Antonina KHANAYCHENKO, Vladimir MUKHANOV, Larisa AGANESOVA, Şengül BEŞİKTEPE, Nelly GAVRILOVA

Grazing and Feeding Selectivity of Oithona davisae in the Black Sea: Importance of Cryptophytes

Feeding of non-indigenous cyclopoid copepod Oithona davisae in natural coastal phytoplankton assemblages from theSevastopol Bay, the Black Sea, in late July and in late November 2013 and in artificial phytoplankton assemblage (mixture of5 cultured microalgae) have been studied in laboratory experiments using flow cytometry. Three distinct main clusters ofphytoplankton (2 μm < ESD < 20 μm) were identified in the natural water samples in both sampling period: photosyntheticpicoeukaryotes, nanophytoplankton and nanoplanktonic cryptomonads (NanoPE). Female O. davisae grazed on all 3phytoplankton groups but the highest ingestion rate in terms of carbon was on NanoPE with the value of 0.29±0.03 μg Cpreycop-1 d-1 in July. Low abundance of 3 phytoplankton groups in late November resulted in a very low but significant carboningestion on cryptophytes (0.008±0.002 μg Cprey cop-1 d-1) than on the other groups. Clearance rates and electivity indicesconfirmed positive selection only for cryptophytes from natural phytoplankton assemblages, and for cryptophyte strain IBSSCr54 and Tetraselmis suecica from artificial plurialgal mixture. Highest daily specific carbon-rations of O. davisae femaleswere found on cryptophytes (ESD 7 - 12 μm): up to 135% and 184% body carbon d-1 in late July and on artificial phytoplanktonassemblage, respectively.

PDF

___

Altukhov, D.A., Gubanova, A.D. & Mukhanov, V.S. (2014). New invasive copepod Oithona davisae Ferrari and Orsi, 1984: Seasonal dynamics in Sevastopol Bay and expansion along the Black Sea coasts. Marine Ecology, 35(1), 28-34. https://dx.doi.org/10.1111/maec.12168.

Altukhov, D., Siokou, I., Pantazi, M., Stefanova, K., Timofte, F., Gubanova, A., Nikishina, A. & Arashkevich, E. (2015). Intercomparison of five nets used for mesozooplankton sampling. Mediterranean Marine Science, 16(3), 550-561. https://dx.doi.org/10.12681/mms.1100.

Ambler, J. W., Cloern, J. E. & Hutchinson, A. (1985). Seasonal cycles of zooplankton from San Francisco Bay. Hydobiologia, 129, 177-197.

Andersen, R.A. (2005). Algae Culturing Technique. New York, Elsevier Academic Press., 578 pp.

Atkinson, A. (1995). Omnivory and feeding selectivity in five copepod species during spring in the Bellingshausen Sea, Antarctica. ICES Journal of MarineScience, 52 (3-4), 385-396. https://dx.doi.org/10.1016/1054-3139(95)80054-9.

Baytut, O. & Gonulol, A. (2016). Phytoplankton distribution and variation a long a freshwater-marine transition zone (Kızılırmak River) in the Black Sea. Oceanological and Hydrobiological Studies, 45,453- 465. https://dx.doi.org/10.1515/ohs-2016-0039.

Calbet, A., Vaqué, D., Felipe, J., Vila, M., Sala, M. M., Alcaraz, M. & Estrada, M. (2003).Relative grazing impact of microzooplankton and mesozooplankton on a bloom of the toxic dinoflagellate Alexandrium minutum. Marine Ecology Progress Series, 259, 303- 309.

Cheng, W., Akiba, T., Omura, T. & Tanaka, Y. (2014). On the foraging and feeding ability of Oithona davisae (Crustacea, Copepoda). Hydrobiologia, 741(1), 167- 176. https://dx.doi.org/10.1007/s10750-014-1867-8.

Choi, K.H, Kimmerer, W., Smith, G., Ruiz, G.M., & Lion, K. (2005). Post-exchange zooplankton in ballast water of ships entering the San Francisco Estuary. Journal of Plankton Research, 27, 707–714. https://dx.doi.org/10.1093/plankt/fbi044.

Cloern, J. E. & Dufford, R. (2005). Phytoplankton community ecology: principles applied in San Francisco Bay. Marine Ecology Progress Series, 285, 11-28.

Cornils, A. & Wend-Heckmann, B. (2015). First report of the planktonic copepod Oithona davisae in the northern Wadden Sea (North Sea): Evidence for recent invasion? Helgoland Marine Research, 69 (2), 243 - 248. https://dx.doi.org/10.1007/s10152-015-0426-7.

Cucci, T.L., Shumway, S.E., Brown W. S. & Newel, C.R. (1989). Using phytoplankton and flow cytometry to analyze grazing by marine organisms. Cytometry, 10, 659-669. https://dx.doi.org/10.1002/cyto.990100523.

Dahms, H.U., Tseng, L.C. & Hwang, J.S. (2015). Biogeographic distribution of the cyclopoid copepod genus Oithona - from mesoscales to global scales. Journal of Experimental Marine Biology and Ecology, 467, 26-32. https://dx.doi.org/10.1016/j.jembe.2015.02.009.

Doğan, G. & Isinibilir, M. (2016). First Report of a New Invasive Species Oithona davisae Ferrari and Orsi, 1984 (Copepoda: Cyclopoida) in the Sea of Marmara. Turkish Journal of Fisheries and Aquatic Sciences 16, 469-473. https://dx.doi.org/10.4194/1303-2712-v16_2_27.

Eker-Develi, E. Berthon, J.F., Canuti, E., Slabakova, N. Moncheva, S., Shtereva, G. & Dzhurova, B. (2012). Phytoplankton taxonomy based on CHEMTAX and microscopy in the northwestern Black Sea. Journal of Marine Systems, 94, 18-32. https://dx.doi.org/10.1016/j.jmarsys.2011.10.005.

Ferrari, F.D. & Orsi, J. (1984). Oithona davisae, new species, and Limnoithona sinensis (Burkckhard, 1912) (Copepoda: Oithonidae) from the Sacramento-San Joaquin Estuary, California. Journal of Crustacean Biology, 4(1), 106–126.

Frost, B.W. (1972). Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnology and Oceanography, 6, 805-815. https://dx.doi.org/10.4319/lo.1972.17.6.0805.

Gifford, D.J. (1993). Consumption of protozoa by copepods feeding on natural microplankton assemblages, in: Kemp, P.F., Sherr, B.F., Sherr, E.B. and Cole, J.J. (Eds.), Handbook of methods in aquatic microbial ecology (pp.723-729), Boca Raton, FL, Lewis Publication, 777 pp.

Gifford, S.M., Rollwagen-Bollens, G. & Bollens, S.M. (2007). Mesozooplankton omnivory in the upper San Francisco Estuary. Marine Ecology Progress Series, 348, 33-46. https://dx.doi.org/10.3354/meps07003.

Gubanova, A.D. & Altukhov, D.A. (2007). Establishment of Oithona brevicornis Giesbrecht, 1892 (Copepoda: Cyclopoida) in the Black Sea. Aquatic Invasions, 2, 407–410. https://dx.doi.org/10.3391/ai.2007.2.4.10.

Han, M.S. & Furuya, K. (2000). Size and species-specific primary productivity and community structure of phytoplankton in Tokyo Bay. Journal of Plankton Research, 22(7), 1221-1235. https://dx.doi.org/10.1093/plankt/22.7.1221.

Haq, S. (1965). The larval development of Oithona nana. Journal of Zoology,146, 555 - 566. Hirakawa, K. (1988). New records of the North Pacific coastal planktonic copepods, Acartia omorii (Acartiidae) and Oithona davisae (Oithonidae) from southern Chile. Bulletin of Marine Science, 42, 337- 339.

Hiromi, J. (1996). Potential impact of grazing by Oithona davisae (Copepoda: Cyclopoida) in Tokyo Bay, summer 1989. Bulletin of the College of Agriculture and Veterinary Medicine-Nihon University, 53, 47-55.

Hirota, R. (1990). Microdistribution of the marine copepod Oithona davisae in the shallow waters of Ariake-kai mudflats, Japan. Marine Biology, 105, 307 -312. https://dx.doi.org/10.1007/BF01344300.

Hwang, J.S., Kumar, R., Dahms, H.U., Tseng, L.C. & Chen, Q.C. (2007). Mesh size affects abundance estimates of Oithona spp. (Copepoda), Cyclopoida).Crustaceana, 80(7), 827-837. https://dx.doi.org/10.1163/156854007781363169.

Isinibilir, M., Svetlichny, L. & Hubareva, E. (2016). Competitive advantage of the invasive copepod Oithona davisae over the indigenous copepod Oithona nana in the Marmara Sea and Golden Horn Estuary. Marine Freshwater Behaviour and Physiology, 49 (6), 392-405. https://dx.doi.org/10.1080/10236244.2016.1236528.

Islam, M. S., Ueda, H., & Tanaka, M. (2005). Spatial distribution and trophic ecology of dominant copepods associated with turbidity maximum along the salinity gradient in a highly embayed estuarine system in Ariake Sea, Japan. Journal of Experimental Marine Biology and Ecology, 316(1), 101-115. https://dx.doi.org/10.1016/j.jembe.2004.11.001.

Kasyan, V.V. (2010). Holoplankton of ship ballast water in the Port of Vladivostok. Russian Journal of Marine Biology, 36(3), 167-175.

Khanaychenko, A., Aganesova, L., Mukhanov, V., Sakhon, E. & Rauen, T. (2016). Microalgae feeding selectivity of copepods from different ecological groups, in: Gayevskaya, A.V. (Ed.), Marine Biology Achievements and Perspectives, Proceedings of AllRussian Practical Conference 145th anniversary of Sevastopol Biological Station (Sevastopol, 19 -24 September 2016), Ekosi-Gidrofizika, Sevastopol, pp. 323 -326 (in Russian with English Summary).

Lampitt, R.S. & Gamble, J.C. (1982). Diet and respiration of the small planktonic marine copepod Oithona nana. Marine Biology, 66(2), 185-190. https://dx.doi.org/10.1007/BF00397192.

Lawrence, D.J. & Cordell, J.R. (2010). Relative contributions of domestic and foreign sourced ballast water to propagule pressure in Puget Sound, Washington, USA. Biological Conservation, 143 (3), 700-709. https://dx.doi.org/10.1016/j.biocon.2009.12.008.

Menden-Deuer, S. & Lessard, E.J. (2000). Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography, 45(3), 569-579. https://dx.doi.org/10.4319/lo.2000.45.3.0569.

Mihneva, V. & Stefanova, K. (2013). The non-native copepod Oithona davisae (Ferrari F.D. and Orsi, 1984) in the Western Black Sea: seasonal and annual abundance variability. BioInvasions Records, 2(2): 119–124. https://dx.doi.org/10.3391/bir.2013.2.2.04.

Moal, J., Martin-Jezequel, V., Harris, R. P., Samain, J. F. & Poulet, S. A. (1987). Interspecific and intraspecific variability of the chemical-composition of marinephytoplankton. Oceanologica acta, 10 (3), 339-346.

Montagnes, D.J., Berges, J.A., Harrison, P.J.& Taylor, F. (1994). Estimating carbon, nitrogen, protein, and chlorophyll a from volume in marine phytoplankton. Limnology and Oceanography, 39(5), 1044-1060. https://dx.doi.org/10.4319/lo.1994.39.5.1044.

Moshiri, G.A., Crumpton, W.G., Aumen, N.G., Allen, J.A., Blaylock, D.A. & Gaetz, C.T. (1978). Water-column and benthic invertebrate and plant associations as affected by the physico-chemical aspects in a mesotrophic bayou estuary, Pensacola, Florida. Gainesville: University of Florida, Water Resources Research Center Publ. 41:160 pp.

Nakamura, Y.& Hirata, A. (2006). Plankton community structure and trophic interactions in a shallow and eutrophic estuarine system, Ariake Sound, Japan. Aquatic Microbial Ecology, 44 (1), 45-57.

Nakamura, Y. & Turner, J.T. (1997). Predation and respiration by the small cyclopoid copepod Oithona similis: How important is feeding on ciliates and heterotrophic flagellates? Journal of Plankton Research, 19(9), 1275-1288. https://dx.doi.org/10.1093/plankt/19.9.1275.

Nejstgaard, J. C., Gismervik, I. & Solberg, P. T. (1997). Feeding and reproduction by Calanus finmarchicus, and microzooplankton grazing during mesocosm blooms of diatoms and the coccolithophore Emiliania huxleyi. Marine Ecology Progress Series, 147, 197- 217.

Nishida, S. (1985). Taxonomy and distribution of the family Oithonidae (Copepoda, Cyclopoida) in the Pacific and Indian Oceans. Bulletin of the Ocean Research Institute, University of Tokyo, 20, 1-167.

Olson, R.J., Zettler, E.R. & DuRand, M.D. (1993). Phytoplankton analysis using flow cytometry, in: Kemp, P.F., Sherr, B.F., Sherr, E.B., Cole, J.J. (Eds.), Handbook of methods in aquatic microbial ecology. Publishers, Boca Raton, FL, pp.175-186.

Paffenhöfer, G.A. (1993). On the ecology of marine cyclopoid copepods (Crustacea, Copepoda). Journal of Plankton Research, 15(1), 37-55. https://dx.doi.org/10.1093/plankt/15.1.37.

Saiz, E., Calbet, A., Broglio, E. & Mari, P. (2003). Effects of small-scale turbulence on copepods: The case of Oithona davisae. Limnology and Oceanography, 48(3), 1304–1311. https://dx.doi.org/10.4319/lo.2003.48.3.1304.

Saiz, E., Griffell, K., Calbet, A. & Isari, S. (2014). Feeding rates and prey: predator size ratios of the nauplii and adult females of the marine cyclopoid copepod Oithona davisae. Limnology and Oceanography, 59(6), 2077- 2088. https://dx.doi.org/10.4319/lo.2014.59.6.2077.

Svetlichny, L., Hubareva, E., Khanaychenko, A., Gubanova, A., Altukhov D.& Besiktepe S. (2016). Adaptive strategy of thermophilic Oithona davisae in the cold Black Sea environment. Turkish Journal of Fisheries and Aquatic Sciences, 16, 77-90. https://dx.doi.org/10.4194/1303-2712-v16_1_09.

Temnykh, A. & Nishida, S. (2012). New record of the planktonic copepod Oithona davisae Ferrari and Orsi in the Black Sea with notes on the identity of “Oithona brevicornis”. Aquatic Invasions, 7(3), 425-431. https://dx.doi.org/10.3391/ai.2012.7.3.013.

Timofte, F. & Tabarcea, C. (2012). Oithona brevicornis Giesbrecht, 1892 (Copepoda: Cyclopoida) - first record in the Romanian Black Sea waters. Journal of Environmental Protection and Ecology. 13 (3 A), 1683-1687.

Tsuda, A. & Nemoto, T. (1988). Feeding of copepods on natural suspended particles in Tokyo Bay. Journal of the Oceanographical Society of Japan, 44(5), 217- 227.

Turner, J.T. (2004). The importance of small planktonic copepods and their roles in pelagic marine food webs. Zoological Studies, 43(2), 255-266.

Uchima, M. (1988). Gut content analysis of neritic copepods Acartia omorii and Oithona davisae by a new method. Marine Ecology Progress Series, 48, 93–97.

Uchima, M. & Hirano, R. (1986). Food of Oithona davisae (Copepoda: Cyclopoida) and the effect of food concentration at first feeding on the larval growth. Bulletin of the Plankton Society of Japan, 33(1), 21– 28.

Üstün, F. & Terbıyık Kurt, T. (2016). First report of the occurrence of Oithona davisae Ferrari F.D. & Orsi, 1984 (Copepoda: Oithonidae) in the Southern Black Sea, Turkey. Turkish Journal of Fisheries and Aquatic Sciences,16, 413-420. https://dx.doi.org/ 10.4194/1303-2712-v16_2_21.

Uye, S.I. (1982). Length-weight relationships of important zooplankton from the Inland Sea of Japan. Journal of the Oceanographical Society of Japan, 38(3), 149- 158.

Uye, S. I. & Sano, K. (1998). Seasonal variations in biomass, growth rate and production rate of the small cyclopoid copepod Oithona davisae in a temperate eutrophic inlet. Marine Ecology Progress Series,163, 37-44.

Uye, S.I. & Sano, K. (1995). Seasonal reproductive biology of the small cyclopoid copepod Oithona davisae in a temperate eutrophic inlet. Marine Ecology Progress Series, 118(1), 121-128.

Vanderploeg, H.A., Scavia, D. (1979). Two electivity indices for feeding with special reference to zooplankton grazing. Journal of the Fisheries Research Board of Canada, 36(4), 362-365. https://dx.doi.org/10.1139/f79-055.

Verity, P.G., Robertson, C.Y., Tronzo, C.R., Andrews,M. G., Nelson, J.R. & Sieracki, M.E. (1992). Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnology and Oceanography, 37(7), 1434-1446. https://dx.doi.org/10.4319/lo.1992.37.7.1434.

Vogt, R.A., Ignoffo, T.R., Sullivan, L.J., Herndon, J., Stillman, J.H. & Kimmerer, W.J. (2013). Feeding capabilities and limitations in the nauplii of two pelagic estuarine copepods, Pseudodiaptomus marinus and Oithona davisae. Limnology and Oceanography,58(6), 2145-2157. https://dx.doi.org/10.4319/lo.2013.58.6.2145.

Yıldız, İ., Feyzioglu, A. M. & Besiktepe, S. (2016). First observation and seasonal dynamics of the new invasive planktonic copepod Oithona davisae Ferrari and Orsi, 1984 along the southern Black Sea (Anatolian Coast). Journal of Natural History, 1-13. https://dx.doi.org/10.1080/00222933.2016.1229060.

Zagorodnyaya, Yu. (2002). Oithona brevicornis in the Sevastopol Bay: is it a single event or a new invader in the Black Sea fauna? Morsk. Ekol. J. (Marine Ecological Journal in Russian). 61, 43.

Zamora-Terol, S. & Saiz, E. (2013). Effects of food concentration on egg production and feeding rates of the cyclopoid copepod Oithona davisae. Limnology and Oceanography, 58(1), 376-387. https://dx.doi.org/10.4319/lo.2013.58.1.0376