Advertisement

Aquatic Ecology

, Volume 53, Issue 2, pp 217–232 | Cite as

Application of stable isotopic analyses for fish host–parasite systems: an evaluation tool for parasite-mediated material flow in aquatic ecosystems

  • Gen Kanaya
  • Mikhail M. Solovyev
  • Shuichi Shikano
  • Jun-ichi Okano
  • Natalia M. Ponomareva
  • Natalia I. YurlovaEmail author
Article

Abstract

Parasites potentially have important roles in aquatic ecosystems, although relatively little is known about their contributions to the complexity of food web structure. In this study, stable carbon and nitrogen isotope analyses (δ13C and δ15N) were applied for fish host–parasite systems in a shallow swamp–lake ecosystem to assess the validity of stable isotope technics to reveal the parasite-mediated trophic linkages in the food web. Forty host–parasite pairs, including seven parasite taxa (cestodes, trematodes, crustaceans, and hirudinids), found on six host fish species (cyprinids and percids) were examined. The parasites showed unusual δ15N fractionation, with an overall average of − 1.9‰, suggesting the intake of 14N-rich ammonia for amino acid synthesis and/or selective absorption of 15N-depleted amino acids in the host fluid. The isotopic signatures of fish hosts and their parasites were positively correlated, suggesting the absorption and transfer of host-derived nutrients during infection. A δ13C-based isotope mixing model showed that each host fish species exhibited unique dependencies on POM, land-derived organic matter, and macrophytes, suggesting the host-specific trophic niche of the associated parasites in the lake–swamp food web. These emphasized that parasites are potential pathways of material and energy flows in aquatic ecosystems, contributing substantially to the food web complexity. Stable isotope analyses are the useful tools to elucidate the host–parasite trophic linkages, and case-specific isotopic fractionation factors are the mandatory information for a better understanding of the parasite-mediated material flow in ecosystems.

Keywords

Fish parasites Material flow Stable isotope analysis Trematode parasites Trophic enrichment Trophic niche Wetland food web 

Notes

Acknowledgements

We thank Dr. SS. Matsuzaki, NIES, for allowing use of the mass spectrometer and Dr. A.K., Yurlov, ISEA SB RAS, for his support throughout the research. Staffs in the Chany Lake field station are acknowledged for their help in field and laboratory works. All experiments and sampling complied with the current laws in the Russian Federation.

Funding

This study was supported partly by the International Joint Research Programs (2009 to 2010, 2012 to 2013, and 2015 to 2016) from JSPS and the Russian Foundation for Basic Research (RFBR research projects No. 09-04-92104 and 12-04-92111).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: margolis et al revisited. J Parasitol 83:575–583CrossRefPubMedGoogle Scholar
  2. Bykhovskaya-Pavlovskaya IE (1962) Trematodes of birds in the fauna of the USSR. Izdatel’stvo Akademii Nauk SSSR, Moscow and Leningrad, Russia, p 407. (in Russian)Google Scholar
  3. DeNiro MJ, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197:261–263CrossRefPubMedGoogle Scholar
  4. Deudero S, Pinnegar JK, Polunin NVC (2002) Insights into fish host-parasite trophic relationships revealed by stable isotope analysis. Dis Aquat Org 52:77–86CrossRefPubMedGoogle Scholar
  5. Dogel VA (1962) General parasitology. Oliver and Boyd, Edinburgh, p 464 (in Russian) Google Scholar
  6. Doi H, Yurlova N, Vodyanitskaya S, Kanaya G, Shikano S, Kikuchi E (2010) Estimating isotope fractionation between cercariae and host snail with the use of isotope measurement designed for very small organisms. J Parasitol 96:314–317CrossRefPubMedGoogle Scholar
  7. Dönges J (1964) Der Lebenszyklus von Posthodiplostomum cuticola (v. Nordmann 1832) Dubois 1936 (Trematoda, Diplostomatidae). Zeitschrift für Parasitenkunde 24:169–248 (in German) Google Scholar
  8. Dubinina MN (1966) Cestoda Remnetsy: Ligulidae of the USSR fauna. Nauka Leningrad, Leningrad, Russia, p 268. (in Russian)Google Scholar
  9. Dubois SY, Savoye N, Sauriau P-G, Billy I, Martinez P, de Montaudouin X (2009) Digenean trematodes–marine mollusc relationships: a stable isotope study. Dis Aquat Org 84:65–77CrossRefPubMedGoogle Scholar
  10. Gόmez-Dìaz E, González-Solìs J (2010) Trophic structure in a seabird host-parasite food web: insights from stable isotope analyses. PLoS ONE 5:e10454CrossRefGoogle Scholar
  11. Hare PE, Fogel ML, Stafford TW Jr, Mitchell AD, Hoeringa TC (1991) The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. J Archaeol Sci 18:211–292Google Scholar
  12. Harvey CJ, Kitchell JF (2000) A stable isotope evaluation of the structure and spatial heterogeneity of a Lake Superior food web. Can J Fish Aquat Sci 57:1395–1403CrossRefGoogle Scholar
  13. Hoffman GL (1977) Argulus a branchiuran parasite of freshwater fishes. US Fish and Wildlife Services. Fish Dis Leafl 49:1–9Google Scholar
  14. Kanaya G, Yadrenkina EN, Zuykova EI, Kikuchi E, Doi H, Shikano S, Mizota C, Yurlova NI (2009) Contribution of organic matter sources to cyprinid fishes in the Chany Lake-Kargat River estuary, western Siberia. Mar Freshw Res 60:510–518CrossRefGoogle Scholar
  15. Kaplan AT, Rebhal S, Lafferty KD, Kuris AM (2009) Small estuarine fishes feed on large Trematode cercariae: lab and field investigations. J Parasitol 95:477–480CrossRefGoogle Scholar
  16. Kasahara S (1962) Studies on the biology of the parasitic copepod Lernaea cyprinacea Linnaeus and the methods for controlling this parasite in fish-culture ponds. Contrib Fish Lab Fac Agric Univ Tokyo 3:103–196 (in Japanese) Google Scholar
  17. Köhler P, Voigt W (1988) Nutrition and metabolism. In: Mehlhorn H (ed) Parasitology in focus. Springer, Berlin, pp 412–452CrossRefGoogle Scholar
  18. Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini FT, Mora AB, Pickering M, Talhouk NL, Torchin ME, Lafferty KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518CrossRefPubMedGoogle Scholar
  19. Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. PNAS 103:11211–11216CrossRefPubMedGoogle Scholar
  20. Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Let 11:533–546CrossRefGoogle Scholar
  21. Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48CrossRefGoogle Scholar
  22. McCutchan JH Jr, Lewis WM Jr, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon nitrogen and sulfur. Oikos 102:378–390CrossRefGoogle Scholar
  23. Miura O, Kuris AM, Torchin ME, Hechinger RF, Chiba S (2006) Parasites alter host phenotype and may create a new ecological niche for snail hosts. Proc R Soc B 273:1323–1328CrossRefPubMedGoogle Scholar
  24. Morley NJ (2012) Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691:7–19CrossRefGoogle Scholar
  25. Navarro J, Albo-Puigserver M, Coll M, Saez R, Forero MG, Kutcha R (2014) Isotopic discrimination of stable isotopes of nitrogen (δ 15N) and carbon (δ 13C) in a host-specific holocephalan tapeworm. J Helminthol 88:371–375CrossRefPubMedGoogle Scholar
  26. Ogawa N, Ogura N (1997) Dynamics of particulate organic matter in the Tamagawa Estuary and inner Tokyo Bay. Estuar Coast Shelf Sci 44:263–273CrossRefGoogle Scholar
  27. Olive PJW, Pinnegar JK, Polunin NVC, Richards G, Welch R (2003) Isotope trophic-step fractionation: a dynamic equilibrium model. J Anim Ecol 72:608–617CrossRefGoogle Scholar
  28. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672CrossRefPubMedPubMedCentralGoogle Scholar
  29. Pinnegar JK, Campbell N, Polunin NVC (2001) Unusual stable isotope fractionation patterns observed for fish host–parasite trophic relationships. J Fish Biol 59:494–503Google Scholar
  30. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  31. Power M, Klein GM (2004) Fish host-cestode parasite stable isotope enrichment patterns in marine estuarine and freshwater fishes from Northern Canada. Isot Environ Health Stud 40:257–266CrossRefGoogle Scholar
  32. Shigin AA (1964) To the issue on the life span of Diplostomum spathaceum in the body of the second intermediate host. Proc Helminthol Lab Acad Sci USSR 14:262–272 (in Russian) Google Scholar
  33. Shigin AA (1993) Trematodes of the fauna of Russia and neighbouring regions. Genus Diplostomum. Adults. Nauka, Moscow, Russia, p 206. (in Russian) Google Scholar
  34. Solov'ev MM, Kashinskaya EN, Glupov VV (2010) Infection with metacercaria of the family Diplostomidae and activity of digesting enzymes of the young of the Siberian dace Leuciscus leuciscus baicalensis (Dyb) in the Kargat River of the basin of Lake Chany. Contemp Probl Ecol 3:555–561CrossRefGoogle Scholar
  35. Solovyev MM, Kashinskaya EN, Izvekova GI, Gisbert E, Glupov VV (2014) Feeding habits and ontogenic changes in digestive enzyme patterns in five freshwater teleosts. J Fish Biol 85:1395–1412CrossRefPubMedGoogle Scholar
  36. Sudarikov VE, Lomakin VV, Ataev AM, Semenova NN (2006) Metacercariae of trematodes parasites of freshwater hydrobionts of Russia. vol 2. Nauka, Moscow, Russia, p 182. (in Russian)Google Scholar
  37. Syväranta J, Hamalainen H, Jones RI (2006) Within-lake variability in carbon and nitrogen stable isotope signatures. Freshw Biol 51:1090–1102CrossRefGoogle Scholar
  38. Toledo R, Esteban J-G, Fried B (2009) Recent advances in the biology of echinostomes. Adv Parasitol 69:147–204CrossRefPubMedGoogle Scholar
  39. Vander Zanden MJ, Vadeboncoeur Y (2002) Fishes as integrators of benthic and pelagic food webs in lakes. Ecology 83:2152–2161CrossRefGoogle Scholar
  40. Vodyanitskaya SN, Yurlova NI (2013) Parthenites and cercaria of trematodes in the snails Lymnaea saridalensis (Gastropoda Pulmonata) which inhabits the watershed area of Chany Lake (the South of Western Siberia). Contemp Probl Ecol 6:12–19CrossRefGoogle Scholar
  41. Yadrenkina EN (2014) Differences in the infestation rate of young cyprinid fishes (Cypriniforms) by metacercaria of Posthodiplostomum cuticola (Digenea Diplostomatidae) in river and lake systems of the Lake Chany basin (Western Siberia). Parazitologiia 48:234–244 (in Russian) Google Scholar
  42. Yurlova NI (1990). The infection of snails genus Lymnaea by Diplostomum volvens, Nordman, 1832 in Chany Lake. In: Parasiti i bolesni gidrobiontov Ledovitomorskoi provincii. Novosibirsk, Acad. Press, pp 99–107. (in Russian)Google Scholar
  43. Yurlova NI, Vodyanitskaya SN, Serbina EA, Biserkov VY, Georgiev BB, Chipev NH (2006) Temporal variation in prevalence and abundance of metacercariae in the pulmonate snail Lymnaea stagnalis in Chany Lake, West Siberia, Russia: Long-term patterns and environmental covariates. J Parasitol 92:249–259CrossRefPubMedGoogle Scholar
  44. Yurlova NI, Shikano S, Kanaya G, Rastyazhenko NM, Vodyanitskaya SN (2014) The evaluation of snail host-trematode parasite trophic relationships using stable isotope analysis. Parazitologiia 48:193–205 (in Russian) Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Gen Kanaya
    • 1
  • Mikhail M. Solovyev
    • 2
  • Shuichi Shikano
    • 3
  • Jun-ichi Okano
    • 3
  • Natalia M. Ponomareva
    • 2
  • Natalia I. Yurlova
    • 2
    Email author
  1. 1.National Institute for Environmental Studies (NIES)TsukubaJapan
  2. 2.Institute of Systematics and Ecology of AnimalsSiberian Branch of Russian Academy of Sciences (ISEA SB RAS)NovosibirskRussia
  3. 3.Center for Northeast Asian StudiesTohoku UniversitySendaiJapan

Personalised recommendations