An excerpt from
Headless Males Make
From whence arrived the praying mantis?
From outer space, or lost Atlantis?
I glimpse the grim, green metal mug
That masks this pseudo-saintly bug,
Orthopterous, also carnivorous,
And faintly whisper, Lord deliver us.
—Ogden Nash, from Custard and Company
Continue having sex after your head has been chewed off? That’s what intrigued my fifteen-year-old son. He was writing a report on the sex lives of praying mantids—the first time all semester I’d seen him do any biology homework.
Rob knew that mantids are relentless predators. As a kid, he’d seen them lie in wait for prey, with their spiny, grasping front legs upraised and their pincers partially opened, poised for action. He’d watched mantids’ heads swivel three hundred degrees as the huge eyes tracked their moving prey. And he’d witnessed unwary grasshoppers and caterpillars get nailed and then consumed. He’d read that female mantids sometimes eat their mates, but until freshman biology class he hadn’t known that headless males make great lovers.
Imagine the following scenario: a male mantid, attracted by the smell of a female hidden in a lilac bush, creeps up behind her and when close enough leaps onto her, secures a perfect grip on her body, and copulates. No courtship, no permission asked or granted. He has behaved “appropriately” for a male mantid.
If a male doesn’t behave appropriately, he may incite trouble. Positioning is everything. A male that approaches a female from the front may meet immediate death by decapitation. If he sneaks up behind her but is just a little off on his grip, the female might bite off his head and dine on her brainless suitor as he continues to pass sperm into her body. Sometimes the impetuous female partially eats the male before he even mounts her. In this case, the headless wonder swings his legs around until his body touches hers, climbs onto her back, and copulates as though nothing were amiss.
Headless sex? How can it be? Copulatory movements in mantids are controlled by masses of nerve tissue in the abdomen rather than the brain. Males of some mantid species mate more effectively when decapitated. Why? A nerve center in the male’s head inhibits mating until a female is clasped. If this nerve is removed, such as when the female bites off the male’s head, all control is lost and the result is repeated copulation.
Sometimes the female devours her mate under circumstances outside the male’s control. If the pair is disturbed and the temperamental female becomes frightened, her immediate reaction is to whip around, snatch the male’s head in her greedy mandibles, and gnaw it off. In some species, a female’s propensity to consume her mate is unrelated to the male’s behavior or outside disturbance. It’s simply part of the mating ritual.
In all fairness to the eighteen hundred or so species of mantids, cannibalism is far from universal. Sexual cannibalism—defined as a female killing and eating her mate during courtship, copulation, or shortly after copulation—probably occurs in a minority of mantids.
Considering mantids’ potential cannibalistic behavior, why do people worldwide endow these insects with holiness? It’s their characteristic posture of supplication—front legs held together outstretched toward heaven—that commands respect. People living in the Middle Ages believed that mantids spent most of their lives praying to God, and some Muslims insisted that mantids always pray with their heads facing Mecca. Mantis is a Greek word meaning “prophet” or “clairvoyant.” Soothsayers used mantids, believed capable of foretelling events, to distinguish the fortunate from the unfortunate. Ancient Egyptians believed that mantids carried a person to the gods after death. Some Africans worshipped mantids because they believed these insects could resurrect the dead. Some ancient beliefs are still with us: If a mantid alights on your hand, you’ll meet a distinguished person; if it alights on your head, you’ll receive a great honor.
Even the mantids’ cannibalistic reputation has earned them respect. The Asmats, a native tribe that lives in southern New Guinea, greatly admire these insects. Until the mid-1940s, Asmats were fierce headhunters and cannibals, so it was natural they should admire an insect as fearless and cannibalistic as themselves. To honor these insects, Asmats commonly decorated their drums, shields, and spears with mantid figures.
Rob’s question was why do some females eat their lovers? Biologists, long fascinated by sexual cannibalism, have suggested various explanations for why such bizarre behavior should evolve and be maintained in some mantids, spiders, and other invertebrates. There are different, nonmutually exclusive explanations depending on the species and its natural history and whether the female eats the male before or after mating.
Mistaken identity may explain why females eat their prospective mates before copulation. Females that engage in sexual cannibalism are aggressive and predaceous by nature, and they may mistake a potential mate for food. This rationalization probably fails to explain many instances of sexual cannibalism, however. If females couldn’t discriminate between potential mates and food, many would end up virgins and never reproduce.
An alternative explanation for cannibalizing a prospective mate before copulation is discrimination among potential mates. Female garden spiders are more likely to cannibalize small wimpy males than large macho males. Why doesn’t a female just reject the small guys and allow them to move on? The small ones make nutritious treats. Just one male, even a small one, gives the female energy to produce more eggs.
A third explanation for why a female might eat her suitor before copulation is that perhaps she weighs the value of a courting male as a sperm donor versus a food item. If she hasn’t been very successful finding food recently and it’s early in the breeding season, she should eat the male. On the other hand, if courting males seem to be a rare commodity and especially if it’s late in the breeding season, she should mate with him. Females that have already mated once would be expected to attack courting males more often than should virgin females. A recent study with fishing spiders lends some support for this idea but does not exclude the possibility that sexual cannibalism may be simply misplaced aggression.
Why would a female eat her mate after copulation? In some cases, males might offer themselves up for food as an investment in their offspring, especially if they have little chance of mating again. For example, female orb-weaving spiders often eat their mates after copulation, but even if a male is not attacked, he will die soon after his first mating. A male might increase his reproductive success if the extra nutrition provided by his body increases the number of young his mate can produce or if it improves his offspring’s health, size, or survival. This explanation at one time was suggested for black widow spiders. They’ve been falsely accused, however. Sexual cannibalism is not as common in these spiders as originally believed. Furthermore, like mantids, male black widow spiders do not willingly sacrifice themselves. Although studies of some species of spiders and mantids have shown a positive effect of sexual cannibalism on the female’s reproduction, other studies have shown no effect. Obviously, this is not the rationale for all species.
Another explanation for eating a male during or after copulation is assurance of paternity. In many biting midges (tiny flies called no-see-ums or sand flies), the female eats the male during copulation, treating her mate the way she does any other insect prey. She pierces his cuticle and dissolves and sucks out his body contents, draining him in about thirty minutes. When the female disengages from her lifeless mate, a portion of his body remains attached to her. This “plug” may keep other males from mating with her, thus assuring not only paternity of the now-deceased male but also fertilization of all the female’s eggs. By dying in this way, the male increases his reproductive success.
If a male’s fitness benefits from his being eaten during or after copulation, he might facilitate cannibalism, especially if he is unlikely to mate again. One example where males actually encourage sexual cannibalism is the Australian redback spider (Latrodectus hasselti), closely related to the black widow spider.
Mating in Australian redback spiders occurs on the female’s web. After a male probes, taps, and nuzzles the female, he inserts a palp (the appendage that transfers sperm) into his much larger mate. Then he flails his legs in the air and turns a somersault, bringing his abdomen up against the female’s mouthparts. He effectively says, “Here I am—eat me.” The female slowly consumes her mate during copulation. The male withdraws once he has completed sperm transfer five to thirty minutes later. Mutilated, he grooms himself in preparation for the next lovemaking session. About ten minutes later, he briefly probes, taps, and nuzzles his mate and then engages his second palp. Again he somersaults and presents his now-shrunken abdomen to his mate. She sinks her mouthparts into his body and continues to digest. After completing insemination, the now-weakened male withdraws, and the female wraps him in silk. It will take her less than fifteen minutes to finish her meal.
A field study of Australian redback spiders reveals that females eat their mates about 65 percent of the time. Males always do the somersault, offering themselves up for a meal, but only hungry females accept the offer. A male is only 1 to 2 percent of the female’s mass, and cannibalism by the female does not increase the number or mass of eggs she produces. So why such behavior from the males? Cannibalized male spiders receive two paternity advantages. First, they copulate twice as long and therefore fertilize about twice as many eggs as uneaten males. Second, cannibalized males are more likely to father offspring because females are less inclined to re-mate after eating a male. If a female mated again, the second male would father some of her eggs. The cost of suicide is low for these spiders because even if they survive a copulation, they’re unlikely to mate again. Whereas females live up to two years, males live only two to four months after they mature. Males rarely eat after reaching maturity, and if they survive a mating, they often stay on their mate’s web.
After my son turned in his report, I enlightened him further on the macabre behavior of sexual cannibalism. “Real guys don’t lose their heads,” I confided. “They have ways of avoiding being eaten by their mates.”
Some scorpions use a variation on the “wham, bam, thank you ma’am” technique. Female scorpions release sexual attractants that guide males to them. Once a male locates a female, he grasps her claws with his and leads her in a prolonged mating waltz, referred to as a promenade à deux, in search of a hard surface, a stick or rock. Once the scorpions find an appropriate object, the male deposits a sperm-bearing packet on the object and then drags the female over it. She sucks the sperm into her genital pore, and almost immediately the male violently smacks her with his tail and scurries off. Why? Because if he isn’t fast enough, she may eat him.
Male spiders have trouble even getting close enough to a female for sex. The minute a female feels vibrations on her web, she assumes food has arrived. Males are almost always smaller than females, so they’re often mistaken for food. Males must identify themselves as males before the females’ hunting instincts and gastric juices take control.
In some species, the male vibrates, twitches, or drums on the female’s web in a characteristic way that announces he’s a potential suitor rather than food. Sometimes a male wolf spider must signal his intentions by waving his legs for hours, circling a female at a discreet distance, before she submits. If a male stumbles upon a female unexpectedly and has no time to wave his legs, woe unto him! Male jumping spiders signal their intentions to females through complex courtship dances. They zigzag to and fro, jerking their abdomens about in styles reminiscent of Hawaiian hula dances. Some just sway as if in a drunken stupor.
Some male spiders don’t announce their presence at all but have ingenious ways of avoiding being cannibalized. For some, patience pays off. A male waits on the sidelines of the web until the object of his desire has captured something to eat. Then, while she’s otherwise occupied, he makes his move.
Bribes also do the job. Some spiders offer nuptial gifts to their prospective mates. Once a male common European nursery web spider matures, instead of eating a juicy insect, he wraps it in silk, holds the enshrouded corpse in his jaws, and searches for a female. Once she’s found, he approaches her cautiously and offers his gift. If the offering is too small, the female walks away. If it’s acceptably large, she bites into it and begins to suck out the juices. Once she’s distracted by eating, the male mates with her.
A little brute force also works wonders. Courtship in some tarantulas begins with the male drumming his front legs against the female’s body. Though she lifts her front legs in a threatening gesture, the suitor taps and strokes her. She responds to his overtures by lifting her body higher and exposing her fangs. A stab by the female could prove fatal, so the male wraps a pair of hooks on his front legs over her fangs, yielding them ineffective. In this position, he can safely transfer sperm.
Would you believe kidnapping as a strategy? Males of one crab spider kidnap immature females and build silken tents around them that serve as prisons. Standing guard over their captives, these males chase away other males. Once the females are barely mature, the males assault them before they’re strong enough to resist.
And then there’s good old-fashioned trickery. Males of some spiders, including crab spiders, slowly creep up on females and throw a silk net over them before mating. After mating, the male escapes while the impregnated female disentangles her legs. These males can depart nonchalantly since the females are roped down. In most other spiders, the male dashes seemingly panic-stricken from his ex-lover. If he doesn’t escape quickly, she may tie him up, kill, and devour him.
The prize for cleverness and ingenuity in avoiding sexual cannibalism goes to male dance flies. These common small to medium-sized flies often swarm around trees and fly in an up-and-down or circular motion, thus the common name. Females are hotheaded and aggressive—a bad combination for male dance flies. As in some spiders, distraction is the solution. And males have developed brilliant tricks.
Most dance flies eat other small flies, such as mosquitoes and midges. In some species, the male dance fly offers the female a nuptial gift—an insect he has caught. He can then mate safely while the female is distracted by eating. In other species, the male is more imaginative and artistic. He wraps his gift in silk before offering it to the female, gaining precious time as she unwraps the insect before consuming it. We’ve all known stingy people. But dance flies? One species captures an insect, sucks out the juices for his own meal, and then wraps it in silk. He offers a female the parcel and begins to copulate. By the time she has unwrapped the empty insect shell, he has completed mating and even gotten a meal to boot.
I think I convinced my fifteen-year old son that the mating game can be dangerous. As he walked away, I imagined him thinking, “What if you gave a girl a Whitman’s sampler box with nothing left but the papers? Or sucked out the cream insides and gave her the chocolate shells?”
Copyright notice: Excerpt from pages 18-24 of Headless Males Make Great Lovers and Other Unusual Natural Histories by Marty Crump, published by the University of Chicago Press. ©2005 by the University of Chicago. All rights reserved. This text may be used and shared in accordance with the fair-use provisions of U.S. copyright law, and it may be archived and redistributed in electronic form, provided that this entire notice, including copyright information, is carried and provided that the University of Chicago Press is notified and no fee is charged for access. Archiving, redistribution, or republication of this text on other terms, in any medium, requires the consent of the University of Chicago Press. (Footnotes and other references included in the book may have been removed from this online version of the text.)
Headless Males Make Great Lovers and Other Unusual Natural Histories
Illustrated by Alan Crump
©2005, 208 pages, 108 line drawings
Cloth $25.00 ISBN: 978-0-226-12199-4
Paper $14.00 ISBN: 978-0-226-12202-1
For information on purchasing the book—from bookstores or here online—please go to the webpage for Headless Males Make Great Lovers.