Pest Control: Hiding in plain smell
If you look carefully at a plant, you may start to notice a few telltale signs of feeding insects: holes chewed in a leaf, little mazes of trails, shiny spots of honeydew. You might even catch a caterpillar hiding along a leaf’s midvein – one of many strategies that plant-eating insects have evolved to camouflage themselves (Duncan, 1922). If you lean in, you will smell a planty scent, which herbivores use to choose the plants they eat (Bruce et al., 2005). At the same time, plants also release smells to attract species that prey on these herbivores (Turlings and Erb, 2018).
In fact, recent evidence suggests that plant odors are the subject of an ‘information arms race’, which plants seem to be winning so far. In this arms race, plants evolve new scents to become harder for herbivores to 'sniff out' in a crowd, while herbivores evolve to use more odors to find the plants they eat (Zu et al., 2020). In addition, plants also attract predators of herbivores, using smells that change depending on the herbivores feeding on the plant (Dicke and Baldwin, 2010). Together, these observations may explain why all plants studied so far produce rich, situation-dependent odor bouquets.
Now, in eLife, Yunhe Li from the Chinese Academy of Agricultural Sciences and colleagues from Switzerland and China – including Xiaoyun Hu as first author – report that a common crop pest can use the plant odors released by the feeding of another herbivore to hide from its own enemies (Figure 1; Hu et al., 2020). This strategy is known as ‘olfactory camouflage’ (Ruxton, 2009).
Hu et al. focused on two widespread rice pests: the striped stem borer caterpillar and the brown planthopper. Rice can make different blends of odors to attract animals that rid the plant of feeding herbivores. One such animal is a species of wasp called Anagrus nilaparvatae, which lays its eggs inside planthopper eggs. Hu et al. first observed that brown planthoppers preferred to lay their eggs on caterpillar-infested rice plants rather than undamaged plants (Figure 1A). Next, experiments were performed to test whether Anagrus nilaparvatae wasps chose the plant on which to lay their eggs based on the presence of caterpillars. The results showed that, in the absence of caterpillars, wasps preferred plants with more planthoppers. However, when the plants had both planthoppers and caterpillars, the wasps instead preferred plants with fewer caterpillars (Figure 1B). This indicates that one or more odors emitted by the caterpillar-infested plants were masking the presence of planthoppers.
To test this hypothesis, Hu et al. identified 20 odor compounds whose levels varied depending on the densities of planthoppers and caterpillars on the plants. These compounds were then used to test which odors the wasps preferred. Finally, to test whether odor alone was sufficient to explain the wasps’ choice, Hu et al. made synthetic blends of 13 odors that affected the wasps’ behavior. This experiment had exactly the same results as using infested plants: wasps did not choose any odor blends that smelled like plants eaten by caterpillars, with or without planthoppers (Figure 1C). In fact, both in the glasshouse and in the field, wasps parasitize a smaller share of eggs on caterpillar-infested plants, even when the larger number of eggs on those plants is accounted for (Figure 1D). This corresponds to wasps’ preference for the odors of plants hosting only planthoppers, and not caterpillars.
Hu et al.’s results suggest that planthoppers currently have the advantage in their information arms race with rice plants and wasps. How did this happen? The blend of odors that rice produces to encode ‘caterpillar’ appears to be more complex than the blend for ‘planthopper’, so when both are present, information about the planthoppers may be lost. However, the information arms race model indicates that rice plants should evolve a counter-strategy (Zu et al., 2020); and indeed, Hu et al. further showed that olfactory camouflage is less effective in wild rice than in cultivated plants. Unlike wild rice, cultivated rice is under artificial selection pressure by humans and is not free to respond to natural selection.
These results indicate that reducing striped stem borer caterpillar infestations in rice can yield additional benefits, as it may promote biological control of the brown planthopper by parasitoid wasps. From an evolutionary perspective, however, this is shortsighted: if efforts to reduce caterpillar populations fail, planthoppers will continue using the caterpillars as camouflage unless rice plants and wasps evolve ways to elude this mechanism. Unfortunately, waiting for rice plants to evolve a response would entail several generations of reduced rice yield – a disaster for our food supply. An alternative may be to artificially select plants with an advantage in this evolutionary arms race. Doing so will first require dissecting exactly how the planthopper’s olfactory camouflage works, and better understanding how plant odors direct interactions between species.
References
-
Insect host location: a volatile situationTrends in Plant Science 10:269–274.https://doi.org/10.1016/j.tplants.2005.04.003
-
The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'Trends in Plant Science 15:167–175.https://doi.org/10.1016/j.tplants.2009.12.002
-
Non-visual crypsis: a review of the empirical evidence for camouflage to senses other than visionPhilosophical Transactions of the Royal Society B: Biological Sciences 364:549–557.https://doi.org/10.1098/rstb.2008.0228
Article and author information
Author details
Publication history
- Version of Record published: August 11, 2020 (version 1)
Copyright
© 2020, Joo and Schuman
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,232
- views
-
- 142
- downloads
-
- 0
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Ecology
- Evolutionary Biology
Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.
-
- Ecology
Declines in biodiversity generated by anthropogenic stressors at both species and population levels can alter emergent processes instrumental to ecosystem function and resilience. As such, understanding the role of biodiversity in ecosystem function and its response to climate perturbation is increasingly important, especially in tropical systems where responses to changes in biodiversity are less predictable and more challenging to assess experimentally. Using large-scale transplant experiments conducted at five neotropical sites, we documented the impacts of changes in intraspecific and interspecific plant richness in the genus Piper on insect herbivory, insect richness, and ecosystem resilience to perturbations in water availability. We found that reductions of both intraspecific and interspecific Piper diversity had measurable and site-specific effects on herbivory, herbivorous insect richness, and plant mortality. The responses of these ecosystem-relevant processes to reduced intraspecific Piper richness were often similar in magnitude to the effects of reduced interspecific richness. Increased water availability reduced herbivory by 4.2% overall, and the response of herbivorous insect richness and herbivory to water availability were altered by both intra- and interspecific richness in a site-dependent manner. Our results underscore the role of intraspecific and interspecific richness as foundations of ecosystem function and the importance of community and location-specific contingencies in controlling function in complex tropical systems.