Skip to main content
SpringerLink
Log in

Spatial and interspecific variation in the food sources of sympatric estuarine nereidid polychaetes: stable isotopic and enzymatic approaches

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Carbon and nitrogen stable isotope ratios (δ13C and δ15N) of sympatric nereidid polychaetes including Hediste diadroma, H. atoka, Tylorrhynchus osawai, and Simplisetia erythraeensis were examined at six stations along the Japanese coast to reveal the trophic niches of nereidid polychaetes in estuarine benthic food webs. The species studied exhibited a large degree of spatial variation in δ13C values (− 25.3 to − 13.7‰) among stations, suggesting site-based differences in nereidid dietary components. The low δ13C values of nereidids suggest that terrestrial plant materials are important components of their diets in river-affected estuarine habitats, which were also shown by a δ13C-based stable isotope mixing model (SIAR). δ13C values of H. diadroma and H. atoka were 0.3–3.1‰ lower than those of the sympatric T. osawai and S. erythraeensis, while no significant difference was found between Hediste species. A biochemical assay revealed cellulase activity in H. diadroma, H. atoka, and T. osawai (S. erythraeensis was not examined), while the apparent molecular size of cellulase differed between the two genera. These observations suggest that some nereidids can directly assimilate terrestrial plant matters using cellulases, although the dietary importance of terrestrial matter varies among genera. Species with the ability to digest cellulose may be better able to colonize river-dominated estuarine habitats, where refractory terrestrial detritus is a major carbon source.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aberson MJR, Bolam SG, Hughes RG (2016) The effect of sewage pollution on the feeding behavior and diet of Hediste (Nereis diversicolor (O.F. Müller, 1776)) in three estuaries in south-east England, with implications for saltmarsh erosion. Mar Pollut Bull 105:150–160

    Article  PubMed  CAS  Google Scholar 

  • Antonio ES, Kasai A, Ueno M, Kurikawa Y, Tsuchiya K, Toyohara H, Ishihi Y, Yokoyama H, Yamashita Y (2010) Consumption of terrestrial organic matter by estuarine molluscs determined by analysis of their stable isotopes and cellulase activity. Estaurine Coast Shelf Sci 86:401–407

    Article  CAS  Google Scholar 

  • Beguin P (1983) Detection of cellulase activity in polyacrylamide gels using Congo red-stained agar replicas. Anal Biochem 131:333–336

    Article  PubMed  CAS  Google Scholar 

  • Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annu Rev Ecol Syst 42:411–440

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Chanton J, Lewis FG (2002) Examination of coupling between primary and secondary production in a river-dominated estuary: Apalachicola Bay, Florida, USA. Limnol Oceanogr 47:683–697

    Article  Google Scholar 

  • Doi H, Matsumasa M, Toya T, Satoh N, Mizota C, Maki Y, Kikuchi E (2005) Spatial shifts in food sources for macrozoobenthos in an estuarine ecosystem: carbon and nitrogen stable isotope analyses. Estaurine Coast Shelf Sci 64:316–322

    Article  Google Scholar 

  • Fauchald K, Jumars PA (1979) The diet of worms: a study of polychaete feeding guilds. Oceanogr Mar Biol Annu Rev 17:193–284

    Google Scholar 

  • Heip CHR, Goosen NK, Herman PMJ, Kromkamp J, Middelburg JJ, Soetaert K (1995) Production and consumption of biological particles in temperate tidal estuaries. Oceanogr Mar Biol Annu Rev 33:1–149

    Google Scholar 

  • Imajima M (1996) Annelid polychaetes (Japanese title: Kankei Doubutu Tamourui). Seibutu Kenkyusha, Tokyo, Japan (in Japanese)

  • Ito K, Nozaki M, Ohta T, Miura C, Tozawa Y, Miura T (2011) Differences of two polychaete species reflected in enzyme activities. Mar Biol 158:1211–1221

    Article  CAS  Google Scholar 

  • Jue CK, Lipke PN (1986) Determination of reducing sugars in the nanomole range with tetrazolium blue. J Biochem Biophys Methods 11:109–115

    Article  Google Scholar 

  • Kanaya G (2010) Food source estimation of benthic invertebrates using carbon and nitrogen stable isotope ratios: applications to estuarine ecosystems. Jpn J Benthol 65:28–40 (in Japanese with English abstract)

    Article  Google Scholar 

  • Kanaya G (2017) Rivers, paddy fields, and estuaries: responses of the macrozoobenthos to environmental fluctuation in estuaries. Jpn J Benthol 71:102–110 (in Japanese with English abstract)

    Article  Google Scholar 

  • Kanaya G, Takagi S, Nobata E, Kikuchi E (2007) Spatial dietary shift of macrozoobenthos in a brackish lagoon revealed by carbon and nitrogen stable isotope ratios. Mar Ecol Prog Ser 345:117–127

    Article  CAS  Google Scholar 

  • Kanaya G, Takagi S, Kikuchi E (2008) Spatial dietary variations in Laternula marilina (Bivalva) and Hediste spp. (Polychaeta) along environmental gradients in two brackish lagoons. Mar Ecol Prog Ser 359:133–144

    Article  CAS  Google Scholar 

  • Kanaya G, Suzuki T, Kikuchi E (2011) Spatio-temporal variations in macrozoobenthic assemblage structures in a river-affected lagoon (Idoura Lagoon, Sendai Bay, Japan): influences of freshwater inflow. Estuarine Coast Shelf Sci 92:169–179

    Article  Google Scholar 

  • Kanaya G, Suzuki T, Kikuchi E (2015) Impacts of the 2011 tsunami on sediment characteristics and macrozoobenthic assemblages in a shallow eutrophic lagoon, Sendai Bay, Japan. PLoS One 10:e0135125

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kang C-K, Choy EJ, Paik S-K, Park HJ, Lee K-S, An S (2007) Contributions of primary organic matter sources to macroinvertebrate production in an intertidal salt marsh (Scirpus triqueter) ecosystem. Mar Ecol Prog Ser 334:131–143

    Article  CAS  Google Scholar 

  • Karlson AML, Nascimento FJA, Näslund J, Elmgren R (2010) Higher diversity of deposit-feeding macrofauna enhances phytodetritus processing. Ecology 91:1414–1423

    Article  PubMed  Google Scholar 

  • Kasai A, Nakata A (2005) Utilization of terrestrial organic matter by the bivalve Corbicula japonica estimated from stable isotope analysis. Fish Sci 71:151–158

    Article  CAS  Google Scholar 

  • Kasai A, Toyohara H, Nakata A, Miura T, Azuma N (2006) Food sources for the bivalve Corbicula japonica in the foremost fishing lakes estimated from stable isotope analysis. Fish Sci 72:105–114

    Article  CAS  Google Scholar 

  • Kawaida S, Kimura T, Toyohara H (2013) Habitat segregation of two dotillid crabs Scopimera globosa and Ilyoplax pusilla in relation to their cellulase activity on a marsh-dominated estuarine tidal flat in central Japan. J Exp Mar Bio Ecol 449:93–99

    Article  Google Scholar 

  • Kikuchi E, Wada E (1996) Carbon and nitrogen stable isotope ratios of deposit-feeding polychaetes in the Nanakita River Estuary, Japan. Hydrobiologia 321:69–75

    Article  CAS  Google Scholar 

  • Kristensen JH (1972) Carbohydrases of some marine invertebrates with notes on their food and on the natural occurrence of the carbohydrates studied. Mar Biol 14:130–142

    Article  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Levin LA, Boesch DF, Covich A, Dahm C, Erséus C, Ewel KC, Kneib RT, Moldenke A, Palmer MA, Snelgrove P, Strayer D, Weslawski JM (2001) The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems 4:430–451

    Article  CAS  Google Scholar 

  • Liu W, Tanimura A, Imai T, Kanaya G, Niiyama T, Maegawa S, Kohzu A, Kimura T, Toyohara H (2014) Distribution of gastropods in a tidal flat in association with digestive enzyme activities. Plankton Benthos Res 9:156–167

    Article  CAS  Google Scholar 

  • Nakamura Y, Kerciku F (2000) Effects of filter-feeding bivalves on the distribution of water quality and nutrient cycling in a eutrophic coastal lagoon. J Mar Syst 26:209–221

    Article  Google Scholar 

  • Nanami A, Saito H, Akita T, Motomatsu K, Kuwahara H (2005) Spatial distribution and assemblage structure of macrobenthic invertebrates in a brackish lake in relation to environmental variables. Estuarine Coast Shelf Sci 63:167–176

    Article  CAS  Google Scholar 

  • Nelson JA, Deegan L, Garritt R (2015) Drivers of spatial and temporal variability in estuarine food webs. Mar Ecol Prog Ser 533:67–77

    Article  CAS  Google Scholar 

  • Niiyama T, Toyohara H (2011) Widespread distribution of cellulase and hemicellulase activities among aquatic invertebrates. Fish Sci 77:649–655

    Article  CAS  Google Scholar 

  • Nishizawa R, Sato M, Furota T, Tosuji H (2014) Cryptic invasion of northeast Pacific estuaries by the Asian polychaete, Hediste diadroma (Nereididae). Mar Biol 161:187–194

    Article  Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS One 5:e9672

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316

    Article  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Riera P, Richard P (1996) Isotopic determination of food sources of Crassostrea gigas along a trophic gradient in the estuarine bay of Marennes-Oleron. Estaurine Coast Shelf Sci 42:347–360

    Article  Google Scholar 

  • Sakamaki T, Shum JY, Richardson JS (2010) Watershed effects on chemical properties of sediment and primary consumption in estuarine tidal flats: importance of watershed size and food selectivity by macrobenthos. Ecosystems 13:328–337

    Article  CAS  Google Scholar 

  • Sakamoto K, Toyohara H (2009) A comparative study of cellulase and hemicellulase activities of brackish water clam Corbicula japonica with those of other marine Veneroida bivalves. J Exp Biol 212:2812–2818

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto K, Touhata K, Yamashita M, Kasai A, Toyohara H (2007) Cellulose digestion by common Japanese freshwater clam Corbicula japonica. Fish Sci 73:675–683

    Article  CAS  Google Scholar 

  • Sato M (2004) Diversity of polychaetes and environments in tidal flats: a study on the Hediste species group (Nereididae). Fossils 76:122–133 (in Japanese with English abstract)

    Google Scholar 

  • Sato M (2017) Nereididae (Annelida) in Japan, with special reference to life-history differentiation among estuarine species. In: Motokawa M (eds) Species diversity of animals in Japan. Springer Japan, Tokyo, pp 477–512

    Chapter  Google Scholar 

  • Sato M, Nakashima A (2003) A review of Asian Hediste species complex (Nereididae, Polychaeta) with descriptions of two new species and a redescription of Hediste japonica (Izuka, 1908). Zool J Linn Soc 137:403–455

    Article  Google Scholar 

  • Sato T, Miyajima T, Ogawa H, Umezawa Y, Koike I (2006) Temporal variability of stable carbon and nitrogen isotopic composition of size-fractionated particulate organic matter in the hypertrophic Sumida River Estuary of Tokyo Bay, Japan. Estuarine Coast Shelf Sci 68:245–258

    Article  CAS  Google Scholar 

  • Toba Y, Sato M (2013) Filter-feeding behavior of three Asian Hediste species (Polychaeta: Nereididae). Plankton Benthos Res 8:159–165

    Article  Google Scholar 

  • Tosuji H, Furota T (2016) Molecular evidence for the expansion of the Asian cryptic invader Hediste diadroma (Nereididae: Annelida) into the northeast Pacific habitats of the native H. limnicola. Zool Sci 33:162–169

    Article  CAS  Google Scholar 

  • Tosuji H, Sato M (2008) Identification of three Asian Hediste species (Polychaeta: Nereididae) by PCR-RFLP analysis of the mitochondrial 16S rRNA gene. Plankton Benthos Res 3:50–52

    Article  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (2007) Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology 80:1395–1404

    Article  Google Scholar 

  • Watanabe H, Tokuda G (2001) Animal cellulases. Cell Mol Life Sci 58:1167–1178

    Article  PubMed  CAS  Google Scholar 

  • Yokoyama H, Ishihi Y (2007) Variation in food sources of the macrobenthos along a land-sea transect: a stable isotope study. Mar Ecol Prog Ser 346:127–141

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. K. Ito for allowing us to use the mass spectrometer at the Department of Agriculture, Tohoku University. E. Kikuchi, T. Kanaya, R. Kanaya, H. Saito, and H. Sawada are acknowledged for their supports in this study. We acknowledged Dr. H. Doi for allowing us to use isotopic data at St. KT, Dr. M. Matsumasa, and T. Suzuki for their comments on species composition of nereidid polychaetes, and Dr. S. Kawaida for his help in using the stable isotope mixing model in R (SIAR). We are also grateful for the editor Dr. M. Huettel and the referees Dr. U. Hoeger and I. Preciado for their critical comments to the manuscript.

Funding

This study was supported partly by KAKENHI (21770013, 17K07538, 17K07580) from JSPS.

Author information

Author notes

  1. Gen Kanaya

    Present address: National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, 305-8506, Japan

Authors and Affiliations

  1. The Center for Northeast Asian Studies, Tohoku University, Sendai, 980-8576, Japan

    Gen Kanaya

  2. Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan

    Takatoshi Niiyama, Aya Tanimura & Haruhiko Toyohara

  3. Graduate School of Bioresources, Mie University, Tsu, 514-8507, Japan

    Taeko Kimura

  4. Research Field in Science, Science and Engineering Area, Kagoshima University, Kagoshima, 890-0065, Japan

    Hiroaki Tosuji & Masanori Sato

Authors
  1. Gen Kanaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takatoshi Niiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aya Tanimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Taeko Kimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haruhiko Toyohara
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hiroaki Tosuji
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Masanori Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gen Kanaya.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for sampling, care and experimental use of organisms for the study have been followed and all necessary approvals have been obtained.

Additional information

Responsible Editor: M. Huettel.

Reviewed by U. Hoeger and I. Preciado.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kanaya, G., Niiyama, T., Tanimura, A. et al. Spatial and interspecific variation in the food sources of sympatric estuarine nereidid polychaetes: stable isotopic and enzymatic approaches. Mar Biol 165, 101 (2018). https://doi.org/10.1007/s00227-018-3361-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-018-3361-8

Search

Navigation