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Luminescent defensive behaviors of polynoid polychaete worms to natural predators

Abstract

The intertidal polynoid scale worm Harmothoe imbricata emits a bright green luminescence from its elytra when provoked. These worms are hypothesized to use both luminescence and autotomization (voluntary loss of body parts) as specialized defenses against predators. Previous studies had focused on the mechanisms of light production or used human manipulation to provoke luminescent displays, rather than using actual predators. Worms and local crustacean predators collected in Cumberland County, Maine at three intertidal locations between June 2011 and March 2013 were placed in a small chamber with a removable center divider and their interaction was recorded with infrared cameras, a night vision device with an infrared barrier filter, and photomultipliers. Three different luminescent responses were observed: attached scale flashing, autotomized glowing scales, and autotomized flashing/glowing posterior segments. In some cases, autotomized scales/segments acted as successful decoys, with the anterior portion of the worm crawling away while the attacker focused on the posterior glowing portion. Worms appeared to use different combinations of defensive behaviors in different scenarios, such as when attacked by different predators. Luminescent defensive displays were also more complex than predicted and suggest that the predator’s actions during and following an attack may inadvertently aid in the scale worm’s escape. The use of live predators was pivotal to describing the worm’s defense mechanism and providing insight into how luminescence may be used in nature.

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Acknowledgements

The authors would like to thank the editor and three anonymous reviewers for their constructive and insightful comments that contributed to improving the final version of this paper. The authors would like to acknowledge Marko Melendy for critical support in the collection, care, and shipment of specimens and the Doherty Marine Biology Postdoctoral Scholar Fund (TJR), the Henry L. and Grace Doherty Coastal Studies Research Fellowship (JL, TP), the Howard Hughes Medical Institute post-baccalaureate fellowship (TP), and Peter J. Grua and Mary G. O’Connell Research Award (JL) for funding. Finally, the authors would further like to thank Amy Johnson (Bowdoin College), Jon Allen (College of William and Mary), and Christine Rholl (Bowdoin College) for discussions about experimental design.

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Correspondence to Trevor Rivers.

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Research involving human participants and/or animals

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution at which the studies were conducted. As no live vertebrate animals or cephalopods were used in this study, no formal approval from the Bowdoin College Institutional Animal Care and Use Committee was necessary. This article does not contain any studies with human participants performed by any of the authors.

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Responsible Editor: M. Thiel.

Reviewed by R. Jones, W.R. Francis and an undisclosed expert.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1 Recording under red light of researcher grabbing an H. imbricata using a forceps to demonstrate anterior to posterior flashing behavior and tail autotomization (MP4 1678 kb)

Online Resource 3 Recording of a lobster attacking a scale worm during a behavioral trial. The top two frames and lower left frame are different IR camera angles, while the bottom left frame is the NVD with an IR barrier filter recording of only the luminescence (MOV 75591 kb)

227_2018_3403_MOESM5_ESM.mov

Online Resource 7 Close up of H. imbricata scale and tail autotomization display during an attack from a green crab recorded through an NVD with an IR barrier filter (MOV 30118 kb)

Online Resource 2

Photo of two variations of the recording chamber. The version on the left has a small ledge at a 45-degree angle around the bottom edges of the tank while the version on the right has a circular groove in the bottom surface (TIFF 2305 kb)

Supplementary material 4 (DOCX 143 kb)

Online Resource 7

Close up of H. imbricata scale and tail autotomization display during an attack from a green crab recorded through an NVD with an IR barrier filter (MOV 30118 kb)

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Livermore, J., Perreault, T. & Rivers, T. Luminescent defensive behaviors of polynoid polychaete worms to natural predators. Mar Biol 165, 149 (2018). https://doi.org/10.1007/s00227-018-3403-2

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  • DOI: https://doi.org/10.1007/s00227-018-3403-2