Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Zoobenthos are minor dietary components of small omnivorous fishes in a shallow eutrophic lake

Natsuru Yasuno A E , Yuki Chiba A , Yasufumi Fujimoto B , Kentaro Shindo B , Tetsuo Shimada B , Shuichi Shikano C and Eisuke Kikuchi D
+ Author Affiliations
- Author Affiliations

A Graduate School of Life Sciences, Tohoku University 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi 980-8577, Japan.

B Miyagi Prefectural Izunuma-Uchinuma Environmental Foundation 17-2 Shikimi, Wakayanagi, Kurihara, Miyagi, 989-5504, Japan.

C Center for Northeast Asian Studies, Tohoku University 41 Kawauchi, Aoba-ku, Sendai, Miyagi 980-8576, Japan.

D Environmental Education Center, Miyagi University of Education 149 Aramaki Aza Aoba, Aoba-ku, Sendai, 980-0845, Japan.

E Corresponding author. Present address: Sendai City Hall, 3-7-1 Kokubun-cho, Aoba-ku, Sendai, Miyagi, 980-0803, Japan. Email: plumosussia@yahoo.co.jp

Marine and Freshwater Research 67(10) 1562-1568 https://doi.org/10.1071/MF15156
Submitted: 1 November 2014  Accepted: 22 June 2015   Published: 30 September 2015

Abstract

We examined whether small omnivorous fishes (smaller than ~100 mm long) integrate littoral, pelagic and benthic pathways in a shallow, eutrophic lake (Lake Izunuma, Japan). The surface of the lake was covered by a dense vegetation of floating-leaved macrophytes, and small species dominated the icthyofauna. We determined the δ13C and δ15N ratios of five dominant species of small omnivorous fishes. Using a stable isotope analysis in the R mixing model, we determined the possible contribution of three potential food sources (epiphytic algae, zooplankton and zoobenthos (larval chironomids)) to omnivorous fish tissue compositions. Four omnivorous fishes (Gnathopogon elongatus elongatus, Pseudorasbora parva, Biwia zezera and Tridentiger obscurus) subsisted largely on epiphytic algae and zooplankton, whereas zoobenthos contributed little to their diets. Acheilognathus rhombeus subsisted mostly on epiphytic algae. Thus, in this shallow, eutrophic lake, omnivorous fishes incorporated both littoral and pelagic production into the food web, but rarely benthic production. The dominant benthic chironomid larvae often burrow several centimetres into the sediment, and the low dietary contribution of zoobenthos to small fishes may be due to inefficiency at foraging on buried benthos associated with fish body size.

Additional keywords: chironomid, cyprinid, δ13C and δ15N, isotope mixing model, methane-oxidising bacteria.


References

Agasild, H., Zingel, P., Tuvikene, L., Tuvikene, A., Timm, H., Feldmann, T., Salujõe, J., Toming, K., Jones, R. I., and Nõges, T. (2014). Biogenic methane contributes to the food web of a large shallow lake. Freshwater Biology 59, 272–285.
Biogenic methane contributes to the food web of a large shallow lake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXktFCjtg%3D%3D&md5=01223d312ac19d858a896efd67f3925bCAS |

Carlson, R. E. (1977). A trophic state index for lakes. Limnology and Oceanography 22, 361–369.
A trophic state index for lakes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXktFWhtbs%3D&md5=a182a0ae9db3d688492c39481cff5fcaCAS |

Cole, J. J., Carpenter, S. R., Pace, M. L., Van de Bogert, M. C., Kitchell, J. L., and Hodgson, J. R. (2006). Differential support of lake food webs by three types of terrestrial organic carbon. Ecology Letters 9, 558–568.
Differential support of lake food webs by three types of terrestrial organic carbon.Crossref | GoogleScholarGoogle Scholar | 16643301PubMed |

Dolson, R., McCann, K., Rooney, N., and Ridgway, M. (2009). Lake morphometry predicts the degree of habitat coupling by a mobile predator. Oikos 118, 1230–1238.
Lake morphometry predicts the degree of habitat coupling by a mobile predator.Crossref | GoogleScholarGoogle Scholar |

Fujimoto, Y., Kawagishi, M., and Shindo, K. (2008). Freshwater fishes in Lake Izunuma–Uchinuma basin, Japan: distribution patterns of native species and invasive species. Izunuma–Uchinuma Wetland Research 2, 13–25.

Gozlan, R. E., Andreou, D., Asaeda, T., Beyer, K., Bouhadad, R., Burnard, D., Caiola, N., Cakic, P., Djikanovic, V., Esmaeili, H. R., Falka, I., Golicher, D., Harka, A., Jeney, G., Kováč, V., Musil, J., Nocita, A., Povz, M., Poulet, N., Virbickas, T., Wolter, C., Tarkan, A. S., Tricarico, E., Trichkova, T., Verreycken, H., Witkowski, A., Zhang, C., Zweimueller, I., and Britton, J. R. (2010). Pan-continental invasion of Pseudorasbora parva: towards a better understanding of freshwater fish invasions. Fish and Fisheries 11, 315–340.
Pan-continental invasion of Pseudorasbora parva: towards a better understanding of freshwater fish invasions.Crossref | GoogleScholarGoogle Scholar |

Hampton, S. E., Fradkin, S. C., Leavitt, P. R., and Rosenberger, E. E. (2011). Disproportionate importance of nearshore habitat for the food web of a deep oligotrophic lake. Marine and Freshwater Research 62, 350–358.
Disproportionate importance of nearshore habitat for the food web of a deep oligotrophic lake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlt1Gku7o%3D&md5=0e63a83c0f0d178b261d5c387653fce4CAS |

Harrod, C., and Grey, J. (2006). Isotopic variation complicates analysis of trophic relations within the fish community of Plußsee: a small, deep, stratifying lake. Archiv für Hydrobiologie 167, 281–299.
Isotopic variation complicates analysis of trophic relations within the fish community of Plußsee: a small, deep, stratifying lake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtF2ls7%2FN&md5=dae5b7f2290266095158713e81e1a39aCAS |

Jacobsen, L., and Perrow, M. R. (1998). Predation risk from piscivorous fish influencing the diel use of macrophytes by planktivorous fish in experimental ponds. Ecology Freshwater Fish 7, 78–86.
Predation risk from piscivorous fish influencing the diel use of macrophytes by planktivorous fish in experimental ponds.Crossref | GoogleScholarGoogle Scholar |

Jones, R. I., and Grey, J. (2011). Biogenic methane in freshwater food webs. Freshwater Biology 56, 213–229.
Biogenic methane in freshwater food webs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVCls7g%3D&md5=49a228ed38aa177eeea3af6fe7b3771fCAS |

Jones, J. I., and Waldron, S. (2003). Combined stable isotope and gut contents analysis of food webs in plant-dominated, shallow lakes. Freshwater Biology 48, 1396–1407.
Combined stable isotope and gut contents analysis of food webs in plant-dominated, shallow lakes.Crossref | GoogleScholarGoogle Scholar |

Kajan, R., and Frenzel, P. (1999). The effect of chironomid larvae on production, oxidation and fluxes of methane in a flooded rice soil. FEMS Microbiology Ecology 28, 121–129.
The effect of chironomid larvae on production, oxidation and fluxes of methane in a flooded rice soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFCrsbY%3D&md5=4299e61d8b979415de979770750ce250CAS |

Kanaya, G., Yadrenkina, E. N., Zuykova, E. I., Kikuchi, E., Doi, H., Shikano, S., Mizota, C., and Yurlova, N. I. (2009). Contribution of organic matter sources to cyprinid fishes in the Chany Lake–Kargat River estuary, western Siberia. Marine and Freshwater Research 60, 510–518.
Contribution of organic matter sources to cyprinid fishes in the Chany Lake–Kargat River estuary, western Siberia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsVensrc%3D&md5=ef9a3bab4540d05e889df3c9ecf0add5CAS |

Karlsson, J., and Byström, P. (2005). Littoral energy mobilization dominates energy supply for top consumers in subarctic lakes. Limnology and Oceanography 50, 538–543.
Littoral energy mobilization dominates energy supply for top consumers in subarctic lakes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFahsL4%3D&md5=f242fdb38fcad7eff66f3cd1622021acCAS |

Kawanabe, H., and Mizuno, N. (1989). ‘Freshwater Fishes in Japan.’ (Yama-kei: Tokyo) [In Japanese].

Lammens, E. H. R. R., and Hoogenboezem, W. (1991). Diet and feeding behaviour. In ‘Cyprinid Fishes: Systematics, biology and exploitation’. (Eds I. J. Winfield and J. S. Nelson.) pp. 353–376. (Chapman Hall: London.)

Luek, A., Morgan, G. E., Wissel, B., Gunn, J. M., and Ramcharan, C. W. (2013). Impaired littoral energy pathways cause a shift to pelagic resources by fish in recovering lake food webs. Ecology Freshwater Fish 22, 348–360.
Impaired littoral energy pathways cause a shift to pelagic resources by fish in recovering lake food webs.Crossref | GoogleScholarGoogle Scholar |

Mao, Z., Gu, X., Zeng, Q., Zhou, L., and Sun, M. (2012). Food web structure of a shallow eutrophic lake (Lake Taihu, China) assessed by stable isotope analysis. Hydrobiologia 683, 173–183.
Food web structure of a shallow eutrophic lake (Lake Taihu, China) assessed by stable isotope analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVeqtLs%3D&md5=e84f8d55c052ff2214c8a97fe76c4aa8CAS |

Meerhoff, M., Mazzeo, N., Moss, B., and Rodriguez-Gallego, L. (2003). The structuring role of free-floating versus submerged plants in a subtropical shallow lake. Aquatic Ecology 37, 377–391.
The structuring role of free-floating versus submerged plants in a subtropical shallow lake.Crossref | GoogleScholarGoogle Scholar |

Nakamura, M. (1969). ‘Cyprinid Fishes of Japan: Studies on the Life History of the Cyprinid Fishes of Japan.’ Special Publications. (The Research Institute for Natural Resources: Tokyo.) [In Japanese].

Parnell, A. C., Inger, R., Bearhop, S., and Jackson, A. L. (2010). Source partitioning using stable isotopes: coping with too much variation. PLoS One 5, e9672.
Source partitioning using stable isotopes: coping with too much variation.Crossref | GoogleScholarGoogle Scholar | 20300637PubMed |

Phillips, D. L., Newsome, S. D., and Gregg, J. W. (2005). Combining sources in stable isotope mixing models: alternative methods. Oecologia 144, 520–527.
Combining sources in stable isotope mixing models: alternative methods.Crossref | GoogleScholarGoogle Scholar | 15711995PubMed |

Pinnegar, J. K., and Polunin, N. V. C. (1999). Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology 13, 225–231.
Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions.Crossref | GoogleScholarGoogle Scholar |

Pomerleau, C., Winkler, G., Sastri, A., Nelson, R. J., and Williams, W. J. (2014). The effect of acidification and the combined effects of acidification/lipid extraction on carbon stable isotope ratios for sub-arctic and arctic marine zooplankton species. Polar Biology 37, 1541–1548.
The effect of acidification and the combined effects of acidification/lipid extraction on carbon stable isotope ratios for sub-arctic and arctic marine zooplankton species.Crossref | GoogleScholarGoogle Scholar |

Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.
Using stable isotopes to estimate trophic position: models, methods, and assumptions.Crossref | GoogleScholarGoogle Scholar |

Ravinet, M., Syväranta, J., Jones, R. I., and Grey, J. (2010). A trophic pathway from biogenic methane supports fish biomass in a temperate lake ecosystem. Oikos 119, 409–416.
A trophic pathway from biogenic methane supports fish biomass in a temperate lake ecosystem.Crossref | GoogleScholarGoogle Scholar |

Scheffer, M. (1998). ‘Ecology of Shallow Lakes.’ (Chapman Hall: London.)

Schindler, D. E., and Scheuerell, M. D. (2002). Habitat coupling in lake ecosystems. Oikos 98, 177–189.
Habitat coupling in lake ecosystems.Crossref | GoogleScholarGoogle Scholar |

Shidara, S. (1992). Social conditions surrounding Izunuma and Uchinuma Lakes. In ‘Report for Environmental Preservation Measures of Izunuma and Uchinuma Lakes’. pp. 155–164. (Advisory Committee for Environmental Preservation Measures: Sendai, Miyagi Prefecture, Japan) [In Japanese].

Vander Zanden, M. J., and Vadeboncoeur, Y. (2002). Fishes as integrators of benthic and pelagic food webs in lakes. Ecology 83, 2152–2161.
Fishes as integrators of benthic and pelagic food webs in lakes.Crossref | GoogleScholarGoogle Scholar |

Vander Zanden, M. J., Chandra, S., Park, S. K., Vadeboncoeur, Y., and Goldman, C. R. (2006). Efficiencies of benthic and pelagic trophic pathways in a subalpine lake. Canadian Journal of Fisheries and Aquatic Sciences 63, 2608–2620.
Efficiencies of benthic and pelagic trophic pathways in a subalpine lake.Crossref | GoogleScholarGoogle Scholar |

Vander Zanden, M. J., Vadeboncoeur, Y., and Chandra, S. (2011). Fish reliance on littoral–benthic resources and the distribution of primary production in lakes. Ecosystems 14, 894–903.
Fish reliance on littoral–benthic resources and the distribution of primary production in lakes.Crossref | GoogleScholarGoogle Scholar |

Yasuno, N., Chiba, Y., Shindo, K., Shimada, T., Shikano, S., and Kikuchi, E. (2009). Changes in the trophic state and the benthic fauna in Lake Izunuma, with special reference to the chironomid species. Izunuma-Uchinuma Wetland Research 3, 49–63.

Yasuno, N., Shikano, S., Muraoka, A., Shimada, T., Ito, T., and Kikuchi, E. (2012). Seasonal increase of methane in sediment decreases δ13C of larval chironomids in a eutrophic shallow lake. Limnology 13, 107–116.
Seasonal increase of methane in sediment decreases δ13C of larval chironomids in a eutrophic shallow lake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVOhtr8%3D&md5=478ab155113bea6df88eef6d3c51ba5cCAS |

Yasuno, N., Shikano, S., Shimada, T., Shindo, K., and Kikuchi, E. (2013). Comparison of the exploitation of methane-derived carbon by tubicolous and non-tubicolous chironomid larvae in a temperate eutrophic lake. Limnology 14, 239–246.
Comparison of the exploitation of methane-derived carbon by tubicolous and non-tubicolous chironomid larvae in a temperate eutrophic lake.Crossref | GoogleScholarGoogle Scholar |