Stable isotope compositions of dominant zooplankton species in relation to environmental factors in the Dardanelles
Keywords:δ13C, δ15N, zooplankton, environmental variables, Dardanelles
- Stable isotopes in marine ecosystem are used to determine the food web and trophic interactions among marine species.
- Stable isotope studies on marine ecosystem are conducted on size-based groups of species. The present study was conducted on species abundant in the study area in the Dardanelles Strait. Although the stations were close to each other, the δ13C and δ15N signatures of the primary consumers varied.
- As this study was conducted at the species level, it differs from previous studies in the Mediterranean and the Aegean Sea. The results can provide an important reference for future work in the region.
Abstract: Samples were collected seasonally from three stations in the Dardanelles between April 2016 and October 2017 to determine the effects of biological and physicochemical properties of the coastal system on the isotopic compositions of the most abundant copepod species, Acartia clausi and Calanus helgolandicus, and a cladoceran, Penilia avirostris. Plankton samples were collected horizontally with a 200-µm-mesh plankton net and isotopic analyses were performed by mass spectrometry after identification to species level. Total zooplankton abundance reached its maximum in spring and summer. The δ13C values of copepods showed statistically significant differences both between stations and seasons. As a selective feeder, C. helgolandicus had the highest values in both δ13C and δ15N. Being a filter feeder, P. avirostris distinctly differed from C. helgolandicus and A. clausi. Enrichment was observed in δ15N values of copepods in winter, when the highest values of total suspended solids and chlorophyll-a were determined. The results showed that δ13C values of the copepods were under the influence of environmental and biological factors. Additionally, dietary differences between herbivorous groups and other groups were clearly demonstrated, as well as differences in the diets of filter-feeding and selectively-feeding zooplanktonic species.
Received: October 3, 2018; Revised: November 30, 2018; Accepted: December 18, 2018; Published online: December 27, 2018
How to cite this article: Uzundumlu S, Büyükateş Y. Stable isotope compositions of dominant zooplankton species in relation to environmental factors in the Dardanelles. Arch Biol Sci. 2019;71(1):177-85.
Saiz E, Calbet A, Atienza D, Alcaraz M. Feeding and production of zooplankton in the Catalan Sea (NW Mediterranean). Prog Oceanogr. 2007;74(2-3):313-28.
Espinasse B, Tiano M, Guilloux L. Patterns of variations in C and N stable isotope ratios in size-fractionated zooplankton in the Gulf of Lion, NW Mediterranean Sea. J Plankton Res. 2018;36(05):1204-15.
Darnaude AM, Salen-Picard C, Polunin NVC, Harmelin-Vivien ML. Trophodynamic linkage between river runoff and coastal fishery yield elucidated by stable isotope data in the Gulf of Lions (NW Mediterranean). Oecologia. 2004;138(3):325-32.
Bode A, Alvarez-Ossorio MT, Varela M. Phytoplankton and macrophyte contributions to littoral food webs in the Galician upwelling estimated from stable isotopes. Mar Ecol Prog Ser. 2006;318:89-102.
Hauss H, Franz JMS, Hansen T, Struck U, Sommer U. Relative inputs of upwelled and atmospheric nitrogen to the eastern tropical North Atlantic food web: Spatial distribution of δ15N in mesozooplankton and relation to dissolved nutrient dynamics. Deep Sea Res Part I Oceanogr Res. 2013;75:135-45.
Mompeán C, Bode A, Benítez-Barrios VM, Domínguez-Yanes JF, Escánez J, Fraile-Nuez E. Spatial patterns of plankton biomass and stable isotopes reflect the influence of the nitrogen-fixer Trichodesmium along the subtropical North Atlantic. J Plankton Res. 2013;35(3):513-25.
Tarling G A, Stowasser G, Ward P, Poulton AJ, Zhou M, Venables HJ, McGill RAR, Murphy EJ. Seasonal trophic structure of the Scotia Sea pelagic ecosystem considered through biomass spectra and stable isotope analysis. Deep Sea Res Part II Top Stud Oceanogr. 2012;59-60:222-36.
Décima M, Landry MR, Popp BN. Environmental perturbation effects on baseline δ15N values and zooplankton trophic flexibility in the southern California current ecosystem. Limnol Oceanogr. 2013;58(2):624-34.
Sano M, Maki K, Nishibe Y, Nagata T, Nishida S. Feeding habits of mesopelagic copepods in Sagami Bay: Insights from integrative analysis. Prog Oceanogr. 2013;110:11-26.
Fanelli E, Cartes JE, Papiol V. Food web structure of deep-sea macrozooplankton and micronekton off the Catalan slope: Insight from stable isotopes. J Mar Syst. 2011;87(1):79-89.
Minagawa M, Wada E. Stepwise enrichment of 15N along food chains: Further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta. 1984;48(5):1135-40.
Post D M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology. 2002;83(3):703-18.
DeNiro M J, Epstein S. Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta. 1978;42:495-506.
Fry B, Sherr E B. 13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contr Mar Sci. 1984;27:13-47.
Bănaru D, Carlotti F, Barani A, Grégori G, Neffati N, Harmelin-Vivien M. Seasonal variation of stable isotope ratios of size-fractionated zooplankton in the Bay of Marseille (NW Mediterranean Sea). J Plankton Res. 2014;36(1):145-56.
Vizzini S, Mazzola A. Sources and transfer of organic matter in food webs of a Mediterranean coastal environment: Evidence for spatial variability. Estuar Coast Shelf Sci. 2006;66(3-4):459-67.
Koppelmann R, Böttger-Schnack R, Möbius J, Weikert H. Trophic relationships of zooplankton in the eastern Mediterranean based on stable isotope measurements. J Plankton Res. 2009;31(6):669-86.
Sommer F, Sommer U. δ15N signatures of marine mesozooplankton and seston size fractions in Kiel Fjord, Baltic Sea. J Plankton Res. 2004;26(4):495-500.
Gunnerson CG, Ozturgut E. The Bosporus. In: Degens E, Ross D, editors. The Black Sea geology, chemistry, and biology. Oklahama: AAPG Memoir 20; 1974;99-114.
Latif M A, Özsoy E, Oguz T, Ünlüata Ü. Observations of the Mediterranean inflow into the Black Sea. Deep Sea Res A. 1991;38:711-23.
Besiktepe Ş T, Sur H I, Özsoy E, Abdul Latif M, Temel O, Ünlüata Ü. The circulation and hydrography of the Marmara Sea. Prog Oceanogr. 1994;34(4):285-334.
Tarkan AN, İşinibilir M, Tarkan AS. Seasonal variations of the zooplankton composition and abundance in the istanbul strait. Pak J Biol Sci. 2005;8(9):1327-36.
Ozturk B, Ozturk A A. On the biology of the Turkish straits system. Bull Inst Oceanogr. 1996;17:205-21.
Türkoğlu M, Yenici E, İşmen A, Kaya S. Çanakkale Boğazı ’nda Nütrient ve Klorofil-a Düzeylerinde Meydana Gelen Aylık Değişimler. Ege Üniversitesi Su Urunleri Dergisi. 2004;21(1-2):93-8.
Odabaşi S, Büyükateş Y. Klorofil-a, Çevresel parametreler ve besin elementlerinin günlük deǧişimleri: Sariçay akarsuyu örneǧi (Çanakkale, Türkiye). Ekoloji. 2009;19(73):76-85.
Buyukates Y, Inanmaz Ö̈ E. Cladocerans of an urbanized harbour: Effects of environmental parameters on vertical distribution, occurrence, abundance, and seasonal variation. Crustaceana. 2009;82(5):543-54.
Buyukates Y, Inanmaz Ö̈ E. The Annual Mesozooplankton Dynamics and Influence of Environmental Parameters in an Urbanized Harbor (Kepez Harbor-Dardanelles Strait, Turkey). Ekoloji. 2010;68:60-8.
Cihangir H., Papadopoulou M A. Spatial and temporal variation of soft-bottom peracarid (Crustacea: Peracarida) infauna in the Canakkale Strait (Turkey). Mediterr Mar Sci. 2011;12:153-82.
Turkoglu M, Oner C. Short Time Variations of Winter Phytoplankton, Nutrient and Chlorophyll a of Kepez Harbor in the Dardanelles (Çanakkale Strait, Turkey). Turk J Fish Aquat Sci. 2010;10(4):537-48.
Özdilek Ş Y, Jones R I. The Diet Composition and Trophic Position of Introduced Prussian Carp Carassius gibelio (Bloch, 1782) and Native Fish Species in a Turkish River. Turk J Fish Aquat Sci. 2014;14:713-26.
Tarkan A, Karakus U, Tepekoy EG, Top N, Ozdilek SY, Partal N, Britton JR. Trophic interactions of two Ponto-Caspian gobies in the Turkish part of their native range. Turk J Fish Aquat Sci. 2018;18:1279-86.
American Public Health Association (USA); American Water Works Association (USA); Water Environment Federation (USA). Standard methods for the examination of water and wastewater. Washington DC;. 1995.
Clesceri LS, Greenberg A E, Eaton A D. Standard methods for the examination of water and wastewater. 20th ed. Washington, DC: American Public Health Association; 1998. 1220 p.
Tregouboff G, Rose M. Manuel de planctonologie Mediterranéenne. Paris: Centre National de la Recherce Scientifique; 1957. 587 p.
Todd C, Laverack M S, Boxshall G A. Coastal marine zooplankton: a practical manual for students. Cambridge: Cambridge University Press; 2006. 106 p.
Bode A, Carrera P, Lens S. The pelagic foodweb in the upwelling ecosystem of Galicia (NW Spain) during spring: Natural abundance of stable carbon and nitrogen isotopes. ICES J Mar Sci. 2003;60(1):11-22.
Bunn S., Loneragan NR, Kempster MA. Effects of acid washing on stable isotope ratios of C and N in penaeid shrimp and seagrass: Implications for food-web studies using multiple stable isotopes. Limnol Oceanogr. 1995;40(3):622-5.
Jennings S, Reñones O, Morales-Nin B, Polunin N V C, Moranta J, Coll J. Spatial variation in the δ15N and δ13C stable isotope composition of plants, invertebrates and fishes on Mediterranean reefs: Implications for the study of trophic pathways. Mar Ecol Prog Ser. 1997;146(1-3):109-16.
Yang G, Li C, Guilini K, Wang X, Wang Y. Regional patterns of δ13C and δ15N stable isotopes of size-fractionated zooplankton in the western tropical North Pacific Ocean. Deep Sea Res Part I Oceanogr Res Pap. 2017;120(12):39-47.
Smyntek P M, Teece M A, Schulz K L, Thackeray S J. A standard protocol for stable isotope analysis of zooplankton in aquatic food web research using mass balance correction models. Limnol Oceanogr. 2007;52(5):2135-46.
Cass C J, Daly K L, Wakeham S G. Assessment of storage lipid accumulation patterns in eucalanoid copepods from the eastern tropical Pacific Ocean. Deep Sea Res Part I Oceanogr Res Pap. 2014;93:117-30.
Buyukates Y, Celikkol B, Yigit M, Decew J, Bulut M. Environmental Monitoring Around an Offshore Fish Farm with Copper Alloy Mesh Pens in the Northern Aegean Sea. Am J Environ Protect. 2017;6(2):50-61.
Matthews B, Mazumder A. Compositional and interlake variability of zooplankton affect baseline stable isotope signatures. Limnol Oceanogr. 2003;48(5):1977-87.
Buyukates Y, Inanmaz Ö̈ E. Temporal variations in vertical distribution and occurrence of marine cladocerans in an urbanized harbour, Dardanelles, Turkey. Crustaceana. 2007;80(11):1293-302.
Zervoudaki S, Christou E D, Assimakopoulou G, Örek H, Gucu A C, Giannakourou A, Pitta P, Terbiyik T, Yücel N, Moutsopoulos T, Pagou K, Psarra S, Özsoy E, Papathanassiou E. Copepod communities, production and grazing in the Turkish Straits System and the adjacent northern Aegean Sea during spring. J Mar Syst. 2011;86(3-4):45-56.
Fanelli E, Cartes J E, Rumolo P, Sprovieri M. Food-web structure and trophodynamics of mesopelagic-suprabenthic bathyal macrofauna of the Algerian Basin based on stable isotopes of carbon and nitrogen. Deep Sea Res Part I Oceanogr Res Pap. 2009;56(9):1504-20.
Mullin M M, Rau G H, Eppley R W. Stable nitrogen isotopes in zooplankton: some biographic and temporal variations in the North Pacific. Limnol Oceanogr. 1984;29(6):1267-73.
Fry B, Quinones R B. Biomass spectra and stable isotopes indicators of trophic level in zooplankton in the northwest Atlantic. Mar Ecol Prog Ser. 1994;112(1):201-4.
Bode A, Alvarez-Ossorio M T, Cunha M E, Garrido S, Peleteiro J B, Porteiro C, Valdes L, Varela M. Stable nitrogen isotope studies of the pelagic food web on the Atlantic shelf of the Iberian Peninsula. Prog Oceanogr. 2007;74(2-3):115-31.
Costalago D, Navarro J, Álvarez-Calleja I, Palomera I. Ontogenetic and seasonal changes in the feeding habits and trophic levels of two small pelagic fish species. Mar Ecol Prog Ser. 2012;460:169-81.
Meyer B, Irigoien X, Graeve M, Head R., Harris R. Feeding rates and selectivity among nauplii, copepodites and adult females of Calanus finmarchicus and Calanus helgolandicus. Helgol Mar Res. 2002;56(3):169-76.
Felpeto A B, Frangopulos M. Feeding strategies of the copepod Acartia clausi on single and mixed diets of toxic and non-toxic strains of the dinoflagellate Alexandrium minutum. Mar Ecol Prog Ser. 2006;316:115-25.
Calliari D, Tiselius P. Feeding and Reproduction in a Small Calanoid Copepod: Acartia Clausi Feeding and reproduction in a small calanoid copepod: Acartia clausi can compensate quality with quantity. Mar Ecol Prog Ser. 2014;298(05):241-50.
Turner JT, Tester PA, Ferguson RL. The marine cladoceran Pennilia arrostis and the microbial loop of pelagic food webs. Limnol Oceanogr. 1988;33(2):245-55.
Katechakis A, Stibor H, Sommer U, Hansen T. Feeding selectivities and food niche separation of Acartia clausi, Penilia avirostris (Crustacea) and Doliolum denticulatum (Thaliacea) in Blanes Bay (Catalan Sea, NW Mediterranean). J Plankton Res. 2004;26(6):589-603.
Atienza D, Calbet A, Saiz E, Alcaraz M, Trepat I. Trophic impact, metabolism, and biogeochemical role of the marine cladoceran Penilia avirostris and the co-dominant copepod Oithona nana in NW Mediterranean coastal waters. Mar Biol. 2006;150(2):221-35.
Paffenhöfer G A, Strıckland JDH. A note on the feeding of Calanus helgolandicus on detritus. Mar Biol. 1970;5:97-9.
How to Cite
Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.