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.
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References
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
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
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
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
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
Conover RJ (1956) Oceanography of Long Island Sound, 1952–1954, VI. Biology of Acartia clausi and A. tonsa. Bull Bingham Oceanogr Collect 15:156–233
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
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
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
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
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
Holling CS (1959b) Some characteristics of simple types of predation and parasitism. Can Entmol 91:385–398. https://doi.org/10.4039/Ent91385-7
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
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
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
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
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
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
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
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
Kos MS (1958) Some data on the coastal planktonic Copepoda from South-Kuril Bay. Dokl Akad Nauk SSSR 120:191–192
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
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
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
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
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
Mauchline J (1998) The biology of calanoid copepods. In: Blaxter JHS, Southward AJ, Tyler PA (eds) Adv Mar Biol. Academic Press, London
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
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
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
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
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
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
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
Onoue Y, Shimode S, Toda T, Kikuchi T (2006) Reproductive strategy of Acartia steueri in Sagami Bay, Japan. Coast Mar Sci 30(1):353–359
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
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
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
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
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
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
Smirnov S (1936) Beschreibung einer neuen Acartia-Art aus dem Japanischen Meer nebst einiger Bemerkungen uber die Untergattung Euacartia Steuer. Zool Anz 114:87–92
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
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
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
Turner JT (1984) The feeding ecology of some zooplankters that are important prey items of larval fish. NOAA Tech Rep NMFS 7:1–28
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
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 54:171–194
Uye S (1980) Development of neritic copepods Acartia clausi and A. steueri. Bull Plankton Soc Jpn 27(1):1–9
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
Warlen SM, Burke JS (1990) Immigration of larvae of fall/winter spawning marine fishes into a North Carolina estuary. Estuaries 13:453–461
White R, Roman MR (1992) Seasonal study of grazing by metazoan zooplankton in the mesohaline Chesapeake Bay. Mar Ecol Prog Ser 86:251–261
Yoo KI, Hue HK, Lee WC (1991) Taxonomical revision on the genus Acartia (Copepoda: Calanoida) in the Korean waters. Bull Korean Fish Soc 24:255–265
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.
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Natori, N., Toda, T. A multi-factor empirical model for calculation of naupliar ingestion rate of the embayment copepod Acartia steueri Smirnov (Copepoda: Calanoida). Mar Biol 165, 120 (2018). https://doi.org/10.1007/s00227-018-3378-z
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DOI: https://doi.org/10.1007/s00227-018-3378-z