Natural host‐plant quality affects immune defence of an insect herbivore

Klemola, Netta; Klemola, Tero; Rantala, Markus J.; Ruuhola, Teija

doi:10.1111/j.1570-7458.2007.00533.x

Cited by 96 publications

(104 citation statements)

References 64 publications

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“…Crucial additional support is also provided by differences in defoliation levels between forest types. Meanwhile, the lack of evidence that induced defenses affect other insects may be a consequence of the lack of large-scale variation in tree-species composition within forests attacked by those insects (11,26), rather than a true lack of effect of induced defenses. Given enough experimental data with which to estimate parameters, however, our models could in principle be used to detect effects of induced defenses in defoliation data even in the absence of variability in forest type.…”

Section: Discussionmentioning

confidence: 99%

“…czerepanovii) can similarly alter the responses of autumnal moth (Epirrita autumnata) larvae to artificially implanted plastic filaments in the laboratory (25), but efforts to detect induction effects on autumnal moths in the field were likewise unsuccessful. Also, there is no obvious signature of induced defenses in time series of autumnal moth defoliation (26).…”

Section: Significancementioning

confidence: 99%

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Induced plant defenses, host–pathogen interactions, and forest insect outbreaks

Elderd

Rehill

Haynes

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Cyclic outbreaks of defoliating insects devastate forests, but their causes are poorly understood. Outbreak cycles are often assumed to be driven by density-dependent mortality due to natural enemies, because pathogens and predators cause high mortality and because natural-enemy models reproduce fluctuations in defoliation data. The role of induced defenses is in contrast often dismissed, because toxic effects of defenses are often weak and because induceddefense models explain defoliation data no better than naturalenemy models. Natural-enemy models, however, fail to explain gypsy moth outbreaks in North America, in which outbreaks in forests with a higher percentage of oaks have alternated between severe and mild, whereas outbreaks in forests with a lower percentage of oaks have been uniformly moderate. Here we show that this pattern can be explained by an interaction between induced defenses and a natural enemy. We experimentally induced hydrolyzable-tannin defenses in red oak, to show that induction reduces variability in a gypsy moth's risk of baculovirus infection. Because this effect can modulate outbreak severity and because oaks are the only genus of gypsy moth host tree that can be induced, we extended a natural-enemy model to allow for spatial variability in inducibility. Our model shows alternating outbreaks in forests with a high frequency of oaks, and uniform outbreaks in forests with a low frequency of oaks, matching the data. The complexity of this effect suggests that detecting effects of induced defenses on defoliator cycles requires a combination of experiments and models. host-pathogen model | Lymantria dispar | complex population dynamics | spatial model | hydrolyzable tannins P eriodic outbreaks of forest-defoliating insects severely damage valuable timber and increase atmospheric CO 2 levels by converting forests from carbon sinks to carbon sources (1). Decades of research have produced multiple hypotheses to explain defoliator outbreak cycles (2), but a decisive experiment to choose between competing hypotheses faces almost insurmountable logistical difficulties, because outbreaks occur at 5-30 y intervals and typically cover thousands of square kilometers (3). Efforts to support particular hypotheses have therefore instead relied on a mixture of observational field data, small-scale field and laboratory experiments, and mathematical models.For example, the most widely accepted hypothesis is that defoliator cycles are driven by natural enemies. Support for this hypothesis comes first of all from observational data showing that defoliators experience high rates of infection by specialist pathogens and parasitoids in peak populations (2, 4) and high rates of attack by generalist predators and parasitoids in trough populations (5). Second, experimental data have confirmed key assumptions of defoliator-natural-enemy models, and the models produce longperiod, large-amplitude cycles resembling time series of insect densities and defoliation levels (6).Neither data nor models have provided meani...

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Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Induced plant defenses, host–pathogen interactions, and forest insect outbreaks

Elderd

Rehill

Haynes

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…However, it is known that lepidopteran larvae also possess potent counter adaptations to parasitoid attack, such as the production of haemocytes and other factors that play an important role in the encapsulation process (Lavine and Strand 2002). As a result, immune responses of hosts may be either positive or negative, depending on the severity of a given factor, like induced changes in food plant quality (Klemola et al 2007) or on trade-oVs between diVerent traits being inXuenced by plant quality in the herbivore or the parasitoid (Adamo 2004;Rantala and RoV 2005). To tease apart the underlying physiological interactions between plants and herbivores, and hosts and parasitoids, a mechanistic approach is needed where host plant eVects on immune competence (phenoloxidase activity; haemocyte counts) and encapsulation levels are also measured (Adamo 2004;Kraaijeveld et al 2001) with information on the cascading eVects of plant chemistry on host vigour.…”

Section: Plant Defences and Herbivore Immune Responsementioning

confidence: 99%

Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism

et al. 2009

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The mechanisms through which trophic interactions between species are indirectly mediated by distant members in a food web have received increasing attention in the Weld of ecology of multitrophic interactions. Scarcely studied aspects include the eVects of varying plant chemistry on herbivore immune defences against parasitoids. We investigated the eVects of constitutive and herbivoreinduced variation in the nutritional quality of wild and cultivated populations of cabbage (Brassica oleracea) on the ability of small cabbage white Pieris rapae (Lepidoptera, Pieridae) larvae to encapsulate eggs of the parasitoid Cotesia glomerata (Hymenoptera, Braconidae). Average encapsulation rates in caterpillars parasitised as Wrst instars were low and did not diVer among plant populations, with caterpillar weight positively correlating with the rates of encapsulation. When caterpillars were parasitised as second instar larvae, encapsulation of eggs increased. Caterpillars were larger on the cultivated Brussels sprouts plants and exhibited higher levels of encapsulation compared with caterpillars on plants of either of the wild cabbage populations. Observed diVerences in encapsulation rates between plant populations could not be explained exclusively by diVerences in host growth on the diVerent Brassica populations. Previous herbivore damage resulted in a reduction in the larval weight of subsequent herbivores with a concomitant reduction in encapsulation responses on both Brussels sprouts and wild cabbage plants. To our knowledge this is the Wrst study demonstrating that constitutive and herbivore-induced changes in plant chemistry act in concert, aVecting the immune response of herbivores to parasitism. We argue that plant-mediated immune responses of herbivores may be important in the evaluation of Wtness costs and beneWts of herbivore diet on the third trophic level.

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“…The encapsulation kills an intruder either by suffocation or through the production of necrotizing compounds (Nappi et al 1995). In our study, the strength of insect immune defense was determined by measuring the melanotic degree of an encapsule formed around a foreign object (Kapari et al 2006;Klemola et al 2007). In the autumnal moth, the encapsulation rate correlates with the resistance against entomopathogenic fungi, which are known to cause substantial mortality in E. autumnata .…”

Section: Methodsmentioning

confidence: 99%

Immunological Memory of Mountain Birches: Effects of Phenolics on Performance of the Autumnal Moth Depend on Herbivory History of Trees

et al. 2007

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Plants have been suggested to have an immunological memory comparable to animals. The evidence for this, however, is scarce. In our study with the mountain birchEpirrita autumnata system, we demonstrated that birches exposed as long as 5 yr to feeding of E. autumnata larvae (delayed induced resistance, DIR), responded more strongly to a new challenge than trees without an herbivory history. Pupal weights remained lower, and the duration of the larval period was prolonged in the DIR trees, although immunity, measured as an encapsulation rate, was not affected. We further demonstrated that the effects of birch phenolics on performance of E. autumnata were different in the exposed (DIR) trees from naive control trees, although we found only one significant change in chemistry. The quercetin:kaemferol ratio was increased in DIR trees, suggesting that herbivory caused oxidative stress in birches. In DIR trees, phenolics, especially hydrolyzable tannins (HTs), affected pupal weights negatively, whereas in control trees, the effects were either nonsignificant or positive. HTs also prolonged the duration of the larval period of females, whereas peroxidase (POD) activity prolonged that of males. We suggest that the causal explanation for the induced resistance was an enhanced oxidation of phenolic compounds from the DIR trees in the larval digestive tract. Phenolic oxidation produces semiquinones, quinones, free radicals, and ROS, which may have toxic, antinutritive, and/or repellent properties against herbivores.

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Natural host‐plant quality affects immune defence of an insect herbivore

Cited by 96 publications

References 64 publications

Induced plant defenses, host–pathogen interactions, and forest insect outbreaks

Induced plant defenses, host–pathogen interactions, and forest insect outbreaks

Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism

Immunological Memory of Mountain Birches: Effects of Phenolics on Performance of the Autumnal Moth Depend on Herbivory History of Trees

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