Lords of the Flies Insects, humans, and the fate of the world we share.

Since the earliest days of the film industry, war movies have been a staple. A substantial proportion of the most popular and financially remunerative films in history are those in which the forces of good do battle with (and triumph over) the forces of evil. In the days of silent films, notably westerns, good guys and bad guys were easily recognized by their respective white and black hats. In subsequent years, actual global conflicts provided easily identifiable heroes and villains. Even today, seven decades after the end of World War II, Nazis onscreen represents evil incarnate and provoke instant antipathy; a quarter-century after the end of the Cold War, sinister Russians are reliably reviled as villains in action, adventure, crime, drama, horror, science fiction and even Muppet comedy films. Such stereotyping can elicit objections about fairness, particularly when the “bad guys” are in a broader context oppressed minorities experiencing routine prejudice and abuse in their real, vs. screen, lives (Shaheen, 2003).

There is one group, however, that everybody seems content to loathe and that is easily recognized as representing death and destruction—these are the members of Class Insecta. From the perspective of Hollywood, insects are the perfect villains. They are clearly different from the “good guys”—i.e., humans. For one thing, they look alien, from the human perspective, with compound eyes, antennae, an oversupply of legs, and a skeleton on the outside of their bodies instead of on the inside. Moreover, there are enough insects around that are demonstrably destructive that almost any despicable act a screenwriter would have them commit would be believable—they steal our food, they suck our blood, they spread disease, they destroy our possessions, and they even annoy our pets. Moreover, insects are about the only group that is for the most part socially acceptable to hate. Even legislation aimed at safeguarding laboratory animal welfare exempts insects from consideration (Sekimizu et al. 2012).

It is beyond dispute that insects are involved in countless adversarial interactions with humans. They have caused millennia of misery as the vectors of microbes that cause human disease, suffering, and death. Mosquitoes alone, acting as vectors of the protozoans that cause malaria, the viruses that cause yellow fever, dengue, chikungunya, Zika and a half-dozen types of encephalitis, and the nematodes that cause filariasis and elephantiasis, are responsible for sickening 200 million people annually (Cibulskis et al. 2016). Plague wiped out one-third of Europe’s population in the 14th century; although the deaths were due to infection by the bacterium Yersinia pestis, the Oriental rat flea was the bacterium’s enabler (along with the black rat Rattus rattus, an alternate host that transported the fleas around the continent).

There are, however, inherent cinematic problems with casting insects as the bad guys with whom heroes must do battle.  First, there is the reality that life on this planet as we know it would not be possible without them. Two-thirds of angiosperm plants, the dominant chlorophyll-containing life form on terrestrial Earth, depend on animal partners for pollination and the vast majority of those pollinators are insects. Even the makers of The Swarm (1978), about a swarm of vicious African killer bees that succeed in, among other things, triggering the explosion of a nuclear power plant, acknowledge the importance of honey bees as pollinators with a disclaimer at the end of the film: “The African killer bee portrayed in this film bears absolutely no relationship to the industrious hard-working American honey bee to which we are indebted for pollinating vital crops that feed our nation.”

Waste recycling is also uniquely dependent upon insects—few other organisms can subsist consuming dung, and recycling of carrion depends on the unique biochemical capabilities of a handful of necrophagous insects with enzymes that can break down the refractory proteins making up the bulk of hair, fur, and feathers. Dung beetles alone contribute an estimated $380 million in losses averted due to their ability to accelerate burial of livestock manure, thereby freeing up pastureland for foraging, depriving pest fly species of their breeding grounds, and enhancing the rate of nitrogen recycling (Losey and Vaughan 2006). In contrast with pollinators, there have not yet been any onscreen acknowledgments of these contributions largely because of dung beetles, blow flies, and hide beetles are not the stuff of which matinee idols are generally made.

Perhaps the greatest challenge presented by insects to filmmakers is that the most dangerous among insects are far from physically imposing. Even the deadliest are rarely more than a fraction of an inch or so in size (and their brains have only about a millionth the number of neurons of a human’s). So Hollywood has to embellish the story a bit to add to dramatic tension. Stories with insects as human adversaries generally exaggerate their size and their number—both are ways to make their ability to destroy humanity more credible. As myrmecologist Harold Medford solemnly intones in Them, the 1954 film about ants mutated into giants by exposure to atomic radiation, “No. We haven’t seen the end of them. We have only had a close view of the beginning of what may be the end of us.” A quarter-century later, entomologist Brad Crane, confronted by a swarm of killer bees in The Swarm, says solemnly, “We have been invaded by an enemy far more lethal than any human force,” and, in Kingdom of the Spiders (1977), a scientist observes that “There are many theories about how man would come out if the insects were to turn on him and he doesn’t come out on top very often.”

The reality, though, is quite different. Humans are, according to Palumbi (2001), “the world’s greatest evolutionary force” and it is demonstrably the case that human forces are more lethal to insects than any single insect has ever been to humans. Human activities have so altered Earth’s nutrient cycles and energy flows that they have threatened the existence of thousands of species and in some cases contributed to their extinction.

Admittedly, in the interest of fairness, note must be taken of the fact that humans have created opportunities for arthropod species on a grand scale. There are at least two species of lice, one maggot, and a true bug that feed more or less exclusively on humans, along with multiple ticks, mites, fleas, and flies that occasionally consume human tissues (and not only in situ—dust mites, Dermatophagoides species, live in house dust in mattresses and under beds, feasting on shed skin flakes from oblivious sleepers). The invention of agriculture allowed humans to produce more food than could be consumed at one time by all members of a population; storing surpluses could thus provide food security and allowed human populations to become sedentary rather than nomadic. At the same time, these surpluses expanded the niches of a diversity of arthropods specialized to feed on stored products, which hitherto were effectively restricted to small caches of grain kept by rodents. Moreover, humans developed methods for processing grains, producing even more opportunities for arthropods. While there is a suite of species capable of infesting intact kernels, the human practice of milling reduced the physical barriers that prevented many insects from utilizing some form of dried plant material as food. Thus, humans essentially created environments suitable for flour beetles, flour moths, Indianmeal moths, drugstore beetles and about 50 other species associated with stored grain and flour, over and above at least 450 species of insects and mites that infest other types of stored products (Jayas et al. 1995). Annual losses to stored product pests can exceed 10 percent in the developed world and 30 percent in the developing world; losses arise not only from actual consumption but from impaired germination, contamination with shed skins and excrement, decreased milling quality of flour, and enhancement of microbial growth and spoilage.

Food surpluses also created food waste, another opportunity for insects. In a recent study (Youngsteadt et al. 2015), investigators monitored the rate at which junk food (comprising cookies, potato chips, and hot dogs) was removed from New York streets and, based on their experimental observations, calculated that, just on medians in the Broadway/West Street corridor, arthropods could be responsible for consuming more than a ton of food, the equivalent of 60,000 hot dogs, in a year. Drosophilid fruit flies, which evolved to feed on what has historically been a relatively rare resource—fallen fruits that have begun to ferment—are now established as pests in wineries, where fermenting fruit is available in superabundant quantities.

Human structures are also exploited by insects; the larvae of certain mosquito species, for example, previously confined to living in relatively rare treeholes have adapted easily to life in tires, rainbarrels, flowerpots, beer cans, and other water-holding containers (including baptismal fonts). Even plastic garbage has expanded niches for insects. One explanation that has been offered for the dearth of insects in deep oceans is an absence of substrates on which to lay eggs. In recent years, microplastic pellets, products of plastic refuse, provide an abundance of oviposition sites for the ocean skater, Halobates sobrinus, which for most of its existence had been restricted to ovipositing on occasional flotsam or jetsam (Berenbaum, 2017).

But human food waste and garbage can pose novel evolutionary hazards to insects, leading not to opportunities but to decline and imperiled existence. Perhaps the saddest example is that of the males of the Australian jewel beetle species Julodimporpha bakewellii (Hawkeswood 2005). These males mistake stubbies—the brown bumpy bottles of local beer–for the shiny brown bodies of female of their species and attempt to copulate with them, with frequently fatal results—while beetles cling to beer bottles with the soft parts of their genitalia unproductively exposed, they can be attacked and killed by ants that take ruthless advantage of their distracted state.

Adverse impacts of human activity, beyond those directed at insects for purposes of pest control, are by far the rule rather than the exception. Chief among these activities are habitat degradation and destruction; human activity can so profoundly alter landscapes as to reduce or eliminate insect populations entirely unbeknownst to anyone. In terms of deliberate contamination, pesticide use probably tops the list with respect to rendering vast stretches of habitat uninhabitable by insects. That spraying insecticides against a pest might kill beneficial insects in the same neighborhood was not even recognized as a possibility until late in the 19th century, when beekeepers began to express concern that the arsenic-containing insecticides being sprayed on fruit trees to control pests were killing their honey bees. The fact that broadcast spraying of the broadly lethal arsenical pesticides could result in bee death seems obvious today but the nontarget impacts of pesticide use were not widely acknowledged until carefully controlled experiments provided indisputable evidence that such was the case (Berenbaum 2015). Every new generation of pesticides since that time has been designed to reduce nontarget mortality but so far an insecticide that kills only pestiferous species has yet to be invented. Even DDT, now legendary for its tendency to persist in the environment and undergo biomagnification in food webs, was initially touted as a more environmentally compatible alternative to arsenicals.

A more recent example of unsurprising yet unanticipated nontarget impacts of insecticides on insects is the relatively new class of insecticides called neonicotinoids, introduced in the late 1990s. These pesticides were introduced as suitable for use as systemics—that is, applied as a coating on seeds, to be taken up after germination by the plant’s vascular system and distributed throughout all of the plant’s tissues. The logic behind this “environmentally friendly” approach was that only those insects consuming crop plant tissues, ostensibly pests, would encounter them. Use of systemics undeniably reduces levels of environmental contamination—according to their manufacturers, spraying neonicotinoids over one hectare of ground can contaminate more than 10,000 m² of soil surface, whereas seed treatment, in theory, contaminates only the soil in contact with the seed, which comprises less than 60 m². It is now apparent, however, that among the plant tissues that end up containing systemic neonicotinoids are nectar and pollen, which then can be consumed by pollinators, particularly bees, to ill effect (Goulson 2013). Neonicotinoids have been implicated in recent dramatic declines in abundance of honey bees and other pollinators. In one recent study (Codling et al. 2016), two different neonicotinoids were found in two-thirds to three-quarters of honey samples and in more than half of the bees tested in hives in Saskatchewan, Canada. The presence of neonicotinoids in honey and pollen stores year-round means that bees are continually exposed to pesticide stress. Moreover, because neonicotinoids are water-soluble, they often end up in groundwater and are taken up through the roots by plants outside of agricultural fields, which means that wildflowers growing in crop field margins can end up with higher levels than the crop plants, presenting a risk to both managed and wild pollinators (David et al. 2016).

Beyond weeds and wildflowers, human pest control practices can make even manure inhospitable to insects. Endectocides are drugs that are administered orally to livestock to rid them of internal parasites, such as bot flies. Ivermectin is one such drug that does not break down completely post-administration and ends up excreted in manure, where residues can persist for 20 years or more, rending the dung a killing field for beetles and other members of the dung fauna (Floate 1998).

Urbanization has rendered the world less hospitable to insects on a grander scale than has agriculture. The four million miles of roads in the United States present a particular challenge to arthropods. Collisions with cars are not an insignificant source of direct mortality for many species. In one six-week-long survey of butterfly roadkill in central Illinois, more than 1,800 dead butterflies were collected; this rate extrapolated statewide suggests that 20 million butterflies die on roads every week (McKenna et al. 2001). Roads also cause indirect mortality by fragmenting habitats and increasing insect exposure to de-icing salt, gasoline, exhaust fumes, and asphalt. In fact, although honey bees typically collect tree resins to make propolis, a “bee glue” used to seal cracks within hives and protect the colony against microbial invasion, city bees in some places are now collecting asphalt, which lacks the antimicrobial activity of tree resins, and incorporating it into their propolis with uncertain consequences (Alqami et al. 2015).

Beyond runoff from roads, pesticides from agricultural fields, spills and leakage from mining operations, and wastewater from sewage treatment facilities all present a threat to aquatic arthropod communities; among the most vulnerable members of these communities are aquatic insects that occupy sediments where contaminants accumulate. Nymphs of mayflies, stoneflies, and caddisflies are often the first to feel the effects of anthropogenic inputs to streams, rivers and other natural bodies of water, and some of these species are exceedingly sensitive to vanishingly low levels of contamination. Game and sport fish depend on these insects for food and when the aquatic insect community begins to decline the fish communities decline along with them—a ripple effect, as it were.

Just as human activity can disrupt patterns of biogeochemical cycling, it can also interfere with pathways of energy flow through ecosystems. Thermal effluents from nuclear power stations or steel mills can degrade water quality and even a change in water temperature of one or two degrees can disrupt the life cycles of a wide range of aquatic insects with narrow temperature tolerances (Dallas and Ross-Gillespie 2016). Since the turn of the 20th century, light pollution—the use of artificial light at night– has been suspected of contributing to the decline of moths, which famously are attracted to light at night.  City lights can distract moths and interfere with the ability of males to follow pheromone trails and find mates and the ability of adults of both sexes to find pollen and nectar sources. Moreover, artificial illumination can disrupt seasonal cycles of species that depend on light cues for timing and can waylay migrating populations that depend on celestial navigation to arrive at breeding or overwintering sites. To add insult to injury, artificial light can make moths more conspicuous and thus more vulnerable to predation.

A particularly insidious form of light pollution can be found in the form of bugzappers. These devices use ultraviolet light to attract mosquitoes and other nocturnal biting flies and induce them to fly into an electric grid, with lethal consequences. Unfortunately, while not all nocturnal biting flies are attracted to UV light, a vast diversity of other nocturnal insects are, to their detriment. Over the course of one summer in Newark, Delaware, almost 14,000 insects were killed by bugzappers; of these, fewer than 0.2 percent (only 31) were “biting flies”; most were beneficial predators or parasitoids or innocuous aquatic species that present no threat to humans. Again, extrapolating these mortality rates to the nation’s 4 billion bugzappers leads to an estimated 71 billion nontarget insect deaths over 40 nights during a typical summer (Frick and Tallamy 1996).

Other accidental inputs that have had impacts on arthropods include human-mediated transfer of insects from their native range to other parts of the world. Several thousand of America’s insects and arachnids arrived here from elsewhere. Among these ranks are some of the nation’s most important pests from the human perspective—yellow fever mosquitoes, household cockroaches, gypsy moths, Formosan termites, and Japanese beetles, to name a few. Collectively, non-native arthropods cost the U.S. economy more than $20 billion annually (Pimentel et al. 2000). The toll inflicted on America’s native arthropods, however, by non-indigenous invaders is far greater in terms of lives lost. Invasive insects are among the greatest threats to America’s native insect fauna; these interlopers (who, it is important to remember, more often than not arrived here with human assistance) compete with native species for food, space, and even on occasion mates (causing interspecific hybridization and all of the problems associated with that phenomenon). Exotic ant species, for example, threaten the existence of at least nine rare butterfly species in Florida; just one invasive ant, the red imported fire ant Solenopsis invicta, is considered a danger to five species of rare cave beetles in Texas (Wagner and van Driesche 2010).

The greatest challenge insects face from humans today is almost certainly global climate change, brought about by increasing inputs of greenhouse gases into the atmosphere from human activities; these inputs have contributed to rising global temperatures and to increasing unpredictability of weather. Unpredictability is a major issue for insects in particular, which, relative to much larger organisms, tend to display extreme specialization for particular habitats and climate conditions. Endoparasitoid wasps are such extreme specialists—these wasps lay their eggs inside the bodies of insect hosts and the hatching grubs develop along with their hosts until, when the grubs are ready to pupate, they cause the death of their hosts by bursting out through the body wall to spin a cocoon and pupate. An intricate suite of physiological adaptations is required to allow an insect to develop inside its host without killing it in the process, so it is not altogether surprising that these wasps tend to be very specialized, sometimes attacking only a single host species. Such specialists are particularly vulnerable to the climatic unpredictability associated with global climate change; as climate varies, the ability of the parasitoids to track their hosts seasonally breaks down and, as a consequence, the levels of parasitism in locations from Canada to Brazil decrease as the year-to-year variation in annual rainfall increases (Stireman et al. 2005).

Rising global temperatures also threaten many insects that lead lives according to strict temperature requirements. Again, the most vulnerable insects are those that lead specialized lifestyles. Alpine and Arctic bumble bees are adapted to cold-temperature climates and, like polar bears, global warming has left them with no place to go.  Like all species, bumble bees have a “thermal range”–a geographic distribution that reflects the range of temperatures at which they can survive. Bumble bees are unusual among insects, however, by virtue of their ability to function at cold temperatures. An examination of more than 400,000 geographic records of 67 species of bumble bees in North America and Europe over the past century showed that, since 1974, as mean global temperatures have risen, several species have disappeared from the historical southern limit of their range (retreating by as much as 300 kilometers). While some species at southern limits of their distribution have shifted their ranges to higher elevations (by 300 meters or more), few if any species have expanded their ranges further north or to higher elevations with rising mean temperatures. It is not immediately clear why the most cold-adapted species cannot move further north on the ground or higher up on a mountain, but this pattern may explain why so many bumble bees are disappearing. The rusty-patched bumble bee, Bombus affinis, for example, is essentially missing today from parts of the southeastern U.S., where a century ago it was reliably abundant.

Human activities, then, have done, repeatedly, what many people have thought would have been an impossibility—they have driven insect species to extinction. In the United States, the Natural Heritage Program identifies 160 insects as either “presumed extinct” or “missing and possibly extinct” (Black and Vaughan 2009). That number is likely a massive undercount due to the fact that many more species have likely gone extinct before any entomologist could find and name them. Because of the tremendous diversity of lifestyles adopted by insects, they are integrated into food webs and ecological communities in countless ways; when an insect species goes extinct, it is a virtual certainty that its absence will be felt by other species. That tremendous diversity of lifestyles also means that there is no single strategy that is effective for conserving insect biodiversity. Moreover, it is often hard to make the case to protect a particular insect species unless its absence is felt directly by Homo sapiens. Particularly at risk are ectoparasites of endangered vertebrates—conservation efforts for ticks, fleas, and lice are hard to sell, particularly if they are pests of critically endangered charismatic vertebrates (Dunn 2005). The captive breeding program that was undertaken to save the California condor involved systematic de-lousing of the birds being bred in captivity—today, although the condors have been saved, the California condor louse Colpocephalum californici now appears to have gone extinct.

Because, by virtue of the many and varied ecosystem services they provide so well, insects can be keystones, species on whose existence entire communities depend directly or indirectly, paying attention to their viability is a necessity. Because of the interconnectedness of all living things, an otherwise seemingly inconsequential extinction can ultimately have an impact on the one species that matters the most to us. There are only 85 insect species officially listed as endangered or threatened under the 1973 Endangered Species Act, almost one-third of which are butterflies. That may seem like a lot of endangered butterflies, but there are at least 750 described species of butterflies in the country; with climate change, habitat degradation, and all the other human insults they are dealing with, it seems unlikely that, only 3 percent of them are in trouble. As for the 85 insects that are federally protected, they represent only 0.09 percent of America’s insects.

Were insects capable of making movies, it is highly likely that humans would be the bad guys in most of them. That might be a little depressing as a thought exercise. We can take some comfort, though, in the fact that, although we may be responsible for so many of the problems insects face today, we are also capable of mitigating those problems. Through adopting environmentally compatible ways of going about our business and enacting smart, evidenced-based conservation policies for those species in jeopardy, we have a good chance of ending up the heroes in at least some of the stories.

Acknowledgments: I thank the University of Missouri-St Louis, the Missouri Botanical Garden, the Saint Louis Zoo, and the Academy of Science-St. Louis for the invitation to present the Jane and Whitney Harris Lecture and the opportunity to talk about insect conservation to a broad audience, and I thank Ben Fulton not only for inviting me to prepare a written version of the lecture for the Common Reader but also for forgiving me for missing several deadlines in doing so. I am grateful to Edward Hsieh, Daniel Pearlstein and Richard Leskosky for catching errors in an early draft and I thank the National Science Foundation and the Agriculture and Food Research Initiative at the USDA National Institute of Food and Agriculture for providing me the wherewithal to study invasive species, pesticides, and global climate change, in the hope of reducing the harm inflicted on at least a few insect species.