Skip to main content

Advertisement

Log in

Anadromy sustained in the artificially land-locked population of Sakhalin taimen in northern Japan

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

The conservation of land-locked populations of migratory fishes is increasingly important in the era of dam removal and habitat reconnection. We used an otolith strontium (Sr) tracer (87Sr/86Sr) to test the hypothesis that a land-locked population of an endangered salmonine species, Sakhalin taimen (Parahucho perryi), retains the capacity for anadromy, and that some individuals out-migrate from the reservoir to the sea. Years later, these individuals return but are blocked by the migration barrier of the reservoir dam and are denied reproduction in their natal streams. Juvenile taimen collected from the reservoir and two nearby regions were classified based on their otolith Sr isotopic signatures to their regions of origin with an overall accuracy of 88%. When the same classifier was applied to ocean-caught adult taimen, we predicted some individuals had originated from the reservoir with high posterior probabilities (> 0.9). Whether the land-locked Sakhalin taimen can help sustain the metapopulation dynamics of the species at the watershed scale may depend on whether, and how soon, the disrupted migration pathway is restored.

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

Access this article

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

  • Arai T, Kotake A, Morita K (2004) Evidence of downstream migration of Sakhalin taimen, Hucho perryi, as revealed by Sr:Ca ratios of otolith. Ichthyol Res 51:377–380

    Article  Google Scholar 

  • Barnett-Johnson R, Pearson TE, Ramos FC, Grimes CB, MacFarlane BR (2008) Tracking natal origins of salmon using isotopes, otoliths, and landscape geology. Limnol Oceanogr 53:1633–1642

    Article  CAS  Google Scholar 

  • Brennan SR, Fernandez DP, Zimmerman CE, Cerling TE, Brown RJ, Wooller MJ (2015) Strontium isotopes in otoliths of a non-migratory fish (slimy sculpin): implications for provenance studies. Geochim Cosmochim Ac 149:32–45

    Article  CAS  Google Scholar 

  • Bunn S, Arthington A (2002) Basic principles and ecological consequences of altered flow regimes for aquatic biodiversity. Environ Manag 30:492–507

    Article  Google Scholar 

  • Cleveland WS (1979) Robust locally weighted regression and smoothing scatterplots. J Am Stat Assoc 74:829–836

    Article  Google Scholar 

  • Crook DA, Lacksen K, King AJ, Buckle DJ, Tickell SJ, Woodhead JD, Maas R, Townsend SA, Douglas MM (2017) Temporal and spatial variation in strontium in a tropical river: implications for otolith chemistry analyses of fish migration. Can J Fish Aquat Sci 74:533–545

    Article  CAS  Google Scholar 

  • Dauble D, Watson D (1997) Status of fall Chinook salmon populations in the mid-Columbia River, 1948–1992. N Am J Fish Manag 17:283–300

    Article  Google Scholar 

  • Donohoe CJ, Adams PB, Royer CF (2008) Influence of water chemistry and migratory distance on ability to distinguish progeny of sympatric resident and anadromous rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 65:1060–1075

    Article  CAS  Google Scholar 

  • Fukushima M, Shimazaki H, Rand PS, Kaeriyama M (2011) Reconstructing Sakhalin taimen Parahucho perryi historical distribution and identifying causes for local extinctions. Trans Am Fish Soc 140:1–13

    Google Scholar 

  • Godbout L, Wood C, Withler R, Latham S, Nelson R, Wetzel L, Barnett-Johnson R, Grove M, Schmitt A, McKeegan K, Bradford M (2011) Sockeye salmon (Oncorhynchus nerka) return after an absence of nearly 90 years: a case of reversion to anadromy. Can J Fish Aquat Sci 68:1590–1602

    Article  CAS  Google Scholar 

  • Gross MR (1987) Evolution of diadromy in fishes. Am Fish Soc Symp 1:14–25

    Google Scholar 

  • Hayes SA, Hanson CV, Pearse DE, Bond MH, Garza J, MacFarlane BR (2012) Should I stay or should I go? The influence of genetic origin on emigration behavior and physiology of resident and anadromous juvenile Oncorhynchus mykiss. N Am J Fish Manag 32:772–780

    Article  Google Scholar 

  • Hegg JC, Kennedy BP, Chittaro P (2019) What did you say about my mother? The complexities of maternally derived chemical signatures in otoliths. Can J Fish Aquat Sci 76:81–94

    Article  CAS  Google Scholar 

  • Hodell DA, Mueller PA, McKenzie JA, Mead GA (1989) Strontium isotope stratigraphy and geochemistry of the late Neogene Ocean. Earth Planet Sc Lett 92:165–178

    Article  CAS  Google Scholar 

  • Hodge BW, Wilzbach MA, Duffy WG, Quiñones RM, Hobbs JA (2016) Life history diversity in Klamath River steelhead. Trans Am Fish Soc 145:227–238

    Article  Google Scholar 

  • Hokkaido Government (2014) Koetoi River improvement work - environmental assessment. Hokkaido Wakkanai Kensetsu Kanribu

  • Holčík J, Hensel K, Nieslanik J, Skácel L (1988) The Eurasian Huchen, Hucho hucho. Largest salmon of the world. Dr. W Junk Publishers, Dordrecht

    Book  Google Scholar 

  • Holecek DE, Scarnecchia DL, Miller SE (2012) Smoltification in an impounded, adfluvial Redband trout population upstream from an impassable dam: does it persist? Trans Am Fish Soc 141:68–75

    Article  Google Scholar 

  • Honda K, Arai T, Takahashi N, Miyashita K (2010) Life history and migration of Sakhalin taimen, Hucho perryi, caught from Lake Akkeshi in eastern Hokkaido, Japan, as revealed by Sr:ca ratios of otoliths. Ichthyol Res 57:416–421

    Article  Google Scholar 

  • HRDB (2009) River development plans for the Koetoi River system [online]. Hokkaido Regional Development Bureau. https://www.hkd.mlit.go.jp/ky/ki/chousei. Accessed 20 Feb 2019

  • Jackson MG, Hart SR (2006) Strontium isotopes in melt inclusions from Samoan basalts: implications for heterogeneity in the Samoan plume. Earth Planet Sc Lett 245:260–277

    Article  CAS  Google Scholar 

  • Kalish JM (1990) Use of otolith microchemistry to distinguish the progeny of sympatric anadromous and non-anadromous salmonids. Fish Bull 88:657–666

    Google Scholar 

  • Kendall NW, McMillan JR, Sloat MR, Buehrens TW, Quinn TP, Pess GR, Kuzishchin KV, McClure MM, Zabel RW, Bradford M (2015) Anadromy and residency in steelhead and rainbow trout (Oncorhynchus mykiss): a review of the processes and patterns. Can J Fish Aquat Sci 72:319–342

    Article  CAS  Google Scholar 

  • Kennedy BP, Blum JD, Folt CL, Nislow KH (2000) Using natural strontium isotopic signatures as fish markers: methodology and application. Can J Fish Aquat Sci 57:2280–2292

    Article  CAS  Google Scholar 

  • Kennedy BP, Klaue A, Blum JD, Folt CL, Nislow KH (2002) Reconstructing the lives of fish using Sr isotopes in otoliths. Can J Fish Aquat Sci 59:925–929

    Article  Google Scholar 

  • Komiyama E, Takahashi G (1988) Chapter 2 freshwater fish. In: Ohtaishi N, Nakagawa H (eds) Animals of Shiretoko – vertebrate fauna in their natural state and their conservation in the Shiretoko Peninsula, Hokkaido. Japan. Hokkaido University Press, Sapporo, pp 15–58

    Google Scholar 

  • McCulloch M, Cappo M, Aumend J, Müller W (2005) Tracing the life history of individual barramundi using laser ablation MC-ICP-MS Sr-isotopic and Sr/Ba ratios in otoliths. Mar Freshw Res 56:637–644

    Article  CAS  Google Scholar 

  • Muhlfeld CC, Thorrold SR, McMahon TE, Marotz B, Gillanders B (2012) Estimating westslope cutthroat trout (Oncorhynchus clarkii lewisi) movements in a river network using strontium isoscapes. Can J Fish Aquat Sci 69:906–915

    Article  CAS  Google Scholar 

  • Padilla AJ, Brown RJ, Wooller MJ (2015) Strontium isotope analyses (87Sr/86Sr) of otoliths from anadromous Bering cisco (Coregonus laurettae) to determine stock composition. ICES J Mar Sci 72:2110–2117

    Article  Google Scholar 

  • Pearse DE, Campbell MA (2018) Ancestry and adaptation of rainbow trout in Yosemite National Park. Fisheries 43:472–484

    Article  Google Scholar 

  • Pearse DE, Hayes SA, Bond MH, Hanson CV, Anderson EC, Macfarlane BR, Garza J (2009) Over the falls? Rapid evolution of ecotypic differentiation in steelhead/rainbow trout (Oncorhynchus mykiss). J Hered 100:515–525

    Article  CAS  PubMed  Google Scholar 

  • Pess G, Hilborn R, Kloehn K, Quinn T, Bradford M (2012) The influence of population dynamics and environmental conditions on pink salmon (Oncorhynchus gorbuscha) recolonization after barrier removal in the Fraser River, British Columbia, Canada. Can J Fish Aquat Sci 69:970–982

    Article  Google Scholar 

  • Phillis CC, Sturrock A, Johnson RC, Weber PK (2018) Endangered winter-run Chinook salmon rely on diverse rearing habitats in a highly altered landscape. Biol Conserv 217:358–362

    Article  Google Scholar 

  • Quinn TP, Bond MH, Brenkman SJ, Paradis R, Peters RJ (2017) Re-awakening dormant life history variation: stable isotopes indicate anadromy in bull trout following dam removal on the Elwha River, Washington. Environ Biol Fish 100:1659–1671

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/. Accessed 20 Feb 2019

    Google Scholar 

  • Rand PS (2006) Hucho perryi. The IUCN red list of threatened species 2006: e.T61333A12462795. https://www.iucnredlist.org. Accessed 20 Feb 2019

  • Suzuki K, Yoshitomi T, Kawaguchi Y, Ichimura M, Edo K, Otake T (2011) Migration history of Sakhalin taimen Hucho perryi captured in the Sea of Okhotsk, northern Japan, using otolith Sr:Ca ratios. Fish Sci 77:313–320

    Article  CAS  Google Scholar 

  • Thrower FP, Joyce JE (2004) Effects of 70 years of freshwater residency on survival, growth, early maturation, and smolting in a stock of anadromous rainbow trout from Southeast Alaska. Am Fish Soc Symp 44:485–496

    Google Scholar 

  • Venables WN, Ripley BD (1999) Modern applied statistics with S-PLUS, 3rd edn. Springer, New York

    Book  Google Scholar 

  • Walther B, Limburg K (2012) The use of otolith chemistry to characterize diadromous migrations. J Fish Biol 81:796–825

    Article  CAS  PubMed  Google Scholar 

  • Walther BD, Thorrold SR (2009) Inter-annual variability in isotope and elemental ratios recorded in otoliths of an anadromous fish. J Geochem Explor 102:181–186

    Article  CAS  Google Scholar 

  • Walther BD, Dempster T, Letnic M, McCulloch MT (2011) Movements of diadromous fish in large unregulated tropical rivers inferred from geochemical tracers. PLoS One 6(4):e18351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winans GA, Gayeski N, Timmins-Schiffman E (2015) All dam-affected trout populations are not alike: fine scale geographic variability in resident rainbow trout in Icicle Creek, WA, USA. Conserv Genet 16:301–315

    Article  CAS  Google Scholar 

  • Zimmerman CE, Reeves GH (2002) Identification of steelhead and resident rainbow trout progeny in the Deschutes River, Oregon, revealed with otolith microchemistry. Trans Am Fish Soc 131:986–993

    Article  Google Scholar 

  • Zimmerman CE, Rand PS, Fukushima M, Zolotukhin SF (2012) Migration of Sakhalin taimen (Parahucho perryi): evidence of freshwater resident life history types. Environ Biol Fish 93:223–232

    Article  Google Scholar 

Download references

Acknowledgements

We thank Hiroki Mizumoto and Yuki Shimamoto for assistance with water and fish sampling. Pete Rand and Naoki Murakami provided adult taimen samples. Marino Research Co., Ltd. prepared otolith samples for Sr isotopic analysis. We are grateful to Hirokazu Urabe, Koichi Osanai and the members of the Sarufutsu Sakhalin Taimen Conservation Group for providing logistical support. We also appreciate the information provided on various topics by the following individuals: Mitsugu Katayama on the Hokushin Dam and Reservoir, Yuji Seo on taimen habitats in the study area, and Toshiyuki Kawajiri on river works in the Koetoi Basin. Kotaro Shirai provided in-house calcium carbonate standards used for the MC-ICP-MS assays. Pete Rand, Kurt Fausch and two anonymous referees provided valuable comments that improved this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michio Fukushima.

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

Fukushima, M., Harada, C., Yamakawa, A. et al. Anadromy sustained in the artificially land-locked population of Sakhalin taimen in northern Japan. Environ Biol Fish 102, 1219–1230 (2019). https://doi.org/10.1007/s10641-019-00904-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-019-00904-4

Keywords

Navigation