Forest Ecology and Management

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1 Forest Ecology and Management 257 (2009) Contents lists available at ScienceDirect Forest Ecology and Management journal homepage: Effects of forest restoration treatments on the abundance of bark beetles in Norway spruce forests of southern Finland Tero Toivanen a, *, Veli Liikanen a, Janne S. Kotiaho a,b a Department of Biological and Environmental Science, PO Box 35, University of Jyväskylä, Jyväskylä, Finland b Natural History Museum, PO Box 35, University of Jyväskylä, Jyväskylä, Finland ARTICLE INFO ABSTRACT Article history: Received 18 December 2007 Received in revised form 19 August 2008 Accepted 21 August 2008 Keywords: Boreal forests Controlled burning Dead wood Harvesting Pest management Scolytinae Restoration of protected areas in boreal forests frequently includes creating substantial volumes of dead wood. While this benefits a wide range of dead wood dependent invertebrate species, some of these are regarded as forest pests. Therefore, the risk of elevated levels of tree mortality in surrounding commercial forests must be considered. In a large-scale field experiment in southern Finland, we studied the effects of restoration treatments on the abundance of bark beetles within and in the vicinity of restored areas, in particular focusing on Ips typographus and Pityogenes chalcographus. The treatments applied to managed Norway spruce forests were controlled burning and partial harvesting combined with retaining 5, 30 or 60 m 3 /ha of cut down wood. We found that the abundance of bark beetles increased by both burning and harvesting with down wood retention, being highest where burning and harvesting had been combined. The actual volume of down wood retention had no significant effect. The effect of burning on the number of bark beetles along host tree boles was negative which suggests that burnt spruces provided a less suitable resource for bark beetles than unburnt dead spruces. The abundance of bark beetles along host trees also decreased with increasing volume of down wood retention. The abundance of P. chalographus was slightly elevated up to 50 m outside restored areas but the abundance was very low compared to that within the areas. The abundance of I. typographus was extremely low outside restored areas. We conclude that restoration treatments increase the abundance of bark beetles via increased availability of resources, but that the effect of burning is likely to be counteracted by decreased resource quality. Thus, burning might be the safest way to produce large quantities of dead wood. Furthermore, the fact that only few beetles were collected in adjacent areas suggests that restored areas pose little threat of serving as refugia in which bark beetle populations increase in sufficient numbers to attack live trees in adjacent forests. However, restoration actions repeated at consecutive years within a small area might enable the populations to grow to outbreak levels. ß 2008 Elsevier B.V. All rights reserved. 1. Introduction Restoration-oriented approach to forest management and conservation is needed to protect the biodiversity of boreal forests (Kouki et al., 2001; Kuuluvainen et al., 2002). Today, natural disturbance dynamics are often used as a guideline to develop sustainable forest management practices and restoration methods that enable the persistence of natural processes, structures and species composition in human-utilized ecosystems (Fries et al., 1997; Angelstam, 1998; Bergeron et al., 2002; Kuuluvainen et al., 2002). In boreal forests of Fennoscandia, the most commonly used restoration tools have been reintroducing fire to the boreal forest * Corresponding author. Tel.: ; fax: address: tertoiv@cc.jyu.fi (T. Toivanen). ecosystem and increasing the volume of dead wood at protected areas that have formerly been under intensive forest management. Forest restoration is likely to be effective in maintaining and increasing species diversity since it benefits a large number of saproxylic (dead wood dependent) species, and rare and red-listed (IUCN classes CR, EN, VU and NT) species in particular (Hyvärinen et al., 2006; Toivanen and Kotiaho, 2007). However, restoration practices that create substantial volumes of dead wood can also be seen to form a contradiction with the traditional view of forest hygiene. For example, the Forest Insect and Fungal Damage Prevention Act of Finland obligates forest owners to remove windfelled trees from the forest if the proportion of damaged trees is >10% of the total number of trees or if the damaged conifers form groups of >20 trees (Anonym, 1991). These thresholds are not based on data from any specific studies (Eriksson et al., 2005), but it is nevertheless clear that the number of dead and weakened trees /$ see front matter ß 2008 Elsevier B.V. All rights reserved. doi: /j.foreco

2 118 T. Toivanen et al. / Forest Ecology and Management 257 (2009) created in restoration practices (controlled burning in particular) is so high that it might eventually result in an increase of bark beetle species that are typically regarded as forest pests capable of attacking vigorous trees. Therefore, restoration of protected areas may cause a risk that forest damage will occur at nearby commercial forests and thus the economic risks should also be considered in planning restoration treatments and in studying the effects of restoration. Bark beetles (Coleoptera: Curculionidae, Scolytinae) are the most abundant group colonizing recently killed and weakened trees. Bark beetles are an essential component in forest ecosystem dynamics as they often start the decomposition of wood (Wermelinger, 2004), provide resources for a large number of associated species (Weslien, 1992) and may even facilitate forest succession by creating disturbances of various scales (Martikainen et al., 1999). Under certain conditions, in particular when a surplus of breeding material is available (Mulock and Christiansen, 1986), bark beetle populations may increase such that the species are able to attack vigorous trees and overcome host tree defenses. The spruce bark beetle, Ips typographus (L.), is regarded as the most significant forest pest in Europe. In Norway spruce (Picea abies [L.] Karst) forests in Central Europe, there have been many massive outbreaks of I. typographus after severe windstorms or tree deaths caused by heavy snow load that have caused significant forest damage during the last decades (Wermelinger, 2004). In Northern Europe, outbreaks leading to large-scale forest damage have been scarce (see Christiansen and Bakke, 1988; Eidmann, 1992). For example, in Finland no extensive outbreaks have been reported (Eriksson et al., 2005). This is likely due to the fact that I. typographus is able to produce only one generation per year at northern latitudes (Sauvard, 2004; Johansson et al., 2006). However, it is worth noting that several univoltine bark beetles (e.g., mountain pine beetle, Dendroctonus ponderosae Hopkins, in North America) are capable of causing large-scale forest damage (Westfall and Ebata, 2008). In Europe, Pityogenes chalcographus (L.) is sometimes mentioned as a potential forest pest that can occasionally attack stands of young Norway spruce. It is unclear to what extent P. chalcographus can overcome the defenses of vigorous trees, but it seems unlikely to cause tree deaths in the absence of attack by other bark beetle species (Hedgren, 2004). This may be due to the fact that, unlike I. typographus, P. chalcographus is not consistently associated with tree-killing fungi (Krokene and Solheim, 1996). In the absence of large-scale disturbances, populations of bark beetles are likely to remain at endemic levels in natural forests (Martikainen et al., 1999). It has been suggested that intensively managed forests may be more susceptible to bark beetle outbreaks (Martikainen et al., 1999) due to the favourable microclimates (Väisänen et al., 1993), a lack of predators and competition (Nuorteva, 1968; Schlyter and Lundgren, 1993), and a lack of heterogeneity in tree genetics, age structure of trees and forest structure and composition (Wermelinger, 2004). In addition, managed forests may provide a relatively high amount of breeding material for bark beetles due to the abundance of logging residues and the increased probability of windfalls at forest edges (Schlyter and Lundgren, 1993). In managed forests, I. typographus is known to be able to kill solitary healthy trees at the margin of recently harvested areas (Peltonen, 1999; Hedgren et al., 2003). To reduce the amount of bark-beetle-caused tree mortality in managed forests, thinning to reduce tree competition and increase individual tree growth, shorter rotation times, and maintenance of multiple tree species and age classes, are often suggested (Fettig et al., 2007). To minimize the socioeconomic risks, restoration practices are not recommended in the vicinity of privately owned lands in Finland (Kuuluvainen et al., 2002). However, this recommendation is not based on empirical evidence and there are practically no studies concerning the negative effects of forest restoration on the abundance of forest pests. Here, we report the results of a study focusing on the effects of restoration on the abundance and dispersal of bark beetles. In a large-scale field experiment, the treatments applied included controlled burning and partial harvesting with down wood retention (DWR). We sought to determine: (1) whether treatments increase the abundance of bark beetles within restored areas; (2) what is the effect of burning and harvesting on the number of bark beetles along host tree boles; and (3) whether restoration treatments result in elevated abundance of bark beetles in adjacent, untreated forests and whether there is a risk of elevated tree mortality in those forests. 2. Materials and methods 2.1. Study plots The study area was located in the vicinity of Evo, southern Finland ( N, E, altitude m), within the south boreal vegetation zone. For the study, 24 two-hectare plots located within 25 km 15 km area were selected. The lands were owned by Finnish Forest and Park Service (6 plots), Finnish Forest Research Institute (4), forest product company UPM (4), Häme Polytechnic University of Applied Sciences (6), and the town of Hämeenlinna (4). All of the plots were originally on average 80-year-old managed mesic forests. The initial volume of standing wood on the plots was m 3 /ha (mean S.D.) and the volume of dead wood m 3 /ha. The volumes of living or dead wood did not differ between the plots (Lilja et al., 2005). Dead wood consisted almost exclusively of logging waste, i.e., small-diameter (<20 cm) logs and cut stumps (Lilja et al., 2005). The dominant tree species of the plots (i.e., about 90% of the volume of standing trees) was Norway spruce with some birch (Betula spp.) and Scots pine (Pinus sylvestris L.) Experimental design Controlled burning and partial harvesting with DWR were applied as restoration treatments at the study plots. During February and March 2002, 18 plots were harvested such that the volume of standing retention trees was set to 50 m 3 /ha. On the harvested plots, 5, 30 or 60 m 3 /ha of cut down wood was retained (six plots of each DWR treatment). Six study plots were left unharvested. In summer 2002, 12 study plots (9 harvested and 3 unharvested plots) were burnt. The first five burnings were conducted in mid-june, the following five in mid-july and the last two in the beginning of August (for detailed description of the treatments, see Lilja et al., 2005). In addition, to allow us to compare burnt and unburnt host trees, three Norway spruces were killed by mechanical girdling (stripping off a piece of bark at 1.3 m height to prevent water and nutrient flow) at each unburnt plot in the beginning of June Sampling of beetles To study the effect of restoration treatments on the relative abundances of bark beetles, beetles were sampled with flightintercept traps. The traps consisted of two crosswise-set transparent plastic panes with a funnel and container below them. The traps were set hanging from a string between two trees or poles in order to collect samples independent of the effect of individual host trees. Saline water with detergent was used in the containers to preserve the beetles. Five traps were set in random locations at each study plot. The trapping period was 10 May to 10 September To study the effect of restoration on the numbers of bark beetles along host tree boles, we used window traps attached to recently dead standing trees. The upper edge of the funnel was modified

3 T. Toivanen et al. / Forest Ecology and Management 257 (2009) heart-shaped such that the length that it touched the tree trunk was about 25 cm. We selected three burnt spruces at each of the burnt plots and three girdled spruces at each of the unburnt plots. The trapping period was 10 May to 10 July To study the effect of restoration on the abundance of bark beetles in forests adjacent to restored areas, we constructed a line of six free-hanging flight-intercept traps perpendicular to the edge of the study plots. Traps were located 25 m inside each plot, at the edge of each plot, and at 25, 50, 75 and 100 m outside each plot. The trapping period was 10 May to 10 July 2003, which covers the main dispersal season of I. typographus and P. chalcographus in Finland (Heliövaara et al., 1998) Statistical analyses The analyses were performed with SPSS 13.0 for Windows software (SPSS Inc., Chicago, Illinois). In all the analyses, we analyzed the effects of the restoration treatments on the total number of bark beetles and on the abundances of the species that are most likely to attack healthy trees (I. typographus and P. chalcographus). The species abundance data were log 10 (x + 1)- transformed before the analyses. To analyze the effect of treatments on the abundance of bark beetles, we used the pooled data of the five free-hanging traps of each study plot. We used two-way ANOVA in which the factors were burning (burnt or unburnt) and harvesting with DWR (unharvested, harvested with 5, 30, and 60 m 3 /ha DWR, respectively) followed by Tukey s pairwise comparisons. If there was an interaction between factors, the ANOVA was followed by simple effects tests and pairwise comparisons. The effect of treatments on the number of bark beetles along host trees was analyzed with two-way ANOVA in which the factors were burning (burnt or unburnt [girdled] spruce) and harvesting with DWR. Data from three spruces on each plot was pooled for the analysis. If there was an interaction between factors, the ANOVA was followed by simple effects tests and pairwise comparisons. To analyse how the abundance of bark beetles changed with the distance from restored areas, the treatments were grouped in four classes (burnt harvested, burnt unharvested, unburnt harvested and unburnt unharvested). The volume of DWR on the harvested plots was not included since it had only minor effect on the abundance of bark beetles within restored areas (see results). The effects of distance and treatment on the abundance of bark beetles were analyzed with repeated measures factorial ANOVA followed by simple effects tests and pairwise comparisons. 3. Results 3.1. The effect of restoration treatments on the abundance of bark beetles In total, we collected 21,695 bark beetles representing 33 species, including 421 I. typographus and 9487 P. chalcographus (which was the most numerous species), in flight-intercept traps (Table 1). In Table 1 The total number of bark beetle individuals collected in flight-intercept traps within restored plots (N = 120) in 10 May to 10 September 2003, in traps attached to boles of dead Norway spruces (N = 72) in 10 May to 10 July 2003, and in traps along lines perpendicular to the edge of restored plots (N = 144) in 10 May to 10 July 2003 Species Flight-intercept traps Traps attached to host trees Trap lines Cryphalus saltuarius Weise Crypturgus cinereus (Herbst) Crypturgus hispidulus Thomson Crypturgus pusillus (Gyllenhal) Crypturgus subcribrosus Eggers 295 2, Dendroctonus micans (Kugelann) Dryocoetes autographus (Ratzeburg) 3,368 5, Dryocoetes hectographus Reitter Hylastes brunneus Erichson 329 3, Hylastes cunicularius Erichson 4,017 26, Hylastes opacus Erichson 263 2, Hylurgops glabratus (Zetterstedt) Hylurgops palliatus (Gyllenhal) 280 1, Ips amitinus (Eichoff) Ips typographus (Linnaeus) 421 1, Orthotomicus laricis (Fabricius) Orthotomicus proximus (Eichoff) Orthotomicus suturalis (Gyllenhal) 301 1, Phloeotribus spinulosus (Rey) Pityogenes bidentatus (Herbst) Pityogenes chalcographus (Linnaeus) 9,478 23, Pityogenes quadridens (Hartig) Pityophthorus lichtensteini (Ratzeburg) Pityophthorus micrographus (Linnaeus) Polygraphus poligraphus (Linnaeus) Polygraphus punctifrons Thomson Polygraphus subopacus Thomson Scolytus ratzeburgi Janson Tomicus minor (Hartig) Tomicus piniperda (Linnaeus) Trypodendron domesticum (Linnaeus) Trypodendron lineatum (Olivier) 1,550 3, Trypodendron laeve Eggers Trypodendron signatum (Fabricius) Trypophloeus bispinulus Eggers Xyleborus dispar (Fabricius) Xylechinus pilosus (Ratzeburg) Total 21,695 75,

4 120 T. Toivanen et al. / Forest Ecology and Management 257 (2009) Table 2 The simple effects tests for the effects of burning and harvesting with DWR on the abundance of bark beetles Species Factor Simple effects test F p All Burning Among unharvested F 1,16 = <0.001 Among DWR5 F 1,16 = <0.001 Among DWR30 F 1,16 = Among DWR60 F 1,16 = Harvesting Among burnt F 3,16 = with DWR Among unburnt F 3,16 = I. typographus Burning Among unharvested F 1,16 = <0.001 Among DWR5 F 1,16 = <0.001 Among DWR30 F 1,16 = Among DWR60 F 1,16 = Harvesting Among burnt F 3,16 = with DWR Among unburnt F 3,16 = P. chalcographus Burning Among unharvested F 1,16 = <0.001 Among DWR5 F 1,16 = Among DWR30 F 1,16 = Among DWR60 F 1,16 = Harvesting Among burnt F 3,16 = with DWR Among unburnt F 3,16 = <0.001 general, the total number of bark beetles collected was positively affected by burning (F 1,16 = 65.03, p < 0.001) and by harvesting with down wood retention (DWR) (F 1,16 =6.01,p = 0.006) but there was an interaction between the factors (F 1,16 =5.34,p = 0.010). The effect of burning was not significant among harvested with 60 m 3 /ha DWR treatment, and the effect of harvesting with DWR was significant among unburnt treatment but not among burnt treatment (Table 2). Among unburnt treatment, the number of bark beetles collected was increased by harvesting but the volume of DWR had no effect (Table 3). The number of I. typographus collected was positively affected by burning (F 1,16 = 36.31, p < 0.001) and by harvesting with DWR (F 1,16 = 4.90, p = 0.013) but there was an interaction between the factors (F 1,16 = 4.76, p = 0.015) (Fig. 1). Burning increased the number of I. typographus among unharvested and harvested with 5m 3 /ha DWR treatments but not among harvested with 30 and 60 m 3 /ha DWR treatments (Table 2). Among unburnt treatment, the number of I. typographus collected was increased by harvesting but the volume of DWR had no effect (Table 3). Among burnt treatment, more I. typographus were collected on harvested with 5m 3 /ha DWR treatment than on other treatments (Table 3). Fig. 1. The effect of burning and harvesting with DWR on the number of I. typographus collected in five flight-intercept traps in 10 May to 10 September 2003 (mean S.E., N = 3 in each treatment). The number of P. chalcographus collected was positively affected by burning (F 1,16 = 44.25, p < 0.001) and by harvesting with DWR (F 1,16 = 20.39, p < 0.001) but there was an interaction between the factors (F 1,16 = 14.18, p < 0.001) (Fig. 2). The effect of burning was not significant among harvested with 60 m 3 /ha DWR treatment, and the effect of harvesting with DWR was significant among unburnt treatment but not among burnt treatment (Table 2). Among unburnt treatment, the number of P. chalcographus collected was increased by harvesting but the volume of DWR had no effect (Table 3) The effect of fire, harvesting and DWR on the number of bark beetles along host trees In total, we collected 75,110 bark beetles representing 29 species, including 1941 I. typographus and 23,585 P. chalcographus, along the boles of recently killed Norway spruce (Table 1). The total Table 3 The pairwise comparisons following the simple effects tests for the effects of harvesting with DWR on the abundance of bark beetles Species Comparison Unburnt plots MD a p Burnt plots MD a p All Unharvested vs. DWR Unharvested vs. DWR < Unharvested vs. DWR < DWR5 vs. DWR DWR5 vs. DWR DWR30 vs. DWR I. typographus Unharvested vs. DWR Unharvested vs. DWR Unharvested vs. DWR DWR5 vs. DWR DWR5 vs. DWR DWR30 vs. DWR P. chalcographus Unharvested vs. DWR < Unharvested vs. DWR < Unharvested vs. DWR < DWR5 vs. DWR DWR5 vs. DWR DWR30 vs. DWR a Mean difference between treatments. The abundances have been log-transformed.

5 T. Toivanen et al. / Forest Ecology and Management 257 (2009) Table 4 The simple effects tests for the effects of burning and harvesting with DWR on the number of bark beetles along host tree boles Species Factor Simple effects test F p I. typographus Burning Among unharvested F 1,16 = Among DWR5 F 1,16 = Among DWR30 F 1,16 = Among DWR60 F 1,16 = Harvesting Among burnt F 3,16 = with DWR Among unburnt F 3,16 = P. chalcographus Burning Among unharvested F 1,16 = Among DWR5 F 1,16 = <0.001 Among DWR30 F 1,16 = Among DWR60 F 1,16 = Harvesting Among burnt F 3,16 = with DWR Among unburnt F 3,16 = <0.001 Fig. 2. The effect of burning and harvesting with DWR on the number of P. chalcographus collected in five flight-intercept traps in 10 May to 10 September 2003 (mean S.E., N = 3 in each treatment). number of bark beetles in traps attached to dead spruces was decreased by burning (F 1,16 = 23.76, p < 0.001), affected by harvesting with DWR (F 3,16 =4.42,p = 0.019) and there was no interaction between the factors (F 3,16 =0.12, p = 0.948). The number of bark beetles collected on harvested with 5 m 3 /ha DWR treatment was higher than on unharvested treatment (Tukey s pairwise comparison, p = 0.028), and it tended to be higher than on harvested with 60 m 3 /ha DWR treatment (p =0.062). The number of I. typographus in traps attached to dead spruces was decreased by burning (F 1,16 = 25.52, p < 0.001) and increased by harvesting with DWR (F 3,16 = 4.33, p = 0.020) (Fig. 3). There was no significant interaction between the factors (F 3,16 = 2.13, p = 0.137), but nevertheless the simple effects test revealed that the effect of burning was not significant among unharvested treatment and that harvesting with DWR did not affect the number of I. typographus among traps attached to burnt spruces (Table 4). Among traps attached to unburnt spruces, the number of I. typographus was higher on harvested than on unharvested treatment but the volume of DWR had no effect (Table 5). The number of P. chalcographus in traps attached to dead spruces was decreased by burning (F 1,16 = 19.10, p < 0.001), affected by harvesting with DWR (F 3,16 = 11.27, p < 0.001) and there was an interaction between the factors (F 3,16 = 13.30, p < 0.001) (Fig. 4). Among unharvested treatment, more P. chalcographus was collected in traps attached to burnt spruces than in those attached to unburnt spruces, but among harvested with DWR treatments, more P. chalcographus was collected in traps attached to unburnt spruces than in those attached to burnt spruces (Table 4). Among traps attached to unburnt spruces, more P. chalcographus were collected on harvested with DWR treatments than on unharvested treatment, and the number of P. chalcographus was higher on harvested with 5 m 3 /ha than on harvested with 60 m 3 /ha DWR treatment (Table 5). Among traps attached to burnt spruces, less P. chalcographus were collected on harvested Fig. 3. The effect of burning and harvesting with DWR on the number of I. typographus collected in three traps attached to dead Norway spruces in 10 May to 10 July 2003 (mean S.E., N = 3 in each treatment). Fig. 4. The effect of burning and harvesting with DWR on the number of P. chalcographus collected in three traps attached to dead Norway spruces in 10 May to 10 July 2003 (mean S.E., N = 3 in each treatment).

6 122 T. Toivanen et al. / Forest Ecology and Management 257 (2009) Table 5 The pairwise comparisons following the simple effects tests for the effects of harvesting with DWR on the number of bark beetles along host tree boles Species Comparison Unburnt plots MD a p Burnt plots MD a p I. typographus Unharvested vs. DWR Unharvested vs. DWR Unharvested vs. DWR DWR5 vs. DWR DWR5 vs. DWR DWR30 vs. DWR P. chalcographus Unharvested vs. DWR < Unharvested vs. DWR < Unharvested vs. DWR < DWR5 vs. DWR DWR5 vs. DWR DWR30 vs. DWR a Mean difference between treatments. The abundances have been log-transformed. with 60 m 3 /ha DWR treatment than on other harvested with DWR treatments (Table 5) The abundance of bark beetles in forests adjacent to restored areas In total, we collected 9441 bark beetle individuals representing 32 species, including 82 I. typographus and 3182 P. chalcographus, in traps along the lines leading to adjacent forests (Table 1). The number of bark beetles collected was affected by distance from the plot (F 5,100 = 29.68, p < 0.001) and treatment (F 3,20 = 6.20, p = 0.004) and there was interaction between treatment and distance (F 15,100 = 2.89, p = 0.001) (Fig. 5). Inside the plots (simple effects test: F 3,20 = 17.68, p < 0.001), the number of bark beetles was higher on restored than on control treatments (pairwise comparisons: burnt harvested vs. control, p < 0.001; burnt unharvested vs. control, p < 0.001; unburnt harvested vs. control, p = 0.001). At the edge of the plots (simple effects test: F 3,20 = 6.75, p = 0.003), restoration treatments still increased the number of bark beetles (burnt harvested vs. control, p < 0.001; burnt unharvested vs. control, p = 0.043; unburnt harvested vs. control, p = 0.002). At 25 m outside the plots, there was no general treatment effect (simple effects test, F 3,20 = 2.34, p = 0.105) but burnt harvested treatment differed from control (pairwise comparison, p = 0.048). At 50, 75 and 100 m outside the plots, there were no significant treatment effects (p > 0.21, all cases). The abundance of I. typographus was affected by distance (F 5,100 = 2.57, p = 0.031) and treatment (F 3,20 = 3.78, p = 0.027) but there was no interaction between distance and treatment (F 15,100 = 0.74, p = 0.742). No differences were found between restoration treatments and controls at any distance along the line (p > 0.08, all cases), but analyzing the abundance of I. typographus within the lines revealed some differences. Within burnt harvested treatment, the abundance of I. typographus was higher inside the plots than at 25, 50, 75, and 100 m outside the plots (pairwise comparisons, p < 0.01 in all comparisons). At the edge of the burnt harvested plots, there were more I. typographus than at 100 m outside the plots (pairwise comparison, p = 0.047) and there tended to be more I. typographus than at m outside the plots (pairwise comparisons, 0.05 < p < 0.10 in all comparisons). Within unburnt harvested treatment, the abundance of I. typographus was higher inside the plots (pairwise comparison, p = 0.045) and at the edge of the plots (pairwise comparison, p = 0.037) than at 50 m outside the plots, and the abundances inside the plots and at the Fig. 5. The effect of restoration treatments on the number of all bark beetles collected in flight-intercept traps along a line perpendicular to the edge of the study plots (one trap per distance) in 10 May to 10 July (mean S.E., N = 9 for harvested and N = 3 for unharvested treatments). Fig. 6. The effect of restoration treatments on the number of P. chalcographus collected in flight-intercept traps along a line perpendicular to the edge of the study plots (one trap per distance) in 10 May to 10 July 2003 (mean S.E., N = 9 for harvested and N = 3 for unharvested treatments).

7 T. Toivanen et al. / Forest Ecology and Management 257 (2009) edge of the plots tended to be higher than at 25, 75 and 100 m outside the plots (pairwise comparisons, 0.05 < p < 0.10 in all comparisons). Within burnt unharvested treatment, there were no significant differences among distances (p > 0.66, all cases). The abundance of P. chalcographus was affected by distance (F 5,100 = 63.60, p < 0.001) and treatment (F 3,20 = 11.57, p < 0.001) and there was an interaction between distance and treatment (F 15,100 = 4.58, p < 0.001) (Fig. 6). Inside the plots, the abundance of P. chalcographus was higher on restored than on control treatments (simple effects test: F 3,20 = 21.02, p < 0.001; pairwise comparisons: p < in all comparisons). At the plot edge, significantly more P. chalcographus were collected on restored than on control treatments (simple effects test: F 3,20 = 9.27, p < 0.001, pairwise comparisons, p < in all comparisons). The abundance of P. chalcographus was also elevated at 25 m outside the plots (simple effects test: F 3,20 = 3.32, p = 0.041; pairwise comparisons: burnt harvested vs. control, p < 0.005; burnt unharvested vs. control, p = 0.107; unburnt unharvested vs. control, p = 0.019) and at 50 m outside the plots (simple effects test: F 3,20 = 6.82, p = 0.002; pairwise comparisons: burnt harvested vs. control, p = 0.001, burnt unharvested vs. control, p = 0.058; unburnt unharvested vs. control, p = 0.055) At 75 and 100 m, no significant treatment effects were observed (p > 0.14, all cases). 4. Discussion 4.1. The effect of restoration on the abundance of bark beetles The abundance of bark beetles in flight-intercept traps increased by both burning and harvesting with DWR, being highest where burning and harvesting had been combined. On burnt harvested plots, mortality among the standing retention trees was very high, the majority of spruces dying immediately after the fire (Lilja et al., 2005). Therefore, the increase in the abundance of bark beetles was most likely caused by increase in the availability of resources and attraction of beetles to host volatiles (e.g., monoterpenes) released from weakened trees. However, the effect of burning was dependent on the volume of DWR such that burning increased the number of bark beetles at low or intermediate volume of DWR but not at high volume of DWR. This is likely due to the fact that the intensity of fire increased with the volume of DWR (Lilja et al., 2005) which may have decreased the quality of resources (discussed below). In a concurrent study that was conducted on the same restored areas, it was shown that the breeding success of I. typographus and P. chalcographus was generally low in burnt logs, and that it further decreased with increasing volume of DWR (Eriksson et al., 2006). While the volume of DWR had a negative effect on the abundance of bark beetles when burning was included (probably due to increased fire intensity), it had no clear effects without burning. Although larger amounts of damaged spruces generally attract more colonizing bark beetles into restored or windfall areas (Eriksson et al., 2005), the number of colonized logs was negatively correlated with the volume of DWR on the harvested plots of this restoration experiment (Eriksson et al., 2006). We found that the number of P. chalcographus collected along the boles of unburnt spruces decreased strongly with increasing DWR level. Thus, the number of bark beetles dispersing to the restored areas may have been restricted by the sizes of the source populations. Another possible explanation for the lack of effect of DWR level is that the harvested plots were characterized by the wealth of logging residue such as branches and cut stumps that is known to be utilized by several saproxylic species (Sippola et al., 2002), including also bark beetles such as P. chalcographus (Hedgren, 2004). The volume of logging residue was likely to be equal among all the harvesting with DWR treatments making the proportional differences in the amount of resources smaller between the treatments The effect of fire and harvesting on the abundance of bark beetles along host tree boles Samples collected in traps attached to host trees represent a collection of beetles emerging from and colonizing the trees and also reflect beetle activity around the trees. We found that the number of bark beetles in these traps was particularly high (compared to the flight-intercept traps, the number of beetles per trapping day was tenfold) and that the majority of beetles collected were newly emerged from the trees (i.e., callow adults identified by not fully developed coloration). This suggests that most of the beetles collected were truly associated to the particular trees. In addition, the treatment effects were not consistent with those observed by flight-intercept traps (i.e., burning increased the abundance of bark beetles in flight-intercept traps but less beetles were collected along burnt than unburnt host trees). Therefore, our interpretation is that samples collected in traps attached to host trees reflect the quality of the trees as breeding substrate for bark beetles and can thus be used as indirect measure of resource quality. However, results must be interpreted with some caution because the reproductive success of beetles was not directly measured. We found that the abundance of bark beetles was lower in the traps attached to burnt spruces than those attached to unburnt spruces, and that in particular the abundance of I. typographus was negatively affected by fire. In addition, the abundance of P. chalcographus in the traps attached to burnt spruces was lowest at highest volumes of DWR, at which the fire was most intense (Lilja et al., 2005), while the abundance of I. typographus in the traps was low at all harvesting with DWR levels. Thus, although burnt areas provide a wealth of dead wood resources for bark beetles and burning makes trees more susceptible to bark beetle attacks (Fettig et al., 2007), fire may decrease the nutritional quality of phloem material and burnt trees may desiccate rapidly making the resource less suitable for bark beetles (Wikars, 2002; Johansson et al., 2006). This effect may be particularly strong in Norway spruce because of its thin bark. The numbers of three common phloem-feeding bark beetle species have been found to be decreased in fire-damaged stands in pine forests in Florida (Hanula et al., 2002), and in particular heavily charred trees are known to host very low insect densities (Saint-Germain et al., 2004), although they may host high species diversity (Wikars, 2002). The abundance of bark beetles along tree boles was also affected by harvesting, and the effect differed between burnt and unburnt trees. Among traps attached to unburnt spruces, harvesting increased the number of bark beetles, which was probably due to that the logged habitat itself attracted more bark beetles because of sun-exposed conditions and volatiles released from logging residues. Sun-exposed disturbance areas are favoured by several dead wood dependent species (Kouki et al., 2001). For example, I. typographus (Peltonen, 1999; Göthlin et al., 2000) and P. chalcographus (Hedgren, 2004; Johansson et al., 2006), are known to prefer open areas and forest edges over forest interior. In contrast, among traps attached to burnt spruces, bark beetle numbers were negatively affected by harvesting, which is likely to reflect differences in the quality of dead wood resource. While the fires were intense on harvested plots, the unharvested plots did not burn particularly well and the proportion of trees directly killed by fire was low (see Lilja et al., 2005). Thus, the weakened trees on burnt unharvested plots may have provided a better resource to bark beetles compared to the heavily charred trees on burnt harvested plots.

8 124 T. Toivanen et al. / Forest Ecology and Management 257 (2009) The abundance of bark beetles and the risk of elevated tree mortality outside restored areas Bark beetles are capable of dispersing several kilometers in forests (Wermelinger, 2004). However, the majority of newly attacked trees by I. typographus have been found to occur within 100 m of an old attack (Wichmnann and Ravn, 2001). Thus, the spatial scale of our study to determine whether restoration treatments lead to elevated abundance of bark beetles outside restored areas appears reasonable. The abundance of bark beetles in the adjacent forests was studied during the flying season of the species of interest in the first post-treatment year (in 2003) based on the assumption that the primary colonizers had colonized the restored plots immediately after treatments (in 2002) and would disperse from the plots following successful reproduction. We found that although the abundance of bark beetles was strongly elevated within burnt and harvested plots, the numbers of bark beetles in the adjacent forests remained relatively low. Only few I. typographus were collected along the trap lines. Although the abundance of P. chalcographus was significantly elevated up to 50 m outside restored plots, abundances were nevertheless very low compared to that inside the plots. Eriksson et al. (2006) found that the number of dead spruces with I. typographus was very low at the edges of the harvested plots of this experiment during 3 years after treatments, and that there were no differences between the treatments. This suggests that bark beetles are not likely to disperse into the healthy forests around restored areas. Even if the abundance of bark beetles strongly increased after restoration treatments, it seems that the population densities did not reach the level in which bark beetles would have been able to attack live trees and overcome host defenses. The reasons for this may include reduced breeding success in fire-killed trees, originally small source populations, and the fact that all the dead wood was created simultaneously that led to lack of breeding material once the resource was fully utilized. However, if must be noted that if colonization is not limited by small size of source populations, providing large quantities of dead wood might enable the populations grow large enough to successfully attack healthy trees after the original resource has been exhausted Conclusions and practical implications Controlled burning and partial harvesting with DWR increased the number of bark beetles, including species that are potential forest pests of Norway spruce forests. The abundance of bark beetles was highest when restoration treatments included both burning and harvesting. This is likely due to burnt areas providing more resources for bark beetles than unburnt areas, however, burnt Norway spruces were a less suitable resource for bark beetles than unburnt dead spruces. In addition, the abundance of bark beetles on burnt areas decreased with the volume of DWR, probably because DWR levels also influenced fire intensity (Lilja et al., 2005) which may have negatively affected resource quality (e.g., nutritional quality of cambium and amount of moisture). Therefore, in terms of pest management, burning might be a safer way to create large quantities of dead wood than simply girdling or felling the trees. Without burning, the volume of DWR had no clear effect on the abundance of bark beetles, which may have been due to that the number of colonizing individuals was restricted by the size of source populations or that the effect of DWR was masked by the effect of logging residue. Under the conditions of our study, restoration does not seem to cause any severe risk of elevated levels of tree mortality in the adjacent forests. However, we note that creating large quantities of dead wood within a small area at consecutive years, or low-intensity burnings that do not directly kill the trees but make them susceptible to bark beetle attacks for several years, might enable the populations to grow to outbreak levels. The results we reported here may also not be applicable to other geographic regions, especially to those where I. typographus is able to produce more than one generation per year which is very unlikely in Finland. Acknowledgements The restoration experiment was established by the Forest Ecology section of the University of Helsinki, and we thank especially Timo Kuuluvainen, Saara Lilja and Pasi Puttonen for cooperation. The burning and harvesting treatments were carried out by the land-owners and helped by numerous students and volunteers. Jarno Nevalainen and Satu Kuntsi carried out a substantial part of beetle identification. Jarno Nevalainen helped also in the field work and the material was sorted by Satu Kuntsi and Elina Manninen. Two referees provided valuable comments on the manuscript. The study was funded by the MOSSE research program of the Ministry of Agriculture and Forestry, Otto A. Malm s Foundation (research grant to T.T.), Jenny and Antti Wihuri s Foundation (research grant to T.T.), Metsämiesten Säätiö Foundation (research grant to V.L.), The Academy of Finland and The Centre of Excellence in Evolutionary Research of University of Jyväskylä. 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