Modulation of plant-mediated interactions between herbivores of different feeding guilds: Effects of parasitism and belowground interactions

Herbivory affects subsequent herbivores, mainly regulated by the phytohormones jasmonic (JA) and salicylic acid (SA). Additionally, organisms such as soil microbes belowground or parasitoids that develop inside their herbivorous hosts aboveground, can change plant responses to herbivory. However, it is not yet well known how organisms of trophic levels other than herbivores, below- and above-ground, alter the interactions between insect species sharing a host plant. Here, we investigated whether the parasitoid Aphidius colemani and different soil microbial communities (created through plant-soil feedbacks) affect the JA and SA signalling pathways in response to the aphid Myzus persicae and the thrips Frankliniella occidentalis, as well as subsequent thrips performance. Our results show that the expression of the JA-responsive gene CaPINII in sweet pepper was more suppressed by aphids than by parasitised aphids. However, parasitism did not affect the expression of CaPAL1, a biosynthetic gene of SA. Furthermore, aphid feeding enhanced thrips performance compared with uninfested plants, but this was not observed when aphids were parasitised. Soils where different plant species were previously grown, did not affect plant responses or the interaction between herbivores. Our study shows that members of the third trophic level can modify herbivore interactions by altering plant physiology.This work and T.V.’s activities were supported by Spanish Ministry of Science and Innovation, (CGL2016-79054), the Open Technology Program of NWO (TTW-13848), and the STSM Cost Action FA1405 funded by the European Union. A.P. research activities were supported by the Netherlands Organisation for Scientific Research (NWO, project no. 870.15.080)

Odours of Plasmodium falciparum-infected participants influence mosquito-host interactions.

Malaria parasites are thought to influence mosquito attraction to human hosts, a phenomenon that may enhance parasite transmission. This is likely mediated by alterations in host odour because of its importance in mosquito host-searching behaviour. Here, we report that the human skin odour profile is affected by malaria infection. We compared the chemical composition and attractiveness to Anopheles coluzzii mosquitoes of skin odours from participants that were infected by Controlled Human Malaria Infection with Plasmodium falciparum. Skin odour composition differed between parasitologically negative and positive samples, with positive samples collected on average two days after parasites emerged from the liver into the blood, being associated with low densities of asexual parasites and the absence of gametocytes. We found a significant reduction in mosquito attraction to skin odour during infection for one experiment, but not in a second experiment, possibly due to differences in parasite strain. However, it does raise the possibility that infection can affect mosquito behaviour. Indeed, several volatile compounds were identified that can influence mosquito behaviour, including 2- and 3-methylbutanal, 3-hydroxy-2-butanone, and 6-methyl-5-hepten-2-one. To better understand the impact of our findings on Plasmodium transmission, controlled studies are needed in participants with gametocytes and higher parasite densities

Molecular quantification of Plasmodium parasite density from the blood retained in used RDTs.

Most malaria-endemic countries are heavily reliant upon rapid diagnostic tests (RDT) for malaria case identification and treatment. RDT previously used for malaria diagnosis can subsequently be used for molecular assays, including qualitative assessment of parasite species present or the carriage of resistance markers, because parasite DNA can be extracted from the blood inside the RDT which remains preserved on the internal components. However, the quantification of parasite density has not previously been possible from used RDT. In this study, blood samples were collected from school-age children in Western Kenya, in the form of both dried blood spots on Whatman filter paper, and the blood spot that is dropped into rapid diagnostic tests during use. Having first validated a robotic DNA extraction method, the parasite density was determined from both types of sample by duplex qPCR, and across a range of densities. The methods showed good agreement. The preservation of both parasite and human DNA on the nitrocellulose membrane inside the RDT was stable even after more than one year's storage. This presents a useful opportunity for researchers or clinicians wishing to gain greater information about the parasite populations that are being studied, without significant investment of resources

Plasmodium-associated changes in human odor attract mosquitoes.

Malaria parasites (Plasmodium) can change the attractiveness of their vertebrate hosts to Anopheles vectors, leading to a greater number of vector-host contacts and increased transmission. Indeed, naturally Plasmodium-infected children have been shown to attract more mosquitoes than parasite-free children. Here, we demonstrate Plasmodium-induced increases in the attractiveness of skin odor in Kenyan children and reveal quantitative differences in the production of specific odor components in infected vs. parasite-free individuals. We found the aldehydes heptanal, octanal, and nonanal to be produced in greater amounts by infected individuals and detected by mosquito antennae. In behavioral experiments, we demonstrated that these, and other, Plasmodium-induced aldehydes enhanced the attractiveness of a synthetic odor blend mimicking "healthy" human odor. Heptanal alone increased the attractiveness of "parasite-free" natural human odor. Should the increased production of these aldehydes by Plasmodium-infected humans lead to increased mosquito biting in a natural setting, this would likely affect the transmission of malaria

Prey and Non-prey Arthropods Sharing a Host Plant: Effects on Induced Volatile Emission and Predator Attraction

It is well established that plants infested with a single herbivore species can attract specific natural enemies through the emission of herbivore-induced volatiles. However, it is less clear what happens when plants are simultaneously attacked by more than one species. We analyzed volatile emissions of lima bean and cucumber plants upon multi-species herbivory by spider mites (Tetranychus urticae) and caterpillars (Spodoptera exigua) in comparison to single-species herbivory. Upon herbivory by single or multiple species, lima bean and cucumber plants emitted volatile blends that comprised mostly the same compounds. To detect additive, synergistic, or antagonistic effects, we compared the multi-species herbivory volatile blend with the sum of the volatile blends induced by each of the herbivore species feeding alone. In lima bean, the majority of compounds were more strongly induced by multi-species herbivory than expected based on the sum of volatile emissions by each of the herbivores separately, potentially caused by synergistic effects. In contrast, in cucumber, two compounds were suppressed by multi-species herbivory, suggesting the potential for antagonistic effects. We also studied the behavioral responses of the predatory mite Phytoseiulus persimilis, a specialized natural enemy of spider mites. Olfactometer experiments showed that P. persimilis preferred volatiles induced by multi-species herbivory to volatiles induced by S. exigua alone or by prey mites alone. We conclude that both lima bean and cucumber plants effectively attract predatory mites upon multi-species herbivory, but the underlying mechanisms appear different between these species

Scientists' warning on climate change and insects

Climate warming is considered to be among the most serious of anthropogenic stresses to the environment, because it not only has direct effects on biodiversity, but it also exacerbates the harmful effects of other human-mediated threats. The associated consequences are potentially severe, particularly in terms of threats to species preservation, as well as in the preservation of an array of ecosystem services provided by biodiversity. Among the most affected groups of animals are insects—central components of many ecosystems—for which climate change has pervasive effects from individuals to communities. In this contribution to the scientists' warning series, we summarize the effect of the gradual global surface temperature increase on insects, in terms of physiology, behavior, phenology, distribution, and species interactions, as well as the effect of increased frequency and duration of extreme events such as hot and cold spells, fires, droughts, and floods on these parameters. We warn that, if no action is taken to better understand and reduce the action of climate change on insects, we will drastically reduce our ability to build a sustainable future based on healthy, functional ecosystems. We discuss perspectives on relevant ways to conserve insects in the face of climate change, and we offer several key recommendations on management approaches that can be adopted, on policies that should be pursued, and on the involvement of the general public in the protection effort

Sex determination in the Hymenoptera

The dominant and ancestral mode of sex determination in the Hymenoptera is arrhenotokous parthenogenesis, in which diploid females develop from fertilized eggs and haploid males develop from unfertilized eggs. We discuss recent progress in the understanding of the genetic and cytoplasmic mechanisms that make arrhenotoky possible. The best-understood mode of sex determination in the Hymenoptera is complementary sex determination (CSD), in which diploid males are produced under conditions of inbreeding. The gene mediating CSD has recently been cloned in the honey bee and has been named the complementary sex determiner. However, CSD is only known from 4 of 21 hymenopteran superfamilies, with some taxa showing clear evidence of the absence of CSD. Sex determination in the model hymenopteran Nasonia vitripennis does not involve CSD, but it is consistent with a form of genomic imprinting in which activation of the female developmental pathway requires paternally derived genes. Some other hymenopterans are not arrhenotokous but instead exhibit thelytoky or paternal genome elimination

Range-expansion in processionary moths and biological control

Global climate change is resulting in a wide range of biotic responses, including changes in diel activity and seasonal phenology patterns, range shifts polewards in each hemisphere and/or to higher elevations, and altered intensity and frequency of interactions between species in ecosystems. Oak (Thaumetopoea processionea) and pine (T. pityocampa) processionary moths (hereafter OPM and PPM, respectively) are thermophilic species that are native to central and southern Europe. The larvae of both species are gregarious and produce large silken ‘nests’ that they use to congregate when not feeding. During outbreaks, processionary caterpillars are capable of stripping foliage from their food plants (oak and pine trees), generating considerable economic damage. Moreover, the third to last instar caterpillars of both species produce copious hairs as a means of defence against natural enemies, including both vertebrate and invertebrate predators, and parasitoids. These hairs contain the toxin thaumetopoein that causes strong allergic reactions when it comes into contact with human skin or other membranes. In response to a warming climate, PPM is expanding its range northwards, while OPM outbreaks are increasing in frequency and intensity, particularly in northern Germany, the Netherlands, and southern U.K., where it was either absent or rare previously. Here, we discuss how warming and escape from co-evolved natural enemies has benefitted both species, and suggest possible strategies for biological control

raw data on gene expression and thrips performance on sweet pepper plants

This excel data file contains one worksheet per figure presented in the manuscript and in the supplementary information. Variable names, and levels are explained in the last worksheet, named "readme