Marine Biology

, 163:127 | Cite as

Sound production and associated behaviours of benthic invertebrates from a coastal habitat in the north-east Atlantic

  • Laura Coquereau
  • Jacques Grall
  • Laurent Chauvaud
  • Cédric Gervaise
  • Jacques Clavier
  • Aurélie Jolivet
  • Lucia Di Iorio
Original paper

Abstract

Maerl beds are among the most endangered habitats in coastal temperate waters and a priority for conservation. Passive acoustics is a potential non-intrusive approach for surveying this fragile ecosystem with minor disturbances. Invertebrate sounds can be major contributors to natural coastal soundscapes but are not well studied. We conducted controlled tank-based experiments to identify sound-producing invertebrates inhabiting north-east Atlantic maerl beds and to characterise their sounds in terms of frequency features and source levels. We also determined which sound types are able to be detected above natural maerl ambient noise and suitable for in situ monitoring. Tank recording sessions of 20 abundant and potentially soniferous invertebrates from maerl beds revealed eight soniferous species and 15 different sound types. Two new sound-producing families were identified, Calyptraeidae and Majidae. Six sound types had properties consistent with detectability and identification for in situ acoustic studies: the feeding sound of sea urchins Echinus esculentus, Paracentrotus lividus and Psammechinus miliaris, snapping sound of the snapping shrimp Athanas nitescens, and feeding and other sounds of the spider crab Maja brachydactyla. Estimated detection distances ranged from a few metres for sea urchin feeding sounds up to about 40 m for A. nitescens snaps and spider crab feeding sounds. These invertebrates, particularly A. nitescens, probably make a substantial contribution to the maerl ambient noise. This invertebrate sound library sets a basis for in situ acoustic studies.

Supplementary material

227_2016_2902_MOESM1_ESM.pdf (341 kb)
Supplementary material 1 (PDF 341 kb)
227_2016_2902_MOESM2_ESM.pdf (128 kb)
Supplementary material 2 (PDF 127 kb)
227_2016_2902_MOESM3_ESM.pdf (129 kb)
Supplementary material 3 (PDF 128 kb)
227_2016_2902_MOESM4_ESM.wav (10.5 mb)
Supplementary material 4 (WAV 10778 kb)
227_2016_2902_MOESM5_ESM.wav (5.5 mb)
Supplementary material 5 (WAV 5636 kb)
227_2016_2902_MOESM6_ESM.wav (6 mb)
Supplementary material 6 (WAV 6181 kb)
227_2016_2902_MOESM7_ESM.wav (6.6 mb)
Supplementary material 7 (WAV 6770 kb)
227_2016_2902_MOESM8_ESM.wav (3.2 mb)
Supplementary material 8 (WAV 3256 kb)
227_2016_2902_MOESM9_ESM.wav (10.4 mb)
Supplementary material 9 (WAV 10640 kb)
227_2016_2902_MOESM10_ESM.wav (4.1 mb)
Supplementary material 10 (WAV 4211 kb)
227_2016_2902_MOESM11_ESM.wav (797 kb)
Supplementary material 11 (WAV 796 kb)

Supplementary material 12 (MP4 34522 kb)

227_2016_2902_MOESM13_ESM.pdf (127 kb)
Supplementary material 13 (PDF 126 kb)
227_2016_2902_MOESM14_ESM.pdf (469 kb)
Supplementary material 14 (PDF 468 kb)
227_2016_2902_MOESM15_ESM.pdf (469 kb)
Supplementary material 15 (PDF 468 kb)

References

  1. Akamatsu T, Okumura T, Novarini N, Yan HY (2002) Empirical refinements applicable to the recording of fish sounds in small tanks. J Acoust Soc Am 112:3073–3082CrossRefGoogle Scholar
  2. Alongi DM (1990) The ecology of tropical soft-bottom benthic ecosystems. Oceanogr Mar Biol Annu Rev 28:381–496Google Scholar
  3. Andrew N, Agatsuma Y, Ballesteros E, Bazhin A, Creaser E, Barnes D, Botsford L, Bradbury A, Campbell A, Dixon J (2003) Status and management of world sea urchin fisheries. Oceanogr Mar Biol Annu Rev 40:343–425Google Scholar
  4. Au WWL, Banks K (1998) The acoustics of the snapping shrimp Synalpheus parneomeris in Kaneohe Bay. J Acoust Soc Am 103:41–47CrossRefGoogle Scholar
  5. Au WWL, Hastings MC (2008) Principles of marine bioacoustics. Springer, New YorkCrossRefGoogle Scholar
  6. Au WWL, Richlen M, Lammers MO (2012) Soundscape of a nearshore coral reef near an urban center. In: Popper AN, Hawkins A (eds) The effects of noise on aquatic life. Springer, New York, pp 345–351CrossRefGoogle Scholar
  7. Bremner J, Rogers S, Frid C (2003) Assessing functional diversity in marine benthic ecosystems: a comparison of approaches. Mar Ecol Prog Ser 254:11–25CrossRefGoogle Scholar
  8. Budelmann BU (1992) Hearing in crustacea. In: Webster D, Popper A, Fay R (eds) The evolutionary biology of hearing. Springer, New York, pp 131–139CrossRefGoogle Scholar
  9. Buscaino G, Filiciotto F, Gristina M, Bellante A, Buffa G, Di Stefano V, Maccarrone V, Tranchida G, Buscaino C, Mazzola S (2011) Acoustic behaviour of the European spiny lobster Palinurus elephas. Mar Ecol Prog Ser 441:177–184CrossRefGoogle Scholar
  10. Buscaino G, Gavio A, Galvan D, Filiciotto F, Maccarrone V, de Vincenzi G, Mazzola S, Orensanz JM (2015) Acoustic signals and behaviour of Ovalipes trimaculatus in the context of reproduction. Aquat Biol 24:61–73CrossRefGoogle Scholar
  11. Cato DH (1978) Marine biological choruses observed in tropical waters near Australia. J Acoust Soc Am 64:736–743CrossRefGoogle Scholar
  12. Chitre M, Legg M, Koay T-B (2012) Snapping shrimp dominated natural soundscape in Singapore waters. Contrib Mar Sci 2012:127–134Google Scholar
  13. Clay CS, Medwin H (1977) Acoustical oceanography: principles and applications. Wiley, New YorkGoogle Scholar
  14. D’Spain GL, Batchelor HH (2006) Observations of biological choruses in the Southern California Bight: a chorus at midfrequencies. J Acoust Soc Am 120:19–42Google Scholar
  15. Di Iorio L, Gervaise C, Jaud V, Robson AA, Chauvaud L (2012) Hydrophone detects cracking sounds: non-intrusive monitoring of bivalve movement. J Exp Mar Biol Ecol 432–433:9–16CrossRefGoogle Scholar
  16. Erbe C (2010) Underwater acoustics: noise and the effects on marine mammals. JASCO Applied Sciences, BrisbaneGoogle Scholar
  17. Everest FA, Young RW, Johnson MW (1948) Acoustical characteristics of noise produced by snapping shrimp. J Acoust Soc Am 20:137–142CrossRefGoogle Scholar
  18. Freeman SE, Rohwer FL, D’Spain GL, Friedlander AM, Gregg AK, Sandin SA, Buckingham MJ (2014) The origins of ambient biological sound from coral reef ecosystems in the Line Islands archipelago. J Acoust Soc Am 135:1775CrossRefGoogle Scholar
  19. Grall J (2002) Biodiversité spécifique et fonctionnelle du maerl: réponses à la variabilité de l’environnement côtier. Ph.D. dissertation, Université de Bretagne OccidentaleGoogle Scholar
  20. Grall J, Hall-Spencer JM (2003) Problems facing maerl conservation in Brittany. Aquat Conserv Mar Fresh Ecosyst 13:S55–S64CrossRefGoogle Scholar
  21. Gray J, Aschan M, Carr M, Clarke K, Green R, Pearson T, Rosenberg R, Warwick R (1988) Analysis of community attributes of the benthic macrofauna of Frierfjord/Langesundfjord and in a mesocosm experiment. Mar Ecol Prog Ser 46:151–165CrossRefGoogle Scholar
  22. Guillou M, Grall J, Connan S (2002) Can low sea urchins densities control macro epiphytic biomass in NE Atlantic maerl beds. J Mar Biol Assoc 82:867–876CrossRefGoogle Scholar
  23. Hall-Spencer JM (1998) Conservation issues relating to maerl beds as habitats for molluscs. J Conchol 2:271–286Google Scholar
  24. Hall-Spencer JM, Moore PG (2000) Scallop dredging has profound, long-term impacts on maerl habitats. ICES J Mar Sci 57:1407–1415CrossRefGoogle Scholar
  25. Hall-Spencer JM, White NA, Gillespie E, Gillham K, Foggo A (2006) Impact of fish farms on maerl beds in strongly tidal areas. Mar Ecol Prog Ser 326:1–9CrossRefGoogle Scholar
  26. Harley CD, Hughes AR, Hultgren KM, Miner BG, Sorte CJ, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241CrossRefGoogle Scholar
  27. Harmelin JG, Bouchon C, Hong JS (1981) Impact de la pollution sur la distribution des échinodermes des substrats durs en Provence (Méditerranée Nord-occidentale). Thétys 10:13–36Google Scholar
  28. Harrold C, Pearse JS (1987) The ecological role of echinoderms in kelp forests. Echinoderm Stud 2:137–233Google Scholar
  29. Iversen RTS, Perkins PJ, Dionne RD (1963) An indication of underwater sound production by squid. Nature 199:250–251CrossRefGoogle Scholar
  30. Johnson MW, Everest FA, Young RW (1947) The role of snapping shrimp (Crangon and Synalpheus) in the production of underwater noise in the sea. Biol Bull 93:122–138CrossRefGoogle Scholar
  31. Kamenos NA, Moore PG, Hall-Spencer JM (2004a) Small-scale distribution of juvenile gadoids in shallow inshore waters; what role does maerl play? ICES J Mar Sci 61:422–429CrossRefGoogle Scholar
  32. Kamenos NA, Moore PG, Hall-Spencer JM (2004b) Attachment of the juvenile queen scallop (Aequipecten opercularis (L.)) to maerl in mesocosm conditions; juvenile habitat selection. J Exp Mar Biol Ecol 306:139–155CrossRefGoogle Scholar
  33. Kamenos NA, Moore PG, Hall-Spencer JM (2004c) The importance of maerl grounds for recruitment of queen scallops (Aequipecten opercularis) and other invertebrates. Mar Ecol Prog Ser 274:183–189CrossRefGoogle Scholar
  34. Kay SM (1998) Fundamentals of statistical signal processing. In: Detection theory, vol II. Prentice Hall, Upper Saddle RiverGoogle Scholar
  35. Kelly JR, Sceibling RE, Balch T (2011) Invasion-mediated shifts in the macrobenthic assemblage of a rocky subtidal ecosystem. Mar Ecol Prog Ser 437:69–78CrossRefGoogle Scholar
  36. Kennedy EV, Holderied MW, Mair JM, Guzman HM, Simpson SD (2010) Spatial patterns in reef-generated noise relate to habitats and communities: evidence from a Panamanian case study. J Exp Mar Biol Ecol 395:85–92CrossRefGoogle Scholar
  37. Kim BN, Hahn J, Choi BK, Kim BC (2010) Snapping shrimp sound measured under laboratory conditions. Jpn J Appl Phys 49:1–4Google Scholar
  38. Kinda GB, Simard Y, Gervaise C, Mars J, Fortier L (2013) Under-ice ambient noise in Eastern Beaufort Sea, Canadian Arctic, and its relation to environmental forcing. J Acoust Soc Am 134:77–87CrossRefGoogle Scholar
  39. Knowlton RE, Moulton JM (1963) Sounds production in the snapping shrimps Alpheus (Crangon) and Synalpheus. Biol Bull 125:311–331CrossRefGoogle Scholar
  40. Koay TB, Tan ET, Chitre M, Potter JR (2003) Estimating the spatial and temporal distribution of snapping shrimp using a portable, broadband 3-dimensional acoustic array. In: Proceedings of the Oceans 2003. Marine Technology and Ocean Science Conference, pp 2706–2713Google Scholar
  41. Lammers MO, Brainard RE, Au WWL, Mooney TA, Wong KB (2008) An ecological acoustic recorder (EAR) for long-term monitoring of biological and anthropogenic sounds on coral reefs and other marine habitats. J Acoust Soc Am 123:1720–1728CrossRefGoogle Scholar
  42. Lawrence JM (1975) On the relationships between marine plants and sea urchins. Oceanogr Mar Biol Annu Rev 13:213–286Google Scholar
  43. Lawrence JM (2006) Edible sea urchins: biology and ecology. Elsevier, OxfordGoogle Scholar
  44. Le Foll D (1993) Biologie et exploitation de l’araignée de mer Maja squinado Herbst en Manche Ouest. Ph.D. dissertation, Université de Bretagne OccidentaleGoogle Scholar
  45. Lillis A, Eggleston DB, Bohnenstiehl DR (2013) Oyster larvae settle in response to habitat-associated underwater sounds. PLoS One 8:e79337CrossRefGoogle Scholar
  46. Lillis A, Eggleston DB, Bohnenstiehl DR (2014) Estuarine soundscapes: distinct acoustic characteristics of oyster reefs compared to soft-bottom habitats. Mar Ecol Prog Ser 505:1–17CrossRefGoogle Scholar
  47. Lobel PS (2002) Sounds produced by spawning fishes. Environ Biol Fishes 33:351–358CrossRefGoogle Scholar
  48. Lucrezi S, Schlacher TA (2014) The ecology of ghost crabs. Oceanogr Mar Biol Annu Rev 52:201–256Google Scholar
  49. Luczkovich JJ, Mann DA, Rountree RA (2008) Passive acoustics as a tool in fisheries science. Trans Am Fish Soc 137:533–541CrossRefGoogle Scholar
  50. Mathias D, Gervaise C, Di Iorio L (2016) Wind dependence of shallow water ambient noise in a biologically rich temperate coastal area. J Acous Soc Am 139:EL839CrossRefGoogle Scholar
  51. McCauley RD, Cato DH (2000) Patterns of fish calling in a nearshore environment in the Great Barrier Reef. Philos Trans R Soc Lond B Biol Sci 355:1289–1293CrossRefGoogle Scholar
  52. Mellinger DK, Stafford KM, Moore SE, Dziak R, Matsumoto H (2007) An overview of fixed passive acoustic observation methods for cetaceans. Oceanography 20:36–45CrossRefGoogle Scholar
  53. Meyer-Rochow VB, Penrose JD (1976) Sound production by the western rock lobster Panulirus longipes (Milne Edwards). J Exp Mar Biol Ecol 23:191–209CrossRefGoogle Scholar
  54. Moore SE, Stafford KM, Mellinger DK, Hildeband JA (2006) Listening for large whales in off-shore waters of Alaska. Bioscience 56:49–55CrossRefGoogle Scholar
  55. Myrberg AA (1981) Sound communication and interception in fishes. In: Tavolga W, Popper A, Fay R (eds) Hearing and sound communication in fishes. Springer, New York, pp 395–426CrossRefGoogle Scholar
  56. Nedelec SL, Simpson SD, Holderied M, Radford AN, Lecellier G, Radford C, Lecchini D (2015) Soundscapes and living communities in coral reefs: temporal and spatial variation. Mar Ecol Prog Ser 524:125–135CrossRefGoogle Scholar
  57. Okumura T, Akamatsu T, Yan HY (2002) Analyses of small tank acoustics: empirical and theoretical approaches. Bioacoustics 12:330–332CrossRefGoogle Scholar
  58. Parvulescu A (1964) Problems of propagation and processing. In: Tavolga WN (ed) Marine bio-acoutics. Pergamon, Oxford, pp 87–100Google Scholar
  59. Parvulescu A (1967) The acoustics of small tanks. In: Tavolga WN (ed) Marine bio-acoutics. Pergamon, Oxford, pp 7–13Google Scholar
  60. Patek SN (2001) Spiny lobsters stick and slip to make sound. Nature 411:153–154CrossRefGoogle Scholar
  61. Patek SN (2002) Squeaking with a sliding joint: mechanics and motor control of sound production in palinurid lobsters. J Exp Biol 205:2375–2385Google Scholar
  62. Patek SN, Caldwell R (2006) The stomatopod rumble: low frequency sound production in Hemisquilla californiensis. Mar Freshw Behav Phys 39:99–111CrossRefGoogle Scholar
  63. Peña V, Bárbara I, Grall J, Maggs CA, Hall-Spencer JM (2014) The diversity of seaweeds on maerl in the NE Atlantic. Mar Biodiv 44:1–19CrossRefGoogle Scholar
  64. Picciulin M, Bolgan M, Codarin A, Fiorin R, Zucchetta M, Malavasi S (2013) Passive acoustic monitoring of Sciaena umbra on rocky habitats in the Venetian littoral zone. Fish Res 145:76–81CrossRefGoogle Scholar
  65. Piercy JJ, Codling EA, Hill AJ, Smith DJ, Simpson SD (2014) Habitat quality affects sound production and likely distance of detection on coral reefs. Mar Ecol Prog Ser 516:35–47CrossRefGoogle Scholar
  66. Popper AN, Salmon M, Horch KW (2001) Acoustic detection and communication by decapods crustaceans. J Comp Phys A 187:83–89CrossRefGoogle Scholar
  67. Radford CA, Jeffs AG, Tindle CT, Montgomery JC (2008a) Resonating sea urchin skeletons create coastal choruses. Mar Ecol Prog Ser 362:37–43CrossRefGoogle Scholar
  68. Radford CA, Jeffs AG, Tindle CT, Montgomery JC (2008b) Temporal patterns in ambient noise of biological origin from a shallow water temperate reef. Oecologia 156:921–929CrossRefGoogle Scholar
  69. Radford CA, Stanley JA, Tindle CT, Montgomery JC, Jeffs AG (2010) Localised coastal habitats have distinct underwater sound signatures. Mar Ecol Prog Ser 401:21–29CrossRefGoogle Scholar
  70. Salmon M (1967) Coastal distribution, display and sound production by Florida fiddler crabs (Genus Uca). Anim Behav 15:449–459CrossRefGoogle Scholar
  71. Salmon M (1983) Acoustic “calling” by fiddler and ghost crabs. Mem Aust Mus 18:63–76CrossRefGoogle Scholar
  72. Schmitz B (2002) Sound production in Crustacea with special reference to the Alpheidae. In: Wiese K (ed) The crustacean nervous system. Springer, New York, pp 536–547CrossRefGoogle Scholar
  73. Simpson SD, Meekan M, Montgomery JC, McCauley R, Jeffs AG (2005) Homeward sound. Science 308:221CrossRefGoogle Scholar
  74. Smaldon G, Holthuis LB (1993) Coastal shrimps and prawns: keys and notes for identification of the species. Linnean Society of London and the Estuarine and Coastal Sciences Association by Field Studies Council, ShrewsburyGoogle Scholar
  75. Staaterman ER, Clark CW, Gallagher AJ, deVries MS, Claverie T, Patek SN (2011) Rumbling in the benthos: acoustic ecology of the California mantis shrimp Hemisquilla californiensis. Aquat Biol 13:97–105CrossRefGoogle Scholar
  76. Staaterman ER, Paris CB, DeFerrari HA, Mann DA, Rice AN, Alessandro EK (2014) Celestial patterns in marine soundscapes. Mar Ecol Prog Ser 508:17–32CrossRefGoogle Scholar
  77. Stanley JA, Radford CA, Jeffs AG (2012) Location, location, location: finding a suitable home among the noise. Proc Biol Sci 279:3622–3631CrossRefGoogle Scholar
  78. Team BIOMAERL (2003) Conservation and management of northeast Atlantic and Mediterranean maerl beds. Aquat Conserv Mar fresh Ecosyst 13:565–576Google Scholar
  79. Tolimieri N, Jeffs AG, Montgomery JC (2000) Ambient sound as a cue for navigation by the pelagic larvae of reef fishes. Mar Ecol Prog Ser 207:219–224CrossRefGoogle Scholar
  80. Tricas TC, Boyle KS (2014) Acoustic behaviours in Hawaiian coral reef fish communities. Mar Ecol Prog Ser 511:1–16CrossRefGoogle Scholar
  81. Tyack P, Clark C (2000) Communication and acoustic behaviour of dolphins and whales. In: Au WL, Fay R, Popper A (eds) Hearing by whales and dolphins. Springer, New York, pp 156–224CrossRefGoogle Scholar
  82. Urick RJ (1984) Ambient noise in the sea. McGraw-Hill, New YorkGoogle Scholar
  83. Versluis M, Schmitz B, von der Heydt A, Lohse D (2000) How snapping shrimp snap: through cavitating bubbles. Science 289:2114–2117CrossRefGoogle Scholar
  84. Watanabe M, Sekine M, Hamada E, Ukita M, Imai T (2002) Monitoring of shallow sea environment by using snapping shrimps. Water Sci Technol 46:419–424Google Scholar
  85. Wenz GM (1962) Acoustic ambient noise in the ocean: spectra and sources. J Acoust Soc Am 34:1936–1956CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Laura Coquereau
    • 1
  • Jacques Grall
    • 2
  • Laurent Chauvaud
    • 1
    • 2
  • Cédric Gervaise
    • 3
    • 4
  • Jacques Clavier
    • 1
  • Aurélie Jolivet
    • 1
    • 5
  • Lucia Di Iorio
    • 3
  1. 1.Laboratoire des Sciences de l’Environnement Marin, UMR 6539, Institut Universitaire Européen de la MerUniversité de Bretagne OccidentalePlouzanéFrance
  2. 2.Observatoire Marin, UMS 3113Institut Universitaire Européen de la MerPlouzanéFrance
  3. 3.Chaire CHORUS, Fondation Grenoble INPGrenobleFrance
  4. 4.GIPSA-LABSaint Martin d’HèresFrance
  5. 5.TBM Environnement/SommePlouzanéFrance

Personalised recommendations