Compsilura concinnata: A Hidden Force Behind The Decline of North American Moths?

A female Compsilura concinnata tachinid fly. By Tony T, from the Diptera.info forums.

National Moth Week is coming up in less than a month, but experienced mothing enthusiasts are already deep into the summer season. The past few months have seen the steady emergence of the most charismatic family of moths in North America: the Saturniidae, the giant silk moths. American naturalists have admired the huge, colorful moths, and their equally large and ornamented larvae, before there was even an American nation to speak of.

But even their large size and fame have not saved them from the environmental assaults of the 20^th century. The population declines observed for some saturniid species has been well-documented in regions like New England, where the cecropia moth (Hyalophora cecropia), regal moth (Citheronia regalis), and imperial moth (Eacles imperialis) are now rare and/or extinct. In fact, evidence is suggesting that many other moth species are also experiencing regional declines. Many hypotheses have been put forth to explain their disappearance, including habitat loss, electric street lamps, and the indiscriminate use of pesticides. But could it be a plain-looking fly that holds the key to the loss of giant silk moths in parts of the United States?

The European fly Compsilura concinnata is one of a variety of flies in a diverse family, the Tachinidae, that has evolved a curious lifestyle called parasitoidism in which the larval stage feeds and grows on a single host insect’s tissues, like a regular parasite, but always kills it, like a slow-motion, single-target predator. But unlike many parasitoids, which selectively attack only a few species, C. concinnata has very catholic tastes, with a recorded host range of about 180 species ranging from butterfly and moth caterpillars to even beetle larvae and sawfly larvae. The mother fly, discovering a suitably-sized caterpillar, swiftly dive-bombs the host and uses her sharp, hook-like ovipositor to inject eggs, already containing fully-formed embryos, inside its body. These immediately hatch and burrow into the midgut, where they feed on the caterpillar’s gut contents. During this time, they evade the host’s immune response and hijack its respiratory system, attaching themselves to the caterpillar’s network of tracheoles (breathing tubes) near the midgut. When the caterpillar completes development and stops feeding in preparation for metamorphosis, the maggots inside suddenly feed and grow rapidly, killing it. After scavenging the rest of their dying host, the larvae bore out of its body to complete their own development into adult flies.

A polyphemus moth caterpillar (Antheraea polyphemus) infected by tachinid fly larvae. By LunaGraphics2005, from Flickr (beware, the pictures in this series get nasty)

Knowing that it feeds on caterpillars during its larval stage, entomologists initially released C. concinnata into the US in 1906 in a bid to control the invasive gypsy moth, Lymantria dispar, and browntail moth, Euproctis chrysorrhoea. Sporadic introductions of the fly continued throughout the 20^th century. Today, we now know that C. concinnata does play an important role in controlling populations of L. dispar, and may have almost single-handedly eradicated E. chrysorrhoea from most of the United States. Among its compatible hosts are other multiple agricultural pests, though its effectiveness in controlling those species is unclear. But what was the price paid by native butterflies and moths?

Even then, the scientists knew that the fly wasn’t picky in choosing what its larvae would eat. Not only can C. concinnata attack caterpillars besides gypsy moths, it is required to, since its fast generation time is incompatible with the gypsy moth’s longer life cycle. A single field observation noted that the fly accounted for most of the parasitism on the buck moth Hemileuca leucina. However, work attempting to characterize the extent of this damage in the field didn’t begin until 1995, when a team of scientists at the University of Massachusetts-Amherst set out to describe the effects of the fly on wild silk moth mortality. In a series of field experiments in which caterpillars were exposed to the outside environment, C. concinnata infected nearly 70% of Callosamia promethea caterpillars in the course of just 6 days. In another experiment, they showed that Compsilura parasitism caused a vast majority (81%) of mortality in young caterpillars of Hyalophora cecropia; in the end, not one of the 500 H. cecropia caterpillars survived to pupate. Another study done in Virginia showed that C. concinnata flies accounted for 28 of 36 parasitoids recovered from luna moth caterpillars (Actias luna) over the course of the summer of 2001.

Of course, the most obvious problem caused by the introduction of C. concinnata to North America is the threat it poses to butterflies and moth populations, arguably the most cherished component of our native insect biodiversity. And this is certainly an important issue: Not only are they enjoyed by the general public, they play an important role as herbivores, often specializing on a few species each, and also provide food for predators. But it is also possible that C. concinnata, with its generalist appetite and enormous impact on native caterpillars, may be directly competing with native specialist parasitoid species that have evolved to parasitize only a few species. Although the fly inhabits the host midgut, and can thus coexist with parasitoids that develop in the body cavity or other organs, the heavy burden of sustaining multiple larvae outpaces the host’s capacity to nourish all its parasites, resulting in higher mortality and smaller body sizes for all the parasitoids that develop.

There is some hope, however. C. concinnata is itself attacked at high frequencies by its own parasitoids, called hyperparasitoids, which are small wasps that access the fly larvae by laying their eggs onto leaves that are ingested by host caterpillars. The wasp larvae develop as internal parasites of the fly larvae, ultimately killing them (but only after the maggots have already emerged from their host). Some evidence shows that properly managing and protecting habitats can mitigate the parasitism rate of C. concinnata on at least one silk moth species, the buck moth Hemileuca hera. Most of the moths whose declines have been documented are still relatively common throughout the United States, though some species attacked by the fly are considered threatened in certain regions. Overall, however, it is still impossible to draw definite conclusions and set conservation policy without more data on the ecology and population dynamics of the hosts, their parasitoids, and the parasitoids’ parasitoids, all of which are understudied in an environmental context. If anything, the story of C. concinnata has been increasingly cited as an example of biological control going wrong, and hopefully will inform future efforts to utilize natural enemies as a counter to the slew of invasive insects in North American forests.