Environment

Within the Ritualistic Arena of Spider Sex, Male Darwin’s Bark Spiders Add a New Twist

None of self-mutilation, cannibalism, bondage and genital plugging among the spiders surprised the researchers as much as the males performing oral sex as well.

After mating, the male of Darwin's bark spider (Caerostris darwini) chews on his palps. The emasculation presumably renders the eunuch more aggressive, being better at fighting off rival males that might also want to mate with 'his' female. Credit: Research Centre of the Slovenian Academy of Sciences and Arts

After mating, the male of Darwin’s bark spider (Caerostris darwini) chews on his palps. The emasculation presumably renders the eunuch more aggressive, being better at fighting off rival males that might also want to mate with ‘his’ female. Credit: Research Centre of the Slovenian Academy of Sciences and Arts

Animals do the most amazing things. Read about them in this series by Janaki Lenin.

Darwin’s bark spiders are exceptional in many ways. Females of the species spin the world’s largest webs, covering up to 2.8 square metres in area. Slung across rivers and streams, the orbs’ anchor lines stretch up to 25 metres in length. Their silk is the toughest biomaterial in the world, 10-times stronger than bullet-proof Kevlar. Besides these superlative qualities, Slovenian researchers say this extraordinary creature has one of the most interesting sex lives in the animal kingdom as well.

Native to Madagascar, the Darwin’s bark spider was described scientifically only in 2010. The females are 14-times heavier and more than twice as large as males. But they are not monstrous; they are no more than two centimetres in length. This size difference between the genders, called sexual size dimorphism, is common among spiders. Many tiny males vie for the sexual attention of a large mamma at great personal cost. She could emasculate or eat them.

Sexual cannibalism in the Darwin’s bark spider (Cearostris darwini). Females are on average 14x heavier than males. Credit: Research Centre of the Slovenian Academy of Sciences and Arts

Researchers from Scientific Research Centre of the Slovenian Academy of Sciences and Arts, Ljubljana, noticed male bark spiders preferred to mate with freshly moulted females. As soon as they shed their skins, females are soft, placid, and unable to attack. Males can copulate with them for a long time without fearing for their lives. But once their skins harden, females turn predatory. To protect themselves, males bind them with silk before hazarding copulation.

“Mate binding slows down female attacks, but does not prevent them,” Matjaž Gregorič told The Wire. “Thus, the male just increases his survival chances, instead of avoiding cannibalism completely.”

The male needs to bind his mate in silk. This behaviour might reduce the risk of sexual cannibalism. Credit: Research Centre of the Slovenian Academy of Sciences and Arts

The male needs to bind his mate in silk. This behaviour might reduce the risk of sexual cannibalism. Credit: Research Centre of the Slovenian Academy of Sciences and Arts

Indeed, about 30% of older female bark spiders ate their mates. How could a spider trussed up with the world’s toughest biomaterial break free? The females are not bound up like a mummy, says Gregorič. “It is some silk wrapped around the female. Getting free is not a problem.”

Males didn’t bother with this S&M manoeuvre when pairing up with defenceless, freshly moulted females. Spiders’ penises are in their heads. Males have an extra pair of leg-like appendages near the mouth called palps. They transfer sperm by inserting their palps into an opening called epigyne, high up in the females’ abdomen.

The small male took the chance of mating with a freshly moulted female. The female’s exoskeleton is still soft and she cannot attack the male. Credit: Research Centre of the Slovenian Academy of Sciences and Arts

While mating, male Darwin’s bark spiders damaged their palps. In half the mating events, the male organs broke off inside the females, acting as genital plugs to prevent females from mating again. This is a common strategy when female spiders are disproportionately larger than males. In another species of orb-weaving spider, researchers found the severed male bits continued to transfer sperm.

Male Darwin’s bark spiders took their emasculation further. Within 24 hours of copulation, they chewed off what remained of their maimed palps and became eunuchs. What do they gain by self-castration?

“This [removal of palps] results in hormonal changes that render eunuch males more aggressive, and such males are good at fighting off rival intact males,” says Gregorič.

Before, during, and after mating, the male Darwin's bark spider salivates over the female's epigyne, presumably to increase his reproductive success. Credit: Research Centre of the Slovenian Academy of Sciences and Arts

Before, during, and after mating, the male Darwin’s bark spider salivates over the female’s epigyne, presumably to increase his reproductive success. Credit: Research Centre of the Slovenian Academy of Sciences and Arts

By force of circumstance, males of the species are monogynous, having sex with one female. Occasionally, they may mate with two, but no more. However, evolution favours female Darwin’s bark spiders by rendering the plugs inefficient. Subsequent suitors may remove the plugs, so the females were free to mate with multiple partners.

None of this – self-mutilation, cannibalism, bondage, genital plugging – surprised the researchers as much as the males’ oral sexual behaviour. “Sexually size dimorphic animals, including spiders, show among the most bizarre sexual behaviours,” says Gregorič. “So we expected the Darwin’s bark spider to exhibit some of them. However, we didn’t expect to see oral sexual behaviour.”

After mating, the male Darwin’s bark spider chews on his palps​. Credit: Research Centre of the Slovenian Academy of Sciences and Arts

The tiny male hooked his jaws, or chelicerae as spider mouthparts are called, to the female’s epigyne and salivated.  “Since it seems to be liquid excreted from the mouth, we simply call it saliva,” says Gregorič. “At this time, we cannot know for sure if other glands contribute to this liquid, for example, venom or other glands.”

The age, condition and aggressiveness of the female were immaterial. The males drooled over the genitals of any female mate – freshly moulted ones, older ones, and females that had mated before. The performance wasn’t restricted to foreplay alone. They went at it between bouts and even after copulation, as many as 100 times in a session. It wasn’t a fetish restricted to a few. All male spiders in the study performed oral sex.

With the exception of mammals, oral sex is rare in animals. Bonobos, hyenas, cheetahs, dolphins and bats are some that practice fellatio-like behaviour. Researchers knew of only bonobos, Indian flying fox, and fruit flies performing cunnilingus-like behaviour until now.

“I hypothesise this behaviour to be more widespread in the spider world, perhaps connected to sexually size dimorphic spiders,” says Gregorič. “For example, oral sexual contact, although salivation was not mentioned, was already described 114 years ago in black widows, but remained unexplored and forgotten in the literature.”

The Slovenian researchers speculate why this behaviour evolved in Darwin’s bark spiders. It’s unlikely to avert cannibalism since males perform oral sex with freshly moulted females that don’t pose a threat. Nor could it be to remove any genital plugs from previous mating because the males salivate during copulation as well as afterwards.

The researchers offer two possible explanations. Males may use oral sex to boost their chances of paternity or enzymes in the saliva could grant an advantage over rivals’ sperm. The researchers say these speculations need to be tested.

The study was published in the journal Scientific Reports on April 29, 2016.

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.