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Population-related variation in plant defense more strongly affects survival of an herbivore than its solitary parasitoid wasp.

Harvey JA, Gols R - J. Chem. Ecol. (2011)

Bottom Line: Moreover, development was prolonged and biomass was reduced on herbivore-induced plants.However, GS chemistry could not explain the reduced performance on induced plants since only indole GS concentrations increased in response to herbivory, which did not affect insect performance based on multivariate statistics.This result suggests that, in addition to aliphatic GS, other non-GS chemicals are responsible for the decline in insect performance, and that these chemicals affect the parasitoid more strongly than the host.

View Article: PubMed Central - PubMed

Affiliation: Department of Terrestrial Ecology, Netherlands Institute of Ecology, Wageningen, The Netherlands. j.harvey@nioo.knaw.nl

ABSTRACT
The performance of natural enemies, such as parasitoid wasps, is affected by differences in the quality of the host's diet, frequently mediated by species or population-related differences in plant allelochemistry. Here, we compared survival, development time, and body mass in a generalist herbivore, the cabbage moth, Mamestra brassicae, and its solitary endoparasitoid, Microplitis mediator, when reared on two cultivated (CYR and STH) and three wild (KIM, OH, and WIN) populations of cabbage, Brassica oleracea. Plants either were undamaged or induced by feeding of larvae of the cabbage butterfly, Pieris rapae. Development and biomass of M. brassicae and Mi. mediator were similar on both cultivated and one wild cabbage population (KIM), intermediate on the OH population, and significantly lower on the WIN population. Moreover, development was prolonged and biomass was reduced on herbivore-induced plants. However, only the survival of parasitized hosts (and not that of healthy larvae) was affected by induction. Analysis of glucosinolates in leaves of the cabbages revealed higher levels in the wild populations than cultivars, with the highest concentrations in WIN plants. Multivariate statistics revealed a negative correlation between insect performance and total levels of glucosinolates (GS) and levels of 3-butenyl GS. However, GS chemistry could not explain the reduced performance on induced plants since only indole GS concentrations increased in response to herbivory, which did not affect insect performance based on multivariate statistics. This result suggests that, in addition to aliphatic GS, other non-GS chemicals are responsible for the decline in insect performance, and that these chemicals affect the parasitoid more strongly than the host. Remarkably, when developing on WIN plants, the survival of Mi. mediator to adult eclosion was much higher than in its host, M. brassicae. This may be due to the fact that hosts parasitized by Mi. mediator pass through fewer instars, and host growth is arrested when they are only a fraction of the size of healthy caterpillars. Certain aspects of the biology and life-history of the host and parasitoid may determine their response to chemical challenges imposed by the food plant.

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Conceptual diagram showing the relationship between herbivore (healthy or parasitized) growth curves and cumulative mortality on food plants that differ in their quality. Solid linea and short dashed linee represent herbivore growth curves on non-induced plants; long dashed lineb, dotted linec and alternating dot-dashed lined lines represent herbivore growth curves on induced plants. In this example, the parasitoid is solitary and the host caterpillar must reach a much smaller critical size to support parasitoid development (left dashed black vertical line) than to successfully pupate (right vertical black dashed line). In this study, induction steepens the mortality curve (lines a, b) reducing survival of both the parasitoid and the herbivore; the latter does not survive at all on induced plants because it cannot grow large enough to reach a minimum viable size for pupation. If the plant is even more toxic, then the parasitized host does not even reach a critical size and all parasitoids die before egression form the host (line c). In some instances, perhaps due to stress caused by parasitism, parasitoids may experience higher mortality on induced plants than their hosts (line d), or else herbivore and parasitoid mortality on non-induced plants does not differ (line e). Many different combinations are possible, depending on the effects of the plant on the herbivore and parasitoid, the parasitoid on the herbivore, and quantitative differences in the required growth of healthy and parasitized hosts
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Fig4: Conceptual diagram showing the relationship between herbivore (healthy or parasitized) growth curves and cumulative mortality on food plants that differ in their quality. Solid linea and short dashed linee represent herbivore growth curves on non-induced plants; long dashed lineb, dotted linec and alternating dot-dashed lined lines represent herbivore growth curves on induced plants. In this example, the parasitoid is solitary and the host caterpillar must reach a much smaller critical size to support parasitoid development (left dashed black vertical line) than to successfully pupate (right vertical black dashed line). In this study, induction steepens the mortality curve (lines a, b) reducing survival of both the parasitoid and the herbivore; the latter does not survive at all on induced plants because it cannot grow large enough to reach a minimum viable size for pupation. If the plant is even more toxic, then the parasitized host does not even reach a critical size and all parasitoids die before egression form the host (line c). In some instances, perhaps due to stress caused by parasitism, parasitoids may experience higher mortality on induced plants than their hosts (line d), or else herbivore and parasitoid mortality on non-induced plants does not differ (line e). Many different combinations are possible, depending on the effects of the plant on the herbivore and parasitoid, the parasitoid on the herbivore, and quantitative differences in the required growth of healthy and parasitized hosts

Mentions: In many plant–herbivore associations, early instars are more susceptible to plant allelochemicals and other plant quality characteristics than later instars. In this case, mortality spikes during the first instar and then levels off as the larvae grow and become better able to detoxify and/or excrete the plant’s toxins (Zalucki et al., 2002). However, in our study, the effects of plant quality in WIN plants on the survival of M. brassicae and Mi. mediator were gradual on non-induced and induced plants. Microplitis mediator terminates its relationship with the host at an earlier stage of development (typically L3 or early L4), a point when the host is only approximately 5% of the mass of a fully grown healthy caterpillar (Fig. 4). We also noted that some caterpillars of M. brassicae feeding on WIN plants successfully molted to the 5th instar, but were quite small (<500 mg) and refused to eat after molting, generally perishing within a week or so. Furthermore, whereas the larval development of a healthy M. brassicae caterpillar can last up to 3 weeks or even longer, that of a parasitized caterpillar is less than half of this duration. This means that parasitized caterpillars are under fewer host-growth-related constraints than healthy caterpillars, and this may explain the discrepancy in survival of the host and parasitoid on induced and undamaged WIN leaf tissues, compared with the other strains/populations (Fig. 4). We have provided a conceptual graph (Fig. 4) showing that koinobiont parasitoids, such as Mi. mediator, which terminate their relationship with the host at a very early stage of development (e.g., when it is very small), may be less susceptible to plants of low quality than parastioids that either require the host to grow to a large final size or healthy hosts. This is because the effects of plant toxins may be cumulative over the course of herbivore/parasitoid development, or else because the insects are forced to interact with the plant for a longer period of time.Fig. 4


Population-related variation in plant defense more strongly affects survival of an herbivore than its solitary parasitoid wasp.

Harvey JA, Gols R - J. Chem. Ecol. (2011)

Conceptual diagram showing the relationship between herbivore (healthy or parasitized) growth curves and cumulative mortality on food plants that differ in their quality. Solid linea and short dashed linee represent herbivore growth curves on non-induced plants; long dashed lineb, dotted linec and alternating dot-dashed lined lines represent herbivore growth curves on induced plants. In this example, the parasitoid is solitary and the host caterpillar must reach a much smaller critical size to support parasitoid development (left dashed black vertical line) than to successfully pupate (right vertical black dashed line). In this study, induction steepens the mortality curve (lines a, b) reducing survival of both the parasitoid and the herbivore; the latter does not survive at all on induced plants because it cannot grow large enough to reach a minimum viable size for pupation. If the plant is even more toxic, then the parasitized host does not even reach a critical size and all parasitoids die before egression form the host (line c). In some instances, perhaps due to stress caused by parasitism, parasitoids may experience higher mortality on induced plants than their hosts (line d), or else herbivore and parasitoid mortality on non-induced plants does not differ (line e). Many different combinations are possible, depending on the effects of the plant on the herbivore and parasitoid, the parasitoid on the herbivore, and quantitative differences in the required growth of healthy and parasitized hosts
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3197929&req=5

Fig4: Conceptual diagram showing the relationship between herbivore (healthy or parasitized) growth curves and cumulative mortality on food plants that differ in their quality. Solid linea and short dashed linee represent herbivore growth curves on non-induced plants; long dashed lineb, dotted linec and alternating dot-dashed lined lines represent herbivore growth curves on induced plants. In this example, the parasitoid is solitary and the host caterpillar must reach a much smaller critical size to support parasitoid development (left dashed black vertical line) than to successfully pupate (right vertical black dashed line). In this study, induction steepens the mortality curve (lines a, b) reducing survival of both the parasitoid and the herbivore; the latter does not survive at all on induced plants because it cannot grow large enough to reach a minimum viable size for pupation. If the plant is even more toxic, then the parasitized host does not even reach a critical size and all parasitoids die before egression form the host (line c). In some instances, perhaps due to stress caused by parasitism, parasitoids may experience higher mortality on induced plants than their hosts (line d), or else herbivore and parasitoid mortality on non-induced plants does not differ (line e). Many different combinations are possible, depending on the effects of the plant on the herbivore and parasitoid, the parasitoid on the herbivore, and quantitative differences in the required growth of healthy and parasitized hosts
Mentions: In many plant–herbivore associations, early instars are more susceptible to plant allelochemicals and other plant quality characteristics than later instars. In this case, mortality spikes during the first instar and then levels off as the larvae grow and become better able to detoxify and/or excrete the plant’s toxins (Zalucki et al., 2002). However, in our study, the effects of plant quality in WIN plants on the survival of M. brassicae and Mi. mediator were gradual on non-induced and induced plants. Microplitis mediator terminates its relationship with the host at an earlier stage of development (typically L3 or early L4), a point when the host is only approximately 5% of the mass of a fully grown healthy caterpillar (Fig. 4). We also noted that some caterpillars of M. brassicae feeding on WIN plants successfully molted to the 5th instar, but were quite small (<500 mg) and refused to eat after molting, generally perishing within a week or so. Furthermore, whereas the larval development of a healthy M. brassicae caterpillar can last up to 3 weeks or even longer, that of a parasitized caterpillar is less than half of this duration. This means that parasitized caterpillars are under fewer host-growth-related constraints than healthy caterpillars, and this may explain the discrepancy in survival of the host and parasitoid on induced and undamaged WIN leaf tissues, compared with the other strains/populations (Fig. 4). We have provided a conceptual graph (Fig. 4) showing that koinobiont parasitoids, such as Mi. mediator, which terminate their relationship with the host at a very early stage of development (e.g., when it is very small), may be less susceptible to plants of low quality than parastioids that either require the host to grow to a large final size or healthy hosts. This is because the effects of plant toxins may be cumulative over the course of herbivore/parasitoid development, or else because the insects are forced to interact with the plant for a longer period of time.Fig. 4

Bottom Line: Moreover, development was prolonged and biomass was reduced on herbivore-induced plants.However, GS chemistry could not explain the reduced performance on induced plants since only indole GS concentrations increased in response to herbivory, which did not affect insect performance based on multivariate statistics.This result suggests that, in addition to aliphatic GS, other non-GS chemicals are responsible for the decline in insect performance, and that these chemicals affect the parasitoid more strongly than the host.

View Article: PubMed Central - PubMed

Affiliation: Department of Terrestrial Ecology, Netherlands Institute of Ecology, Wageningen, The Netherlands. j.harvey@nioo.knaw.nl

ABSTRACT
The performance of natural enemies, such as parasitoid wasps, is affected by differences in the quality of the host's diet, frequently mediated by species or population-related differences in plant allelochemistry. Here, we compared survival, development time, and body mass in a generalist herbivore, the cabbage moth, Mamestra brassicae, and its solitary endoparasitoid, Microplitis mediator, when reared on two cultivated (CYR and STH) and three wild (KIM, OH, and WIN) populations of cabbage, Brassica oleracea. Plants either were undamaged or induced by feeding of larvae of the cabbage butterfly, Pieris rapae. Development and biomass of M. brassicae and Mi. mediator were similar on both cultivated and one wild cabbage population (KIM), intermediate on the OH population, and significantly lower on the WIN population. Moreover, development was prolonged and biomass was reduced on herbivore-induced plants. However, only the survival of parasitized hosts (and not that of healthy larvae) was affected by induction. Analysis of glucosinolates in leaves of the cabbages revealed higher levels in the wild populations than cultivars, with the highest concentrations in WIN plants. Multivariate statistics revealed a negative correlation between insect performance and total levels of glucosinolates (GS) and levels of 3-butenyl GS. However, GS chemistry could not explain the reduced performance on induced plants since only indole GS concentrations increased in response to herbivory, which did not affect insect performance based on multivariate statistics. This result suggests that, in addition to aliphatic GS, other non-GS chemicals are responsible for the decline in insect performance, and that these chemicals affect the parasitoid more strongly than the host. Remarkably, when developing on WIN plants, the survival of Mi. mediator to adult eclosion was much higher than in its host, M. brassicae. This may be due to the fact that hosts parasitized by Mi. mediator pass through fewer instars, and host growth is arrested when they are only a fraction of the size of healthy caterpillars. Certain aspects of the biology and life-history of the host and parasitoid may determine their response to chemical challenges imposed by the food plant.

Show MeSH
Related in: MedlinePlus