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Keywords:

  • Complementarity of sampling methods;
  • dead wood;
  • emergence trap;
  • flight intercept trap;
  • forestry;
  • habitat requirements;
  • parasitoid–host associations

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendices

Abstract.  1. Species of higher trophic levels are predicted to be more vulnerable to disturbances (e.g. by forestry) than their prey because of low population densities, extreme specialisation and reliance on intact trophic chains.

2. The aim of this study was to acquire some much-needed basic information on saproxylic parasitoids in boreal forest landscapes. To obtain reliable estimates of species richness, abundance, assemblage composition and host associations of saproxylic parasitoids in different stand types (clear-cuts, mature managed forests and old-growth reserves), we used two different methods (emergence traps and window traps).

3. Window traps caught more species and gave a better measure of the species pool in different stand types, while emergence traps were more suitable for detailed analyses concerning substrate requirements, hatching periods and to some extent host choice.

4. The general distribution pattern revealed no significant differences in species richness among stand types, but parasitoid assemblages were affected by forest successional stage. Idiobionts, dominated by Ontsira antica and Bracon obscurator, preferred clear-cuts over forested sites, while koinobionts, especially Cosmophorus regius, were more common in mature forests and reserves. We conclude that the stand types studied were complementary in assemblage composition, but that none held a complete assemblage of saproxylic parasitoids and we suggest that a range of successional stages be retained to help conserve the entire parasitoid community.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendices

We lack important biological and ecological data for many forest-dwelling organisms, and we especially need to learn more about the species interactions that take place in forest ecosystems in order to improve conservation-oriented measures. In particular, species belonging to higher trophic levels, and which are often highly specialised and occur in small and variable population sizes (Kruess & Tscharntke, 2000; Shaw & Hochberg, 2001), should be of conservation concern. Such species are potentially more sensitive to disturbances than their associated hosts (Komonen et al., 2000; Siitonen, 2001) and might serve as indicators of ecosystem changes and provide useful insights into the effects of modern forestry practices. For example, we have some basic knowledge about habitat and substrate requirements of many saproxylic beetles (i.e. beetles dependent on dead wood, see Speight, 1989) (Jonsell et al., 1998; Siitonen, 2001; Grove, 2002; Jonsell & Weslien, 2003; Dahlberg & Stokland, 2004; Gibb et al., 2006), but stand and substrate characteristics may be of even greater importance for associated predators and parasitoids (Martikainen et al., 1999; Weslien & Schroeder, 1999; Hilszczański et al., 2005; Johansson et al., 2007a; Gibb et al., 2008). In this study, we focus on sampling saproxylic parasitoids (Hymenoptera, Ichneumonoidea) in different stand types and identifying host-relationships, which may provide valuable information for managing biodiversity and maintaining whole insect communities in managed boreal forest landscapes.

Parasitic Hymenoptera are globally one of the most species-rich insect groups (Gaston, 1991) and have been suggested to be even more diverse in temperate than in tropical regions (Sime & Brower, 1998; Shaw & Hochberg, 2001), although this may be an artefact of low sampling effort and undescribed species (Sääksjärvi et al., 2004; Jones et al., 2009). Parasitic Hymenoptera play an important role in ecosystems (see Shaw & Hochberg, 2001 and references within), but have mainly been studied in agricultural biological control programs, where they are used to suppress herbivorous pest insect populations (Neuenschwander, 2003; Mills, 2005). Surprisingly, however, parasitoids have been severely neglected in conservation ecology studies (Shaw & Hochberg, 2001) and little is known about these species and their complex interactions in forest ecosystems (but see Hilszczański et al., 2005; Klein et al., 2006; Fraser et al., 2007; Gibb et al., 2008). Furthermore, because of their specialisation and their position at high trophic levels, parasitoids are considered extinction prone (La Salle & Gauld, 1993; Kruess & Tscharntke, 1994, 2000; Shaw & Hochberg, 2001). This suggests that they might be rather sensitive to environmental changes caused by modern forestry like fragmentation, habitat loss or a shortage of substrate (i.e. dead wood).

Many saproxylic beetles have become rare as a result of intense forestry and are on the IUCN Red List of Threatened Species: e.g. in Sweden 501 of 1257 saproxylic beetles are red listed (Dahlberg & Stokland, 2004; Gärdenfors, 2005). However, no saproxylic parasitoids (Hymenoptera, Ichneumonoidea) have yet entered the Swedish red-list (Gärdenfors, 2005). This is mainly due to insufficient information for most of the species within this group (Weslien & Schroeder, 1999; Gärdenfors, 2005). In fact, most of our current knowledge is in large part based on simple host records (Kenis & Hilszczański, 2004; Kenis et al., 2004). Thus, while it is very important to collect basic information on factors like distribution, occurrence, habitat and substrate requirements, it is also important to continuously improve our knowledge about host-relationships of saproxylic parasitoids. However, when collecting species with small populations and patchy distributions it can be of utmost importance what method to use, and thus we also need to improve our knowledge about how to sample saproxylic parasitoids (see however Fraser et al., 2008; Pucci, 2008).

In conclusion, there is an urgent need both to evaluate methods to collect parasitoids and to determine their habitat, substrate requirements and host associations for understanding their role in boreal forests and how this might be influenced by forestry. In this study, we therefore use two different kinds of methods: (i) emergence (eclector) traps and (ii) flight intercept (window) traps in three different stand types (i.e. clear-cut, mature managed forest, and old-growth reserve), to assess the desired information above. We addressed the following questions:

  • 1
     Are there differences between emergence- and window-traps in catching saproxylic parasitoids?
  • 2
     How are the assemblages of saproxylic parasitoids affected by forestry?

Material and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendices

Study area and experimental design

The study areas were located in the middle boreal forest zone (Ahti et al., 1968) in the counties of Västernorrland and Västerbotten in northern Sweden (between the latitudes 63.6208°N and 64.2858°N, and longitudes 16.8898°E and 20.1328°E). All areas were dominated by Norway spruce (Picea abies (L.) Karst.) with a mix of Scots pine (Pinus sylvestris L.) and birch (Betula spp.). The understorey vegetation was of moist to mesic Vaccinium myrtillus L. type (Ebeling, 1978), and the altitude ranged from 200 to 500 m a.s.l.

The large-scale field experiment consisted of ten localities, each including three different stand types, i.e. an old-growth reserve (mean stand age of 151 years), a mature managed forest (mean stand age 108 years), and a clear-cut (cut in 2000 or 2001). On each site, we used a randomised block design (Hurlbert, 1984) with three blocks per site and six different dead wood types in each block, i.e. a standing spruce snag of ∼3 m in height and five lying spruce logs (length = 4 m, mean ± SE diameter = 20.8 ± 6.3 cm): an untreated control log, a burned log, a naturally shaded log and two fungi-inoculated logs (Fomitopsis pinicola (Swartz ex Fr.) Karst. and Resinicium bicolor (Alb. & Schwein) Parmasto, respectively). To guard against any effects being confounded by variation in the quality of dead wood, all logs were produced in the same felling operations early in 2001 (one locality) and in autumn 2001 (nine localities). The logs were introduced to the experimental sites in spring 2001 (one locality) and between September 2001 and March 2002 (nine localities). The snags were created in situ at the forested sites, while on clear-cuts snags created at the logging operation were used. This experimental set-up gives us good possibilities to determine habitat- and substrate requirements of saproxylic beetles and their parasitoids and may allow us to detect possible effects from modern forestry. Note, however, that in this document, we use this variety of experimentally treated substrates to assess the community of saproxylic parasitoids in different stand types, and not to evaluate the effect of these individual treatments per se. For effects of treatments on parasitic wasps see Hilszczański et al., 2005, who found that snags held different parasitoid assemblages than the other dead wood types.

To capture insects, both trunk emergence traps and trunk window traps were used. The emergence traps measure the production of saproxylic insects in the logs and snags and were attached at a random position on each log/snag. The emergence traps were designed to catch all insects that emerge from a particular piece of dead wood by wrapping a polypropylene weed barrier of 30 cm of width around the logs and snags (see Johansson et al., 2006 and Alinvi et al., 2007 for further details). The barrier allowed passage of moisture and oxygen, but not light. To seal the sides of the trap and to attach it to the log, we used an underlay of foam and tightened iron wires around the trap. A translucent 250 ml plastic bottle, half-filled with 50% propylene glycol with a small amount of detergent to reduce surface tension was attached to the top of the trap to collect the insects (Southwood & Richard, 1978; Schiegg, 2001). The window traps were attached at a random position on the logs and at breast height on the snags. The window traps give a measure of which insects are attracted to a certain dead wood type (i.e. are in its vicinity), and do not treat the logs or snags as a source for emerging insects as the emergence traps do. The window traps consisted of a transparent piece of polycarbonate (10 × 15 cm) that was attached vertically to each log/snag as a flight intercept. To collect the insects, an aluminium tray (11 × 15 cm) half-filled with 50% propylene glycol with a small amount of detergent was attached under the polycarbonate window (see Johansson et al., 2006 and Alinvi et al., 2007 for further details).

The sampling with emergence traps took place in four periods: late September 2002–late May 2003, late May–late June 2003, late June–late July 2003, and late July–late September 2003. The trapping with window traps only took place in the period of late June–late July 2003. All saproxylic parasitoids of the superfamily Ichneumonoidea (Ichneumonidae and Braconidae, see Yu & Horstmann, 1997; Yu et al., 2005) were extracted from the samples and determined to species by experts. For the taxonomically difficult Rhimphoctona spp. we were able to separate three different species, but not identify them to species entities. We divided the parasitoids into koinobionts and idiobionts (Haeselbarth, 1979; Askew & Shaw, 1986). Koinobionts have a narrow host range and are mostly endoparasitoids, whereas the guild of idiobionts often has a wider host range and includes many ectoparasitoids, which kill or paralyse their host permanently before the egg hatches (Askew & Shaw, 1986; Fitton et al., 1988).

Data analysis

To reduce zeroes in our dataset we pooled the data for all three blocks per stand type and each site. Thus site was used as block factor and was fixed in our analyses. We also pooled data for all the different log treatments (for treatment effects see Hilszczański et al., 2005). Species accumulation curves (per sample site) were created to show how different trap types sample the boreal parasitoid fauna. We performed two randomised block anovas (analysis of variance) to test the effect of trap type and stand type on the response variables: total species richness, total abundance, the abundance of the two trophic guilds of idiobionts and koinobionts, and the two most common species in each of these guilds. In the first anova, we tested for differences between trap types, and here we only used data from July 2003 because this was the period when both trapping methods were used. In the second anova, we specifically compared different stand types, not trapping methods, and therefore used the emergence trap data from all trapping periods and pooled it with the window trap data to get a bigger sample size. This could be done as we detected no interactions between trap type and stand type in the first anova. We used SYSTAT version 12 (Systat Software Inc, 2007) for the above analysis and the data were log (x + 1) transformed to meet the assumptions of normality and homogeneity of variances. However, in large balanced experiments such as this one, anova is rather robust to many departures from the assumptions (Underwood, 1997). When significant effects appeared between stand- or trap types, we examined these differences with Tukey’s honestly significant difference (HSD) test (Sokal & Rohlf, 1995).

To compare species assemblage composition between trap types and between stand types, we used permanova (permutational multivariate analysis of variances) (Anderson, 2003) in the program PRIMER 6 (PRIMER-E Ltd, 2007). The non-parametric permanova is a useful tool when working with ecological data, which do not meet assumptions of normality and homoscedasticity, because it still allows us to investigate complex models which include interactions (Anderson, 2001; McArdle & Anderson, 2001). To reduce the weighting of the most abundant species, while still preserving relative abundances, we fourth-root transformed our data (Clarke, 1993). We used the Bray-Curtis similarity measure, which is not affected by joint absences (Field et al., 1982), no standardisation was used and we ran 4999 permutations of residuals under a reduced model. To identify which species contributed most to observed differences in species assemblages between stand types and between trap types we used SIMPER (Similarity Percentage Analysis, Clarke & Gorley, 2006), again on fourth-root transformed data. This is not a test of statistical probabilities per se, but a way of conceptualising differences in species relative abundances between two sets of data: SIMPER calculates the overall percentage contribution that each species makes to the average dissimilarity between two groups and lists the species in decreasing order of their importance in discriminating the two sets of samples (Clarke & Gorley, 2006).To graphically illustrate differences in the assemblages of parasitoids, we used non-metric MultiDimensional Scaling (nMDS hereafter) (Clarke & Warwick, 2001).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendices

In total, we caught 1456 individuals of saproxylic parasitoids, belonging to 43 different species (Appendix A). In the subset of our data which was used to compare window traps with emergence traps (July sample), we still had the same 43 species and only a modest reduction to 1175 individuals (Appendix A). In other words, most saproxylic parasitoids were caught in the July trapping period (i.e. late June–late July), e.g. especially koinobiont species, of which none were caught in the June sample (i.e. late May–late June). The idiobiont Bracon obscurator was mainly collected in June, while Ontsira antica was more abundant in the late trapping period (late July–late September) (see Appendix B).

Trap type

Window traps collected significantly more species than emergence traps (Fig. 1), but no significant differences were detected for total abundance or the abundances of idiobionts or koinobionts as groups (Table 1, Fig. 2a). However, on a species level, both O. antica, B. obscurator and Cosmophorus regius were more abundant in emergence traps. These species, along with Helconidea dentator and Bracon hylobii, contributed most to the significant differences in species assemblages (Table 2) detected between the trapping methods (SIMPER: 73.55% dissimilarity). Whereas the catch in emergence traps to a large extent was dominated by the four dominant species, the window traps caught a much wider range of species (Appendix A). Notably, window traps caught 23 unique species, e.g. Xorides irrigator, compared to only three unique species in emergence traps, e.g. Cosmophorus cembrae. Neither the anova nor the permanova showed any significant interactions between trap type and stand type. Differences between sites were detected in several cases, but might be due to varying characteristics of the sites, e.g. location, altitude and management history (Gibb et al., 2008).

image

Figure 1.  Species accumulation curves for saproxylic parasitoids captured using window and emergence traps, separately as well as combined.

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Table 1.   Trap type anova and post hoc Tukey's HSD tests showing differences in species richness and abundances of saproxylic parasitoids between emergence and window traps. Statistically significant differences are shown in bold.
Sourced.f.MSFPTukey’s tests
  1. Only based on data from the July period, anova on ranked values was used for B. obscurator because normality could not be achieved by transformation.

  2. CC, clear-cut; F, forest (mature managed); R, reserve (old-growth) for the different stand types; for the trap types Emer, emergence trap and Win, window trap.

  3. * 0.005, ** 0.001.

Species richness
 Trap type11.1865.5420.023Win > Emer
 Stand type20.1360.6360.534 
 Site91.0564.936<0.001 
 Trap × stand20.0040.0190.982 
 Error450.214   
Total abundance
 Trap type10.4650.5900.446 
 Stand type20.6390.8110.451 
 Site93.7134.713<0.001 
 Trap × stand20.0080.0100.990 
 Error450.788   
Total idiobionts
 Trap type10.1120.2410.626 
 Stand type24.0978.8450.001CC > F**, R*
 Site92.0794.490<0.001 
 Trap × stand20.0830.1790.837 
 Error450.463   
Total koinobionts
 Trap type11.0661.4070.242 
 Stand type29.05211.948<0.001CC < F**, R*
 Site95.3437.053<0.001 
 Trap × stand20.1630.2150.807 
 Error450.758   
Bracon obscurator
 Trap type1763.36.9040.012Emer > Win
 Stand type2119110.772<0.001CC > F**, R**
 Site9106.80.9660.479 
 Error47110.6   
Ontsira antica
 Trap type14.03611.0090.002Emer > Win
 Stand type20.9902.7010.078 
 Site91.4543.9650.001 
 Trap × stand20.0080.0210.979 
 Error450.367   
Cosmophorus regius
 Trap type15.7048.2130.006Emer > Win
 Stand type215.3322.081<0.001CC < F**, R**
 Site93.0224.352<0.001 
 Trap × stand20.1260.1820.835 
 Error450.694   
Helconidea dentator
 Trap type10.0110.0130.910 
 Stand type24.7375.6190.007CC < F*
 Site91.3821.6390.133 
 Trap × stand20.4970.5900.559 
 Error450.843   
image

Figure 2.  Mean ± SE species richness and abundance of saproxylic parasitoids (total, idiobionts, koinobionts, and the four most common species) per site between different: (a) trap types and between different, (b) stand types. Bars with different letters denote statistically significant differences between stand types or trap types (Tukey test < 0.05).

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Table 2. permanovas and pairwise a posteriori comparisons between the parasitoid assemblages in different (a) trap types (only July data) and (b) stand types (all data), respectively. Statistically significant differences are shown in bold. [Correction added on 4 March 2010, after first online publication: CC ≠ F was changed to CC ≠ F, R.]
Sourced.f.MSFPPairwise tests
  1. CC, clear-cut; F, forest (mature managed); R, reserve (old-growth) for the different stand types; for the trap types Emer, emergence trap and Win, window trap.

(a) Trap type assemblages
 Trap type19133.35.60750.0026Emer ≠ Win
 Stand type2134306.52640.0002CC ≠ F, R
 Site94017.21.95220.0002 
 Trap  × stand21881.20.914160.5456 
 Trap × site91628.80.791510.8718 
 Res362057.8   
 Total59    
(b) Stand type assemblages
 Stand type26963.23.65590.0002CC ≠ F, R
 Site92365.31.24180.1500 
 Res181904.7   
 Total29    

Stand type

There were no significant differences in species richness or total abundance between stand types (anova: = 0.288 and 0.823 respectively, Fig. 2b). However, stand type had a significant impact on the abundance of different groups of saproxylic parasitoids, i.e. idiobionts (anova: = 0.002) were more abundant on clear-cuts than in mature managed forests and old-growth reserves (Tukey HSD: = 0.002 and 0.011, respectively) while koinobionts (anova: = 0.012) were found in higher densities in mature managed forests and reserves than on clear-cuts (Tukey HSD: = 0.013 and 0.048, respectively). Further, the two dominating idiobionts, O. antica and B. obscurator, were indeed more abundant on clear-cuts (anova: = 0.022 and = 0.002; Tukey HSD: = 0.020 & 0.122 and = 0.006 & 0.005, respectively). Of the most common koinobionts, C. regius was the only species significantly more abundant in forests and reserves than on clear-cut areas (anova: < 0.001; Tukey HSD: = 0.001 and 0.002, respectively). Another koinobiont, H. dentator, was marginally affected by stand type (anova: = 0.066), but were also more frequent in forests and reserves (Appendix A). No significant interactions were detected.

The species assemblages differed between clear-cuts and the other stand types (permanova: = 0.0002, Table 2, Fig. 3), but not between mature managed forests and reserves. According to SIMPER analysis (76.22% dissimilarity clear-cuts and forests; 72.41% dissimilarity clear-cuts and reserves) the main contribution to these differences were by the most common species; i.e. C. regius and H. dentator (more common in forests and reserves), B. obscurator and O. antica (more common on clear-cuts); but also by Rhimphoctona sp. 3 and Odontocolon dentipes, which also were more common on clear-cuts (Appendix A). Thus, Rhimphoctona sp. 3 did not follow the pattern of koinobionts being more common in forested habitats. Similarly, the idiobiont B. hylobii was mainly found in mature forests and reserves and not on clear-cuts as other idiobiont-species. Again, no significant interactions were detected.

image

Figure 3.  Non-metric multidimensional scaling ordination showing the species assemblages in different stand types for all the ten localities (emergence and window traps pooled).

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendices

We collected 1456 individuals of 43 species of saproxylic parasitoids in this study, compared to the 30 611 individuals of 240 species of saproxylic beetles collected in the same emergence traps as in this study (Johansson et al., 2007b). This confirms the small population sizes of saproxylic parasitoids compared to their hosts, and (because of the inevitable budget considerations) suggests that the choice of an efficient sampling method may be even more crucial when studying saproxylic parasitoids than their hosts.

To assess the assemblages of saproxylic parasitoids in different stand types, the usage of emergence traps alone could lead to underestimations of species richness as many species of the parasitoid community were not collected by these traps (Fig. 1). Although emergence traps are very suitable for detailed analyses, such as the choice of substrate (see Hilszczański et al., 2005) for the most abundant species (here C. regius, O. antica, B. obscurator and H. dentator), the use of emergence traps only may be too restrictive because they only sample species of a certain dead wood type (in this study, parasitoids connected to early successional stages of dead wood of spruce). To truly sample the entire community of saproxylic parasitoids with emergence traps alone, it would be necessary to put traps on all species of dead wood, and of all stages of decomposition. We suggest that window traps provided a better estimate of stand type associations because they caught more parasitoid species than emergence traps (Appendix A). However, one must be careful in declaring a particular habitat association for the species which were represented by only one or two individuals in the window traps, because some parasitoids might be good dispersers and ‘tourist’ species are possible in these traps. In conclusion, we suggest that the differences in the assemblages collected in window and emergence traps indicate that window traps can give a better measure of the available local species pool, but provide limited information on substrate use (see also Økland, 1996; Hyvärinen et al., 2006; Alinvi et al., 2007).

From a temporal point of view, window traps should also be used throughout the season with samples collected in short intervals to give an activity measure of saproxylic parasitoids in different habitats (see also Fraser et al., 2007). This would be complementary to the information about natural hatching periods that emergence traps provide: the greatest number of parasitoids emerged in July (Appendix B). Note however, that no koinobionts were caught in the emergence traps in June and very few were caught in September, while the two dominant idiobiont-species O. antica and B. obscurator actually had their highest recorded catches in September and June, respectively. This could be explained by the fact that idiobionts are synovigenic, which means that females do not have developed eggs after hatching. They need to eat, i.e. through supplementary feeding on flowers, honeydew or host feeding (e.g. on larval haemolymph), prior to egg-laying. This activity is time consuming, so they live considerably longer than koinobionts, which are proovigenic, having fully developed eggs after hatching (Askew & Shaw, 1986; Mayhew & Blackburn, 1999; Jervis et al., 2001). Open sunny habitats like clear-cuts provide a longer activity period, which might be suitable for the life-history strategy of idiobionts.

In addition, idiobionts have a broader host range and are thus probably more tolerant to habitat disturbances and adapted to early successional stages like clear-cuts (Hawkins, 1994). This becomes evident in the clearly differentiated assemblage compositions among stand types, which was mainly attributed to the different life-history strategies. Idiobionts, strongly dominated by O. antica and B. obscurator, were much more common in clear-cuts than in closed forests. In contrast, koinobionts showed the opposite pattern and were more common in mature managed forests and old-growth reserves, especially C. regius, which is a shade-preferring parasitoid on bark beetles (Hedqvist, 1998; Hilszczański et al., 2005; Gibb et al., 2008). Koinobionts are more specialised in their host selection, and as specialised species are more dependent on intact food chains (Komonen et al., 2000), therefore koinobionts are probably better adapted to stable habitats of later successional stages (Hilszczański et al., 2005). For example, the reserves in our study contain considerably more dead wood of larger diameters and of later decay stages, whereas the dead wood on clear-cuts mainly belong to early decay stages (Gibb et al., 2005). However, we did not detect any differences in the saproxylic parasitoids between mature managed forests and reserves, which may be because the mature managed forests in this study only have been selectively logged, but never subjected to modern clear-cutting forestry. Even though the dead wood volume in these forests is much lower than in the old-growth reserves, i.e. 23.3 and 72.6 m3 ha−1 respectively (Gibb et al., 2005), they seem to provide suitable habitats for saproxylic species (Gibb et al., 2006; Johansson et al., 2007b). Gustafsson et al. (2004) also found mature managed forests suitable for many bryophyte- and lichen-species. Thus, such forests should be of considerable conservation concern and could be of great value for preserving viable populations of species associated with old-growth forests, i.e. keeping old-growth forest reserves functionally connected (Elmqvist et al., 2004). However, the much higher amount and variety of dead wood in reserves suggests that reserves support higher populations of saproxylics than managed forests and therefore probably are important as source habitats in the landscape. Our results regarding saproxylic parasitoids and stand type effects are consistent with an earlier study based only on emergence trap data (Hilszczański et al., 2005). Thus, in this case combining emergence and window data did not change the overall patterns despite a larger sample size, but can provide more information than when using only one trapping method (see Discussion).

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendices

For assessment of the species pool in different stand types, our analysis suggests that window traps, ideally combined with emergence traps, are preferable because the efficiency of window traps gives a better measure of the local species pool – quite simply, parasitoids are difficult to sample in any numbers. Emergence traps on the other hand, are very restrictive in catching species connected to a specific substrate, but contribute more detailed information about microhabitat importance when parasitoids locate hosts. Emergence traps can also provide information about natural hatching periods, and a level of detail about parasitoid-prey associations. For even more precise parasitoid-prey relationships, debarking of logs may be a very suitable method (Stenbacka et al., unpubl. data), even though it is a destructive type of sampling.

The small population sizes of saproxylic parasitoids probably make them more vulnerable to habitat disturbances than their hosts. Both habitat degradation and variation in host populations may reduce the viability of parasitoid populations (Shaw & Hochberg, 2001), but depending on the degree of specialisation the choice of habitat or microhabitat may be of primary importance for these species, while the actual presence of a specific host may be less important (Hilszczański et al., 2005). We did not find any difference in species richness between stand types, but our results indicate that none of the individual stand types studied hold the whole community of saproxylic parasitoids. However, the lack of difference between mature managed stands and reserves in our analysis indicates that many mature managed forests still hold intact trophic chains and should be included in species conservation efforts.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendices

We are grateful to the forest companies Holmen skog, Sveaskog and SCA for providing sites and logs, and to Jan Stenlid for providing the wood fungi. We thank Åke Nordström, Eric Andersson, Johan Nilsson and Christer Zakrisson for invaluable fieldwork. Further, we thank Mark R. Shaw from Edinburgh for verification and determination of parasitoid, and anonymous reviewers for valuable comments. The study was financed by the Swedish University of Agricultural Sciences (grant to Kjell Danell and Stig Larsson), Formas, The Centre for Environmental Research (Umeå) and The Kempe Foundation (grant to Joakim Hjältén).

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendices
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Appendices

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendices
Table AppendixA..   Rank abundance of collected parasitoid species (Hymenoptera: Ichneumonoidea: Braconidae/Ichneumonidae) in different stand types and trap types. Stand type comparisons based on all data, but trap type abundances only based on July when both trapping methods were used. Species divided into different life-history strategies, i.e. idiobionts and koinobionts.
Life strategy/speciesFamilyStand typeTrap type
Clear-cutForestReserveTotalEmergenceWindowTotal
Idiobionts
 Ontsira antica (Wollaston)Brac.185717833410644150
 Bracon obscurator NeesBrac.1082211237441
 Xorides irrigator (Fabricius)Ichn.237434 3333
 Odontocolon dentipes (Gmelin)Ichn.29113122729
 Bracon hylobii RatzeburgBrac.6111128131427
 Atanycolus denigrator (Linnaeus)Brac.20 12112820
 Dolichomitus terebrans RatzeburgIchn.10282021820
 Rhyssa persuasoria (Linnaeus)Ichn.542115510
 Ischnoceros caligatus (Gravenhorst)Ichn.235103710
 Xorides ater (Gravenhorst)Ichn.44210189
 Spathius rubidus (Rossi)Brac.9  9628
 Dolichomitus tuberculatus (Geoffroy)Ichn.4228 66
 Neoxorides collaris (Gravenhorst)Ichn.1427 77
 Bracon exhilarator NeesBrac.5 16 44
 Doryctes mutillator (Thunberg)Brac.3216134
 Odontocolon spinipes (Gravenhorst)Ichn.1135325
 Coeloides abdominalis (Zetterstedt)Brac. 112 22
 Dolichomitus sericeus (Hartig)Ichn. 2 22 2
 Neoxorides varipes (Holmgren)Ichn.2  2 22
 Dolichomitus sp.3Ichn.11 2 11
 Odontocolon punctulatus (Thomson)Ichn.  22 11
 Chartobracon huggerti van AchterbergBrac.1  1 11
 Cyanopterus flavator (Fabricius)Brac.1  1 11
 Echthrus reluctator (Linnaeus)Ichn.1  11 1
 Helcostizus restaurator (Fabricius)Ichn.  11 11
 Megarhyssa emarginatoria (Thunberg)Ichn. 1 1 11
 Ontsira imperator (Haliday)Brac. 1 1 11
 Poemenia hectica (Gravenhorst)Ichn.1  1 11
 Rhyssella approximator (Fabricius)Ichn.  11 11
 Xorides alpestris (Habermehl)Ichn.  11 11
 Xorides sepulchralis (Holmgren)Ichn.1  1 11
 Idiobionts Total 423120129672194207401
Koinobionts
 Cosmophorus regius NiezabitowskiBrac.13253185451315133448
 Helconidea dentator (Fabricius)Brac.2100521547279151
 Rhimphoctona sp.1Ichn.10513192276188
 Rhimphoctona sp.3Ichn.372140162440
 Cosmophorus cembrae (Ruschka)Brac.122163030 30
 Meteorus corax (Marshall)Brac.1247 77
 Eubazus semirugosus NeesBrac. 314 44
 Rhimphoctona sp.2Ichn. 2 2112
 Coleocentrus caligatus (Gravenhorst)Ichn. 1 1 11
 Eubazus sp.Brac.1  1 11
 Meteorus rubens NeesBrac.1  1 11
 Triaspis sp.Brac.1  1 11
 Koinobionts Total 78416290784461313774
Grand total 50153641914566555201175

Appendix B. Rank abundance of parasitoid species collected using emergence traps during different trapping periods. Species divided into idiobionts and koinobionts.

Life strategy/speciesFamilyTrapping period
JuneJulySeptemberTotal
Idiobionts
 Ontsira antica (Wollaston)Brac.3106181290
 Bracon obscurator NeesBrac.7137 108
 Bracon hylobii RatzeburgBrac. 13114
 Atanycolus denigrator (Linnaeus)Brac. 12113
 Spathius rubidus (Rossi)Brac. 617
 Rhyssa persuasoria (Linnaeus)Ichn.15 6
 Odontocolon dentipes (Gmelin)Ichn.22 4
 Odontocolon spinipes (Gravenhorst)Ichn. 3 3
 Ischnoceros caligatus (Gravenhorst)Ichn. 3 3
 Doryctes mutillator (Thunberg)Brac.21 3
 Xorides ater (Gravenhorst)Ichn. 112
 Dolichomitus sericeus (Hartig)Ichn. 2 2
 Dolichomitus terebrans RatzeburgIchn. 2 2
 Bracon exhilarator NeesBrac.2  2
 Dolichomitus tuberculatus (Geoffroy)Ichn.2  2
 Xorides irrigator (Fabricius)Ichn.1  1
 Dolichomitus sp.3Ichn.  11
 Odontocolon punctulatus (Thomson)Ichn.  11
 Echthrus reluctator (Linnaeus)Ichn. 1 1
 Idiobionts Total 84194187465
Koinobionts
 Cosmophorus regius NiezabitowskiBrac. 3153318
 Helconidea dentator (Fabricius)Brac. 72375
 Rhimphoctona sp.1Ichn. 27431
 Cosmophorus cembrae (Ruschka)Brac. 30 30
 Rhimphoctona sp.3Ichn. 16 16
 Rhimphoctona sp.2Ichn. 1 1
 Koinobionts Total  46110471
Grand total 84655197936