Tansy plants (Tanacetum vulgare L.) exhibit high chemical variation, particularly in mono- and sesquiterpenes that are stored in specialised glands on the plant surface. In the present work we investigated the effects of terpene chemotypes on Metopeurum fuscoviride, an aphid species specialised on tansy, and their tending ants, at the field scale. Previous studies have chemotyped tansy by assessing dominant compounds; here we propose a method of chemotyping using all volatile compounds that are likely emitted from the storage glands. The analysis is based on two extraction methods: GC-MS analysis of leaf hexane extracts and SBSE analysis of headspace emissions. In an initial screening we identified the subset of compounds present in both chemical patterns, labelled as ‘compounds likely emitted from storage’. In a large field survey we could show that the putative chemotypic emission pattern from storage pools significantly affected the early aphid colonisation of tansy. Moreover, the statistical analyses revealed that minor compounds exerted a stronger influence on aphid and tending-ant presence than dominant compounds. Overall we demonstrated that within the enormous chemotypic variation of terpenes in tansy plants, chemical signatures of volatile terpenes can be related to the occurrence of insects on individual plants in the field.
1. Spatially distributed resources can lead to the formation of metapopulations, where individual subpopulations are often small and can experience frequent local extinction events followed by recolonisation. An example of terrestrial metapopulations are specialised phytophagous insects on their patchily distributed host plants.2. The present study investigated the population dynamics of a specialised aphid (Metopeurum fuscoviride) on its patchily distributed host plant (Tanacetum vulgare) and associated community of mutualistic ants and predators in a small-scale field site. Furthermore, aphid habitat differences (plant size, C/N ratio, location and surrounding vegetation) were quantified, and seasonal timing and precipitation were considered.3. Seasonal timing and precipitation both had effects on aphid colonisation, extinction events and aphid colony persistence. Towards the end of the season, and after higher precipitation, aphid colonisation events decreased and extinction events increased. Plant size and location as well as aphid within-field dispersal determined the spatio-temporal distribution of aphid colonies.4. Mutualistic ants (Lasius niger and Myrmica rubra) increased the chance of establishment of aphid colonies. However, when M. rubra was tending, aphid colony persistence was reduced. Aphid persistence and extinction were dependent on aphid abundance, as a higher colony size reduced the probability of extinction by predation.5. The results emphasise the importance of dispersal limitation, population growth and the presence of mutualists when studying the spatio-temporal dynamics of tansy aphids, particularly in a small-scale field site.
Forisomes are protein polymers found in leguminous plants that have the remarkable ability to undergo reversible "muscle-like" contractions in the presence of divalent cations and in extreme pH environments. To gain insight into the molecular basis of forisome structure and assembly, we used confocal laser scanning microscopy to monitor the assembly of fluorescence-labeled artificial forisomes in real time, revealing two distinct assembly processes involving either fiber elongation or fiber alignment. We also used scanning and transmission electron microscopy and X-ray diffraction to investigate the ultrastructure of forisomes, finding that individual fibers are arranged into compact fibril bundles that disentangle with minimal residual order in the presence of calcium ions. To demonstrate the potential applications of artificial forisomes, we created hybrid protein bodies from forisome subunits fused to the B-domain of staphylococcal protein A. This allowed the functionalization of the artificial forisomes with antibodies that were then used to target forisomes to specific regions on a substrate, providing a straightforward approach to develop forisome-based technical devices with precise configurations. The functional contractile properties of forisomes are also better preserved when they are immobilized via affinity reagents rather than by direct contact to the substrate. Artificial forisomes produced in plants and yeast therefore provide an ideal model for the investigation of forisome structure and assembly and for the design and testing of tailored artificial forisomes for technical applications.
Cascading effects in ecological systems acting across three or more trophic levels can be either of a resource‐based (bottom‐up) or natural enemy‐based (top‐down) nature. But, due to their complexity, these effects are often considered separately and their relative strength, acting simultaneously, remains unknown. In a semi‐natural field experiment using tansy (Tanacetum vulgare L.) and the specialised tansy‐aphid Metopeurum fuscoviride Stroyan as a model system, we compared the effects of four distinct plant chemotypes (i.e., bottom‐up), defined by the bouquet of their volatile terpenoids, on aphid population dynamics by manipulating the presence/absence of mutualistic ants and presence/absence of naturally occurring predators (i.e., top‐down). Predators reduced aphid abundance and colony survival but did not reduce initial growth rate due to a time‐lag until predators arrived on the plants. Ants directly benefited initial aphid growth rates and abundance, even in the absence of predators, but not the number of days an aphid colony persisted on the plant. Plant chemotype directly affected aphid growth rate and final abundances across the different plants and indirectly affected the abundances of tending ants and predators through effects on aphids. We found that tending ants were more abundant on one plant chemotype. Although ant abundance did not affect aphid population development, it became clear that ants had a preference towards aphids on certain chemotypes. However, a higher number of predators led to a lower number of aphids. The results confirm the importance of plant chemical variation, acting through multiple effects on many species in arthropod communities, and support results from field studies. In a natural population, with a diverse selection of host‐plant variants, aphid populations and their interacting species can therefore be structured at the level of an individual plant. Specialist aphids on patchily distributed host plants can exhibit metacommunity dynamics at very local scales. Plant within‐species variation within a local population is often ignored in metacommunity ecology, yet our work shows that this can have strong effects on insect–ant–natural enemy dynamics, and therefore, future research should incorporate this into current theory and experimental studies. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13227/suppinfo is available for this article.
Honeydew is a sugar-rich resource excreted by many hemipteran species and is a key food source for other insect species such as ants and parasitoid wasps. Here, we evaluated the nutritional value of 14 honeydews excreted by 13 aphid species for the generalist aphid parasitoid Lysiphlebus testaceipes to test a series of hypotheses concerning variation in the nutritional value of honeydew. There was a positive correlation between the body sugar content of honeydew-fed parasitoids and their longevity. This information is valuable for biological control researchers because it demonstrates that the nutritional state of honeydew-fed parasitoids in the wild can indicate their fitness, independently of the honeydew source they have fed on. Although the carbohydrate content and longevity of L. testaceipes differed greatly among the different honeydews, we did not find a significant effect of aphid or host plant phylogeny on these traits. This result suggests that honeydew is evolutionarily labile and may be particularly subject to ecological selection pressures. This becomes apparent when considering host aphid suitability: Schizaphis graminum, one of the most suitable and commonly used hosts of L. testaceipes, produced honeydew of the poorest quality for the parasitoid whereas Uroleucon sonchi, one of the few aphids tested that cannot be parasitized by L. testaceipes, excreted the honeydew with the highest nutritional value. These data are consistent with the hypothesis that hemipterans are subject to selection pressure to minimize honeydew quality for the parasitoids that attack them.
Background Tansy plants (Tanacetum vulgare L.) are known for their high intraspecific chemical variation, especially of volatile organic compounds (VOC) from the terpenoid compound group. These VOCs are closely involved in plant-insect interactions and, when profiled, can be used to classify plants into groups known as chemotypes. Tansy chemotypes have been shown to influence plant-aphid interactions, however, to date no information is available on the response of different tansy chemotypes to simultaneous herbivory by more than one insect species. Results Using a multi-cuvette system, we investigated the responses of five tansy chemotypes to feeding by sucking and/or chewing herbivores (aphids and caterpillars; Metopeurum fuscoviride Stroyan and Spodoptera littoralis Boisduval). Herbivory by caterpillars following aphid infestation led to a plant chemotype-specific change in the patterns of terpenoids stored in trichome hairs and in VOC emissions. The transcriptomic analysis of a plant chemotype represents the first de novo assembly of a transcriptome in tansy and demonstrates priming effects of aphids on a subsequent herbivory. Overall, we show that the five chemotypes do not react in the same way to the two herbivores. As expected, we found that caterpillar feeding increased VOC emissions, however, a priori aphid infestation only led to a further increase in VOC emissions for some chemotypes. Conclusions We were able to show that different chemotypes respond to the double herbivore attack in different ways, and that pre-treatment with aphids had a priming effect on plants when they were subsequently exposed to a chewing herbivore. If neighbouring chemotypes in a field population react differently to herbivory/dual herbivory, this could possibly have effects from the individual level to the group level. Individuals of some chemotypes may respond more efficiently to herbivory stress than others, and in a group environment these “louder” chemotypes may affect the local insect community, including the natural enemies of herbivores, and other neighbouring plants.
Plants exhibit impressive genetic and chemical diversity, not just between species but also within species, and the importance of plant intraspecific variation for structuring ecological communities is well known. When there is variation at the local population level, this can create a spatially heterogeneous habitat for specialised herbivores potentially leading to non‐random distribution of individuals across host plants. Plant variation can affect herbivores directly and indirectly via a third species, resulting in variable herbivore growth rates across different host plants. Herbivores also exhibit within‐species variation, with some genotypes better adapted to some plant variants than others. We genotyped aphids collected across 2 years from a field site containing ~200 patchily distributed host plants that exhibit high chemical diversity. The distribution of aphid genotypes, their ant mutualists, and other predators was assessed across the plants. We present evidence that the local distribution of aphid (Metopeurum fuscoviride) genotypes across host‐plant individuals is associated with variation in the plant volatiles (chemotypes) and non‐volatile metabolites (metabotypes) of their host plant tansy (Tanacetum vulgare). Furthermore, these interactions in the field were influenced by plant‐host preferences of aphid‐mutualist ants. Our results emphasise that plant intraspecific variation can structure ecological communities not only at the species level but also at the genetic level within species and that this effect can be enhanced through indirect interactions with a third species.
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