Abstract
Estuaries are one of the most productive regions in ecosystems and serve as important nursery and recruitment habitats for various living resources. However, information on the trophic dynamics of estuarine copepods along the salinity gradient is not well known. Here, we investigated resource partitioning among three copepods, Pseudodiaptomus japonicus, Sinocalanus tenellus, and Tortanus dextrilobatus in the Seomjin River estuary of the Korea using stable carbon and nitrogen isotope analyses. Among the three copepods, S. tenellus showed the lowest δ13C values, while the highest δ13C values were observed in T. dextrilobatus. Stable Isotope Analysis in R (SIAR) showed that S. tenellus fed mainly on terrestrial particulate organic matter (POM), while the contribution of marine POM was relatively high in the diet of T. dextilobatus. In contrast, P. japonicus showed relatively high trophic flexibility between terrestrial and marine POM. Thus, the Stable Isotope Bayesian Ellipses in R (SIBER) showed no dietary niche overlap among the three copepods. Therefore, we suggest that the coexistence of S. tenellus, P. japonicus, and T. dextrilobatus in the Seomjin River estuary can be closely associated with species-specific differences in resource utilization along the salinity gradient.
References
Ambler JW, Frost BW (1974) The feeding behaviour of a predatory planktonic copepod, Tortanus discaudatus. Limnol Oceanogr 19:446–451. https://doi.org/10.4319/lo.1974.19.3.0446
Bodin N, Le Loc F, Hily C (2007) Effect of lipid removal on carbon and nitrogen stable isotope ratios in crustacean tissues. J Exp Mar Biol Ecol 341:168–175. https://doi.org/10.1016/j.jembe.2006.09.008
Conover WJ (1999) Practical nonparametric Statistics, 3rd edn. John Wiley and Sons, New York
Conway DVP (2006) Identification of the copepodite developmental stages of twenty-six North Atlantic copepods. Mar Biol Assoc UK 21:1–28
Dauvin JC (2008) Effects of heavy metal contamination on the macrobenthic fauna in estuaries: the case of the Seine estuary. Mar Pollut Bull 57:160–169. https://doi.org/10.1016/j.marpolbul.2007.10.012
David V, Sautour B, Galois R (2006) The paradox high zooplankton biomass-low vegetal particulate organic matter in high turbidity zones: what way for energy transfer? J Exp Biol Ecol 333:202–218. https://doi.org/10.1016/j.jembe.2005.12.045
Fry B, Sherr EB (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci 27:13–47
Greenwood JG (1981) Occurrences of congeneric pairs of Acartia and Pseudodiaptomus species (Copepoda, Calanoida) in Moreton Bay, Queensland. Estuar Coast Shelf Sci 13:591–596. https://doi.org/10.1016/S0302-3524(81)80060-6
Hada A, Uye S (2000) Cannibalistic feeding behavior of the brackish-water copepod Sinocalanus tenellus. J Plankton Res 13:155–166. https://doi.org/10.1093/plankt/13.1.155
Heinle DR, Flemer DA (1975) Carbon requirements of a population of the estuarine copepod Eurytemora affinis. Mar Biol 31:235–247. https://doi.org/10.1007/BF00387152
Ho TW, Hwang JS, Cheung MK, Kwan HS, Wong CK (2017) DNA-based study of the diet of the marine calanoid copepod Calanus sinicus. Ecology 494:1–9. https://doi.org/10.1016/j.jembe.2017.04.004
Hooff RC, Bollens SM (2004) Functional response and potential predatory impact of Tortanus dextrilobatus, a carnivorous copepod recently introduced to the San Francisco Estuary. Mar Ecol-Prog Ser 277:167–179. https://doi.org/10.3354/meps277167
Hutchinson GE (1961) The paradox of the plankton. Am Nat 92:137–145
Im DH, Suh HL (2016) Ontogenetic feeding migration of the euphausiid Euphausia pacifica in the East Sea (Japan Sea) in autumn: a stable isotope approach. J Plankton Res 38:901–914. https://doi.org/10.1093/plankt/fbw041
Im DH, Suh HL (2019) Evidence for resource partitioning by ontogeny and species in calanoid copepods. Prog Oceanogr 176:102111. https://doi.org/10.1016/j.pocean.2019.05.003
Im DH, Wi JH, Suh HL (2015) Evidence for ontogenetic feeding strategies in four calanoid copepods in the East Sea (Japan Sea) in summer, revealed by stable isotope analysis. Ocean Sci J 50:481–490. https://doi.org/10.1007/s12601-015-0044-y
Isari S, Antó M, Saiz E (2013) Copepod foraging on the basis of food nutritional quality: can copepods really choose? PLoS ONE 8:e8742. https://doi.org/10.1371/journal.pone.0084742
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER–Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
Jerling HL, Wooldridge TH (1991) Population dynamics and estimates of production for the calanoid copepod Pseudodiaptomus hessei in a warm temperate estuary. Estuar Coast Shelf Sci 33:121–135. https://doi.org/10.1016/0272-7714(91)90002-S
Kimmerer WJ, Burau JR, Bennett WA (1998) Tidally oriented vertical migration and position maintenance of zooplankton in a temperate estuary. Limnol Oceanogr 43:1697–1709. https://doi.org/10.4319/lo.1998.43.7.1697
Kleppel GS (1993) On the diets of calanoid copepods. Mar Ecol-Prog Ser 99:183–195
Kobari T, Moku M, Takahashi K (2008) Seasonal appearance of expatriated boreal copepods in the Oyashio-Kuroshio mixed region. ICES J Mar Sci 65:469–476. https://doi.org/10.1093/icesjms/fsm194
Laprise R, Dodson JJ (1994) Environmental variability as a factor controlling spatial patterns in distribution and species diversity of zooplankton in the St. LawrenceEstuary. Mar Ecol-Prog Ser 107:67–81. https://doi.org/10.3354/meps107067
Mauchline J (1998) The biology of calanoid copepods. Adv Mar Biol 33:1–710
McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390. https://doi.org/10.1034/j.1600-0706.2003.12098.x
McLusky DS, Elliott M (2004) The estuarine ecosystem: ecology, threats and management. Oxford University Press, Oxford, 224 p
Michener RH, Kaufman L (2007) Stable isotope ratios as tracers in marine food webs: an update. In: Michener R, Lajtha K (eds) Stable isotopes in ecology and environmental science. Blackwell Scientific Publications, Boston, pp 238–282
Michener RH, Schell DM (1994) Stable isotopes ratios as tracers in marine aquatic food webs. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology and environmental sciences. Blackwell Scientific Publications, Oxford, pp 138–158
Mintenbeck K, Brey T, Jacob U, Knust R, Struck U (2008) How to account for the lipid effect on carbon stable-isotope ratio (δ13C): sample treatment effects and model bias. J Fish Biol 72:815–830. https://doi.org/10.1111/j.1095-8649.2007.01754.x
Morgan CA, Cordell JR, Simenstad CA (1997) Sink or swim? Copepod population maintenance in the Columbia River estuarine turbidity-maxima region. Mar Biol 129:309–317. https://doi.org/10.1007/s002270050171
Orsi J, Ohtsuka S (1999) Interdoction of the Asian copepods Acartiella sinensis, Tortanus dextrilobatus (Copepoda: Calanoida), and Limnoithona tetraspina (Copepoda: Cyclopoida) to the San Francisco Estuary. Plankton Biol Ecol 46:128–131
Park EO, Rahman MS, Seo MH, Kim JG, Soh HY (2013) Distribution patterns of calanoid copepods along the Seomjin River estuary in southern Korea during summer. Korean J Environ Biol 31:165–171. https://doi.org/10.11626/KJEB.2013.31.2.165
Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672. https://doi.org/10.1371/journal.pone.0009672
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718. https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2
Rau GH, Teyssie JL, Rassoulzadegan F, Fowler SW (1990) 13C/12C and 15N/14N variations among size-fractionated marine particles: implications for their origin and trophic relationships. Mar Ecol-Prog Ser 59:33–38. https://doi.org/10.3354/meps059033
Rolff C (2000) Seasonal variation in δ13C and δ15N of size-fractionated plankton at a coastal station in the northern Baltic proper. Mar Ecol-Prog Ser 203:47–65. https://doi.org/10.3354/meps203047
Sakaguchi SO, Ueda H (2018) Genetic analysis on Pseudodiaptomus inopinus (Copepoda, Calanoida) species complex in Japan: revival of the species name of P. japonicus Kikuchi, 1928. Plankton Benthos Res 13:173–179. https://doi.org/10.3800/pbr.13.173
Schoener TW (1968) The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726. https://doi.org/10.2307/1935534
Smyntek PM, Teece MA, Schulz KL, Thackeray SJ (2007) A standard protocol for stable isotope analysis of zooplankton in aquatic food web research using mass balance correction models. Limnol Oceanogr 52:2135–2146. https://doi.org/10.4319/lo.2007.52.5.2135
Soh HY, Kwon SW, Lee W, Yoon YH (2012) A new Pseudodiaptomus (Copepoda, Calanoida) from Korea supported by molecular data. Zootaxa 3368:229–244. https://doi.org/10.11646/zootaxa.3368.1.11
Stricker D (2008) BrightStat.com: free statistics online. Comput Meth Prog Bio 92:135–143. https://doi.org/10.1016/j.cmpb.2008.06.010
Suzuki KW, Kasai A, Nakayama K, Tanaka M (2012) Year-round accumulation of particulate organic matter in the estuarine turbidity maximum: comparative observations in three macrotidal estuaries (Chikugo, Midori, and Kuma Rivers), southern Japan. J Oceanogr 68:453–471. https://doi.org/10.3390/w12092561
Suzuki KW, Ueda H, Nakayama K, Tanaka M (2014) Spatiotemporal dynamics of stable carbon isotope ratios in two sympatric oligohaline copepods in relation to the estuarine turbidity maximum (Chikugo River, Japan): implications for food sources. J Plankton Res 36:461–474. https://doi.org/10.1093/plankt/fbt094
Syväranta J, Vesala S, Rask M, Ruuhijärvi J, Jones RI (2008) Evaluating the utility of stable isotope analyses of archived freshwater sample materials. Hydrobiologia 600:121–130. https://doi.org/10.1007/s10750-007-9181-3
Ueda H (1987) Temporal and spatial distribution of the two closely related Acartia species A. omorii and A. hudsonica (Copepoda, Calanoida) in a small inlet water of Japan. Estuar Coast Shelf Sci 24:691–700. https://doi.org/10.1016/0272-7714(87)90107-7
Ueda H, Sakaguchi SO (2019) Pseudodiaptomus yamato n sp. (Copepoda, Calanoida) endemic to Japan, with redescriptions of the two closely related species P. inopinus Burckhardt and P. japonicus Kikuchi. Plankton Benthos Res 14:29–38. https://doi.org/10.3800/pbr.14.29
Uye SI, Kayano Y (1994) Predatory feeding behavior of Tortanus (Copepoda: Calanoida): life-stage differences and the predation impact on small planktonic crustaceans. J Crust Biol 14:473–483. https://doi.org/10.1163/193724094X00056
Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066. https://doi.org/10.4319/lo.2001.46.8.2061
Acknowledgements
This research was a part of the project entitled ‘Long-term change of structure and function in marine ecosystems of Korea’, funded by the Ministry of Oceans and Fisheries, Korea. This work was also supported by a grant from the National Institute of Fisheries Science (R2021063).
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Im, DH., Suh, HL. Resource Utilization of Three Copepods Along Salinity Gradient in the Seomjin River Estuary, Revealed by Stable Isotope Analysis. Ocean Sci. J. 56, 106–116 (2021). https://doi.org/10.1007/s12601-021-00010-6
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DOI: https://doi.org/10.1007/s12601-021-00010-6