RESUMEN
BACKGROUND: Predicting the host range of biocontrol agents is important for the safe and effective implementation of biocontrol of weeds. In this study, we examined the phylogenetic pattern of host selection and acceptance by the biocontrol beetle, Cassida rubiginosa. The beetle was released in New Zealand for control of Cirsium arvense, its primary host plant, but has potential to attack many Cardueae (thistles and knapweeds) species. We conducted a series of no-choice and choice experiments and modelled the responses of Cassida rubiginosa in relation to phylogenetic distance from Cirsium arvense. RESULTS: The olfactory recognition (single odour) and preference (two odours) of the beetle showed a significant phylogenetic relationship. These relationships showed a high degree of correlation with 66.9% of the variation in olfactory recognition and 82.8% of the variation in olfactory preference explained by phylogeny. Where the beetle could contact plants, under no-choice conditions there was no phylogenetic pattern to host plant acceptance. However, under choice conditions, phylogenetic distance was a strong predictor of feeding and oviposition preference. These relationships showed a high degree of correlation, with 63.4% of the variation in feeding preference, and 89.0% of the variation in oviposition preference, explained by phylogeny. CONCLUSIONS: As far as we are aware, this is the first demonstration of an herbivorous insect that exhibits a phylogenetic pattern to olfactory host plant selection. Host plant utilisation by Cassida rubiginosa in New Zealand will be mostly restricted to Cirsium and Carduus species, with minimal potential for impact on other Cardueae weeds. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
RESUMEN
The majority of herbivorous insects are specialized feeders restricted to a plant family, genus, or species. The evolution of specialized insect-plant interactions is generally considered to be a result of trade-offs in fitness between possible hosts. Through the course of natural selection, host plants that maximize insect fitness should result in optimal, specialized, insect-plant associations. However, the extent to which insects are tracking plant phylogeny or key plant traits that act as herbivore resistance or acceptance characters is uncertain. Thus, with regard to the evolution of host plant specialization, we tested if insect performance is explained by phylogenetic relatedness of potential host plants, or key plant traits that are not phylogenetically related. We tested the survival (naive first instar to adult) of the oligophagous leaf-feeding beetle, Cassida rubiginosa, on 16 selected representatives of the Cardueae tribe (thistles and knapweeds), including some of the worst weeds in temperate grasslands of the world in terms of the economic impacts caused by lost productivity. Leaf traits (specific leaf area, leaf pubescence, flavonoid concentration, carbon and nitrogen content) were measured as explanatory variables and tested in relation to survival of the beetle, and the phylogenetic signal of the traits were examined. The survival of C. rubiginosa decreased with increasing phylogenetic distance from the known primary host plant, C. arvense, suggesting that specialization is a conserved character, and that insect host range, to a large degree is constrained by evolutionary history. The only trait measured that clearly offered some explanatory value for the survival of C. rubiginosa was specific leaf area. This trait was not phylogenetically dependant, and when combined with phylogenetic distance from C. arvense gave the best model explaining C. rubiginosa survival. We conclude that the specialization of the beetle is explained by a combination of adaptation to an optimal host plant over evolutionary time, and key plant traits such as specific leaf area that can restrict or broaden host utilization within the Cardueae lineage. The phylogenetic pattern of C. rubiginosa fitness will aid in predicting the ability of this biocontrol agent to control multiple Cardueae weeds.
RESUMEN
Defoliation has frequently been proposed as a means of controlling Cirsium arvense (L.) Scop. (Californian thistle, Canada thistle, creeping thistle, perennial thistle), an economically damaging pastoral weed in temperate regions of the world, but its optimization has remained obscure. We developed a matrix model for the population dynamics of C. arvense in sheep-grazed pasture in New Zealand that accounts for the effects of aerial shoot defoliation on a population's photosynthetic opportunity and consequential overwintered root biomass, enabling mowing regimes varying in the seasonal timing and frequency of defoliation to be compared. The model showed that the long-term population dynamics of the weed is influenced by both the timing and frequency of mowing; a single-yearly mowing, regardless of time of year, resulted in stasis or population growth, while in contrast, 14 of 21 possible twice-yearly monthly mowing regimes, mainly those with mowing in late spring, summer, and early autumn, resulted in population decline. Population decline was greatest (with population density halving each year) with twice-yearly mowing either in late spring and late summer, early summer and late summer, or early summer and early autumn. Our results indicate that mowing can be effective in reducing populations of C. arvense in pasture in the long term if conducted twice each year when the initial mowing is conducted in mid spring followed by a subsequent mowing from mid summer to early autumn. These mowing regimes reduce the photosynthetic opportunity of the C. arvense population and hence its ability to form the overwintering creeping roots upon which population growth depends.
RESUMEN
Plants emit specific blends of volatile organic compounds (VOCs) that serve as multitrophic, multifunctional signals. Fungi colonizing aboveground (AG) or belowground (BG) plant structures can modify VOC patterns, thereby altering the information content for AG insects. Whether AG microbes affect the emission of root volatiles and thus influence soil insect behaviour is unknown. The endophytic fungus Neotyphodium uncinatum colonizes the aerial parts of the grass hybrid Festuca pratensis × Lolium perenne and is responsible for the presence of insect-toxic loline alkaloids in shoots and roots. We investigated whether endophyte symbiosis had an effect on the volatile emission of grass roots and if the root herbivore Costelytra zealandica was able to recognize endophyte-infected plants by olfaction. In BG olfactometer assays, larvae of C. zealandica were more strongly attracted to roots of uninfected than endophyte-harbouring grasses. Combined gas chromatography-mass spectrometry and proton transfer reaction-mass spectrometry revealed that endophyte-infected roots emitted less VOCs and more CO2. Our results demonstrate that symbiotic fungi in plants may influence soil insect distribution by changing their behaviour towards root volatiles. The well-known defensive mutualism between grasses and Neotyphodium endophytes could thus go beyond bioactive alkaloids and also confer protection by being chemically less apparent for soil herbivores.
