. However, branches from the stems of DWR spruces (DWRS = spruces felled and left in the stand) were left untouched. The restorative cuttings were conducted in February and March 2002 and the burnings during June–August 2002. The burnings were carried out using the traditional Finnish prescribed burning technique (Lemberg and Puttonen, 2003). With this method, ignition lines form a circle around the stand and the burning front advances partly against the wind, which decreases the risk of escape. In addition, extra ignition lines were lit inside the circle. For a detailed description of the experimental stands and the methods used in restoration, see Lilja et al. (2005). 2.2. Insect sampling In July 2003, DWRS were inspected for bark beetle galleries. Although half of the stands were burned after the main swarming period of I. typographus and P. chalcographus, the galleries of both species were visible and countable in most of the inspected spruces. In most DWRS, on burned stands, the bark was only slightly charred and branches were burned. Some of the DWRS were not burned at all. Only a few trees were not qualified for inspection because of burning. A sample of 6–41 DWRS per restoration area (Table 1) was inspected, depending on the amount of available DWRS outside the sample plots (two 30 m 50 m plots on each stand), which were reserved for other uses. Pieces of bark (15 cm 60 cm) were removed and egg galleries and exit holes of I. typographus were counted at
207
1.3 and 4 m, and at intervals of 4 m until the diameter of tree trunk decreased to less than 10 cm. P. chalcographus mating chambers were counted at the same heights from a smaller area (15 cm 15 cm). DWRS were counted in each stand and the inspected spruces were measured for diameter at breast height (1.3 m above the cut point) and at the last inspection height. New dead standing spruces with I. typographus damages on forest edges (0–20 m from the forest edge) directly surrounding experimental stands were counted each autumn in the years 2003–2005. 2.3. Calculations The DWR level, including volumes of Pinus, Picea, and Betula spp., was assessed using the volume equations of Laasasenaho (1982) based on tree diameter at breast height (D1.3) and tree height. The volume of all other deciduous trees was estimated using the equations for Betula. The volumes of DWRS were assessed using the equations based on tree diameter (Laasasenaho, 1982) and cylinder formulae were used to compute the bark area of the inspected trees. For calculating the total number of egg galleries and mating chambers per experimental stand, sampled trunks were divided into sections so that each insect sample represented a section of the tree trunk (sample from 1.3 m represented stem section from 0 to 2.00 m, sample from 4 m represented stem section from 2.01 to 6.00 m, sample from 8 m represented stem section from 6.01 to 10.00 m and so on). Total number of galleries and chambers per tree were obtained by first calculating the number of galleries and chambers per m2, then multiplying the result with the area of the corresponding trunk section and finally summing the
Table 1 Experimental stands, DWR level, stand area, number of inspected DWRS, DWRS characteristics (total number, total volume, and mean D1.3), proportion of colonized trees, the total number of I. typographus (I.t.) egg galleries and P. chalcographus (P.c.) mating chambers, and the number of dead spruces in forest edges Experimental DWR-level Area Inspected DWRS stand (m3 ha1) (ha) DWRS
230 291 552 168 271 496 37 196 617 165B 250B 301B 41B 85B 203B 55B 205B 327B
5 5 5 30 30 30 60 60 60 5 5 5 30 30 30 60 60 60
2.66 1.30 2.16 2.10 1.08 1.31 1.36 2.86 1.09 1.06 1.57 0.78 2.55 0.86 2.15 2.56 3.37 1.65
19 16 13 29 12 41 25 26 22 6 19 16 34 10 25 29 40 28
Proportion Number of of DWRS colonized by
Dead spruces in forest edges
Number Volume (m3) Mean D1.3 (cm) I.t
P.c.
I.t. egg galleries P.c. mating chambers
40 23 15 126 24 162 125 104 53 9 22 16 210 25 75 140 206 147
1.00 0.94 1.00 1.00 1.00 1.00 0.96 0.96 0.95 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00
4050 1765 4674 1133 11303 2096 15001 9821 5234 9442 4856 4931 1426 4074 3208 28296 1278 15539
10.6 6.2 8.3 28.7 10.4 27.4 42.2 44.0 29.4 6.5 5.1 6.0 34.3 13.8 35.0 56.6 38.1 43.1
B after the stand number indicates the burning treatment.
19.7 19.5 26.0 18.8 24.8 16.9 21.9 24.4 25.8 30.2 18.6 23.0 16.3 26.8 25.2 23.3 17.1 20.1
0.37 0.63 0.62 0.24 0.92 0.17 0.80 0.58 0.55 1.00 0.53 1.00 0.09 0.80 0.40 0.55 0.13 0.36
85253 44526 46757 240876 66478 237505 169314 133331 93319 17370 37837 30375 315280 63233 168413 189926 338053 264473
2 0 4 0 5 3 4 0 1 1 0 0 0 0 8 1 0 0
208
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
number of galleries or chambers in each section. The average of the number of egg galleries or mating chambers in sample trees in each experimental stand was taken and multiplied with the total number of DWRS’s to obtain the total number of egg galleries or mating chambers per each experimental stand. The number of egg galleries or mating chambers per hectare was obtained by dividing the total number of galleries or chambers with the size (ha) of the experimental stand. The breeding success (female offspring per mother beetle) of I. typographus was calculated: 0.5 (the number off exit holes/the number of egg galleries). It was assumed that one beetle had left through each exit hole. The data for felled spruces (DWRS) were collected during insect sampling, but the data on other species and standing trees is based on the data collected from the sample plots in each restoration area (see Lilja et al., 2005). 2.4. Statistical analysis The effects of DWR level and burning treatment on the colonization of DWRS and tree deaths on the restoration area forest border were tested. Response variables included the proportion of DWRS colonized (both beetle species separately), the estimated number of I. typographus egg galleries ha1, the estimated number of P. chalcographus mating chambers ha1, the reproductive success of I. typographus and tree deaths on the restoration area forest border. Since burning treatments were carried out after the main swarming period of both bark beetle species, it did not influence (tested as nonsignificant predictor in models concerned with colonization) the colonization of DWRS. Non-burned and burned stands were therefore combined for analyzing the proportions of colonized DWRS and the numbers of egg galleries and mating chambers. Alternative models with more specific continuous predictors were constructed on account of the large variation in the mean D1.3 of DWRS and the size of the restoration areas (Table 1), which meant that DWR level did not give much information about the total number or the size of DWRS. Response variables in these alternative models included the proportion of colonized DWRS (for both beetle species separately), the total number of egg galleries, mating chambers, and tree deaths per restoration area. Predictors included the number of DWRS, the mean diameter (D1.3) of DWRS and the size of the restoration stand (Table 2). Furthermore, the total number of colonized DWRS (I.
typographus) and insect gallery or chamber numbers per stand were included in the alternative analysis of tree deaths (Table 2). Generalized linear models (GLM) were used for the analyses. The proportion of colonized DWRS was analyzed by weighted regression, using the individual sample sizes as weights (Crawley, 2003: p. 513–536). In the model handling the proportion of DWRS colonized by I. typographus, overdispersion was taken into account by using a quasibinomial family with logit link function. Counts of both species on felled spruces had a highly skewed distribution. For this reason quasilikelihood, introduced by Wedderburn in 1974, which uses only the variance–mean relationship of the response variable, was utilized. The link function ‘‘log’’ was used to linearize the response, and the variance function was specified as ‘‘m2’’ (‘‘m’’ as the mean of the distribution) to take into account the increase in variance with the square of the mean (Crawley, 2003: p. 544). Minimal models (i.e. final models with only statistically significant predictors left) were determined by assessing the increase in deviance (the measure of discrepancy in a GLM used to assess the goodness of fit of the model to the data) attributable to the removal of individual predictors through F goodness-of-fit tests comparing the deviance of the models with and without the particular term included (Crawley, 2003). Only the analysis of I. typographus breeding success was conducted using a square root transformed response variable and two-way analysis of variance. Predictors were deemed significant at the P < 0.05 probability level. The analyses were carried out in R (R Development Core Team, 2005). 3. Results The total volume of DWRS per experimental area varied somewhat even within the same DWR-level because of the variation in both the size of the areas and the amount of other tree species. The total number and volume of DWRS per experimental area varied from 9 to 210 and from 5 to 57 m3, respectively (Table 1). There was also variation in the size of DWRS as the mean D1.3 of felled spruces varied from 16.3 to 30.2 cm. Large variation, between areas, was also found in total I. typographus egg gallery and P. chalcographus mating chamber numbers (from 1133 to 28,296 and from 17,370 to 338,053,
Table 2 Predictors (with mean and SD) used in alternative models
Stand area (ha) No. DWRS Mean D1.3 of DWRS No. DWRS colonized No. egg galleries No. mating chambers
Mean
S.D.
1.80 84.56 22.13 31.55 7118 141240
0.77 68.78 3.95 25.09 6951 103207
Stand area, no. DWRS and mean D1.3 were used in all five models. No. DWRS colonized by I. typographus, no. egg galleries (I. typographus), and no. mating chambers (P. chalcographus) were used only in the model concerning tree deaths in forest edges.
Fig. 2. Tree deaths on forest edges surrounding experimental areas in 2003– 2005. Burned stands are marked with the letter B after the site number.
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
Fig. 3. The proportion (S.E.) of DWRS colonized by I. typographus and P. chalcographus at three DWR levels.
respectively) (Table 1). The mean I. typographus egg gallery density per m2 of colonized bark was overall rather low, varying from 18.1 to 96.0 (mean 50.9 4.8) and correlated negatively with the number of DWRS (Pearson, r = 0.55, P = 0.02). The breeding success of I. typographus varied from 3.5 to 11.5 (mean 6.1 0.9) female offspring per egg gallery in sites with no burning and from 0.3 to 3.0 (mean 1.7 0.3) in sites with burning treatment. Numbers of dead spruces on forest edges surrounding the experimental areas were low during the first 3 years after the experimental treatments, varying from 0 to 8 per restoration area (Fig. 2). There were altogether 19 (mean 2.1 0.7) dead standing spruces, with I. typographus, on forest edges surrounding stands with no burning and 10 (mean 1.1 0.9) dead spruces on forest edges surrounding stands with burning treatment. The number of tree deaths among the three DWR levels, 5, 30, and 60 m3 ha1, were 6 (mean 1 0.6), 16 (mean 2.7 1.4), 7 (mean 1.2 0.7), respectively. DWR-level did not affect the proportion of colonized DWRS of either I. typographus or P. chalcographus (Fig. 3). Also there were no differences between DWR levels concerning the number
209
Fig. 5. The effect of DWR level and burning on I. typographus breeding success (number of female offspring per egg gallery) (S.E.). The two lowest levels of DWR are combined.
of I. typographus egg galleries per hectare (Fig. 4a). On the other hand the number of P. chalcographus mating chambers per hectare was higher at the two highest DWR levels when compared to the lowest level (Fig. 4b). When the two lowest levels of DWR were combined, to save an extra degree of freedom by reducing factor levels, burning treatment significantly decreased the breeding success of I. typographus (Fig. 5, Table 3). DWR level alone did not have an effect on breeding success but the interaction between DWR level and burning treatment was significant (Table 3). The effect of burning on decreasing breeding success was clearly stronger in experimental areas with a high DWR level (60 m3 ha1). The number of tree deaths on forest edges surrounding experimental areas was not affected by the DWR level or by the burning treatment. The use of alternative models for estimating the proportion of colonized trees, the total numbers of egg galleries and breeding chambers all explained a larger proportion of the deviance than did models using only DWR level (Table 4). The proportion of trees colonized by I. typographus decreased as the total number
Fig. 4. The number (S.E.) of I. typographus egg galleries ha1 (a) and P. chalcographus mating chambers ha1 (b) at three DWR levels.
210
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
Table 3 Deviance table of the effects of DWRS characteristics and DWR level on the proportion of colonized DWRS, the number of I. typographus egg galleries and the number of P. chalcographus mating chambers
Proportion of DWRS colonized by I. typographus Intercept Number of DWRS Mean D1.3 of DWRS
Deviance (residual)
Deviance (null model)
47.29
135.30
Number of I. typographus egg galleries Intercept Number of DWRS D1.3 of DWRS Number of DWRS D1.3 of DWRS
6.13
Number of P. chalcographus mating chambers ha1 Intercept DWRL 30/60
2.23
Total number of P. chalcographus mating chambers Intercept Number of DWRS
1.94
Coefficient
S.E.
Change in deviance
P
2.775 0.009 0.163
1.668 0.004 0.068
16.32 16.78
0.030 0.028
7.348 0.039 0.039 0.002
1.483 0.013 0.062 0.001
3.30 0.18 4.35
0.011 NS 0.005
10.238 1.295
0.151 0.185
5.57
<0.001
10.622 0.011
0.126 0.001
9.53
<0.001
14.41
7.79
11.47
Only models with significant predictors are included.
Fig. 6. The predicted proportion (a) and number (b) of DWRS colonized by I. typographus in relation to the total number and mean D1.3 of DWRS.
of DWRS increased (Fig. 6a). Increasing tree size (D1.3) increased the proportion of DWRS colonized by I. typographus (Fig. 6a). As P. chalcographus colonized almost 100% of DWRS in all areas, there were obviously no significant predictors. The total number and the mean D1.3 of DWRS and their interaction were included in the final model predicting the total number of I. typographus egg galleries. The model predicts an increase in egg gallery numbers along with the increase in mean D1.3 (Fig. 7). In stands with DWRS of small mean D1.3, the number of egg galleries slightly decreases as the number of DWRS increases. However, as the mean D1.3 increases the effect of increasing
numbers of DWRS also has a positive effect on the number of egg galleries. The total number of DWRS was the only significant predictor included in the model predicting the number of P. chalcographus mating chambers. An increase in this predictor also increases the number of mating chambers (Fig. 8).
Table 4 Factorial ANOVA table of the effects of DWR level and burning treatment on I. typographus breeding success
DWRL Burning treatment DWRL Burning treatment
Sum of squares
Mean squares
F
P
0.227 6.367 0.931
0.227 6.367 0.931
1.491 41.831 6.115
NS <0.001 0.027
Fig. 7. The predicted number of I. typographus egg galleries in relation to the total number and D1.3 of DWRS.
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
Fig. 8. The predicted number of P. chalcographus mating chambers in relation to the total number of DWRS.
4. Discussion 4.1. Colonization of felled spruces These together with our previous (Eriksson et al., 2005) results support the idea that larger amounts of damaged spruces attract more colonizing bark beetles into restoration or windthrow areas. Although the proportion of DWRS colonized by I. typographus decreased as the number of DWRS increased (Fig. 6a), the number of colonized DWRS still increased (Fig. 6b). The same trend in the number of colonized DWRS also applies to P. chalcographus, with the exception that this species colonized almost every DWRS at all DWR levels. However, when we compared the models estimating the number of colonizing beetles, the differences in host preferences become clear. Where there were numerous large felled spruces large quantities of I. typographus egg galleries harbored, while the same numbers of smaller trees almost totally lacked egg galleries (Fig. 7). This is understandable, as I. typographus is known to prefer host trees of large diameter (Butovitsch, 1938; Butovitsch, 1971; Go¨thlin et al., 2000) or stands with wind-felled spruces of large mean D1.3 (Eriksson et al., 2005). On the other hand, the number of P. chalcographus mating chambers was significantly affected only by the number of DWRS (Fig. 8). The observed difference between species is best explained by the ability of P. chalcographus to exploit trees of all sizes and even small diameter logging waste. To our knowledge this is the first study that experimentally attempts to estimate the significance of the amount of felled retention trees on the number of colonizing bark beetles. However, there are a few studies of the colonization of windfelled spruces in northern Europe (e.g. Butovitsch, 1938; Annila and Peta¨isto¨, 1978; Go¨thlin et al., 2000). These nonexperimental studies included only a few windthrow areas. Therefore, they do not give much information about the effect of the amount of damaged trees on the magnitude of colonization. The present and our earlier study on wind-felled spruces in 65 stands (Eriksson et al., 2005) do indicate that there
211
is a connection between the amount of damaged trees and the number of colonizing beetles. One possible link between the amount of damaged trees and the attractiveness of a stand is the amount of volatiles emitted from damaged spruces. These volatiles, mainly ethanol and acetaldehyde, are known to attract I. typographus (Lindelo¨w and Risberg, 1992). If the amount of volatiles emitted increases along with an increase in the amount of damaged spruces, large amounts of felled spruces should be very attractive for I. typographus. Earlier studies also show that the host volatiles emitted by damaged spruces strengthen the impact of the aggregation pheromones of I. typographus (Austara˚ et al., 1986; Franklin et al., 2000). The possible interaction of these two factors might further increase the attractiveness of large amounts of damaged spruces. The minimal model using stand or tree characteristics as predictors for estimating the number of I. typographus egg galleries in this study explained 57% of the null model’s deviance. The comparable model in our earlier study (Eriksson et al., 2005), with wind-felled spruces, explained 51%. The models used in both studies include the number of wind-felled or man-felled spruces per stand and the mean D1.3 of felled spruces. Furthermore, the model in the earlier study included the basal area of recently dead spruces, which was not included in this study, since all the experimental stands were managed and hence had only a very low number of dead trees. The slightly better fit of the model in this study is probably due the uniformity of the experimental stands and the smaller geographic area they represent (26 km 12 km versus 200 km 200 km). Furthermore, as cut trees have no resistance at all, the colonization of felled spruces is more predictable than the colonization of wind-felled spruces, which have varying degree of root connection and resistance. 4.2. I. typographus breeding success Breeding success in non-burned stands was significantly higher than in areas which had undergone burning treatment (Fig. 5). It also seems that burning treatment had a more devastating effect on offspring survival in areas with a high DWR level (60 m3) than at the two lowest levels. Actually, studies by Lilja et al. (2005) in the same experimental areas show that the living tree mortality, inside experimental areas was highest with a high DWR level, because the flames climbed up to the canopy, using down retention trees as a ‘‘ladder’’. Thus, the low breeding success at the highest level of DWR with burning treatment was attributable to the intensity of the fire. 4.3. Tree killing The number of trees killed, with I. typographus, in forest edges surrounding experimental stands during the three summers following the year when the treatments were applied, was overall very low (Fig. 2). The treatments, DWR level or burning, or the other predictors had no significant effect on tree deaths. Similar results have been obtained when using not more than five cut spruces (Hedgren et al., 2003) or when using
212
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213
wind-felled trees (Peltonen, 1999) on clear-cut forest edges. In both studies the number of dead standing spruces attacked by I. typographus did not depend on the amount of cut trees or windthrows at the same site. In another study, where the amount of wind-felled spruces per windthrow area is more comparable with that of our study, Schroeder and Lindelo¨w (2002) reported an almost perfect linear relationship between the number of wind-felled spruces colonized by I. typographus and the number of trees killed in the 4 years following the storm felling. Naturally our experimental stands differ from windthrow areas since the trees were cut down leaving no root contact left, which lead to rapid desiccation of the felled trees. While I. typographus can successfully breed in 2 year old wind-felled spruces (Butovitsch, 1971; Annila and Peta¨isto¨, 1978; Go¨thlin et al., 2000; Eriksson et al., 2005) the rapid desiccation of cut trees means that successful breeding is possible only during the first summer after cutting. Since there were altogether 19 dead spruces in forest edges surrounding stands that had not been burned and 10 where surrounding stands had been burned, the results do suggest that, with a larger sample size, burning might have had a considerable effect on tree deaths in surrounding forest edges. This would be understandable, because most of the bark beetles breeding in felled spruces were scorched alive in stands with burning treatment. Burning treatment might also be the source of some of the unexplained variation in the model, as in all our burning treatments patches were left unburned, and paludified biotopes contributed most to the stand heterogeneity of the burning mosaic (Lilja et al., 2005). Standing retention spruces that are not killed but slightly weakened might be very attractive for I. typographus in the years following the burning treatment. However, data based on window trappings (trunk window-traps) by Toivanen et al. (in prep.), in the same experimental areas, suggest that I. typographus colonized fire damaged spruces at a much lower intensity than they did girdled trees in non-burnt areas. Further studies concerning I. typographus are, however, needed to find out whether burning increases the attraction range of a stand with damaged trees. Another point requiring clarification concerns the potential of spruces damaged and weakened by fire to sustain or even increase I. typographus populations.
by the amount and quality of suitable breeding material. If the damaged trees are of very small diameter, for example, under 15 cm (D1.3), then the probability of attacks on nearby standing trees might increase. Logging residues probably have the same effect. It is, however, unlikely that restoration operations of this magnitude would have any long-distance effects as earlier studies indicate that only years of large windfall episodes have a significant effect on the population level of I. typographus (Økland and Bjørnstad, 2003; Økland and Berryman, 2004). To minimize the risks of restoration, restorative operations should be avoided in the same area in consecutive years or after severe storms with windthrows, or at least considered thoroughly. Although no significant effects of burning treatment on tree deaths were found, it seems that burning after bark beetle colonization decreases the risks of restoration. This hypothesis is supported by our results, which showed a significant decrease in the breeding success of I. typographus. On the other hand, trees only mildly damaged by fire might become very susceptible to insect attacks in the years following the burning treatment and thereby increase the risk of further damage on nearby forest edges.
5. Conclusions
References
The risks involved in restoration, in terms of tree deaths seem to be minor, at least when populations of I. typographus are at endemic levels. However, large amounts of damaged trees seem to attract more beetles than smaller amounts. Beetles probably use the volatiles from injured or decaying trees (Lindelo¨w and Risberg, 1992) as a cue when seeking out suitable host trees. Obviously I. typographus cannot discriminate between suitable (large enough) and unsuitable spruces simply on the basis of host volatiles. Thus, the number of beetles, arriving in stand with damaged trees is probably the result of interaction between the amount of host volatiles, the local bark beetle population levels and weather conditions. Furthermore, the number of colonizing beetles is also affected
Acknowledgements We would like to thank all those who participated in the burning activities and field inventory work, especially Liina Kjellberg, Tero Toivanen, and Veli Liikanen for their assistance in insect inventories, Seppo Neuvonen for his valuable comments on the manuscript, and Rosemary Mackenzie for checking the English. The Ha¨me Polytechnic, the Finnish Forest and Park Service, UPM-Kymmene Ltd., the City of Ha¨meenlinna and the Finnish Forest Research Institute provided the stands for the study and implemented the treatments. This study was funded by the Finnish Ministry of Agriculture and Forestry and the Graduate School in Forest Sciences. The study is part of the FIRE-project in the Sustainable use of Natural Resources (SUNARE) 2001–2004 program financed by the Academy of Finland and part of the EU-project forest fire spread prevention and mitigation (SPREAD).
Ahti, T., Ha¨met-Ahti, L., Jalas, J., 1968. Vegetation zones and their sections in northwestern Europe. Ann. Bot. Fenn. 5, 169–211. Annila, E., Peta¨isto¨, R.-L., 1978. Insect attack on windthrown trees after the december 1975 storm in western Finland. Commun. Inst. For. Fenn. 94, 1– 24. Anon, 2002. Etela¨-Suomen, Oulun la¨a¨nin la¨nsiosan ja Lapin la¨a¨nin lounaisosan metsien monimuotoisuuden turvaamisen toimintaohjelma. Ehdotus Etela¨Suomen, Oulun la¨a¨nin la¨nsiosan ja Lounais-Lapin metsien suojelun tavoite, rahoitus-, ja toimintaohjelmaksi. Etela¨-Suomen metsien suojelutoimikunta (Metso) (in Finnish). Anon, 2003. Restoration in protected areas, report by the working group on restoration 2003. The Finnish Environment. 618, 1–220 (in Finnish with Abstract in English). Austara˚, O., Bakke, A., Midtgaard, F., 1986. Response in Ips typographus to logging waste odours and synthetic pheromones. J. Appl. Ent. 101, 194– 198.
M. Eriksson et al. / Forest Ecology and Management 231 (2006) 205–213 Bradshaw, A.D., 1997. What do we mean by restoration? In: Urbanska, K.M., Webb, N.R., Edwards, P.J. (Eds.), Restoration ecology and sustainable development. Cambridge University Press, Cambridge, U.K., pp. 8–14. Butovitsch, V., 1938. Om granbarkborrens massfo¨ro¨kning i so¨dra Dalarna. Norrl. Skogsv. Fo¨rb. Tidskr. Ha¨fte 2, 1–36 (in Swedish with abstract in German). Butovitsch, V., 1971. Underso¨kningar o¨ver skadeinsekternas upptra¨dande i de stormha¨rjade skogarna i mellersta Norrlands kustland a˚ren 1967–1969. Inst. Skogszool. Rapp. Upps. 8, 1–204 (in Swedish). Cajander, A.K., 1926. The theory of forest types. Acta Forestalia. Fennica. 29, 1–108. Crawley, M.J., 2003. Statistical Computing. John Wiley & Sons Ltd., Wiltshire. Eriksson, M., Pouttu, A., Roininen, H., 2005. The influence of windthrow area and timber characteristics on colonization of wind-felled spruces by Ips typographus (L.). For. Ecol. Manage. 216, 105–116. Esseen, P.A., Ehnstro¨m, B., Ericson, L., Sjo¨berg, K., 1997. Boreal forests. Ecol. Bull. 46, 16–47. Franklin, A.J., Debruyne, C., Gre´goire, J.-C., 2000. Recapture of Ips typographus L. (Col., Scolytidae) with attractants of low release rates, localized dispersion and environmental influences. Agric. For. Entomol. 2, 259–270. Fridman, J., Walheim, M., 2000. Amount, structure and dynamics of dead wood on managed forestland in Sweden. For. Ecol. Manage. 31, 23–26. ˚ ., 2000. Attacks by Ips typographus Go¨thlin, E., Schroeder, L.M., Lindelo¨w, A and Pityogenes chalcographus on windthrown spruces (Picea abies) during the two years following a storm felling. Scand. J. Forest Res. 15, 542–549. Hedgren, P.O., 2004. The bark beetle Pityogenes chalcographus (L.) (Scolytidae) in living trees, reproductive success, tree mortality and interaction with Ips typographus. J. Appl. Ent. 128, 161–166. Hedgren, P.O., Schroeder, L.M., Weslien, J., 2003. Tree killing by Ips typographus (Coleoptera: Scolytidae) at stand edges with and without colonized felled spruce trees. Agric. For. Entomol. 5, 67–74. Jonsell, M., Weslien, J., Ehnstro¨m, B., 1998. Subtrate requirements of red-listed saproxylic invertebrates in Sweden. Biodiver. Conserv. 7, 749–764. Kuuluvainen, T., Tukia, H., Aapala, K., 2005. Ecological restoration of forested ecosystems in Finland. in: Stanturf, J.A., Madsen, P. (Eds.), Restoration of boreal and temperate forests. pp. 285–298, ISBN 1-56670-635-1. Laasasenaho, J., 1982. Taper curve and volume functions for pine, spruce and birch. Comm. Inst. For. Fenn. 108, 1–74. Lekander, B., 1972. A mass outbreak of Ips typographus in Ga¨strikland, Central Sweden, in 1945–1952. Department of Forest Zoology, Research notes, 10. Royal College of Forestry, Stockholm (in Swedish with English summary). Lemberg, T., Puttonen, P., 2003. Kulottajan ka¨sikirja. Metsa¨lehti kustannus, Vammalan kirjapaino Oy. pp. 113. ISBN 952-5118-41-X (in Finnish).
213
Lilja, S., de Chantal, M., Kuuluvainen, T., Vanha-Majamaa, I., Puttonen, P., 2005. Restoring natural characteristics in boreal Norway spruce (Picea abies L. Karst) stands with partial cutting, dead wood creation and fire, immediate treatment effects. Scan. J. For. Res. 20 (Suppl. 6), 68– 78. ˚ ., Risberg, B., 1992. Attraction during flight of scolytids and other Lindelo¨w, A bark- and wood-dwelling beetles to volatiles from fresh and stored spruce wood. Can. J. For. Res. 22, 224–228. Mulock, P., Christiansen, E., 1986. The threshold of successful attack by Ips typographus on Picea abies, a field experiment. For. Ecol. Manage. 14, 125– 132. Økland, B., Bjørnstad, O.N., 2003. Synchrony and geographical variation of the spruce bark beetle (Ips typographus) during a non-epidemic period. Population Ecol. 45, 213–219. Økland, B., Berryman, A., 2004. Resource dynamic plays a key role in regional fluctuations of the spruce bark beetles Ips typographus. Agr. For. Entom. 6, 141–146. Peltonen, M., 1999. Windthrows and dead-standing trees as bark beetle breeding material at forest-clearcut edge. Scand. J. Forest Res. 14, 505–511. R Development Core Team, 2005. R, A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org. Saalas, U., 1949. Suomen metsa¨hyo¨nteiset. Werner So¨derstro¨m Oy, Porvoo, Helsinki (in Finnish). Schroeder, L.M., 2001. Tree mortality by the bark beetle Ips typographus (L.) in storm-disturbed stands. Int. Pest Manage. Rev. 6, 169–175. ˚ ., 2002. Attacks on living spruce trees by the bark Schroeder, L.M., Lindelo¨w, A beetle Ips typographus (Col. Scolytidae) following a storm felling, a comparison between stands with and without removal of wind felled trees. Agr. For. Entom. 4, 47–56. Siitonen, J., 2001. Forest management, coarse woody debris and saproxylic organisms. Fennoscandian boreal forests as an example. Ecol. Bull. 49, 11– 39. Siitonen, J., Martikainen, P., Punttila, P., Rauh, J., 2000. Coarse woody debris and stand characteristics in mature managed and old-growth boreal mesic forests in southern Finland. For. Ecol. Manage. 128, 211–225. Tomppo, E., Henttonen, H., Korhonen, K., Aarnio, A., Ahola, A., Ihalainen, A., Heikkinen, J., Tuomainen, T., 1999. Keski-Suomen metsa¨keskuksen alueen metsa¨varat ja niiden kehitys 1967–1996. Metsa¨tieteen aikakausikirja 2B/ 1999, 309–387 (in Finnish). Wedderburn, 1974. Quasi-likelihood functions, generalized linear models, and the Gauss–Newton method. Biometrika 61, 439–447.