A Cannibal's Advantage... Cannibalistic Caterpillars at LSU
Cannibalism may be just what the doctor ordered.
Bret Elderd, an associate professor in the LSU Department of Biological Sciences, investigates how various factors affect disease transmission in insects, particularly in Lepidoptera, an order of insects including butterflies and moths. With his lab group, Elderd looks at how factors including protective chemicals produced by plants insects eat and changes in temperature can either quicken or dampen the spread of disease. By studying these and other factors, Elderd’s work may help other researchers create environmentally friendly bioinsecticides to protect crops like soybeans, for example.
Insects including two species that Elderd studies, the fall armyworm and the gypsy moth, regularly go through boom and bust cycles that can wipe out a crop or completely defoliate a forest. Elderd and his lab group investigate how these boom and bust cycles are affected by disease outbreaks, climate change and other environmental resources and factors... and now, cannibalism.
Elderd was recently conducting field-based experiments with fall armyworm caterpillars (Spodoptera frugiperda) to mimic and study the spread of a lethal baculovirus in this lepidopteran when he noticed something strange.
The experiments involved enclosing individual plants in mesh bags, releasing diseased larvae into the bags to contaminate the plant with a virus, and following disease spread as the healthy individuals consume the plant and inadvertently the virus. At the end of these experiments, when Elderd and his lab group were collecting healthy larvae from the plants and transporting them back to the lab to study more closely how the disease had spread, they ran into what was at first simply an annoying problem.
Elderd and his colleagues were returning from the field with bags full of half-eaten fall armyworms.
“With the fall armyworms, we would lose a large portion of a number of samples we transported back to the lab because when the larvae got close to each other during transport, they started to eat one another,” Elderd said. “I started cursing my luck for conducting these studies with these dang bugs that would eat each other.”
At first, Elderd considered moving to a different species of insect to continue his research. But over time, he started questioning whether, rather than being simply a nuisance to his field experiments, cannibalism among armyworms was serving a bigger purpose.
(Elderd’s lab group also now places larvae from field experiments into individual cups before transporting them back to the lab to guard against cannibalism!)
“Cannibalism is ubiquitous in nature,” Elderd said. “A cannibalistic species will readily eat others of its own species, or conspecifics. But for a long time cannibalism was seen as an aberration when it occurred in any species.”
The fact that cannibalism is often seen as a negative attribute could be related to bias in observations of cannibalism in nature.
“As population densities increase, cannibalism and disease spread can also increase,” Elderd said. “Because cannibalism may increase in populations affected by a disease outbreak, we tend to associate cannibalism in a population with the spread of disease.”
Prompted by their research on disease outbreaks in caterpillars, Elderd and Benjamin Van Allen, a former LSU postdoctoral researcher in Elderd’s lab and currently a postdoctoral researcher at the University of California, San Diego, delved further into published works on cannibalism and disease. Together with colleagues in the Elderd lab at LSU and Volker Rudolf’s lab at Rice University, they developed theoretical models for the interaction between cannibalism and disease across the animal kingdom and found that, counter to its taboo nature, cannibalism can be advantageous. Their findings are published today in a paper in American Naturalist.
“A cannibal that eats a victim has essentially found ‘the perfect meal,’” Elderd said. “If I’m a cannibal, my prey has all the protein ratios and micronutrients that I need, because it’s essentially me. The disadvantage, however, is that my victim is also the perfect host for any suite of pathogens or parasites that would also like to feast on me. The thought here is that I shouldn’t be cannibalistic because I have a high probability of contracting a particular disease if I feed on an organism of my own species.”
This perspective on cannibalism as a risky and often disadvantageous behavior has pervaded biological research for many years, with the thought that cannibalism can bolster the spread of disease through a population. Another study published just this week in Nature Ecology & Evolution highlights how some plants behave in ways that align with this perspective, producing defensive chemicals that may prompt insects that feed on them to become more cannibalistic. But using theoretical models and examples from across the animal kingdom, Van Allen, Elderd and colleagues show in their new American Naturalist paper that cannibalism is not always disadvantageous for the cannibals. Cannibalism may in fact decrease the spread of disease and prevent disease outbreaks in some species.
“We are flipping the paradigm, with regards to cannibalism,” Elderd said. And it makes sense, if you look at it from the perspective of a population susceptible to disease outbreaks.
“What a disease really wants to do is reproduce,” Elderd said. “Say that I have the flu. To anthropomorphize this virus, it wants ideally to spread to more than just one other person. In our paper, we explore the idea that if I have a disease and another organism of my own species eats me, any pathogen or parasite I have is only spread to one other individual. An outbreak would require transfer of that pathogen or parasite to multiple individuals, not just one other cannibal.”
Cannibalism by itself is a poor mechanism for the spread of disease, says study first author Ben Van Allen. When a cannibal eats a healthy individual, it kills a potential future host for the disease, which is bad for the disease. When a cannibal eats an infected individual, there’s always the possibility that a cannibalistic individual won’t even catch any parasite or contract any disease its prey has, which makes cannibalism even more advantageous from a cannibal’s perspective, or dangerous from the pathogen’s perspective!
“There’s a chance that a disease might essentially become extinct within a population through such one-on-one cannibalism, unless more than one individual feasts on victims, and even then the disease must spread to more than one cannibal more often than it spreads to none,” Elderd said. Volker Rudolf, one of the American Naturalist study co-authors, originally posed this idea.
One of the models in the paper was constructed with the lepidopteran system that Elderd and his colleagues are studying. Elderd’s research is generally focused on caterpillars, or butterfly and moth larvae.
“These organisms are very easy to manipulate, and we can investigate answers to questions that would be difficult to ask in other systems,” Elderd said. “Butterflies and moths reproduce relatively quickly, so we can generate and study multiple generations of individuals over a short period of time. We can even generate artificial mini-epidemics in the field to study the impact of environmental conditions on the spread of disease through populations. And finally, we can apply resulting mathematical models regarding the spread of disease among lepidopterans to other organisms, including humans.”
Although the mathematical models described in the study can be applied to many other organisms, Van Allen and Elderd specifically developed a model to explain the spread of a lethal lepidopteran-specific baculovirus through populations of cannibalistic caterpillars, or fall armyworms. The virus has the particularly gruesome effect of eating an infected caterpillar from the inside out.
“What happens is that a caterpillar consumes virus particles that are sitting on a piece of leaf tissue,” Elderd said. “The virus particles are so large that we can readily diagnose infection by looking at a caterpillar’s hemolymph, or blood, under the microscope. An infected caterpillar becomes essentially a walking jelly bowl full of virus. Eventually the caterpillar splits open and oozes virus all over whatever it is eating. When we check for infection in the lab, we tap on cups in which the larvae are reared in, and they essentially explode. The undergrads in my lab get a kick out of that.”
But let’s back to cannibalism. When an individual caterpillar becomes sick with this virus, its growth is stunted. Sick individuals end up being smaller and easier for healthy individuals to consume, or cannibalize.
“What we show in our paper is that if these caterpillars become cannibalistic and consume smaller, sick individuals in the population, transmission of this virus through the population is reduced,” Elderd said.
The paper also contrasts the human activity of culling to remove sick individuals and prevent disease spread, for example in the case of foot-and-mouth outbreaks in populations of livestock, to cannibalism. It turns out that cannibalism can be far more effective at culling diseased individuals from a population.
“Culling is typically achieved by removing diseased individuals at a constant rate,” Elderd said. “Cannibalism, however, increases as you increase population size. For a disease outbreak, you need not only to have sick individuals but also a large number of potentially susceptible individuals for the disease to spread to. Cannibalism can knock a population below the threshold number of susceptible individuals necessary for an outbreak to occur and be maintained.”
Elderd describes the American Naturalist study as a math-based and theoretical investigation of cannibalism. The next step is conducting field-based experiments to demonstrate these ideas empirically.
“We didn’t include it in this paper, but we do have empirical work showing that our theories hold water,” Elderd said. Using experiments in the fall armyworm system, Elderd’s group has found that cannibalism decreases the rate of disease spread. In other systems, there is observational evidence that cannibalism hinders the spread of disease. “In some species, mothers will cannibalize their young to weed out the sick and weak, ensuring higher survival rates for healthy offspring,” Elderd said. “But there hasn’t been a lot of empirical research to back up these observations.”
Van Allen, Elderd and colleagues have provided a first step toward empirical evidence of exactly how cannibalism affects disease spread in insect populations. While there are parasites that may benefit from cannibalism indirectly by exploiting loopholes in the host life cycle, Van Allen and Elderd’s work suggests that at least for some populations, cannibalism may be just what the doctor ordered.