Skip to main content

Advertisement

SpringerLink
Log in

Effect of diurnal temperature difference on lipid accumulation and development in Calanus sinicus (Copepoda: Calanoida)

  • Biology
  • Published:
Chinese Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

Calanus sinicus, the dominant copepod in the Yellow Sea, develops a large oil sac in late spring to prepare for over-summering in the Yellow Sea Cold Water Mass (YSCWM). The lipid accumulation mechanism for the initiation of over-summering is unknown. Here, we cultured C3 copepodites at four constant temperatures (10, 13, 16, and 19°C) and at three temperature regimes that mimicked the temperature variations experienced during diurnal vertical migration (10–13°C, 10–16°C, and 10–19°C) for 18 days to explore the effects of temperature differences on copepod development and lipid accumulation. C. sinicus stored more lipid at low than at high temperatures. A diurnal temperature difference (10–16°C and 10–19°C) promoted greater lipid accumulation (1.9–2.1 times) than a constant temperature of either 16°C or 19°C, by reducing the energy cost at colder temperatures and lengthening copepodite development. Thereafter, the lipid reserve supported gonad development after final molting. Only one male developed in these experiments. This highly female-skewed sex ratio may have been the result of the monotonous microalgae diet fed to the copepodites. This study provides the first evidence that diurnal temperature differences may promote lipid accumulation in C. sinicus, and provides a foundation for future investigations into the mechanisms involved in over-summering in the YSCWM.

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

Similar content being viewed by others

References

  • Bergvik M, Leiknes Ø, Altin D, Dahl K R, Olsen Y. 2012. Dynamics of the lipid content and biomass of Calanus finmarchicus (copepodite V) in a Norwegian fjord. Lipids, 47(9): 881–895.

    Article  Google Scholar 

  • Campbell R W, Dower J F. 2003. Role of lipids in the maintenance of neutral buoyancy by zooplankton. Mar. Ecol. Prog. Ser., 263: 93–99.

    Article  Google Scholar 

  • Camus T, Zeng C S. 2010. Roles of microalgae on total egg production over female lifespan and egg incubation time, naupliar and copepodite survival, sex ratio and female life expectancy of the copepod Bestiolina similis. Aquacult. Res., 41(11): 1717–1726.

    Article  Google Scholar 

  • Camus T, Zeng C S. 2012. Reproductive performance, survival and development of nauplii and copepodites, sex ratio and adult life expectancy of the harpacticoid copepod, Euterpina acutifrons, fed different microalgal diets. Aquacult. Res., 43(8): 1159–1169.

    Article  Google Scholar 

  • Chen Q C. 1964. A study of the breeding periods, variation in sex ratio and in size of Calanus sinicus Brodsky. Oceanol. Limnol. Sin., 6(3): 272–288. (in Chinese with English abstract)

    Google Scholar 

  • Chess D W, Stanford J A. 1999. Experimental effects of temperature and prey assemblage on growth and lipid accumulation by Mysis relicta loven. Hydrobiologia, 412: 155–164.

    Article  Google Scholar 

  • Enright J T. 1977. Diurnal vertical migration: adaptive significance and timing. Part 1. Selective advantage: a metabolic model. Limnol. Oceanogr., 22(5): 856–872.

    Article  Google Scholar 

  • Escribano R, McLaren I A. 1992. Influence of food and temperature on lengths and weights of marine copepods. J. Exp. Mar. Biol. Ecol., 159(1): 77–88.

    Article  Google Scholar 

  • Falk-Petersen S, Mayzaud P, Kattner G, Sargent J R. 2009. Lipids and life strategy of Arctic Calanus. Mar. Biol. Res., 5(1): 18–39.

    Article  Google Scholar 

  • Fiksen Ø. 2000. The adaptive timing of diapause-a search for evolutionarily robust strategies in Calanus finmarchicus. ICES J. Mar. Sci., 57(6): 1825–1833.

    Article  Google Scholar 

  • Graeve M, Albers C, Kattner G. 2005. Assimilation and biosynthesis of lipids in Arctic Calanus species based on feeding experiments with a 13C labelled diatom. J. Exp. Mar. Biol. Ecol., 317(1): 109–125.

    Article  Google Scholar 

  • Gusmao L F M, Mckinnon A D. 2009. Sex ratios, intersexuality and sex change in copepods. J. Plankton Res., 31(9): 1101–1117.

    Article  Google Scholar 

  • Hagen W, Auel H. 2001. Seasonal adaptations and the role of lipids in oceanic zooplankton. Zool ogy, 104(3–4): 313–326.

    Article  Google Scholar 

  • Hagen W, Kattner G, Graeve M. 1993. Calanoides acutus and Calanus propinquus, Antarctic copepods with different lipid storage modes via wax esters or Triacylglycerols. Mar. Ecol. Prog. Ser., 97: 135–142.

    Article  Google Scholar 

  • Hakanson J L. 1984. The long and short term feeding condition in field-caught Calanus pacificus, as determined from the lipid content. Limnol. Oceanogr., 29(4): 794–804.

    Article  Google Scholar 

  • Hirche H J, Kattner G. 1993. Egg production and lipid content of Calanus glacialis in spring: indication of a fooddependent and food-independent reproductive mode. Mar. Biol., 117(4): 615–622.

    Article  Google Scholar 

  • Hirche H J. 1996. Diapause in the marine copepod, Calanus finmarchicus-a review. Ophelia, 44(1–3): 129–143.

    Article  Google Scholar 

  • Hirst A G, Bonnet D, Conway D V P, Kiørboe T. 2010. Does predation controls adult sex ratios and longevities in marine pelagic copepods? Limnol. Oceanogr., 55(5): 2193–2206.

    Google Scholar 

  • Hu D X, Wang Q Y. 2004. Interannual variability of the southern Yellow Sea Cold Water Mass. Chin. J. Oceanol. Limnol., 22(3): 231–236.

    Article  Google Scholar 

  • Huang C, Uye S, Onbé T. 1993. Ontogenetic diel vertical migration of the planktonic copepod Calanus sinicus in the Inland Sea of Japan. III. Early summer and overall seasonal pattern. Mar. Biol., 117(2): 289–299.

    Article  Google Scholar 

  • Huo Y Z, Wang S W, Sun S, Li C L, Liu M T. 2008. Feeding and egg production of the planktonic copepod Calanus sinicus in spring and autumn in the Yellow Sea, China. J. Plankton Res., 30(6): 723–734.

    Article  Google Scholar 

  • Hygum B H, Rey C, Hansen B W, Tande K. 2000. Importance of food quantity to structural growth rate and neutral lipid reserves accumulated in Calanus finmarchicus. Mar. Biol., 136(6): 1057–1073.

    Article  Google Scholar 

  • Ikeda T, Kanno Y, Ozaki K, Shinada A. 2001. Metabolic rates of epipelagic marine copepods as a function of body mass and temperature. Mar. Biol., 139(3): 587–596.

    Article  Google Scholar 

  • Irigoien X, Obermüller B, Head R N, Harris R P, Rey C, Hansen B W, Hygum B H, Heath M R, Durbin E G. 2000. The effect of food on the determination of sex ratio in Calanus spp.: evidence from experimental studies and field data. ICES J. Mar. Sci., 57(6): 1752–1763.

    Article  Google Scholar 

  • Irigoien X. 2004. Some ideas about the role of lipids in the life cycle of Calanus finmarchicus. J. Plankton Res., 26(3): 259–263.

    Article  Google Scholar 

  • Ji R B. 2011. Calanus finmarchicus diapause initiation: new view from traditional life history-based model. Mar. Ecol. Prog. Ser., 440: 105–114.

    Article  Google Scholar 

  • Johnson C L, Leising A W, Runge J A, Head E J H, Pepin P, Plourde S, Durbin E G. 2008. Characteristics of Calanus finmarchicus dormancy patterns in the Northwest Atlantic. ICES J. Mar. Sci., 65(3): 339–350.

    Article  Google Scholar 

  • Jónasdóttir S H. 1999. Lipid content of Calanus finmarchicus during overwintering in the Faroe-Shetland Channel. Fish. Oceanogr., 8(S1): 61–72.

    Article  Google Scholar 

  • Kattner G, Hagen W, Lee R F, Campbell R, Deibel D, Falk-Petersen S, Graeve M, Hansen B W, Hirche H J, Jónasdóttir S H, Madsen M L, Mayzaud P, Müller-Navarra D, Nichols P D, Paffenhöfer G A, Pond D, Saito H, Stübing D, Virtue P. 2007. Perspectives on marine zooplankton lipids. Can. J. Fish. Aquat. Sci., 64(11): 1628–1639.

    Article  Google Scholar 

  • Kattner G, Krause M. 1987. Changes in lipids during the development of Calanus finmarchicus s.l. from Copepodid I to adult. Mar. Biol., 96(4): 511–518.

    Article  Google Scholar 

  • Kiørboe T. 2006. Sex, sex-ratios, and the dynamics of pelagic copepod populations. Oecologia, 148(1): 40–50.

    Article  Google Scholar 

  • Lee R F, Hagen W, Kattner G. 2006. Lipid storage in marine zooplankton. Mar. Ecol. Prog. Ser., 307: 273–306.

    Article  Google Scholar 

  • Lee R F, Nevenzel J C, Paffenhöfer G A. 1972. The presence of wax esters in marine planktonic copepods. Naturwissenschaften, 59(9): 406–411.

    Article  Google Scholar 

  • Li C L, Sun S, Wang R, Wang X. 2004. Feeding and respiration rates of a planktonic copepod (Calanus sinicus) oversummering in Yellow Sea Cold Bottom Waters. Mar. Biol., 145(1): 149–157.

    Article  Google Scholar 

  • Li C L, Sun S, Wang R. 2007. An experimental study on grazing selectivity of Calanus sinicus to natural food particles. Oceanol. Limnol. Sin., 38(6): 529–535. (in Chinese with English abstract)

    Google Scholar 

  • Liu M T, Li C L, Sun S. 2011a. Identification of trophic relationships between marine algae and the copepod Calanus sinicus in a fatty acid approach. Acta Ecol. Sin., 31(4): 933–942. (in Chinese with English abstract)

    Google Scholar 

  • Liu M T, Li C L, Sun S. 2011b. Seasonal variation in fatty acid composition of seston and the copepod Calanus sinicus (Brodsky, 1962) in Jiaozhou Bay and its trophic implications. Chin. J. Oceanol. Limnol., 29(6): 1164–1173.

    Article  Google Scholar 

  • Madsen M L, Gaard E, Hansen B W. 2008. Wax-ester mobilization by female Calanus finmarchicus (Gunnerus) during spring ascendance and advection to the Faroe Shelf. ICES J. Mar. Sci., 65(7): 1112–1121.

    Article  Google Scholar 

  • Maps F, Plourde S, Zakardjian B. 2010. Control of dormancy by lipid metabolism in Calanus finmarchicus: a population model test. Mar. Ecol. Prog. Ser, 403: 165–180.

    Article  Google Scholar 

  • McAllister C D. 1970. Zooplankton rations, phytoplankton mortality, and the estimation of marine production. In: Steele J H ed. Marine Food Chains. University of California Press, Berkeley. p.419–457.

    Google Scholar 

  • McLaren I A. 1963. Effects of temperature on growth of zooplankton, and the adaptive value of vertical migration. J. Fish. Res. Board Can., 20(3): 685–727.

    Article  Google Scholar 

  • Miller C B, Crain J A, Morgan C A. 2000. Oil storage variability in Calanus finmarchicus. ICES J. Mar. Sci., 57(6): 1786–1799.

    Article  Google Scholar 

  • Miller C B, Morgan C A, Prahl F G, Sparrow M A. 1998. Storage lipids of the copepod Calanus finmarchicus from Georges Bank and the Gulf of Maine. Limnol. Oceanogr., 43(3): 488–497.

    Article  Google Scholar 

  • Niehoff B, Hirche H J. 2005. Reproduction of Calanus glacialis in the Lurefjord (western Norway): indication for temperature-induced female dormancy. Mar. Ecol. Prog. Ser., 285: 107–115.

    Article  Google Scholar 

  • Niehoff B, Madsen S, Hansen B, Nielsen T. 2002. Reproductive cycles of three dominant Calanus species in Disko Bay, West Greenland. Mar. Biol., 140(3): 567–576.

    Article  Google Scholar 

  • Niehoff B, Runge J A. 2003. A revised methodology for prediction of egg production of the marine planktonic copepod Calanus finmarchicus from preserved samples. J. Plankton Res., 25(12): 1581–1587.

    Article  Google Scholar 

  • Pepin P, Head E J H. 2009. Seasonal and depth-dependent variations in the size and lipid contents of stage 5 copepodites of Calanus finmarchicus in the waters of the Newfoundland Shelf and the Labrador Sea. Deep Sea Res., Part I, 56(6): 989–1002.

    Article  Google Scholar 

  • Pepin P, Parrish C C, Head E J H. 2011. Late autumn condition of Calanus finmarchicus in the northwestern Atlantic: evidence of size-dependent differential feeding. Mar. Ecol. Prog. Ser, 423: 155–166.

    Article  Google Scholar 

  • Pu X M, Sun S, Yang B, Zhang G T, Zhang F. 2004. Life history strategies of Calanus sinicus in the southern Yellow Sea in summer. J. Plankton Res., 26(9): 1059–1068.

    Article  Google Scholar 

  • Pu X M. 2003. Life strategy of Calanus sinicus in the southern Yellow Sea in summer. University of Chinese Academy of Sciences, Qingdao, China. (in Chinese with English abstract)

    Google Scholar 

  • Rey-Rassat C, Irigoien X, Harris R, Carlotti F. 2002. Energetic cost of gonad development in Calanus finmarchicus and C. helgolandicus. Mar. Ecol. Prog. Ser., 238: 301–306.

    Article  Google Scholar 

  • Sargent J R, Falk-Petersen S. 1988. The lipid biochemistry of calanoid copepods. In: Boxshall G, Schminke H K eds. Biology of Copepods. Netherlands: Springer. p.101–114.

    Chapter  Google Scholar 

  • Saumweber W J, Durbin E G. 2006. Estimating potential diapause duration in Calanus finmarchicus. Deep Sea Res., Part II, 53(23–24): 2597–2617.

    Article  Google Scholar 

  • Song S Q. 2010. Phytoplankton functional groups in the Yellow Sea and the East China Sea. University of Chinese Academy of Sciences, Qingdao, China. (in Chinese with English abstract)

    Google Scholar 

  • Sun J, Liu D Y, Qian S B. 1999. Study on phytoplankton biomass I. Phytoplankton measurement biomass from cell volume or plasma volume. Acta Oceanol. Sin., 21(2): 75–85. (in Chinese with English abstract)

    Google Scholar 

  • Sun S, Wang S W, Li C L. 2011. Preliminary study on the oil storage of Calanus sinicus fifth copepodites (C5) in the Yellow Sea. Oceanol. Limnol. Sin., 42(2): 165–169. (in Chinese with English abstract)

    Google Scholar 

  • Sun S, Zhang G. 2005. Over-summering strategy of Calanus sinicus. GLOBEC Int. Newsl., 11: 34.

    Google Scholar 

  • Svetlichny L S, Kideys A E, Hubareva E S, Besiktepe S, Isinibilir M. 2006. Development and lipid storage in Calanus euxinus from the Black and Marmara seas: variabilities due to habitat conditions. J. Mar. Syst., 59(1–2): 52–62.

    Article  Google Scholar 

  • Swalethorp R, Kjellerup S, Dünweber M, Nielsen T G, Moller E F, Rysgaard S, Hansen B W. 2011. Grazing, egg production, and biochemical evidence of differences in the life strategies of Calanus finmarchicus, C. glacialis and C. hyperboreus in Disko Bay, western Greenland. Mar. Ecol. Prog. Ser., 429: 125–144.

    Article  Google Scholar 

  • Tarrant A M, Baumgartner M F, Hansen B H, Altin D, Nordtug T, Olsen A J. 2014. Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus. Front. Zool., 11(1): 91–105.

    Article  Google Scholar 

  • Tarrant A M, Baumgartner M F, Verslycke T, Johnson C L. 2008. Differential gene expression in diapausing and active Calanus finmarchicus (Copepoda). Mar. Ecol. Prog. Ser., 355: 193–207.

    Article  Google Scholar 

  • Uye S, Huang C, Onbe T. 1990. Ontogenetic diel vertical migration of the planktonic copepod Calanus Sinicus in the Inland Sea of Japan. Mar. Biol., 104(3): 389–396.

    Article  Google Scholar 

  • Uye S. 1988. Temperature-dependent development and growth of Calanus sinicus (Copepoda: Calanoida) in the laboratory. Hydrobiologia, 167-168(1): 285–293.

    Article  Google Scholar 

  • Wang S W, Li C L, Sun S, Ning X R, Zhang W C. 2009. Spring and autumn reproduction of Calanus sinicus in the Yellow Sea. Mar. Ecol. Prog. Ser., 379: 123–133.

    Article  Google Scholar 

  • Wang S W. 2009. Reproduction, population recruitment and life history of Calanus sinicus in the Yellow Sea. University of Chinese Academy of Sciences, Qingdao, China. (in Chinese with English abstract)

    Google Scholar 

  • Wang Y Q, Li C L, Liu M T, Sun X X. 2014. Spatial distribution and lipid related energy-consumption strategies of Calanus sinicus in summer in the southern Yellow Sea and East China Sea. Acta Ecol. Sin., 34(16): 4632–4639. (in Chinese with English abstract)

    Google Scholar 

  • Wei Q S, Fu M Z, Li Y, Wang B D, Yu Z G. 2013. Observation of the seasonal evolution of DO, chlorophyll a maximum phenomena and nutrient accumulating in the southern Huanghai (Yellow) Sea Cold Water Mass area. Acta Oceanol. Sin., 35(4): 142–154. (in Chinese with English abstract)

    Google Scholar 

  • Zhang G T, Li C L, Sun S, Zhang H Y, Sun J, Ning X R. 2006. Feeding habits of Calanus sinicus (Crustacea: Copepoda) during spring and autumn in the Bohai Sea studied with the herbivore index. Sci. Mar., 70(3): 381–388.

    Article  Google Scholar 

  • Zhang G T, Sun S, Yang B. 2007. Summer reproduction of the planktonic copepod Calanus sinicus in the Yellow Sea: influences of high surface temperature and cold bottom water. J. Plankton Res., 29(2): 179–186.

    Article  Google Scholar 

  • Zhang W C, Wang R, Wang K. 2000. Effect of temperature on metabolic rates of Calanus sinicus. Mar. Sci., 24(2): 42–44. (in Chinese with English abstract)

    Google Scholar 

  • Zhou K L, Sun S, Wang M X, Wang S W, Li C L. 2016. Differences in the physiological processes of Calanus sinicus inside and outside the Yellow Sea Cold Water Mass. J. Plankton. Res., 38(3): 551–563.

    Article  Google Scholar 

Download references

Acknowledgement

We thank WANG Shiwei and LIU Mengtan for their guidance with the copepod classification. We thank LUO Xuan for help with microalgae cultivation. We are grateful to TANG Hongjun and FENG Song for assistance during sampling.

Author information

Authors and Affiliations

  1. Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Konglin Zhou  (周孔霖) & Song Sun  (孙松)

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Konglin Zhou  (周孔霖)

  3. Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, China

    Konglin Zhou  (周孔霖) & Song Sun  (孙松)

  4. Jiaozhou Bay Marine Ecosystem Research Station, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Song Sun  (孙松)

Authors
  1. Konglin Zhou  (周孔霖)
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Song Sun  (孙松)
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Song Sun  (孙松).

Additional information

Supported by the State Key Program of National Natural Science Foundation of China (No. 41230963), the Strategic Priority Research Program of Chinese Academy of Sciences (No. XDA11020305) and the NSFC-Shandong Joint Fund for Marine Ecology and Environmental Sciences (No. U1406403)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, K., Sun, S. Effect of diurnal temperature difference on lipid accumulation and development in Calanus sinicus (Copepoda: Calanoida). Chin. J. Ocean. Limnol. 35, 745–753 (2017). https://doi.org/10.1007/s00343-017-6039-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-017-6039-z

Keywords

Search

Navigation