Cannibalism

by Bill Schutt

  “These look like two different species,” I said, examining a handful of tadpoles that I’d just scooped up. I also noted that the larger individuals were light tan in color while the little guys had bodies flecked with dark green.

  “Initially, people thought they were different species,” Pfennig replied.

  Using a magnifying glass to get a better look at my squirmy captives, I saw that the differences went beyond body size and color. The larger tadpoles were also sporting powerful tails and serious-looking beaks.

  “Yikes, nice choppers,” I commented, always the scientist.

  “They’re made of keratin,” Pfennig said. This was the same tough, structural protein found in our nails and hair.

  Later, while comparing the two tadpole morphs under a dissecting ’scope, I saw that behind a set of frilly lips, the flat keratinous plates (which worked fine for detritus dining) had been transformed into a jack-o-lantern row of sharp-edged teeth in the cannibalistic forms. It was also evident that the jaw muscles were significantly enlarged in the cannibals, especially the jaw-closing levator mandibulae, whose bulging appearance reminded me of a kid with six pieces of Dubble Bubble jammed into each cheek (a dangerous behavior I only rarely attempt anymore ). Studies had shown that myofibers, the cells making up these muscles, were larger and greater in number (or hypertrophied and hyperplasious, respectively)—producing a more powerful bite. Of course, the extra bite force was necessary because, beyond latching onto the occasional unshaved human leg, these critters were using bulked-up bodies and the weaponry that accompanied it to subdue and consume their omnivorous pondmates.

  Not quite so obvious was a significant shortening of the gastrointestinal (GI) tract in the cannibals, with the explanation relating to the dietary differences that accompanied the tadpole transformations. In the omnivores, a long GI tract is required for the breakdown of tough-to-digest plant matter, while a shorter GI tract works just fine when the diet is a fleshy one.4

  Over a three-day period, I watched and captured tadpoles in bodies of water that ranged from tire-carved puddles to bovine swimmin’ holes of the double-wide Olympic variety. Accompanied at various times by Pfennig, his wife, Karin, their two young daughters, and a pair of extremely personable UNC grad students, Antonio Serrato and Nick Levis, I learned a great deal about the three species of Spea that laid their eggs in such dangerously unpredictable conditions. Much of this information centered on the ecology, behavior, and evolution of these creatures. Of course, the cannibalism angle was there as well, although these researchers (including the kids) treated that particular behavior as perfectly normal.

  Until relatively recently though, and with a very few exceptions, cannibalism in nature would have been regarded as anything but normal. As a result, until the last two decades of the 20th century, few scientists spent time studying a topic thought to have little, if any, biological significance. Basically, the party line was that cannibalism, when it did occur, was either the result of starvation or the stresses related to captive conditions.

  It was as simple as that.

  Or so we thought.

  In the 1970s, Laurel Fox, a University of California Santa Cruz ecologist, took some of the first steps towards a scientific approach to cannibalism. She had been studying the feeding behavior of predatory freshwater insects called backswimmers (belonging to the order Hemiptera, the “true bugs”). Fox determined that, while the voracious hunters relied primarily on aquatic prey, “cannibalism was also a consistent part of their diets.”

  I contacted Fox and asked her about the transition that had taken place in the scientific community regarding this behavior. She told me that her observations in the field had sparked her interest and that, soon after, she began compiling a list of scientific papers in which cannibalism had been reported. Although there turned out to be hundreds of references documenting the behavior in various species, no one had linked these instances together or come up with any generalizations regarding the behavior. By the time Fox’s review paper came out in 1975, she had concluded that cannibalism was not abnormal behavior at all, but a completely normal response to a variety of environmental factors.

  Significantly, Fox also determined that cannibalism was a far more widespread occurrence than anyone had previously imagined and that it took place in every major animal group, including many that were long considered to be herbivores . . . like butterflies. She emphasized that cannibalism in nature, which some researchers referred to as “intraspecific predation,” also demonstrated a complexity that seemed to match its frequency. Fox suggested that the occurrence of cannibalism in a particular species wasn’t simply a “does occur” or “doesn’t occur” proposition, but was often dependent on variables like population density and changes in local environmental conditions. Fox even followed cannibalism’s environmental connection onto the human branch of the evolutionary tree. After pondering reports that humans practicing non-ritual cannibalism lived in “nutritionally marginal areas,” she proposed that consuming other humans might have provided low-density populations with 5 to 10 percent of their protein requirements. Conversely, she suggested that cannibalism was rare in settlements where populations were dense enough to allow for the production of an adequate and predictable food supply.

  In 1980, ecologist and scorpion expert Gary Polis picked up the animal cannibalism banner and began looking at invertebrates that consumed their own kind. Like Fox, he noted that while starvation could lead to increases in the behavior, it was certainly not a requirement. Perhaps Polis’s most important contribution to the subject of cannibalism in nature was assembling a list of cannibalism-related generalizations under which most examples of invertebrate cannibalism could be placed. 1) Immature animals get eaten more often than adults; 2) Many animals, particularly invertebrates, do not recognize individuals of their own kind, especially eggs and immature stages, which are simply regarded as a food source; 3) Females are more often cannibalistic than males; 4) Cannibalism increases with hunger and a concurrent decrease in alternative forms of nutrition; and 5) Cannibalism is often directly related to the degree of overcrowding in a given population.

  Polis emphasized that these generalizations were sometimes found in combination, such as overcrowding and a lack of alternative forms of nutrition (a common cannibal-related cause and effect), both of which now fall under the broader banner of “stressful environmental conditions.”5

  In 1992, zoologists Mark Elgar and Bernard Crespi edited a scholarly book on the ecology and evolution of cannibalism across diverse animal taxa. In it, they refined the scientific definition of cannibalism in nature as “the killing and consumption of either all or part of an individual that is of the same species.” Initially the researchers excluded instances where the individuals being consumed were already dead or survived the encounter—the former they considered to be a type of scavenging. Eventually, though, they decided these were variants of cannibalistic behavior observed across the entire animal kingdom. Although there are certainly gray areas (encompassing things like breastfeeding or eating one’s own fingernails), my fallback definition of cannibalism for this book is: The act of one individual of a species consuming all or part of another individual of the same species. In the animal kingdom, this would include behavior like scavenging (as long as the scavenged body was from the same species as the scavenger) and maternal care in which tissue (i.e., skin or uterine lining) was consumed. In humans, cannibalism would extend beyond the concept of nutrition into the realms of ritual behavior, medicine, and mental disorder.

  As the study of cannibalism gained scientific validity in the 1980s, more and more researchers began looking at the phenomenon, bringing with them expertise in a variety of fields. From ecologists we learned that cannibalism was often an important part of predation and foraging, while social scientists studied its connection to courtship, mating, and even parental care. Anatomists found strange, cannibalism-related structures to examine (like the keratinous beak of the spade
foot toad), and field biologists studied cannibalism under natural conditions, thus countering the previous mantra that the behavior was captivity-dependent.

  By the 1990s, Polis’s generalizations had been observed among widely divergent animal groups, both with and without backbones, supporting the conclusion that the benefits of consuming your own kind could outweigh the often substantial costs. Once these generalizations became established, and as a new generation of researchers built upon foundations constructed by pioneers like Fox and Polis, cannibalism in nature, with all of its intricacies and variation, began to make perfect evolutionary sense.

  Arizona’s lowland scrub stood in stark contrast to the lush peaks and bolder-strewn valleys of the state’s Chiricahua Mountains. These “sky islands” (isolated mountains surrounded by radically different lowland environments) provided a spectacular backdrop for my afternoon wade through yet another transient pond.

  The air temperature had risen to 95 degrees Fahrenheit, which kept most of the area’s terrestrial denizens hiding in shade or below ground, but the inhabitants of Horseshoe Pond reminded me of sugared-up kindergarteners tearing around a playground (albeit with fewer legs and more cannibalism). By this time, I had already begun to see distinct patterns of behavior in the spadefoot tadpoles that motored hyperactively just below the water’s surface.

  I noticed that the smaller, omnivorous morphs generally stuck to the shallows bordering the shoreline. They buzzed through the brown water in a non-stop, seemingly random quest for food, changing direction abruptly and often. One explanation for the patternless swimming behavior became apparent as I waded farther away from the shore, for here in the deeper water was the realm of the cannibals. I stood quietly and watched as hundreds of conspicuously larger tadpoles crisscrossed the pond, making frequent excursions from the deeper water toward the shore in a relentless search for prey.

  Immature animals get eaten more than adults, I thought. Certainly, although in this case the youngsters were eating each other.

  “They remind me of killer whales hunting for seals,” said Ryan Martin, a former student of Pfennig’s, now a professor at Case Western Reserve, who was also studying spadefoot toads here in Arizona.

  Martin’s comparison was spot on, and I threw him a nod, watching as a tiny hunter swam away from the shore with an even tinier pondmate clamped tightly between its serrated jaws.

  So why did the local spadefoot larvae exhibit cannibalistic behavior? There certainly seemed to be enough organic matter suspended in these algae-tinted ponds to feed the entire brood and more.

  As I spoke to Pfennig and his team of researchers, I learned that the answer was directly linked to the aquatic environments in which the adult amphibians deposited their egg masses.6 Formed by spring and early-summer monsoons, the transient ponds frequented by the spadefoots (spadefeet?) are often little more than puddles, and as such they can evaporate quite suddenly in the hot, dry environment of southeastern Arizona. Natural selection, therefore, would favor any adaptations enabling the water-dependent tadpoles to “get out of the pool” as quickly as possible (i.e., to grow legs). In this instance, the phenomenon that evolved can be filed under the rather broad ecological heading of phenotypic plasticity: When changing environmental conditions allow multiple phenotypes (observable characteristics or traits) to arise from a single genotype (the genetic makeup of an organism). To clarify this concept, here are a couple of non-cannibalism-related examples.

  Water fleas (Daphnia) are tiny aquatic crustaceans, named for a swimming style in which they appear to jump like fleas. In response to the appearance of backswimmers (Laurel Fox’s favorite predatory insects), Daphnia develop tail spikes and protective crests. Although the genetic potential for body armor is always there (in the Daphnia’s genotype), it doesn’t exhibit itself until a specific environmental change occurs, in this case the arrival of Daphnia-munching backswimmers.

  Here’s another example, unrelated to cannibalism. The reef-inhabiting bluehead wrasse (Thalassoma bifasciatum) is famous for its habit of removing parasites from much larger fish, even entering into their mouths. In this case, however, it’s the removal of a male wrasse from its harem of 30 to 50 females that alters their local environment. Rather than waiting for a new male to arrive, something extraordinary takes place in the harem. Within minutes, one of the females begins exhibiting male-typical behaviors. Relatively quickly, the former female transforms into a male, a form of phenotypic plasticity known in the trade as protogyny. The opposite occurs in protandry, in which individuals begin life as males and transform into females. Examples include the clownfish (Amphiprion), whose behavior could have offered an intriguing alternative resolution to the animated film Finding Nemo.

  In spadefoot toads, though, it’s not the appearance of a predator or the loss of a harem’s personal sperm bank that initiates the alternate phenotype (i.e., cannibalistic larvae). The selection pressure lies in the temporary nature of the brood ponds, where the eggs are deposited and hatch and where the tadpoles develop into toadlets. The period from egg to juvenile toad normally takes around 30 days unless, that is, the pond dries out first, killing the entire brood. In response to this particular environmental selection pressure, what evolved was a means by which some of the tadpoles can mature in about two-thirds of the time (20 days). The increased growth rate occurs because the cannibal larvae are getting a diet high in animal protein as well as a side order of veggies, the latter in the form of nutrient-rich plant matter their omnivorous prey had consumed during what turned out to be their last meal.

  In an interesting note, Spea couchii does not transform into cannibalistic morphs but has evolved an alternative solution to the transient pond problem. Couch’s spadefoot can go from egg to toad in only eight days—an amphibian record.

  Though the story of spadefoot toad cannibalism has been well researched, it is not fully resolved. The reason is that no one has been able to identify the precise stimulus within these brood ponds that triggers the appearance of the cannibal morphs. Until recently, the prime candidates were a pair of microscopic fairy shrimp species (order Anostraca). David Pfennig and his colleagues proposed that the consumption of the shrimp by some of the spadefoot tadpoles served to trigger the cascade of genetically controlled developmental changes that transformed the shrimp-munchers into outsized cannibals.

  But what was it about eating fairy shrimp that set this transformation into motion? Pfennig hypothesized that iodine-containing compounds found in the shrimp might cause the activation of specific genes in the tadpoles, genes that weren’t turned on in the individuals that didn’t consume shrimp. The prime candidate for a trigger substance turns out to be thyroxin, a thyroid hormone whose functions include stimulating metabolism and promoting tissue growth. A new set of experiments, though, have shown that even tadpoles that weren’t fed fairy shrimp could still undergo the transformation to cannibals, indicating that (at the very least) something besides thyroxin intake must initiate the changes.

  “What if it’s not what they’re eating but the mechanism of chewing itself that serves as a trigger?” I made the suggestion while brainstorming the problem with biologist Ryan Martin. “What if chewing on something alive like a fairy shrimp, something larger or something that struggles when you clamp onto it, sets this developmental cascade into motion?”

  Martin shot me a “not bad for a bat biologist” look. “Sounds like a good grad student project.”

  “Hey, it’s all yours,” I said with a laugh. We then set to work, drawing up an outline for a potential experiment to test the hypothesis.

  Although the jury is still out on the stimulus for the spadefoot transformations, Pfennig and his coworkers previously worked on a completely different cannibalism-triggering stimulus in another amphibian. And this one happened to be one of North America’s most spectacular species.

  Tiger salamanders (Ambystoma tigrinum) are the largest salamanders in the United States, reaching lengths of up to 13 inches. These thick-b
odied, sturdy-limbed urodelans are widespread across much of the country.7 Their markings, yellow blotches against a black body, make them easy to identify, but they are rarely seen in the open except during annual marches to a nuptial pond. Tiger salamander eggs are laid in the late winter or early spring, and like other salamanders (and their cousins the frogs and toads), their larvae are fully aquatic with external gills and fishlike tails. They typically feed on zooplankton and other micro-invertebrates, but under certain environmental conditions a small percentage of them develop traits that include huge heads, wide mouths, and elongated teeth. Consequently, these toothy individuals exploit larger prey, among them other tiger salamander larvae.

  Pfennig and his colleagues set up lab experiments on fertilized A. tigrinum eggs to investigate the stimuli that set these changes into motion. First the researchers determined that the cannibal morphs only developed when larvae were placed into crowded conditions. Next, they used a variety of experiments to determine whether the larval transformation might be triggered by visual cues (that didn’t work), smell (nope), or touch.

  “It looks like they had to have the tactile cues,” Pfennig told me. “There’s something about bumping into each other that triggers the production of the cannibals.”