Animals do the most amazing things. Read about them in this series by Janaki Lenin.
She squeezed out the last of her eggs in a sheltered thicket of reeds on the banks of a pond and took to the air. A patrolling male dove on her. She could make a dash for it but her chances of outmanoeuvring him were poor. She fell out of the sky, crash-landing into a bush where she lay inert on her back. Seeing her lifeless body, the male abandoned his pursuit and flew away to await the appearance of another female. When the coast was clear, the female common hawker (Aeshna juncea) took off. Of course, another male dragonfly may accost her – but she could always play dead. Besides her suitor, the dragonfly fooled another observer.
Rassim Khelifa, a doctoral student at the University of Zurich, Switzerland, first observed this behaviour at a pond near Arosa in the Swiss Alps in the summer of 2015. When he went closer to the inert common hawker, she flipped over on her feet and flew away.
Many animals, from water bugs and hognose snakes to North American and white-eared opossums, feign death to escape their assailants. Some go to great lengths to put on an act, contorting their bodies, flipping over on their backs and hanging their tongues out of gaping mouths. When you set a hognose snake that is pretending to be dead right side up, it immediately rolls over on its back and resumes its act. And for good reason. Prey movement triggers predatory behaviour. Playing dead is the last resort of desperate prey, even if it means allowing the predator close enough to take a bite. If a quail pretends to be dead, a marauding cat would most likely ignore it and continue stalking one that’s running away. A pygmy grasshopper (Criotettix japonicus) feigning death erects prominent spines that would make swallowing it a painful business for a frog.
While such pretence to escape predators is relatively common, using the same strategy to avoid sexual encounters is rare and restricted to a handful of creatures – mostly insects. Male spiders fear their Goliath-sized predatory mates. They offer silk-wrapped insects as gifts before approaching females. If their mates accept the gifts and start feeding, the males have nothing to worry about. They can go forth and copulate. But sometimes females may ignore the meals, their predatory instincts triggered by even the males’ slow and cautious approach. And like prey animals, the males draw in their legs and pretend to be lifeless.
To female dragonflies, sex-obsessed males are no different than hungry predators. On seeing the female common hawker take off as soon as he came close, Khelifa was surprised and perplexed. He recounted his observation to colleagues, and everyone laughed. “They were both surprised and amused since the story is quite relatable,” he told The Wire.
He investigated whether this was a widespread behaviour in the species. When males chased 35 female common hawkers after they had laid their eggs, 31 crashed into bushes. The four that didn’t take evasive action were forced to mate with the males. Of the ones that plummeted to the ground, 27 lay still on their backs.
But why did those four flap their wings? “There might be behavioural variability among females of the same population – that is, not all females express death feigning,” says Khelifa. “Moreover, it might be related to the fact that after landing, females’ wings get stuck in vegetation and they may flap their wings to escape.” Some males seemed to cotton on to the trick. Of the 27 that played dead, the males saw through the pretence of six.
“It is difficult to say why they detected them because different factors may come into play, such as intrapopulation variation in detection efficiency,” says Khelifa, “or the contrast between female coloration and the background colour where she lands.”
Only 21 – about 60% of the observed females – successfully evaded the males. Since so many female dragonflies tried this trick, Khelifa thinks this is a common behaviour in the species. To check if the female common hawkers were conscious and alert after they crash-landed, he tried to catch them. Of 31 attempts, he caught only four; 27 escaped. He held 50% of the males patrolling two ponds captive for a day. With fewer males to escape from, the females grew bold, laying their eggs in more open vegetation. And they had fewer encounters with males when they soared into the sky.
Is the cost of mating so high that the females have to resort to such extreme measures? “The function of the male penis is not only limited to sperm transfer but also to remove sperm left in the female’s storage organ from previous matings,” says Khelifa. The sophisticated penis structure could damage the females’ reproductive tract while scooping out another male’s sperm. “One copulation is enough to fertilise all eggs. It is not in the females’ interest to carry out multiple copulations per day.”
Sexual harassment is common in the species because, according to Khelifa, males outnumber females at nesting sites and the ones that coerce females are more successful. The females’ tendency to lay eggs solitarily makes them vulnerable to such bullying. A combination of female vulnerability and male-biased sex ratio creates the conditions for the evolution of this behaviour.
Although Khelifa writes that sexual death feigning is restricted only to arthropods, a study published early last year showed female Iberian ribbed newts (Pleurodeles waltl) that were reluctant to mate played dead, lying motionless on their backs.
“It is more likely to evolve in species where males use an aggressive approach of ‘conquering a female’ by constraining them, not giving the females a choice,” says Sunita Leentje Janssenswillen, a postdoctoral fellow at Vrije Universiteit, Brussels, and the main author of the publication on newts. “This leads to an inventive strategy: thanatosis [feigning death]. Also, it will be more likely to evolve in species that use faking death as a defence mechanism. In salamander species, where males ‘politely’ invite females by waving pheromones towards them, we did not observe this female tactic.”
Other species of dragonflies, especially adult Philonomon luminans of South Africa and nymphs of orange shadowdragon (Neurocordulia xanthosoma) of Texas feign death to escape from predators. Khelifa suggests female common hawkers may have adapted this anti-predator defence mechanism to dodge the coercive males of their species. But common hawkers don’t play possum when threatened by predators.
“I have not witnessed that in the field,” says Khelifa. “Although I handled many females, none of them feigned death in my hands. Further observations are needed to confirm anti-predatory death feigning in this species.”
The reproductive history of a closely related species, the southern hawker (Aeshna cyanea) is similar. Males outnumber females at nesting sites and females individually seek sheltered spots away from the gaze of coercive males to lay their eggs. When males try to interrupt their egg-laying and drag them away, these females cling tightly to plants instead of playing dead. They also clap their wings and shake their bodies to signal their unwillingness to mate again say researchers. Other species bend their abdomens to make swift U-turns or fly in loops to evade males.
However, there may be another explanation for this behaviour. “It may also be a way by which females ‘test’ male persistence to assess male quality and choose a partner,” Alex Córdoba-Aguilar, Universidad Nacional Autónoma de México and editor of the book Dragonflies and Damselflies, told The Wire.
Females use various means to gauge whether males are good partners. They may adopt either passive indicators, like a male peacock’s plumage, or put potential suitors through their paces. Female black scavenger flies shake vigorously when males mount them and only mate with those that resist. “This possibility, I agree, is difficult to test but is the rival hypothesis in all cases where sexual coercion is invoked,” says Córdoba-Aguilar.
Crashing into bushes could possibly hurt the females, a high price to pay to avoid sex or test males. “Given the speed at which they crash-land, there is a possibility that repeated crashes leads to physical damages, particularly in the wings,” says Khelifa. “However, it was remarkable that females landed in vegetated areas so the crash-landing impact might be buffered by plants.”
If females pretend to be dead in order to choose males, then they may trade shorter lifespan for more offspring that would inherit their fathers’ persistence, says Córdoba-Aguilar. This could work out in favour of females.
If the behaviour offers benefits, why isn’t it more widespread? “Although thanatosis seems impressive in moorland [or common] hawkers, I guess such behaviour has not been intentionally looked for in other species,” according to Córdoba-Aguilar. Little is known of the sexual behaviour of dragonflies because they are difficult to catch, mark and observe in the wild. “I have observed that females of black saddlebags (Tramea lacerata), green darners (Anax junius), and giant darners (Anax walsinghami) stop flying and fall down to water or vegetation when taken by males. Females remain motionless, at times upside down. Possibly, these other species do not show elaborate behaviour such as moorland hawkers, but they definitely have similar responses.”
Janssenswillen says she observed female European common brown frog (Rana temporaria) play dead, but she hasn’t published the observation. Perhaps this tactic is more common than we realise.
Besides exploring the prevalence of death feigning in insects and other animal groups, Khelifa says another interesting aspect for future study is the influence of population density on the behaviour.
The study was published in the journal Ecology on April 24, 2017.
Janaki Lenin is the author of My Husband and Other Animals. She lives in a forest with snake-man Rom Whitaker and tweets at @janakilenin.