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Outsourced hearing in spiders by using their webs as auditory sensors

View ORCID ProfileJian Zhou, Junpeng Lai, Gil Menda, Jay A. Stafstrom, Carol I. Miles, Ronald R. Hoy, Ronald N. Miles
doi: https://doi.org/10.1101/2021.10.17.464740
Jian Zhou
1Department of Mechanical Engineering, Binghamton University, Binghamton, NY 13902, USA
4Center for Nanoscale Materials, Argonne National Laboratory, 9700 South Cass Avenue, Argonne, 60439, Illinois, USA
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  • For correspondence: miles@binghamton.edu rrh3@cornell.edu zhouj@anl.gov
Junpeng Lai
1Department of Mechanical Engineering, Binghamton University, Binghamton, NY 13902, USA
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Gil Menda
2Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA
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Jay A. Stafstrom
2Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA
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Carol I. Miles
3Department of Biological Sciences, Binghamton University, Binghamton, NY 13902, USA
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Ronald R. Hoy
2Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA
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  • For correspondence: miles@binghamton.edu rrh3@cornell.edu zhouj@anl.gov
Ronald N. Miles
1Department of Mechanical Engineering, Binghamton University, Binghamton, NY 13902, USA
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  • For correspondence: miles@binghamton.edu rrh3@cornell.edu zhouj@anl.gov
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Abstract

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, selfmanufactured 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.

Competing Interest Statement

The authors have declared no competing interest.

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Posted October 18, 2021.
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Outsourced hearing in spiders by using their webs as auditory sensors
Jian Zhou, Junpeng Lai, Gil Menda, Jay A. Stafstrom, Carol I. Miles, Ronald R. Hoy, Ronald N. Miles
bioRxiv 2021.10.17.464740; doi: https://doi.org/10.1101/2021.10.17.464740
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Outsourced hearing in spiders by using their webs as auditory sensors
Jian Zhou, Junpeng Lai, Gil Menda, Jay A. Stafstrom, Carol I. Miles, Ronald R. Hoy, Ronald N. Miles
bioRxiv 2021.10.17.464740; doi: https://doi.org/10.1101/2021.10.17.464740

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