Differential Performance of a Specialist and Two Generalist Herbivores and Their Parasitoids on Plantago lanceolata

Abstract

The ability to cope with plant defense chemicals differs between specialist and generalist species. In this study, we examined the effects of the concentration of the two main iridoid glycosides (IGs) in Plantago lanceolata, aucubin and catalpol, on the performance of a specialist and two generalist herbivores and their respective endoparasitoids. Development of the specialist herbivore Melitaea cinxia was unaffected by the total leaf IG concentration in its host plant. By contrast, the generalist herbivores Spodoptera exigua and Chrysodeixis chalcites showed delayed larval and pupal development on plant genotypes with high leaf IG concentrations, respectively. This result is in line with the idea that specialist herbivores are better adapted to allelochemicals in host plants on which they are specialized. Melitaea cinxia experienced less post-diapause larval and pupal mortality on its local Finnish P. lanceolata than on Dutch genotypes. This could not be explained by differences in IG profiles, suggesting that M. cinxia has adapted in response to attributes of its local host plants other than to IG chemistry. Development of the specialist parasitoid Cotesia melitaearum was unaffected by IG variation in the diet of its host M. cinxia, a response that was concordant with that of its host. By contrast, the development time responses of the generalist parasitoids Hyposoter didymator and Cotesia marginiventris differed from those of their generalist hosts, S. exigua and C. chalcites. While their hosts developed slowly on high-IG genotypes, development time of H. didymator was unaffected. Cotesia marginiventris actually developed faster on hosts fed high-IG genotypes, although they then had short adult longevity. The faster development of C. marginiventris on hosts that ate high-IG genotypes is in line with the “immunocompromized host” hypothesis, emphasizing the potential negative effects of toxic allelochemicals on the host’s immune response.

Impact of the dual defence system of Plantago lanceolata (Plantaginaceae) on performance, nutrient utilisation and feeding choice behaviour of Amata mogadorensis larvae (Lepidoptera, Erebidae)

“…Due to the protein-denaturing capacity that fresh leaves exhibit after destroying the compartmentalisation of plant β-glucosidases and iridoid glycosides , we expected that larvae should perform better on artificial diets with significantly reduced enzymatic activities in comparison to fresh leaves with high β-glucosidase activities. Based on findings of previous studies (Harvey et al, 2005;Reudler et al, 2011) and as predicted by the optimal defence hypothesis (McCall and Fordyce, 2010;McKey, 1974McKey, , 1979Rhoades, 1979), we expected higher concentrations of iridoid glycosides (as in young leaf diets) to reduce larval growth rates more than lower iridoid glycoside concentration (as in old-leaf diet), thus providing the plant with an increased resistance against herbivores. To functionally relate the toxic mechanism of hydrolysed iridoid glycosides to a reduced larval performance, we determined the nutrient utilisation of larvae reared on the different diets.…”

Performance of secondary parasitoids on chemically defended and undefended hosts

“…Though the need for defence might be presumed to decrease at higher trophic levels, developing G. agilis potentially fall prey to tertiary parasitoids, adults may be prey to spiders and other arthropods, and for any animal there is the need for generalized defence against disease. Iridoid glycosides are associated with defence against all of these enemies in lower trophic level species (Theodoratus & Bowers 1999;Biere et al, 2004;Reudler et al 2011), and should function in the same way at higher trophic levels. Finnish G. agilis concentrated more of the iridoid glycoside catalpol than did G. agilis from the Netherlands.…”

“…Notably, the idea that higher trophic level generalists are deterred by plantderived chemicals sequestered by their hosts is well supported for predators (Montllor, Bernays, & Cornelius 1991;Dyer & Bowers 1996;Hristov & Conner 2005;Baden & Dobler 2009), but is less clear for endoparasitoids (Reudler, Biere, Harvey, & van Nouhuys 2011). This may be because regardless of host range endoparasitoids have a more intimate physiological relationship with their prey than do predators, and thus must be better able to detoxify or avoid plantderived toxins (Ode 2006;Smilanich, Dyer, Chambers, & Bowers 2009).…”

Microbial Root Mutualists Affect the Predators and Pathogens of Herbivores above Ground: Mechanisms, Magnitudes, and Missing Links

“…For example, hydrolysable tannins in quaking aspen (Populus tremuloides) correlate negatively with immune defense in the autumnal moth Epirrita autumnata (Haviola et al, 2007), and high iridoid glycoside concentrations in P. lanceolata compromise immune responses in the common buckeye caterpillar Junonia coenia (Smilanich et al, 2009). Lower immune defense can lead to higher performance of parasitoids (Reudler et al, 2011;Kos et al, 2012). While microbial root mutualists affect the expression of these (and other) secondary chemicals (tannins, Beyeler and Heyser, 1997; iridoid glycosides, Bennett et al, 2009), to our knowledge, no study has directly explored effects of soil organisms on host insect immunity through changes in secondary chemistry.…”