The Carnal Carnival is a new science-blog carnival that collects “posts covering, mostly from a scientific perspective, a variety of bodily functions, fluids and excretions that are usually not discussed in polite company over an elegant meal.” That’s just our cup of tea! And this month’s theme is poop! Hence, this article. That is all.
Sometimes, scientists find themselves in a position to right injustice. Back in the late 1990s, Georgetown University biologist Martha Weiss noted that animal researchers had, up to that point, spent far more time examining the details of feeding behavior than that of defecation. This, she thought, was a bias worth correcting. And since Weiss was especially interested in insect evolution, that’s where she turned her attention. Specifically, she wondered about the following intriguing problem:
Why do caterpillars like the silver-spotted skipper (Epargyreus clarus), which live inside small, self-made structures (such as cut, tied, or rolled-up leaves) for days or weeks at a time, seem especially likely to fling their frass?
("Frass" is what entomologists call individual pellets of insect excrement, and I do not know why this name was chosen but I do know it makes for some incredibly satisfying alliteration.)
In the 2003 report I’ll be referring to throughout this post, Martha recounts a personal observation that clearly struck her (not literally, thankfully). She had seen, she writes, a 4-cm long silver-spotted skipper larva “launch a pellet a remarkable 153 cm, or 38 times its body length.” Not only that, but when Weiss deliberately inserted pellets into a shelter (proving that sometimes you have to be cruel to be kind), she’d see caterpillars methodically remove the offending pieces of debris, “either by butting them out with their heads or picking them up in their mandibles.” As a result of these twin compulsions—to forcibly eject new poop pellets and to meticulously clean out any stray poop—both the shelters themselves and the surrounding leaves of the plants that host these creatures are always immaculately free of frass.
But what, exactly, is the evolutionary advantage of flinging frass far afield?
Weiss had three plausible theories to investigate:
1. Frass is dirty. Keeping frass around could create an environment that promotes the growth of pathogens, like bacteria, viruses, or fungi, that would be harmful to the caterpillars.
2. Frass clutters. It takes a lot of time and energy to build a shelter, and besides, when a caterpillar is busy constructing a home, it’s dangerously exposed. Accumulated frass could take up too much space, forcing caterpillars to fashion new shelters more often.
3. Where there’s frass, there’s a frass-maker. Maybe keeping poop around serves as an unwanted signal to predators about the precise address of the delicious caterpillar that made it.
In order to evaluate each of these hypotheses individually, Weiss created a carefully calibrated research environment. First, she caught silver-spotted skipper butterflies from the Georgetown campus, waited for them to lay eggs, and collected the resulting larvae. Then she constructed three experimental tests.
Is Frass Unhygenic?
To test this hypothesis, Weiss followed two groups of caterpillars from hatching through to pupation. Each group lived inside a small plastic box with an abundant supply of kudzu leaves to eat. With one group, Weiss used paper towels to remove all the frass produced each day. With the other, she left the frass alone (but lifted each leaf up to make sure each box was equally disturbed by human hands). It didn’t take long to see fungi growing on the frass pellets that remained in the first box.
But did the caterpillars in the “frassy box” take longer to make it pupation? Did fewer of them survive? Did they weigh less along the way? Over two years’ worth of dedicated frass-interference, the answer to almost all these questions was an emphatic no. (In one year’s study, slightly more of the caterpillars in the clean box survived to pupation.)
Does Frass Clutter?
Weiss had already shown that inserting large quantities of frass into a caterpillar’s shelter, so that it took up half or more of the space, caused the insects to leave and build a new home. To test her clutter hypothesis, therefore, she didn’t bother with frass at all. She simply forced some caterpillars to build new homes more often than others, by personally evicting them from the leaf-structures they’d already built. One group had to build a new home every four days; another every three days; another every single day. Control groups were left to their own devices, except for being gently poked with a paintbrush in order to disturb them about as much as the evicted caterpillars.
Would all this have any detrimental effect on their growth? Again, Weiss measured each group’s weight gain, days to pupation, and survival to pupation. And again, there was little effect. Only the group that had to build a new structure every day showed some stress, gaining—on average—slightly less weight as they grew from larva to pupa.
Does Frass Attract Predators?
Weiss’s final experiment involved a little more engineering. She wondered if paper wasps (Polistes fuscatus) would find the scent of her caterpillars’ frass enticing. To find out, she tore off small pieces of scotch tape, and then carefully stuck to each piece either six pellets of “fresh frass,” or six glass beads of the same color and size.
(You know what? I just want to take a moment here to recognize the intense scientific dedication shown by Martha Weiss in pursuit of the understanding of frass-flinging. Can we do that?
Then she placed each piece of tape into one of two shelters that had just been made by a caterpillar larva (she removed the larva, presumably to little protest, and made sure neither tape nor poop nor bead could not be seen from the outside of the leaf structure). Finally, each shelter was put inside a cage where paper wasps were marauding.
At last! A hit! Paper wasps visited the shelters containing frass significantly more than they did those containing beads. They also spent much longer periods of time on the frassy shelters. This poop-preference was exhibited by both “experienced” and “naive” wasps (wasps which had or hadn’t previously killed a silver-spotted skipper).
But Weiss wasn’t done. She also presented individual wasps with
“a choice of two similarly sized kudzu leaflets, each bearing a sheltered second or third instar caterpillar, and either frass or a visual control (more glass beads)...I recorded which caterpillar the wasp discovered first, the amount of time it took the wasp to discover the caterpillar, and which caterpillar the wasp killed first. I conducted 17 trials, alternating leaflet positions each trial. Trials lasted for 5 min, or until the first caterpillar was killed.”
(Lucky second caterpillars.) With these trials,
“Larvae on frass-bearing leaﬂets were signiﬁcantly more likely to be killed during a 5-min trial than were larvae with beads on their leaﬂets. Only three of the 17 frass-associated larvae survived a 5-min trial with a foraging wasp, compared to 14 of the bead-associated larvae...Again, both naıve and experienced wasps participated in these trials, and showed no difference in behaviour.”
Conclusion: Caterpillars Fling to Avoid a Frass-Kicking
Or, as Weiss puts it, “Frass ejection behaviour allows larvae to distance themselves from olfactory cues that might provide information to their enemies"—an answer, I’d say, that really isn’t too crappy.
I encourage you to read the whole report, which also contains an entertaining description of how Weiss discovered the average ejection distance for frass pellets (as a reminder, the longest observed distance was 153 cm), and—something which perhaps I could have lived without—an explanation for why the first keyword that appears in the paper’s abstract is “anal comb.”
P.S. Martha Weiss is also responsible for a somewhat less scatological, but equally charming, insect study from 2008. In that paper, she showed that post-metamorphosis moths can retain memories, such as aversive associations with specific odors, that they formed as caterpillars. I know! How amazing is that? Anyway, now that we’re done talking about insect-backsides, you can go read about their brains.