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Journal of Comparative Physiology A

, Volume 202, Issue 7, pp 489–501 | Cite as

Loudness-dependent behavioral responses and habituation to sound by the longfin squid (Doryteuthis pealeii)

  • T. Aran MooneyEmail author
  • Julia E. Samson
  • Andrea D. Schlunk
  • Samantha Zacarias
Original Paper

Abstract

Sound is an abundant cue in the marine environment, yet we know little regarding the frequency range and levels which induce behavioral responses in ecologically key marine invertebrates. Here we address the range of sounds that elicit unconditioned behavioral responses in squid Doryteuthis pealeii, the types of responses generated, and how responses change over multiple sound exposures. A variety of response types were evoked, from inking and jetting to body pattern changes and fin movements. Squid responded to sounds from 80 to 1000 Hz, with response rates diminishing at the higher and lower ends of this frequency range. Animals responded to the lowest sound levels in the 200–400 Hz range. Inking, an escape response, was confined to the lower frequencies and highest sound levels; jetting was more widespread. Response latencies were variable but typically occurred after 0.36 s (mean) for jetting and 0.14 s for body pattern changes; pattern changes occurred significantly faster. These results demonstrate that squid can exhibit a range of behavioral responses to sound include fleeing, deimatic and protean behaviors, all of which are associated with predator evasion. Response types were frequency and sound level dependent, reflecting a relative loudness concept to sound perception in squid.

Keywords

Noise Bioacoustics Soundscape Auditory scene Invertebrate 

Notes

Acknowledgments

We thank Roger Hanlon and members of the Hanlon Lab for providing initial advice. Thank you also to Vicke Starczak, Jesús Pineda, Scott Gallager and Michael Moore from WHOI for suggestions on experimental design, analyses and facilities space. Members of Mooney’s Lab and WHOI assisted with the experiments at various stages, including Margot Wilsterman and Max Kaplan. Rick Galat, Joe, Ed, Steve Allsopp, Kristopher Newhall and Jim Dunn helped make the tank and seawater adjustments. Thanks to Sander Kranenbarg, Henk Schipper and Kees Voesenek from the Experimental Zoology Group at the Wageningen University for their help with the analyses program. This work was supported by WHOI’s Ocean Life Institute.

Supplementary material

359_2016_1092_MOESM1_ESM.docx (29 kb)
Supplementary material 1 (DOCX 30kb)

References

  1. André M, Solé M, Lenoir M, Durfort M, Quero C, Mas A, Lombarte Antoni, Mvd Schaar, López-Bejar M, Morell M, Zaugg S, Houégnigan L (2011) Low-frequency sounds induce acoustic trauma in cephalopods. Front Ecol Evol 9:489–493CrossRefGoogle Scholar
  2. Au WWL, Hastings MC (2009) Principles of marine bioacoustics. Springer, New YorkGoogle Scholar
  3. Boyle P, Rodhouse P (2005) Cephalopods: ecology and fisheries. Blackwell Science, OxfordCrossRefGoogle Scholar
  4. Budelmann BU (1990) The statocysts of squid. In: Gilbert DL, Adelman WJ, Arnold JM (eds) Squid as experimental animals. Plenum Press, New York, pp 421–442CrossRefGoogle Scholar
  5. Budelmann BU (1992) Hearing in non-arthropod invertebrates. In: Webster DB, Fay RR, Popper N (eds) The evolutionary biology of hearing. Springer, New York, pp 141–155CrossRefGoogle Scholar
  6. Budelmann BU, Bleckmann H (1988) A lateral line analogue in cephalopods: water waves generated microphonic potentials in the epidermal head and lines of Sepia and Lolliguncula. J Comp Physiol A 164:1–5CrossRefPubMedGoogle Scholar
  7. Coombs S, Janssen J, Montgomery J (1992) Functional and evolutionary implications of peripheral diversity in lateral line systems. In: Webster DB, Fay RJ, Popper AN (eds) The evolutionary biology of hearing. Springer-Verlag, New York, pp 267–294CrossRefGoogle Scholar
  8. Denton EJ, Gray JAB (1982) The rigidity of fish and patterns of lateral line stimulation. Nature (London) 297:679–681CrossRefGoogle Scholar
  9. Dijkgraaf S (1963) Verusche uber Schallwahrnehmung bei Tintenfischen. Naturwissenschaften 50:50CrossRefGoogle Scholar
  10. Edmunds M (1974) Defense in animals. Longman, HarlowGoogle Scholar
  11. Fay RJ (1988) Hearing in vertebrates: a psychophysics databook. Hill-Fay, WinnetkaGoogle Scholar
  12. Fay RR (2009) Soundscapes and the sense of hearing of fishes. Integr Zool 4:26–32CrossRefPubMedGoogle Scholar
  13. Fewtrell JL, McCauley RD (2012) Impact of air gun noise on the behavior of marine fish and squid. Mar Pollut Bull 64:984–993CrossRefPubMedGoogle Scholar
  14. Fish MP, Mowbray WH (1970) Sounds of Western North Atlantic fishes. The Johns Hopkins Press, BaltimoreGoogle Scholar
  15. Fletcher H, Munson WA (1933) Loudness, its definition, measurement and calculation. J Acoust Soc Am 5:82–108CrossRefGoogle Scholar
  16. Gade (1982) Sound intensity (Part I. Theory). Brüel Kjær Tech Rev 3:3–39Google Scholar
  17. Green DM, Birdsall T, Tanner WP (1957) Signal detection as a function of signal intensity and duration. J Acoust Soc Am 29:523–531CrossRefGoogle Scholar
  18. Hanlon R, Budelmann BU (1987) Why cephalopods are probably not “deaf”. Am Nat 129:312–317CrossRefGoogle Scholar
  19. Hanlon RT, Messenger JB (1988) Adaptive coloration in young cuttlefish (Sepia officinalis L.): the morphology and development of body patterns and their relation to behavior. Philos Trans R Soc B 320:437–487CrossRefGoogle Scholar
  20. Hanlon R, Messenger JB (1996) Cephalopod behavior. Cambridge University Press, New YorkGoogle Scholar
  21. Hanlon R, Messenger JB (1998) Cephalopod behavior. Cambridge University Press, New YorkGoogle Scholar
  22. Hanlon RT, Hixon RF, Hulet WH (1983) Survival, growth and behavior of the loliginid squids, Loligo plei, Loligo pealei and Lolliguncula brevis (Mollusca: Cephalopoda) in closed seawater systems. Biol Bull 165:637–685CrossRefGoogle Scholar
  23. Hatch L, Clark C, Merrick R, Parijs SV, Ponirakis D, Schwehr K, Thompson M, Wiley D (2008) Characterizing the relative contributions of large vessels to total ocean noise fields: a case study using the Gerry E. Studds Stellwagen Bank National Marine Sanctuary. Environ Manag 42:735–752CrossRefGoogle Scholar
  24. Henninger HP, Watson WH (2005) Mechanisms underlying the production of carapace vibrations and associated waterborne sounds in the American lobster, Homarus americanus. J Exp Biol 208:3421–3429CrossRefPubMedGoogle Scholar
  25. Higgs DM, Radford CA (2016) The potential overlapping roles of the ear and lateral line in driving “acoustic” responses. Fish hearing and bioacoustics. Springer, Berlin, pp 255–270Google Scholar
  26. Humphries DA, Driver PM (1970) Protean defence by prey animals. Oecologia 5:285–302CrossRefGoogle Scholar
  27. Hunsicker ME, Essington TE, Watson R, Sumaila UR (2010) The contribution of cephalopods to global marine fisheries: can we have our squid and eat them too? Fish Fish 11:421–438CrossRefGoogle Scholar
  28. Jacobson (NOAA) LD (2005) Essential fish habitat source document: longfin inshore squid, Loligo pealeii, life history and habitat characteristics. NOAA Technical Memorandum NOS NCCOS, NMFS-NE 96:193Google Scholar
  29. Johnson CS (1968) Relation between abolute threshold and duration of tone pulse in the bottlenosed porpoise. J Acoust Soc Am 43:737–763CrossRefGoogle Scholar
  30. Kaifu K, Akamatsu T, Segawa S (2008) Underwater sound detection by cephalopod statocyst. Fish Sci 74:781–786CrossRefGoogle Scholar
  31. Ketten DR (1994) Functional analyses of whale ears: adaptations for underwater hearing. IEEE Proc Underw Acoust 1:264–270Google Scholar
  32. Lillis A, Eggleston D, Bohnenstiehl D (2013) Oyster larvae settle in response to habitat-associated underwater sounds. PLoS One 8:e79337CrossRefPubMedPubMedCentralGoogle Scholar
  33. Maniwa Y (1976) Attraction of bony fish, squid and crab by sound. In: Schuijf A, Hawkins AD (eds) Sound reception in fish. Elsevier, Amsterdam, pp 271–283Google Scholar
  34. Mäthger LM, Hanlon RT (2007) Malleable skin coloration in cephalopods: selective reflectance, transmission and absorbance of light by chromatophores and iridophores. Cell Tissue Res 329:179–186CrossRefPubMedGoogle Scholar
  35. Mooney TA, Hanlon RT, Christensen-Dalsgaard J, Madsen PT, Ketten DR, Nachtigall PE (2010) Hearing by the longfin squid (Loligo pealeii) studied with auditory evoked potentials: sensitivity to low-frequency particle motion and not pressure. J Exp Biol 213:3748–3759CrossRefPubMedGoogle Scholar
  36. Moynihan M (1985) Why are cephalopods deaf? Am Nat 125:465–469CrossRefGoogle Scholar
  37. Myrberg AA (1981) Sound communication and interception in fishes. In: Fay RR, Popper AN, Tavolga WN (eds) Hearing and sound communication in fishes. Springer, New York, p 608Google Scholar
  38. Myrberg AA (2001) The acoustical biology of elasmobranchs. Environ Biol Fishes 60:31–45CrossRefGoogle Scholar
  39. Niesterok B, Hanke W (2013) Hydrodynamic patterns from fast-starts in teleost fish and their possible relevance to predator-prey interactions. J Comp Physiol A 199:139–149CrossRefGoogle Scholar
  40. Nixon M, Young JZ (2003) The brains and lives of cephalopods. Oxford University Press, New YorkGoogle Scholar
  41. Norris KS (1966) Some observations on the migration and orientation of marine mammals. In: Storm RM (ed) Animal orientation and navigation. Oregon State University Press, Corvalis, pp 101–125Google Scholar
  42. Norris KS, Møhl B (1983) Can odontocetes debilitate prey with sound. Am Nat 122:85–104CrossRefGoogle Scholar
  43. O’Dor R, Miloslavich P, Yarincik K (2010) Marine biodiversity and biogeography—regional comparisons of global issues, an introduction. PLoS One 5:e11871CrossRefPubMedPubMedCentralGoogle Scholar
  44. Otis TS, Gilly WF (1990) Jet-propelled escape in the squid Loligo opalescens: concerted control by giant and non-giant motor axon pathways. Proc Natl Acad Sci 87:2911–2915CrossRefPubMedPubMedCentralGoogle Scholar
  45. Overholtz W, Link J, Suslowicz L (2000) The impact and implications of fish predation on pelagic fish and squid on the eastern USA shelf. ICES J Mar Sci 57:1147–1159CrossRefGoogle Scholar
  46. Packard A, Karlsen HE, Sand O (1990) Low frequency hearing in cephalopods. J Comp Physiol A 166:501–505CrossRefGoogle Scholar
  47. Radford C, Jeffs A, Tindle C, Montgomery JC (2008) Resonating sea urchin skeletons create coastal choruses. Mar Ecol Prog Ser 362:37–43CrossRefGoogle Scholar
  48. Rodhouse P (2001) Managing and forecasting squid fisheries in variable environments. Fish Res 54Google Scholar
  49. Ruiz-Cooley RI, Gendron D, Aquiniga S, Mesnick S, Carriquiry JD (2004) Trophic relationships between sperm whales and jumbo squid using stable isotopes of C and N. Mar Ecol Progr Ser 277:275–283CrossRefGoogle Scholar
  50. Samson J, Mooney TA, Guskerloo S, Hanlon RT (2014) Graded behavioral responses and habituation to sound in the common cuttlefish Sepia officinalis. J Exp Biol 217:4347–4355CrossRefPubMedGoogle Scholar
  51. Sole M, Lenoir M, Durfort M, Lopez-Bejar M, Lombarte A, Schaar Mvd, Andre M (2012) Does exposure to noise from human activities compromise sensory information from cephalopod statocysts? Deep Sea Res IIGoogle Scholar
  52. Stanley JA, Radford CA, Jeffs AG (2009) Induction of settlement in crab megalopae by ambient underwater reef sound. Behav Ecol 21:113–120CrossRefGoogle Scholar
  53. Stanley JA, Radford CA, Jeffs AG (2012) Location, location, location: finding a suitable home among the noise. Proc R Soc B Biol Sci 279:3622–3631CrossRefGoogle Scholar
  54. Staudinger MD, Hanlon RT, Juanes F (2011) Primary and secondary defences of squid to cruising and ambush predators: variable tactics and their survival value. Anim Behav 81:585–594CrossRefGoogle Scholar
  55. Suzuki Y, Takeshima H (2004) Equal-loudness-level contours for pure tones. J Acoust Soc Am 116Google Scholar
  56. Tricas TC, Boyle KS (2014) Acoustic behaviors in Hawaiian coral reef fish communities. Mar Ecol Progr Ser 511:1–16CrossRefGoogle Scholar
  57. Urick RJ (1983) Principles of underwater sound. Mc-Graw-Hill, New YorkGoogle Scholar
  58. Vermeij MJA, Marhaver KL, Huijbers CM, Nagelkerken I, Simpson SD (2010) Coral larvae move toward reef sounds. PLoS One 5:e10660CrossRefPubMedPubMedCentralGoogle Scholar
  59. Wensveen PJ, Huijser LA, Hoek L, Kastelein RA (2014) Equal latency contours and auditory weighting functions for the harbour porpoise (Phocoena phocoena). J Exp Biol 217:359–369CrossRefPubMedGoogle Scholar
  60. Wilson M, Hanlon RT, Tyack PL, Madsen PT (2007) Intense ultrasonic clicks from echolocating toothed whales do not elicit anti-predator responses or debilitate the squid Loligo pealeii. Biol Lett (UK) 3:225–227CrossRefGoogle Scholar
  61. York CA, Bartol IK (2014) Lateral line analogue aids vision in successful predator evasion for brief squid Lolliguncula brevis. J Exp Biol 217:2437–2439CrossRefPubMedGoogle Scholar
  62. Yost WA (1994) Fundamentals of hearing: an introduction. Academic Press, New YorkGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • T. Aran Mooney
    • 1
    Email author
  • Julia E. Samson
    • 1
    • 2
  • Andrea D. Schlunk
    • 1
  • Samantha Zacarias
    • 1
  1. 1.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA
  2. 2.Biology DepartmentUniversity of North Carolina at Chapel HillChapel HillUSA

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