by Bill Schutt
Support for this hypothesis comes from studies on a wide variety of mantis species, including those in which worse-for-wear females that cannibalized their mates later exhibited improved body condition, produced larger egg cases (ootheca) and more offspring. Significantly, well-fed female mantises showed no cannibalistic tendencies during mating encounters.
Before we blame mantid cannibalism on captive conditions or starvation, though, the fact remains that both wild and captive males exhibit extreme caution as a normal preamble to copulation. Depending on the species, the males’ initial approach can vary from simple (slow and deliberate movement toward the female, followed by a flying leap onto her back) to complex (the male fixes its stare on the female, goes through a series of stereotypical movements like antennal oscillations and abdominal flexing, then takes a flying leap onto her back). Researchers believe that these movements serve to either circumvent or inhibit the females’ aggressive, predatory response. It is, therefore, extremely unlikely that these forms of cautionary behavior by males would have ever evolved if there weren’t at least some risk of being attacked by females.
And what about the male’s famous ability to “keep the beat” even after losing its head? Biologists Eckehard Liske and W. Jackson Davis have an explanation for that phenomenon as well. They believe that, rather than acting as a stimulus for copulation (by releasing sexual movements), decapitation artificially induces the behavior. This would be similar to the way in which lopping off a chicken’s head artificially induces locomotor movements that can temporarily propel a headless bird around a barnyard. According to these researchers, from an evolutionary perspective, reflexive abdominal contractions and the subsequent release of sperm may insure that fertilization takes place, even if the males are left feeling a bit lightheaded after sex. As such, it serves as a prime example of how cannibalism can benefit the individual being cannibalized.
As in the praying mantises, in certain well-known spiders, truth has been masked by myth. After several papers in the 1930s and 1940s reported that female Latrodectus mactans spiders devoured their mates after copulation, L. mactans and two additional North American species became widely known as black widows. Although most of the initial observations turned out to be anecdotal, cannibalism and black widows became forever linked, appearing in an array of literature that ranged from storybooks to college textbooks on evolution, ecology, and animal behavior. The cannibal association continued through the 1970s and 1980s, even though researchers working with these spiders were beginning to discover that the behavior in black widows was actually a rare occurrence. They determined that not only did most male spiders depart unharmed after copulation, but some of them lived in the female’s web for several weeks, even sharing her prey.
“The supposed aggressiveness of the female spider toward the male is largely a myth,” said spider expert Rainer Foelix. “When a female is ready for mating, there is little danger for the male.” Foelix did add that all bets were off if a male mistakenly showed up in the web of a hungry female.
Readers who might be disappointed to learn that the black widow’s reputation is apparently worse than its bite may be consoled by the fact that sexual cannibalism has been reported in 16 out of 109 spider families (although the list is described as not “exhaustive nor definitive” regarding frequency). One of the most interesting examples takes place in the black widow’s Aussie cousin, the redback spider (L. hasselti). In this species, males go to extreme lengths, not only to guarantee their own demise, but their consumption as well.
The Australian redback spider is common throughout Australia, and in a country renowned for its notorious creatures, the redback ranks among the most dangerous. The reasons behind this spider’s bad reputation start with a neurotoxic bite that can cause severe pain and swelling, and in rare instances, seizures, coma, and even death. Like the North American black widows, Australian redbacks are often found in close proximity to human residences, especially sheds and garages offering the spiders undisturbed areas full of clutter. Presumably because of the abundance of flies, both black widows and redback spiders were once common in outhouses, where their fondness for living under privy seats was never quite as unpopular as their habit of biting anything that blocked their escape routes. Slim Newton’s song “Redback on the Toilet Seat” details one such encounter. “There was a redback on the toilet seat when I was there last night—I didn’t see him in the dark but boy I felt his bite.” The song reached #3 on the Australian pop record charts in August 1972, well ahead of artists like The Bee Gees and Elton John.
Although encounters with humans are rarely fatal (at least for the human), the same cannot be said for male redback spiders attempting to mate. In the first stage of courtship, the male approaches the female’s web and proceeds to get himself noticed (which takes a bit of doing, since he is only about one-fifth her size). He does so by bouncing his body up and down, throwing some silk around, and waving his front legs. As a point of information, while insects have six legs, spiders have eight of them, plus an additional pair of anteriorly located appendages called pedipalps. In male spiders, the pedipalps are modified for transferring sperm to the female’s body, a chore necessitated by the fact that spiders lack penises. Furthermore, there is no internal connection between the pedipalps and the testes, which are located within the abdomen. Instead, sperm is initially extruded from a furrow on the male’s abdomen into a spun receptacle called a sperm web. As a male dips his pedipalps into the pooled sperm, a pair of coiled structures called emboli and their associated muscles work like tiny turkey basters to suck up the liquid and store it until copulation.
The next phase of redback courtship begins as the male initiates repeated bouts of physical contact with his potential mate, behavior that includes tapping, probing, and nuzzling. The real heavy petting begins once the male locates the female’s epigynal opening. According to spider expert L.M. Forster, this behavior includes “nibbling, palpal boxing, and knocking, embolus stretching, push-ups, abdominal vibration, and epigynal scraping.”
By now, if the female hasn’t already eaten the male (which can put a serious dent into all of this foreplay) the spiders briefly assume “Gerhardt’s position 3.” To visualize this, picture two people in the missionary position. Now tweak the imagery a bit so that the guy is approximately the size of your favorite throw pillow. Okay, now add another eight limbs. (All right, maybe you shouldn’t picture this.)
Gerhardt’s position 3 appears to be favored by all Latrodectus species except the Australian redback, where it is abandoned immediately after the male penetrates the female’s epigynal opening with the tip of a sperm-charged embolus. At that point, things take a hard turn toward the strange. The male slowly performs a 180-degree somersault that ends with his abdomen resting against the female’s mouthparts and she immediately expresses her gratitude by vomiting enzyme-laden gut juice onto the tiny acrobat. She then begins to consume the male’s abdomen as they copulate, pausing from time to time to spit out small blobs of white matter. Upon the completion of the sex act, which takes anywhere from five to 30 minutes, the male crawls off a short distance, reportedly making repeated attempts to reel in his spent embolus “by stretching it with his forelegs and then releasing it abruptly.”
Approximately ten minutes later, rather than fretting over missing body parts or a less-than-tightly-coiled sperm applicator, the male returns to the fray, this time wielding the second embolus. The half-eaten spider then proceeds to reenact its earlier copulatory acrobatics, although this time minus some viscera. By way of a “welcome back,” the female resumes her meal, consuming more and more of the male’s abdomen. At the end of this round, though, rather than allowing him to crawl off, the female wraps her shredded partner in silk, eventually snorking up his now enzyme-liquefied innards like a spider-flavored Slurpee.
While the benefits of a risk-free meal for the redback mom-to-be are fairly obvious, one has to wonder what the hell is in it for the male? Because of this ver
y question, the mating habits of L. hasselti have drawn interest from spider experts. The puzzled scientists determined that females that had recently eaten their mates were less receptive to the approach of subsequent suitors. Cannibalized males also copulated longer and fathered more offspring than non-cannibalized males. Ultimately, then, it seems that this rather extreme example of paternal investment optimizes the likelihood that the cannibalized dad gets to pass his genes on to a new generation.
Things get dicey, though, when trying to determine the benefits for redback males eaten before mating takes place, a situation that has also been reported in orb-weaving spiders like Araneus diadematus. Mark Elgar and zoologist David Nash worked with this species and proposed that pre-mating cannibalism allows the female to choose which male will get to inseminate her. The researchers supported their hypothesis with the observation that smaller males were eaten more often than larger—and presumably healthier—individuals. They also used modeling studies to hypothesize that pre-mating cannibalism would occur only in instances where there was no shortage of males from which to choose. Alternately, post-mating cannibalism appears to make good evolutionary sense when short-lived males are relatively few in number and have a low probability of encountering receptive females. In these instances, when a potential mate is encountered, it pays to give it your all, even if that means paying with your life.
Observations related to mantis and spider cannibalism serve to illustrate the Gary Polis generalization that among invertebrate cannibals, males get cannibalized far more frequently than females. This behavior occurs in species that exhibit sexual dimorphism, a condition in which there are anatomical differences between males and females of the same species.
Besides body size, other examples of sexual dimorphism include coloration and ornamentation, and here it’s usually the males that display bright colors, or exhibit elaborate structures like horns, frills, and crests. Essentially, these showy accouterments are used to advertise the wares of a presumably healthy male to potential mates (in other words: “If I can spend energy advertising just how beautiful I am, then I’m also a great bet to father a clutch of healthy offspring”).
As it relates to cannibalism, the most common example of sexual dimorphism is body size, and among the invertebrates, females are often substantially larger than males. But why is this so?
The benefits appear related to the ability of larger mothers to better carry, protect, and provide for their young. Relatively small body size can also provide males with a gravity-related biomechanical advantage. Since gravity is less of a constraint on lightweight bodies than it is on heavier ones, this is especially evident in males that must climb in order to reach females. Likewise, in other species, tiny adult males are able to “balloon” like spiderlings, using the wind as an energy-efficient means of travel. Presumably this increases their chances of finding a potential mate.
On the other side of the web, but still supporting the small-get-cannibalized rule, are the rare instances in which male spiders are larger than females. This spider role reversal occurs in two species that exhibit some very unspiderlike behavior. In the sand dwelling wolf spiders (Allocosa brasiliensis), females undertake risky visits to burrows built by the larger males. Because these structures represent a high reproductive investment, male wolf spiders become extremely picky when females show up and initiate courtship—which they do by alternately waving their forelegs around in the universal signal for “Pick me! Pick me!” In many cases, though, researchers noted that instead of mating, the females were often attacked and cannibalized.
To determine why, arachnologist Anita Aisenberg and her colleagues performed experiments in which twenty male spiders were consecutively exposed to one virgin and one previously mated female (in alternating order). Findings revealed that only 10 percent of the virgin females were cannibalized while 25 percent of the mated females were eaten, especially those exhibiting lower body condition indices. In other words, male wolf spiders chose their mates based on looks and sexual history. The researchers concluded that by selecting younger, fitter females, male spiders maximized the likelihood that their mate would survive to produce a successful batch of spiderlings. Older, less fit females, also served a purpose—as food.
Cannibalism by males also occurs in the aptly named water spiders (Argyroneta aquatica), the only living arachnids that exist completely underwater. In this species, females spend most of their lives inside web-shrouded air bells, where their smaller bodies require less oxygen than their male counterparts. Natural selection may favor larger body size in male water spiders by providing them with enhanced swimming and diving abilities. While females are ambush predators, males are active hunters, and although their diets consist primarily of insect larvae, they will kill and cannibalize smaller males during intense competition for females. The female water spiders’ preference for larger males can also turn deadly in a hurry, specifically during failed mating encounters in which females are chased down and consumed.
These two examples illustrate that when cannibalism occurs, it’s size, rather than sex, that is the key determinant, with the smallest individuals (usually the males) ending up on the menu. This generalization also extends from invertebrates like spiders to some of the most familiar and beloved creatures on the planet. But before you come away thinking that praying mantises and spiders have maintained their stranglehold on cannibalistic copulatory behavior, we need to drop in on yet another member of the animal kingdom.
When terrestrial snails cross paths (or more accurately, slime trails), the potential for bizarre sexual encounters can rival a bachelor party in a Hangover film. For the snails, the high hook-up ratio stems from the fact that most of the participants are simultaneous hermaphrodites, enabling them to exchange sperm while at the same time having their own eggs fertilized. And while this particular sexual orientation increases the likelihood that any two individuals that meet will be able to mate, things can go downhill quickly once the lovers begin biting chunks out of each other.
Snails and slugs, their shell-challenged relatives, are mollusks, a biologically diverse invertebrate group that also contains the bivalves (clams, oysters, and their shelly relatives) and cephalopods (squid, octopuses, and cuttlefish). Known collectively as gastropods, the approximately 85,000 species of snails and slugs have a worldwide distribution, inhabiting a variety of marine, freshwater, and terrestrial environments. To put this into perspective, there are approximately 17 times as many gastropod species on the planet as there are mammals.
Along with their popularity as escargots or scungilli, gastropods are renowned for their slow-footed locomotion—a point celebrated annually by pub-going “researchers” in the UK. At the World Snail Racing Championship in 1995, a garden snail named Archie rocketed across a 13-inch course at an average speed of 0.0053 miles per hour, the fastest ever recorded for a snail. Scientists believe that snail speed (or lack thereof) is actually an adaptation related to energy efficiency. In other words, by devoting less energy to locomotion, gastropods can spend more of it involved in alternative behavior—like mating.
Although snail sex can last for up to six hours in some herbivorous species, this is definitely not the case in certain carnivorous gastropods, where foreplay can turn into cannibalism in the blink of a turreted eye. In these species, since even copulating individuals will bite their mates, each potential sexual partner is also a potential predator. As a result, they often employ the wham-bam-scram approach during sexual encounters, which can sometimes linger on for as long as six seconds.
An even more cringeworthy behavior is exhibited by banana slugs (genus Ariolimax), which become so entwined during sex that they sometimes chew off their partner’s corkscrew-shaped penis in an effort to disengage. During this process, which is known as apophallation, penises are slurped down spaghetti-style, occasionally by their owners. Although this usually puts an end to the festivities, the fact that the penises do not grow back presents fewer problems than one would e
xpect. The hermaphroditic slugs simply carry on the remainder of their lives as females.
In some land snails, however, things get bizarre even before the member-munching starts—especially once the partners begin shooting calcified “love darts” at each other, an exchange initiated when the body of one snail touches that of a potential mate. This tactile stimulation triggers the release of built-up hydraulic pressure in a sac surrounding the dart. As a result, the barbed projectile (known as a gypsobelum) explodes outward, embedding itself in the body wall of the second individual. In most instances, the skewered snail responds by shooting a dart of its own, and shortly thereafter the couple appear to remember why they had gotten together in the first place.
Often, though, the exchange proceeds with something less than textbook precision. Since most snails are nocturnal, their visual systems are simple. They can differentiate between light and dark, but an inability to determine details about their slimy targets (or anything else, for that matter) can lead to a serious lack of accuracy. As a result, headshots and similar misfirings are a common occurrence.
The obvious question is: Why do some snails fire miniature harpoons at each other? The proposed function of this behavior (which is rarely observed in humans anymore!) has undergone some revision. Earlier snail experts thought that love darts were the equivalent of an exchange of wedding gifts—in this instance, calcium carbonate, a major component of the snails’ shell and eggs. Another suggestion was that the projectiles might act as an aphrodisiac or that they somehow signaled the shooter’s willingness to mate. But support for these hypotheses never materialized.
I posed the question to McGill University biologist Ronald Chase, whose work in the 1990s helped solve the mystery of this baffling behavior. “The darts serve to increase paternity,” he told me, since snails scoring love dart hits on their partners before mating fathered twice as many offspring as those that didn’t hit their targets. The key to the enhanced reproductive effect was the tiny projectile’s chemical coating. Chase and his colleagues showed that this hormonelike substance prevented digestive enzymes from destroying the majority of incoming sperm, something that occurred in non-skewered snails. Spared the buzzkill of being digested, the snail sperm sped onward, eventually fertilizing a greater number of eggs than those that wound up in non-speared snails.