Oecologia (2011) 167:1–9 DOI 10.1007/s00442-011-1968-2

CONCEPTS, REVIEWS AND SYNTHESES

Herbivore-induced resource sequestration in : why bother?

Colin M. Orians • Alexandra Thorn • Sara Go´mez

Received: 4 September 2010 / Accepted: 8 March 2011 / Published online: 24 March 2011 Ó Springer-Verlag 2011

Abstract can cause numerous changes in will depend on certain external factors: abiotic conditions, primary metabolism. Recent studies using radioiso- types of herbivores, and trophic interactions. We hope the topes, for example, have found that insect herbivores and concepts presented here will stimulate more focused related cues can induce faster export from and research on the ecological and evolutionary costs and ben- and greater partitioning into tissues inaccessible to foraging efits of -induced resource sequestration. herbivores. This process, termed induced resource seques- tration, is being proposed as an important response of plants Keywords Defense Á Plant–herbivore interactions Á to cope with herbivory. Here, we review the evidence for Storage Á Tolerance Á Resource allocation resource sequestration and suggest that associated allocation and ecological costs may limit the benefit of this response because resources allocated to storage are not immediately Introduction available to other plant functions or may be consumed by other enemies. We then present a conceptual model that For all organisms, allocation of resources to the primary describes the conditions under which benefits might out- functions of growth and reproduction must be balanced weigh costs of induced resource sequestration. Benefits and with the various secondary functions required to survive costs are discussed in the context of differences in plant life- and deal with abiotic and biotic stresses. Plants rely on history traits and biotic and abiotic conditions, and new physiological, chemical, biomechanical, and developmen- testable hypotheses are presented to guide future research. tal processes to deal with stress. Stresses that vary in time, We predict that intrinsic factors related to life history, such as drought and attack by herbivores, require constant ontogeny and phenology will alter patterns of induced adjustment and these adjustments are essential to growth sequestration. We also predict that induced sequestration and survival of plants (Mooney and Winner 1991; Karban and Baldwin 1997; Agrawal and Karban 1999). In response to herbivory, for example, plants can employ two general Communicated by Caroline Mu¨ller. strategies: production of chemical and morphological defense traits to deter herbivores (‘‘resistance’’), and C. M. Orians (&) Á A. Thorn Á S. Go´mez Department of Biology, Tufts University, mobilization of storage reserves for regrowth and repro- Medford, MA 02155, USA duction after loss (‘‘tolerance’’) (Karban and Baldwin e-mail: [email protected] 1997). Tolerance mechanisms are often linked to regrowth A. Thorn processes after a herbivory event (Tschaplinksi and Blake e-mail: [email protected] 1989a, b; Tiffin 2000). Less appreciated, however, is the S. Go´mez herbivore-induced change in resource allocation and e-mail: [email protected] physiology that can increase plant tolerance to herbivory (Schwachtje and Baldwin 2008). This phenomenon, termed S. Go´mez Department of Biological Sciences, induced resource sequestration, refers to rapid herbivore- University of Rhode Island, Kingston, RI 02882, USA induced changes in resource allocation patterns that result 123 2 Oecologia (2011) 167:1–9 in an increase in export of existing or newly acquired partitioning in wild tobacco extends flowering time and resources from attacked tissues (and/or systemic tissues thereby increases fitness. Given the increasing evidence for with vascular connections) into storage organs. These induced sequestration, there is a need to examine the resources are thus temporarily sequested (unavailable) for conditions likely to favor this strategy. growth, defense or storage in the tissues from which they were exported. Storage: benefits and costs

Evidence for induced resource sequestration It is well known that constitutive storage represents an important buffer against abiotic and biotic stresses There is growing evidence that herbivore feeding, herbi- (Trumble et al. 1993; Kobe et al. 2010). For example, vore cues and signal molecules associated with herbivory drought often triggers a change in the distribution of starch cause changes in resource export and allocation to storage and sugar reserves and frequently results in greater trans- tissue (Holland et al. 1996; Schwachtje et al. 2006; Babst port to roots or to young developing leaves (Geiger and et al. 2008; Kaplan et al. 2008). Holland et al. (1996), for Servaites 1991). Similarly, defoliation is well known to example, found that feeding by grasshoppers causes 14Cto result in the mobilization of starch reserves to fuel new accumulate in roots. Kaplan et al. (2008) showed a similar plant growth (Tschaplinksi and Blake 1989a, b; Kosola pattern in tobacco roots after folivory by chewing herbi- et al. 2001), and the presence of these storage reserves is a vores using 13C. Recent studies have adopted the use of key factor determining post-defoliation survival (Canham 11 short-lived radioisotopes (such as CO2), which allows et al. 1999). The buffering capacity of storage implies that quantification of resource dynamics in vivo and the com- herbivore-induced storage could be adaptive. parison of allocation patterns before and after treatment. There can be costs of storage. Although studies of wild 11 This is possible because of the rapid decay of CO2 and cultivated species have shown that species with higher (t1/2 = 20.4 min). This approach has been used to docu- rates of storage are more likely to survive stressors such as ment an increase in leaf photosynthate export to stems and/ shading (Kobe 1997; Myers and Kitajima 2007), drought or or roots within hours of treatment with jasmonic acid nutrient stress (Shaw et al. 2002; Paula and Pausas 2011), (Babst et al. 2005), caterpillar regurgitant (Schwachtje and defoliation (Anten et al. 2003; Myers and Kitajima et al. 2006), or feeding by gypsy moth larvae (Babst et al. 2007), these same studies show that these species grow 2008). In addition to Babst et al. (2005), other studies have more slowly. Induced storage may provide a buffering also used jasmonates to study induced sequestration. mechanism without the long-term growth costs of consti- Methyl jasmonate increases photosynthate export from tutive storage. treated leaves (Go´mez et al. 2010) and treatment of roots We note that costs may be transient by varying with with jasmonates causes photosynthate to be diverted away plant ontogeny and phenology (Boege and Marquis 2005; from the treated roots and into untreated roots (Henkes Boege et al. 2007; Orians et al. 2010; Van Dam et al. et al. 2008). Interestingly, silencing the jasmonate pathway 2001). In particular, deflection from growth may be most in wild tobacco does not prevent induced export and par- costly during periods of rapid growth, including periods of titioning (Schwachtje et al. 2006), suggesting that other leaf production and fruit maturation. A recent study that signaling pathways may also be involved. focused on growth–defense tradeoffs in willow illustrates Changes in resource allocation in response to herbivory this concept (Orians et al. 2010). This study found evidence are not limited to photosynthate. For example, Frost and for a trade-off between allocation to roots and defense in Hunter (2008) did not observe increased carbon accumu- younger seedlings but a positive correlation in older lation in storage tissues of oaks following herbivory, but seedlings, a result consistent with the observation that did observe an increase in nitrogen within these tissues. larger plants often grow faster and produce higher con- When methyl jasmonate is applied to leaves of tomato, it centrations of chemical defenses (e.g., Briggs and Schultz increases nitrogen (13N) export and partitioning to roots 1990; Orians et al. 2003). (Go´mez et al. 2010), and when applied to roots of alfalfa it In contrast to the cost of constitutive storage, the costs of increases nitrogen storage within the tap (Meuriot herbivore-induced resource sequestration has received little et al. 2004). attention. It may result in allocation costs (fewer resources Relatively little is known about the long-term conse- for growth or reproduction), or ecological costs (higher quences of induced sequestration. Beardmore et al. (2000) performance of enemies that consume storage tissues). showed that chronic exposure of leaves to methyl jasmo- Evidence for allocation costs comes from a study on wild nate can increase protein concentrations in storage tissues tobacco (Schwachtje et al. 2006). They found that induc- in poplar. Schwachtje et al. (2006) found that induced root tion of wild-type plants increased carbon allocation to roots 123 Oecologia (2011) 167:1–9 3

(10%) and resulted in smaller plants that exhibited delayed reproduction. Moreover, a transformed genotype that had constitutively greater allocation to roots was shorter and produced fewer reproductive capsules. Interestingly, the transformed genotype mobilized the root reserves after elicitation and this resulted in greater flower production later in the season. Clearly there are costs and potential benefits of induced sequestration. We expect that costs might be even larger in other plants since photosynthate allocation to stems and/or roots has been shown to be as high as 25% (Babst et al. 2008). Moreover, many studies have shown that plants grow more slowly and exhibit reduced fitness after simulated attack (Baldwin et al. 1998; Zavala et al. 2004; Walls et al. 2005; reviewed by Cipollini et al. 2003). While this is usually attributed to the cost of resistance, an increase in induced sequestration could contribute to this difference. There are also potential ecological costs (Kaplan et al. 2008). Herbivore-induced resource sequestration and potential subsequent exudation into the can alter or create new interactions between plants and other organisms in the soil (Bardgett et al. 1998; Henry et al. 2008). In some cases, induced allocation changes can lead to positive interactions by promoting the colonization by mutualists such as mycorrhizae (Tejeda-Sartorius et al. 2008), but in other cases induced sequestration might incur ecological costs if it attracts or improves the performance Fig. 1 Conceptual model for resource flows in plants. The labile of consumers of the organs where resources are being resource pool is derived from newly captured pools of carbon and stored. For example, Kaplan et al. (2009) showed that nutrient pools or from remobilized storage reserves. The labile carbon pool is generated from , primarily by mature source aboveground herbivory in tobacco resulted in an increased leaves. The labile nutrient pool is obtained from roots. The resulting allocation of carbon to roots and this was linked to an labile resource pool can then be allocated to support the growth of increase in fecundity of a root nematode. sink tissues (roots, leaves, or reproductive tissues), to defense traits, and to storage tissues. Herbivore-induced export of resources from leaves or from fine roots (dashed arrows) into stems and storage roots functions to sequester resources in tissues inaccessible to the Conceptual model for resource allocation respective herbivores but may incur opportunity costs if resources allocated for storage limit growth and reproduction or ecological costs While it is apparent that trade-offs often exist under- if other enemies specialize on these storage tissues standing the ways in which intrinsic and extrinsic factors are expected to affect resource allocation requires a Nichols-Orians and Schultz 1990). Allocation to stem and detailed examination of the status of different tissues. In root storage may be increasingly favored as the probability Fig. 1, we present a conceptual model for possible path- of continued defoliation increases, but this depends on the ways of resource flow within a plant. In general, mature vulnerability of these storage pools to attack by stem and source leaves are responsible for the majority of carbon root herbivores or pathogens (see ecological costs above), fixation, and fine roots for the majority of nutrient uptake. and intrinsic traits of the plant (see Fig. 2 below). These resources may be allocated locally to growth, defense, or storage (Blossey and Hunt-Joshi 2003; Karban and Baldwin 1997), or exported for use elsewhere in the Herbivore-induced resource sequestration: a predictive plant. For a plant in vegetative growth phase that is not framework experiencing herbivory, investment in new leaves repre- sents the best assurance of long-term growth, but this may We present a fulcrum model that explores conditions that not be the case when herbivores are present, since these will tend to favor greater induced sequestration relative to young leaves are often particularly vulnerable to attack growth and/or defense (Fig. 2). We note that most plants even when these young leaves are highly defended (e.g., simultaneously grow, defend and allocate to storage so our 123 4 Oecologia (2011) 167:1–9

Fig. 2 A fulcrum model for GROWTH AND/OR DEFENSE INDUCED SEQUESTRATION predicting herbivore-induced FAVORED FAVORED sequestration in plants. Outcomes depend upon the relative strength of intrinsic and extrinsic factors. See text for Annuals Perennials presentation of specific predictions LIFE Low storage in leaves High storage in leaves HISTORY High constitutive storage Low constitutive storage (in roots/stems) (in roots/stems)

ONTOGENY Developing plants Mature plants NTRINSIC FACTORS I During leaf flushing Post-leaf expansion PHENOLOGY During seed/fruit production Prior to seed/fruit production

Low light High light ABIOTIC High nutrient Low nutrient

Generalist herbivores Specialist herbivores

Mobile (specially if small) Immobile or mobile (if large)

Solitary Gregarious/outbreaking species BIOTIC Browsing mammals or Leaf chewing insects XTRINSIC FACTORS

E piercing/sucking insects

High abundance of storage organ Low abundance of storage organ attackers attackers goal is to highlight conditions that will maximize the extent 2011). For species with high constitutive storage, the of induced resource sequestration. First, we evaluate amount of carbon that can be sequestered during a folivore intrinsic factors such as life history, ontogeny and phe- attack is likely to be a small fraction of the total storage pool. nology. Second, we review extrinsic factors including the Induced carbon sequestration may provide little benefit in abiotic and biotic environment, including resource avail- these cases. In contrast, for species with little root storage or ability and attributes of the herbivores themselves. for species that maintain high storage pools in their leaves during the growing season, induced export is predicted to be Intrinsic factors beneficial. In these plants, resources deflected from growth and into storage during an attack may provide a critical pool of To understand how patterns of resource allocation change resources necessary for regrowth. in response to herbivory, it is necessary to characterize the Although these expectations have not been explicitly status of the plant prior to herbivory. This status depends tested, a few studies fit the predictions. Photosynthate on a range of factors, but centrally on aspects of plant life export to roots in the annual Nicotiana attenuata increased history, plant ontogeny and phenology. only 10% (Schwachtje et al. 2006). In contrast, induced sequestration of photosynthate was close to 25% in Pop- Life history ulus (Babst et al. 2008), a woody perennial with high concentrations of starch in its leaves (Babst et al. 2005). Plant species diverge greatly in their inherent patterns of Red oak, however, exhibited no induced sequestration of allocation to storage. Many plants constitutively allocate photosynthate (Frost and Hunter 2008). Compared to other large amounts of resources to rhizome and root storage. species, oaks have a large root system and readily resprout This is true for cultivated crops such as beets, carrots and following cutting (Abrams 2003). The lack of induced potato, for biennial and perennial wild plants such as Al- sequestration is consistent with the prediction that induced liaria petiolata (biennial) and Pastinaca sativa (biennial to sequestration would be low in species with high constitu- perennial; Sosnova´ and Klimesˇova´ 2009), and for species tive storage. Clearly further research explicitly comparing that have a high capacity for resprouting (Paula and Pausas species with different intrinsic traits is warranted.

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Other life-history traits may also be important. Grime (especially in annuals) since reproductive tissues are strong (2001) classified species as being ruderal (short-lived sinks. weedy species), competitive (long-lived dominant species), or stress tolerators (species adapted to stressful environ- Extrinsic factors ments). These differences are likely to influence a plant’s relative resource allocation to growth, defense and storage. Abiotic Rapid growth is a characteristic of ruderal species, and individuals that do not prioritize growth are likely to be Light and soil nutrient availability have large effects on overgrown, making the opportunity costs of induced stor- patterns of allocation to roots and to storage. In response to age very high. Only after establishment might we expect light limitation, both the ratio of roots to shoot (Mooney induced sequestration in these species. In contrast, both and Winner 1991) and the concentration of storage com- competitive and stress tolerant species are expected to pounds are much lower (Nichols-Orians 1991), suggesting invest significant resources in storage as a way to buffer that induced resource sequestration will be constrained by against environmental fluctuations (Kobe et al. 2010; Paula light availability. In contrast, root:shoot ratios increase in and Pausas 2011). While induced resource sequestration response to soil nutrient limitation, and a recent study by may be more common in these species, we expect it to be Kobe et al. (2010) showed that investment in non-structural negatively correlated with constitutive levels of storage as within roots contributed to this pattern. This species with more constitutive storage already have the leads us to predict that the capacity for induced seques- capacity to recover from tissue loss. tration may be greater for plants experiencing low nutrient conditions. Ontogeny Biotic Herbivore-induced sequestration is also postulated to vary with plant ontogeny (Fig. 2). Young plants and their young The extent of damage, herbivore specialization, mobility, tissues are particularly prone to attack due to a higher feeding guild, and gregariousness are all likely to affect the nitrogen content and less developed physical properties likelihood of induced resource sequestration (Fig. 2). (McKey 1974; Coley and Barone 1996; Fenner et al. 1999; Evolutionarily, species typically consumed by large Wainhouse et al. 2009). Their small size also makes it browsing mammals, for example, may maintain high con- likely that herbivores can rapidly remove most if not all of stitutive storage and exhibit little induced storage. Insect the leaf area (e.g., Fritz et al. 2001). This may limit the herbivores, whose populations fluctuate widely from year benefits of induced sequestration and favor defense and to year, represent a more variable selective pressure growth. In contrast, older plants may benefit from induced (Hunter 1991), and could select for an induced sequestra- export of resources to short-term storage pools prior to tion response. Even within insect herbivores, the benefits of reproduction or to late-season sequestration of resources induced sequestration are likely to vary and this could lead for overwintering (perennials only). to the evolution of specific plant responses (Agrawal 2000). To date, the evidence for induced sequestration comes from Phenology plant responses to herbivorous insects. Below, we examine how the extent of damage and characteristics of the her- Both leaf and reproductive phenology are predicted to bivorous insect are both likely to affect patterns of resource influence patterns of induced sequestration (Fig. 2). At leaf sequestration. flush, young expanding leaves are generally highly sus- ceptible to herbivores (Coley and Barone 1996), making Extent of damage Ecologically, under mild or moderate rapid maturation a key defensive trait (Aide 1988). We herbivore defoliation, allocation of storage should be costly expect minimal induced sequestration during periods of since stored resources are unavailable for investment in leaf expansion; rather, the production of new leaf tissue new tissues. A smaller leaf area not only limits growth and the defense of existing tissue is likely to be particularly rates during herbivory but would also be expected to limit important to both young annuals and first-year perennial regrowth potential. In contrast, if leaf area loss eventually plants as predicted by the Optimal Defense Hypothesis leads to complete defoliation, the growth rate of leaves (McKey 1974; van Dam et al. 1996; de Boer 1999). Once during herbivore attack is irrelevant (all leaves are expanded, induced sequestration rates are predicted to be removed), and the increase in stored carbon pools from higher. We also expect higher rates of induced sequestra- induced storage would be expected to increase the tion prior to reproduction. During seed and fruit matura- regrowth potential. Similarly, induced storage during a tion, however, we expect minimal induced sequestration mild attack is expected to be beneficial if early season 123 6 Oecologia (2011) 167:1–9 herbivory predicts more severe future attack or if late are often the most frequently observed herbivores on their season defoliation is common for and is predicted by early- host plants (Bjo¨rkman et al. 2000; Carson and Root 2000; season herbivory. In particular, if complete defoliation later Dalin 2006). Solitary species, in contrast, are less likely to in the growing season is likely, induced storage in response become numerically dominant and often exhibit conspe- to prior attack would be beneficial. Moreover, since young cific avoidance and even experience higher mortality rates tissues are often more vulnerable to subsequent damage when aggregated (Jones 1987; Eber 2004). This will tend to than mature tissues (Denno and McClure 1983; Nichols- limit the magnitude of damage, unless individual herbi- Orians and Schultz 1990), allocation to new growth could vores are large (e.g., later instars of some insect species result in higher total leaf removal. This could shift the such as Manduca sexta). Induced sequestration may be balance to favor storage over continued production of new critical to regrowth following attack by gregarious species leaves. whereas for solitary species it would more likely represent an opportunity cost. Specialist versus generalist species We suggest that induced sequestration may be a more effective strategy Feeding guild To date, studies documenting induced against specialist herbivores than induced chemical sequestration have used leaf-chewing herbivores as mod- defenses (Fig. 2). Many specialist herbivores have evolved els, either by releasing herbivores on the plants, inducing effective detoxification mechanisms, and even use the toxic them with regurgitants/salivary cues, or by treating plants chemicals as feeding or oviposition cues (Macel and Vri- with jasmonates. To our knowledge, no studies have eling 2003;Mu¨ller-Scha¨rer et al. 2004; Hopkins et al. examined the effects of mammalian browsers or piercing/ 2009). The failure of many chemical defenses to deter sucking insects such as aphids, whiteflies, adelgids and specialist herbivores leads to the prediction that induced scale insects. Several lines of evidence suggest that induced sequestration would be prevalent in response to specialists. sequestration will be limited in response to both. Browsers In contrast, induced chemical defenses are quite effective can rapidly defoliate an entire plant and thus there would against generalists, and therefore we predict plants to be little time to respond. Although piercing/sucking insects allocate more resources to defense than to storage when do not cause defoliation, we still expect little induced attacked by generalists. sequestration. By feeding directly from the phloem, they cause less tissue damage, and thus tend to cause little or no Sedentary versus mobile species For sessile herbivores, induction (Walling 2000, 2008). Some even silence plant larvae develop in the tissue on which the adult females defense responses (Walling 2008). Still other piercing/ lay their eggs. Unless other ovipositing females are sucking insect species are able to hormonally manipulate present, the risk of attack to uninfested leaves is zero. the plant and thus actually increase sink strength within the Moreover, it is not uncommon for these sedentary species attacked tissues (Giordanengo et al. 2010). to aggregate (Whitham 1983;OriansandBjo¨rkman 2009). We therefore predict that damage by sedentary Communities of attackers: from aboveground to below- herbivores will favor export of resources from the ground The adaptive value of induced sequestration of attacked leaves (Fig. 2), although the opposite pattern carbohydrates in the roots and stems depends on the may be observed if herbivores are able to hormonally security of this pool of storage reserves (Fig. 2). Despite manipulate the plant (Giron et al. 2007). Indeed, high the benefits that resource sequestration can confer to plants densities of leaf miners are known to trigger early leaf in response to herbivory, exporting resources to storage abscission (Bultman and Faeth 1986). In contrast, mobile organs can have far-reaching consequences that may not herbivores often move between leaves. We therefore always have a positive effect on plant performance. Plants expect mobile herbivores to induce export both locally are simultaneously attacked above- and belowground by a and systemically, as has been observed for gypsy moths myriad of herbivores and pathogens (Masters et al. 1993; on Populus (Babst et al. 2008). Van der Putten et al. 2001; Blossey and Hunt-Joshi 2003; Dicke 2009; Kaplan et al. 2009). Therefore, the presence of Gregarious versus solitary species We predict that the root attackers could represent a major cost to export of ability to rapidly sequester resources into storage organs material from the leaves by providing additional resources may be an essential response to gregarious herbivores to root herbivores and pathogens (Kaplan et al. 2008). (Fig. 2). In fact, the propensity to aggregate is the one Similarly, stem-borers could also exploit the sequestered factor repeatedly associated with insect species that com- resources. Thus, the success of exporting aboveground monly reach outbreak densities and cause extensive defo- resources into stems or roots as a strategy to safeguard liation (Nothnagle and Schultz 1987; Larsson et al. 1993; valuable resources will depend on the herbivore/pathogen reviewed by Hunter 1991). Moreover, gregarious species pressure on those tissues. 123 Oecologia (2011) 167:1–9 7

Conclusions Blossey B, Hunt-Joshi TR (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annu Rev Entomol 48:521–547 There is increasing evidence showing that plants increase Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the their allocation to storage tissues in response to herbivory. ontogeny of resistance in plants. Trends Ecol Evol 20:441–448 All else being equal, however, allocation to storage rep- Boege K, Dirzo R, Siemens D, Brown P (2007) Ontogenetic switches resents an allocation cost since investment in new growth from plant resistance to tolerance: minimizing costs with age? Ecol Lett 10:177–187 would increase plant size and ultimately reproductive Briggs MA, Schultz JC (1990) Chemical defense production in Lotus potential. Yet certain conditions are more or less likely to corniculatus L. II. Trade-offs among growth, reproduction and favor such a strategy. We have argued that greater attention defense. Oecologia 83:32–37 to the ecological context is needed before testing when and Bultman TL, Faeth SH (1986) Selective oviposition by a leaf miner in response to temporal variation in abscission. Oecologia where induced sequestration is likely to be common and to 69:117–120 evaluate its adaptive value. In Fig. 2, we have outlined Canham CD, Kobe RK, Latty EF, Chazdon RL (1999) Interspecific several conditions predicted to favor induced sequestration and intraspecific variation in tree seedling survival: effects of and other conditions that make such a strategy less likely. allocation to roots versus reserves. Oecologia 121:1–11 The balance of these forces is expected to determine the Carson WP, Root RB (2000) Herbivory and plant species coexistence: magnitude of induced storage in a given species or popu- community regulation by an outbreaking phytophagous insect. lation. We hope this paper stimulates further research into Ecol Monogr 70:73–99 the benefits, costs and mechanisms of this phenomenon. Cipollini DF, Purrington CB, Bergelson J (2003) Costs of induced responses in plants. Basic Appl Ecol 4:79–89 Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical Acknowledgments We thank the anonymous reviewers for their forests. Annu Rev Ecol Syst 27:305–335 valuable comments on the manuscript. The project was supported by Dalin P (2006) Habitat difference in abundance of willow leaf beetle the National Research Initiative (or the Agriculture and Food Phratora vulgatissima (Coleoptera: Chrysomelidae): plant qual- Research Initiative) of the USDA National Institute of Food and ity or natural enemies. Bull Entomol Res 96:629–635 Agriculture, grant number # 2007-35302-18351. de Boer NJ (1999) Pyrrolizidine alkaloid distribution in Senecio jacobaea rosettes minimises losses to generalist feeding. 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