Leaf traits of congeneric host plants explain differences in performance of a specialist herbivore

Abstract

1. Within the host range of herbivorous insects, performance hierarchies are often correlated with relatedness to a primary host plant, as plant traits are phylogenetically conserved. Therefore, it was hypothesised that differences in herbivore performance on closely related plant species are due to resistance traits that vary in magnitude, rather than in the nature of the traits.2. This hypothesis was tested by manipulating putative resistance traits of three congeneric thistle species (Cirsium arvense, Cirsium palustre, and Cirsium vulgare) and assessing the performance of the oligophagous, leaf-feeding beetle, Cassida rubiginosa. Measurements were done of survival, weight gain, and development time of the beetle on its primary host, C. arvense, and two alternative hosts under low and high nutrient availability, and on shaved and unshaved leaves.3. Survival of C. rubiginosa was strongly dependent on plant species with final mean survival rates of 47%, 16%, and 8% on C. arvense, C. palustre, and C. vulgare, respectively. Survival was primarily explained by leaf trichome densities, and to a lesser extent by specific leaf area. Leaf flavonoid concentrations did not explain differences in beetle survival, and there were no differences in beetle weight gain or development time of individuals that survived to adulthood.4. No beetles survived on unshaved (hairy) C. vulgare plants, but manipulating leaf trichome densities of the thistle species by shaving the leaves moderated the plant-specific resistance, and equalised the survival rates. Survival of C. rubiginosa on alternative congeneric hosts was explained by a common physical resistance trait that varied in magnitude.

Genetically Based Trait Differentiation but Lack of Trade-offs between Stress Tolerance and Performance in Introduced Canada Thistle

“…The EICA hypothesis predicts that introduced plant species will be released from native specialist predators, but here we simulated herbivory, which might not accurately represent the effects of specialist herbivores ( Blossey and Notzold, 1995 ). For example, leaf trichome/spine densities have been shown to reduce the performance of a specialized herbivore on Canada thistle ( Cripps et al., 2015 ), but we did not assay variation in leaf trichome/spine densities in our experiment. Alternatively, it might be that tolerance to different stresses in Canada thistle is largely uncoupled from performance, similar to that reported for introduced populations of diffuse knapweed ( Turner et al., 2014 ).…”

Evolution of Specialization of Cassida rubiginosa on Cirsium arvense (Compositae, Cardueae)

“…This also conferred with our hypothesis that defensive traits, in addition to phylogenetic relationship, affect insect survival. Plant species with high SLA have many features conducive to herbivore feeding, such as lower dry matter, faster growth rate, and reduced leaf toughness ( Salgado-Luarte and Gianoli, 2010 ), and this trait was shown to be an important factor explaining survival of Cassida on plants congeneric to C. arvense ( Cripps et al, 2015 ). The only plant trait found to have a clear phylogenetic signal was leaf pubescence, but this trait was not related to Cassida survival.…”

“…The fact that leaf pubescence showed a phylogenetic signal is likely an artifact of low sample size since this trait is common in plant species across the Cardueae subtribes ( Susanna and Garcia-Jacas, 2007 ), and is therefore unlikely to be part of the underlying phylogenetic explanation for Cassida survival. Leaf pubescence is known to provide resistance against most types of insect herbivores, including both generalist and specialist feeders ( Hanley et al, 2007 ), and previously trichome density was found to be an important factor determining survival rates of Cassida on plants congeneric to C. arvense ( Cripps et al, 2015 ). In the present study, leaf pubescence was measured as a proportion of total leaf dry weight and specific pubescence structures that might differently affect Cassida survival were not distinguished.…”

“…Previously, the fitness of the leaf-feeding beetle, Cassida rubiginosa , was tested in relation to plant defensive traits in a phylogenetically controlled experiment with three Cirsium species ( Cripps et al, 2015 ). The beetle is classified as an oligophagous feeder restricted to plants in the tribe Cardueae (thistles and knapweeds), but has a well-known primary host plant, Cirsium arvense ( Zwölfer and Eichhorn, 1966 ).…”

“…Flavonoids are known to act as feeding deterrents or stimulants in many insect–plant systems, depending on their concentration ( Harborne and Grayer, 1993 ; Simmonds, 2001 ), and are the predominant secondary chemical group in the Cardueae ( Wagner, 1977 ; Jordon-Thaden and Louda, 2003 ). Similarly, leaf pubescence and toughness are well documented as herbivore resistance traits ( Hanley et al, 2007 ), and were identified as key defensive traits reducing Cassida fitness on congeners of C. arvense ( Cripps et al, 2015 ). This raised the question of whether or not host plant utilization within the Cardueae was driven by key defensive traits (i.e., any given Cardueae species could be equally suitable, depending on key traits), or if there was a broad phylogenetic pattern explaining host plant specialization (i.e., adaptation to an optimal host over evolutionary time, independent of defensive traits).…”