Intraspecific differences in plant chemotype determine the structure of arthropod food webs

Abstract

It is becoming increasingly appreciated that the structure and functioning of ecological food webs are controlled by the nature and level of plant chemicals. It is hypothesized that intraspecific variation in plant chemical resistance, in which individuals of a host-plant population exhibit genetic differences in their chemical contents (called 'plant chemotypes'), may be an important determinant of variation in food web structure and functioning. We evaluated this hypothesis using field assessments and plant chemical assays in the tansy plant Tanacetum vulgare L. (Asteraceae). We examined food webs in which chemotypes of tansy plants are the resource for two specialized aphids, their predators and mutualistic ants. The density of the ant-tended aphid Metopeurum fuscoviride was significantly higher on particular chemotypes (borneol) than others. Clear chemotype preferences between predators were also detected. Aphid specialist seven-spotted ladybird beetles (Coccinella septempunctata) were more often found on camphor plants, while significantly higher numbers of the polyphagous nursery web spider (Pisaura mirabilis) were observed on borneol plants. The analysis of plant chemotype effects on the arthropod community clearly demonstrates a range of possible outcomes between plant-aphid-predator networks. The findings help to offer a deeper insight into how one important factor--plant chemical content--influences which species coexist within a food web on a particular host plant and the nature of their trophic linkages.

Additive effects of plant chemotype, mutualistic ants and predators on aphid performance and survival

“…Bottom‐up effects mediated by intraspecific variation among plants can arise through various genetically based traits leading, for example, to differences in plant growth habit or metabolic diversity (Bálint et al, ; Johnson, ; Johnson & Agrawal, ; Kareiva & Sahakian, ; Mooney & Agrawal, ; Williams & Avakian, ; Züst & Agrawal, ; Zytynska & Weisser, ). Host‐plant biochemistry is a key factor in affecting herbivore performance and often mediates herbivore preferences (Bernays & Chapman, ; Karban & Baldwin, ; Rosenthal & Berenbaum, ).…”

“…Plants use these volatile compounds for direct defence (Martin & Bohlmann, ) or for internal, intra‐ or interspecific communication (e.g., Riedlmeier et al, ) as well as for communicating with higher trophic levels (reviewed in de Vos & Jander, ; Holopainen & Blande, ; Paré & Tumlinson, ). One example is the recruitment of predators or parasitoids by herbivore‐infested plants (plant–natural enemy–herbivores; e.g., Bálint et al, ; Linhart, Keefover‐Ring, Mooney, Breland, & Thompson, ; Ninkovic, Al Abassi, & Pettersson, ). Some herbivore species (Erb & Robert, ; Goodey, Florance, Smirnoff, & Hodgson, ; Opitz & Müller, ; Prudic, Khera, Sólyom, & Timmermann, ) have also evolved to take advantage of host‐plant‐derived secondary metabolites (including nonvolatile defensive compounds, e.g., salicin derivatives or glucosinolates, and volatile defensive compounds, e.g., benzaldehyde) to use them in their own defence strategies against predation (Dyer, ; Gauld, Gaston, & Janzen, ).…”

“…It consists of (a) common tansy ( Tanacetum vulgare L.; Asteraceae), an aromatic plant with a high chemical diversity regarding quantity and quality of stored and emitted VOCs (i.e., different plant chemotypes; Clancy et al, ; Forsén & Von Schantz, ; Rohloff, Mordal, & Dragland, ); (b) the highly specialised aphid Metopeurum fuscoviride Stroyan (Homoptera, Aphidoidea), an obligate myrmecophilous species, commonly tended by (c) ants such as Lasius niger L. (Formicidae); and (d) predated on by various common aphidophagous predators. In field studies on this system, the occurrence of aphids, tending ants and aphidophagous predators were associated with differences in the blend of volatile terpenoids across different plant chemotypes (Bálint et al, ; Clancy et al, ). This bottom‐up effect of plant chemotype may therefore mediate effects of mutualists and predators on aphid populations (i.e., indirect effects of the chemotype), which could contribute to the distinct distribution of aphids observed in field surveys (Senft et al, ); for example, through higher predation pressure or reduced protection by ants on certain plant chemotypes.…”

Chemotypic variation in terpenes emitted from storage pools influences early aphid colonisation on tansy

“…The aphids interact with their tending ant species, with other specialised tansy aphid species and the myriad of natural enemies to form a metacommunity. Previous work242728 has shown that tansy chemotypes dominated by camphor, β-thujone, artemisia ketone and borneol can influence the community of associated invertebrates1829. However, many of these studies classified the plants into chemotypes based on the dominant terpenes, yet often it is the whole ‘blend’ of a plant’s emitted terpenes that has been found to influence plant-insect interactions30.…”

Aphid specialism as an example of ecological–evolutionary divergence

“…Distinct chemotype preferences between predators were also detected. Aphid‐specialist seven‐spotted ladybirds, C. septempunctata were more often found on Camphor‐containing plants, while significantly higher numbers of the polyphagous nursery web spider Pisaura mirabilis Clerk (Arachnida: Araneae: Pisauridae) were observed on Borneol‐containing plants (Bálint et al, ). Furthermore, Clancy et al .…”