Log in

Two species of seabirds foraged in contrasting marine habitats across the cold-water belt along the coast of northern Hokkaido in the southwestern Okhotsk Sea

  • Original Article
  • Biology
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

To understand the environmental factors affecting the density of foraging seabirds across the cold-water belt in the southwestern Okhotsk Sea, we conducted a 1-day (180-km transect length) shipboard seabird survey off the northeastern coast of Hokkaido during summer in 2019, along with acoustic observations of potential prey (zooplankton and fish) biomass, thermosalinograph measurements, and CTD observations. Planktivorous short-tailed shearwaters Ardenna tenuirostris (66% of total seabirds) and piscivorous rhinoceros auklets Cerorhinca monocerata (28%) were predominant, but foraged in contrasting habitats. A large foraging flock of shearwaters was observed in the cold-water belt zone, including its front with coastal Soya Warm Current Water and the offshore Fresh Surface Okhotsk Sea Water, where surface chlorophyll a concentrations were the highest but not related to their prey (zooplankton) biomass at any spatial scale between 4.6 and 9.2 km. In contrast, the density of auklets was high in the coastal Soya Warm Current Water, where the acoustically determined fish biomass was large, and showed a positive relationship with the fish biomass especially in the lower layer (29–104 m depth) at any spatial scale. This species-specific difference in response to prey biomass might be related to prey-searching behaviors; i.e., rhinoceros auklets search prey underwater visually, but short-tailed shearwater can use both visual and olfactory cues to locate zooplankton patches from the air.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Baduini CL, Hunt GL Jr, Pinchuk AI, Coyle KO (2006) Patterns in diet reveal foraging site fidelity of short-tailed shearwaters in the southeastern Bering Sea. Mar Ecol Prog Ser 320:279–292

    CAS  Google Scholar 

  • Biodiversity Center of Japan (2017) Monitoring site 1000 seabird investigation report fiscal year 2016. Nature Conservation Bureau, Ministry of the Environment, Fujiyoshida, Japan (in Japanese with English abstract)

  • Bost CA, Cotté C, Bailleul F, Cherel Y, Charrassin JB et al (2009) The importance of oceanic fronts to marine birds and mammals of the southern oceans. J Mar Syst 78:363–376

    Google Scholar 

  • Burger AE, Wilson RP, Garnier D, Wilson MPT (1993) Diving depths, diet, and underwater foraging of Rhinoceros Auklets in British Columbia. Can J Zool 71:2528–2540

    Google Scholar 

  • Dalpadado P, Arrigo KR, van Dijken GL, Skjoldal HR, Bagøien E, Dolgov AV, Prokopchuk IP, Sperfeld E (2020) Climate effects on temporal and spatial dynamics of phytoplankton and zooplankton in the Barents Sea. Prog Oceanogr 185:102320

    Google Scholar 

  • De Robertis A, McKelvey DR, Ressler PH (2010) Development and application of an empirical multifrequency method for backscatter classification. Can J Fish Aquat Sci 67:1459–1474

    Google Scholar 

  • Fauchald P, Erikstad KE (2002) Scale-dependent predator-prey interactions: the aggregative response of seabirds to prey under variable prey abundance and patchiness. Mar Ecol Prog Ser 231:279–291

    Google Scholar 

  • Foote KG, Knudsen HP, Vestnes G, MacLennan DN, Simmonds EJ (1987) Calibration of acoustic instruments for fish density estimation: practical guide. ICES Coop Res Rep 144:57

    Google Scholar 

  • Gaston AJ, Jones IL (1998) The Auks. Oxford University Press, Oxford

    Google Scholar 

  • Harris RP (1988) Interactions between diel vertical migratory behavior of marine zooplankton and the subsurface chlorophyll maximum. Bull Mar Sci 43:663–674

    Google Scholar 

  • Hasebe M, Senzaki M (2016) Records of seabirds breeding on Rebun Island, Hokkaido. Rishiri Stud 35:25–29 ((in Japanese with English abstract))

    Google Scholar 

  • Hazen EL, Suryan RM, Santora JA, Bograd SJ, Watanuki Y, Wilson RP (2013) Scales and mechanisms of marine hotspot formation. Mar Ecol Prog Ser 487:177–183

    Google Scholar 

  • Hokkaido national fisheries research institute (2017) Assessment of stock size of Japanese sand lance on soya straits in 2016. http://abchan.fra.go.jp/digests28/details/2851.pdf (Accessed 4 Feb 2021) (in Japanese)

  • Holland GJ, Greenstreet SPR, Gibb IM, Fraser HM, Robertson MR (2005) Identifying sandeel Ammodytes marinus sediment habitat preferences in the marine environment. Mar Ecol Prog Ser 303:269–282

    Google Scholar 

  • Hooker SK, Gerber LR (2004) Marine reserves as a tool for ecosystem-based management: the potential importance of megafauna. Bioscience 54:27–39

    Google Scholar 

  • Hunt GL Jr, Schneider D (1987) Scale-dependent processes in the physical and biological environment of marine birds. In: Croxall JP (ed) Seabirds: feeding ecology and role in marine ecosystems. Cambridge University Press, Cambridge, pp 7–41

    Google Scholar 

  • Hunt GL Jr, Heinemann D, Everson I (1992) Distributions and predator-prey interactions of macaroni penguins, Antarctic Fur seals, and Antarctic krill near Bird Island, South Georgia. Mar Ecol Prog Ser 86:15–30

    Google Scholar 

  • Hunt GL Jr, Coyle KP, Hoffman S, Decker MB, Flint EN (1996) Foraging ecology of short-tailed shearwaters near the Pribilof Islands, Bering Sea. Mar Ecol Prog Ser 141:1–11

    Google Scholar 

  • Hunt GL Jr, Baduini C, Jahncke J (2002) Diets of short-tailed shearwaters in the southeastern Bering Sea. Deep-Sea Res II 49:6147–6156

    Google Scholar 

  • Iida H, Isoda Y, Kobayashi N, Horio K (2018) Observation and model experiments of the diurnal eddy of the Cold Water Belt along the Offshore Side of the Soya Warm Current. Umi No Kenkyu 27(4):155–174

    Google Scholar 

  • Ishizu M, Kitade Y, Matsuyama M (2006) Formation mechanism of the cold-water belt formed off the Soya Warm Current. J Oceanogr 62:457–471

    Google Scholar 

  • Ishizu M, Kitade Y, Matsuyama M (2008) Characteristics of the cold-water belt formed off Soya warm current. J Geophys Res 113:C12010

    Google Scholar 

  • Ito M, Minami H, Tanaka Y, Watanuki Y (2009) Seasonal and inter-annual oceanographic changes induce diet switching in a piscivorous seabird. Mar Ecol Prog Ser 393:273–284

    Google Scholar 

  • Kazama K, Nishizawa B, Tsukamoto S, Gonzalez JE, Kazama MT, Watanuki Y (2018) Male and female Black-tailed Gulls Larus crassirostris feed on the same prey species but use different feeding habitats. J Ornithol 159:923–934

    Google Scholar 

  • Kokubun N, Iida K, Mukai T (2008) Distribution of murres (Uria spp.) and their prey south of St. George Island in the southeastern Bering Sea during the summers of 2003–2005. Deep-Sea Res Part II 55:1827–1836

    Google Scholar 

  • Kondratyev AY, Litvinenko NM, Shibaev YV, Vyatkin PS, Konfratyeva LF (2000) The breeding seabirds of the Russian Far East. In: Kondratyev AY, Litvinenko NM, Kaiser GW (eds) Seabirds of the Russian Far East. Special Publication, Canadian Wildlife Service, Ottawa, pp 37–81

    Google Scholar 

  • Korneliussen RJ (2018) Acoustic target classification. ICES Coop Res Rep 344:104. https://doi.org/10.17895/ices.pub.4567

    Article  Google Scholar 

  • Kurasawa K, Honda S, Watanuki Y (2011) Distribution of migrating short-tailed shearwater and breeding rhinoceros auklet and their prey in the northern Sea of Japan, Hokkaido in spring. Jpn J Ornithol 60:216–227

    Google Scholar 

  • Kuroki M, Kato A, Watanuki Y, Niizuma Y, Takahashi A, Naito Y (2003) Diving behavior of an epipelagically-feeding alcid, the rhinoceros auklet (Cerorhinca monocerata). Can J Zool 81:1249–1256

    Google Scholar 

  • Moeller HV, Laufkötter C, Sweeney EM, Johnson MD (2019) Light-dependent grazing can drive formation and deepening of deep chlorophyll maxima. Nat Commun 10:1978

    PubMed  PubMed Central  Google Scholar 

  • Nakanowatari T, Ohshima KI, Mensah V, Mitani Y, Hattori K, Kobayashi M, Roquet F, Sakurai Y, Mitsudera H (2017) Hydrographic observations by instrumented marine mammals in the Sea of Okhotsk. Polar Sci 13:56–65

    Google Scholar 

  • Nevitt GA, Veit RR, Kareiva P (1995) Dimethyl sulphide as a foraging cue for Antarctic procellariiform seabirds. Nature 376:680–682

    CAS  Google Scholar 

  • Nishizawa B, Matsuno K, Labunski EA, Kuletz KJ, Yamaguchi A, Watanuki Y (2017) Seasonal distribution of short-tailed shearwaters and their prey in the Bering and Chukchi seas. Biogeosciences 14:203–214

    Google Scholar 

  • Nishizawa B, Yamada N, Hayashi H, Wright C, Kuletz KJ, Ueno H, Mukai T, Yamaguchi A, Watanuki Y (2020) Timing of spring sea-ice retreat and summer seabird-prey associations in the northern Bering Sea. Deep-Sea Res II 182:104898

    Google Scholar 

  • Ogi H, Kubodera T, Nakamura K (1980) The pelagic feeding ecology of the Short-tailed Shearwaters Puffinus tenuirostris in the Subarctic Pacific Region. J Yamashina Inst Ornithol 12:157–182

    Google Scholar 

  • R Development Core Team (2020) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org/

  • Reiss CS, Cossio AM, Loeb V, Demer DA (2008) Variations in the biomass of Antarctic krill (Euphausia superba) around the South Shetland islands, 1996–2006. ICES J Mar Sci 65:497–508

    Google Scholar 

  • Safruddin (2013) Estimates of Japanese sandeel (Ammodytes personatus) distribution and biomass in the northern coast of Hokkaido, Japan, using a quantitative echo sounder. Doctoral thesis, Graduate School of Fisheries Sciences, Hokkaido University.

  • Santora JA, Ralston S, Sydeman WJ (2011) Spatial organization of krill and seabirds in the central California Current. ICES J Mar Sci 68:1391–1402

    Google Scholar 

  • Savoca MS, Nevitt GA (2014) Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators. Proc Natl Acad Sci USA 111:4157–4161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider DC (1990) Spatial autocorrelation in marine birds. Polar Res 8:89–97

    Google Scholar 

  • Sokal RR, Oden NL (1978) Spatial autocorrelation in biology 1. Methodol Biol J Linn Soc 10:199–228

    Google Scholar 

  • Suryan RM, Sato F, Balogh GR, David Hyrenbach K, Sievert PR, Ozaki K (2006) Foraging destinations and marine habitat use of short-tailed albatrosses: a multi-scale approach using first-passage time analysis. Deep Sea Res II 53:370–386

    Google Scholar 

  • Sydeman WJ, Brodeury RD, Grimes CB, Bychkov AS, McKinnell S (2006) Marine habitat “hotspots” and their use by migratory species and top predators in the North Pacific Ocean: introduction. Deep Sea Res II 53:247–249

    Google Scholar 

  • Takahashi A, Kuroki M, Niizuma Y, Kato A, Saitoh S, Watanuki Y (2001) Importance of the Japanese Anchovy (Engraulis japonicus) to breeding Rhinoceros Auklets (Cerorhinca monocerata) on the Teuri Island, Sea of Japan. Mar Biol 139:361–371

    Google Scholar 

  • Takizawa T (1982) Characteristics of the Soya Warm current in the Okhotsk Sea. J Oceanogr 38:281–292

    Google Scholar 

  • Tanaka H, Kajiwara T (1979) The distribution of Fulmarus glacialis and Puffinus tenuirostris, in the North Pacific Ocean and the Okhotsk Sea during the summer. J Yamashina Inst Ornith 11:79–86 ((In Japanese with English summary))

    Google Scholar 

  • Tasker M, Jones PH, Dixon T, Blake B (1984) Counting seabirds at sea from ships: a review of methods employed and suggestions for a standardized approach. Auk 101:567–577

    Google Scholar 

  • Townsend DW, Cucci TL, Berman T (1984) Subsurface chlorophyll maxima and vertical distribution of zooplankton in the Gulf of Maine. J Plankton Res 6:793–802

    CAS  Google Scholar 

  • Watanuki Y (1987) Breeding biology and foods of Rhinoceros Auklets on Teuri Island, Japan. Proc NIPR Symp Polar Biol 1:175–183

    Google Scholar 

  • Wright PJ, Jensen H, Tuck I (2000) The influence of sediment type on the distribution of the lesser sandeel, Ammodytes marinus. J Sea Res 44:243–256

    Google Scholar 

  • Yamamoto T, Hoshina K, Nishizawa B, Meathrel CE, Phillips RA, Watanuki Y (2015) Annual and seasonal movements of migrating short-tailed shearwaters reflect environmental variation in sub-Arctic and Arctic waters. Mar Biol 162:413–424

    CAS  Google Scholar 

Download references

Acknowledgements

We thank the captain, officers, and crews of the T/S Oshoro-maru for their help with field surveys. Keizo Ito and Sarufutsu Fishery Cooperative provided marine information on the study region. Nodoka Yamada helped with acoustic data analysis. We also thank two anonymous referees for their helpful comments that greatly improved the manuscript. This study was supported by JSPS KAKENHI Grant Number 20H03054 (Y. Mitani) and 19J01267 (B. Nishizawa) and by the Environment Research and Technology Development Fund (JPMEERF20214002) of the Environmental Restoration and Conservation Agency of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bungo Nishizawa.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nishizawa, B., Okado, J., Mitani, Y. et al. Two species of seabirds foraged in contrasting marine habitats across the cold-water belt along the coast of northern Hokkaido in the southwestern Okhotsk Sea. Fish Sci 88, 109–118 (2022). https://doi.org/10.1007/s12562-021-01576-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-021-01576-9

Keywords

Navigation