ARTICLE IN PRESS Basic and Applied Ecology 7 (2006) 1—11
Effects of tree stand species composition on insect herbivory of silver birch in boreal forests Harri Vehvila ¨inena,, Julia Korichevab, Kai Ruohoma ¨kia, Tord Johanssonc, Sauli Valkonend a
Section of Ecology, Department of Biology, University of Turku, FIN-20014 Turku, Finland School of Biological Sciences, Royal Holloway University of London, Egham, Surrey TW20 0EX, UK c Department of Bioenergy, Swedish University of Agricultural Sciences, P.O. Box 7060, S-75007 Uppsala, Sweden d Finnish Forest Research Institute, Vantaa Research Centre, P.O. Box 18, FIN-01301 Vantaa, Finland b
Received 3 September 2004; accepted 24 May 2005
KEYWORDS Associational resistance; Associational susceptibility; Forest diversification; Herbivore community; Pest management; Species mixtures
Summary Pure forest stands are commonly believed to be more susceptible to insect herbivore attacks than mixed stands. However, the existing experimental evidence of tree species diversity effects on herbivores in forest ecosystems is scarce and contradictory. In the present study, we compared insect herbivore abundance and leaf damage on silver birch (Betula pendula) in monocultures and paired mixtures with Scots pine (Pinus sylvestris) and Norway spruce (Picea abies) in three experiments in the boreal forest zone (SW Sweden, SW and central Finland). In the Finnish experiment, total densities of insect defoliators were highest in birch monocultures and decreased with increase in the proportion of Scots pine in a stand. Densities of leaf rollers, gall mites and aphids also tended to be higher in birch monocultures than in mixed stands. At the beginning of the season the proportion of birch leaves damaged by chewing insects in the Finnish experiment was significantly lower in mixed stands containing 25% of birch and 75% of pine as compared to birch monocultures and mixtures with 50% of birch and 50% of pine. However, by the end of the season there were no significant differences in herbivore damage between the treatments. In the Swedish experiment, where herbivory monitoring was conducted at the end or at the middle of summer, neither herbivore abundance nor damage differed between birch monocultures and paired mixtures with Scots pine and Norway spruce. Our results provide only a partial support for the hypothesis that pure forest stands are more susceptible to insect herbivores and demonstrate that the benefits of mixed forests in terms of reduced herbivory are not as straightforward as commonly thought. ¨ kologie. Published by Elsevier Gmbh. All rights reserved. & 2005 Gesellschaft fu ¨r O
Corresponding author. Tel.: +358 2 3336381; fax: +358 2 3336550.
E-mail address: [email protected]
(H. Vehvila ¨inen). ¨ kologie. Published by Elsevier Gmbh. All rights reserved. 1439-1791/$ - see front matter & 2005 Gesellschaft fu ¨r O doi:10.1016/j.baae.2005.05.003
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H. Vehvila ¨inen et al.
Zusammenfassung Im Allgemeinen wird angenommen, dass reine Waldbesta ¨nde fu ¨r Angriffe von herbivoren Insekten anfa ¨lliger sind als gemischte Besta ¨nde. Die existierenden experimentellen Nachweise fu ¨r die Auswirkungen der Baumarten-Diversita ¨t auf die Herbivoren in Waldo ¨kosystem sind jedoch selten und widerspru ¨chlich. In der vorliegenden Untersuchung verglichen wir die Abundanz herbivorer Insekten und die Blattscha ¨den bei der Ha ¨nge-Birke (Betula pendula) in Monokulturen und in paarweisen Mischungen mit der Waldkiefer (Pinus sylvestris) und der Fichte (Picea abies) in drei Experimenten in der borealen Waldzone (SW-Schweden, SW- und Zentralfinnland). Im finnischen Experiment waren die Gesamtdichten der Blattscha ¨dlinge in Birkenmonokulturen am ho ¨chsten und nahmen mit dem Anteil der Waldkiefern in einem Bestand ab. Die Dichten der Blattroller, Gallmilben und –la ¨use tendierten im Gegensatz zu gemischten Besta ¨nden in Birkenmonokulturen zu ho ¨heren Werten. Zu Beginn der Saison war im finnischen Experiment der Anteil der Birkenbla ¨tter, die durch Insektenfraß bescha ¨digt wurden, in gemischten Besta ¨nden, die 25% Birke und 75% Kiefer enthielten, signifikant geringer als in Birkenmonokulturen und Mischungen von 50% Birke und 50% Kiefer. Zum Ende der Saison gab es jedoch keine signifikanten Unterschiede im Herbivorenschaden der verschiedenen Behandlungen. Im schwedischen Experiment, bei dem die Herbivorieerfassungen am Ende oder in der Mitte des Sommers durchgefu ¨hrt wurden, unterschieden sich weder die Herbivorenabundanzen noch die Scha ¨den zwischen Birkenmonokulturen und paarweisen Mischungen mit Waldkiefer oder Fichte. Unsere Ergebnisse liefern nur eine teilweise Besta ¨tigung der Hypothese, dass reine Waldbesta ¨nde fu ¨r Insektenherbivore anfa ¨lliger sind und demonstrieren, dass die Vorteile von gemischten Wa ¨ldern in Bezug auf eine reduzierte Herbivorie nicht so einfach sind wie allgemein angenommen. ¨ kologie. Published by Elsevier Gmbh. All rights reserved. & 2005 Gesellschaft fu ¨r O
Introduction The relationship between plant species diversity and herbivore abundance has long been of interest to ecologists because of its theoretical and applied importance (Andow, 1991; Elton, 1958; Pimentel, 1961). The finding that man-made monocultures are more vulnerable to pest outbreaks than natural species-rich plant communities has been used as one of the most important sources of evidence supporting the diversity–stability hypothesis, which states that the greater the diversity of a community the greater its stability (Goodman, 1975; MacArthur, 1955; McCann, 2000). To explain greater susceptibility of simple plant communities to herbivore attacks, Tahvanainen and Root (1972) suggested that plant species growing in a diverse plant community experience, in addition to the resistance of individual plant species, associational resistance to herbivores by an association with other plant species. The underlying mechanisms may be diverse and include factors such as chemical and physical interference between the plant species of the community, higher abundance and diversity of natural enemies, and lower density and nutritional quality of host plants (Finch & Collier, 2000; Hamba ¨ck & Beckerman, 2003; Meiners & Obermaier, 2004; Sperber, Nakayama, Valverde, & Neves, 2004). When the complex
pattern of natural vegetation is broken down by growing plants in monocultures, most of this associational resistance is lost. Most of the evidence of the associational resistance comes from agricultural systems where crop diversification through intercropping and other similar techniques is commonly used as a means of pest control (reviewed by Andow, 1991; Trenbath, 1993; Tonhasca & Byrne, 1994). In forest ecosystems, associational resistance has not been studied as extensively as in agricultural systems. However, a recent review of studies comparing insect herbivore densities and damage in pure and mixed forest stands by Jactel, Brockerhoff, and Duelli (2005) provides an overall support for the hypothesis that mixed stands suffer less pest damage or have lower pest populations than pure stands. Interestingly, strongest effects of stand diversity on insect pests were observed in speciespoor boreal forests where an addition or a loss of a single tree species is likely to have more dramatic effects than in more species-rich temperate and tropical forests. However, only five out of 29 studies on insect herbivore responses to forest diversification included in the review by Jactel et al. (2005) were dealing with pests of boreal forests, and none of these studies was experimental. Conclusions drawn from observational studies can be seriously flawed because the replication of
ARTICLE IN PRESS Stand type affects insect herbivory of birch observations is often problematic due to natural variability in environmental conditions (Moore, Warrington, & Whittaker, 1991; Muzika & Liebhold, 2000) and differences in herbivore and natural enemy fauna. These problems can be greatly reduced by using forest stands where tree species diversity and composition have been experimentally manipulated. The effects of stand diversity on herbivore densities and damage thus have to be tested experimentally by using different tree species in different locations and biomes before generalisations on the relative commonness of associational resistance phenomenon in forest ecosystems can be made. The studies reporting experimental manipulations of forest tree species diversity and their effects on insect herbivores are few and their results are inconsistent (Moore et al., 1991; Peacock & Herrick, 2000; Peacock, Hunter, Turner, & Brain, 2001; White & Whitham, 2000). In the present study, we compared insect herbivore abundance and leaf damage on silver birch (Betula pendula Roth) in monocultures and paired mixtures with Scots pine (Pinus sylvestris L.) and Norway spruce [Picea abies (L.) Karst.] in three experiments in the boreal forest zone (SW Finland, central Finland and SW Sweden). Silver birch usually occurs as an admixture in coniferous forests, but the number of planted pure birch stands has increased in Finland recently due to increase in prices for the birch wood (Luostarinen & Verkasalo, 2000). Since birch is a host species for a large number of insect herbivores some of which can occur at high population densities (Atkinson, 1992; Shaw, 1984), it is important to know whether birch monocultures are likely to suffer from substantial insect pest problems. Most of the studies on the effects of forest diversity on insect herbivores conducted so far have examined responses of individual pest species (Jactel et al., 2005). It is, however, the total damage to a tree caused by different pests which is of main economical and ecological importance. Therefore, in our study we examine both patterns in total leaf damage as well as in abundance of and damage by individual herbivore groups. We address the following questions: (1) How does the stand tree species composition affect insect herbivore abundance and leaf damage on birch? (2) Do herbivores respond to the stand diversification similarly in geographically distant experiments? (3) Are herbivore responses consistent temporally (between years and within the season)? (4) Does the growth form, and subsequently the apparency, of the host tree differ between different stand types?
Materials and Methods Finnish experiment The experiment was established by the Finnish Forest Research Institute in two locations approximately 229 km apart. Both locations contained the following treatments used in this study: birch monoculture (birch100), 50% birch: 50% pine (birch50–pine50) and 25% birch: 75% pine (birch25– pine75) mixtures planted at the same time. Treatments were substitutive, i.e. the total density of trees is similar in all diversity classes. ¨hta A ¨ri (621N, 241E). The experiment was established in 1983 in a clear-cut area. There are three blocks each containing seven plots (0.16–0.36 ha each) randomly allocated to the treatments. There are six replicates of birch50–pine50 treatment and three replicates of all other treatments. Planting interval of trees is 2.2 m. In addition to the treatments used in this study, the locality also contains pine monocultures and 50:50 and 75:25 mixtures, in which birch has been removed 7–8 years after planting. Jokioinen (601N, 231E). The experiment was established in 1982. The clear-cut area (approximately 3.3 ha) was divided into 12 plots (0.21– 0.38 ha each), which were randomly allocated to the treatments. Each treatment is replicated twice. The planting interval is 2.2 m. In addition to the treatments used in this study, the locality also contains pine monocultures and 50:50 and 75:25 mixtures in which birch has been planted 7 years later than pine (1989).
Swedish experiment ¨ stad (571N, 161E). The experiment was estabO lished by the Swedish University of Agricultural Sciences in 1989 on the abandoned farmland near ¨ stad, SW Sweden. There are four blocks each O containing 10 plots (0.16 ha each) randomly allocated to monocultures and paired mixtures of silver birch, Scots pine and Norway spruce planted simultaneously or at different time intervals. For the present study, we used only birch monocultures and simultaneously planted birch–pine and birch–spruce mixtures. There were four replicate plots of each treatment used (one in each block). Each plot contains 729 (27 27) trees planted at 1.5 m intervals. In mixed stands, rows planted with birch alternate with rows in which every second tree is either pine or spruce resulting in 560 (77%) birch and 169 (23%) spruce or pine trees per plot. The plantations are surrounded by an electric fence to
ARTICLE IN PRESS 4 prevent browsing by moose and roe deer. The experimental plots were thinned in spring 2002. In the case of birch monocultures and birch–spruce mixtures, the proportion of different species remained the same. However, in the birch–pine mixture all the pines were removed and the stands were thus converted to birch monoculture.
Herbivore densities and damage Monitoring of herbivore densities and foliar damage on birch trees in pure and mixed stands was conducted in 1999 and 2002. In 1999, all the experimental localities were visited only once ¨hta ¨ stad: (A ¨ri: 12–14 July, Jokioinen: 16 July, O 10–12 August). Ten birch trees were haphazardly selected within the central area of each plot and ¨hta four (A ¨ri) or three (all other experiments) branches per tree were inspected for the presence of herbivores and signs of feeding damage. On average 30 leaves per branch and 100–120 leaves per tree were examined. Numbers of the leaffeeding insects present (aphids, leafhoppers, psyllids, leaf rollers, lepidopteran and sawfly larvae, and weevils) were recorded in situ. Leaves with signs of feeding damage were collected and examined further in the lab. Five categories of damage to birch leaves were distinguished: (1) chewing; (2) sceletonising; (3) mining; (4) whitish erineum galls caused by the gall mite Acalitus rudis (Canestrini); (5) cephaloneon galls caused by the gall mite Aceria leionotus (Nalepa). The number of A. leionotus galls per leaf and the number of leaves with mines in the sample were counted directly whereas the intensity of damage types (1), (2) and (4) was scored as follows: (1) less than 25% of the leaf area damaged; (2) 25–50% of the leaf area damaged; (3) 51–75% of leaf area damaged; (4) more than 75% of leaf area damaged. Damage by chewers and sceletonisers was combined in the analyses and they were no longer classified separately in 2002. In 2002, herbivory monitoring in the Finnish experiment was conducted twice: once in early ¨hta season (A ¨ri: 17–19 June, Jokioinen: 6–7 June) ¨hta and once in late season (A ¨ri: 13–15 August, Jokioinen: 8–9 August). In the early season, monitored trees were marked and the same trees were used in the late season monitoring. In the Swedish experiment, herbivory monitoring was conducted only once in mid-season (8–13 July). The monitoring was conducted as in 1999, except that due to the increased tree height, insects present on branches could not be recorded in situ. Instead, two branches per tree with ca. 100 leaves
H. Vehvila ¨inen et al. each were cut down and the damage by chewers and numbers of sessile herbivores (gall mites, rollers and miners) was recorded. In addition, the damage by chewers and the presence of sessile herbivores in early season was classified only as number of leaves damaged because almost all leaves observed belonged to the first damage class (less than 25% of leaf area damaged).
Tree growth measurements Heights and trunk diameters of experimental trees in the Finnish experiment were measured in 2003. The measurements were taken from 10 trees per species per plot; with few exceptions the measured trees were the same as the ones that were used for herbivore monitoring in 2002. Heights were measured with optical hypsometer. Diameters were measured at breast height. The ratio between tree height and trunk diameter was calculated to characterise tree shape.
Statistical analyses All statistical analyses were performed using the SAS 8.2 statistical package (SAS, 1999). Herbivore abundance and damage in the Swedish experiment were analysed by repeated-measures ANOVA model with stand type as the between-subject effect, year as the within-subject effect and plot nested within stand type block interaction as the repeated subject. The Finnish experiment was also analysed using repeated-measures ANOVA with stand type as the between-subject effect, location and year or season (in 2002) as the within-subject effect, and plot nested within location stand type interaction as the repeated subject. In terms of temperature sums, the period of herbivory monitoring in the Finnish experiment in 1999 falls between the two monitoring periods in 2002 and may thus be considered as a mid-summer observation. To be able to analyse both years together in the same model in the Finnish experiment, we therefore used arithmetic average of the two observation periods in 2002 as the dependent variable. The tree growth measurements and the in situ observations of different herbivores during 1999 monitoring were analysed by two-way mixed ANOVA using location and stand type as fixed effects and plot nested within location stand type interaction as random effect in the Finnish experiment. In the Swedish experiment, stand type was the only fixed effect and plot nested within block stand type interaction was the random effect.
ARTICLE IN PRESS
The response variables studied in the repeatedmeasures models were the proportion of leaves with signs of feeding damage and the proportion of leaves with sessile herbivores (miners, rollers, A. rudis and A. leionotus) present. The response variables in the two-way ANOVAs for the in situ observations of herbivores in 1999 were the numbers of lepidopteran larvae, sawfly larvae, weevil adults, defoliators (lepidopteran and sawfly larvae and weevils combined), aphids, leafhoppers, psyllids and Psocoptera (all counted as the number of individuals per leaf). The response variables in the two-way ANOVA for the tree growth form were tree height, trunk diameter at breast height and the height/diameter ratio. In all models, the degrees of freedom were assessed using Satterwaithe’s method (Littell, Milliken, Stroup, & Wolfinger, 1996) and covariances were modelled as unstructured. The response variables were averaged over plots. Natural logarithm transformation was applied to the proportion of leaves with signs of feeding damage in the Finnish experiments and to the proportion of leaves with A. rudis present in order to obtain normal distribution of residuals. P values of the multiple comparisons between least-squares means of the treatments were Tukey–Kramer adjusted. Least-squares means are presented in the figures and tables. Power tests were performed on modelbased values using finv and probf-functions (SAS, 1999).
5 Percentage of leaves with defoliators present
Stand type affects insect herbivory of birch 1.4 1.2
b 0.8 0.6 0.4 0.2 0.0 birch100
birch50-pine50 birch25-pine75 Stand type
Fig. 1. Percentage of silver birch leaves with insect defoliators (lepidopteran larvae+sawfly larvae+weevils) present in different stand types in the Finnish experiment observed in situ in 1999. Least-squares means and 95% confidence limits are shown. Different letters denote significant differences between stand types.
p ¼ 0.013, Fig. 2), where they were more abundant in monocultures than in mixed stands, but not in Jokioinen (F2,3 ¼ 1.84, p ¼ 0.301, Fig. 2). Contrary to defoliators and aphids, abundance of sessile herbivores (miners, rollers and gall mites) was estimated both in 1999 and in 2002 and was thus analysed by the repeated-measurements models. The only sessile herbivores that tended to show responses to stand type were the gall mite A. rudis (p ¼ 0.047) and leaf rollers (p ¼ 0.098), which were more abundant in monocultures than in mixed stands (Figs. 3 and 4) (pX0.241 for other sessile herbivores).
Results ¨hta Finnish experiment (A ¨ri & Jokioinen) Herbivore abundance In 1999, abundance of insect defoliators as a group (lepidopteran larvae+sawfly larvae+weevils) differed significantly between stand types (F2,12 ¼ 4.84, p ¼ 0.029) and was highest in birch monocultures and lowest in mixed stands with 25% birch and 75% Scots pine (Fig. 1). Location effect was also significant (F1,12 ¼ 80.61, po0.001), but the location stand type interaction was not (F2,12 ¼ 0.05, p ¼ 0.956). When analysed separately, abundances of individual groups of defoliators were not significantly affected by stand type. Among other leaf-feeding herbivores, the number of aphids in 1999 showed a significant location stand type interaction (F2,12 ¼ 6.41, p ¼ 0.013), but the main effect of stand type was non-significant (F2,12 ¼ 1.83, p ¼ 0.202). Stand type affected ¨hta the number of aphids in A ¨ri (F2,9 ¼ 7.32,
Leaf damage by herbivores When data on leaf damage for both years were included in the same model, neither stand type nor its interactions with other variables reached statistical significance (pX0.150 in all tests). However, in the combined analysis of the two sampling periods in 2002, both stand type and stand type season interaction were significant (Table 1, Fig. 5). In the early season, birch monocultures and birch50–pine50 mixtures were more severely damaged than birch25–pine75 mixtures, whereas later in the season there were no significant differences in leaf damage between the treatments (Fig. 5). Tree growth form Stand type affected the height/diameter ratio of silver birches (stand type: F2,12 ¼ 4.01, p ¼ 0.046, location stand type interaction: F2,12 ¼ 3.12, p ¼ 0.081). For birches, the height/diameter ratio was significantly lower in birch25–pine75 stands than in more birch-dominated stand types (Table 2).
ARTICLE IN PRESS 6
H. Vehvila ¨inen et al. 8 Ähtäri
6 Percentage of leaves with aphids present
ab b 4 2 0 10 Jokioinen a
4 2 0 birch100
Fig. 2. Percentage of silver birch leaves with aphids present in different stand types in the Finnish experiment observed in situ in 1999. Least-squares means and 95% confidence limits are shown. Different letters denote significant differences between stand types.
7 Acalitus rudis
Percentage of leaves with herbivore present
3 2 1 0 0.7
birch50-pine50 Stand type
0.4 0.3 0.2 0.1 0.0 birch100
Fig. 3. Percentage of silver birch leaves with the gall mite Acalitus rudis and leaf rollers present in different stand types in the Finnish experiment in 1999 and 2002. Least-squares means and 95% confidence limits (backtransformed for Acalitus rudis) are shown. Different letters denote significant differences between stand types.
ARTICLE IN PRESS Stand type affects insect herbivory of birch
16 Percentage of leaves with Acalitus rudis present
12 10 8 6 4 2 0 14 12
10 8 6 4 2 0 birch100
birch50-pine50 Stand type
Fig. 4. Percentage of silver birch leaves with the gall mite Acalitus rudis present in different stand types in the Finnish experiment in early and late season 2002. p-values for stand type: Early season p ¼ 0.340, Late season p ¼ 0.074. Stand type location interaction was non-significant in both early and late season. Least-squares means and 95% confidence limits are shown.
Results of repeated ANOVA for leaf damage in Finnish experiment between early and late season in 2002
Location Stand type Stand type location Season Season location Stand type season Stand type location season
1 2 2 1 1 2 2
260.66 5.09 0.06 1780.47 399.36 10.85 0.05
o 0.001 0.025 0.941 o 0.001 o 0.001 0.002 0.947
Denominator DF ¼ 12 in all cases.
Silver birches also tended to be taller in birch50– pine50 mixture than in other stand types (F2,12 ¼ 3.58, p ¼ 0.061, location stand F2,12 ¼ 3.20, p ¼ 0.077, Table 2). Stand type did not have any significant effect on diameter of silver birches (pX0.179). Tree height, trunk diameter and the height/diameter ratio of pines did not differ between the stand types (pX0.111 in all tests).
¨ stad) Swedish experiment (O Herbivore abundance Stand type affected neither insect herbivore abundance observed in situ in 1999 (for Psocoptera p ¼ 0.085, other herbivores pX0.457) nor abun-
dance of sessile herbivores recorded in both 1999 and 2002 (for rollers p ¼ 0.074, A. leionotus p ¼ 0.092, other sessile herbivores pX0.375). Leaf damage by herbivores Stand type had no significant effect on leaf damage (F2,9 ¼ 0.25, p ¼ 0.787, Fig. 6). Damage levels varied between years (F1,9 ¼ 384.43, po0.001), but stand type year interaction was non-significant (F2,9 ¼ 3.20, p ¼ 0.089). Leaf damage in birch100 and birch77–spruce23 treatments was more similar to each other in both years, whereas birch77–pine23 treatment was the most damaged in 1999 and the least damaged in 2002 (Fig. 6), which may be the result of thinning in spring 2002.
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H. Vehvila ¨inen et al. 16
Early season a a
Percentage of leaves damaged
Late season a
Fig. 5. Silver birch leaf damage in different stand types in the Finnish experiment in early and late season 2002. Backtransformed least-square means and 95% confidence limits are shown. Different letters denote significant differences between stand types. Power of tests: Early season—94.7%, Late season—90.2%. Table 2. Silver birch height, trunk diameter at breast height (DBH) and height/DBH-ratio in different stand types in the Finnish experiment. Values are least-square means measured in metres and their 95% confidence limits Stand type
Birch100 Birch50–pine50 Birch25–pine75
12.6 13.2 12.3
12.0–13.1 a 12.7–13.7 a 11.8–12.9 a
0.12 0.13 0.13
0.12–0.14 a 0.12–0.13 a 0.12–0.14 a
107.8 104.3 98.0
102.4–113.1 a 99.5–109.1 ab 92.6–103.4 b
Different letters denote significant differences in between stand types.
Discussion The results of our study provide only partial support for the hypothesis that mixed forest stands are less susceptible to herbivore damage than pure stands. Results from the Finnish experiment demonstrate that birch trees growing in mixtures with
Scots pine support lower herbivore densities and suffer less damage than birches in pure stands. However, the effect of stand diversity on herbivore damage was significant only in early summer and only when the proportion of birch in a stand was sufficiently low (25%). The leaf damage in stands where birch has been planted in equal proportion
ARTICLE IN PRESS Stand type affects insect herbivory of birch 35
30 25 Percentage of leaves damaged
20 15 10 5 110 2002 100 90 80 70 60 50 40 birch100
Fig. 6. Silver birch leaf damage in different stand types in the Swedish experiment in 1999 and 2002. Least-square means and 95% confidence limits are shown. Power of tests: 1999—93.8%, 2002—84.3%.
to pine was similar to the damage in the birch monocultures. In the Swedish experiment, herbivore abundance and leaf damage were similar in birch monocultures and in birch mixtures with Scots pine and Norway spruce. Moreover, herbivore abundance and leaf damage on birch did not increase when birch–pine mixtures were converted to birch monocultures as a result of thinning. Differences in tree diversity effects on herbivore abundance and damage between the Finnish and the Swedish experiments could be due to differences in the experimental design since the proportion of conifers in mixed stands in the Swedish experiment (23%) was lower than in the Finnish experiment (50% or 75%) and thus might not have been enough to influence birch insect herbivores. In addition, the stands in the Swedish experiment are 6–7 years younger than in the Finnish experiment, and the treatment effects may not have manifested themselves yet. Another explanation for the lack of the diversity effects on herbivory in the Swedish experiment could be the timing of observations, which may have been too late on both occasions to reveal early season herbivory, which seems to be more affected than late season herbivory by the tree species diversity of stands. Finally, greater abundance of broadleaves in southern Sweden as compared to central and southern Finland may
result in more abundant and diverse herbivore fauna in the former area and a larger proportion of herbivores being polyphagous, and, thus, less susceptible to changes in stand diversity (Levins & MacArthur, 1969; Jactel et al., 2005). Evidence of associational resistance of birch in mixed stands was found only in the Finnish experiment in early summer in birch–pine mixtures with 25% of birch. The most important mechanism of the associational resistance in insects is believed to be host-finding interference via physical, visual or olfactory masking of host plants by associated plant species (Finch & Collier, 2000; Hamba ¨ck & Beckerman, 2003). Apparently, the host-finding interference experienced by birch-feeding insects is strongest in the early season when the birch leaves have not fully opened and are least apparent and when the proportion of birch in a stand is sufficiently low. The birches growing in mixtures with 75% pine also differed in shape (had lower height/diameter ratio) from other stand types, which may have reduced their apparency or suitability to herbivores (Mo, Tanton & Bygrave, 1997). In addition, as the season progresses, the dispersion of herbivores already present may decrease the observed effects of diversity. Indeed, the more sessile and dispersion-limited herbivores such as gall mites did not show differentiating
ARTICLE IN PRESS 10 trend within season. In the case of A. rudis the effects of treatments did in fact seem to increase towards late season. The lower early season damage in birches associated with pines may be of great importance to trees. Young leaves are of higher value for the plant than old leaves, and, therefore, damage caused in the early season may have more detrimental consequences for a tree than at the end of the summer when leaves have matured and are of less importance for growth and photosynthesis (Harper, 1989; Haukioja & Honkanen, 1996; Meyer & Montgomery, 1987). The early season damage has also been shown to affect negatively subsequent herbivory of trees (Awmack & Leather, 2002; Neuvonen, Hanhima ¨ki, Suomela, & Haukioja, 1988; Riihima ¨ki, Kaitaniemi, & Ruohoma ¨ki, 2003). Indeed, in our experiments the stand types that experienced highest early season damage did have equal damage as the other stand types at the late season. These observations highlight the importance of studying the total herbivore fauna when determining the effects of tree species mixtures. Taken together, the results of our study suggest that while responses of individual types of birch herbivores to tree species diversity may differ between the sites and within season, pure silver birch stands are unlikely to suffer higher total insect herbivory than mixed birch–pine or birch–spruce stands. One limitation of our study, however, is a relatively small size of experimental plots which makes it difficult to extrapolate the results obtained from our experiments to the scale of stands used in practical forestry (several hectares). A recent meta-analysis by Bommarco and Banks (2003) demonstrated that in agricultural experiments the magnitude of crop diversity effects on herbivores and predators strongly depended on the plot size. Diversification experiments performed in small plots yielded a large negative effect on herbivores whereas the largest plots exhibited a negligible effect. Bommarco and Banks (2003) speculated that effects of crop diversification are enhanced in small plots where insects were able to move among plots and aggregate in monocultures that provide a more concentrated resource (see also Bergelson & Kareiva, 1987; Meiners & Obermaier 2004). If the same is true for forest diversification experiments, using larger plots would result in even smaller effects on insect herbivores than those described in the present study. To summarise, our results demonstrate that the benefits of mixed forests in terms of total insect herbivory are not as straightforward as in the case
H. Vehvila ¨inen et al. of individual insect pests (reviewed by Jactel et al., 2005). Effects of stand diversity on total insect herbivore densities and damage vary both spatially and temporally even within narrow geographical scale and for the same tree species combinations, which may complicate the use of forest diversification as an effective strategy for pest control in boreal forests. Before making suggestions and management plans for mixed boreal forests, more experimental evidence is needed on the effects of different tree species and their interactions on herbivores. Studies that would at the same time measure total herbivory and explore the behaviour of herbivores in a large-scale experimental set-up should be especially encouraged.
Acknowledgements We thank Samuli Helle, Henna Pieka ¨inen and Lassi Suominen for assistance in the field and the ¨ stad field station of the Swedish staff of the O University of Agricultural Sciences for their hospitality. Seppo Neuvonen provided constructive comments on the manuscript. The study was financially supported by the Academy of Finland (project 76735) and the Finnish Society of Forest Science (grant to HV).
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