Leonid SVETLICHNY, Elena HUBAREVA, Antonina KHANAYCHENKO, Alexandra GUBANOVA, Denis ALTUKHOV, ŞENGÜL BEŞİKTEPE

Adaptive Strategy of Thermophilic Oithona davisae in the Cold Black Sea Environment

Karadeniz'de yeni yayılmacı siklopoid tür olan Oithona davisae'nin yıl içindeki bolluk dinamikleri, cinsiyet kompozisyonu, mevsimlik üreme ve solunum oranları ile lokomotor aktiviteleri Sivastopol Körfezi'nde Ocak 2013'dan Temmuz 2014'e kadar incelenmiştir. Körfezdeki en yüksek bolluk deniz suyu sıcaklığının 15-23 oC olduğu Eylül-Kasım aylarındadır ve bolluk, sıcaklığın

Soğuk Karadeniz Ortamına Termofilik Oithona davisae'nin Uyum Stratejisi

Annual dynamics of abundance and gender composition, seasonal variations in reproduction, respiration rate and locomotor activity of the new invasive cyclopoid species Oithona davisae were investigated in Sevastopol Bay (Black Sea) from January 2013 till July 2014. The abundance of O. davisae in Sevastopol Bay was highest in September - November at 15 - 23 ºC and decreased dramatically in winter - spring period at a temperature equal or less than 8ºC. From the end of February (8 ºC) till the middle of May (17.5 ºC) the population of O. davisae was represented only by adult females. Copepodites were observed first only when the water temperature increased to 17.5 ºC, and males appeared only in late May at 22 ºC. The revealed seasonal trends in copepod abundance and reproduction from field and experimental data suggest that winter population of O. davisae survives the cold season in the Black Sea at the stage of fertilized females which give the birth to the next generation in favorable spring conditions. To save energy resources, overwintering females have significantly lower temperature-related weight-specific respiration rate and moving activity than females from summer population. Such unique adaptation strategy facilitated the invasion and successful development of this thermophilic species in the cold Black Sea environment.

PDF

___

Alekseev, V.R. and Starobogatov, Y.I. 1996. Types of diapause in the Crustacea: definitions, distribution, evolution. Hydrobiologia, 320, 15-26. doi: 10.1007/BF00016801.
Almeda, R., Alcaraz, M., Calbet, A. and Saiz, E. 2011. Metabolic rates and carbon budget of early developmental stages of the marine cyclopoid copepod Oithona davisae. Limnology and Oceanography, 56 (1), 403-414. doi: 10.4319/lo.2011.56.1.0403.
Almeda, R., Alcaraz, M., Calbet, A., Yebra, L. and Saiz E. 2010. Effect of temperature and food concentration on survival, development and growth rates of naupliar stages of Oithona davisae (Copepoda, Cyclopoida). Marine Ecology Progress Series, 410, 97-109. doi: 10.3354/meps08625.
Altukhov, D.A., Gubanova, A.D. and 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 (Suppl. 1), 28-34. doi: 10.1111/maec.12168.
Anninsky, B.E., Finenko, G.A., Datsyk, N.A. and Ignatyev, S.M. 2013. Gelatinous macroplankton in the Black Sea in the autumn of 2010. Oceanology, 53 (6), 676-685. doi: 10.1134/S0001437013060015.
Auel, H., Hagen, W., Ekau, W. and Verheye, H.M. 2005. Metabolic adaptations and reduced respiration of the copepod Calanoides carinatus during diapause at depth in the Angola-Benguela Front and northern Benguela upwelling regions. African Journal of Marine Science, 27 (3), 653-657. doi 10.2989/18142320509504125
Buskey, E.J. 1998. Energetic costs of swarming behavior for the copepod Dioithona oculata. Marine Biology, 130, 425-431. doi: 10.1007/s002270050263.
Castellani, C. and Altunbaş, Y. 2014. Seasonal change in acclimatized respiration rate of Temora longicornis. Marine Ecology Progress Series, 500, 83-101. doi:10.3354/meps10661.
Castellani, C., Robinson, C., Smith, T. and Lampitt, R.S. 2005. Temperature affects respiration rate of Oithona similis. Marine Ecology Progress Series, 285, 129-135. doi:10.3354/meps285129
Ceballos, S., Kiørboe, T. 2011. Senescence and sexual selection in a pelagic copepod. PLoS ONE, 6 (4), e18870. doi: 101371/journal.pone.0018870.
Cordell, J.R., Bollens, S.M., Draheim, R. and Sytsma M. 2008. Asian copepods on the move: recent invasions in the Columbia-Snake River system, USA. ICES Journal of Marine Science, 65, 753-758. doi: 10.1093/icesjms/fsm195.
Cornils, A. and Heckmann, B.-W. 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. doi: 10.1007/s10152-015-0426-7.
Ferrari, F. and 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. doi: 10.1163/1937240X84X00110.
Finenko, G.A., Abolmasova, G.I., Romanova, Z.A., Datsyk, N.A. and Anninskii, B.E. 2013. Population dynamics of the ctenophore Mnemiopsis leidyi and its impact on the zooplankton in the coastal regions of the Black Sea of the Crimean coast in 2004 - 2008. Oceanology 53, (1), 80 - 88. doi: 10.1134/S0001437012050074.
Gallienne, C.P. and Robins, D.B. 2001. Is Oithona the most important copepod in the world's oceans? Journal of Plankton Research, 23, 1421-1432. doi: 10.1093/plankt/23.12.1421.
Greze, V.N., Baldina, E.P. and Bileva, O.K. 1971. Dynamics of number and production of zooplankton basic components in neritic zone of the Black Sea. Biologiya Morya, 24, 12 - 49 (in Russian).
Gubanova, A.D. and Altukhov, D.A. 2007. Establishment of Oithona brevicornis Giesbrecht, 1892 (Copepoda: Cyclopoida) in the Black Sea. Aquatic Invasions, 2 (4), 407-410. doi: 10.3391/ai.2007.2.4.10. ·
Gubanova, A.D., Prusova, I.Yu., Niermann, U., Shadrin, N.V. and Polikarpov, I.G. 2001. Dramatic change in the copepod community in Sevastopol Bay (Black Sea) during two decades (1976-1996). Senckenbergiana maritima, 31 (1), 17-27. doi: 10.1007/BF03042833.
Heuschele, J. and Kiørboe, T. 2012. The smell of virgins. Mating status of females affects male swimming behaviour in Oithona davisae. Journal of Plankton Research, 34, 929- 935. doi: 10.1093/plankt/fbs054.
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. 1994. Further studies on respiration of the small planktonic copepod Oithona davisae with special reference to the effect of feeding. Bulletin of the College of Agriculture and Veterinary Medicine Nihon University (Japan), 51, 149-153.
Hiromi, J., Nagata, T. and Kadota, S. 1988. Respiration of the small planktonic copepod Oithona davisae at different temperatures. Bulletin of the Plankton Society of Japan, 35, 143-148.
Hubareva, E. and Svetlichny, L. 2013. Salinity and temperature tolerance of alien copepods Acartia tonsa and Oithona davisae in the Black Sea. Rapp. Comm. int. Mer Medit. 40, 742. doi: 10.13140/2.1.1145.3445.
Hubareva, E., Svetlichny, L., Kideys, A. and Isinibilir, M. 2008. Fate of the Black Sea Acartia clausi and A. tonsa (Copepoda) penetrating into the Marmara Sea through the Bosphorus. Estuarine, Coastal and Shelf Science, 76, 131- 140. doi: 10.1016/j.ecss.2007.06.009. ·
Ikeda, T., Kanno, Y., Ozaki, K. and Shinada, A. 2001. Metabolic rates of epipelagic marine copepods as a function of body mass and temperature. Marine Biology, 139, 587-596. doi: 10.1007/s002270100608.
Isinibilir, M., Svetlichny, L., Hubareva, E., Yilmaz, I.N., Ustun, F., Belmonte, G. and Toklu-Alicli, B. 2011. Adaptability and vulnerability of zooplankton species in the adjacent regions of the Black and Marmara Seas. Journal of Marine Systems, 84, 18-27. doi: 10.1016/j.jmarsys.2010.08.002.
Isinibilir, M., Kideys, A.E., Tarkan, A. and Yilmaz, N.I. 2008. Annual cycle of zooplankton abundance and species composition in Izmit Bay (the northeastern Marmara Sea). Estuarine, Coastal and Shelf Science, 78, 739-747. doi:10.1016/j.ecss.2008.02.013.
Islam, M. S., Hibino, M., Nakayama, K., and Tanaka, M. 2006. Condition of larval and early juvenile Japanese temperate bass Lateolabrax japonicus related to spatial distribution and feeding in the Chikugo estuarine nursery ground in the Ariake Bay, Japan. Journal of Sea Research, 55(2), 141- 155. doi: 10.1016/j.seares.2005.08.004.
Jewett, S.C. and Feder, H.M. 1977. Biology of the harpacticoid copepod, Harpacticus uniremis Kröyer on Dayville Flats, Port Valdez, Alaska. Ophelia, 16 (1), 111-129. doi: 10.1080/00785326.1977.10425464.
Jiang, H. and Kiørboe, T. 2011. The fluid dynamics of swimming by jumping in copepods. Journal of the Royal Society Interface, 8 (61), 1090-103. doi:10.1098/rsif.2010.0481
Kiørboe, T., Andersen, A., Langlois, V.J., Jakobsen, H.H. and Bohr, T. 2009. Mechanisms and feasibility of prey capture in ambush feeding zooplankton. Proceedings of the National Academy of Sciences of the United States of America, 106 (30), 12394-12399. doi: 10.1073/pnas.0903350106.
Kovalev, A.V., Bingel, F., Kideys, A.E., Niermann, U., Skryabin, V.A., Uysal, Z. and Zagorodynyaya, Yu.A. 1999. The Black Sea zooplankton: composition, spatial/temporal distribution and history of investigations. Turkish Journal of Zoology, 23, 195-209.
Krishnaswamy, S. 1959. Respiration in Chondracanyhus zei De La Roche (Copepoda). Journal of the Marine Biological Association of the United Kingdom, 38, 263-266.
Lampitt, R.S. and Gamble, J.C. 1982. Diet and respiration of the small planktonic marine copepod Oithona nana. Marine Biology, 66, 185-190. doi: 10.1007/BF00397192.
Lawrence, D. and Cordell, J. 2010. Relative contributions of domestic and foreign sourced ballast water to propagule pressure in Puget Sound, Washington, USA. Biological Conservation, 143, 700-709. doi:10.1016/j.biocon.2009.12.008.
Marcus, N.H. 1996. Ecological and evolutionary significance of resting eggs in marine copepods: past, present, and future studies. Hydrobiologia, 320, 141-152. doi: 10.1007/BF00016815. ·.
Mavrodieva, R. 2012. Mechanisms of interactions between phytoplankton and marine environmental factors (biotic and abiotic) in the Bulgarian Black Sea coastal waters (Sozopol Bay). PhD Thesis. Institute of Biodiveristy and Ecosystem Research (Bulgarian Academy of Science), Sofia, 193 pp.
Mihneva, V. and 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. doi: http://dx.doi.org/10.3391/bir.2013.2.2.04.
Næss, T. and Nilssen, J.P. 1991. Diapausing fertilized adults. Oecologia (Berlin) 86, 368-371. doi: 10.1007/BF00317602. Nakata, K. and Nakane, T. 1987. Respiration of plankton in the Mikawa Bay. Pollution Control, 22, 281-294.
Nesterova, D., Moncheva, S., Mikaelyan, A. et al., 2008. The state of phytoplankton. In: State of the environment of the Black Sea (2001-2006/7). Oguz T (ed). The Commission on the Protection of the Black Sea against Pollution publication, Istanbul. pp. 173-200.
Paffenhöfer, G.A. 1993. On the ecology of marine cyclopoid copepods (Crustacea, Copepoda). Journal of Plankton Research, 15, 37-55. doi: 10.1093/plankt/15.1.37.
Saiz, E., Calbet, A., Broglio, E. and Marı, P. 2003. Effects of small-scale turbulence on copepods: The case of Oithona davisae. Limnology and Oceanography, 48 (3), 1304-1311. doi: 10.4319/lo.2003.48.3.1304.
Selifonova, Zh.P. 2011. Oithona brevicornis Giesbrecht (Copepoda: Cyclopoida), invader into the Black Sea and in the Sea of Azov. Russian Journal of Biological Invasions, 2, 142-150 (in Russian). doi: 10.1134/S2075111711030131. ·
Shushkina, E., Nikolaeva, G. and Lukasheva, T. 1990. Changes in the structure of the plankton community in the Black Sea during the mass development of the ctenophore Mnemiopsis leidyi (Agassiz). Journal of General Biology, 51 (1), 54-60 (in Russian).
Smyly, W.J.P. 1970. Observations on rate of development, longevity and fecundity of Acanthocyclops viridis (Jurine) (Copepoda, Cyclopoida) in relation to type of prey. Crustaceana, 18 (1), 21-36. doi: 10.1163/156854070X00031.
Svetlichny, L. and Hubareva, E. 2014. Salinity tolerance of alien copepods Acartia tonsa and Oithona davisae in the Black Sea. Journal of Experimental Marine Biology and Ecology, 461, 201-208. doi: 10.1016/j.jembe.2014.08.012.
Svetlichny, L.S. and Umanskaya, A.V. (1991) Oxygen consumption cost and locomotion in Calanus helgolandicus (Crustacea, Copepoda). Oceanology, 31, 566-571 (in Russian).
Svetlichny, L.S., Hubareva, E.S. and Arashkevich, E.G. 1998.) Physiological and behavioural response to hypoxia in active and diapausing copepodites Stage V Calanus euxinus. Arch. Hydrobiol. Spec. Issues Advanc. Limnol., 52, 507- 519.
Svetlichny, L., Hubareva, E. and Khanaychenko, A. 2012a. Calanipeda aquae dulcis and Arctodiaptomus salinus: an exceptionally euryhaline osmoconformers as evident from mortality, oxygen consumption and mass density patterns. Marine Ecology Progress Series, 470, 15-29. doi: 10.3354/meps09907.
Svetlichny, L., Khanaychenko, A., Hubareva, E. and Aganesova, L. 2012b. Partitioning of respiratory energy and environmental tolerance in Calanipeda aquaedulcis and Arctodiaptomus salinus. Estuarine, Coastal and Shelf Science, 114, 199-207. doi: 10.1016/j.ecss.2012.07.023.
Svetlichny, L., Hubareva, E., Isinibilir, M., Kideys, A., Belmonte, G. and Giangrande, E. 2010. Salinity tolerance of Calanus euxinus in the Black and Marmara Seas. Marine Ecology Progress Series, 404, 127-138. doi:10.3354/meps08475.
Temnykh, A. and Nishida, Sh. 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, 425-431. doi: http://dx.doi.org/10.3391/ai.2012.7.3.013.
Tkach, A.V., Gordina, A.D., Niermann, U., Kideys, A.E. and Zaika, V.E. 1998. Changes in the larval nutrition of the Black Sea fishes with respect to plankton. In: Ivanov, L., Oguz, T. (eds) Ecosystem Modeling as a management tool for the Black Sea. Kluwer Academic Publishers, London. pp. 235-248.
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. 1979. Morphological observation of developmental stages in Oithona brevicornis (Copepoda, Cyclopoida). Bulletin of Plankton Society of Japan, 26 (2), 59-76.
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. doi: 10.3354/meps048093.
Uchima, M. and Hirano, R. 1988. Swimming behavior of the marine copepod Oithona davisae: internal control and search for environment. Marine Biology, 99, 47-56. doi: 10.1007/BF00644976.
Uye, S.-I. 1994. Replacement of large copepods by small ones with eutrophication of embayments: cause and consequence. Hydrobiologia, 292/293, 513-519. doi: 10.1007/BF00229979.
Uye, S.-I. and Sano, K. 1995.) Seasonal reproductive biology of the small cyclopoid copepod Oithona davisae in a temperate eutrophic inlet. Marine Ecology Progress Series, 118, 121-128. doi: 10.3354/meps118121.
Uye, S.-I. and 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. doi: 10.3354/meps163037.
Zagorodnyaya, Yu.?. 2002. Oithona brevicornis in the Sevastopol Bay: is it a single event or a new invader in the Black Sea fauna? Ecologiya Morya, 61, 43 (in Russian).
Zamora-Terol, S. and 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. doi: 10.4319/lo.2013.58.1.0376.