Skip to main content
SpringerLink
Log in

Embryonic development and morphology of eggs and newly hatched larvae of Pacific herring Clupea pallasii

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

Abstract

The embryonic development and morphology of eggs and newly hatched larvae of the Pacific herring Clupea pallasii were described using laboratory-reared specimens originating from the Miyako Bay stock. The eggs were almost spherical in shape, 1.33–1.46 mm (mean: 1.38 mm) in diameter, and had a thick adherent chorion. They had a segmented pale yellow yolk, no oil globule, and a relatively wide perivitelline space. A subgerminal cavity was observed during the gastrula period, whereas the blastocoel did not appear. Mass hatching occurred by 271 h 45 min after fertilization, and the newly hatched larvae were 7.1–7.7 mm (mean: 7.5 mm) in total length with 53–56 myomeres at 9.6°C. The embryonic development of Pacific herring was substantially similar to that of zebrafish Danio rerio, American shad Alosa sapidissima, as well as Atlantic herring Clupea harengus, and generally followed the basic developmental pattern of teleosts. However, Pacific herring larvae hatched at a more developed stage than some other clupeoids, such as Japanese sardine Sardinops melanostictus, and the progressed developmental stage at hatching could be interpreted as an advanced adaptation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Hay DE (1985) Reproductive biology of Pacific herring (Clupea harengus pallasi). Can J Fish Aquat Sci 42:111–126

    Google Scholar 

  2. Hanamura N (1963) A study on the method of prediction of the Hokkaido spring herring resources (in Japanese with English abstract). Bull Hokkaido Reg Fish Res Lab 26:1–66

    Google Scholar 

  3. Kobayashi T (2002) History of herring fishery in Hokkaido and the review of population study (in Japanese with English abstract). Sci Rep Hokkaido Fish Exp Stn 62:1–8

    Google Scholar 

  4. Pearson WH, Elston RA, Bienert RW, Drum AS, Antrim LD (1999) Why did the Prince William Sound, Alaska, Pacific herring (Clupea pallasi) fisheries collapse in 1993 and 1994? Review of hypotheses. Can J Fish Aquat Sci 56:711–737

    Article  Google Scholar 

  5. Hershberger PK, Elder NE, Wittouck J, Stick K, Kocan RM (2005) Abnormalities in larvae from the once-largest Pacific herring population in Washington State result primarily from factors independent of spawning location. Trans Am Fish Soc 134:326–337

    Article  Google Scholar 

  6. Sweetnam D (2008) Review of some California fisheries for 2007: coastal pelagic finfish, market squid, dungeness crab, California spiny lobster, highly migratory species, ocean salmon, groundfish, California halibut, hagfish, Pacific herring, and recreational. CalCOFI Rep 49:15–38

    Google Scholar 

  7. National Association for the Promotion of Productive Seas (2010) Annual statistics of seed production and release in 2008 (in Japanese). National Association for the Promotion of Productive Seas, Tokyo

  8. Iizuka A (1966) Studies on the early life history of herring (Clupea pallasi C. et V.) in Akkeshi Bay and lake Akkeshi. Bull Hokkaido Reg Fish Res Lab 31:18–63

    Google Scholar 

  9. Chimura M, Watanabe Y, Okouchi H, Shirafuji N, Kawamura T (2009) Hatch-period-dependent early growth and survival of Pacific herring Clupea pallasii in Miyako Bay, Japan. J Fish Biol 74:604–620

    Article  CAS  PubMed  Google Scholar 

  10. Okouchi H, Chimura M (2001) Ecology and homing of artificially produced herring juveniles released in Miyako Bay (in Japanese). Kaiyo Monthly 33:252–258

    Google Scholar 

  11. Jones BC (1972) Effect of intertidal exposure on survival and embryonic development of Pacific herring spawn. J Fish Res Board Can 29:1119–1124

    Google Scholar 

  12. Griffin FJ, Pillai MC, Vines CA, Kaaria J, Hibbard-Robbins T, Yanagimachi R, Cherr GN (1998) Effects of salinity on sperm motility, fertilization, and development in the Pacific herring, Clupea pallasi. Biol Bull 194:25–35

    Article  Google Scholar 

  13. Kuwatani Y, Shibuya S, Wakui T, Nakanishi T (1978) Study on the egg development and breeding of the herring juvenile. I. Effect of temperature on the egg development (in Japanese). In: Sasaoka H (ed) Report on the development of enhancement techniques and market-feasibility research of herring. Hokkaido National Fisheries Research Institute and Research Department, Fisheries Agency of Japan, Kushiro, pp 11–29

  14. Ojaveer E (2006) On the external and parental effects in early development of herring (Clupea pallasi) at the NE Kamchatka. Fish Res 81:1–8

    Article  Google Scholar 

  15. Griffin FJ, Smith EH, Vines CA, Cherr GN (2009) Impacts of suspended sediments on fertilization, embryonic development, and early larval life stages of the Pacific herring, Clupea pallasi. Biol Bull 216:175–187

    PubMed  Google Scholar 

  16. Uchida K, Imai S, Mito S, Fujita S, Ueno M, Shojima Y, Senta T, Tahuku M, Dotu Y (1958) Studies on the egg, larvae and juvenile of Japanese fishes. Series I (in Japanese). Second Laboratory of Fisheries Biology, Fisheries Department, Faculty of Agriculture, Kyushu University, Fukuoka, Japan

  17. Kobayashi T (1993) Biochemical analyses of genetic variability and divergence of populations in Pacific herring (in Japanese). Bull Nat Res Inst Far Seas Fish 30:1–77

    Google Scholar 

  18. Takahashi Y, Hirokawa J, Kumagai A (1984) Studies on the methods of egg-taking and incubation of Pacific herring, Clupea pallasi. Suisanzoushoku 31:167–172

    Google Scholar 

  19. Purcell JE, Grosse D, Grover JJ (1990) Mass abundances of abnormal Pacific herring larvae at a spawning ground in British-Columbia. Trans Am Fish Soc 119:463–469

    Article  Google Scholar 

  20. Ojaveer E (1981) Influence of temperature, salinity, and reproductive mixing of Baltic herring groups on its embryonal development. Rapp P-v Réun Cons Int Explor Mer 178:409–415

    Google Scholar 

  21. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic-development of the zebrafish. Dev Dyn 203:253–310

    CAS  PubMed  Google Scholar 

  22. Hill J, Johnston IA (1997) Photomicrographic atlas of Atlantic herring embryonic development. J Fish Biol 51:960–977

    Article  Google Scholar 

  23. Shardo JD (1995) Comparative embryology of teleostean fishes. I. Development and staging of the American shad, Alosa sapidissima (Wilson, 1811). J Morphol 225:125–167

    Article  Google Scholar 

  24. Mabee PM, Olmstead KL, Cubbage CC (2000) An experimental study of intraspecific variation, developmental timing, and heterochrony in fishes. Evolution 54:2091–2106

    CAS  PubMed  Google Scholar 

  25. Johnston IA (1993) Temperature influences muscle differentiation and the relative timing of organogenesis in herring (Clupea harengus) larvae. Mar Biol 116:363–379

    Article  Google Scholar 

  26. Beacham TD, Schweigert JF, MacConnachie C, Le KD, Flostrand L (2008) Use of microsatellites to determine population structure and migration of Pacific herring in British Columbia and adjacent regions. Trans Am Fish Sci 137:1795–1811

    Article  Google Scholar 

  27. Sugaya T, Sato M, Yokoyama E, Nemoto Y, Fujita T, Okouchi H, Hamasaki K, Kitada S (2008) Population genetic structure and variability of Pacific herring Clupea pallasii in the stocking area along the Pacific coast of northern Japan. Fish Sci 74:579–588

    Article  CAS  Google Scholar 

  28. Martin KL, Moravek CL, Flannery JA (2009) Embryonic staging series for the beach spawning, terrestrially incubating California grunion Leuresthes tenuis with comparisons to other Atherinomorpha. J Fish Biol 75:17–38

    Article  CAS  PubMed  Google Scholar 

  29. Mito S (1979) Fish egg (in Japanese). Mar Sci Mon 11:126–130

    Google Scholar 

  30. McGowan MF, Berry FH (1984) Clupeiformes: development and relationships. In: Moser HG, Richards WJ, Cohen DM, Fahay MP, Kendall AW, Richardson SL (eds) Ontogeny and systematics of fishes. Allen, Lawrence, pp 108–126

  31. Jones PW, Martin FD, Hardy JD (1978) Development of fishes in the Mid-Atlantic Bight: an atlas of egg, larval, and juvenile stages, vol. 1: Acipenseridae through Ictaluridae. Fish and Wildlife Service, US Department of the Interior, Fort Collins

  32. Takita T (1966) Egg development and larval stages of the small clupeoid fish, Harengula zunasi Bleeker and some informations about the spawning and nursery in Ariake Sound (in Japanese with English abstract). Bull Fac Fish Nagasaki Univ 21:171–179

    Google Scholar 

  33. Long WL, Ballard WW (2001) Normal embryonic stages of the longnose gar, Lepisosteus osseus. BMC Dev Biol 1:6

    Google Scholar 

  34. Ballard WW (1986) Stages and rates of normal development in the holostean fish, Amia calva. J Expl Zool 238:337–354

    Article  Google Scholar 

  35. Price JW (1934) The embryology of the whitefish, Coregonus clupeaformis (Mitchill) part I. Early embryology. Ohio J Sci 34:287–305

    Google Scholar 

  36. Swarup H (1958) Stages in the development of the stickleback Gasterosteus aculeatus (L.). J Embryol Exp Morphol 6:373–383

    CAS  PubMed  Google Scholar 

  37. Yamamoto K, Yamauchi K, Kasuga S (1975) On the development of the Japanese eel, Anguilla japonica (in Japanese with English abstract). Bull Jpn Soc Sci Fish 41:21–28

  38. Finch E, Cruz C, Sloman KA, Kudoh T (2010) Heterochrony in the germ ring closure and tail bud formation in embryonic development of rainbow trout (Oncorhynchus mykiss). J Exp Zool (Mol Dev Evol) 314B:187–195

    Google Scholar 

  39. Arezo MJ, Pereiro L, Berois N (2005) Early development in the annual fish Cynolebias viarius. J Fish Biol 66:1357–1370

    Article  Google Scholar 

  40. Collazo A, Bolker JA, Keller R (1994) A phylogenetic perspective on teleost gastrulation. Am Nat 144:133–152

    Article  Google Scholar 

Download references

Acknowledgments

We are sincerely grateful to the members of the Miyako Station, National Center for Stock Enhancement (the former Japan Sea Farming Association) of the Fisheries Research Agency, for helping with the rearing experiments and providing valuable information. Thanks are also due to Y. Nagakura of the Miyako Station, National Center for Stock Enhancement, for providing salinity data in Miyako Bay. We also thank M. J. Miller for assistance with this manuscript. This study was partly supported by a grant-in-aid for creative scientific research, no. 12NP0201 (DOBIS), from the Ministry of Education, Science and Culture of Japan. T.K. was supported by Research Fellowships from the Japan Society for the Promotion of Science for Young Scientists. K.T. was partly supported by the Research Foundation from Toyo Suisan and the Eel Research Foundation Nobori-kai.

Author information

Author notes

  1. Hiroyuki Okouchi

    Present address: Head Office of Fisheries Research Agency, Yokohama, Kanagawa, 220-6115, Japan

Authors and Affiliations

  1. Atmosphere and Ocean Research Institute, University of Tokyo, Kashiwa, Chiba, 277-8564, Japan

    Tatsuya Kawakami, Jun Aoyama & Katsumi Tsukamoto

  2. Miyako Station, National Center for Stock Enhancement, Fisheries Research Agency, Miyako, Iwate, 027-0097, Japan

    Hiroyuki Okouchi & Masato Aritaki

  3. Seikai National Fisheries Research Institute, Nagasaki, Nagasaki, 851-2213, Japan

    Masato Aritaki

Authors
  1. Tatsuya Kawakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroyuki Okouchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masato Aritaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jun Aoyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katsumi Tsukamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tatsuya Kawakami.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kawakami, T., Okouchi, H., Aritaki, M. et al. Embryonic development and morphology of eggs and newly hatched larvae of Pacific herring Clupea pallasii . Fish Sci 77, 183–190 (2011). https://doi.org/10.1007/s12562-010-0317-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-010-0317-4

Keywords

Search

Navigation