Animals that choose to eat in the presence of a predator run the risk of being eaten themselves, so they often go into a defensive mode and pay a physical penalty for the lack of nutrients.
But that’s not so for the crop pest hornworm caterpillar, a study shows.
While other animals increase metabolism and stop growing or developing during a defensive period, hornworm caterpillars slow or stop eating but actually keep up their weight and develop a little faster in the short term. Ian Kaplan, a Purdue University assistant professor of entomology; Jennifer S. Thaler, an associate professor of entomology at Cornell University; and Scott H. McArt, a graduate student at Cornell, noticed that hornworm caterpillars ate 30 percent to 40 percent less when threatened by stink bugs but weighed the same as their non-threatened counterparts.
“It was a little puzzling. If you’re going to shut down, there should be a cost associated with that,” said Kaplan, who studied the caterpillars as a postdoctoral researcher at Cornell. “We usually think that you can either grow really fast and not defend yourself, or defend yourself but pay a physical penalty. That wasn’t happening here.”
Threatened hornworm caterpillars adapt to increase the efficiency by which they convert food into energy. They also increase the amount of nitrogen they extract from their food and their bodies’ lipid content. In the first three days of the study, the caterpillars weighed the same and reached the next developmental stage faster than caterpillars eating in safety.
Over the long term, however, their body compositions change and their ability to turn food into energy is reduced in later developmental stages. The findings, published in the Proceedings of the National Academy of Science, reveal that hornworm caterpillars are the first insect species shown to delay the physical penalties associated with protecting themselves from predators.
Hornworm caterpillars eat tomato, tobacco, pepper and other crops. Kaplan said understanding their physiology may lead to better ways to control the pests.
Kaplan said the scientists found an interesting way to work around a major roadblock in studying the physiological changes in the caterpillars exposed to predators. They “disarmed” the predators.
Stink bugs normally would use their mouthparts to stab the caterpillar and suck out its internal parts. But the scientists removed part of the stink bugs’ mouthparts, allowing them to hunt but not eat.
“We created a predator that couldn’t kill its prey,” Kaplan said. “It was a way to be able to expose the prey to a risk and still be able to study the physiological responses of the prey.”
The scientists also wondered whether the physiological responses were due to the presence of the predator or simply from a lack of food. To test, they removed food from some caterpillars that had eaten as much as a caterpillar facing a predator. Other caterpillars were given food off and on until they had eaten the same amount as one facing a predator to better mimic those same feeding patterns.
In both cases, the caterpillars weighed less and did not exhibit the same physiological changes as their hunted counterparts.
“This is a predator response rather than a physiological response due to a lack of food,” Kaplan said.
The U.S. Department of Agriculture funded the research.
Compensatory Mechanisms for Ameliorating the Fundamental Trade-off Between Predator Avoidance and Foraging
Jennifer S. Thaler, Scott H. McArt, and Ian Kaplan
Most organisms face the problem of foraging and maintaining growth while avoiding predators. Typical animal responses to predator exposure include reduced feeding, elevated metabolism and altered development rate, all of which can be beneficial in the presence of predators but detrimental in their absence. How then do animals balance growth and predator avoidance? In a series of field and greenhouse experiments, we document that the tobacco hornworm caterpillar, Manduca sexta, reduced feeding by 30–40% owing to the risk of predation by stinkbugs, but developed more rapidly and gained the same mass as unthreatened caterpillars. Assimilation efficiency, extraction of nitrogen from food, and percent body lipid content all increased during the initial phase (1-3 d) of predation risk, indicating that enhanced nutritional physiology allows caterpillars to compensate when threatened. However, we report physiological costs of predation risk, including altered body composition (decreased glycogen) and reductions in assimilation efficiency later in development. Our findings indicate that hornworm caterpillars use temporally dynamic compensatory mechanisms that ameliorate the trade-off between predator avoidance and growth in the short term, deferring costs to a period when they are less vulnerable to predation.