Outbreaking herbivore escapes parasitoid by attaining only a small body size

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1 Outbreaking herbivore escapes parasitoid by attaining only a small body size JOHAN A. STENBERG Swedish University of Agricultural Sciences, Department of Plant Protection Biology, P.O. Box 102, SE Alnarp, Sweden Citation: Stenberg, J. A Outbreaking herbivore escapes parasitoid by attaining only a small body size. Ecosphere 6(2):21. Abstract. The reason why parasitoids are often unable to control insect herbivores during outbreak years has remained unclear to modern ecologists. Here I show that the blue willow beetle (Phratora vulgatissima) can escape parasitoids (Perilitus brevicollis) by reaching only a small body size during the increased competition which coincides with outbreaks. Different phases of outbreaks were simulated by allowing leaf-beetle larvae to develop at different densities on willow. The denser the herbivore populations, the smaller body sizes they attained. In the field too, herbivore body size decreased when the level of defoliation increased. The parasitoids were clearly limited by herbivore body size, exhibiting reduced survival in parallel with decreasing herbivore size, with none of them surviving in beetles from larvae reared at the highest density. The results demonstrate how bottom-up control of the herbivore becomes more important as outbreaks intensify, while top-down control gradually becomes less important and collapses during the outbreak peak. Because the mechanism limiting P. brevicollis parasitoids involves herbivore body size, which is reduced at high densities, I anticipate that these parasitoids are unable to terminate herbivore outbreaks. Key words: biocontrol; conservation biological control; herbivory; integrated pest management; IPM; Perilitus brevicollis; Phratora vulgatissima; population cycles; population dynamics; Salix cinerea; Salix viminalis; trophic interaction. Received 10 October 2014; revised 2 December 2014; accepted 5 December 2014; final version received 1 January 2015; published 10 February Corresponding Editor: D. P. C. Peters. Copyright: Ó 2015 Stenberg. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. johan.stenberg@slu.se INTRODUCTION Parasitoids are used as biocontrol agents against pest insects in many forest and agroecosystems. This practice builds on the idea that parasitoids are important natural enemies of herbivores, and really can exert top-down control over herbivore populations (Hassell and Waage 1984, Murdoch et al. 1995, Stenberg et al. 2007). Nevertheless, although this approach to control normally works well (Murdoch et al. 1995), there are sometimes outbreaks of herbivores with devastating effects on their host plants (Bylund 1995). Long-term field data on the population dynamics of parasitoids and herbivores actually suggest that some parasitoid populations become marginalized during herbivore outbreaks, and contribute little to arresting herbivore population growth during these critical events (Parry et al. 2003, Schott et al. 2010). Thus, parasitoids are often not significant factors in terminating herbivore outbreaks (Satake et al. 2004, Hagen et al. 2010). In fact, parasitism often does not increase until later when the outbreak has already peaked and the situation is stabilizing (Bylund 1995, Tanhuanpää et al. 2002, Turchin et al. 2003). Consequently, the release of parasitoids in agroecosystems is often only recommended as long as the target herbivore has not reached critical densities. The absence of positive densityv 1 February 2015 v Volume 6(2) v Article 21

2 dependent parasitism, and the presence of inverse density-dependence, seems to be especially apparent in coleopteran herbivores (Stiling 1987, Rand 2013). Bottom-up factors, like resource limitation or induced plant defenses, are increasingly considered to be more significant than parasitoids for arresting population growth and reducing herbivore numbers when these have reached outbreak levels (Kapari et al. 2006). In cropping systems, this means that outbreaks are brought to an end only at the cost of reduced yield or the use of insecticides. Plant-herbivore-parasitoid dynamics have been surprisingly resistant to explanation, and the literature provides no definitive conclusion as to which mechanism is most significant. Hyperparasitoids and intraguild predation are factors that, in some systems, can restrict the effectiveness of parasitoids especially in agricultural landscapes with low structural complexity (Mackauer and Volkl 1993, Sullivan and Volkl 1999, Jonsson et al. 2012, Poelman et al. 2013). For example, in a well-studied system based on Brassica plants, Poelman, Harvey, and colleagues have shown that field hyperparasitism rates of a common primary parasitoid (Cotesia glomerata) can reach 90% (e.g., Poelman et al. 2013). Previous studies also have tested whether bottom-up food limitation of herbivores affects parasitoids by weakening herbivore immune responses (Myers et al. 2011). Little evidence, however, has been found for this hypothesis. Finally, several studies have tested whether plant quality, including induced plant defenses which increase with increasing herbivore density, have negative effects on parasitoids (Haukioja 2005, Soler et al. 2005, Kapari et al. 2006, Stenberg 2012). Here I introduce a new hypothesis, namely that insect herbivores attain smaller sizes during outbreaks than otherwise, and that parasitoids, which are restricted to the limited resources within their herbivore hosts (Harvey et al. 1995, Harvey et al. 2005, Pennacchio and Strand 2006, Stenberg and Hambäck 2010, Stenberg 2012), fail to develop when their hosts are small. I test the hypothesis in a system based on willows (Salix), which is widely used as a bioenergy crop in European short rotation coppices. Outbreaks of the detrimental Blue willow beetle (Phratora vulgatissima) are often reported to occur both in coppices and in natural populations (Dalin et al. 2009). Both natural enemies and intraspecific competition play important roles in the population growth of the herbivore (Björkman et al. 2003), but it is still unclear how important these two factors are during the different phases of herbivore outbreaks. The beetle is gregarious, often reaching high densities on individual host plants, which during outbreaks are completely defoliated, while neighboring host plants are ignored and remain intact ( personal observation). One of the most important natural enemies of the beetle is the braconid solitary parasitoid Perilitus brevicollis (Baffoe et al. 2012, Stenberg 2012), which in turn is not known to host hyperparasitoids. In order to test the hypothesis, I measured beetle body size in 16 different wild populations with varying levels of outbreak intensity. I also reared beetle larvae in a controlled laboratory environment at eight different density classes (from no competition, representing normal years, to very high competition, representing outbreak peaks), and parasitized the emerging adults individually. Both field and laboratory studies showed that the beetles attain a smaller body size in parallel with the decreasing food availability during outbreaks. The parasitoids, which are not able to utilize small beetles (Stenberg 2012), showed decreasing survival in parallel with increasing beetle density, and the population collapsed at the highest density classes. These results suggest that the herbivore is able to escape parasitoids when outbreaks intensify and provide a mechanistic explanation as to why parasitoids are sometimes unable to bring herbivore outbreaks to an end. METHODS Study species Two Salix (Salicaceae) species were used for this study: S. viminalis L. and S. cinerea L. The former is fast-growing, but susceptible to Phratora vulgatissima (Stenberg et al. 2010, Lehrman et al. 2012), and is commonly used in short rotation willow coppices in Sweden. It was introduced to Sweden in the 18th century and has become naturalized. The latter (S. cinerea) is native and is the most common wild host plant for the Blue willow beetle, Phratora vulgatissima (L.) (Coleoptera: Chrysomelidae). S. cinerea has, in contrast to S. viminalis, an induced trichome-based defense v 2 February 2015 v Volume 6(2) v Article 21

3 against the beetle (Dalin and Björkman 2003, Dalin et al. 2004, Björkman et al. 2008). The beetle is restricted to the genus Salix; there are frequent reports of it completely defoliating coppices, as well as wild Salix plants. P. vulgatissima is gregarious and univoltine in the study area (Dalin 2011). It overwinters as an adult, and in Uppsala it normally emerges in late April when it feeds on the leaves of Salix. Even though the adult beetles can cause substantial damage to the plants, the greatest defoliation is caused by the larvae. Egg clutches (normally consisting of 1 20 eggs) are laid on Salix leaves in May, and the emerging larvae defoliate the plants in May and June. Both larvae and adults feed gregariously on the leaves. As indicated previously, the defoliation can be very intense during outbreak years, and in such situations the larvae experience extreme intraspecific competition through depletion of resources (Dalin et al. 2009). The body size of the adult beetle is plastic and is determined by larval development. Small beetles are fecund (J. A. Stenberg et al., unpublished data), but may potentially suffer from reduced winter survival (not tested). The larvae pupate in the ground, and the emerging beetles feed on Salix leaves for a few weeks before they move to their overwintering sites outside the coppices. Perilitus brevicollis Haliday 1835 (Hymenoptera: Braconidae) is a solitary endoparasitoid that attacks adult P. vulgatissima beetles. It is imagobiont, meaning that it parasitizes the adult stage of the beetles. This parasitoid has a wide geographical distribution, occurring at least from Spain in the south to Scandinavia in the north. In Central Europe it has occasionally been reported to parasitize a few closely related beetle species in addition to P. vulgatissima, but in Sweden it is restricted to P. vulgatissima. Two other chrysomelids (Galerucella lineola and Lochmea capreae) of similar size to P. vulgatissima occur on Salix but they have never been found parasitized. The parasitoid overwinters inside the living adult host, and the parasitoid larva emerges 1 2 weeks after the beetle starts to feed in the spring. The emerging parasitoid larva immediately spins a cocoon in which it pupates. The adult parasitoid emerges from the cocoon after about 1 2 weeks and starts to parasitize new beetles. It is currently not known whether the parasitoid can produce two generations per summer in the study area. Parasitism levels in the field are typically around 15 40% in Uppsala during normal (non-outbreak) conditions, and it occurs in all P. vulgatissima populations in the study area (pers. obs.). I only know of one other parasitoid that attacks P. vulgatissima in the area, namely Anthomyiopsis nigrisquamata (Diptera: Tachinidae), which is very rare (;1% parasitism). Hyperparasitism has not been observed in the study area ( personal observation). In order to obtain beetles and parasitoids for this study, I collected overwintering P. vulgatissima beetles from several populations around Uppsala, Sweden. The overwintering parasitoid generation is present within adult beetles. The beetles and the emerging parasitoids were reared in plastic containers in climate chambers at 198C, 80% RH, with a 16:8 light regime. Salix plants were reared from winter cuttings in a greenhouse at 208C, with a 16:8 light regime. Experimental setup In order to test for the effect of herbivore larval crowding on intraspecific competition and parasitoid survival, I established different densities of neonate herbivore larvae in plastic containers (30 ml, mm cylinders, perforated lid). Group sizes of 1, 2, 3, 5, 7, 9, 11, and 15 larvae were used. Forty replicates (containers) were established for group sizes 1 3, and twenty replicates for group sizes Thus, in total, 1180 herbivore larvae were reared. Extra replicates were established for the small group sizes because random mortality can wipe out such groups completely, and I wanted adult beetles to emerge from at least twenty containers per group size. One Salix viminalis leaf was inserted into each container every third day, so that small larval groups would have an abundance of food at all times, while large groups would quickly consume the leaf, and suffer starvation. The leaves used were detached from the middle part of the host plants, and varied little in size. The larvae were checked every day and the larval development time, survival, and pupal weight were measured for each individual larva when it had reached the pupal stage. A Mettler Toledo MX5 microbalance with a precision of 1 lg was used for all weight measurements. One pupa from each container v 3 February 2015 v Volume 6(2) v Article 21

4 was randomly selected and placed individually in a plastic container until the adult emerged. The beetles were parasitized by a randomly chosen parasitoid as soon as they reach adulthood (sensu Stenberg 2012). They were placed in individual plastic jars to be parasitized, and were watched continuously until parasitization took place to ensure that every beetle really was parasitized. Parasitized beetles were kept individually in the plastic containers and fed one Salix leaf every second day to ensure that they never experienced food shortage during parasitoid development. The reason for giving all parasitized beetles a surplus of food was to make sure that any effect on parasitoid survival was the result of herbivore density during the beetle s larval development (i.e., before parasitization). The parasitized beetles were kept in climate chambers at 198C, 80% RH, with a 16:8 light regime. All parasitized beetles were examined every day and the parasitoids larval development time, cocoon survival, as well as successful parasitism (number of adult parasitoids divided by the number of parasitized beetles), were calculated for each herbivore larval density class. Parasitoid cocoon size was not measured in this experiment, but has previously been shown to be related to beetle size (Stenberg 2012). Field observations of body sizes during outbreaks A field survey was undertaken during the last week in July, 2013 in order to investigate P. vulgatissima body sizes on plants in different outbreak phases in the wild. The timing of the survey was chosen to coincide with adult beetle emergence after pupation in the field. The young adult beetles found at this time have not yet been parasitized. The distribution of beetle body sizes is thus mainly due to bottom-up effects of food availability, and not due to any possible selection by parasitoids. Because higher beetle densities were found on Salix cinerea than S. viminalis in the wild, the former host species was chosen for the field study. Sixteen wild S. cinerea plants located in Uppsala ( N, E), North of Stockholm, Sweden, were included in the survey. The minimum distance between the plants was at least two kilometers. The level of defoliation (%) was estimated by eye for each plant. This is possible as the skeletonized leaves remain on the plant for the whole summer. All beetle individuals located below a height of 3 m were collected and weighed using a Mettler Toledo MX5 microbalance with a precision of 1 lg. Statistical analysis Controlled laboratory experiment. First, mean values for the herbivore larval development time and pupal weight for each individual group (container) were calculated. These mean values were used in one-way ANOVAs to evaluate the importance of herbivore larval density class on herbivore larval development time and pupal weight. In addition, linear regression analyses were performed to evaluate the relationship between density and larval development time or pupal weight. The survival rate (number of herbivore larvae that reached the pupal stage divided by the original number of beetles in the container) was also calculated for each individual group (container) and a linear regression analysis was performed to evaluate whether the survival rate was related to density for group sizes The smallest group sizes (1 2) were not included in the latter linear regression because they obviously fell outside the seemingly linear part of the range. Finally, the effect of herbivore density on successful parasitism, cocoon survival, and parasitoid development time was evaluated using linear regression. The analysis of parasitoid development time was only undertaken for a proportion of the data (n ¼ 48) as some data points were lost. The statistical software package R was used when analyzing the laboratory experiment. Field study. A generalized additive model (GAM) (Wood 2011) was used to test whether the beetles mean body size was reduced with increased defoliation. The R package mgcv in R was used for the GAM analysis. RESULTS Controlled laboratory experiment Herbivore larval density class had a highly significant effect on larval development time (ANOVA: df ¼ 7, MS ¼ 86.69, F ¼ 21.27, P, 0.001), pupal weight, (ANOVA: df ¼ 7, MS ¼ 36.27, F ¼ 40.40, P, 0.001; Fig. 1) and survival (ANOVA: df ¼ 7, MS ¼ 0.58, F ¼ 4.97, P, 0.001) v 4 February 2015 v Volume 6(2) v Article 21

5 Fig. 1. Effects of larval densities of the blue willow beetle, Phratora vulgatissima, on its pupal weight and the survival of imagobiont Perilitus brevicollis parasitoids (from egg to cocoon and adult, respectively). Each data point in the top panel represents a mean value, and in the bottom panel, a fraction (number of surviving cocoons, and adult parasitoids, respectively, divided by the total number of cocoons and adults), derived from all the herbivores in a group with a certain herbivore density (1 15 herbivore larvae per group). In the top panel, n, 40 for group sizes 1 3, and n, 20 for group sizes In the lower panel, n ¼ 1 per group size. Note that many data points overlap. of the herbivore Phratora vulgatissima (Fig. 1). Larval development time increased linearly (Fig. 2a), and pupal weight decreased linearly (Fig. 1) with increasing larval densities. Larval survival decreased linearly with increasing larval densities (Fig. 2). Although, statistically, the relationship between density and body size is linear, the decline in mean body size seems to be reduced at the very highest herbivore larval density (Fig. 1). This is probably an effect of the high larval mortality, which eventually reduced larval density as well as competition in the groups which, v 5 February 2015 v Volume 6(2) v Article 21

6 Fig. 2. Effects of larval densities of the blue willow beetle, Phratora vulgatissima, on (a), larval development time (from egg hatching to pupa), and (b), larval survival. Each data point in (a) represents a mean value, and in (b), a fraction (number of surviving larvae divided by the total number of larvae), derived from all the larvae in a group with a certain herbivore density (1 15 larvae per group). For group sizes 1 3, n, 40 and n, 20 for group sizes Note that many data points overlap. The linear trend line in (b) covers group sizes 3 15 as larval survival peaked at a group size of 3. initially, were most crowded. As is normal within the genus Perilitus (Berkvens et al. 2010, Stenberg 2012), the parasitoid larvae experienced a relatively high mortality. Successful parasitism varied between 0 (no parasitoids survived to adulthood) and 0.25 (one in four of the parasitoids survived to adulthood) (Fig. 1). Parasitoid survival decreased in parallel with increasing herbivore larval density. The decline was evident for the whole developmental period (egg stage to adult stage, linear regression: df ¼ 6, R 2 ¼ 0.753, t ¼ 4.272, P ¼ 0.005; Fig. 1), but most pronounced in the cocoon stage (linear regression: df ¼ 6, R 2 ¼ 0.800, t ¼ 4.897, P ¼ 0.003; Fig. 1). Thus, even though many parasitoids managed to develop and spin a cocoon, they often died before emerging as adults. Those few parasitoid larvae that survived to the cocoon stage despite having been reared in association with high-density herbivores (15 herbivores per cage) all died during the cocoon stage, while all cocoons produced by parasitoids of low-density herbivores (1 2 herbivores per cage) survived and emerged as adults (Fig. 1). v 6 February 2015 v Volume 6(2) v Article 21

7 decline much further until more than about 70% defoliation, after which it (the third group) again drops markedly. Altogether, the field data on how herbivore body weight declines in parallel with increased defoliation resemble the laboratory data, although the latter indicate a more continuous decline as compared to the putative thresholds identified in the field. DISCUSSION Fig. 3. Effects of defoliation level on sixteen Salix cinerea plants in the field (Uppsala, Sweden) on the mean adult body weight of the blue willow beetle (Phratora vulgatissima) individuals on them. The number of beetle individuals on each plant varied between 1 and 81. Parasitoid body size was not measured in this experiment, but has previously been shown to be negatively related to beetle size (Stenberg 2012).The parasitoid s larval development time was not affected by herbivore larval density class (linear regression: df ¼ 48, R 2, 0.001, t ¼ 0.132, P ¼ 0.895). Field study The degree of defoliation varied between 1% and 90% on the investigated S. cinerea plants (Fig. 3). The number of beetles found on the plants varied between 1 and 81 individuals; low numbers were found on plants with,2% or.85% defoliation. The GAM analysis showed that the percentage defoliation significantly affected the mean beetle body weight (F ¼ 5.041, P ¼ , R 2 ¼ 0.543) on the 16 S. cinerea plants examined. The body weights found can be roughly divided into three groups with respect to the plant defoliation pattern. First, by far the highest body weights were found on plants with very limited defoliation (,3% defoliation; Fig. 3), thereafter rapidly declining. Second, the mean body weight seems to stabilize at an intermediate level above about 3% defoliation and does not This study was undertaken to investigate why parasitoids often fail to utilize the increased number of hosts available during herbivore outbreaks. Two distinct patterns emerged when rearing herbivores in different density classes. First, the herbivore was increasingly controlled bottom-up; herbivore body size decreased, and larval development time increased in parallel with increasing herbivore larval density class. At high herbivore larval densities, the food plant was eventually totally consumed, suggesting that the beetles faced starvation and sometimes had to pupate prematurely. A similar pattern was found on S. cinerea in the field: beetle body size declined markedly and significantly in parallel with increasing level of defoliation (see Fig. 4 for an example of wild Salix plant skeletonized by Phratora vulgatissima). However, on S. cinerea in the field, the decline is not gradual, but occurs in two major steps. The first major decline in body weight happened at around 3% defoliation, which fits nicely with previous findings showing that moderate beetle grazing induces trichomes in S. cinerea which drastically reduce larval performance, including body weight (Dalin and Björkman 2003). The initial reduction in body weight on plants with relatively low defoliation may thus be due to induced defense in the plant. The second reduction in body weight occurs at roughly 70% defoliation, and this is probably due to food limitation. Second, while bottom-up control increased, it is evident that parasitoid survival declined at high herbivore densities. This suggests that, in this case, the top-down control is itself controlled bottom-up. That parasitoid fitness is dependent on herbivore size has been shown in a number of studies (e.g., Harvey et al. 1995, Harvey et al. 2005, Pennacchio and Strand 2006, Stenberg and Hambäck 2010), not least for this particular v 7 February 2015 v Volume 6(2) v Article 21

8 STENBERG Fig. 4. Wild Salix being skeletonized by Phratora vulgatissima leaf beetles. species (Stenberg 2012). Generally, parasitoids perform less well in small host bodies. In the current context, this relationship should provide an opportunity for the herbivores to escape the parasitoids and increase until they are unable to sustain themselves and the outbreak collapses. One of the findings that has emerged from the literature on parasitoids and the impact of host body size is that many parasitoids are able to discriminate between host sizes and preferentially oviposit on hosts of a more optimal size (Jervis et al. 2008). Such behavior could potentially stabilize the system and mitigate the parasitoid decline suggested by my data. Even though this is a possibility, the potential to find hosts of optimal size will be greatly reduced during outbreaks (Fig. 1). The results presented here suggest that the parasitoid decline is principally self-driven once the herbivore population has reached a high density. When the herbivore population grows, the individual herbivores reach a smaller average size due to increased competition (Figs. 1 and 3). Parasitoids respond immediately with a reduction in their fitness (Fig. 1), which in turn should produce lower parasitism pressure in the next v beetle generation. Following this train of thought the reduced top-down pressure should result in higher herbivore survival, and even increased herbivore competition, leading to even smaller herbivore body sizes, and so on until the parasitoid population collapses. In the absence of efficient trophic interactions, the herbivore population should be able to survive and grow until the outbreak is countered by bottom-up forces. Although speculative, this suggestion accords with previous findings that herbivores are food limited during outbreaks, rather than being regulated by parasitoids (White 2011). Many previous studies have examined whether parasitoids control the population dynamics of their herbivore hosts, or if the herbivores control the parasitoids (Hassell and Waage 1984, Tanhuanpa a et al. 2002, Turchin et al. 2003, Hagen et al. 2010, Schott et al. 2010, White 2011). This study suggests that, during P. vulgatissima outbreaks, it is the herbivores that control the parasitoids, and not vice versa. Parasitoids undoubtedly play a very important role between outbreaks in many systems, and may very well constitute an important reason why herbivores rarely reach the threshold level above which 8 February 2015 v Volume 6(2) v Article 21

9 outbreaks are initiated (DeBach and Rosen 1991). Thus, the solution to outbreaks in cropping systems is not to stop using parasitoids, but to use additional biocontrol agents that are less sensitive to herbivore body size during outbreaks (e.g., predators). In the Salix system it has been suggested that omnivorous egg-feeding heteropterans could be used for this purpose (Björkman et al. 2003, Stenberg et al. 2010). As indicated previously, plant-herbivore-parasitoid dynamics have been surprisingly resistant to explanation and their complexity should not be underestimated. Nevertheless, density-dependent body size seems to be one important factor, and I hope that this study will inspire theoretical ecologists to incorporate it into future models. In addition, the seemingly negative interaction between induced plant defenses affecting herbivore body size, and indirect defenses through parasitoids that are sensitive to reduced prey sizes, should be studied further. Taking herbivore body size into consideration will probably improve mathematical models of species interactions as well as programs for biological control of insect pests. ACKNOWLEDGMENTS I thank Warren Kunce and Ling Shen for technical assistance in the laboratory. This study was funded by The Foundation in Memory of Oscar and Lili Lamm and the Swedish Research Council Formas. LITERATURE CITED Baffoe, K. O., P. Dalin, G. Nordlander, and J. A. Stenberg Importance of temperature for the performance and biocontrol efficiency of the parasitoid Perilitus brevicollis (Hymenoptera: Braconidae) on Salix. Biocontrol 57: Berkvens, N., J. Moens, D. Berkvens, M. A. Samih, L. Tirry, and P. De Clercq Dinocampus coccinellae as a parasitoid of the invasive ladybird Harmonia axyridis in Europe. Biological Control 53: Björkman, C., P. Dalin, and K. Ahrne Leaf trichome responses to herbivory in willows: induction, relaxation and costs. New Phytologist 179: Björkman, C., P. Dalin, and K. Eklund Generalist natural enemies of a willow leaf beetle (Phratora vulgatissima): abundance and feeding habits. Journal of Insect Behavior 16: Bylund, H Long-term interactions between the autumnal moth and mountain birch: the roles of resources, competitors, natural enemies, and weather. Swedish University of Agricultural Sciences, Uppsala, Sweden. Dalin, P Diapause induction and termination in a commonly univoltine leaf beetle (Phratora vulgatissima). Insect Science 18: Dalin, P., and C. Björkman Adult beetle grazing induces willow trichome defence against subsequent larval feeding. Oecologia 134: Dalin, P., C. Björkman, and K. Eklund Leaf beetle grazing does not induce willow trichome defence in the coppicing willow Salix viminalis. Agricultural and Forest Entomology 6: Dalin, P., O. Kindvall, and C. Björkman Reduced population control of an insect pest in managed willow monocultures. PLoS ONE 4:e5487. DeBach, P., and D. Rosen Biological control by natural enemies. Second edition. Cambridge University Press, Cambridge, UK. Hagen, S. B., J. U. Jepsen, T. Schott, and R. A. Ims Spatially mismatched trophic dynamics: cyclically outbreaking geometrids and their larval parasitoids. Biology Letters 6: Harvey, J. A., I. F. Harvey, and D. J. Thompson The effect of host nutrition on growth and development of the parasitoid wasp Venturia canescens. Entomologia Experimentalis et Applicata 75: Harvey, J. A., S. Van Nouhuys, and A. Biere Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids. Journal of Chemical Ecology 31: Hassell, M. P., and J. K. Waage Host-parasitoid population interactions. Annual Review of Entomology 29: Haukioja, E Plant defenses and population fluctuations of forest defoliators: mechanism-based scenarios. Annales Zoologici Fennici 42: Jervis, M. A., J. Ellers, and J. A. Harvey Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annual Review of Entomology 53: Jonsson, M., H. L. Buckley, B. S. Case, S. D. Wratten, R. J. Hale, and R. K. Didham Agricultural intensification drives landscape-context effects on host-parasitoid interactions in agroecosystems. Journal of Applied Ecology 49: Kapari, L., E. Haukioja, M. J. Rantala, and T. Ruuhola Defoliating insect immune defense interacts with induced plant defense during a population outbreak. Ecology 87: Lehrman, A., M. Torp, J. A. Stenberg, R. Julkunen- Tiitto, and C. Björkman Estimating direct resistance in willows against a major insect pest, Phratora vulgatissima, by comparing life history traits. Entomologia Experimentalis et Applicata v 9 February 2015 v Volume 6(2) v Article 21

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