May 2000

Kick aside a pile of fresh horse droppings, and a small cloud of flies is sure to explode around you. Maggots squirm in the nutritious sea of manure, and beetles scurry this way and that. Among the crowd of insects are the ones I have been studying for the past ten years: beetles in the genus Onthophagus. Small (often no bigger than the eraser on a new pencil) and sluggish, these beetles are easy to overlook as your eyes fix on other, faster, more brightly colored species or on beetles that are industriously pushing balls of dung away from the pile. But if you look closely, especially right where the dung meets the soil, you will be rewarded with a look at some of the most bizarre and—at their scale—formidable creatures on Earth.

There are 2,000 named species of onthophagine dung beetles, and certainly half again as many waiting to be described. They inhabit every continent except Antarctica and can be found as readily in tropical rainforests as in temperate pastures, African savannas, and the Australian outback. They feed on almost every type of dung imaginable, from cow to kangaroo and toad to tapir.

Despite this variety of habitats, all these beetles do basically the same thing: they fly to pieces of dung and dig tunnels in the soil below it. The females then pull small pieces of dung into the tunnels, fashion them into balls, and lay one egg inside each ball. A few days later, when the eggs hatch, the young larvae feed on the dung in relative peace, shielded from the competitive aboveground world.

The bodies of onthophagine beetles reflect their subterranean lifestyle. Durable, ovoid digging machines, they have a smooth, rigid exoskeleton and sharp, toothed forelegs, which they use to dig into sun-scorched clay and other hard soils. Like the front end of a bulldozer, a dung beetle's head is flattened into a broad plate that can push soil up and out of the tunnel; lying safely beneath this protective shield are its delicate organs of taste and vision.

The exceptions to this streamlined body plan are the knobs, barbs, and spikelike outgrowths that protrude from the males. You might need a magnifying glass to see these “horns” clearly, but in many species they rival the antlers of bull moose in both shape and proportion. The largest males produce the biggest horns (small males and females generally have none). In some species, such as O. nigriventris, they may be longer than the rest of the body.

Why produce such extravagant horns? They make it difficult even to fit into a tunnel, let alone run, turn, or maneuver inside one. My work has led me to conclude that the tunnels themselves—and the need to guard the females breeding inside them—are key to the evolution of the horns.

With the help of glass observation chambers, video cameras, and plenty of patience, my team at the University of Montana and researchers at several other institutions have been watching these beetles inside their tunnels. The first thing we learned was that provisioning the eggs is a laborious process. One female in the species O. acuminatus made more than fifty separate trips to the surface to collect enough dung to make just one brood ball; over the course of several days, a female might make five to twenty such balls.

A female dung beetle in her tunnel is sure to attract suitors big and small.

Immediately before and during egg laying, the female essentially lives under the ground. This presents the male of the species with a challenge: to mate with the female, he must get inside the tunnel. It also presents him with an opportunity: once inside, if he can keep rival males away, he can mate repeatedly with the resident female and be the only one to fertilize her eggs.

And this is precisely what many males endeavor to do. The first hurdle is the tunnel entrance. Standing guard here, the resident male will try to fight off other males that attempt to enter. In a typical contest, the resident male braces himself against the tunnel walls and uses his head and long horns to block entry or to push the rival out. An intruding male, for his part, tries to squeeze past the resident male. By wedging his head beneath the other beetle and pushing or twisting, the challenger may create a gap into which he propels himself. The resident male's horns get in the way, however, and the two males usually end up locking head to head. Sometimes brute strength and strategic maneuvers enable the intruder to force his way past the guard and into the tunnel, where the sparring resumes. At times, the previous resident is pushed all the way out of the tunnel and has to try to fight his way back in.

Fights between males may last only a few seconds or may entail half an hour of head butting and sparring. Although the sequence of events during a fight varies, the outcome is remarkably predictable. I staged contests between O. acuminatus males, for example, and found that the winner is generally the bigger individual and, in particular, the one with the longer horns. Duke University graduate student Armin Moczek and I have found an identical outcome for a second species, O. taurus. Since success at guarding tunnels—thanks in part to horns—translates into success at passing genes on to future generations, this process of selection could easily have led to the evolution of bigger and bigger horns. Indeed, the males of many species have such large horns that often they cannot even turn around inside a tunnel but instead must push all the way down to the enlarged brood chamber below, or must back all the way up and out the entrance, before they can turn and face the other way.

There is, however, a twist to this story. Not all the males in each species are large, and not all the males grow horns. In fact, the males in the populations I study come in two basic classes: large, with horns, and small, with either very rudimentary horns or none at all. For a small male, fighting is not an effective option; the only way he can reach a female is on the sly. Sometimes he will wait until the guarding male leaves the tunnel briefly (returning to the dung pile to feed, for instance) and then dash inside to find the female. If he is small enough and smooth enough, he may even be able to sneak right past a guarding male without being detected.

The small O. acuminatus male has another ploy if these tactics fail. He may move a short distance away and excavate a tunnel of his own. After burrowing about half an inch below the surface, he cuts horizontally and sometimes succeeds in intercepting the guarded tunnel below the surface. Having evaded the guarding male, the “sneaker” male mates with the female and then returns to his side tunnel and waits. Hours later, he either tries to reenter the guarded tunnel or continues to dig horizontally. In a densely excavated area, one of these small males may gain access to several guarded tunnels via a single side tunnel of his own.

For her part, the female does not discriminate among suitors, mating readily with both sneaker and guarding males. Unfortunately for the sneak, a single mating does not guarantee that he will sire offspring. The female has undoubtedly already mated with the guarding male and is likely to do so again after the smaller male leaves. And if the resident male detects the intruder, he will not only chase him out of the tunnel but will rush back to copulate again with the female. Still, a persistent small male may be able to get inside a tunnel several times, and one of those times might be just when the female is ready to lay an egg.

Horns may grow at the expense of other body parts. Depending on the species, big horns may mean smaller eyes, wings, or antennae.

A second way that small males deal with the competition is by producing—and transferring—more sperm than their larger counterparts. Leigh Simmons, Joe Tomkins, and John Hunt, of the University of Western Australia, found that small O. binodis males had disproportionately large testes. These males also ejaculated more seminal fluid and produced longer sperm than did their guarding competitors. Hence, smaller males (which make up about 50 percent of the male population) may compensate for having fewer matings by transferring more sperm each time they copulate, thereby increasing the odds that they will fertilize an egg each time they do mate.

Onthophagine beetles are not the only invertebrates to have two classes of males, each with its own mating strategy. In the ground-nesting bee Perdita portalis, for example, Bryan Danforth, now at Cornell University, found that large males have exaggerated mandibles that they use in contests over subterranean burrows containing females. Because the smaller males lack these large mandibles, their only chance of mating is to intercept a female as she forages on a flower. Paracerceis sculpta is a marine isopod studied for many years by Stephen Shuster, now at the University of Northern Arizona. In these creatures, males come not in two but in three morphs, each with its own specialized way of encountering females.

What determines which embryos or larvae will pursue a macho path and which will become little sneaks? In the isopods Shuster studied, both the morphology of a male and his mating tactics depend primarily on the genes inherited from the parents. In the beetles I study, it turns out, horn growth is more flexible and is affected by the course of larval development. Supplied with ample food for their entire larval stage, males become large and develop long horns. Larvae that run out of food prematurely do not grow as large, and if they fail to reach a critical minimum body size, they dispense with horn production altogether. The physiological “decision” whether or not to produce horns occurs toward the very end of the larval feeding period. H. Frederik Nijhout, of Duke University, and I discovered that painting minute amounts of what is called juvenile hormone onto small males at this time causes them to produce horns despite their small size, suggesting that this hormone is the critical link between male body size and horn production. With insufficient juvenile hormone, horn growth never starts.

Onthophagine beetle horns begin when small sections of the larval skin, or epidermis, start growing rapidly. In O. taurus, there are two such regions of rapid growth, one on each side of the head. The horns are not visible in the larval stage because they are trapped under the cuticle and thus forced to grow inward, as dense clusters of folded tissue. When a male molts from a larva to a pupa, the horns evert, unfold, and stretch out to their full shape and length—not unlike extending a collapsed telescope. During the final molt, from pupa to adult, the epidermal cells secrete special enzymes that rigidify the horns as well as hardening all the other adult structures.

Growing horns takes time. In O. taurus, Hunt and Simmons found, the process adds several days to a larva's development. This extra time is dangerous, they suggest, because it significantly increases the larva's risk of falling prey to nematodes in the soil. And horns are likely to continue to exact a cost even after the beetles have emerged above ground: males must fly from dung source to dung source in order to locate females, and bulky horns may make flight slower, clumsier, or more energy draining, possibly increasing the risk that these males will be spotted and captured by predators.

Constituting up to 15 percent of a male's total body weight, horns also require nutrients, energy, and other resources to grow. Dung beetle larvae develop in isolation, with nothing to feed on but the dung in which their mother packed the eggs. In this world of finite resources, devoting a portion of their share to horns means making less available for other body parts. O. acuminatus and O. taurus males, for example, cannot have both long horns and large eyes: horned individuals have fewer ommatidia, or eye facets (making their visual field like a computer screen with fewer pixels). When Nijhout and I experimentally manipulated the growth of male horns, we found that suppressing horn development resulted in larger eyes.

The beetles develop in isolation, with nothing to feed on but the dung in which their mother packed the eggs.

Various tradeoffs occur in other Onthophagus species. In some, horns extend from the thorax, and my preliminary data suggest that in this case, horns grow at the expense of wing size. In other species, horns extend from the front of the face, where they seem to squelch the antennae. Different types of horns thus incur different types of costs.

As we tease apart the factors shaping the horns, we are realizing just how intricate and numerous are the connections between ecology, evolution, and development. Discoveries in one arena open up exciting and often unanticipated research questions in the others. I suspect we will be spying on these little black beetles for a long time to come.

As a graduate student, Douglas Emlen was looking for a splashy beetle with big horns to study. When biologist William Eberhard showed him a box of tiny black dots and said, “These are the beetles you should work on,” he was reluctant. Now, a decade later, he is very glad he took the advice. Onthophagine dung beetles—in addition to having impressive horns (if you look very closely) and interesting mating behavior—are nearly ubiquitous, which makes them perfect for studying both in the laboratory and in the field. They have taken him to Panama, Ecuador, Australia, and several parts of the United States. Emlen hopes next to explore species in which gender roles are reversed--that is, in which the females wear the horns. Emlen is assistant professor in the Division of Biological Sciences at the University of Montana in Missoula.

Copyright © 2000 American Museum of Natural History

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