Skip to main content
Log in

Inducible defenses as factor determining trophic pathways in a food web

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Understanding functional roles of prey defense in biological interactions remains a major task in food web ecology. We investigated the role of an inducible defense as a factor that influences the trophic pathway in an aquatic food web. Quantitative information on food web structure in Lake Suwa (a eutrophic lake in Japan) was provided by carbon and nitrogen stable isotope analyses using samples taken during summer and a structural equation model applied to annual monitoring data. As predicted, there was none or only a weak link detected between the prey with induced defenses (Bosmina fatalis) and its invertebrate predator (Leptodora kindtii). The effects of an inducible defense on the trophic links are based mainly on the mortality or population growth rate of organisms using predation, population (or community) level experiments, field data, and model estimates. However, there was no research linking these different data using stable isotope analyses. Our research provides new evidence supporting previous studies by suggesting the importance of the inducible defense in determining food web structure and function.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aránguiz-Acuña, A., R. Ramos-Jiliberto & R. O. Bustamante, 2011. Experimental evidence that induced defenses promote coexistence of zooplanktonic populations. Journal of Plankton Research 33: 469–477.

    Article  Google Scholar 

  • Boeing, W. J. & C. W. Ramcharan, 2010. Inducible defences are a stabilizing factor for predator and prey populations: a field experiment. Freshwater Biology 55: 2332–2338.

    Google Scholar 

  • Bourdeau, P. E. & F. Johansson, 2012. Predator-induced morphological defences as by-products of prey behaviour: a review and prospectus. Oikos 121: 1175–1190.

    Article  Google Scholar 

  • Cabana, G. & J. B. Rasmussen, 1996. Comparison of aquatic food chains using nitrogen isotopes. Proceedings of the National Academy of Sciences of the United States of America 93: 10844–10847.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chang, K. H. & T. Hanazato, 2003. Seasonal and reciprocal succession and cyclomorphosis of two Bosmina species (Cladocera, Crustacea) co-existing in a lake: their relationship with invertebrate predators. Journal of Plankton Research 25: 141–150.

    Article  Google Scholar 

  • Chang, K. H. & T. Hanazato, 2004. Predation impact of Leptodora kindtii on population dynamics and morphology of Bosmina fatalis and B. longirostris in mesocosms. Freshwater Biology 49: 253–264.

    Article  Google Scholar 

  • Chang, K.-H., T. Hanazato, G. Ueshima & H. Tahara, 2005. Feeding habit of pond smelt (Hypomesus transpacificus nipponensis) and its impact on the zooplankton community in Lake Suwa, Japan. Journal of Freshwater Ecology 20: 129–138.

    Article  Google Scholar 

  • Cole, J. J., S. R. Carpenter, J. Kitchell, M. L. Pace, C. T. Solomon & B. Weidel, 2011. Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen. Proceedings of the National Academy of Sciences of the United States of America 108: 1975–1980.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • DeMott, W. R., 1982. Feeding selectivities and relative ingestion rates of Daphnia and Bosmina. Limnology and Oceanography 27: 518–527.

    Article  Google Scholar 

  • DeMott, W. R. & W. C. Kerfoot, 1982. Competition among cladocerans: nature of the interaction between Bosmina and Daphnia. Ecology 63: 1949–1966.

    Article  Google Scholar 

  • Doi, H., K. H. Chang, T. Ando, I. Ninomiya, H. Imai & S. Nakano, 2009. Resource availability and ecosystem size predict food-chain length in pond ecosystems. Oikos 118: 138–144.

    Article  Google Scholar 

  • Engel, K. & R. Tollrian, 2009. Inducible defences as key adaptations for the successful invasion of Daphnia lumholtzi in North America? Proceedings of the Royal Society B 276: 1865–1873.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hambright, K. D., T. Zohary, J. Easton, B. Azoulay & T. Fishbein, 2001. Effects of zooplankton grazing and nutrients on the bloom-forming, N2-fixing cyanobacterium Aphanizomenon in Lake Kinneret. Journal of Plankton Research 23: 165–174.

    Article  Google Scholar 

  • Haney, J. F. & D. J. Hall, 1973. Sugar-coated Daphnia: a preservation technique for Cladocera. Limnology and Oceanography 18: 331–333.

    Article  Google Scholar 

  • Herzig, A. & B. Auer, 1990. The feeding behaviour of Leptodora kindti and its impact on the zooplankton community of Neusiedler See (Austria). Hydrobiologia 198 (Dev. Hydrobiol. 60): 107–117.

  • Jeschke, J. M. & R. Tollrian, 2000. Density-dependent effects of prey defences. Oecologia 123: 391–396.

    Article  Google Scholar 

  • Johansson, F. & E. Wahlstrom, 2002. Induced morphological defence: evidence from whole-lake manipulation experiments. Canadian Journal of Zoology 80: 199–206.

    Article  Google Scholar 

  • Kagami, M., T. Yoshida, T. Gurung & J. Urabe, 2002. Direct and indirect effects of zooplankton on algal composition in in situ grazing experiments. Oecologia 133: 356–363.

    Article  Google Scholar 

  • Kratina, P., E. Hammill & B. R. Anholt, 2010. Stronger inducible defences enhance persistence of intraguild prey. Journal of Animal Ecology 79: 993–999.

    Article  PubMed  Google Scholar 

  • Lacerot, G., C. Kruk, M. Lürling & M. Scheffer, 2013. The role of subtropical zooplankton as grazers of phytoplankton under different predation levels. Freshwater Biology 58: 494–503.

    Article  Google Scholar 

  • Laforsch, C., W. Ngwa, W. Grill & R. Tollrian, 2004. An acoustic microscopy technique reveals hidden morphological defenses in Daphnia. Proceedings of the National Academy of Sciences of the United States of America 101: 15911–15914.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lass, S. & P. Spaak, 2003. Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491: 221–239.

    Article  Google Scholar 

  • Lunte, C. C. & C. Luecke, 1990. Trophic interactions of Leptodora in Lake Mendota. Limnology and Oceanography 35: 1091–1100.

    Article  Google Scholar 

  • Marker, A. F., E. A. Nus, H. Rai & B. Riemann, 1980. The measurement of photosynthetic pigments in freshwater and standardization of methods: conclusions and considerations. Archiv für Hydrobiologie-Beiheft Ergebnisse der Limnologie 14: 91–106.

    CAS  Google Scholar 

  • Okamoto, K., 1984. Size-selective feeding of Daphnia longispina hyalina and Eodiaptomus japonicus on a natural phytoplankton assemblage with the fractionizing method. Memoirs of the Faculty of Science Kyoto University Series of Biology 9: 23–40.

    Google Scholar 

  • Ooms-Wilms, A. L., 1997. Are bacteria an important food source for rotifers in eutrophic lakes? Journal of Plankton Research 19: 1125–1141.

    Article  Google Scholar 

  • Parnell, A. C., R. Inger, S. Bearhop & A. L. Jackson, 2010. Source partitioning using stable isotopes: coping with too much variation. PLoS One 5: e9672.

    Article  PubMed Central  PubMed  Google Scholar 

  • Perga, M. E. & D. Gerdeaux, 2005. ‘Are fish what they eat’ all year round? Oecologia 144: 598–606.

    Article  CAS  PubMed  Google Scholar 

  • Perga, M. E. & D. Gerdeaux, 2006. Seasonal variability in the δ13C and δ15N values of the zooplankton taxa in two alpine lakes. Acta Oecologia 30: 69–77.

    Article  Google Scholar 

  • R Core Team, (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0 [http://www.R-project.org/]. Accessed 10 March 2014.

  • Raimondi, P. T., S. E. Forde, L. F. Delph & C. M. Lively, 2000. Processes structuring communities: evidence for trait-mediated indirect effects through induced polymorphisms. Oikos 91: 353–361.

    Article  Google Scholar 

  • Ramos-Jiliberto, R. & L. Garay-Narváez, 2007. Qualitative effects of inducible defenses in trophic chains. Ecological Complexity 4: 58–70.

    Article  Google Scholar 

  • Rosseel, Y., 2012. lavaan: an R package for structural equation modeling. Journal of Statistical Software 48: 1–36.

    Google Scholar 

  • Sakamoto, M. & T. Hanazato, 2009. Proximate factors controlling the morphologic plasticity of Bosmina: linking artificial laboratory treatments and natural conditions. Hydrobiologia 617: 171–179.

    Article  Google Scholar 

  • Sakamoto, M., K. H. Chang & T. Hanazato, 2006. Inhibition of development of anti-predator morphology in the small cladoceran Bosmina by an insecticide: impact of an anthropogenic chemical on prey-predator interactions. Freshwater Biology 51: 1974–1983.

    Article  CAS  Google Scholar 

  • Sakamoto, M., K. H. Chang & T. Hanazato, 2007. Plastic phenotypes of antennule shape in Bosmina longirostris controlled by physical stimuli from predators. Limnology and Oceanography 52: 2072–2078.

    Article  Google Scholar 

  • Sakamoto, M., Y. Ogamino & Y. Tanaka, 2010. Leptodora kindtii: a cladoceran species highly sensitive to toxic chemicals. Limnology 11: 193–196.

    Article  CAS  Google Scholar 

  • Satorra, A. & P. M. Bentler, 1994. Corrections to test statistics and standard errors in covariance structure analysis. In von Eye, A. & C. C. Clog (eds), Latent Variable Analysis: Applications for Developmental Research. Sage, Thousand Oaks, CA.

    Google Scholar 

  • Steiner, C. F., 2001. The effects of prey heterogeneity and consumer identity on the limitation of trophic-level biomass. Ecology 82: 2495–2506.

    Article  Google Scholar 

  • Syväranta, J., H. Hämäläinen & R. I. Jones, 2006. Within-lake variability in carbon and nitrogen stable isotope signatures. Freshwater Biology 51: 1090–1102.

    Article  Google Scholar 

  • Syväranta, J., P. Högmander, T. Keskinen, J. Karjalainen & R. I. Jones, 2011. Altered energy flow pathways in a lake ecosystem following manipulation of fish community structure. Aquatic Sciences 73: 79–89.

    Article  Google Scholar 

  • Tóth, L. G. & K. Kato, 1997. Size-selective grazing of bacteria by Bosmina longirostris – an image-analysis study. Journal of Plankton Research 19: 1477–1493.

    Article  Google Scholar 

  • Tollrian, R. & S. I. Dodson, 1999. Inducible defenses in Cladocera: constrains, costs, and multipredator environments. In Tollrian, R. & C. D. Harvell (eds), The ecology and evolution of inducible defenses. Princeton university press, New Jersey: 177–202.

    Google Scholar 

  • Tunney, T. D., K. S. McCann, N. P. Lester & B. J. Shuter, 2012. Food web expansion and contraction in response to changing environmental conditions. Nature Communications 3: 1105.

    Article  PubMed  Google Scholar 

  • Urabe, J., K. Kawabata, M. Nakanishi & K. Shimizu, 1996. Grazing and food size selection of zooplankton community in Lake Biwa during BITEX’93. Japanese Journal of Limnology 57: 27–37.

    Article  Google Scholar 

  • Van Der Stap, I., M. Vos, A. M. Verschoor, N. R. Helmsing & W. M. Mooij, 2007. Induced defenses in herbivores and plants differentially modulate a trophic cascade. Ecology 88: 2474–2481.

    Article  PubMed  Google Scholar 

  • Van Donk, E., A. Ianora & M. Vos, 2011. Induced defences in marine and freshwater phytoplankton: a review. Hydrobiologia 668: 3–19.

    Article  Google Scholar 

  • Vanderklift, M. A. & S. Ponsard, 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136: 169–182.

    Article  PubMed  Google Scholar 

  • Verschoor, A. M., M. Vos & I. van der Stap, 2004. Inducible defences prevent strong population fluctuations in bi-and tritrophic food chains. Ecology Letters 7: 1143–1148.

    Article  Google Scholar 

  • Vijverberg, J. & H. P. Koelewijn, 2004. Effect of temperature on development and growth of the raptorial cladoceran Leptodora kindtii under laboratory conditions. Freshwater Biology 49: 1415–1422.

    Article  Google Scholar 

  • Vijverberg, J., H. P. Koelewijn & W. L. T. van Densen, 2005. Effects of predation and food on the population dynamics of the raptorial cladoceran Leptodora kindtii. Limnology and Oceanography 50: 455–464.

    Article  Google Scholar 

  • Vos, M., B. W. Kooi, D. L. DeAngelis & W. M. Mooij, 2004. Inducible defences and the paradox of enrichment. Oikos 105: 471–480.

    Article  Google Scholar 

  • Vos, M., L. E. M. Vet, F. L. Wäckers, J. J. Middelburg, W. H. Van Der Putten, W. M. Mooij, et al., 2006. Infochemicals structure marine, terrestrial and freshwater food webs: implications for ecological informatics. Ecological Informatics 1: 23–32.

    Article  Google Scholar 

  • Yoshida, T., T. Gurung, M. Kagami & J. Urabe, 2001. Contrasting effects of a cladoceran (Daphnia galeata) and a calanoid copepod (Eodiaptomus japonicus) on algal and microbial plankton in a Japanese lake, Lake Biwa. Oecologia 129: 602–610.

    Article  CAS  PubMed  Google Scholar 

  • Yoshioka, T., E. Wada & H. Hayashi, 1994. A stable isotope study on seasonal food web dynamics in a eutrophic lake. Ecology 75: 835–846.

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr. H. D. Park for his helpful comments on this study. This study was supported by Grants-in-Aid to M. Sakamoto (No. 23510031) and to S. Kashiwada (No. 23310026) from Japan Society for the Promotion of Science.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masaki Sakamoto.

Additional information

Handling editor: Karl E. Havens

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sakamoto, M., Nagata, T., Ha, JY. et al. Inducible defenses as factor determining trophic pathways in a food web. Hydrobiologia 743, 15–25 (2015). https://doi.org/10.1007/s10750-014-1999-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-014-1999-x

Keywords

Navigation