Editor’s Choice 57:08 – The mechanisms underlying crop colonisation, aggregation and damage in an insect pest

New research by Lauren Brzozowski and colleagues develops our understanding of how plant preference gradients mediate herbivore behaviour, and how this can ultimately help us manage crop damage from insect pests. Associate Editor, Ian Kaplan collaborates with Christie Shee to introduce our new Journal of Applied Ecology Editor’s Choice article, Attack and aggregation of a major squash pest: Parsing the role of plant chemistry and beetle pheromones across spatial scales.

How do insects rapidly find crop plants and aggregate – sometimes in astronomically high numbers – resulting in massive damage (without intervention)? This question has long motivated ecologists seeking ultimate explanations for insect colonisation and abundance patterns in agricultural fields (e.g. resource concentration hypothesis). At a more proximate level, the mechanisms can be roughly divided into the stepwise processes of host-plant: i) location, ii) acceptance, and iii) attack. A diversity of cues (visual, olfactory, tactile, gustatory) drive these processes, operating at different spatial scales, which has made it challenging to quantify and experimentally illustrate the importance of each stage. Understanding this process from a mechanistic perspective is necessary to devise creative solutions for disrupting pest populations.

The striped cucumber beetle, Acalymma vittatum, is one of the most difficult to manage insect pests in U.S. agriculture. A cucurbit specialist, this species has interested entomologists for almost two centuries and is renowned for its ability to colonise crop fields in large numbers nearly overnight. These beetles largely rely on the odours of their host plants – zucchini [courgette], squash, cucumbers, melons – and an aggregation pheromone, vittatalactone, produced by males. When this pheromone is combined with odours from wounded cucurbit leaves, it creates a synergistic effect that attracts more beetles than either scent alone. However, cucurbit volatiles that are attractive to insects vary based on many factors, including disease, plant part (flowers vs. foliage) and subspecies or cultivar.

Low and high level damage - plot level
Contrast between low (L) and high (R) – level damage at plot level

The new Editor’s Choice article by Brzozowski et al. investigates the stages of colonisation causing cucumber beetles to aggregate at high densities on a preferred crop – Cucurbita pepo pepo (zucchini) – compared with a less preferred subspecies – Cucurbita pepo ovifera (summer squash). To do so, the authors designed a series of elegant experiments aimed at understanding whether this preference is driven by plant (volatiles) or insect (pheromones) traits and the spatial scale over which attraction and retention occurs. Using a cage design that masks visual cues while allowing the diffusion of plant/insect odours, combined with a sticky trap, the study tested the effects of beetle density, beetle sex, feeding damage and plant subspecies on striped cucumber beetle attraction in the field. This long-range colonisation experiment was integrated with smaller-scale bioassays, measuring the rate at which beetles emigrate from the two subspecies in the field and feeding preferences when given a choice.

wind-trap-strips - 1
Close up of trap used in field experiments

Although the authors predicted that cucurbit subspecies volatiles would interact with aggregation pheromones to amplify orientation toward the preferred C. p. pepo, male beetles were highly attractive to other beetles independent of plant type. This confirms the importance of ‘pioneer’ males that initially colonise plants and attract conspecifics, but ultimately this colonisation-aggregation syndrome cannot explain why cucumber beetles attain far higher densities on C. p. pepo. However, when placed on plants and provided the opportunity to leave, more striped cucumber beetles emigrated from the non-preferred subspecies. Upon identifying plant volatile differences between the plant types, two differences stood out: the non-preferred plants possessed an unidentified compound (RT11.8) and linalool emissions were four-fold higher. Combined, these data indicate that while plant subspecies does not affect host-plant location, less preferred cultivars are abandoned at a higher rate, presumably due to short-range volatile repellants, resulting in lower equilibrium densities (i.e., preventing aggregation).

How can this chemical ecology information be used to improve cucumber beetle management in cucurbit fields? For one, confirmation of the potent attractive properties of the aggregation pheromone, vittatalactone, opens new opportunities for population monitoring or attract-and-kill strategies; areas that are just beginning to be explored. However, the work reported here demonstrates that pheromone alone, at least in its natural state, is likely insufficient to cause differences in attack. Trap crop strategies have been developed for striped cucumber beetle, but these tend to work better as a push-pull system where the trap or ‘pull’ is functionally integrated with a ‘push’ that ushers beetles away from the crop. This study shows that the crop itself can act as that push and thus we would predict that trap cropping next to the emigration-prone summer squash works better than with zucchini where beetles are more likely to hunker down and feed, ignoring the allure of the trap. Given that the authors uncovered putative volatile mechanisms for subspecies rejection, these factors could be augmented by breeders in existing cultivars or used to enhance emigration from more preferred varieties.

The full Editor’s Choice article, Attack and aggregation of a major squash pest: Parsing the role of plant chemistry and beetle pheromones across spatial scales, is free to read for a limited time in issue 57:08 of Journal of Applied Ecology.


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