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.

Mystifying trophic cascades

Within ecosystems, trophic cascades may occur when one species, usually a predator, has a negative effect on a second species (its prey), thereby having a positive effect on its prey’s prey. Today’s example considers the interaction between a group of predators (including several fish species, a sea snail and a sea star) their prey (the sea urchin Paracentrotus lividus) and sea urchin prey, which comprise numerous species of macroalgae that attach to the shallow ocean floor. These predators can negatively affect sea urchin populations either by eating them (consumptive effects), or by scaring them so they forage less efficiently (nonconsumptive effects). If sea urchins are less abundant or less aggressive foragers, the net indirect effect of a large population of fish, sea snails and sea stars will be an increase in macroalgal abundance.

Maldonado Halo

A large sea urchin grazing in a macroalgal community.  Notice the white halo surrounding the urchin, indicating that it has grazed all of the algae within that region. Credit: Albert Pessarrodona.

Many humans enjoy eating predatory fish, and we have overfished much of the ocean’s best fisheries including the shallow temperate rocky reefs (4 – 12 m deep) in the northwest Mediterranean Sea. Removing these predators has caused sea urchin populations to explode, overgrazing their favorite macroalgal food source, and ultimately leading to the formation of urchin barrens – large areas with little algal growth, low productivity and a small nondiverse assemblage of invertebrates and vertebrates.


A sea urchin barrens whose macroalgae have been overgrazed by sea urchins. Credit: Albert Pessarrodona

Albert Pessarrodona became interested in this trophic cascade after years of diving in the Mediterranean. He noticed that in Marine Protected Areas, predatory fish abound and there are few visible urchins and lots of macroalgae. In nearby unprotected areas where fishing is permitted, urchins graze out in the open brazenly, and urchin barrens are common. He also wondered whether a second variable – sea urchin size – might play a role in this dynamic. Were large sea urchins relatively immune from predation by virtue of their large size and long spines, allowing them to forage out in the open even if predators were relatively common?


Interactions investigated in this study.  (a) Predators consume either small (left) or large (right) sea urchins (consumptive effects). (b) Sea urchins eat macroalgae. (c) Predators scare small or large sea urchins, reducing their foraging efficiency (nonconsumptive effects). (d) Predatory fish indirectly increase macroalgal abundance.

Pessarrodona and his research team used field and laboratory experiments to explore the relationship between sea urchin size and their survival and behavior in high-predator-risk and low-predator-risk conditions. High-risk was the Medes Islands Marine Reserve, which has had no fishing since 1983 and boasts a large, diverse assemblage of predatory fish, while low-risk was the nearby Montgri coast, which has a similar habitat structure, but allows fishing. The researchers tethered 40 urchins of varying sizes to the sea bottom (about 5m deep) in each of these regions, left them for 24 hours, and then collected the survivors to compare survival in relation to body size in high and low-risk conditions. They discovered that large urchins were much less likely to get eaten than were small urchins, and that the probability of getting eaten was substantially greater in the high-risk site.


Probability of being eaten in relation to sea urchin size (cm) in high-risk (blue line) and low-risk (green line) habitats.

Pessarrodona and his colleagues followed this up by investigating whether the relatively predation-resistant large urchins were less fearful, and thus more likely to forage effectively, even in high-risk sites. Previous studies showed that sea urchins can evaluate risk using chemical cues given off by other urchins injured in a predatory attack, or given off by the actual predators. To explore the relationship between these cues and sea urchin behavior, the researchers put either large or small sea urchins into partitioned tanks with an injured sea urchin. Water flowed from one partition to the other, so the experimental sea urchins received chemical cues from the injured urchins. They also had a group of sea urchins placed in similar tanks without any injured sea urchins as controls. The experimental sea urchins were given seagrass to feed on, and the researchers calculated feeding rates based on how much food remained after seven days.

Small sea urchins were not deterred by the presence of an injured urchin (left graph below), while large sea urchins drastically reduced their feeding rates in response to the presence of an injured urchin (middle graph). This was startling as it flew in the face of the commonsense expectation that small sea urchins (most susceptible to predation) should be most fearful of predator cues. The researchers repeated the experiment (under slightly different conditions) placing an actual predator (a fearsome sea snail) on the other side of the partition. Again, large urchins showed drastically reduced foraging rates (right graph below).


Sea urchin responses to predation risk cues in the laboratory. When exposed to injured urchins – symbolized as having a triangle cut out – (A) small urchins did not reduce their grazing rate, while (B) large urchins drastically curtailed grazing. (C) When exposed to a predatory snail on the other side of a partition, large urchins sharply curtailed grazing. n.s = no significant difference, **P<0.01.

It turns out that large sea urchins are the critical players in this trophic cascade because they do much more damage to algal biomass than do the smaller urchins (we won’t go through the details of that research). The question then becomes how this plays out in natural ecosystems. Do consumptive and non-consumptive effects of predators in high-risk sites reduce sea urchin abundance and reduce the foraging levels of large sea urchins so that macroalgal cover is greatly enhanced? Pessarrodona and his colleagues surveyed high-risk and low-risk sites for sea urchin density and algal abundance. They set up 45 quadrats (40 X 40 cm) at each site, measured each sea urchin’s diameter, and estimated the abundance of each type of algae by harvesting a 20 X 20 cm subsample from each quadrat and drying and weighing the sample.

The findings were striking. Small and large sea urchins were much less abundant at high-risk sites than at low-risk sites (left graph below). At the same time, macroalgae were much more abundant at high-risk sites than at low-risk sites (right graph below).


(Left graph) Density of small and large sea urchins in high-risk and low-risk habitats. (Right graph) Biomass of macroalgae of different growth structures in high-risk and low-risk habitats. Canopy algae are taller than 10 cm, while turf algae are lower stature. Codium algae are generally not grazed by sea urchins. **P<0.01, ***P<0.001.


Summary of interactions.  Arrow width indicates relative importance.

To summarize this system, predators reduce small sea urchin abundance by eating them (consumptive effects), and reduce large sea urchin foraging by intimidating them (nonconsumptive effects). The net indirect effect of predators on macroalgae is a function of these two effects. Large sea urchins are the major macroalgae consumers, but, of course, large sea urchins develop from small sea urchins.

The $64 question is why large sea urchins fear predators so much, while small (more vulnerable) urchins do not. The quick answer is that we don’t know. One possibility is that small sea urchins may be bolder in risky environments since they are more vulnerable to starvation (have fewer reserves), and also have lower reproductive potential since they are likely to die before they get large enough to reproduce. In contrast, large sea urchins can survive many days without food because of their large reserves. In addition, large urchins are close to sexual maturity, and thus may be unwilling to accept even a small risk to their well-being, which could interfere with them achieving reproductive success.

note: the paper that describes this research is from the journal Ecology. The reference is Pessarrodona, A.,  Boada, J.,  Pagès, J. F.,  Arthur, R., and  Alcoverro, T. 2019.  Consumptive and non‐consumptive effects of predators vary with the ontogeny of their prey. Ecology  100( 5):e02649. 10.1002/ecy.2649. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.