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Research Article
Multimodal mechanosensing enables treefrog embryos to escape egg-predators
Julie Jung, Shirley J. Serrano-Rojas, Karen M. Warkentin
Journal of Experimental Biology 2020 223: jeb236141 doi: 10.1242/jeb.236141 Published 22 December 2020
Julie Jung
1Department of Biology, Boston University, 5 Cummington Mall, Boston, MA 02215, USA
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  • For correspondence: jungj@bu.edu
Shirley J. Serrano-Rojas
2Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Panamá, República de Panamá
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Karen M. Warkentin
1Department of Biology, Boston University, 5 Cummington Mall, Boston, MA 02215, USA
2Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Panamá, República de Panamá
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ABSTRACT

Mechanosensory-cued hatching (MCH) is widespread, diverse and important for survival in many animals. From flatworms and insects to frogs and turtles, embryos use mechanosensory cues and signals to inform hatching timing, yet mechanisms mediating mechanosensing in ovo are largely unknown. The arboreal embryos of red-eyed treefrogs, Agalychnis callidryas, hatch prematurely to escape predation, cued by physical disturbance in snake attacks. When otoconial organs in the developing vestibular system become functional, this response strengthens, but its earlier occurrence indicates another sensor must contribute. Post-hatching, tadpoles use lateral line neuromasts to detect water motion. We ablated neuromast function with gentamicin to assess their role in A. callidryas’ hatching response to disturbance. Prior to vestibular function, this nearly eliminated the hatching response to a complex simulated attack cue, egg jiggling, revealing that neuromasts mediate early MCH. Vestibular function onset increased hatching, independent of neuromast function, indicating young embryos use multiple mechanosensory systems. MCH increased developmentally. All older embryos hatched in response to egg jiggling, but neuromast function reduced response latency. In contrast, neuromast ablation had no effect on the timing or level of hatching in motion-only vibration playbacks. It appears only a subset of egg-disturbance cues stimulate neuromasts; thus, embryos in attacked clutches may receive unimodal or multimodal stimuli. Agalychnis callidryas embryos have more neuromasts than described for any other species at hatching, suggesting precocious sensory development may facilitate MCH. Our findings provide insight into the behavioral roles of two mechanosensory systems in ovo and open possibilities for exploring sensory perception across taxa in early life stages.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: J.J., K.M.W.; Methodology: J.J., S.J.S.-R., K.M.W.; Software: J.J.; Validation: J.J., S.J.S.-R., K.M.W.; Formal analysis: J.J.; Investigation: J.J., S.J.S.-R.; Resources: K.M.W.; Data curation: J.J.; Writing - original draft: J.J.; Writing - review & editing: J.J., S.J.S.-R., K.M.W.; Visualization: J.J.; Supervision: K.M.W.; Project administration: K.M.W.; Funding acquisition: K.M.W.

  • Funding

    This research was funded by the Smithsonian Tropical Research Institute (STRI), Boston University and the National Science Foundation (IOS-1354072 to K.M.W. and James Gregory McDaniel), and conducted under permits SC/A-10-18 and SE/A-42-19 from the Panamanian Ministerio de Ambiente and STRI IACUC protocol 2017-0601-2020-2.

  • Data availability

    Data are available from the Dryad Digital Repository (Jung et al., 2020): https://doi.org/10.5061/dryad.prr4xgxkc

  • Supplementary information

    Supplementary information available online at https://jeb.biologists.org/lookup/doi/10.1242/jeb.236141.supplemental

  • Received September 21, 2020.
  • Accepted November 3, 2020.
  • © 2020. Published by The Company of Biologists Ltd
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Keywords

  • Environmentally cued hatching
  • Lateral line system
  • Behavioral plasticity
  • Biotremology
  • Ontogeny
  • Vestibular system

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Research Article
Multimodal mechanosensing enables treefrog embryos to escape egg-predators
Julie Jung, Shirley J. Serrano-Rojas, Karen M. Warkentin
Journal of Experimental Biology 2020 223: jeb236141 doi: 10.1242/jeb.236141 Published 22 December 2020
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Research Article
Multimodal mechanosensing enables treefrog embryos to escape egg-predators
Julie Jung, Shirley J. Serrano-Rojas, Karen M. Warkentin
Journal of Experimental Biology 2020 223: jeb236141 doi: 10.1242/jeb.236141 Published 22 December 2020

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