Planet of the Bugs: Evolution and the Rise of Insects

by Scott Richard Shaw

  In the highest forested slopes,

  Like angular, cryptic constellations:

  Seven up—three across—two down.

  Ironically, in the deep night sky above,

  Not a single star or planet is visible.

  The lights of space are totally obscured,

  By dense Andean fog,

  The haze of auto exhaust,

  And a pale reddish glow of reflected city lights,

  Like clouds of inter-stellar gas,

  At the dawn of the Universe.

  penned at the Hotel Rio Amazonas, Quito, Ecuador

  Outside my hotel room lies Quito’s urban sprawl, enveloped in the Andes Mountains’ verdant, cloud-wrapped peaks. All of this starkly reminds me of the Cenozoic, our most recent geological era. Within the last sixty-five million years, tectonic forces uplifted the Andes, ultimately redirecting the water flows of South America and creating the Amazon River basin. The great diversity of modern neotropical plant and animal life was also shaped over the Cenozoic, and I’m in Ecuador with my students to search for previously unseen and undiscovered microscopic insects in the Yanayacu cloud forest—one of the most species-rich places on earth. Here in Quito, though, the urban chaos reminds me of another significant Cenozoic event: the evolution of the human species.

  Were it not for the necessity of commenting on our origins and our impacts on this planet, I might not have bothered to write this chapter at all. You see, from my peculiar point of view as an entomologist, the mammals’ recent history seems almost like a trivial aside to the insects’ deep history, which, as we have seen, began hundreds of millions of years ago. Here, however, is my condensed version of the story of us. One day, when the dust from the Late Cretaceous, dinosaur-extinguishing asteroid settled and the earth recovered her biological rhythms, some fortunate shrewlike mammals—insectivores, mind you—scrambled in the comfortable leaf litter, hunting for grubs. For the first time in 150 million years or so, they were not being hunted by the dinosaurs. Let loose from the bondage of dinosaur teeth, these small, furry, nipple-bearing, and milk-producing rodents proliferated. Some of these, the early lemurlike primates, evolved to occupy trees. They still ate insects, but some presumably expanded their diets and consumed fruit along with other plant parts. So it went for tens of millions of years, as our ancestors crawled from branch to branch, nibbling on bugs and plants. Then, between 5 and 12 million years ago (during the Miocene epoch), the climate of eastern Africa changed. From fossil pollen records we know that the forests in that region became sparse and grasslands more widespread. We suspect that some of the arboreal primates climbed back down out of the trees and started foraging, more omnivorously, for food on the ground.

  Because many of our cultures still eat insects, we can assume that our highly omnivorous hominid forebears did so as well.1 They probably depended on bugs for protein just like chimpanzees, our nearest living genetic relatives. At certain times of the year chimps can spend up to seven hours a day feeding on termites, for which they fish by plucking a grass stem and inserting it into a nest entrance. The termites bite the stem then are easily extracted and eaten off of it (they’re protein pellets on the cob). Fishing with grass stems is probably the simplest imaginable form of primate tool use, and I think we can also assume that our ancestors shared this curious behavior with the chimps.2 In my opinion, the origins of human tool use, fine motor skills, manual dexterity, and ultimately the rise of human civilization are firmly rooted in our ancestral insectivorous diets. We may owe our very existence to social cockroaches. If termites weren’t abundant, would primates ever have come back down out of the trees? I doubt it.

  The Cenozoic years are popularly called the Age of Mammals, and you can probably guess why: because we are telling the story.3 When humans discovered their own evolutionary history, the self-realization was almost too much to bear. The notion that we were not put here on a pedestal to rule the planet, but that we instead emerged from a long series of random and quirky events—that is a lot to contemplate.

  What if Cambrian predatory arthropods had hunted our lowly ancestor, Pikaia, to extinction? What if Ordovician predatory sea scorpions, trilobites, and squids had eaten all of the early fishes? What if those scuttling Silurian and Devonian scorpions and centipedes had been so deadly as to prevent any vertebrates from colonizing land? What if during the Carboniferous the aquatic immature stages of the giant griffenflies had killed off all the immature stages of pond-dwelling amphibians? What if the Permian protomammals had been one of the casualties of the period’s mass extinctions? What if, at any time during the hundred million years of Mesozoic dinosaur domination, those toothy predators had managed to catch and eat the last of the little mammals? What if the Cretaceous asteroid had missed earth and the dinosaurs continued their reign of terror?

  In each case, the answer is the same: if events had gone slightly differently, humans might not be here at all. The fact that we are here to ponder these things is truly awesome, but it is certainly not inevitable. We not-too-subtly reinforce our fragile human egos by continuing to call the Cenozoic era the Age of Mammals. However, mammals are indeed just one unlikely sidebar on the history of life. The Cenozoic world was still very much dominated by the insects and flowering plants. By focusing on the mammals we distract from what I see as the true success story of the most recent era: the origins and complexity of tropical forest ecosystems and their domination by insects.

  Fifty Shades of Green

  Notes from my Yanayacu diary:

  We live in the Age of Tropical Biodiversity. The tropical forests of this Cenozoic earth are replete with thousands of flowering plant species and millions of insect species. Now I have been in the midst of this majestic biodiversity for one week. The forest at Yanayacu is a remarkable contrast to the street scenes in Quito. Here, during secluded moments deep in the cloud forest, one can almost imagine what the world might have been like had humans never arrived. Every day it rains at Yanayacu. Especially in the afternoon, and late at night, the raindrops pound the tin roof of the research station, sounding much like Wyoming hail on the metal roof of my beat-up old minivan. Now it is mid-afternoon on a quiet and unusually clear day. From my vantage point in the station loft I can see, encircling the valleys, the moist forested hillsides of the Andes’s eastern slopes. The sounds of water splashing over rocks and gushing through narrow passages, dripping everywhere and splashing on leaves—the sounds of water along the stream trail are indelibly imprinted in my auditory memory. Water is everywhere and ever-present at Yanayacu. So much so, that the station dog is named Rain. Even in the rain, at night the blacklight sheet draws in thousands of moths. They cover the windows and walkways in the morning. The hyperdiversity of moth species at Yanayacu rivals that of any place on this planet.

  A hike down the Yanayacu Stream Trail is a great way to appreciate Cenozoic tropical diversity. The trail snakes along the stream, crossing it many times. Sometimes we ford the stream on slick mossy stones, or wade in the cold mountain water. Sometimes we cross like acrobats on slippery algae-covered trees or boards laid loosely across the chilly water gap. On particularly rainy days, the stream rises, and you are sure to get plenty of cold water in your boots. Even on the trail the path is slick with mud and the way is sometimes treacherous. Above the water noise, sometimes we hear the piping and trills of unseen tropical birds—the most successful feathered Cenozoic dinosaurs—hidden in the dense foliage, or high in the forest canopy.

  The forest is as green as it is wet. Even in the dim light of the understory, the forest is painted with riotous shades of green. Bluish-green to yellowish-green, lime green to olive, grass green to sea green, green in fifty shades and more, the color of an endless tropical summer, verdant and lush. Verde, green, the color of plants, the color of life: an ever-present reminder of the pigment chlorophyll, the stuff that allows plants to capture sunlight’s energy. Green, a constant reminder that our sun, our nearest star, provides this radiant energy for our terre
strial ecosystems.

  Competition for sunshine fundamentally shapes the forest. The trees grow tall and spread their upper limbs to make a dense canopy, competing to filter much of that light in the highest layers. The light level at the floor is quite low, even at midday. In a mature tropical forest, 90–95% of the sunlight is filtered away by the plants before it can reach the ground. Some understory plants grow huge leaves, many feet across, to better soak up the filtered sunbeams. In small gaps in the forests, where old trees have fallen, more intense light briefly reaches the surface. Young trees sprout rapidly from huge seeds that provide concentrated nutrition for the race upward. Most are wrapped, entwined in clinging vines seeking to make the same journey. The competition for sunlight, space, and nutrients is fierce, and only a few young seedlings will survive and mature to old forest canopy trees. Small epiphytic plants, like orchids and bromeliads, cannot hope to compete with the towering trees, so they stand on the giants’ shoulders: by sitting on branches, they get closer to the precious sunlight above. The density and weight of these epiphytic plants eventually becomes so great, it is not unusual for huge moss and orchid-laden branches to crack, and come crashing to the forest floor.

  Along the Stream Trail the tree trunks soar high, like the pillars of a green basilica—the basilica of life. Quito is replete with human-built cathedrals, hundreds of years old, but I prefer the natural forest cathedral, millions of years old. All the trees are heavily matted with bromeliads, algae, lichens, and mosses. At close range, the surface of almost any log looks much like the mossy shoreline of a Silurian age stream—that miniature plant community where insects had their earliest terrestrial origins. These mosses still crawl with millipedes, centipedes, and microscopic wingless insects, as they have since the Late Silurian and Early Devonian. Along the path in the forest understory are ten-foot splayed tree-ferns, ancient survivors, reminiscent of the Devonian age forests where true insects first crawled, and later sprouted the earliest wings.

  At this high elevation, it is easy to imagine and appreciate the solar-panel hypothesis for the origin of insect wings. It is cold here, even though we are situated nearly on the equator. The elevation, the forest shade, and the ever-present water conspire to put a definite chill in the air by day. At night it is even more surprisingly cold. Passing the tall tree-ferns, I visualize Devonian-age insects basking themselves on the upper fronds. We have seen some of them today: machilid jumping bristletails on logs and stones, and primitive wingless diplurans under rotting logs and leaf litter—only slightly modified survivors of the ancient times.

  Pausing at a stream crossing, I see taller trees arching over the rivulet; a storm has dislodged one into the stream, from its eroded banks. The water is clotted with decaying, algae-matted, woody debris. I linger here to meditate on the Carboniferous times, and to visualize the masses of plant materials inundating the ancient waterways. At Yanayacu you can touch, smell, and feel the rotting plants, and maybe get a bootful of dark, tannin-tinted mud, suitable for fossilization—if only the insects, worms, algae, and bacteria don’t get to it first. It is easier to imagine the Carboniferous forests at this elevation, because here we are too high up for many termites, and the fallen mossy wood accumulates deeply. Lacking termites, as in Carboniferous days, the storm-wracked trees at Yanayacu, always dripping with water, are more slowly eroded by bacteria, algae, fungi, lichens, and even gigantic tropical earthworms. My coal-swamp reverie is gently broken by the flight of a damselfly along the streamway—an apt reminder of the Carboniferous insects that evolved large wings and could fly. The fair damsel pauses briefly on a fern frond until, disturbed perhaps by a raindrop, she continues her flight upstream. I break from my Carboniferous reflections and continue trekking downslope.

  As we make our way along the trail, I notice further that Yanayacu cloud forest is a mosaic of past survivors. We see the modern relatives of the Permian neuropterans, lacewings, and beetles. We see the descendants of Mesozoic sawflies, and the great-great-grandnephews of feathered dinosaurs still flit and twitter in the treetops. But the Cretaceous innovations—the social wasps, ants, flowers, and especially the exposed-feeding caterpillars—greet us riotously.

  Slipping briefly in the mud, instinctively catching my balance like a soggy Tai Chi master, I flash from my Mesozoic daydreams back to the present, and continue my Cenozoic reverie. We follow the watercourse now along slopes that were uplifted during the Cenozoic years. The chilled waters gurgle down toward the Amazon basin—but that is not our destination. For on the Andes’s eastern slopes, the insects will come to us. Over the course of millions of years, pulses of Amazonian insect species have migrated to the highlands and adapted to its cooler climate.

  My destination is the forest at the base of the stream trail. I reach the site with considerable anticipation and excitement. Anticipation, because near here, two years earlier, my graduate student, Andrew Townsend, fortuitously sampled a specimen of a new euphorine wasp species, which belongs to the group of microscopic parasitic wasps that has become the focus of my life’s research. Drew did not realize his discovery at the time, but I later found the new wasp among his samples when we studied them under microscopes in my remote Wyoming laboratory. My excitement doubled because the specimen was not only a new species, perhaps never seen before by human eyes, it was also a new genus.

  I have returned with my research team to search for more undiscovered insects. I am hoping to find more specimens of my new wasp genus, so we can better understand its variation, but I know that the task is daunting and has little chance of succeeding. Finding one rare three millimeter long wasp in the Ecuador cloud forest is far, far more difficult than attempting to find a needle in a haystack. If only it were that easy.

  We come armed with the knowledge of precisely where and when the wasp was collected, and we know a simple sampling method that might work: yellow pan trapping—the very method Drew used to collect his wasp. Bright yellow plastic bowls are placed along the forest trails. They are filled with slightly soapy water (in this case I’m adding a surfactant, the same stuff you put in your dishwasher to remove water spots), to reduce the surface tension so that tiny insects will more easily fall into the fluid. Flying insects see the Day-Glo yellow bowls as bright spots on the forest floor, and because many of them are strongly attracted to the color, they dive right in. In a dry climate like Wyoming the bowls would dry out quickly and need to be replenished. But at Yanayacu cloud forest the ever-present raindrops keep them filled. You just need to scan the bowls frequently to pick out promising specimens, or filter them out with a fine-mesh net.4 Drew placed 20 bowls and found one golden nugget. I’m here to up the ante by placing 200 along the same trails. But will the method work again? I am troubled by the thought that very likely the insect I’m searching for lives most of its life high up in the forest canopy. I may be hiking directly under thousands of them. Perhaps two years ago that one particular wasp randomly spotted a yellow dot on the floor and flew down to investigate. Perhaps decades might pass before anyone sees it again.

  Rise of the Imagobionts

  My worries, while realistic, proved to be unfounded. After four days of hard work we managed to find one more specimen of the new species, and by the end of the week I was very pleased to have found three of them. The field station manager, Jose Simbaña, had also been running yellow pan traps for ten days a month, every other month, for the last year. His trap samples consisted of pint-sized jars full of tens of thousands of microscopic insects, pickled in alcohol. By day we checked my yellow pans, and by night we worked in the laboratory, sifting through Jose’s samples one spoonful at a time. We looked at so many samples under the microscope that late at night I could close my eyes and see the burned-in images of insects floating in a sample dish. At the beginning of the week, I joked that when I found my wasp, everyone would know it because I would shout “Eureka!” By the time I finally found one, I was so physically and mentally exhausted that all I could manage was a low whistle and �
��Here it is.” I’d estimated that we looked at more than a hundred thousand other insects for each one of my new wasp species that we spotted. Why are some insects so numerous, while others are extremely scarce?

  FIGURE 10.1. A solitary male of a parasitoid wasp, Napo townsendi, perches on a Dendrophorbium leaf in the Yanayacu cloud forest in Ecuador. (Photo by Andy Kulikowski.)

  Different insect species have different behaviors that affect their population levels and relative abundance. In a forest like Yanayacu, good examples of very common insects are the fungus gnats. The maggots of these tiny flies breed in enormous numbers in the forest floor’s decaying leaves. The flies are everywhere, and they dive into the yellow pans like crazy. If you wanted to, you could easily sample hundreds of them in a morning’s work. Other insects, such as ants, are social, so again it’s not difficult to sample large numbers of them.

  My new wasps, on the other hand, are solitary insects that belong to a larger group (subfamily) of microscopic wasps known as the Euphorinae.5 They are also a special kind of parasitoid whose unusual biology contributes to their scarcity: they live and feed as immatures inside the bodies of other adult insects, such as beetles, bugs, bark lice, green lacewings, ants, bees, and even other parasitic wasps—a difficult kind of parasitism that I call imagobiosis.6 Adult insects are the least abundant life stage for any insect population, and are therefore harder to locate, compared with eggs or larvae. An adult insect is densely armored and may defend itself by biting, kicking, or spitting chemicals. It is fully mobile, so if all else fails it can run or fly away. How did imagobionts evolve to overcome these obstacles?

  In our previous discussions of parasitism, we considered idiobiosis, where venom is injected into the host insect, rendering it permanently paralyzed. Idiobionts tend to attack hosts that are embedded in plant tissues or wood (and are therefore barely moving in the first place) and alter them so they can’t move any more. That strategy for living and feeding worked really well when it was first developed back in the Jurassic days, and it still works well for tens of thousands of modern parasitic wasp species. But the idiobionts are pathetically slow at laying their eggs. A wasp that attacks beetle larvae concealed deep in wood commonly spends the better part of an hour or more just laying one egg. It needs to drill a hole through dense wood, insert its ovipositor, locate the host beetle, inject paralyzing venom, lay an egg, then withdraw its ovipositor from the plant substrate. Idiobiont wasps apparently could not evolve to attack mobile adult insects directly. An adult would get fed up and fly away before the wasp could get the job done. The evolution of the ability to parasitize adult hosts required koinobiosis.