The invisible interplay between herbivorous insects and their monitoring ants on a chemically diverse plant

Plants exhibit impressive genetic and chemical diversity, and this variation is important for structuring ecological communities. A recent paper in the Journal of Animal Ecology investigated this with regard to aphids and their host-plant tansy. Lead author Dr Sharon Zytynska from the Technical University of Munich tells us more about this study.

The perennial tansy plant (Tanacetum vulgare) grows steadily throughout the spring, producing heads of bright yellow flowers in the summer. It is native to temperate Europe and Asia, but invasive in North America. It has a long history of cultivation for medicinal uses (although worries about its toxicity have reduced its use), and has even had a moment of fame in the popular Game of Thrones series as one ingredient of ‘moon tea’ used to prevent or abort pregnancies.

Tansy aphids

Tansy aphids feeding on plant leaves (left), the distinctive yellow flowers of this plant in summer (middle), and in the field collecting data (right) (Photos: S Zytynska)

Tansy plants synthesise many different chemical compounds known as essential oils, which are stored in specialised cells on the plant’s leaves. These compounds are released through evaporation into the air around the plant, in particular when the leaves are touched such that the storage cells are damaged – if you squish a tansy leaf between your fingers you can smell the chemical compounds, even detecting different bouquets among neighbouring plants.

The chemical diversity of the plant leads it to being a natural insect repellent, with both the agricultural Colorado potato beetle pest and the common tick avoiding leaves of the plants (Panasiuk 1984; Pålsson et al. 2008). However, not all insects are repelled by the plant. Three specialised aphid species (small, soft-bodied insects that feed on the plant sap) are commonly found on the plants. One of these species, Metopeurum fuscoviride, feeds almost exclusively on tansy and is found living in dense colonies on the upper parts of the plant stems. In the early part of the season, these aphids produce winged morphs that can disperse among plants within a field site and to other field sites. After 2-3 weeks, the majority of aphids are unwinged, limiting their feeding options to their current plant or perhaps the neighbouring plant. This aphid species doesn’t just need its tansy plant host to survive but is also an obligate myrmecophile, which means it also needs ants around for colony growth. As aphids feed on the sugary plant sap, they ingest more than is needed and expel the extra as honeydew droplets. Ants feed on this honeydew, and in return protect the aphids from predators. Without ants, the aphids can also become overwhelmed by the honeydew – often sticking themselves to the plant, becoming easy fodder for predators and an ideal breeding ground for fungi.

Our current paper in Journal of Animal Ecology (Zytynska et al. 2019), is the culmination of a DFG (German Research Foundation) funded project where we investigated the effect of tansy plant chemical variation on its specialised aphids and their mutualist ant partners in a field site located in Bavaria, South Germany. We began the project by following almost 200 individual plants in a field from April until October, where the plants grow in individual patches, forming ‘islands’ for its specialised insect herbivores among the other plants growing in the area. Every week we observed the presence of ants, colonisation and population growth of aphids, and the presence of different natural enemies (e.g. ladybirds, and parasitic wasps) on each plant (Senft, Weisser & Zytynska 2017). We found a strong influence of the ants on aphid colonisation, and that local extinction (at the level of the plant) could only be driven by natural enemies once the aphid population was already small. So, we hypothesised that plant chemical variation could influence aphid colonisation success and subsequent population growth rates, leading to larger or smaller populations of aphids on plants with different chemical profiles.

Collecting chemicals

Collecting the volatile chemicals released by the plants in the laboratory (left; photo: J-P Schnitzler) and in the field (middle left; photo: S Zytynska) using stir bar sorptive extraction (middle right; photo: S Zytynska). In the early season, variation in these plant volatile chemicals influences aphid colonisation whereas later in the season other plant compounds (from metabolomics studies) are more important (right; adapted from Clancy et al. (2018))

From our 200 field plants, we identified 22 volatile compounds that are continually released by the plant (i.e. not induced through stress responses). Each of our naturally-growing field plants had its own unique chemical profile, but we were able to group them into four major ‘chemotype’ classes, and showed these influenced the probability of a plant being colonised by early-season winged aphids (Clancy et al. 2016). A further study using untargeted metabolomics grouped plants by their non-volatile compounds, and we found these could also influence aphid colonisation, and population growth rates of unwinged aphid colonies through the season (Clancy et al. 2018). A semi-natural field experiment then empirically confirmed that different chemical profiles of plants could alter aphid population growth, the number of ants on a plant that are tending the aphids, and also the abundance of predators on the different plants (Senft et al. 2019).

In the current paper, we wanted to also look at variation within the aphids themselves as this can affect colony growth rates but moreover if it can influence their choice of host-plant (reviewed in Zytynska & Weisser 2016). Aphids were collected across two years from each plant and genotyped using 18 specially-designed microsatellite loci. We identified six main genetic groups of aphids (genotypes) at our field site, with surprisingly high levels of genetic variation for an insect that reproduces asexually in the warm summer months. We found that the distribution of aphid genotypes was not random, but that certain aphid genotypes were found more often on certain plant chemotypes/metabotypes. Not only do aphids choose preferred plant chemotypes (or metabotypes) but that different genotypes of aphids show different preferences. Moreover, preferences of the ants for different plant variants also impacted the distribution of aphids with some ‘aphid genotype – plant chemotype’ combinations being enhanced by similar aphid and ant host preferences. Therefore, rather than a generic mass of green in a field, aphids can decipher which are their host plants and show a preference to the particular type of host plant they want to live on; perhaps similar to my preference for broccoli over cauliflower – same plant species (Brassica oleracea), but different variants.

So, as you take walks out into the countryside over the coming summer months, remember that these small insects are quietly getting on with their lives deciding where to feed, reproducing to increase their colony sizes, being poked by ants, and generally trying to avoid getting eaten by predators.


More information

Clancy, M.V., Zytynska, S.E., Moritz, F., Witting, M., Schmitt-Kopplin, P., Weisser, W.W. & Schnitzler, J.P. (2018) Metabotype variation in a field population of tansy plants influences aphid host selection. Plant Cell and Environment, 41, 2791-2805.

Clancy, M.V., Zytynska, S.E., Senft, M., Weisser, W.W. & Schnitzler, J.-P. (2016) Chemotypic variation in terpenes emitted from storage pools influences early aphid colonisation on tansy. Scientific Reports, 6, 38087.

Pålsson, K., Jaenson, T.G., Bæckström, P. & Borg-Karlson, A.-K. (2008) Tick repellent substances in the essential oil of Tanacetum vulgare. Journal of medical entomology, 45, 88-93.

Panasiuk, O. (1984) Response of Colorado potato beetles, Leptinotarsa decemlineata (Say), to volatile components of tansy, Tanacetum vulgare. Journal of chemical ecology, 10, 1325-1333.

Senft, M., Clancy, M.V., Weisser, W.W., Schnitzler, J.-P. & Zytynska, S.E. (2019) Additive effects of plant chemotype, mutualistic ants and predators on aphid performance and survival. Functional Ecology, 33, 139-151.

Senft, M., Weisser, W.W. & Zytynska, S.E. (2017) Habitat variation, mutualism and predation shape the spatio-temporal dynamics of tansy aphids. Ecol Entomology, 42, 389-401.

Zytynska, S.E., Guenay, Y., Sturm, S., Clancy, M.V., Senft, M., Schnitzler, J.P., Pophaly, S.D., Wurmser, C. & Weisser, W. (2019) Effect of plant chemical variation and mutualistic ants on the local population genetic structure of an aphid herbivore. Journal of Animal Ecology.

Zytynska, S.E. & Weisser, W.W. (2016) The effect of plant within-species variation on aphid ecology. Biology and Ecology of Aphids (ed. A. Vilcinskas), pp. 152-170. CRC Press.

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