Specific plant associations may decrease (associational resistance, AR) or increase (associational susceptibility, AS) the likelihood of detection by, and/or vulnerability to, herbivores. We discuss presumed mechanisms leading to AR and AS, suggest others, and conduct meta-analyses on plant and herbivore traits affecting AR and AS, and the effects of habitat. Specific plant associations determine the likelihood of detection and/or vulnerability of focal plants to herbivores. AS is more likely with insects and AR more likely with mammals. Unpalatable neighbors increase the likelihood of AR. An herbivore's feeding guild, diet breadth, and habitat type do not influence the likelihood of AR or AS. The effectiveness of AR in reducing herbivore abundance is independent of whether neighboring plants are within a plot of focal crops or along the edge of a plot. AR and AS may be applicable to associations among herbivores, and may be appropriately studied from a landscape perspective.
SignificanceDecades of research have fostered the now-prevalent assumption that noncrop habitat facilitates better pest suppression by providing shelter and food resources to the predators and parasitoids of crop pests. Based on our analysis of the largest pest-control database of its kind, noncrop habitat surrounding farm fields does affect multiple dimensions of pest control, but the actual responses of pests and enemies are highly variable across geographies and cropping systems. Because noncrop habitat often does not enhance biological control, more information about local farming contexts is needed before habitat conservation can be recommended as a viable pest-suppression strategy. Consequently, when pest control does not benefit from noncrop vegetation, farms will need to be carefully comanaged for competing conservation and production objectives.
The Colorado potato beetle is one of the most challenging agricultural pests to manage. It has shown a spectacular ability to adapt to a variety of solanaceaeous plants and variable climates during its global invasion, and, notably, to rapidly evolve insecticide resistance. To examine evidence of rapid evolutionary change, and to understand the genetic basis of herbivory and insecticide resistance, we tested for structural and functional genomic changes relative to other arthropod species using genome sequencing, transcriptomics, and community annotation. Two factors that might facilitate rapid evolutionary change include transposable elements, which comprise at least 17% of the genome and are rapidly evolving compared to other Coleoptera, and high levels of nucleotide diversity in rapidly growing pest populations. Adaptations to plant feeding are evident in gene expansions and differential expression of digestive enzymes in gut tissues, as well as expansions of gustatory receptors for bitter tasting. Surprisingly, the suite of genes involved in insecticide resistance is similar to other beetles. Finally, duplications in the RNAi pathway might explain why Leptinotarsa decemlineata has high sensitivity to dsRNA. The L. decemlineata genome provides opportunities to investigate a broad range of phenotypes and to develop sustainable methods to control this widely successful pest.
Determining relative strengths of trophic links is critical for ranking predators for conservation biological control. Molecular gut-content analysis enables ranking by incidence of prey remains in the gut, but differential digestive rates bias such rankings toward predators with slower rates. This bias can be reduced by indexing each predator's half-life to that of the middle-most half-life in a predator complex. We demonstrate this with data from key species in the predator complex of Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae), comprising adults and immatures of four taxonomically diverse species. These animals display order-of-magnitude variation in detectability half-life for the cytochrome oxidase I DNA sequence of a single CPB egg: from 7.0 h in larval Coleomegilla maculata (DeGeer) (Coleoptera: Coccinellidae) to 84.4 h in nymphal Perillus bioculatus (Fabricius) (Hemiptera: Pentatomidae). The raw species-specific incidence of L. decemlineata DNA in the guts of 351 field-collected predators ranged from 11 to 95%, ranking them as follows: C. maculata adults < Lebia grandis Hentz (Coleoptera: Carabidae) adults < Podisus maculiventris (Say) (Hemiptera: Pentatomidae) adults < P. maculiventris nymphs < P. bioculatus adults < P. bioculatus nymphs. Half-life adjustment reorders the rankings: C. maculata adults < P. bioculatus adults < P. bioculatus nymphs < P. maculiventris nymphs < L. grandis adults < P. maculiventris adults. These changes in status demonstrate the value of half-lifeadjusted molecular gut-content data for ranking predators. This is the first study to measure prey detectability half-lives for the key arthropod predators of a major insect pest, and to use them to evaluate the relative impact of all adults and immatures in this predator complex.
The process of selecting certain desirable traits for plant breeding may compromise other potentially important traits, such as defences against pests; however, specific phenotypic changes occurring over the course of domestication are unknown for most domesticated plants. Cranberry (Vaccinium macrocarpon) offers a unique opportunity to study such changes: its domestication occurred recently, and we have access to the wild ancestors and intermediate varieties used in past crosses. In order to investigate whether breeding for increased yield and fruit quality traits may indirectly affect anti-herbivore defences, the chemical defences have been examined of five related cranberry varieties that span the history of domestication against a common folivore, the gypsy moth (Lymantria dispar). Direct defences were assessed by measuring the performance of gypsy moth caterpillars and levels of phenolic compounds in leaves, and indirect defences by assaying induced leaf volatile emissions. Our results suggest that breeding in cranberry has compromised plant defences: caterpillars performed best on the derived NJS98-23 (the highest-yielding variety) and its parent Ben Lear. Moreover, NJS98-23 showed reduced induction of volatile sesquiterpenes, and had lower concentrations of the defence-related hormone cis-jasmonic acid (JA) than ancestral varieties. However, induced direct defences were not obviously affected by breeding, as exogenous JA applications reduced caterpillar growth and increased the amounts of phenolics independent of variety. Our results suggest that compromised chemical defences in high-yielding cranberry varieties may lead to greater herbivore damage which, in turn, may require more intensive pesticide control measures. This finding should inform the direction of future breeding programmes.
Many insect pests utilize plant volatiles for host location and untangling the mechanisms of this process can provide tools for pest management. Numerous experimental results have been published on the effect of plant volatiles on insect pests. We used a meta-analysis to summarize this knowledge and to look for patterns. Our goal was to identify herbivore and plant traits that might explain the herbivores' behavioral response to plant volatiles in field applications. We scored a total of 374 unique plant volatile-insect herbivore interactions obtained from 34 published studies investigating 50 herbivore pest species. Attractants had a significant effect on insect herbivore abundance but repellents did not; this latter result could be a result of the comparatively small number of field studies that tested plant volatiles as repellents (3%). Females were significantly more attracted to plant volatile baits than males. The diet breadth of herbivores was independent of a behavioral response to plant volatiles, but more case studies show effects of volatiles on chewers, followed by wood-borers and sap-feeders. There are more demonstrations of attraction to plant volatiles in Lepidoptera than in Thysanoptera. The method of plant volatile application had a significant effect on herbivore abundance and increasing the number of chemicals in individual baits attracted more herbivores. The magnitude of the response of herbivores to plant volatiles in forest and agricultural habitats was similar. We explore consistent patterns and highlight areas needing research in using plant volatiles to manage insect pests.
The increasing resistance to neonicotinoid insecticides raises concerns for the continued effective management of Colorado potato beetles in potatoes and highlights the need for more rigorous practice of integrated pest management methods.
Western honey bees (Apis mellifera) are dominant crop pollinators, and access to summer forage is a critical factor influencing colony health in agricultural landscapes. In many temperate agricultural regions, honey bees forage extensively from non-native plants during the summer, but it is unclear whether the use of these species is due to honey bee preference for these plants or is a result of their relative abundance. The foraging choices made by native bees that have evolved with native plants can reveal the seasonal availability of native plant pollens, and so we quantified the pollen collected by 181 wild bee species native to Michigan. Pollen was also trapped from honey bee colonies during the summer to confirm the peak period of non-native pollen collection in this region. Across the state, the generic richness of native pollens collected by wild bees peaked in May before linearly declining into September. Wild social and solitary bees collected a similar proportion of their pollen from non-native plants from April to July, but during August and September social bees collected a significantly greater proportion from non-natives. At a local scale, honey bees collected the majority of their pollen from non-native plants between 4 July and 21 August, with the same trend seen in both social and solitary bees. Across the region, a significantly greater proportion of the solitary bee species that peak during this time are specialists, most of which collect from native plant species that are little utilized by social bees for pollen, such as Dasiphora, Helianthus, Physalis, and Vernonia. Our results suggest that Michigan has relatively few native flowering resources during the height of the summer, and that many of those which flower during this time are used primarily by specialized solitary bee species rather than the social bee community, including honey bees. As a result, non-native plant species with a late summer flowering phenology fill a forage gap and thus can contribute to the diet of both honey bees and generalist wild bees during this time, despite the well-documented negative impacts of these species on native plant communities.
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