Advertisement

Marine Biology

, 165:120 | Cite as

A multi-factor empirical model for calculation of naupliar ingestion rate of the embayment copepod Acartia steueri Smirnov (Copepoda: Calanoida)

  • Noriaki Natori
  • Tatsuki Toda
Original paper

Abstract

Mathematical approaches with multiple factors are essential for estimating in situ ingestion rates of copepod nauplii. The present study aimed to construct a multi-factor empirical model that could calculate naupliar carbon-specific ingestion rates using food concentrations and individual carbon weights. Laboratory feeding experiments were conducted to derive the functional response model and temperature quotient (Q10) of the naupliar stages of the embayment copepod Acartia steueri from NIII to NVI. Experiments were conducted with haptophyte Isochrysis galbana at different concentrations for all stages and at different temperatures for NV. Carbon-specific ingestion rates in relation to food concentration followed a type III functional response model at every developmental stage, with two constants of a maximum carbon-specific ingestion rate and a half-saturation food concentration. Each of the two constants varied and was significantly related to individual carbon weights, and two relational equations were obtained from the relationships. By substituting the equations into a type III functional response model, an empirical model was constructed. Carbon-specific ingestion rates of NV increased with increasing temperature and Q10 was determined to be 2.37. Estimated carbon-specific ingestion rates calculated using the empirical model and Q10 were significantly related to the measured carbon-specific ingestion rates. This trend was also confirmed in a dataset of ingestion rates of Oithona davisae nauplii quoted from a previous study. This suggests that the empirical model proposed here might be widely applicable for other species of copepod nauplii.

Notes

Acknowledgements

Many thanks to Prof. Tatsushi Matsuyama, Soka University, for his valuable comments on the mathematical model. We thank the referees for their constructive comments that allowed us to improve the article.

Funding

This research received no specific grant from any funding agency, commercial or non-profit sectors.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical statement

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

References

  1. Almeda R, Augustin C, Alcaraz M, Callbet A, Saiz E (2010) Feeding rates and gross growth efficiencies of larval developmental stages of Oithona davisae (Copepoda, Cyclopoida). J Exp Mar Biol Ecol 387:24–35.  https://doi.org/10.1016/j.jembe.2010.03.002 CrossRefGoogle Scholar
  2. Anraku M (1964) Influence of the Cape Cod Canal on the hydrography and on the copepods in Buzzards Bay and Cape Cod Bay, Massachusetts. II. Respiration and feeding. Limnol Oceanogr 9:195–206.  https://doi.org/10.4319/lo.1964.9.2.0195 CrossRefGoogle Scholar
  3. Ara K, Hiromi J (2009) Seasonal variability in plankton food web structure and trophodynamics in the neritic area of Sagami Bay, Japan. J Oceanogr 65:757–779.  https://doi.org/10.1007/s10872-009-0064-2 CrossRefGoogle Scholar
  4. Berggreen U, Hansen B, Kiørboe T (1988) Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production. Mar Biol 99:341–352.  https://doi.org/10.1007/BF02112126 CrossRefGoogle Scholar
  5. Böttjer D, Morales CE, Bathmann U (2010) Trophic role of small cyclopoid copepod nauplii in the microbial food web: a case study in the coastal upwelling system off central Chile. Mar Biol 157:689–705.  https://doi.org/10.1007/s00227-009-1353-4 CrossRefGoogle Scholar
  6. Conover RJ (1956) Oceanography of Long Island Sound, 1952–1954, VI. Biology of Acartia clausi and A. tonsa. Bull Bingham Oceanogr Collect 15:156–233Google Scholar
  7. Frost BW (1972) Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol Oceanogr 17:805–815.  https://doi.org/10.4319/lo.1972.17.6.0805 CrossRefGoogle Scholar
  8. Harris SA, Cyrus DP (1997) Composition, abundance and seasonality of fish larval fish in Richards Bay Harbour, KwaZulu-Natal, South Africa. S Afr J Mar Sci 23:56–78.  https://doi.org/10.1080/10183469.1997.9631388 CrossRefGoogle Scholar
  9. Helenius LK, Saiz E (2017) Feeding behaviour of the nauplii of the marine calanoid copepod Paracartia grani Sars: functional response, prey size spectrum, and effects of the presence of alternative prey. PLoS One 12(3):e0172902.  https://doi.org/10.1371/journal.pone.0172902 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Henriksen CI, Saiz E, Calbet A (2007) Feeding activity and swimming patterns of Acartia grani and Oithona davisae nauplii in the presence of motile and non-motile prey. Mar Ecol Prog Ser 331:119–129.  https://doi.org/10.3354/meps331119 CrossRefGoogle Scholar
  11. Holling CS (1959a) The components of predation as revealed by a study of small mammal predation of the European pine sawfly. Can Entmol 91:293–320.  https://doi.org/10.4039/Ent91293-5 CrossRefGoogle Scholar
  12. Holling CS (1959b) Some characteristics of simple types of predation and parasitism. Can Entmol 91:385–398.  https://doi.org/10.4039/Ent91385-7 CrossRefGoogle Scholar
  13. Holling CS (1965) The functional response of predators to prey density and its role in mimicry and population regulation. Mem Entomol Soc Can 45:5–60.  https://doi.org/10.4039/entm9745fv CrossRefGoogle Scholar
  14. Ikeda T (1977) Feeding rates of planktonic copepods from tropical sea. J Exp Mar Biol Ecol 29:263–277.  https://doi.org/10.1016/0022-0981(77)90070-3 CrossRefGoogle Scholar
  15. Irigoien X, Titelman J, Harris RP, Harbour D, Castellani C (2003) Feeding of Calanus finmarchicus nauplii in the Irminger Sea. Mar Ecol Prog Ser 262:193–200.  https://doi.org/10.3354/meps262193 CrossRefGoogle Scholar
  16. Ismar SMH, Hansen T, Sommer U (2008) Effect of food concentration and type of diet on Acartia survival and naupliar development. Mar Biol 154:335–343.  https://doi.org/10.1007/s00227-008-0928-9 CrossRefGoogle Scholar
  17. Ismar SMH, Kottmann JS, Sommer U (2018) First genetic quantification of sex- and stage-specific feeding in the ubiquitous copepod Acartia tonsa. Mar Biol.  https://doi.org/10.1007/s00227-017-3281-z CrossRefGoogle Scholar
  18. Kang HK, Kang YJ (2005) Production of Acartia steueri (Copepoda: Calanoida) in Ilkwang Bay, southeastern coast of Korea. J Oceanogr 61:237–334.  https://doi.org/10.1007/s10872-005-0043-1 CrossRefGoogle Scholar
  19. Kiørboe T, Sabatini M (1995) Scaling of fecundity, growth and development in marine planktonic copepods. Mar Ecol Prog Ser 120:285–298.  https://doi.org/10.3354/meps120285 CrossRefGoogle Scholar
  20. Kiørboe T, Mohlenberg F, Hamburger K (1985) Bioenergetics of the planktonic copepod Acartia tonsa: relation between feeding, egg production and respiration, and composition of specific dynamic action. Mar Ecol Prog Ser 26:85–97.  https://doi.org/10.3354/meps026085 CrossRefGoogle Scholar
  21. Kos MS (1958) Some data on the coastal planktonic Copepoda from South-Kuril Bay. Dokl Akad Nauk SSSR 120:191–192Google Scholar
  22. Köster M, Karause C, Paffenhöfer GA (2008) Time-series measurements of oxygen consumption of copepod nauplii. Mar Ecol Prog Ser 353:157–164.  https://doi.org/10.3354/meps07185 CrossRefGoogle Scholar
  23. Kurihara H, Shimode S, Shirayama Y (2004) Effects of raised CO2 concentration on the egg production rate and early development of two marine copepods (Acartia steueri and Acartia erythraea). Mar Pollut Bull 49:721–727.  https://doi.org/10.1016/j.marpolbul.2004.05.005 CrossRefPubMedGoogle Scholar
  24. Leandro SM, Tiselius P, Queiroga H (2006) Growth and development of nauplii and copepodites of the estuarine copepod Acartia tonsa from southern Europe (Ria de Aveiro, Portugal) under saturating food conditions. Mar Biol 150:123–129.  https://doi.org/10.1007/s00227-006-0336-y CrossRefGoogle Scholar
  25. Lonsdale DJ, Caron DA, Dennett MR, Schaffner R (2000) Predation by Oithona spp. on protozooplankton in the Ross Sea. Antarctica. Deep Sea Res Part II 47:3273–3283.  https://doi.org/10.1016/S0967-0645(00)00068-0 CrossRefGoogle Scholar
  26. López E, Anadòn R, Harris RP (2007) Functional responses of copepod nauplii using a high efficiency gut fluorescence technique. Mar Biol 150:893–903.  https://doi.org/10.1007/s00227-006-0387-0 CrossRefGoogle Scholar
  27. Mauchline J (1998) The biology of calanoid copepods. In: Blaxter JHS, Southward AJ, Tyler PA (eds) Adv Mar Biol. Academic Press, LondonGoogle Scholar
  28. McKinnon AD, Duggan S (2003) Summer copepod production in subtropical waters adjacent to Australia’s North West Cape. Mar Biol 143:897–907.  https://doi.org/10.1007/s00227-003-1153-1 CrossRefGoogle Scholar
  29. Meyer B, Irigoien X, Graeve M, Head RN, Harris RP (2002) Feeding rates and selectivity among nauplii, copepodites and adult females of Calanus finmarchicus and Calanus helgolandicus. Helgol Mar Res 56:169–176.  https://doi.org/10.1007/s10152-002-0105-3 CrossRefGoogle Scholar
  30. Mullin MM (1963) Some factors affecting the feeding of marine copepods of the genus Calanus. Limnol Oceanogr 8:239–250.  https://doi.org/10.4319/lo.1963.8.2.0239 CrossRefGoogle Scholar
  31. Natori N, Kuwata M, Suzuki T, Toda T (2017) A novel fracturing device to observe the gut contents of copepod nauplii using a scanning electron microscope. Limnol Oceanogr Methods 15:567–571.  https://doi.org/10.1002/lom3.10183 CrossRefGoogle Scholar
  32. Nishida S (1985) Pelagic copepods from Kabira Bay, Ishigaki Island, southwestern Japan, with the description of a new species of the genus Pseudodiaptomus. Publ Seto Mar Biol Lab 30(1–3):125–144.  https://doi.org/10.5134/176098 CrossRefGoogle Scholar
  33. O’Brien WJ (1988) The effect of container size on the feeding rate of Heterocope septentrionalis, a freshwater predaceous copepod. J Plankton Res 10:313–317.  https://doi.org/10.1093/plankt/10.2.313 CrossRefGoogle Scholar
  34. Okada N, Onoue Y, Othman BHR, Kikuchi T, Toda T (2009) Description of naupliar stages in Acartia steueri smirnov (Copepoda: Calanoida). J Crustacean Biol 29(1):70–78.  https://doi.org/10.1651/08-2982.1 CrossRefGoogle Scholar
  35. Onoue Y, Shimode S, Toda T, Kikuchi T (2006) Reproductive strategy of Acartia steueri in Sagami Bay, Japan. Coast Mar Sci 30(1):353–359Google Scholar
  36. Paffenhöfer GA (1971) Grazing and ingestion of nauplii, copepodids and adults of the marine planktonic copepod Calanus helgolandicus. Mar Biol 11:286–298.  https://doi.org/10.1007/BF00401275 CrossRefGoogle Scholar
  37. Paffenhöfer GA (1976) Feeding, growth, and food conversion of the marine planktonic copepod Calanus helgolandicus. Limnol Oceanogr 21(1):39–50.  https://doi.org/10.4319/lo.1976.21.1.0039 CrossRefGoogle Scholar
  38. Potter IC, Hyndes GA (1994) Composition of the fish fauna of a permanently open estuary on the southern coast of Australia, and comparisons with a nearby seasonally closed estuary. Mar Biol 121:199–209.  https://doi.org/10.1007/BF00346727 CrossRefGoogle Scholar
  39. Rey C, Harris R, Irigoien X, Head R, Carlotti F (2001) Influence of algal diet on growth and ingestion of Calanus helgolandicus nauplii. Mar Ecol Prog Ser 216:151–165.  https://doi.org/10.3354/meps216151 CrossRefGoogle Scholar
  40. Roff JC, Turner JT, Webber MK, Hopcroft RR (1995) Bacterivory by tropical copepod nauplii: extent and possible significance. Aquat Microb Ecol 9:165–175.  https://doi.org/10.3354/ame009165 CrossRefGoogle Scholar
  41. Saiz E, Calbet A (2007) Scaling of feeding in marine calanoid copepods. Limnol Oceanogr 52(2):668–675.  https://doi.org/10.4319/lo.2007.52.2.0668 CrossRefGoogle Scholar
  42. Smirnov S (1936) Beschreibung einer neuen Acartia-Art aus dem Japanischen Meer nebst einiger Bemerkungen uber die Untergattung Euacartia Steuer. Zool Anz 114:87–92Google Scholar
  43. Smith JK, Lonsdale DJ, Gobler CJ, Caron DA (2008) Feeding behavior and development of Acartia tonsa nauplii on the brown tide alga Aureococcus anophagefferens. J Plankton Res 30(8):937–950.  https://doi.org/10.1093/plankt/fbn050 CrossRefGoogle Scholar
  44. Stoecker DK, Egloff DA (1987) Predation by Acartia tonsa Dana on planktonic ciliates and rotifers. J Exp Mar Biol Ecol 110:53–68.  https://doi.org/10.1016/0022-0981(87)90066-9 CrossRefGoogle Scholar
  45. Tanaka M, Ueda H, Azeta M, Sudo H (1987) Significance of near-bottom copepod aggregations as food resources for the juvenile red sea bream in Shijiki Bay. Bull Jpn Soc Sci Fish 53(9):1545–1552.  https://doi.org/10.2331/suisan.53.1545 CrossRefGoogle Scholar
  46. Turner JT (1984) The feeding ecology of some zooplankters that are important prey items of larval fish. NOAA Tech Rep NMFS 7:1–28Google Scholar
  47. Turner JT, Tester PA (1992) Zooplankton feeding ecology: bacterivory by metazoan microzooplankton. J Exp Mar Biol Ecol 160:149–167.  https://doi.org/10.1016/0022-0981(92)90235-3 CrossRefGoogle Scholar
  48. Ueda H (1980) Zooplankton investigations in Shijiki Bay-I. Composition of zooplankton and distribution of copepods from April to August, 1975. Bull Seikai Reg Fish Res Lab 54:171–194Google Scholar
  49. Uye S (1980) Development of neritic copepods Acartia clausi and A. steueri. Bull Plankton Soc Jpn 27(1):1–9Google Scholar
  50. Uye S (1981) Fecundity studies of neritic calanoid copepods Acartia clausi Giesbrecht and A. steueri Smirnov: a simple empirical model of daily egg production. J Exp Mar Biol Ecol 50:255–271.  https://doi.org/10.1016/0022-0981(81)90053-8 CrossRefGoogle Scholar
  51. Warlen SM, Burke JS (1990) Immigration of larvae of fall/winter spawning marine fishes into a North Carolina estuary. Estuaries 13:453–461CrossRefGoogle Scholar
  52. White R, Roman MR (1992) Seasonal study of grazing by metazoan zooplankton in the mesohaline Chesapeake Bay. Mar Ecol Prog Ser 86:251–261CrossRefGoogle Scholar
  53. Yoo KI, Hue HK, Lee WC (1991) Taxonomical revision on the genus Acartia (Copepoda: Calanoida) in the Korean waters. Bull Korean Fish Soc 24:255–265Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Restoration Ecology, Graduate School of EngineeringSoka UniversityHachiojiJapan

Personalised recommendations