Luminescent defensive behaviors of polynoid polychaete worms to natural predators
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.
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.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
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.
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)
- Bruno MS, Mote MI, Goldsmith TH (1973) Spectral absorption and sensitivity measurements in single ommatidia of the green crab, Carcinus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 82:151–163Google Scholar
- Crothers J (1968) The biology of the shore crab, Carcinus maenas (L.). 2. The life of the adult crab. Field Stud 2:579–614Google Scholar
- Daly J (1972) The maturation and breeding biology of Harmothoe imbricata (Polychaeta: Polynoidae). Mar Biol 12:53–66Google Scholar
- Daly J (1973) Segmentation, autotomy and regeneration of lost posterior segments in Harmothoe imbricata (L.) (Polychaeta: Polynoidae). Mauri Ora 1:17–28Google Scholar
- DATAQ Instruments (2012) WinDaq: data acquisition and playback software. Akron, Ohio, United StatesGoogle Scholar
- Factor J (1995) Biology of the Lobster: Homarus americanus. Academic, San DiegoGoogle Scholar
- Hastings JW, Morin JG (1991) Bioluminescence. Neural and integrative animal physiology. Wiley Interscience, New York, pp 131–170Google Scholar
- Hobson ES, McFarland WN, Chess JR (1981) Crepuscular and nocturnal activities of Californian nearshore fishes, with consideration of their scotopic visual pigments and the photic environment. Fish Bull 79:1–17Google Scholar
- Landgraf AJ (2016) logisticPCA: binary dimensionality reduction. https://github.com/andland/logisticPCA. Accessed 22 May 2018
- Marine Species Identification Portal (2016). http://species-identification.org/. Accessed 2 Jan 2018
- MathWorks (2013) MATLAB Release 2013b. Natick, Massachusetts, United StatesGoogle Scholar
- Morin JG (1983) Coastal bioluminescence: patterns and functions. Bull Mar Sci 33:787–817Google Scholar
- R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved from https://www.r-project.org/
- Ropes JW (1968) The feeding habits of the green crab, Carcinus maenas (L.). Fish Bull 67:183–203Google Scholar
- Squires H (1970) Lobster (Homarus americanus) fishery and ecology in Port au Port Bay, Newfoundland, 1960–65. Proc Natl Shellfish Assoc 60:22–39Google Scholar
- University of Maine, Gulf of Maine Research Institute (2013) Jonah crab (Cancer borealis): current status & information sources. https://www.gmri.org/sites/default/files/resource/jonah_crab_preassessment_november_1_2013.pdf. Accessed 10 Jul 2016
- Williams A, McDermott J (1990) An eastern United States record for the western Indo-Pacific crab, Hemigrapsus sanguineus (Crustacea: Decapoda: Grapsidae). Proc Biol Soc Wash 103:108–109Google Scholar
- WoRMS (2018) Homarus americanus H. Milne Edwards, 1837. http://www.marinespecies.org/aphia.php?p=taxdetails&id=156134. Accessed 20 Aug 2018