Bark beetles (Coleoptera, Scolytidae) and associated beetle species in mature managed and old-growth boreal forests in southern Finland

Forest Ecology and Management 116 (1999) 233±245

Bark beetles (Coleoptera, Scolytidae) and associated beetle species in mature managed and old-growth boreal forests in southern Finland Petri Martikainena,*, Juha Siitonenb, Lauri Kailac, Pekka Punttilad, Josef Rauhb a

University of Joensuu, Faculty of Forestry, P.O. Box 111, FIN-80101, Joensuu, Finland b Finnish Forest Research Institute, P.O. Box 18, FIN-01301, Vantaa, Finland c Finnish Museum of Natural History, University of Helsinki, P.O. Box 17, FIN-00014, Helsinki, Finland d Finnish Environment Institute, Nature and Land Use Division, P.O. Box 140, FIN-00251, Helsinki, Finland Received 27 February 1998; accepted 12 August 1998

Abstract We compared the assemblages of bark beetles and associated beetle species among mature and overmature managed, and oldgrowth Picea abies (L.) Karst. dominated mesic forests in southern Finland. We established 10, 11 and 9 sample plots in these categories, respectively, within an area of 35  80 km. We took the beetle samples by 10 window-¯ight traps in each 1 ha plot (total number of traps ˆ 300). The species richness of bark beetles was highest in old-growth, lowest in mature, and intermediate in overmature forests. This was due to the greater amount and diversity of decaying wood in old-growth forests. Bark beetles which are dependent on deciduous trees, especially Trypodendron signatum (F.), were signi®cantly more abundant in old-growth than in mature forests, obviously because deciduous trees have decreased in managed forests. The overall abundance of bark beetles was 23% higher in overmature and 30% higher in old-growth than in mature forests, but the differences were not statistically signi®cant. Primary bark beetles comprised only 1% of the total catch, indicating that in nonepidemic conditions secondary scolytids are much more abundant than primary ones in old spruce forests. The abundance of bark beetles was best correlated with the amount of recently dead wood of the stand characteristics studied. Species associated with bark beetles showed patterns similar to those in bark beetles. The number of species was signi®cantly higher in oldgrowth than in mature forests. The abundance of associated species was 61% higher in overmature and 89% higher in oldgrowth than in mature forests, although these differences were not statistically signi®cant because of large inter-stand variation. It is thus likely that in the absence of major disturbances, the populations of primary bark beetles will stay at nonepidemic levels in old-growth forests. The species spectrum of bark beetles and their enemies could be broadened by promoting a deciduous mixture and improving the supply of dead trees in managed forests. This would also be bene®cial to the conservation of species diversity in the managed forest landscape. # 1999 Elsevier Science B.V. All rights reserved. Keywords: Biodiversity; Coarse woody debris; Forest hygiene; Natural enemies; Old-growth; Pest insects

*Corresponding author. Tel.: +358-13-2514064; fax: +358-13-2514444; e-mail: [email protected] 0378-1127/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved. PII: S0378-1127(98)00462-9

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1. Introduction Intensive forest management, including regular thinnings and relatively short rotation cycles, has traditionally been considered as a method to control the population levels of bark beetles (e.g. Christiansen and Bakke, 1988; Schwenke, 1996). Removal of recently dead and weakened trees is supposed to keep the amount of suitable breeding material low and thus limit the numbers of bark beetles. This kind of management (so called forest hygiene, e.g. Schimitschek, 1969) is suggested to decrease the risk of outbreaks especially in situations where trees are temporarily weakened for some reason and thus pre-disposed to beetle attack (Schwenke, 1996). Alternatively, intensive management may actually give opportunities for pest populations to increase (Schowalter and Filip, 1993). Regularly thinned managed stands are relatively open and have a more favourable microclimate for certain primary scolytids (species that can successfully attack live trees), such as Ips typographus (L.) (Nuorteva, 1968; VaÈisaÈnen et al., 1993). A higher amount of optimal breeding material may be maintained in managed forests through windfalls at newly exposed forest edges, logging slash and timber piles (Eidmann, 1985; Schlyter and Lundgren, 1993). Managed stands with only one age class and one dominating tree species favour different scolytid species and possibly a narrower species spectrum than stands in a natural condition (Nuorteva, 1968; Martikainen et al., 1996). This could lead to reduced competition between the pest species and other scolytids (LoÈyttyniemi, 1975), and to reduced predation and parasitism (Schlyter and Lundgren, 1993). Schowalter and Turchin (1993) showed that a deciduous mixture may decrease the infestation spread in Dendroctonus frontalis Zimmermann, suggesting that managed forests with only one prominently dominant tree species can be more favourable for certain bark-beetle species. It has also been suggested that secondary scolytids (species attacking only trees that are weakened or already dead) are more abundant and could maintain higher levels of non-speci®c bark-beetle predators and parasitoids in natural forests than in managed forests (Nuorteva, 1956, 1968), resulting in a less ef®cient control of primary scolytids in the managed forests.

Bark beetles as a group are usually considered as forest pests but they actually constitute and maintain a considerable proportion of species diversity in forest ecosystems. Not only is Scolytidae one of the most species- and individual-rich groups among the saproxylic beetles in boreal forests but from the ecosystem perspective, several scolytids are keystone species causing both small-scale gap disturbances and large-scale disturbances and thus driving forest succession, e.g. I. typographus (L.) in Eurasia (Bakke, 1989) and some Dendroctonus species in North America (Amman, 1977; Schowalter et al., 1981). A large number of other organisms are directly associated with bark beetles. For instance, the arthropod complex associated with I. typographus (L.) includes about 140 species (Weslien, 1992). Bark beetles also have a signi®cant effect on decomposition of trees as vectors of the initial decomposer communities, and by opening the substrate for subsequent colonizers (Carpenter et al., 1988; Edmonds and Eglitis, 1989). The aim of this study was to compare bark-beetle and associated beetle assemblages between oldgrowth Picea abies (L.) Karst. dominated mesic forests, and mature managed forests with a varying supply of decaying wood. Our speci®c questions were: 1. Does the number and species composition of bark beetles differ between mature managed and oldgrowth forests? 2. Does the amount of recently dead trees within a stand explain the numbers of bark beetles? 3. Does the number of associated species differ between mature managed and old-growth forests? 2. Material and methods 2.1. Study area, sample plots and stand characteristics Our study area is situated in the transition zone between southern and middle boreal zones (Ahti et al., 1968) in southern Finland. Our sample plots were located within an area of 35  80 km (618490 ± 628090 N, 238030 ±248400 E). Norway spruce (Picea abies (L.) Karst.) and Scots pine (Pinus sylvestris L.) are the dominant tree species throughout the study

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area. The location of the study area was chosen, because in this part of southern Finland it was possible to ®nd enough old-growth patches to allow independent replicates. All except two sample plots were established in state-owned forests. We focused on mature, spruce-dominated forests growing on mesic Myrtillus site type (Cajander, 1949). The forest stands were divided into three categories according to the average age of the dominant spruces, and on the basis of the occurrence of cut stumps. The categories were as follows: 1. Mature managed forests (called mature below): age between 95±120 years, cut stumps abundant. Forests in this category have reached maturity (the culmination point of mean annual increment of volume) and represent typical state-owned forest stands at the time of regeneration felling in southern Finland. According to the latest national forest inventories (carried out in 1989±1994), the proportion of spruce forests between 101±120 years of age is 10.3% of all spruce-dominated forests in southern Finland (Tomppo and Henttonen, 1996). 2. Overmature, managed forests (overmature below): age over 120 years, cut stumps abundant. Forests in this category consist of managed forests which are considered under-productive in the economical sense because they have substantially passed the economically optimal rotation time. The proportion of overmature stands (age over 120 years) of all spruce-dominated forests in southern Finland has been increasing (Salminen, 1993) and was 4.2% in the latest inventory (Tomppo and Henttonen, 1996). It has been suggested that these overmature, senescent forests could be at risk of barkbeetle damage. 3. Old-growth forests (old-growth below): age mostly over 160 years, no or few old cut stumps present. The forests in this category represent the closest-tonatural forests that remain in southern Finland. Only signs of human interference were a few scattered stumps (0±12 stumps/ha) from past selective cuttings. Two of the forests included in this category had significant signs of selective cuttings (76 and 123 stumps/ha), but as the structure of these stands was otherwise close to other oldgrowth stands, we included these stands in the

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old-growth category. All the stands in this category belong to national parks or old-growth protection areas in which no cutting is allowed. In practice the stands formed a continuum from intensively managed forests to forests in a natural condition. Management intensity varied a lot among the stands within both the mature and overmature categories and thus, the two categories of managed stands do not directly indicate management intensity but rather stand age classes. We established a 1 ha sample plot in each stand. Selection, measurements and stand characteristics of the plots are described in detail in Siitonen et al. (1999). The number of sample plots in the categories was 10, 11 and 9, respectively, making a total of 30 plots. The sample plots are the same as in Siitonen et al. (1999) with two exceptions. One plot in overmature forests in the present study was cut before it was measured. The beetle sample from that forest is used here except for the analyses concerning stand characteristics. Furthermore, one old-growth plot, situated in the same forest stand as another plot, was not included in the present study. Each forest stand was at least 3 ha in size, so that it was possible to place a 1 ha sample plot within it. The minimum distance between sample plots was ca. 1 km. Live stand characteristics (including basal area and volume by tree species) were measured on one half (0.5 ha) of the sample plot. The amount of dead wood with a minimum diameter of 5 cm was measured on the whole 1 ha sample plot. Measurements of dead wood included determination of tree species and decay class. Five decay classes (I±V) were used to describe the stage of decomposition from recently dead trees to completely soft trunks overgrown by forest-¯oor mosses. Measurements were conducted in the autumn of 1995, 1 year after the sampling of the beetles. Because of the large year-to-year variation in mortality of trees, we pooled the decay class I (recently dead, at the most 1-year-old) and II (wood hard, bark partly loose but more than 50% remaining, approximate age less than 10 years), to get an estimate of the recent accumulation of dead trees which have recently been available for bark beetles as breeding material. The most important stand characteristics which can in¯uence the occurrence of bark beetles are summarized in Table 1.

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Table 1 Stand characteristics of the sample plots

Mean age of dominant spruces (years) Number of cut stumps/ha Basal area of live trees (m2/ha) Volume of live trees (m3/ha) Spruce Pine Deciduous Total volume of dead trees (m3/ha) Volume of dead trees in decay classes I and II (m3/ha) Spruce Pine Deciduous Bark area of dead trees (m2/ha)

Mature (n ˆ 10)

Overmature (n ˆ 10)

Old-growth (n ˆ 9)

103.9  7.3 373.0  136.4 27.9  3.8 298.5  51.9 262.7  67.8 27.1  19.0 8.7  8.6 14.4  8.2 5.3  4.5 3.9  3.8 0.7  0.8 0.8  1.9 125.6  115.8

133.0  7.5 299.5  189.8 30.9  5.8 331.3  82.7 224.0  55.6 80.5  64.4 26.8  21.7 22.3  10.6 11.3  6.4 7.3  5.6 1.1  1.1 2.9  4.8 343.4  227.2

159.2  22.2 25.0  44.0 33.4  5.2 381.5  84.1 254.4  88.4 74.1  44.1 53.0  41.7 105.9  34.9 31.8  13.1 18.9  14.9 4.5  5.0 8.4  5.7 794.3  144.3

Data are means  standard deviations.

2.2. Sampling of beetles We used window-¯ight traps to sample the beetles from the forests. The trap consisted of two perpendicular intercepting 40  60 cm transparent polycarbonate panes, with a funnel leading into a 1 l container below the panes. A solution of water, salt and detergent was used to preserve the insects. The trap was set hanging on a string between the tree trunks so that the lower margin of the panes was one metre above the ground. Ten traps were distributed at random in open places within each sample plot. The total number of traps was 300. The sampling period was 16 April±2 September 1994, during which the traps were emptied four times. The sampling period covered the entire ¯ight period for spruce bark beetles. Trypodendron lineatum (Ol.) is the ®rst scolytid beetle on spruce to start swarming in the spring when the maximum temperature reaches 158C (Annila et al., 1972). This temperature was reached on 23 April in Tampere, about 40 km south of our study area (Ilmatieteen Laitos, 1994). At the time of installation there was snow still on the forest ¯oor, which prevents the swarming of T. lineatum (Ol.) (Annila et al., 1972). 2.3. Species included in the study We included two groups of beetles in this study: (I) bark beetles including ambrosia beetles (Coleoptera, Scolytidae) and (II) beetle species which are asso-

ciated with bark beetles. As associated species, we classi®ed only species that are known to occur primarily in the bark-beetle galleries (e.g. Saalas, 1917, 1923; Nuorteva, 1956; Weslien, 1992; and own observations). Consequently, some species that can be found in bark-beetle galleries but which occur frequently in other dead-wood microhabitats as well such as Quedius plagiatus (Mannerh.) were not included in this group. Some of the associated species are important predators of bark beetles (e.g. Rhizophagus grandis Gyll. and Thanasimus formicarius (L.) (King et al., 1991; Weslien and Regnander, 1992) while others may be scavengers or feed on other arthropods or fungi occurring in the galleries (Weslien, 1992). All the individuals were identi®ed by the authors PM and JS. Jyrki Muona veri®ed the identity of some Epuraeaspecimens. For some analyses, we grouped bark beetles into three groups according to their host-tree species: species living on Norway spruce including Hylurgops palliatus (Gyll.), T. lineatum (Ol.) and T. proximum (Niijima) which also frequently occur on pine; species on Scots pine and species on deciduous trees. We considered Dendroctonus micans (Kug.), Pityogenes chalcographus (L.) and I. typographus (L.) as primary bark-beetle species on the basis of their ability to kill healthy trees, and all others as secondary species. References to the biology of the different species in Fennoscandia can be found in Lekander et al. (1977). Nomenclature follows Silfverberg (1992).

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2.4. Statistical analyses We used the pooled sample of the 10 traps in each sample plot in the analysis. The number of species caught per sample plot was used in the comparisons of species richness (as a measure of a-diversity) among the categories. The sample sizes in terms of the individuals caught varied considerably among the plots. However, since the samples were collected with standard traps, in structurally similar habitats we assumed that the differences in the sample sizes re¯ect the real differences in abundances and no adjustment based on sample size was made (Section 4). We used Kruskal-Wallis non-parametric analysis of variance, and, when appropriate, a-posteriori comparisons of mean ranks, to test differences among the categories. Spearman rank correlations were used to study correlations between the beetle samples and stand characteristics. In addition to differences in species richness (adiversity), the heterogeneity of species composition among forest stands (regional g-diversity) may differ between the categories. This should be re¯ected in species accumulation curves, when samples from two, three etc. forest stands belonging to the same category are pooled together. We studied this by calculating the mean number of species (2 SD) in all possible combinations of a given number of stands pooled together. The procedure combines the average number of species per sample plot, and variation in species composition among the stands, into the cumulative number of species (as a measure of g-diversity). 3. Results 3.1. Bark beetles A total of 13 557 bark-beetle individuals belonging to 30 species were caught (Table 2). The number of individuals per sample plot was on average 23±30% higher in overmature and old-growth forests than in mature forests, but the differences were not statistically signi®cant (Fig. 1(A)). Both the lowest and the highest number of individuals per sample plot were observed in mature forests. Species richness was highest in old-growth, intermediate in overmature and lowest in mature forests; the difference was signi®cant between old-growth and

237

mature forests (Fig. 1(B)). The total number of species found in all the old-growth forests was also higher (29 species) than in the overmature (26) and mature forests (25), although the number of sample plots was smallest in the old-growth category. The cumulative number of species was also higher in old-growth forests than in the other two categories (Fig. 2(A)). Abundances of individual species were usually similar among the categories (Table 2). Most of the species occurred in low numbers and/or were absent from more than half of the plots. Because the power of the Kruskal±Wallis test is low when a species is absent from most of the plots, we restricted testing to the 12 species which occurred in more than 50% of the sample plots. Furthermore, standard deviations were often high, owing to the very high numbers of individuals in some plots, which also decreases the power of the test. For example, if the abundance of Dryocoetes autographus (Ratz.) was tested by parametric ANOVA assuming equal variances, 10 replicates in each category and normal distributions, the probability to ®nd two-fold differences among the treatments, at a  ˆ 0.05, would be only approximately 0.6 (Zar, 1984). It is thus obvious, that we were not able to detect all ecologically signi®cant differences. Only the numbers of P. chalcographus (L.) and Trypodendron signatum (F.) differed signi®cantly among the categories. In P. chalcographus (L.), non-parametric ANOVA showed statistically signi®cant differences between mature and old-growth forests (H ˆ 7.18, P ˆ 0.028). However, clearly the highest numbers per sample plot were recorded in two overmature forests. The relatively low but even numbers of this species in old-growth forests resulted in the highest mean of the ranked values in the oldgrowth category. T. signatum (F.) was signi®cantly more abundant in old-growth forests than in mature forests (H ˆ 7.24, P ˆ 0.027). Overmature forests were intermediate to, and did not differ signi®cantly from the other two categories. When the species were grouped according to their host-tree species, the pooled number of individuals per sample plot differed among the categories only in species living on deciduous trees (H ˆ 7.65, P ˆ 0.022). The number of individuals was signi®cantly lower in mature forests (median ˆ 27.5 ind./plot) than in old-growth forests (115.0), but overmature forests (46.0) did not differ from the other two categories.

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Table 2 Bark beetle species: number of individuals per sample plot (mean  standard deviation), frequency of occurrence in each forest category, and total number of individuals in the pooled material Species

Mature (n ˆ 10)

Overmature (n ˆ 11)

Old-growth (n ˆ 9)

Mean  SD

Frequency

Mean  SD

Frequency

Mean  SD

Frequency

10 10 5 10 3 10 ± 3 1 2 3 2 3 5 2 1 1 ± ± 10 10 2 1 2 3 10 10 ± 9 ±

5.7  7.1 59.8  58.4 3.4  6.2 196.2  96.4 0.1  0.3 32.5  13.5 ± 3.6  6.6 ± 0.6  0.9 1.7  3.8 0.5  1.2 1.9  2.5 8.7  19.1 0.1  0.3 0.5  0.8 1.3  2.5 0.5  1.2 ± 28.7  28.8 6.5  5.5 1.6  2.5 0.5  0.8 2.0  4.2 4.2  12.2 55.5  60.0 52.3  41.0 ± 3.9  1.9 0.1  0.3

10 11 6 11 1 11 ± 6 ± 5 3 3 6 9 1 4 4 2 ± 11 10 5 4 4 4 11 11 ± 11 1

6.8  3.3 53.7  33.5 4.1  3.2 166.3  91.2 0.1  0.3 33.6  17.7 0.2  0.7 1.9  1.4 ± 0.4  0.5 2.8  5.0 2.2  3.4 1.2  1.5 3.2  1.8 0.2  0.7 0.4  0.7 0.6  1.3 0.1  0.3 0.1  0.3 32.2  20.5 4.0  2.5 1.1  3.3 0.9  1.6 38.6  75.7 2.4  3.1 32.7  14.2 105.8  49.7 0.1  0.3 4.0  3.7 0.1  0.3

9 9 8 9 1 99 1 9 ± 4 4 4 5 9 1 3 2 1 1 9 8 1 4 4 6 9 9 1 9 1

Hylurgops glabratus (Zett.) 5.1  3.1 Hylurgops palliatus (Gyll.) 42.6  43.1 Hylastes brunneus Er. 1.6  2.1 Hylastes cunicularius Er. 158.1  130.5 Hylastes opacus Er. 0.3  0.5 Xylechinus pilosus (Ratz.) 31.4  36.6 Tomicus minor (Htg.) ± Tomicus piniperda (L.) 0.6  1.1 Dendroctonus micans (Kug.) 0.1  0.3 Phloeotribus spinulosus (Rey) 0.5  1.1 Polygraphus subopacus Thoms. 0.7  1.3 Polygraphus poligraphus (L.) 0.2  0.4 Polygraphus punctifrons Thoms. 1.4  2.7 Pityogenes chalcographus (L.) 1.0  1.2 Pityogenes quadridens (Htg.) 0.2  0.4 Pityogenes bidentatus (Hbst.) 0.1  0.3 Ips typographus (L.) 0.1  0.3 Ips amitinus (Eichh.) ± Dryocoetes alni (Georg) ± Dryocoetes autographus (Ratz.) 29.0  22.0 Dryocoetes hectographus Reitt. 18.7  41.1 Crypturgus subcribrosus Egg. 0.3  0.7 Crypturgus hispidulus Thoms. 0.4  1.3 Trypodendron domesticum (L.) 0.5  1.1 Trypodendron proximum (Niijima) 0.5  1.0 Trypodendron lineatum (Ol.) 41.1  55.5 Trypodendron signatum (F.) 48.2  46.5 Trypophloeus bispinulus Egg. ± Cryphalus saltuarius Weise 3.2  4.3 Pityophthorus micrographus (L.) ± Mean number of individuals Mean number of species Total number of individuals Total number of species

385.9  286.8 12.8  2.6 3859 25

472.6  238.9 15.0  3.0 5199 26

499.9  193.1 16.7  1.8 4499 29

Total number of individuals 175 1567 90 5236 5 74 2 63 1 16 51 28 46 135 5 11 20 6 1 896 294 31 18 374 73 1316 2009 1 111 2

13557

Note that the statistical analyses presented in the text were based on ranked values, not on the means presented here.

Thenumberofbark-beetleindividualspersampleplot correlated best with the amount of decaying wood in decay classes I and II of the examined stand characteristics (Table 3, Fig. 3). This relationship seemed to vary considerably between the categories: in mature forests correlation was very strong (n ˆ 10, rs ˆ 0.92, P < 0.001), low in overmature (n ˆ 10, rs ˆ 0.43, P ˆ 0.214), and in old-growth there was no correlation (n ˆ 9, rs ˆ ÿ0.05, P ˆ 0.898) (Fig. 3). The number of individuals caught was not correlated with the basal area of live trees (indicating also that trapping ef®ciency

was not affected by the density of the stand). Species richness had the strongest correlation with the amount of decaying wood in decay classes I and II (Table 3). The number of individuals living only on deciduous trees correlated best with the amount of dead deciduous trees in decay classes I and II (Table 4). Similarly, spruce-associated beetles had a signi®cant correlation with decaying spruces in classes I and II, whereas the number of individuals of species living on pine did not correlate signi®cantly with the pines which had recently died.

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Fig. 1. Number of bark-beetle individuals (A) and species (B), and number of individuals (C) and species (D) of bark-beetle associated species per sample plot in each category. Data are medians, upper and lower quartiles, maximums and minimums. Kruskal±Wallis test statistics (H) and probability levels (P) are given. Categories with different letters differed from each other at P < 0.05 level in a-posteriori tests. Note the different scales on the y-axes. Table 3 Correlation coefficients (Spearman rank correlation) between the number of individuals and species per sample plot and selected stand characteristics (n ˆ 29) Volume of live trees

Basal area of live trees

Volume of dead trees

Volume of dead trees in decay classes I and II

Bark area of dead trees

Bark beetles No. of individuals / plot No. of species / plot

0.24 0.41*

0.09 0.25

0.41* 0.47*

0.50** 0.57**

0.36 0.50**

Associated species No. of individuals / plot No. of species / plot

0.32 0.38*

0.32 0.30

0.53** 0.57**

0.60** 0.63***

0.47* 0.56**

3.2. Associated species Our sample included 1225 individuals of 28 species associated with bark beetles. Correlations between species richness and abundance of associated species and bark beetles were very signi®cant (Table 5), and

consequently, associated species showed patterns similar to those in bark beetles. The number of individuals per sample plot did not differ signi®cantly between the categories, although it was on average 61% higher in overmature and 89% higher in oldgrowth forests than in mature forests (Fig. 1(C)).

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Fig. 3. Relationship between the number of bark-beetle individuals and the total amount of recently dead wood (decay classes I ‡ II) in the 29 plots.

Fig. 2. (A) Cumulative number of bark-beetle species in each category when the number of sample plots is increased. Mean (2SD for all possible combinations of a given number of plots (n ˆ total number of individuals in each category). (B) Similarly as in (A) for species associated with bark beetles. Table 4 Correlation coefficients (Spearman rank correlation) between pooled number of individuals of bark beetles per sample plot grouped according to the host-tree species and volume of live and dead host trees in decay classes I and II (n ˆ 29) No. of individuals/plot

Volume of live host trees

Volume of dead host trees in decay classes I and II

Species on Norway spruce Species on Scots pine Species on deciduous trees

0.24 0.25 0.40*

0.58** 0.21 0.65***

These differences were larger than the corresponding differences in bark beetles. Species richness was on average 23% higher in overmature and 71% higher in old-growth than in mature forests (Fig. 1(D)). The difference between old-growth and mature forests was signi®cant. The

total number of species in all the old-growth forests was also higher (26 species) than in overmature (23 species) and mature (17 species) forests. The cumulative number of species showed greater differences among the categories in associated species than in bark beetles (Fig. 2(B)). Cumulative number of species was constantly and signi®cantly lower in mature forests than in old-growth forests, and the cumulative number of species in overmature forests was intermediate to the other two categories. Most of the associated species were very scarce in the samples. Only seven species occurred in at least 50% of the plots (Table 6). None of these species showed signi®cant differences in abundance among the categories. Correlations between associated species and stand characteristics were very similar to those in bark beetles (Table 3), but usually stronger. 4. Discussion 4.1. Sampling method The sampling method used to monitor the abundances of bark beetles and their associates has a strong effect on the catch and the results must be interpreted accordingly. Window-¯ight traps without any attractant measure ¯ying activity of beetles. The probability of catching different species is likely to be species-

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Table 5 Correlation coefficients (Spearman rank correlation) between the number of individuals and species of bark beetles and their associated beetle species per sample plot (n ˆ 30)

No. of individuals of associated species No. of species of associated species

No. of individuals of bark beetles

No. of species of bark beetles

0.81*** 0.67***

0.65*** 0.63***

Table 6 Associated species: number of individuals per sample plot (mean  standard deviation), frequency of occurrence in each forest category, and total number of individuals in the pooled material Species Phloeonomus monilicornis (Gyll.) Phloeonomus lapponicus (Zett.) Phloeonomus pusillus (Gravenh.) Phloeonomus sjobergi Strand Phloeopora testacea (Mannerh.) Placusa complanata Er. Placusa depressa MaÈkl. Placusa tachyporoides (Waltl) Placusa incompleta SjoÈb. Plegaderus vulneratus (Panz.) Thanasimus formicarius (L.) Thanasimus femoralis (Zett.) Epuraea laeviuscula (Gyll.) Epuraea rufobrunnea SjoÈb. Epuraea deubeli Reitt. Epuraea angustula Sturm Epuraea oblonga (Hbst.) Epuraea fussi Reitt. Epuraea marseuli Reitt. Epuraea pygmaea (Gyll.) Epuraea muehli Reitt. Pityophagus ferrugineus (L.) Rhizophagus grandis Gyll. Rhizophagus depressus (F.) Rhizophagus ferrugineus (Payk.) Cryptolestes alternans (Er.) Corticaria obsoleta Strand Corticeus linearis (F.) Mean number of individuals Mean number of species Total number of individuals Total number of species

Mature (n ˆ 10)

Overmature (n ˆ 11)

Old-growth (n ˆ 9)

Mean  SD

Frequency

Mean  SD

Frequency

Mean  SD

Frequency

6 1 ± 5 2 ± ± 2 2 ± 1 ± 1 ± 1 1 6 ± 8 9 1 7 ± 1 8 ± ± ±

1.8  2.2 0.1  0.3 0.2  0.6 0.6  0.8 0.1  0.3 0.2  0.4 0.1  0.3 0.1  0.3 0.1  0.3 ± ± ± 0.2  0.6 ± 0.4  0.9 0.4  0.7 2.9  2.5 0.2  0.4 2.5  2.1 11.8  16.7 0.2  0.4 1.5  2.3 0.2  0.6 0.3  0.5 19.6  18.8 0.5  1.5 ± 0.1  0.3

6 1 1 5 1 2 1 1 1 ± ± ± 1 ± 2 3 10 2 9 11 2 7 1 3 11 2 ± 1

2.3  4.2 0.7  1.1 0.2  0.4 0.7  0.7 0.6  0.9 ± 0.2  0.7 0.2  0.4 0.2  0.4 0.1  0.3 0.2  0.4 0.1  0.3 0.3  0.5 0.1  0.3 0.2  0.4 0.8  1.0 2.1  2.0 1.1  1.5 3.1  2.3 16.9  12.5 0.6  0.7 1.3  1.0 0.2  0.7 0.7  0.7 18.7  21.0 0.1  0.3 0.1  0.3 ±

4 3 2 5 3 ± 1 2 2 1 2 1 3 1 2 5 8 5 8 9 4 7 1 5 9 1 1 ±

2.2  3.4 0.1  0.3 ± 0.6  0.7 0.2  0.4 ± ± 0.2  0.4 0.3  0.7 ± 0.1  0.3 ± 0.1  0.3 ± 0.2  0.6 0.1  0.3 1.3  1.8 ± 2.7  3.6 8.7  7.0 0.2  0.6 1.1  1.0 ± 0.2  0.6 9.1  10.5 ± ± ± 27.4  23.2 6.2  2.9 274 17

44.0  33.3 7.6  2.2 484 23

51.9  29.7 10.6  2.5 467 26

Total number of individuals 63 8 4 19 8 2 3 5 6 1 3 1 6 1 8 12 64 12 82 369 9 40 4 11 475 7 1 1

1225

Note that the statistical analyses presented in the text were based on ranked values, not on the means presented here.

speci®c and is affected by many factors, such as typical height and duration of ¯ight of each species. Hence, the catches of different species can not be compared directly. But for an individual species, the

probability of being caught is likely to be equal in structurally similar forests and thus variation in abundance of individual species among stands can be assumed to re¯ect the real differences in species'

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abundances. The trapping in this study was standardized by using equal number of similarly placed traps in each forest. Pheromone traps which are more commonly used in monitoring population levels of bark beetles and their associates have a strong baiting effect, attracting beetles from a radius of several tens of metres (Schlyter, 1992). Samples from pheromone traps probably re¯ect better the potential of bark beetles to attack suitable host trees than their relative abundance (Schlyter and Lundgren, 1993). Pheromones are also species-speci®c, which limits the use of pheromone traps to single or few species of bark beetles and associates at one time. The problem with both window-¯ight traps and pheromone traps is that the samples give a poor estimate of numbers of beetle individuals per unit area, but this is a problem shared by all relative sampling methods (e.g. Ruesink and Kogan, 1982). Absolute methods, such as direct bark sampling, would give estimates of densities per unit area, but the patchy occurrence of bark beetles dictates that the areas sampled have to be large and adequate sampling is extremely laborious (see TraÈgaÊrdh and Butovitsch, 1934). Hence, we suggest that window¯ight trapping is a suitable method to get an overview of the whole complex of bark beetles and their associates in stands which have been managed differently. 4.2. Effects of management on bark-beetle assemblages Forest management can affect bark-beetle assemblages (1) by changing the tree-species composition and stand structure, thereby changing the composition of dead wood available for bark beetles as breeding material, (2) by affecting the mortality rate of live trees and thereby the dynamics of dead wood, (3) by changing the within-stand microclimate, and (4) by affecting the interactions among species, i.e. competition, predation and parasitism. The number of bark-beetle species caught per sample plot was signi®cantly higher in old-growth forests than in mature forests. This was probably a consequence of the greater diversity of live and dead trees, and the higher volume of recently dead trees in oldgrowth than in mature forests. Especially, the amount of recently dead deciduous trees was much higher in

old-growth than in the other two categories. Two of the four species living on deciduous trees (D. alni (Georg) and T. bispinulus Egg.) were only found in old growth. It is possible that the scarcity of suitable breeding material in managed forests has caused a local disappearance of some bark-beetle species, especially those living on aspen (Populus tremula L.). Primary scolytids comprised only about 1% of the total number of individuals in the samples. Although this does not necessarily mean that secondary species were a hundred times more abundant than primary ones it is likely that in non-epidemic conditions secondary species are much more abundant than primary species in old spruce forests. The abundance of most secondary species did not differ signi®cantly among the categories, the only exception being T. signatum (F.), which was most abundant in old-growth forests. Also T. domesticum (L.) occurred in high numbers in two old-growth stands. This can be explained by the much higher amount of deciduous trees in old-growth forests (Table 1). Also Nuorteva (1968) and Martikainen et al. (1996) found that the bark beetles living on deciduous trees were adversely affected by forest management. However, the pooled number of individuals of all secondary species per sample plot was almost 30% higher in old-growth than in mature forests, which may have some ecological signi®cance to for example associated species. Variation among individual stands was large which means that statistical differences among the categories are dif®cult to detect. Thus, our results did not clearly support the hypothesis that secondary scolytids would be more abundant in more natural stands (Nuorteva, 1959, 1968). Several bark-beetle species avoid forest edges and thinned stands which are typical for managed forest landscape (Peltonen et al., 1997). For example Hylurgops glabratus (Zett.), Xylechinus pilosus (Ratz.), Polygraphus-species, Crypturgus subcribrosus Egg. and Cryphalus saltuarius Weise prefer dense and shady forests and tend to withdraw into the interior parts of forest stands (Nuorteva, 1968; Martikainen et al., 1996; Peltonen et al., 1997). The highest mean abundances in these species were usually found in the old-growth category, although the differences were not statistically signi®cant. It is probable that all our forest stands represented interior forest habitats to these species, because the stands were large (>3 ha)

P. Martikainen et al. / Forest Ecology and Management 116 (1999) 233±245

and live stand volume was rather similar among the categories. Forest management changes the spatial and temporal dynamics of dead wood (Eidmann, 1985). In managed forests, most of the suitable breeding material becomes available for bark beetles after thinning and clear-cutting, and mortality of trees is low between logging operations. It has been shown that in managed forest the proportion of I. typographus (L.) individuals originating from the local population in pheromone traps is less than 20% (Weslien and LindeloÈw, 1989) and that a large proportion of beetles disperse long distances up to several kilometres (Weslien and LindeloÈw, 1990). It is possible that a proportion of bark beetles dispersing from their stand of origin and aggregating in stands with suitable breeding material (e.g. logging slash or occasional dying trees) is larger in the managed forest landscape than in old-growth forests, where the supply of dying trees is rather constant. This kind of baiting effect, together with the apparently weaker impact of natural enemies could also explain the stronger correlation between the abundance of bark beetles and the amount of recently dead wood in managed than in old-growth stands in our material (Fig. 3). The overmature stands were considerably beyond the recommended rotation time, which is 90±100 years on Myrtillus-site type in southern Finland (MetsaÈkeskus, 1994). The proportion of overmature spruce stands has increased in southern Finland during the last decades and there has been some concern about their susceptibility to pest damage as the stands start to decline. The amount of recently dead wood was roughly two-fold in overmature as compared with mature forests, but this did not cause signi®cant differences in the general abundance of bark beetles between these two categories. However, our data included too few individuals of primary bark beetles to allow reliable conclusions about their relative abundance in the different categories. 4.3. Associated species Although not all of the associated species included in this study are predators of bark beetles, this group probably has an indicative value when considering the diversity and abundance of bark-beetle enemies (including other groups than beetles) in managed

243

and old-growth forests. The number and abundance of species associated with bark beetles were clearly higher in old-growth forests than in mature managed forests. This is probably a consequence of the higher amount and diversity of recently dead wood, and the higher number of bark-beetle species in old-growth forests as compared with mature forests. Weslien and Schroeder (1998) found that the numbers of certain bark-beetle predators were signi®cantly higher in selected unmanaged stands with continuous attacks of I. typographus (L.) than in corresponding managed stands without attacks, although the catches of I. typographus (L.) did not differ between the categories. The hypothesis that the abundance of bark-beetle enemies would be higher in old-growth than in managed forests (Schlyter and Lundgren, 1993) seems to receive support from these studies. The apparently different spatial and temporal dynamics of recently dead wood and bark beetles in managed and more natural forest landscapes probably also has some consequences to the population dynamics of natural enemies and their bark-beetle hosts. Weslien and Schroeder (1998) showed that some bark-beetle predators arrived sooner in baited traps and logs in unmanaged stands with ongoing attacks of I. typographus (L.) as compared with managed forests without recent attacks. They also suggested that small parasitoids especially would have a poor dispersal ability. Many predators and parasitoids are non-speci®c on bark beetles, attacking also primary species (Nuorteva, 1956; Dahlsten, 1982). 5. Conclusions Our results showed that the assemblages of both bark beetles and their associates are richer in oldgrowth than in mature managed forests. The richer complex of secondary scolytid species and natural enemies in old-growth forests could mean that competition, predation and parasitism control populations of primary scolytid species more ef®ciently in oldgrowth forests where the supply of dying trees is more constant than in managed forests. It is thus obvious that in the absence of major disturbances, populations of primary bark beetles will stay at non-epidemic levels in old-growth forests, although single trees and small groups of trees die each year in the oldgrowth.

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Recent recommendations aiming at ecologically sustainable forestry (Skogsstyrelsen, 1990; MetsaÈkeskus, 1994; HokajaÈrvi, 1997) suggest that the supply of dead trees should be improved and a deciduous mixture should be promoted in managed forests to conserve species diversity. These measures may also increase the amount of suitable breeding material available to bark beetles in managed forest landscape, but as they are likely to enhance the populations of secondary bark beetles and bark-beetle enemies at the same time, populations of primary bark beetles will not necessarily rise. Acknowledgements We would like to thank Juhani MaÈkinen for assistance in the ®eldwork and calculations of stand characteristics and Anu Katainen and Cia Olsson for sorting the trap material. Jyrki Muona checked the identity of some specimens. Pekka NiemelaÈ, Jari Kouki and two anonymous reviewers made valuable comments on the manuscript. Christopher Green checked the language. Division of Population Biology at the University of Helsinki provided the working facilities during early phases of the study for the authors PM and PP. The study was partly ®nanced by the Maj and Tor Nessling foundation, the Academy of Finland (project 35741) and the Finnish Society of Forest Science. References Ahti, T., HaÈmet-Ahti, L., Jalas, J., 1968. Vegetation zones and their sections in north-western Europe. Ann. Bot. Fennici 5, 169± 211. Amman, G.D., 1977. The role of the mountain pine beetle in lodgepole pine ecosystems: impact on succession. In: Matsson, W.J. (Ed.), The Role of Arthropods in Forest Ecosystems, Springer, New York, pp. 3±18. Annila, E., Bakke, A., Bejer-Petersen, B., Lekander, B., 1972. Flight period and brood emergence in Trypodendron lineatum (Oliv.) (Col., Scolytidae) in the Nordic countries. Comm. Inst. For. Fenn. 76, 1±28. Bakke, A., 1989. The recent Ips typographus outbreak in Norway ± experiences from a control program. Holarct. Ecol. 12, 515± 519. Cajander, A.K., 1949. Forest types and their significance. Acta For. Fenn. 56, 1±71.

Carpenter, S.E., Harmon, M.E., Ingham, E.R., Kelsey, R.G., Lattin, J.D., Schowalter, T.D., 1988. Early Patterns of Heterotroph Activity in Conifer Logs, Proc. Royal Soc. Edinburgh, vol. 94B, 33±43. Christiansen, E., Bakke, A., 1988. The spruce bark beetle of Eurasia, In: Berryman, A. (Ed.), Dynamics of Forest Insect Populations, Plenum Press, New York, pp. 480±503. Dahlsten, D.L., 1982. Relationships between bark beetles and their natural enemies. In: Mitton, J.B., Sturgeon, K.B. (Eds.), Bark Beetles in North American Conifers: A System for the Study of Evolutionary Biology. University of Texas Press, Austin, TX, pp. 140±182. Edmonds, R.L., Eglitis, A., 1989. The role of the Douglas-fir beetle and wood borers in the decomposition of and nutrient release from Douglas-fir logs. Can. J. For. Res. 19, 853± 859. Eidmann, H.H., 1985. Silviculture and insect problems. Z. ang. Ent. 99, 105±112. HokajaÈrvi, T. (Ed.), 1997. MetsaÈnhoito-ohjeet (in Finnish), MetsaÈhallituksen metsaÈtalouden julkaisuja, vol. 10. Ilmatieteen Laitos, 1994. Kuukausikatsaus Suomen ilmastoon (in Finnish). Huhtikuu 1994. King, C.J., Fielding, N.J., O'Keefe, T., 1991. Observations on the life cycle and behaviour of the predatory beetle, Rhizophagus grandis Gyll. (Col., Rhizophagidae) in Britain. J. Appl. Ent. 111, 286±296. Lekander, B., Bejer-Petersen, B., Kangas, E., Bakke, A., 1977. The distribution of bark beetles in the Nordic Countries. Acta Ent. Fenn. 32, 1±37. LoÈyttyniemi, K., 1975. On the occurrence of Ips sexdentatus (BoÈrner) (Col., Scolytidae) in south Finland. Ann. Ent. Fenn. 41, 134±135. Martikainen, P., Siitonen, J., Kaila, L., Punttila, P., 1996. Intensity of forest management and bark beetles in non-epidemic conditions: a comparison between Finnish and Russian Karelia. J. Appl. Ent. 120, 257±264. MetsaÈkeskus Tapio, 1994. LuonnonlaÈheinen metsaÈnhoito. MetsaÈnhoitosuositukset, (in Finnish). MetsaÈkeskus Tapion julkaisu 6/ 1994. È ber den Fichtenstamm-BastkaÈfer, Hylurgops Nuorteva, M., 1956. U palliatus Gyll., und seine Insektenfeinde. Acta Ent. Fenn. 13, 1±118. È ber die Vorraussetzungen der biologischen Nuorteva, M., 1959. U BekaÈmpfung der BorkenkaÈfer mit Hilfe ihrer Insektenfeinde in der finnischen Waldpflege. Verhandlungen des IV, Internationalen Pflanzenschutz-Kongresses, Hamburg 1957, Bd. I, pp. 1025±1027. È ber MengenveraÈnderungen der BorkenkaÈNuorteva, M., 1968. U ferfauna in einem suÈdfinnischen Waldgebiet in der Zeit von 1953 bis 1964. Acta Ent. Fenn. 24, 1±50. Peltonen, M., HelioÈvaara, K., VaÈisaÈnen, R., 1997. Forest insects and environmental variation in stand edges. Silva Fennica 31, 129± 141. Ruesink, W.G., Kogan, M., 1982. The quantitative basis of pest management: sampling and measuring. In: Metcalf, R.L., Luckmann, W.H. (Eds.), Introduction to Insect Pest Management, 2nd edn. Wiley, New York, pp. 315±352.

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