Animal Weapons

by Douglas J. Emlen

  I was selecting only five individual males and ten females to found each generation. This is a small sample, and it meant that some shift in the traits of my population could have occurred by chance. If, at the end of my experiment, the males in my artificially selected population had longer horns than before, I couldn’t rule out the possibility that this was a spurious result due to chance.

  To confirm my findings, I would have to do the whole thing again. If you have not one, but two separate populations, both experiencing directional artificial selection for longer horn lengths, and they both result at the end in males with longer horns, it’s a much more compelling result. Random changes are not likely to occur in the same direction both times. Even better, add still more populations selected in the opposite direction—males with the shortest horns selected as the breeders—and keep them in the lab at the same time, feed them the same food, sample the same tiny number of individuals as breeders, and repeat the process for the same number of generations.

  If several generations later we find that in both of the populations selected for long horns, males end up with longer horns than before, and in both of the populations selected for short horns, males have horns that are shorter than before, then we can begin to rule out chance. In fact, I conducted my experiment on six distinct populations of beetles simultaneously. In two of the populations I artificially selected for longer horns in males; in two other populations I selected for shorter horns in males; and in the final two populations I chose the males at random. Keeping all these beetles supplied with food meant many, many mornings racing through the forest in search of monkeys. For six hundred sunrises I combed the damp understory, collecting bags of monkey dung to bring back to the lab so that I could feed the beetles of this huge experiment.2

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  Two years and seven beetle generations later, I had my answer. The weapons had evolved. Males in populations selected for longer horns now sported weapons that were proportionately larger than they had been before, and males in populations selected for shorter horns had weapons that were proportionately smaller. Each of these extremes differed from the populations that had acted as controls, and I’d shown convincingly that animal weapons can evolve fast.3 But weapons weren’t the only trait that changed; increases in horn size came at a price.

  As weapons get big they also get expensive, and males with the longest horns now had stunted eyes. By the end of the experiment, males selected for longer horns had eyes that were 30 percent smaller than males selected for shorter horns. Stunted growth arises because of a limited availability of nutrients. Tissues require energy and materials to grow, and allocating resources to the production of one structure can mean that those same resources are no longer available for the growth of another.

  Resource allocation trade-offs shape the development of all animals, but most of the time the effects are trivial. When animals begin to invest unusually heavily into particular structures, however, the effects of trade-offs become more pronounced. Weapons caught up in arms races get very big very fast, and in these species resources channeled into growth of the weapons can drastically impair bodily functions. In insects, this sometimes means reduced growth of other body parts.4

  In dung beetles, we now realize, horn growth stunts the growth of eyes, wings, antennae, genitalia, and testes, depending on the species.5 In exchange for fighting ability males suffer impaired visual acuity, flying agility, smell, and success in copulation—hefty prices for producing weapons—and similar trade-offs curtail a variety of species with extreme weapons. For example, giant rhinoceros beetles with massive horns have proportionately smaller wings,6 as do stag beetles with the most distended mandibles.7 Even male stalk-eyed flies face impaired testes growth when they invest in large weapons.8

  Male dung beetles with long horns have proportionately smaller eyes.

  Wing reductions in soldier castes of social insects are still more extreme. Big-headed soldiers in bees,9 ants,10 and termites have severely reduced wings and wing muscles, and, most of the time, these fighters are completely wingless. The price for winning fights is not merely impaired flight; it’s an inability to fly.

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  Stunted growth of body parts is just one of many types of price that males pay for their weapons, and the bigger weapons become, the more they cost. Caribou antlers can exceed five feet in length and weigh more than twenty pounds—8 percent of the total body weight of a male. Moose antlers reach spans of six and a half feet weighing forty pounds, and the antlers of the largest extinct “Irish elk” spread more than fourteen feet across and weighed two hundred pounds. However, relative to body mass, the prize for largest animal weapons goes not to the elk, or even to a beetle, but to the fiddler crab, whose enlarged claw can weigh in at half the total weight of a male.11 Half of the resources available to a growing male crab are allocated to weapon growth.

  Stag beetles with big mandibles have smaller wings.

  Not only are the claws bulky and heavy structures to build, they are energetically costly structures to maintain. Crab claws are not mere hollow threats; they are packed with powerful muscles that can crush the skeletal shells of rival males. Muscle tissue is incredibly energy demanding, because muscle cells are loaded with dense concentrations of mitochondria, the microscopic organelles responsible for converting stored nutrients and oxygen into usable energy. Mitochondria are often called the “cellular power plants,” and inside muscle cells they provide energy needed to contract the muscle and close the claw.

  Because of their many mitochondria, muscle cells are expensive to maintain even when they are resting, and males with big claws have the most muscle. Male fiddlers burn energy like crazy to keep their muscle cells alive. Resting metabolic rates of males with big claws are almost 20 percent higher than those of females (who lack enlarged claws) simply because of the costly muscles inside the claw.12 Waving the claw around or using it to fight is even more expensive, and the bigger the claw, the steeper the energetic costs.13

  Running with a bulky claw is also energetically demanding. Bengt Allen and Jeff Levinton devised a clever way to trick fiddler crabs into running on treadmills sealed inside airtight boxes. As the crabs ran, their muscles churned through contraction after contraction, burning oxygen and releasing carbon dioxide into the sealed container. Allen and Levinton measured the changes in concentration of these two gasses as each crab ran its treadmill race and, from this information, they calculated precisely the metabolic cost of running. Imagine running with a big bag of dog food in your arms, and it should come as no surprise that males with large claws burned more energy as they ran than males with smaller claws, or than females without enlarged claws. Actually, let’s be fair to the crabs. To put this in proper perspective, imagine carrying a load that is equal to the weight of your body, as the largest of these claws can be (so, in my case, running with three fifty-pound bags of dog food and a cinder block in my arms). Good luck with that! Crabs with larger claws burned a lot more energy than crabs with smaller claws, and they tired much more quickly.14 Male endurance on the treadmills suffered because of the extraordinary loads that they carried.

  And the list of costs goes on. Female fiddler crabs have two frontal claws that they use to feed, plucking morsels of organic material from the sand and mud. This style of feeding is a delicate and tedious process, and the feeding claws of female fiddlers work incessantly as they scavenge. Males, on the other hand, have only one feeding claw because the other is grossly enlarged into the fighting weapon. The giant “major” claw of males is useless for feeding, so the males must make do with just the one. This can halve the rate of food intake for these already-energy-starved males, and males are forced to compensate either by spending more time feeding,15 or by feeding faster,16 with their remaining claw.

  More time feeding means more time exposed to predators, and these exposed males are cumbersome, heavy, and awkward because of their claws—a dangerous combination. Several field studies of fiddler crabs h
ave now shown that males suffer disproportionately at the hands of avian predators. In my favorite example, John Christy and his colleagues, including Patricia Backwell and Tsunenori Koga, studied a natural population of the fiddler crab Uca beebei on mudflats along the Pacific coast of Panama. They found that fiddlers were heavily preyed upon by great-tailed grackles, and that these birds had a quirky strategy for catching the crabs. Grackles often employed a “feinting reverse lunge” as they chased a crab. Instead of charging directly at a crab, they would charge to the side of the target crab, seemingly passing it by. As soon as they’d passed, they would whirl and lunge backward in a surprise diagonal feint that often caught the crab unaware. Grackles that did this were twice as effective at catching crabs as birds who simply ran straight at a crab and, remarkably, when birds employed the reverse-feint method, they caught almost exclusively males.17 Male crabs, by virtue of their distorted major claws, were more conspicuous targets to the lunging bird. The result: in this population, male fiddlers suffered dramatically higher predation than females.

  Increased exposure to the risk of predation turns out to be an almost universal cost to males for the burden of producing and wielding elaborate weapons. In fiddler crabs, higher predation can result from males being more conspicuous targets;18 from their poor endurance and awkward, slower escape performance;19 and even from predators actively seeking them out as preferred prey (the extra muscle inside the claw makes them more nutritious than female crabs).20

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  The best estimates of the costs of weapons come from studies of deer. Deer don’t fit nicely into little plastic tubes, and they take a lot longer than dung beetles to complete their development. This makes artificial selection experiments problematic. But there are other ways to study sexual selection, and deer have proven to be ideal for many of these. For one thing, they are large, conspicuous, and relatively easy to watch. Deer are also easy to mark and follow as individuals, making it possible to track the fighting and mating success of dozens of different males, and the fawning success of comparable numbers of females. In addition, antlers are shed by males and regrown each successive year. Shed antlers can be weighed and measured and even ground up or incinerated to calculate the caloric and mineral content of the weapon.

  Long-term monitoring of individual bulls can reveal how much time they spend foraging, chasing females, and fighting. Darting them with sedatives lets biologists have access to each male for an hour or so to measure their height, weight, and age (determined from the teeth), as well as count external parasites and sample blood to measure internal parasites and infections. Collecting this information before the breeding season—the rut—and then again after this season, and comparing these values, can shed light on just how expensive this whole mating process is to a male. In fact, rutting stags lose a stunning amount of body weight, and their physical condition plummets during the rut. Weapons, and the stamina, testosterone, and aggression that necessarily go with them, can be devastating to the health of a male.

  Fallow deer (Dama dama) slide in neck and neck with caribou as the living species with the most extreme antler sizes. Fallow deer are native to Eurasia, and archaeological excavations in Israel suggest that they were an important source of meat for people as far back as the Paleolithic period (nineteen thousand to three thousand years ago). This species of deer was carried across central Europe by the Romans and introduced into the United Kingdom by at least the first century CE. Today, one of the best-studied populations resides in a rather unusual setting—an urban park inside the city limits of Dublin, Ireland.

  Phoenix Park is no typical city park. It’s one of the largest walled parks in Europe, with more than 1,750 acres of grasslands, hills, and forest. True, it is interspersed with tree-lined avenues and sidewalks, and the study animals do sometimes intermingle with an eclectic assortment of picnickers, joggers, and the occasional parade. But the deer in this population have lived their lives and died unmolested since the 1600s, and their rich and dramatic mating behaviors are on display for all to see.

  The antlers of fallow deer flatten into giant, curved spoons with tines projecting in a ring from the outer edges like fingers splayed from the palm of a hand. A large buck may have as many as seventy tines fringing the perimeter of his antlers, and their full spread can reach wider than the male is long, a span of more than nine feet. For five weeks in September and October each year, rutting males wave these bulky antlers and bark from small display territories that they guard vigorously. They scream their throaty barks until they are hoarse, and they scrape at the soil, soaking each patch of exposed dirt with testosterone-laden urine to attract females and deter rival males.

  Thomas Hayden and Alan McElligott have followed this population for more than fifteen years, during which it averaged between 300 and 700 animals. They were able to observe the rutting behavior and fighting and mating success over the entire lifetimes of 318 different males, recording who won the fights, who actually succeeded in mating, and how many offspring they sired. They also examined the costs that males paid: how much weight each male lost; how sick he ended up; and whether he was able to make up the lost weight before the onset of winter.

  Not all males fared equally. In fact, in terms of reproductive success, an overwhelming majority of them failed miserably. Three-quarters of the males died before they were large enough—armed heavily enough—to succeed in guarding a territory, and 90 percent of the males never managed to mate with a female even once in their lifetime.21 Of the males who did reach critical size and rank, most suffered catastrophic losses to their body condition as they battled for their tiny pieces of real estate, accumulating stress, slashes, parasites, and pathogens as they locked in battle after battle for territories that the females often ignored anyway.

  Fighting for display territories and the females they might attract was a round-the-clock chore, with males averaging fights every two hours day and night for the duration. Males were not feeding during most of this time, and the displays and fights themselves were extremely energetically demanding. The result was that males typically lost more than a quarter of their body weight during this period. For a typical male, this was more than sixty pounds. By the end of the rut, most of the males were starved, exhausted, riddled with parasites, and nursing battle scars ranging from scrapes and bruises to broken bones and gashes. These battered bucks had only a few short weeks to regain their health and weight before the onset of winter. Males who failed to recoup these losses often died before the following spring.

  Ron Moen and John Pastor used an entirely different approach to measure the price that male moose pay for weapons. By quantifying exactly how many milligrams of each mineral, carbohydrate, lipid, and protein an animal eats, and feeding this information into complex biochemical models of the physiology of vertebrate tissues, they were able to calculate precisely how much a male must shunt away from other body functions in order to sustain weapon growth.22 What they showed was that antler growth in moose demanded 50 percent more energy per day from a male across the growing season, with peak demands reaching 100 percent (literally doubling the basal metabolic rate of all of the rest of the tissues of the body). Summed across the period of antler growth, this resulted in energetic demands as high as five times the energetic requirements of simply maintaining their bodies.23

  Protein requirements of antlers were also high, but protein proved not to be limiting to these animals because the males could secure the extra protein they needed for antler growth through increased foraging. Interestingly, the crucial ingredients turned out to be calcium and phosphorus, both of which were absolutely critical to bone growth in the antlers, and neither of which was readily available to the animals as forage. In both moose and caribou, the calcium and phosphorus demands were so high that animals had to “borrow” these minerals from the other bones in their bodies in order to build their antlers. They could not get enough from their diet, so they pulled calcium and phosphorus from their own skeletons,
reallocating them to the antlers. This is truly a form of deficit spending for these animals because it is not sustainable. The depleted skeletal reserves have to be replenished through feeding after the rut, and failure to do so is generally catastrophic.

  All told, antlers in these animals turned out to be every bit as costly to a male as reproduction was to a female: the cost of building and using antlers was energetically and nutritionally equivalent to the cost of producing and nursing two fawns to weaning. Antler growth dramatically reduces bone mass overall, rendering males more fragile, more brittle, and much more prone to bone breaking. In essence, antler growth induces a seasonal form of osteoporosis exactly when animals are engaged in the most physically demanding and dangerous activities of their lifetimes. The rut is the worst possible time for males to suffer weakened and brittle bones, because this is when they put their strength to the test again and again in relentless brutal battles for dominance and reproduction. Antler-induced seasonal osteoporosis is no doubt part of the reason that, in many large deer species, fighting results in serious injury. Male moose suffer high incidences of fractured ribs and scapulas.24 In red deer, a quarter of all reproductive males suffer bone breakage or other damage from battles during the rut, and 6 percent of stags are irreparably injured each year.25 In bull moose, 4 percent of males are killed each year from injuries sustained during the rut and, across their reproductive lifetime, a third will die from injuries inflicted in battle.

  In a clever extension of this research, Moen, Pastor, and Yosef Cohen applied their model to the extinct giant deer Megaloceros giganteus, otherwise known as the Irish elk. Technically, these deer were neither elk nor especially Irish. Close relatives of fallow deer, Irish elk were widely distributed throughout Europe, northern Asia, and northern Africa, until they eventually went extinct around 11,000 years ago. Most fossil specimens of this species are from Ireland (thus their moniker), from lake deposits of the Allerød period between 12,000–11,000 years before present. These magnificent deer produced the largest antlers known for any species, spanning twelve feet across in the largest bucks.