Marine Biology

, Volume 151, Issue 1, pp 257–269 | Cite as

Seasonal variations in the growth rates of euphausiids (Thysanoessa inermis, T. spinifera, and Euphausia pacifica) from the northern Gulf of Alaska

  • Alexei I. PinchukEmail author
  • Russell R. Hopcroft
Research Article


The euphausiids Thysanoessa inermis (Kroyer 1846), Thysanoessa spinifera (Holmes 1900), and Euphausia pacifica (Hansen 1911) are key pelagic grazers and also important prey for many commercial fish species in the Gulf of Alaska (GOA). To understand the role of the euphausiids in material flows in this ecosystem their growth rates were examined using the instantaneous growth rate (IGR) technique on the northern GOA shelf from March through October in 2001–2004. The highest mean molting increments (over 5% of uropod length increase per molt) were observed during the phytoplankton bloom on the inner shelf in late spring for coastal T. inermis, and on the outer shelf in summer for T. spinifera and more oceanic E. pacifica, suggesting tight coupling with food availability. The molting rates were higher in summer and lower in spring, for all species and were strongly influenced by temperature. Mean inter-molt periods calculated from the molting rates, ranged from 11 days at 5°C to 6 days at 8°C, and were in agreement with those measured directly during long-term laboratory incubations. Growth rate estimates depended on euphausiid size, and were close to 0 in early spring, reaching maximum values in May (0.123 mm day−1 or 0.023 day−1 for T. inermis) and July (0.091 mm day−1 or 0.031 day−1 for T. spinifera). The growth rates for E. pacifica remained below 0.07 mm day−1 (0.016 day−1) throughout the season. The relationship between T. inermis weight specific growth rate (adjusted to 5°C) and ambient chlorophyll-a concentration fit a Michaelis–Menten curve (r2 = 0.48) with food saturated growth rate of 0.032 day−1 with half saturation occurring at 1.65 mg chl-a m−3, but such relationships were not significant for T. spinifera or E. pacifica.


Growth Increment Spring Bloom Carapace Length Antarctic Krill Instantaneous Growth Rate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This research was conducted on the RV Alpha Helix with technical support from the captain, crew, and ship’s technicians. We thank all scientists who participated in the cruises for assistance in the field, and staff at the Seward Marine Center for providing a supportive work environment. Dr. A. J. Paul provided the data on euphausiid dry weights. We thank Dr. K. O. Coyle and Dr. E. A. Pakhomov for valuable discussions and comments on the manuscript. This is contribution number 317 of the US GLOBEC program, jointly funded by the National Science Foundation and the National Oceanic and Atmospheric Administration under NSF Grant OCE-0105236. The experiments comply with the current laws of the USA.


  1. Armstrong JL, Boldt JL, Cross AD, Moss JH, Davis ND, Myers KW, Walker RV, Beauchamp DA, Haldorson LJ (2005) Distribution, size, and interannual, seasonal and diel food habits of northern Gulf of Alaska juvenile pink salmon, Oncorhynchus gorbuscha. Deep-Sea Res II 52:247–265CrossRefGoogle Scholar
  2. Atkinson A, Shreeve RS, Hirst AG, Rothery P, Tarling GA, Pond DW, Korb RE, Murphy EJ, Watkins JL (2006) Natural growth rates in Antarctic krill (Euphausia superba): II. Predictive models based on food, temperature, body length, sex, and maturity stage. Limnol Oceanogr 51:973–987CrossRefGoogle Scholar
  3. Bargu S, Marinovic B, Mansergh S, Silver MW (2003) Feeding responses of krill to the toxin-producing diatom Pseudonitzschia. J Exp Mar Biol Ecol 284:87–104CrossRefGoogle Scholar
  4. Bollens SM, Frost BW, Lin TS (1992) Recruitment, growth, and diel vertical migration of Euphausia pacifica in a temperate fjord. Mar Biol 114:219–228CrossRefGoogle Scholar
  5. Brinton E (1976) Population biology of Euphausia pacifica off southern California. Fish Bull 74:733–762Google Scholar
  6. Buchholz F (1985) Moult and growth in euphausiids. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin, Heidelberg, pp 339–345CrossRefGoogle Scholar
  7. Buchholz F (1991) Moult cycle and growth of Antarctic krill Euphausia superba in the laboratory. Mar Ecol Prog Ser 69:217–229CrossRefGoogle Scholar
  8. Clarke A, Peck LS (1991) The physiology of polar marine zooplankton. Polar Res 10:355–369CrossRefGoogle Scholar
  9. Cooney RT (1971) Zooplankton and micronekton associated with a diffuse sound-scattering layer in Puget Sound, Washington. PhD Thesis, University of Washington, Seattle, WAGoogle Scholar
  10. Coyle KO, Pinchuk AI (2003) Annual cycle of zooplankton abundance, biomass and production on the northern Gulf of Alaska shelf, October 1997 through October 2000. Fish Oceanogr 12:327–338CrossRefGoogle Scholar
  11. Coyle KO, Pinchuk AI (2005) Seasonal cross-shelf distribution of major zooplankton taxa on the northern Gulf of Alaska shelf relative to water mass properties, species depth preferences and vertical migration behavior. Deep-Sea Res II 52:217–245CrossRefGoogle Scholar
  12. Dalpadado P, Ikeda T (1989) Some observations on moulting, growth and maturation of krill (Thysanoessa inermis) from the Barents Sea. J Plankton Res 11:133–139CrossRefGoogle Scholar
  13. Dilling L, Wilson J, Steinberg D, Alldredge A (1998) Feeding by the euphausiid Euphausia pacifica and the copepod Calanus marshallae on marine snow. Mar Ecol Prog Ser 170:189–201CrossRefGoogle Scholar
  14. Endo Y, Hanamura Y, Taniguchi A (1985) In situ observations on the surface swarm of Euphausia pacifica in Sendai Bay in early spring with special reference to their biological characteristics. La mer 23:135–140Google Scholar
  15. Falk-Petersen S, Gatten RR, Hopkins CCE, Sargent JR (1981) Ecological investigations on the zooplankton community of Balsfjorden, Northern Norway: seasonal changes in the lipid class composition of Meganyctiphanes norvegica (M. Sars), Thysanoessa raschii (M. Sars) and Thysanoessa inermis (Krøyer). J Exp Mar Biol Ecol 54:204–209CrossRefGoogle Scholar
  16. Falk-Petersen S, Hagen W, Kattner G, Clarke A, Sargent J (2000) Lipids, trophic relationships, and biodiversity in Arctic and Antarctic krill. Can J Fish Aquat Sci 57(Suppl 3):178–191CrossRefGoogle Scholar
  17. Fowler SW, Small LF, Keckes S (1971) Effects of temperature and size on molting of euphausiid crustaceans. Mar Biol 11:45–51CrossRefGoogle Scholar
  18. Gaudy R, Guerin J-P (1979) Comparative ecophysiology of the mysids Hemimysis speluncola Ledoyer (cave dwelling) and Leptomysis lingvura G. O. Sars (non-cave dwelling). Effect of temperature on growth and breeding. J Exp Mar Biol Ecol 38:101–119CrossRefGoogle Scholar
  19. Hanamura Y, Kotori M, Hamaoka S (1989) Daytime surface swarms of the euphausiid Thysanoessa inermis off the west coast of Hokkaido, northern Japan. Mar Biol 102:369–376CrossRefGoogle Scholar
  20. Hart JL (1973) Pacific fishes of Canada. Fish Res Board Can Bull 180:1–740Google Scholar
  21. Heath WA (1977) The ecology and harvesting of euphausiids in the Strait of Georgia. PhD Thesis, University of British Columbia, Vancouver, BCGoogle Scholar
  22. Hirst AG, Roff JC, Lampitt RS (2003) A synthesis of growth rates in marine epipelagic invertebrate zooplankton. Adv Mar Biol 44:1–142CrossRefPubMedGoogle Scholar
  23. Hopkins CCE, Tande KS, Grovnik S, Sargent JR (1984) Ecological investigation of the zooplankton community of Balsfjorden, northern Norway: an analysis of growth and overwintering tactics in relation to niche and environment in Metridia longa (Lubbock), Calanus finmarchicus (Gunnerus), Thysanoessa inermis (Kroyer) and T. raschii (M.Sars). J Exp Mar Biol Ecol 82:77–99CrossRefGoogle Scholar
  24. Hulsizer E (1971) A study of the reproductive cycle of Euphausia pacifica at two stations in Puget Sound, 1968-1969. MS Thesis, University of Washington, Seattle, WAGoogle Scholar
  25. Huntley M, Boyd C (1984) Food-limited growth of marine zooplankton. Am Nat 124:455–478CrossRefGoogle Scholar
  26. Iguchi N, Ikeda T (1994) Experimental study on brood size, egg hatchability and early development of a euphausiid Euphausia pacifica from Toyama Bay, southern Japan Sea. Bull Jpn Sea Natl Fish Res Inst 44:49–57Google Scholar
  27. Iguchi N, Ikeda T (1995) Growth, metabolism and growth efficiency of a euphausiid crustacean Euphausia pacifica in the southern Japan Sea, as influenced by temperature. J Plankton Res 17:1757–1769CrossRefGoogle Scholar
  28. Iguchi N, Ikeda T (1999) Production, metabolism and P:B ration of Euphausia pacifica (Crustacea: Euphausiacea) in Toyama Bay, southern Japan Sea. Plankton Biol Ecol 46:68–74Google Scholar
  29. Ikeda T (1990) A growth model for a hyperiid amphipod Themisto japonica (Bovallius) in the Japan Sea, based on its intermoult period and moult increment. J Oceanogr Soc Jpn 46:261–272CrossRefGoogle Scholar
  30. Ikeda T, Dixon P (1982) Observations on moulting in Antarctic krill (Euphausia superba Dana). Aust J Mar Freshw Res 33:71–76CrossRefGoogle Scholar
  31. Ikeda T, Thomas PG (1987) Moulting interval and growth of juvenile Antarctic krill (Euphausia superba) fed different concentrations of the diatom Phaeodactylum tricornutum in the laboratory. Polar Biol 7:339–343CrossRefGoogle Scholar
  32. Kawaguchi S, Candy SG, King R, Naganobu M, Nicol S (2006) Modelling growth of Antarctic krill. I. Growth trends with sex, length, season, and region. Mar Ecol Prog Ser 306:1–15CrossRefGoogle Scholar
  33. Kulka DW, Corey S (1982) Length and weight relationships of euphausiids and caloric values of Meganyctiphanes norvegica (M. Sars) in the Bay of Fundy. J Crust Biol 2:239–247CrossRefGoogle Scholar
  34. Landry MR, Monger BC, Selph KE (1993) Time-dependency of microzooplankton grazing and phytoplankton growth in the Subarctic Pacific. Prog Oceanogr 32:205–222CrossRefGoogle Scholar
  35. Lasker R (1966) Feeding, growth, respiration, and carbon utilization of a euphausiid crustacean. J Fish Res Board Can 23:1291–1317CrossRefGoogle Scholar
  36. Lindley JA, Williams R (1980) Plankton of the Fladen Ground during FLEX 76. II. Population dynamics and production of Thysanoessa inermis (Crustacea: Euphausiacea). Mar Biol 57:79–86CrossRefGoogle Scholar
  37. Liu H, Hopcroft RR (2006a) Growth and development of Neocalanus flemingeri/plumchrus in the northern Gulf of Alaska: validation of the artificial cohort method in cold waters. J Plankton Res 28:87–101CrossRefGoogle Scholar
  38. Liu H, Hopcroft RR (2006b) Growth and development of Metridia pacifica (Copepoda: Calanoida) in the northern Gulf of Alaska. J Plankton Res 28:769–781CrossRefGoogle Scholar
  39. Marinovic B, Mangel M (1999) Krill can shrink as an ecological adaptation to temporarily unfavourable environments. Ecol Lett 2:338–343Google Scholar
  40. Mauchline J (1980) The biology of mysids and euphausiids. Adv Mar Biol 18. Academic Press, London:1–680Google Scholar
  41. Miller DG (1983) Variation in body length measurement of Euphausia superba Dana. Polar Biol 2:17–20CrossRefGoogle Scholar
  42. Nakagawa Y, Endo Y, Taki K (2001) Diet of Euphausia pacifica Hansen in Sanriku waters off northeastern Japan. Plankton Biol Ecol 48:68–77Google Scholar
  43. Nakagawa Y, Ota T, Endo Y, Taki K, Sugisaki H (2004) Importance of ciliates as prey of the euphausiid Euphausia pacifica in the NW North Pacific. Mar Ecol Prog Ser 271:261–266CrossRefGoogle Scholar
  44. Nicol S (2000) Understanding krill growth and aging: the contribution of experimental studies. Can J Fish Aquat Sci 57(Suppl 3):168–177CrossRefGoogle Scholar
  45. Nicol S, Stolp M, Cochran T, Geijsel P, Marshall J (1992) Growth and shrinkage of Antarctic krill Euphausia superba from the Indian Ocean sector of the Southern Ocean during summer. Mar Ecol Prog Ser 89:175–181CrossRefGoogle Scholar
  46. Pinchuk AI, Hopcroft RR (2006) Egg production and early development of Thysanoessa inermis and Euphausia pacifica (Crustacea: Euphausiacea) in the northern Gulf of Alaska. J Exp Mar Biol Ecol 332:206–215CrossRefGoogle Scholar
  47. Ponomareva LA (1966) The euphausiids of the North Pacific, their distribution, ecology, and mass species. Israel Program for Scientific Translations, JerusalemGoogle Scholar
  48. Quetin LB, Ross RM, Frazer TK, Amsler MO, Wayatt-Evens C, Oakes SA (2003) Growth of larval krill, Euphausia superba, in fall and winter west of the Antarctic Peninsula. Mar Biol 143:833–843CrossRefGoogle Scholar
  49. Quetin LB, Ross RM, Clarke A (1994) Krill energetics: seasonal and environmental aspects of the physiology of Euphausia superba. In: El-Sayed S (ed) Southern Ocean ecology: the BIOMASS perspective. Cambridge University Press, Cambridge, pp 165–184Google Scholar
  50. Quetin LB, Ross RM (1991) Behavioral and physiological characteristics of the Antarctic krill, Euphausia superba. Am Zool 31:49–63CrossRefGoogle Scholar
  51. Roff JC, Hopcroft RR (1986) High precision microcomputer based measuring system for ecological research. Can J Fish Aquat Sci 43:2044–2048CrossRefGoogle Scholar
  52. Ross RM (1982) Energetics of Euphausia pacifica. II. Complete carbon and nitrogen budgets at 8 and 12 C throughout the life span. Mar Biol 68:15–23CrossRefGoogle Scholar
  53. Ross RM, Quetin LB, Baker KS, Vernet M, Smith RC (2000) Growth limitation in young Euphausia superba under field conditions. Limnol Oceanogr 45:31–43CrossRefGoogle Scholar
  54. Sameoto DD (1976) Respiration rates, energy budgets, and molting frequencies of three species of euphausiids found in the Gulf of St. Lawrence. J Fish Res Board Can 33:2568–2576CrossRefGoogle Scholar
  55. Shaw CT, Feinberg LR, Peterson WT (2004) Moulting and growth rates of two species of euphausiids off the Oregon coast: seasonal, spatial and life stage differences. In: Abstract Book, ASLO/TOS Ocean Research 2004 Conference, Honolulu, HI, 15–20 February 2004, p143Google Scholar
  56. Sigler MF, Rutecki TL, Courtney DL, Karinen JF, Yang M-S (2001) Young of the year sablefish abundance, growth, and diet in the Gulf of Alaska. Alaska Fish Res Bull 8:57–70Google Scholar
  57. Slater LM, Hopcroft RR (2005) Development, growth, and egg production of Centropages abdominalis in the subarctic Pacific. J Plankton Res 27:71–78CrossRefGoogle Scholar
  58. Smiles MC, Pearcy WG (1971) Size structure and growth rate of Euphausia pacifica off the Oregon coast. Fish Bull 69:79–86Google Scholar
  59. Smith SL (1991) Growth, development and distribution of the euphausiids Thysanoessa raschii (M. Sars) and Thysanoessa inermis (Kroyer) in the southeastern Bering Sea. In: Sakshaug E, Hopkins CCE, Oritsland NA (eds) Proceeding of the pro mare symposium on polar marine ecology, Trondheim, 12–16 May 1990. Polar Res 10:461–478Google Scholar
  60. Suh H-L, Choi S-D (1998) Comparative morphology of the feeding basket of five species of Euphausia (Crustacea, Euphausiacea) in the western North Pacific, with some ecological considerations. Hydrobiologia 385:107–112CrossRefGoogle Scholar
  61. Taki K, Ogishima T (1997) Distribution of some developmental stages and growth of Euphausia pacifica Hansen in the northwestern Pacific on the basis of Norpac Net Samples. Bull Tohoku Nat Fish Res Inst 59:95–117Google Scholar
  62. Tanasichuk RW (1998a) Interannual variations in the population biology and productivity of Euphausia pacifica in Barkley Sound, Canada, with special reference to the 1992 and 1993 warm ocean years. Mar Ecol Prog Ser 173:163–180CrossRefGoogle Scholar
  63. Tanasichuk RW (1998b) Interannual variations in the population biology and productivity of Thysanoessa spinifera in Barkley Sound, Canada, with special reference to the 1992 and 1993 warm ocean years. Mar Ecol Prog Ser 173:181–195CrossRefGoogle Scholar
  64. Tarling GA, Shreeve RS, Hirst AG, Atkinson A, Pond DW, Murphy EJ, Watkins JL (2006) Natural growth rates in Antarctic krill (Euphausia superba): I. Improving methodology and predicting intermolt period. Limnol Oceanogr 51:959–972CrossRefGoogle Scholar
  65. Timofeev SF (1996) Ontogenetic ecology of euphausiid crustaceans (Crustacea, Euphausiacea) of the northern seas (in Russian). Nauka, St. PetersburgGoogle Scholar
  66. Vidal J (1980) Physioecology of zooplankton. IV. Effects of phytoplankton concentration, temperature, and body size on the net production efficiency of Calanus pacificus. Mar Biol 56:203–211CrossRefGoogle Scholar
  67. Weingartner TJ, Coyle KO, Finney B, Hopcroft RR, Whitledge TE, Brodeur R, Dagg M, Farley E, Haidvogel D, Haldorson L, Hermann A, Hinckley S, Napp J, Stabeno P, Kline T, Lee C, Lessard E, Royer T, Strom S (2002) The Northeast Pacific GLOBEC program: coastal Gulf of Alaska. Oceanography 15:48–63CrossRefGoogle Scholar
  68. Wilson MT, Jump CM, Duffy-Anderson JT (2006) Comparative analysis of the feeding ecology of two pelagic forage fishes: capelin Mallotus villosus and walleye pollock Theragra chalcogramma. Mar Ecol Prog Ser 317:245–258CrossRefGoogle Scholar
  69. Winberg GG (1983) The Vant-Hoff’s coefficient and the Arrenius equation in biology. Zh (in Russian). Obshei Biologii 44:3–42Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Alaska SeaLife CenterUniversity of Alaska FairbanksSewardUSA
  2. 2.Institute of Marine ScienceUniversity of Alaska FairbanksFairbanksUSA

Personalised recommendations