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Outsourced hearing in spiders by using their webs as auditory sensors

By Jian Zhou, Junpeng Lai, Gil Menda, Jay A Stafstrom, Carol I. Miles, Ronald R. Hoy, Ronald N. Miles

Posted 18 Oct 2021
bioRxiv DOI: 10.1101/2021.10.17.464740

Hearing is a fundamental sense of many animals, including all mammals, birds, some reptiles, amphibians, fish and arthropods1,2. The auditory organs of these animals are extremely diverse in anatomy after hundreds of millions of years of evolution3-5, yet all are made up of cellular tissue and are embodied meaning that its functional anatomy is constrained by developmental morphogenesis. Here we show hearing in the orb-weaving spider, Larinioides sclopetarius is not constrained by embodiment but is extended through outsourcing hearing to its proteinaceous, self-manufactured orb-web, and hence under behavioral control, not developmental biology. We find the wispy, wheel-shaped orb-web acts as a hyperacute acoustic array to capture the sound-induced air particle movements that approach the maximum physical efficiency, better than the acoustic responsivity of all previously known ears6,7. By manipulating the web threads with its eight vibration-sensitive legs8-10, the spider remotely detects and localizes the source of an incoming airborne acoustic wave emitted by approaching prey or predators. By outsourcing its acoustic sensors to its web, the spider is released from embodied morphogenetic constraints and permits the araneid spider to increase its sound-sensitive surface area enormously, up to 10,000 times greater than the spider itself11. The use of the web also enables a spider the flexibility to functionally adjust and regularly regenerate its 'external ear' according to its needs. This finding opens a new perspective on animal hearing - the 'outsourcing' and 'supersizing' of auditory function in a spider, one of the earliest animals to live on land12. The novel hearing mechanism provides unique features for studying extended and regenerative sensing13-15, and designing novel acoustic flow detectors for precise fluid dynamic measurement and manipulation16-18.

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