The buzz on trophic cascades

Herbivores, by their nature, damage plants in natural ecosystems and in agricultural systems.  And predators, by their nature, do a lot of damage to herbivores, either by eating them, or by harassing them in ways that cause them to change their behavior, or in some cases change their morphology or physiology (these are called nonconsumptive effects).  The indirect effect of a trophic cascade in which predators damage herbivores which damage plants, is that predators can benefit plants by their detrimental effect on herbivores.

Much of the research on nonconsumptive effects has focused on aquatic systems because the predator cues are easy to manipulate in the laboratory.  Simply let a predator hang out in a water tank for a while, and then add the predator tank water to a tank with a possible prey item, and study the prey’s response. But there has been little work on nonconsumptive effects in terrestrial systems.  While there has been some research on how auditory cues emitted by terrestrial predators affect vertebrate herbivores, there has been almost no work on how auditory cues affect invertebrate herbivores.  This is surprising, because invertebrates cause enormous damage to agricultural systems. Evan Preisser and his students wondered whether the beet armyworm caterpillar, Spodoptera exigua, a voracious herbivore on many commercially important crops, responded to buzzing emitted by an important predator, the caterpillar-hunting paper wasp (Mischocyttarus sp.). More important, they tested whether the response was substantial enough to have an impact on caterpillar mortality, and subsequent plant development.

Four Spodoptera caterpillars chomp on a soybean leaf. Credit: Michasia Dowdy, University of Georgia,

Perhaps the biggest challenge was technical.  The researchers needed to come up with a mechanism for delivering an auditory cue to one group of caterpillars that would not be detected by any other nearby group.  They tried various conformations, including separating the cages with soundproofing foam, which, unfortunately, was not soundproof to wasp buzzes.

One of the failed attempts at auditory isolation. Unfortunately, the auditory stimulus was detectable up to two boxes away from the source. Credit: Zachary Lee.

Nothing worked until one of the students suggested using boxes that dry ice was shipped in, reasoning correctly that it should have good insulating properties.  The decibel meter failed to detect any sound from adjacent boxes.

This worked! Credit: Zachary Lee.

Having solved the soundproofing problem, the researchers raised 36 groups of five caterpillars in small cups filled with 25 grams of caterpillar diet. Each cup was placed in a box and subjected to one of three treatments: no-sound control, recorded buzzing of a non-predatory mosquito, or recorded buzzing of a predatory wasp.  The volume was the same for both sound treatments. Each tape went for 12 hours per day, with 2 seconds on, followed by 6 seconds off.  The researchers found that survival was substantially lower for caterpillars that received the wasp treatment (top graph below).  Also, caterpillars that survived the wasp treatment took, on average, longer to develop (bottom graph below), though that difference was not statistically significant.

Survival (top graph ), weight (middle) and time to pupation (bottom) of Spodoptera caterpillars subjected to no sound (green bar), mosquito buzz (yellow) and wasp buzz (red). Different letters above bars indicated statistically significant differences between treatments.

Preisser’s graduate student, Zachary Lee, took the lead in organizing the field experiment.  The researchers wanted to know whether the negative effect of wasp buzzes that they detected in the laboratory had real consequences for agricultural systems.  They surrounded each tomato plant (72  in all) with a mesh bag (to keep the caterpillars in and other insects out), and placed an average of 96 newborn caterpillars on each plant.  Each group of four plants surrounded a speaker that emitted either no sound (control), mosquito buzzing, or wasp buzzing, which were broadcast at levels that caterpillars would experience when an insect was 5 cm away from them.  Each sound was played in a loop of 1 minute on, followed by 10 minutes off, for 12 hours per day.  Lee and his colleagues let the experiment run for 3 weeks, by which time all caterpillars had either pupated or died. They harvested each plant, and calculated the percentage of leaves that were damaged by caterpillars.  Then they dried each plant, including the roots, and weighed them.

Field experiment with four tomato plants positioned equidistant from one central speaker. Each group of four received one of the experimental treatments. Credit: Zachary Lee.

Plant leaves associated with wasp buzzing received the least damage, leaves on control plants received the most damage, and leaves on plants with mosquito buzzing received intermediate damage. Aboveground mass was greater in wasp treated plants than in controls, so the sound of wasp buzzing helps to protect the tomato plants against voracious caterpillar herbivores.

Indirect effects of no sound (green bar), mosquito buzz (yellow) and wasp buzz (red) on tomato plants, via the effects of these treatments on Spodoptera herbivory. Different letters above bars indicated statistically significant differences between treatments.

The researchers did not study caterpillar behavioral changes because these caterpillars are easily disturbed, either freezing or dropping off of plants when approached.  Lee and his colleagues point out that we know very little about how invertebrates, in general, respond to sound cues, as their survey of the literature on prey response to sound cues showed that 181/183 experiments used vertebrate prey.  Given how widespread invertebrates are in agricultural systems, and in ecosystems in general, we need more studies to get a better handle on how invertebrates respond to sound, and most important, how their response influences agricultural systems and ecosystem structure and functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Lee, Z.A., Cohen, C.B., Baranowski, A.K., Berry, K.N., McGuire, M.R., Pelletier, T.S., Peck, B.P., Blundell, J.J. and Preisser, E.L., 2023. Auditory predator cues decrease herbivore survival and plant damage. Ecology, p.e4007. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2023 by the Ecological Society of America. All rights reserved.