Population levels of bark beetles and associated insects in managed and unmanaged spruce stands

Forest Ecology and Management 115 (1999) 267±275

Population levels of bark beetles and associated insects in managed and unmanaged spruce stands Jan Wesliena,*, L. Martin Schroederb a The Forestry Research Institute of Sweden (SkogForsk), S-751 83 Uppsala, Sweden Department of Entomology, Swedish University of Agricultural Sciences (SLU), PO Box 7044, S-750 07 Uppsala, Sweden

b

Abstract Relative population levels of the spruce bark beetle, Ips typographus (L.) (Coleoptera, Scolytidae) and associated insects were estimated in 12 spruce stands in central Sweden. Spruce bolts and window traps baited with semiochemicals were used for the monitoring. Six stands were unmanaged and had ongoing attacks on standing trees by I. typographus. This had led to an accumulation of dead spruce trees during several years. These six stands were compared pairwise with six old-managed stands with similar forest structure, but with no attacks during the previous years and with low amounts of dead trees. Catches of 17 species were included in a quantitative analysis. Four species, all known to be common predators in I. typographus galleries, were caught in signi®cantly higher numbers in the unmanaged stands (two- to three-fold difference). In contrast, the number of I. typographus caught was almost identical for the two stand types. Our results indicate that predators of the spruce bark beetle may be more sensitive to certain forestry operations than their prey. Caging or baiting of bolts strongly in¯uenced the colonization of predatory species and the number of I. typographus offspring that emerged. Compared to uncaged, unbaited bolts, offspring production was ca. 30% higher in bolts caged with a ®ne nylon netting and ca. 30% lower in uncaged bolts baited with ethanol and a-pinene. No difference between stand types was found in the production of offspring by I. typographus in the bolts. In a multiple-regression analysis, including the density of certain predators and of I. typographus galleries, one factor, namely `Thanasimus larvae per bolt', could signi®cantly explain some of the variation in I. typographus offspring production in the 36 bolts. # 1999 Elsevier Science B.V. All rights reserved. Keywords: Ips typographus; Natural enemies; Numerical response; Unmanaged forest; Managed forest

1. Introduction Unmanaged and managed forests differ, with regard to population levels and species composition of various groups of organisms. For insects, several studies indicate that the number of species in different groups does not differ much between managed and unma*Corresponding author. Tel.: +4618188500; fax: +4618188600; e-mail: [email protected]

naged forest stands whereas the population levels of certain species differ markedly (e.g. Chandler, 1987, 1991; Chandler and Peck, 1992; Siitonen, 1994; ékland et al., 1995). There are few studies that experimentally seek to explain the dynamics behind the differences found. Interactions between organisms in different trophic levels might be a factor of importance. Insects high up in food chains, e.g. parasites and predators of bark- and wood-feeding insects, or insects feeding on wood-decaying fungi, might be more

0378-1127/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved. PII: S0378-1127(98)00405-8

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J. Weslien, L.M. Schroeder / Forest Ecology and Management 115 (1999) 267±275

sensitive to disturbances by forestry than the organisms depending directly on the dead phloem or wood, e.g. bark beetles and wood borers. In this study, we explore how forest management affects population levels of bark beetle-associated insects and their bark beetle host in different forest stands. The ®rst insects to colonise dead trees are phloemfeeding beetles and their associates. Bark beetles (Scolytidae) establish galleries and breed in the phloem of trees that have recently died or are dying, or else in dead-tree parts. The bark beetles are followed by other arthropods that feed on plant material, living and dead insects, fungi and detritus (see e.g. Nuorteva, 1956; Langor, 1991). Predatory and parasitic arthropod species can strongly reduce rates of bark beetle reproduction (Linit and Stephen, 1983; Miller, 1986; Riley and Goyer, 1986; Weslien, 1992, 1994; Schroeder and Weslien, 1994a, b; Schroeder, 1996). Bark beetles use olfactory cues, such as host tree volatiles and/or pheromones to ®nd suitable breeding material (e.g. Borden, 1982). Also, bark beetle-associated insects, including natural enemies, are attracted by host tree volatiles and bark beetle pheromones (Bakke and Kvamme, 1981; Borden, 1982; Chenier and PhilogeÁne, 1989; Schroeder and LindeloÈw, 1989; Schroeder and Weslien, 1994a). The key species of this study is the spruce bark beetle, Ips typographus (L.). It is a tree-killing species with distribution in spruce forests throughout Eurasia. Its main host tree in Europe is Norway spruce, Picea abies (L.) Karsten. It is regarded as a severe pest in mature spruce forests. Outbreaks often occur following extensive windfelling (Ravn, 1985; Weslien and SchroÈter, 1996) and typically last 5±8 years (Lekander, 1972; Bakke, 1983). Clean management, i.e. removal of downed spruce trees, to prevent bark beetle reproduction is an important part in the population management of this species. The spruce bark beetle has been intensively studied and more than 140 arthropod species have been recorded in the literature as inhabitants of its galleries (Weslien, 1992 and references therein). In Fennoscandia, the species has one generation per year. Numerical responses of bark beetle enemies to changes in prey density may be reproductive, e.g. offspring production increases with increased prey density, or migratory, e.g. bark beetle enemies immigrate to patches with increased prey density. Hypothe-

tically, continuous (yearly) spruce bark beetle attacks in a given stand should favour the build-up of predator and parasite populations in the stand. This hypothesis, however, remains untested and it is not known if such a build-up of local enemy populations has any signi®cance compared to the supposed immigration of enemies from the surroundings. This reasoning also applies to other bark beetle-associated insects and to insects that may utilise latter successions of decaying spruce trees. Many red-listed insects for instance are associated with dead spruce trees in varying stages of decay (Jonsell et al., 1998). In this paper, we investigate, if bark beetle enemies are more sensitive to forest management than their prey, i.e. are population levels of enemies (relative to prey populations) higher in unmanaged than in managed forest stands? Our intention is also to clarify how bark beetle enemies respond numerically to prey density in different forest stands, i.e. are there differences in population density of bark beetle enemies between stands with ongoing I. typographus attacks and those without attacks or are local overwintering populations masked by immigrating conspeci®cs? Finally, we explore how bark beetle-reproduction varies with stand type and enemy density, i.e. are there differences in I. typographus offspring production between stands with ongoing bark beetle attacks and stands without attacks, and can variation in offspring production be related to the density of certain natural enemies? 2. Materials and methods Six unmanaged stands with ongoing attacks by Ips typographus were compared pairwise with six managed stands without attacks during the previous years. In ®ve of the unmanaged stands, no forestry operations had been carried out for decades and these stands had high conservation value. The sixth unmanaged stand was a shelterwood with extensive stormfellings during several consecutive years without any sanitation measures being taken. All stands were old (>100 years) with spruce the dominating tree species (>80% of basal area). Stands within each pair were situated 2±5 km from each other, and the factors sun exposure, age and tree species composition were similar among each pair. The six blocks were situated in the province of Uppland, with 15±50 km between pairs. The forest

J. Weslien, L.M. Schroeder / Forest Ecology and Management 115 (1999) 267±275 Table 1 Number of standing and windfelled (in brackets) spruce trees colonized by Ips typographus in 12 forest stands during the years preceding the study and the study year 1993 Block

Stand type

1991

1992

1993

Skyttorp

unmanaged managed unmanaged managed unmanaged managed unmanaged managed unmanaged managed unmanaged managed

>10 0 5 0 9 2 >10 1 3 0 8 0

39 (8) (1) 8 0 11 0 10 0 4 0 10 0

18 (18) 1 5 (1) 6 1 22 0 4 5 5 0

FroÈtuna Fiby Lunsen GaÊsholmen Hammarskog

stands were fragments in a ¯at landscape (altitude for the stands 10±30 m above the sea level) dominated by clearfellings, young and middle-aged forests. Table 1 gives the numbers of Ips-attacked trees during the preceding years, 1991 and 1992, and the study year 1993. These numbers refer to an inventoried forest area within ca. 100 m radius from the experimental setup in each stand (see below). On 6 May, immediately before the initial ¯ight of Ips typographus, a trap baited with I. typographus pheromone components (plastic bag dispenser containing 1500 mg methylbutenol and 70 mg cis-verbenol) was placed in each stand. The trap consisted of a 15-cm high transparent PVC sheet held over a trough (202010 cm) ®lled with water containing detergent. Thirtysix bolts (diameter 18±22 cm, length 45 cm, bark surface 0.25±0.31 m2) were cut from six spruce trees and taken to the laboratory. The ends of the bolts were sealed with wax to prevent severe desiccation. The bolts were placed in four large net cages. Ips typographus captured in pheromone traps on a clearfelling nearby were released in the cages during 7±9 May. When the bolts were judged to be successfully colonised, they were moved to the forest during 11±13 May. Within each pair, six spruce bolts from the same tree were placed on the ground with 30±50 m interspace. In unmanaged stands, bolts were placed 30 m from a Ips typographus-attacked tree from 1992. The three bolts in each stand were randomly allotted to three

269

treatments: CB ± caged baited; UB ± uncaged baited; and UU ± uncaged unbaited. The cage for the CB treatment consisted of a cylinder (diameter 30 cm, length 60 cm) made of PVC net with 5 cm mesh inserted in a close-®tting nylon bag with 0.5 mm mesh, intended to exclude insects. All bolts were covered with a 5-cm mesh chicken net to protect them from woodpeckers. Caged bolts were included to get an estimate on the total impact of enemies on offspring production (CB vs. UU) in the various stands. Bolts were baited to increase the total catch per stand of associated insects and, thus, attain higher precision in the population estimates. The bait for the CB and UB treatments consisted of two dispensers per bolt releasing (-) -a-pinene (Fluka 97%, []20-4230) and 95% ethanol (5% water). The dispensers were designed to release the two substances in high amounts and in such ratios that are known to be strongly attract bark beetle associates (Schroeder and LindeloÈw, 1989). They were initially tested in an earlier study (Schroeder and Weslien, 1994a) and then found to release a-pinene at the rate of more than 50 mg per day and ethanol at the rate of ca. 2000 mg per day and dispenser measured on a weekly basis. During daytime, in warm weather (when these insects ¯y) over 300 mg per hour was measured for ethanol. The bolt-bait-trap arrangement is illustrated in Schroeder and Weslien (1994a, Fig. 2a) Traps were emptied weekly, during the summer until 13 July, after which the bolts were taken to the laboratory and placed in emergence traps outdoors in the shade. The emergence trap consisted of a white cotton bag (diameter 40 cm, length 110 cm) with a collecting funnel forming the bottom. The traps were emptied once or twice weekly, until insect emergence ceased in October. The bolts were then taken to the laboratory and peeled. All insects found were registered and the number of I. typographus egg galleries counted. Feeding habits of the species encountered were taken from the literature. The most important sources were Saalas (1917), Nuorteva (1956, 1959), Ä unap (1980, 1992) and Mills Palm (1951, 1959), O (1985). 2.1. Statistics The number of bark beetle-associated insects for species, captured in suf®ciently high numbers (>50

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J. Weslien, L.M. Schroeder / Forest Ecology and Management 115 (1999) 267±275

specimens), was analysed in three-factor analysis of variance, the factors were: `Block' (nˆ6); `Treatment' (CB, UB and UU); and `Stand' (unmanaged and managed). To increase the homogeneity of variances, insect numbers were log-transformed prior to analysis. It was assumed that the log-transformed values came from the normally distributed populations. Data associated with the bolts, i.e. number of insects per species (emerging or found under bark) and egg gallery numbers, were subjected to the same type of analysis as trap data. The variation in the number of Ips typographus offspring emerging from the 36 bolts was analysed in a multiple regression with number of potential predators and competitors (six species included) per bolt and egg gallery number per bolt as independent variables. Variables were log-transformed and subjected to residual analysis before being entered in the regression. 3. Results Seventeen species caught in the window traps were subjected to analysis. Of these, four were bark feeding, three had unclear feeding habits (probably saprophagous or mycetophagous), and nine were predators of bark beetle brood (Table 2). Four species, all common predators of I. typographus were caught in signi®cantly (p<0.05) higher numbers in the unmanaged stands than in the managed stands. There were no signi®cant differences in the number of I. typographus caught in pheromone traps between the two stand types (Table 2). The effect of baiting on the number of insects captured was in general, much greater than the effect of stand type. A statistically signi®cant (p<0,05) effect of `treatment' was found for all but two species (Table 2). No differences were found for any species between CB and UB treatments whereas the UU treatment caught signi®cantly fewer insects than at least one of the baited treatments (Tukey test, p<0.05). For three out of the 17 species, temporal catch patterns differed between managed and unmanaged stands, i.e. signi®cantly higher proportions in unmanaged than in managed stands were captured during the ®rst trapping week as compared to the remaining

trapping period (p<0.05, chi-square analysis). These species were Plegaderus vulneratus, Rhizophagus ferrugineus and Tetropium castaneum. A total of 370 insect species caught in the traps where identi®ed to species (339 Coleoptera, 3 Hemiptera, 17 Diptera and 11 Hymenoptera). Of these, 208 species are known to be associated with dead bark or wood. Almost all species were recorded in at least one unmanaged and one managed stand. Eleven red-listed beetle species in the threat category, `care demanding' (EhnstroÈm et al., 1993), were caught, of which three species were caught only in the unmanaged stands (Playsoma deplanatum (Gyllenhal) (Histeridae), Ampedus suecicus Palm (Elateridae), Dendrophagus crenatus (Paykull) (Cucujidae)), ®ve only in the managed stands (Hapalarea linearis (Zetterstedt) (Staphylinidae), Platysoma minus (Rossi)(Histeridae), Buprestis haemorrhoidalis Herbst (Bupresitidae), Enicmus planipennis Strand (Latridiidae), Cis lineatocribratus Mellie (Cisidae)) and three species in both stand types (Paromalus parallelopipedus (Herbst) (Histeridae), Atomaria elongatula Erichson (Cryptophagidae), Serropalpus barbatus (Schaller) (Melandryidae)). Mean numbers of insects found emerging from the bolts are given by species and treatment in Table 3. There was a clear effect of caging and baiting on the offspring production of I. typographus in the bolts. Caging increased offspring production by 23±38% (UU vs. CB) and baiting reduced it by 27% (UU vs. UB). The number of potential predators or competitors in the bolts differed between treatments, being the highest in the UB treatment for all species. There was no signi®cant effect of stand type on number of insects of any species at 5% probability level. However, for Thanasimus spp. larvae, there was a trend to higher number in bolts from unmanaged stands (pˆ0.06). The caging did not prevent colonisation of insects. In fact, some species were more common in the CB bolts than in the UU bolts, e.g. R. ferrugineus. Many small staphylinids (e.g. Leptusa spp., Phloeonomus spp. and Placusa spp.) and minute bark beetles (Crypturgus spp.) emerged from the bolts, but these were not counted. Some other species were identi®ed, but were found in <50 specimens and were not included in Table 3 (four species of parasitic wasps (the pteromalids Roptrocerus xylophagorum Ratze-

J. Weslien, L.M. Schroeder / Forest Ecology and Management 115 (1999) 267±275

271

Table 2 Mean number of bark beetle associated insects captured per trap and per stand in traps distributed in 12 standsa Treatment

Stand

dfˆ2

dfˆ1

CBb

pe

unman.

man.

8.1

<0.001

29.9

10.3

0.012

L, A?

0.2 ±

4.4 ±

<0.001 ±

11.1 5.9

7.6 1.6

0.08 0.04

L, A L, A

1.0

128.5

<0.001

405.2

166.3

0.009

A, L?

0.1

77.6

<0.001

226.9

89.1

0.004

A, L

0.2

2.7

0.002

6.3

3.2

>0.1

L

0.4 2.4

23.3 52.1

<0.001 <0.001

55.0 129.1

51.3 98.5

>0.1 >0.1

A, L A, L?

10.6

10.4

>0.1

16.4

46.2

>0.1

L?

± 59.5 208

± 4.7 15.8

± 45.8 200.7

± <0.001 0.002

824.0 88.5 421.0

872.5 131.3 427.0

>0.1 >0.1 >0.1

2.1 6.9

0.6 0.8

2.4 5.1

<0.001 <0.001

5.8 15.6

4.5 6.7

>0.1 0.09

3.9

0.4

2.3

>0.1

5.6

7.5

>0.1

3.3 6.5

0.6 0.1

1.8 2.8

0.021 <0.001

7.6 9.2

3.8 9.5

>0.1 >0.1

Predators common in Ips typographus galleries Coleoptera Histeridae Plegaderus vulneratus (Panzer) 10.0 Cleridae Thanasimus formicarius (L.) 5.0 Thanasimus femoralisf ± Nitidulidae Epuraea pygmaea (Gyllenhal) 159.0 Rhizophagidae Rhizophagus ferrugineus (Paykull) 80.2 Diptera, Dolichopodidae Medetera signaticornis Loew 1.8 Predators mainly of other bark beetle species Coleoptea, Nitidulidae Pityophagus ferrugineus (L.) 28.0 Epuraea marsueli (Reitter) 58.3 Diptera, Dolichopodidae Medetera infumata 10.2 Phloem-feeding beetles Scolytidae Ips typographus (L.)f Hylastes cunicularius Erichson Dryocoetes autographus (L.) Cerambycidae Rhagium inquisitor (L.) Tetropium castaneum (L.) Saprophagous or unclear feeding habits Diptera, Stratomyidae Zabrachia minutissima Coleoptera, Stapylinidae Leptusa pulchella (Mannerheim) Placusa depressa MaÈklin

UUc

UBd

0.2

Predatory life stage p

a

Species that were captured in >50 specimens. Trap next to caged I. typographus-attacked bolt baited with a-pinene and ethanol. c Trap next to uncaged unbaited I. typographus-attacked bolt. d Trap next to uncaged I. typographus-attacked bolt baited with a-pinene and ethanol. e p-Values refer to F-ratios from factorial Anova of log-transformed values (residual dfˆ25) for all species except those marked with f. f t-test of captured specimens in pheromone traps. b

burg, Rhopalicus tutele Walker and Tomicobia seitneri Ruschka and the braconid Rhopalophorus clavicornis Waesmal) and four beetle species (the histerids Cyl-

ister linearis (Erichson) and Paromalus paralellopipedus (Herbst) and the staphylinids Nudubius lentus (Gravenhorst) and Quedius plagiatus (Mannerheim)).

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J. Weslien, L.M. Schroeder / Forest Ecology and Management 115 (1999) 267±275

Table 3 Means  standard errors for number of Ips typographus egg galleries, Ips typographus offspring and associated insects per bolt and treatment in unmanaged and managed stands, respectively. All values were log-transformed prior to analysis pa

Mean  s.e. unmanaged CB

managed UU

Multiple regression

ANOVA

UB

CB

UU

UB

treatm (dfˆ2)

stand (dfˆ1)

95361.0

Ips typograpus offspring

83665.1 68156.0

496127

68942.3

50259.9

<0.001

>0.1

Ips typographus egg galleries Thanasimus larvae Dryocoetes autographus adults Rhizophagus ferrugineus adults Plegaderus vulneratus adults Rhagium inquisitor larvae Epuraea pygmaea adults

81.25.1 71.55.1 3.51.0 7.62.7 47.326.2 91.226 24.017.8 0.50.3 0.20.2 0 2.30.9 6.53.3 0.80.8 1.01.0

72.57.5 81.75.6 68.55.0 11.53.8 3.87.4 3.32.3 22349.2 77.543.2 99.334.2 49.322.8 21.89.9 7.36.7 15.23.6 0 0.20.2 6.32.1 0.20.2 7.13.7 6.34.2 4.83.8 1.21.2

79.89.5 10.53.2 382107 96.844.0 13.73.7 9.53.8 16.59.7

>0.1 0.007 <0.001 <0.001 <0.001 0.008 0.03

>0.1 0.06 >0.1 >0.1 >0.1 >0.1 >0.1

a

dependent variable 0.06 0.04 >0.1 >0.1 >0.1 >0.1 >0.1

p-Values refer to F-ratios (residual dfˆ25) in analysis of variance and to t-values for multiple regression analysis of 36 bolts.

In a multiple-regression analysis of the 36 bolts, only one variable could signi®cantly (p<0.05) explain the differences in I. typographus offspring production. This variable was the number of Thanasimus larvae per bolt (Table 3). The analysis of variance for the regression showed that although the regression was statistically signi®cant (Fˆ8.7, df 2/33, p<0.001), 67% of the variation remains unexplained (residual mean square divided by the total mean square). The effect of `block' was signi®cant (p<0.05) for 11 out of the 15 species in the analysis of variance of trap catches. In the analysis of variance of data from the bolts, `block' was signi®cant only for one variable, I. typographus offspring per bolt. 4. Discussion For I. typographus and several other species there were no differences in numbers caught between the two stand types. The results indicate that I. typographus and many other insects belonging to this primary guild, i.e. inhabiting newly dead spruce trees, are highly mobile and that the local overwintering populations within stands may be masked by high numbers of conspeci®cs that immigrate in response to host odours. In contrast, the local populations of four species, all predators of I. typographus, were evidently not masked by immigrants. This indicates that the

reproduction of these predators is favoured by yearly bark beetle attacks in the same place. It might be argued that between-stand differences in ¯ying insect populations become smaller as the ¯ight season progresses and insects disperse over large areas. Thus, differences in population levels between unmanaged and managed stands should be largest early in the season for species that overwintered in the stands. Such a pattern was also found for two predatory species, namely R. ferrugineus and P. vulneratus. This supports the theory that a large proportion of these captured beetles had developed the previous year in the killed trees in stands. That `block' had a signi®cant effect on the catch size, for most of the species con®rms that the pairwise experimental set-up was meaningful. Our impression is that a varying degree of sun-exposure between blocks was important in this context. Offspring production was strongly affected by caging and baiting. Differences in predation level by Thanasimus larvae under bark was evidently the main cause for this treatment effect, as indicated by the multiple-regression analysis. Although, Thanasimus larval density did signi®cantly explain the variation in offspring production between the 36 bolts, most of the variation remained unexplained. This is not surprising. Block effects are one source of variation not taken into account in the regression. Another source is bark beetle egg gallery density (pˆ0.06 in

J. Weslien, L.M. Schroeder / Forest Ecology and Management 115 (1999) 267±275

the multiple regression). A third source is the number of Thanasimus larvae caught while emerging from the bolts is a poor measure of predation level. In an earlier study (Schroeder and Weslien, 1994a), we found that 66% of the total number of Thanasimus larvae that emerged from pine bolts colonised by the pine shoot beetle Tomicus piniperda (L.), emerged within 9 weeks from the initial exposure of the bolts in the late April. Also, in the present study, the bolts were exposed for 9 weeks before they were hung in the emergence traps. Thus, it is likely that many of the Thanasimus larvae that had fed under bark are unaccounted for. Moreover, in our earlier study, the course of emergence of Thanasimus larvae from baited bolts was faster than that from the unbaited. This means that Thanasimus larval density for baited bolts may be underestimated relatively more than for unbaited bolts. The negative effect of baiting on bark beetle-offspring production, i.e. UB compared with UU, in this study was much lower than in our earlier study on Tomicus piniperda (27% vs. ca. 80%). This difference might be attributed to different predation levels. In the earlier study, a mean number of 27 Thanasimus adults per baited bolt was captured compared to 5 per unbaited bolt. The corresponding ®gures for the present experiment were 5 and 0.2, respectively. The effect of caging, i.e. CB compared with UU, was ca. 30% in the present study compared with 83% in an earlier study on I. typographus (Weslien, 1992). The difference between these studies might partly be due to the fact that predatory species entered through the cage in the present study. Another factor is that parasitoids (Pteromalidae) and predatory ¯ies (Medetera spp.) found in the bolts were rare in the present study but abundant in the earlier. The number of Thanasimus larvae, emerging from the uncaged bolts, was about the same in both studies. We caught very few parasitoids both, in the window traps and bolts. The reason for this is not known. The bolts remained in the forest, until the I. typographus offspring had entered the late larval or pupal stage and the ®rst emergence holes at sun-exposed sites started to appear. Thus, there should have been plenty of time for the parasitoids to attack the preferred life stages, i.e. late larval or pupal stage (e.g. Berisford et al., 1970; Stephen and Dahlsten, 1976; KruÈger and Mills, 1990). For some reasons, it seems that parasitoid

273

activity was very low around the bolts on all sites. The window traps might have been inef®cient in catching parasitoids but then still the bolts should have contained parasitoids, had there been any activity. In another study, with similar bolts attacked by I. typographus (Weslien, 1992), the method for extracting insects (emergence bags) proved to be very ef®cient for several parasitoid species. It was also evident from that study, which was made in a stand where spruce bark beetle attacks had occurred during several consecutive years, that parasitoids can become locally very abundant. It might be hypothesised that bark beetle parasitoids, due to their fragility, may have poor dispersal capacity and that they should be particularly favoured by yearly bark beetle attacks in the same place. This hypothesis, however, remains to be tested. ékland et al. (1995) demonstrated for saproxylic beetles that the scale at which variables, such as population level and species diversity, is measured is important for how strongly these variables are correlated with different habitat characteristics, e.g. amount of dead wood. For the smallest patch size (ca. 0.2 ha), there was only a weak correlation, whereas correlations grew stronger as patch size increased to 1 and 4 km2. In the light of that study, patch size in our study was probably too small to ®nd any overall differences in species assemblages between the two stand types. Regarding the red-listed species captured here, it seems that the catch of single specimens in ¯ight traps may have limited use as indicators of high conservation values at the stand scale. Little is known about the factors that limit the population density of bark beetle enemies. One important factor is the density of the prey, but the signi®cance of this factor is likely to differ with the level of spatial scale at which density is measured. Weslien (1994) demonstrated a positive reproductive response in the predator T. formicarius to prey density at the tree level. Also at the regional (landscape) level, a positive numerical response has been indicated (Billings, 1988; Weslien, 1994). The present study is the ®rst to demonstrate how population density of several bark beetle predators varies with bark beetle density at the stand scale. Our results indicate that certain predators might be more sensitive to forest operations than their bark beetle hosts. However, removal of I. typographus-attacked trees before brood emergence does

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seem to reduce the risk for new attacks in a stand (Butovitsch, 1941; Ravn, 1985), and our ®ndings do not present new alternatives for stand management. There is empirical evidence that habitat fragmentation may reduce parasitism rates on herbivorous insects, both at a small spatial scale, i.e. in experimentally fragmented clover ®elds (Kruess and Tscharntke, 1994), and at larger scales, i.e. aspen forest landscapes (Roland and Taylor, 1997). We stress that comparative studies on how populations of bark beetles and their associates are affected by forestry at the landscape scale are lacking. Moreover, there is still a large gap in the knowledge of how bark beetle parasitoids are affected by forestry both, at stand and landscape scales. Until such studies have been carried out, it cannot be excluded that forest operations that favour natural enemies in the landscape might be economically favourable compared to traditional stand management tactics. Acknowledgements Ä unap identi®ed and gave us notes on the Heino O biology of Diptera and Hymenoptera, Rune Axelsson and Stig Lundberg helped in identifying beetles, and Mats Jonsell gave us notes on the biology many of the Ä unap and Rune Axelsson also beetle species. Heino O assisted in the ®eld. Thank you. References Bakke, A., Kvamme, T., 1981. Kairomone response in Thanasimus predators to pheromone components of Ips typographus. J. Chem. Ecol. 7, 305±312. Bakke, A., 1983. Host tree and bark beetle interaction during a mass outbreak of Ips typographus in Norway. Z. Ang. Ent. 96, 118±125. Berisford, C.W., Kulman, H.M., Pienowski, R.L., 1970. Notes on the biologies of hymenopterous parasites of Ips spp. bark beetles in Virginia. Can. Ent. 102, 484±490. Billings, R.F., 1988. Forecasting southern pine beetle infestation trends with pheromone traps, in: Payne, T.L., Saarenmaa, H. (Eds.) Proceedings of the IUFRO working party and XVII International Congress of Cutomology Symposium ``Integrated control of bark beetles'' Vancouver Canada, July 4 1988. Virginia Polytechnic Inst. and State Univ. pp. 295±306. Borden, J.H., 1982. Aggregation pheromones. in: Mitton, J.B., Sturgeon, K.B. (Eds.), Bark Beetles in North American Conifers. University of Texas Press, Austin, Texas, pp. 74±139.

Butovitsch, V., 1941. Studien uÈber die Massenvermehrung von Ips typographus in den vom Dezembersturm 1931 heimgesuchten WaÈldern von Nord-Uppland. Medd. Statens Skogsforskningsinst., 32, 297±360 (In Swedish with German summary). Chandler, D.S., 1987. Species richness and abundance of Pselaphidae (Coleoptera) in old-growth and 40-year-old forests in New Hampshire. Can. J. Zool. 65, 608±615. Chandler, D.S., 1991. Comparison of some slime-mold and fungus feeding beetles (Coleoptera: Eucinetoidea, Cucujoidea) in an old-growth and 40-year-old forest in New Hampshire. The Coleopterist Bulletin 45, 239±256. Chandler, D.S., Peck, S.B., 1992. Diversity and seasonality of leiodid beetles (Coleoptera: Leiodidae) in an old-growth an a 40-year-old forest in New Hampshire. Environ. Entomol. 21, 1283±1293. Chenier, J.V.R., PhilogeÁne, B.J.R., 1989. Field response of certain forest Coleoptera to conifer monoterpenes and ethanol. J. Chem. Ecol. 15, 1789±1846. Ê ., 1993. Swedish redlist EhnstroÈm, B., GaÈrdenfors, U., LindeloÈw, A of invertebrates 1993. Databanken foÈr hotade arter, SLU, Uppsala, ISBN 91-88506-02-9. (in Swedish with English abstract). Jonsell, M., Weslien, J., EhnstroÈm, B., 1998. Substrate requirements of red-listed saproxylic invertebrates in Sweden. Biodiversity and Conservation (in press). KruÈger, K., Mills, N.J., 1990. Observations on the biology of three parasitoids of the spruce bark beetle, Ips typographus (Col. Scolytidae): Coeloides bostrichorum, Dendrsoter middendirfii (Hym., Braconidae) and Rhopalicus tutela (Hym. Pteromalidae). J. appl. Ent. 110, 281±291. Kruess, A., Tscharntke, T., 1994. Habitat fragmentation, species loss, and biological control. Science 264, 1581±1584. Langor, D.W., 1991. Arthropods and nematodes co-occurring with the eastern larch beetle. Dendroctonus simplex (Col.: Scolytidae) in Newfoundland. Entomophaga 36, 303±313. Lekander, B., 1972. A mass outbreak of Ips typographus in GaÈstrikland, Central Sweden, in 1945±1952. Research note 10. Dept. Forest Zoology, Royal College of Forestry, 39 pp., Stockholm (in Swedish with English summary). Linit, M.J., Stephen, F.M., 1983. Parasite and predator component of within-tree southern pine beetle mortality (Coleoptera Scolytidae). Mortality. Can. Ent. 115, 679±688. Miller, M.C., 1986. Survival of within-tree Ips calligraphus (Col.: Scolytidae): Effect of insect associates. Entomophaga 31, 305± 328. Mills, N.J., 1985. Some observations on the role of predation in the natural regulation Ips typographus populations. Z. Ang. Ent. 99, 209±215. È ber den Fichtenstamm-BastkaÈfer, Hylurgops Nuorteva, M., 1956. U palliatus und seine Insektenfeinde. Acta Ent. Fenn. 34, 56±65. Nuorteva, M., 1959. Untersuchungen uÈber einige in den Frassbildern der BorkenkaÈfer lebende Medetera-artern (Dipt. Dolichopodidae). Ann. Ent. Fenn. 25, 192±210. Ä unap, H., 1980. On the specific composition of the predatory O Coleoptera established in the boreholes of bark beetles inhabiting conifers. Metsanduslikud Uurimused, 16, 34±43 (In Russian with English summary).

J. Weslien, L.M. Schroeder / Forest Ecology and Management 115 (1999) 267±275 Ä unap, H., 1992. On the specific composition of the predatory O Diptera established in the boreholes of bark beetles inhabiting conifers in Estonia. Metsanduslikud Uurimused, 24, 143±151 (In Russian with English summary). Palm, T., 1951. Die Holz- und RindenkaÈfer der nordschwedishen LaubaÈume. Medd. Stat. Skogsforskningsinst. 40, 1±241. Palm, T., 1959. Die Holz- und RindenkaÈfer der suÈd- und mittelschwedishen LaubaÈume. Opuscula Entomol. Suppl. 16, 1±375. Ravn, H.P., 1985. Expansion of populations of Ips typographus (L.) (Coleoptera, Scolytidae) and their local dispersal following gale disaster in Denmark. Z. Ang. Ent. 99, 26±33. Riley, M.A., Goyer, R.A., 1986. Impact of beneficial insects on Ips spp. (Coleoptera, Scolytidae) bark beetles in felled loblolly and slash pines in Louisiana. Environ. Entomol. 15, 1220±1224. Roland, M.A., Taylor, P.D., 1997. Insect parasitoid species respond to forest structure at different spatial scales. Nature 386, 710± 713. Saalas, U., 1917. Die FichtenkaÈfer Finnlands. 1. Ann. Ac. Sci. Fenn. Ser. A, 8, 547 pp. Schroeder, L.M., 1996. Interactions between the predators Thanasimus formicarius (Col.: Cleridae) and Rhizophagus depressus (Col.: Rhizophagidae), and their bark beetle host Tomicus piniperda (Col.: Scolytidae). Entomophaga 41, 63±75. Ê ., 1989. Attraction of scolytids and Schroeder, L.M., LindeloÈw, A associated beetles by different absolute amounts and proportions of -pinene and ethanol. J. Chem. Ecol. 15, 1591±1599. Schroeder, L.M., Weslien, J., 1994a. Reduced offspring production in the bark beetle Tomicus piniperda in pine bolts baited with

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ethanol and -pinene which attract antagonistic insects. J. Chem. Ecol., 20, 1429±1444. Schroeder, L.M., Weslien, J., 1994b. Interactions between the phloem-feeding species Tomicus piniperda (Col.: Scolytidae) and Acantocinus aedilis (Col.: Cerambycidae), and the predator Thanasimus formicarius (Col.: Cleridae) with special reference to brood production. Entomophaga, 39, 149±157. Siitonen, J., 1994. Decaying wood and saproxylic Coleoptera in two old spruce forests: A comparison based on two sampling methods. Ann. Zool. Fennici 31, 89±95. Stephen, F.H., Dahlsten, D.L., 1976. The arrival sequence of the arthropod complex following attack by Dendroctonus brevicomis (Coleoptera: Scolytidae) in ponderosa pine. Can. Ent. 108, 283±304. Weslien, J., 1992. The arthropod complex associated with Ips typographus (L.): Species composition, phenology, and impact on bark beetle productivity: Entomol. Fennica 3, 205±213. Weslien, J., 1994. Interactions within and between species at different densities of the bark beetle Ips typographus and its predator Thanasimus formicarius. Entomol. Exp. Appl. 71, 133±143. Weslien, J., SchroÈter, H., 1996. NatuÈrliche Dynamik des BorkenkaÈferbefalls nach Windwurf. AFZ der Wald, 1996/19, 1052± 1055. ékland, B., Bakke, A., HaÊgvar, S., Kvamme, T., 1995. What factors influence the diversity of saproxylic beetles? A multi scale study from a spruce forest in southern Norway. Biodiversity and Conservation, 5, 75±100.