ABOVE: The ogre-faced spider Deinopis spinosa not only has the largest eyes of any spider, but is also one of few known to be able to hear at a distance.

If you were able to find the ogre-faced spider Deinopis spinosa during the daytime, you wouldn’t see much movement. Looking like a dead leaf on a branch, it doesn’t move at all, hiding from predators and silently waiting out the day. But during the night, it transforms into one of the most agile of arachnid hunters.

Holding a net stretched between its four front legs, it springs down onto the ground to ensnare insect prey, making use of its hypersensitive, night-vision eyes—the largest of any spider, at nearly 5 mm across together. Using a different maneuver, it strikes out with its web grasped between its front legs to snatch mosquitoes, moths, and flies passing above...

A new study published today (October 29) in Current Biology demonstrates that D. spinosa can hear sounds from two meters away, which allows it to catch prey without relying on vision. The findings place the ogre-faced spider in the ranks of certain jumping spiders, cob-web spiders, and fishing spiders, which have been previously shown to be capable of “hearing.” The study’s results add to evidence that help debunk an old yet persistent myth that spiders, which have no ears, can only detect mechanical vibrations, say, through their webs, and not airborne sound. The new data on D. spinosa confirm earlier clues that spiders can hear through the same organ they use to detect mechanical vibration.

“There have been several hints and actual documentations of acoustic sensitivity in spiders over the years, but this one’s [particularly] interesting,” remarks neuroethologist Andrew Mason of the University of Toronto Scarborough who has worked in one of the coauthor’s labs as a postdoc but wasn’t involved in the current study. “The really new piece of it is providing evidence that the spider’s leg can function as an acoustic transducer and that can be mediated by the sensory organ that’s normally associated with substrate vibration.”

Sensory ecologist Jay Stafstrom, a postdoc in neuroethologist and bioacoustician Ronald Hoy’s lab at Cornell University, had learned in earlier experiments that D. spinosa uses vision for its forward-striking, net-casting maneuvers but not for its back-bending twists. Individuals whose eyes were temporarily blinded couldn’t catch insects off the ground, but they could still catch prey out of the air, suggesting that “they’re probably using some other sensory system” for the backwards maneuver, Stafstrom says.

Deinopis spinosa uses its ability to hear from afar to snatch prey out of the air with a rapid overhead back-twist that unfolds within 60 milliseconds. 
Sam Whitehead 

Stafstrom, Hoy, and colleagues set out to investigate whether the ogre-faced arachnids were capable of picking up acoustic cues produced by the flapping of insect prey. Using techniques developed by lab neuroethologist Gil Menda, the team inserted tiny tungsten electrodes into the brains of living spiders in regions thought to be important for processing sensory information, and separately, into detached legs to detect neural activity of peripheral nerves. To the team’s surprise, neurons both in the brain and legs were responsive to a wide range of tonal frequencies—from 100 to 10,000 Hz—emitted from a loudspeaker 2 meters away. That range goes well beyond the typical wingbeat frequencies of their prey—which would be roughly between 150 and 750 Hz—into the kilohertz range, which would include the calls of passerine birds, for instance, that have been observed foraging around palm plants that ogre-faced spiders live on.

The researchers wondered if the metatarsal organ—an instrument situated at the lowest leg joint that senses mechanical vibration through movements in the spider’s exoskeleton—could play a role in detecting sound. Indeed, further experiments in which the researchers experimentally restricted the movement of detached legs demonstrated that the organ plays a role in detecting a subset of the frequencies they detect.

That suggests that, at least for some frequencies, the metatarsal organ of ogre-faced spiders can pick up airborne sounds that propagate through the air in pressure waves that deflect the tips of their legs, Stafstrom explains. “Even such a small amount of information, like air particles actually deflecting off of this leg, is enough for the spiders to functionally hear,” Stafstrom says.

The team suspects that sensitive leg hairs known as trichobothria—which Hoy’s team has previously shown enable jumping siders to hear from afar—play a role in detecting lower frequencies.

The scientists followed up with behavioral experiments to test if the spiders would respond to sounds. And sure enough, 13 of 25 spiders performed back-twists when they heard frequencies between 150 and 750 Hz, as if an insect had whizzed passed them. Stafstrom also flew out to Florida to find spiders in the wild and repeated the experiments with a Bluetooth speaker—with similar results, he says.

Curiously, the spiders didn’t react behaviorally to higher frequency tones, even though the previous experiments indicated that their central and peripheral neurons are responsive to tones as high as five octaves above a middle A. Perhaps the spiders have the ability to hear those frequencies not in order to hunt but so they can hide from avian predators, which tend to produce high-frequency sounds.

To Natasha Mhatre, a sensory biologist at Western University in Canada who wasn’t involved in the study, the findings address a long-standing mystery. Some previous research in other spider species in which researchers recorded the neural responses to experimental vibrations of the leg suggested that they were in fact more sensitive to frequencies greater than 1,000 Hz than to frequencies below that. That observation was puzzling because most of the vibrations spiders encounter on their web would be below 1,000 Hz, Mhatre says. “For the longest time, we didn’t really know why on Earth spiders were more sensitive to things that are above 1,000 hertz and not sensitive to the things that they’re actually interested in,” she says.

The team’s results suggest that ogre-faced spiders may be sensitive to those higher frequencies because they’re listening to airborne sounds, possibly to avoid birds. “What this study shows is that yes, some sounds are sufficient . . .  to generate joint bending large enough to actually produce a nervous response and therefore for the spider to hear it,” Mhatre adds.

Both Mason and Mhatre say they’re curious about the precise mechanisms involved, such as which leg in the hunting posture “hears” the sound, and whether and how the spider’s webs could play an auxiliary role in hearing by modifying the spider’s sensitivity to certain sounds.

To Mason, the findings also raise a philosophical question about how spiders perceive the world. Scientists tend to think about airborne sound and substrate vibration as two distinct entities. But for the spider, are they two different categories of stimulus, or are they part of a continuous realm of sensory information? “It may be that it’s just all vibration, and the boundary between the air and the web is just not a real boundary.”

For a spider with such a unique Jekyll-and-Hyde lifestyle, still by day and acrobatic at night, Stafstrom says, he’s not surprised they have an advanced sensory toolkit. “Their behavior requires some really impressive sensory equipment to be able to survive and be successful as an animal. Trying to figure out how [exactly] they’re doing it is a question that I’ll be trying to answer for many years to come.”

J.A. Stafstrom et al., “Ogre-faced, net-casting spiders use auditory cues to detect airborne prey,” Current Biology, doi:10.1016/j.cub.2020.09.048.

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