Acoustic occurrence and behavior of ribbon seals (Histriophoca fasciata) in the Bering, Chukchi, and Beaufort seas

Abstract

Due to the difficulty of studying ice seals in their natural environment, distribution and movement patterns of ribbon seals (Histriophoca fasciata) over large spatio-temporal scales are poorly understood. In this study, we analyzed their distribution patterns in the Bering, Chukchi, and Beaufort seas, using passive acoustic data collected between August 2012 and July 2013 at 53 recording sites. Ribbon seal downsweeps were found using spectrogram correlation autodetection, at 30 of these recording sites. These detections were further manually analyzed to investigate the vocal repertoire and quantify the diel pattern in acoustic presence. We found that the Beaufort Sea shelf and the northern Bering Strait/southern Chukchi Sea are ecologically important for ribbon seals during the open-water season. Our results suggest that the northeastern Chukchi Sea serves as part of a migration corridor to and from the Chukchi Plateau and/or Beaufort Sea. In the Bering Sea, most detections occurred from February to June. Vocal activity was higher at nighttime than during the daytime prior to the peak calling period, while during the peak calling period, diel rhythm became less pronounced. The number of calls, proportional use of downsweeps, and bandwidth of downsweeps (estimated broadband source level 170–178 dB re 1 μPa-m) increased during the breeding period, from March to June, peaking in May. An additional call type, the “shuffle”, was identified in this study. These results improve our understanding of the migration, occurrence, and acoustic behavior of ribbon seals in the Bering, Chukchi, and Beaufort seas.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. Aerts LA et al (2013) Marine mammal distribution and abundance in an offshore sub-region of the northeastern Chukchi Sea during the open-water season. Cont Shelf Res 67:116–126

    Article  Google Scholar 

  2. Andersen JM, Skern-Mauritzen M, Boehme L, Wiersma YF, Rosing-Asvid A, Hammill MO, Stenson GB (2013) Investigating annual diving behaviour by hooded seals (Cystophora cristata) within the Northwest Atlantic Ocean. PLoS ONE 8:e80438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Aydin KY, Lapko V, Radchenko V, Livingston P (2002) A comparison of the eastern Bering and western Bering Sea shelf and slope ecosystems through the use of mass-balance food web models. NOAA Technical Memorandum NMFS-AFSC 130

  4. Bivand R, Lewin-Koh NJ (2017) MapTools: tools for reading and handling spatial objects (R package version 0.9–2). https://cran.r-project.org/package=maptools

  5. Boveng PL et al (2008) Status review of the ribbon seal (Histriophoca fasciata). U.S. Dep. Commer., NOAA Tech. Memo. NMFS-AFSC-191

  6. Boveng PL et al (2013) Status review of the ribbon seal (Histriophoca fasciata). U.S. Dep. Commer., NOAA Tech. Memo. NMFSAFSC-255

  7. Braham HW, Burns JJ, Fedoseev GA, Krogman BD (1984) Habitat partitioning by ice-associated pinnipeds: distribution and density of seals and walruses in the Bering Sea, April 1976. Sov Am Cooper Res Mar Mammal 1:25–47

    Google Scholar 

  8. Burns JJ (1970) Remarks on the distribution and natural history of pagophilic pinnipeds in the Bering and Chukchi Seas. J Mammal 51:445–454

    Article  Google Scholar 

  9. Burns JJ (1981) Ribbon seal—Phoca fasciata. In: Ridgway SH, Harrison RJ (eds) Handbook of marine mammals, vol 2 Seals. Academic Press, London, pp 89–110

  10. Cato D (1998) Simple methods of estimating source levels and locations of marine animal sounds. J Acoust Soc Am 104:1667–1678

    Article  CAS  PubMed  Google Scholar 

  11. Clark CW, Berchok CL, Blackwell SB, Hannay DE, Jones J, Ponirakis D, Stafford KM (2015) A year in the acoustic world of bowhead whales in the Bering, Chukchi and Beaufort seas. Prog Oceanogr 136:223–240

    Article  Google Scholar 

  12. Cleator HJ, Stirling I, Smith T (1989) Underwater vocalizations of the bearded seal (Erignathus barbatus). Can J Zool 67:1900–1910

    Article  Google Scholar 

  13. Deguchi T, Goto Y, Sakurai Y (2004) Importance of walleye pollock (Theragra chalcogramma) to wintering ribbon seals (Phoca fasciata) in Nemuro Strait, Hokkaido Japan. Mamm Study 29:55–63

    Article  Google Scholar 

  14. Dehn L-A, Sheffield GG, Follmann EH, Duffy LK, Thomas DL, O'Hara TM (2007) Feeding ecology of phocid seals and some walrus in the Alaskan and Canadian Arctic as determined by stomach contents and stable isotope analysis. Polar Biol 30:167–181

    Article  Google Scholar 

  15. EUMETSAT OaSISAF (2017) Global sea ice concentration climate data record 1979-2015 (v2.0, 2017). Norwegian and Danish Meteorological Institutes. https://doi.org/10.15770/EUM_SAF_OSI_0008

  16. Fedoseev G (2002) Ribbon seal (Histriophoca fasciata). Encyclopedia of marine mammals. Elsevier, Amsterdam, pp 1027–1030

  17. Frost KJ, Lowry LF (1980) Feeding of ribbon seals (Phoca fasciata) in the Bering Sea in spring. Can J Zool 58:1601–1607

    Article  Google Scholar 

  18. Frouin-Mouy H, Mouy X, Martin B, Hannay D (2016) Underwater acoustic behavior of bearded seals (Erignathus barbatus) in the northeastern Chukchi Sea, 2007–2010. Mar Mamm Sci 32:141–160

    Article  Google Scholar 

  19. Hannay DE, Delarue J, Mouy X, Martin BS, Leary D, Oswald JN, Vallarta J (2013) Marine mammal acoustic detections in the northeastern Chukchi Sea, September 2007–July 2011. Cont Shelf Res 67:127–146

    Article  Google Scholar 

  20. Ireland DS, Bisson L, Blackwell SB, Austin M, Hannay DE, Bröker K, Macrander AM (2016) Comprehensive report of marine mammal monitoring and mitigation in the Chukchi and Beaufort seas, 2006–2015. LGL Alaska Report P1363-E. Report from LGL Alaska Research Associates, Inc., Greeneridge Sciences, Inc., and JASCO Applied Sciences Ltd., for Shell Gulf of Mexico, Inc. and National Marine Fisheries Service, U.S. Fish and Wildlife Service

  21. Jay CV, Hills S (2005) Movements of walruses radio-tagged in Bristol Bay, Alaska. Arct 58:192–202

    Google Scholar 

  22. Jay CV, Udevitz MS, Kwok R, Fischbach AS, Douglas DC (2010) Divergent movements of walrus and sea ice in the northern Bering Sea. Mar Ecol Prog Ser 407:293–302

    Article  Google Scholar 

  23. Jones JM et al (2014) Ringed, bearded, and ribbon seal vocalizations north of Barrow, Alaska: seasonal presence and relationship with sea ice. Arct 67:203–222

    Article  Google Scholar 

  24. Kuletz KJ, Ferguson MC, Hurley B, Gall AE, Labunski EA, Morgan TC (2015) Seasonal spatial patterns in seabird and marine mammal distribution in the eastern Chukchi and western Beaufort seas: identifying biologically important pelagic areas. Prog Oceanogr 136:175–200

    Article  Google Scholar 

  25. Laidre KL et al (2015) Arctic marine mammal population status, sea ice habitat loss, and conservation recommendations for the 21st century. Conserv Biol 29:724–737

    Article  PubMed  PubMed Central  Google Scholar 

  26. Lammers MO, Brainard RE, Au WW, 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 123:1720–1728

    Article  PubMed  Google Scholar 

  27. Lowry LF (1985) The ribbon seal (Phoca fisciata). In: Burns JJ, Frost KJ, Lowry LF (eds) Marine mammals species accounts. Alaska Department Fish and Game, Juneau, AK, pp 59–66

    Google Scholar 

  28. MacIntyre KQ, Stafford KM, Conn PB, Laidre KL, Boveng PL (2015) The relationship between sea ice concentration and the spatio-temporal distribution of vocalizing bearded seals (Erignathus barbatus) in the Bering, Chukchi, and Beaufort Seas from 2008 to 2011. Prog Oceanogr 136:241–249

    Article  Google Scholar 

  29. Marcoux M, Ferguson SH, Roy N, Bedard JM, Simard Y (2017) Seasonal marine mammal occurrence detected from passive acoustic monitoring in Scott Inlet, Nunavut, Canada. Polar Biol 40:1127–1138

    Article  Google Scholar 

  30. Martin B, Kowarski K, Mouy X, Moors-Murphy H (2014) Recording and identification of marine mammal vocalizations on the Scotian shelf, and slope. In: OCEANS 2014 MTS/IEEE, St. Johns, Canada

  31. Mellinger DK, Stafford KM, Moore SE, Dziak RP, Matsumoto H (2007) An overview of fixed passive acoustic observation methods for cetaceans. Oceanogr 20:36–45

    Article  Google Scholar 

  32. Miksis-Olds JL, Parks SE (2011) Seasonal trends in acoustic detection of ribbon seal (Histriophoca fasciata) vocalizations in the Bering Sea. Aquat Mamm 37:464

    Article  Google Scholar 

  33. Miksis-Olds JL, Van Opzeeland IC, Van Parijs SM, Jones J (2016) Pinniped sounds in the polar oceans. In: Listening in the ocean. Springer, New York, pp 257–308

  34. Mizuguchi D, Mitani Y, Kohshima S (2016) Geographically specific underwater vocalizations of ribbon seals (Histriophoca fasciata) in the Okhotsk Sea suggest a discrete population. Mar Mamm Sci 32:1138–1151

    Article  Google Scholar 

  35. Mizuguchi D (2016) Underwater vocal repertoire and their function in three ice-breeding seals in the Arctic. Kyoto University

  36. Moore SE et al (2012) Comparing marine mammal acoustic habitats in Atlantic and Pacific sectors of the high Arctic: year-long records from Fram Strait and the Chukchi Plateau. Polar Biol 35:475–480

    Article  Google Scholar 

  37. Moors HB, Terhune JM (2003) Repetition patterns within harp seal (Pagophilus groenlandicus) underwater calls. Aquat Mamm 29:278–288

    Article  Google Scholar 

  38. Moors HB, Terhune JM (2004) Repetition patterns in Weddell seal (Leptonychotes weddellii) underwater multiple element calls. J Acoust Soc Am 116:1261–1270

    Article  PubMed  Google Scholar 

  39. Mouy X, Bahoura M, Simard Y (2009) Automatic recognition of fin and blue whale calls for real-time monitoring in the St. Lawrence. J Acoust Soc Am 126:2918–2928

    Article  PubMed  Google Scholar 

  40. Mouy X et al (2013) Passive acoustic monitoring of marine mammals in the Arctic. In: Samaran O, Samaran F (eds) Detection, classification and localisation of marine mammals using passive acoustics: 2003–2013, 10 years of international research. Dirac NGO, Paris, pp 185–224

    Google Scholar 

  41. Mouy X, Mouy P-A, Hannay D, Dakin T (2015) JMesh—a scalable web-based platform for visualization and mining of passive acoustic data. In: 2015 IEEE international conference on data mining workshop (ICDMW). IEEE, pp 773–779

  42. Olson DL, Delen D (2008) Advanced data mining techniques. Springer, New York

    Google Scholar 

  43. Otsuki M, Akamatsu T, Nobetsu T, Mizuguchi D, Mitani Y (2018) Diel changes in ribbon seal Histriophoca fasciata vocalizations during sea ice presence in the Nemuro Strait, Sea of Okhotsk. Polar Biol 41:451–456

    Article  Google Scholar 

  44. Overland JE, Wang M (2013) When will the summer Arctic be nearly sea ice free? Geophys Res Lett 40:2097–2101

    Article  Google Scholar 

  45. Richardson W, Greene J, Malme CR, Thompson DH (1996) Marine mammals and noise. Academic Press Inc, San Diego

    Google Scholar 

  46. Ripley B (2017) MASS: support functions and datasets for venables and Ripley’s MASS (R package version 7.3-48). https://CRAN.R-project.org/package=MASS

  47. Rogers TL (2014) Source levels of the underwater calls of a male leopard seal. J Acoust Soc Am 136:1495–1498

    Article  PubMed  Google Scholar 

  48. Rogers TL (2017) Calling underwater is a costly signal: size-related differences in the call rates of Antarctic leopard seals. Curr Zool 63:433–443

    Article  PubMed  PubMed Central  Google Scholar 

  49. Rogers T, Cato D (2002) Individual variation in the acoustic behaviour of the adult male leopard seal, hydrurga leptonyx. Behav 139:1267–1286

    Article  Google Scholar 

  50. Rossong M, Terhune J (2009) Source levels and communication-range models for harp seal (Pagophilus groenlandicus) underwater calls in the Gulf of St. Lawrence. Canada. Can J Zool 87:609–617

    Article  Google Scholar 

  51. Shustov AP (1965) The food of the ribbon seal in the Bering Sea (In Russian). Izvestiya TINRO 59:178–183

    Google Scholar 

  52. Simpkins MA, Hiruki-Raring LM, Sheffield G, Grebmeier JM, Bengtson JL (2003) Habitat selection by ice-associated pinnipeds near St. Lawrence Island, Alaska in March 2001. Polar Biol 26:577–586

    Article  Google Scholar 

  53. Stirling I, Calvert W, Spencer C (1987) Evidence of stereotyped underwater vocalizations of male Atlantic walruses (Odobenus rosmarus rosmarus). Can J Zool 65:2311–2321

    Article  Google Scholar 

  54. Stroeve JC, Kattsov V, Barrett A, Serreze M, Pavlova T, Holland M, Meier WN (2012) Trends in Arctic sea ice extent from CMIP5, CMIP3 and observations. Geophys Res Lett 39: L16502

    Article  Google Scholar 

  55. Struzinski WA, Lowe ED (1984) The effect of improper normalization on the performance of an energy detector. J Acoust Soc Am 76:S25–S25

    Article  Google Scholar 

  56. Terhune JM, Dell'Apa A (2006) Stereotyped calling patterns of a male weddell seal (Leptonychotes weddellii). Aquat Mamm 32:175–181

    Article  Google Scholar 

  57. Terhune JM, MacGowan G, Underhill L, Ronald K (1987) Repetitive rates of harp seal underwater vocalizations. Can J Zool 65:2119–2120

    Article  Google Scholar 

  58. Tervo OM, Parks SE, Christoffersen MF, Miller LA, Kristensen RM (2011) Annual changes in the winter song of bowhead whales (Balaena mysticetus) in Disko Bay, Western Greenland. Mar Mamm Sci 27:E241–E252

    Article  Google Scholar 

  59. Thode AT, Kim KH, Blackwell SB, Greene J, C.R., Nations CS, McDonald TL, Macrander AM (2012) Automated detection and localization of bowhead whale sounds in the presence of seismic airgun surveys. J Acoust Soc Am 131:3726–3747

    Article  PubMed  Google Scholar 

  60. Thomas JA, Kuechle VB (1982) Quantitative analysis of Weddell seal (Leptonychotesweddelli) underwater vocalizations at McMurdo Sound, Antarctica. J Acoust Soc Am 72:1730–1738

    Article  CAS  PubMed  Google Scholar 

  61. Tyack PL, Miller EH (2002) Vocal anatomy, acoustic communication and echolocation. In: Hoelzel AR (ed) Marine mammal biology: an evolutionary approach. Blackwell Science, Oxford, England, pp 142–184

    Google Scholar 

  62. Van Opzeeland I et al (2010) Acoustic ecology of Antarctic pinnipeds. Mar Ecol Prog Ser 414:267–291

    Article  Google Scholar 

  63. Van Parijs SM, Hastie GD, Thompson PM (1999) Geographical variation in temporal and spatial vocalization patterns of male harbour seals in the mating season. Anim Behav 58:1231–1239

    Article  PubMed  Google Scholar 

  64. Van Parijs SM, Kovacs KM, Lydersen C (2001) Spatial and temporal distribution of vocalising male bearded seals: implications for male mating strategies. Behaviour 138:905–922

    Article  Google Scholar 

  65. Ver Hoef JM, Cameron MF, Boveng PL, London JM, Moreland EE (2014) A spatial hierarchical model for abundance of three ice-associated seal species in the eastern Bering Sea. Stat Methodol 17:46–66

    Article  Google Scholar 

  66. Wassmann P, Duarte CM, Agustí S, Sejr MK (2011) Footprints of climate change in the Arctic marine ecosystem. Glob Change Biol 17:1235–1249

    Article  Google Scholar 

  67. Watkins WA, Ray GC (1977) Underwater sounds from ribbon seal, Phoca (Histriophoca) fasciata. Fish Bull 75:450–453

    Google Scholar 

  68. Wood SN (2001) mgcv: GAMs and generalized ridge regression for R. R News 1:20–25

    Google Scholar 

  69. Wood SN (2006) Generalized additive models: an introduction with R. Chapman and Hall/CRC Press, Boca Raton, FL

    Google Scholar 

  70. Wright DL, Berchok CL, Crance JL, Clapham PJ (2019) Acoustic detection of the critically endangered North Pacific right whale in the northern Bering Sea. Mar Mamm Sci 35:311–326

    Article  Google Scholar 

Download references

Acknowledgements

In the Chukchi Sea, the data acquisition program was funded jointly by Shell Exploration & Production Company (Dr. A.M. Macrander), ConocoPhillips Company (C. Rea), and Statoil USA E&P, Inc (J. Fenton). The data collection by Greeneridge Sciences in the Beaufort Sea was jointly supported by Shell Exploration & Production Company (Dr. A.M. Macrander) and ION Geophysical (J. Gagliardi). The 2012 science program in the Chukchi Sea was managed by Olgoonik-Fairweather LCC. We thank the captains and crew of all vessels, and all mooring technicians involved in those data collections for assistance with deployments, retrievals, and shipping of the acoustic recorders. The University of Washington instrument was funded by the USA National Science Foundation OPP-0855828. The NOAA data were BOEM-funded (detector development: North Pacific Right Whale Study, IA#M07RG13267, C. Monnett, C. Coon; main analysis: ARCWEST project, IA#M12PG00021, C. Monnett, J. Denton, and C. Fairfield). We thank three reviewers whose comments improved the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Héloïse Frouin-Mouy.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Disclaimer

The findings and conclusions in the paper are those of the authors and do not necessarily represent the views of the National Marine Fisheries Service, NOAA. Reference to trade names does not imply endorsement by the National Marine Fisheries Service, NOAA.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

300_2019_2462_MOESM2_ESM.mp4

Online Resource 2. Ribbon seal acoustic occurrence from 1 August 2012 through 31 July 2013 at the 53 acoustic recorder sites with daily sea ice extent (data files obtained from the ftp site on the ftp://sidads.colorado.edu/DATASETS/NOAA/G02186 directory). Grey dot: Acoustic recorder operational. Green dot: Ribbon seal acoustically detected. (MP4 7725 kb)

Online Resource 3. Yowl, growl, grunt and shuffle sequence from Figure 3 (Inset) (WAV 267 kb)

Online Resource 4. Downsweep from Figure 3 (WAV 70 kb)

Online Resource 5. Roar from Figure 3 (WAV 32 kb)

Online Resource 6. Hiss from Figure 3 (WAV 543 kb)

Electronic supplementary material 1 (PDF 839 kb)

Online Resource 2. Ribbon seal acoustic occurrence from 1 August 2012 through 31 July 2013 at the 53 acoustic recorder sites with daily sea ice extent (data files obtained from the ftp site on the ftp://sidads.colorado.edu/DATASETS/NOAA/G02186 directory). Grey dot: Acoustic recorder operational. Green dot: Ribbon seal acoustically detected. (MP4 7725 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Frouin-Mouy, H., Mouy, X., Berchok, C.L. et al. Acoustic occurrence and behavior of ribbon seals (Histriophoca fasciata) in the Bering, Chukchi, and Beaufort seas. Polar Biol 42, 657–674 (2019). https://doi.org/10.1007/s00300-019-02462-y

Download citation

Keywords

  • Ribbon seal
  • Histriophoca fasciata
  • Passive acoustic monitoring
  • Bering sea
  • Chukchi sea
  • Beaufort sea