Skip to main content
SpringerLink
Log in

Grazing inhibition in Daphnia and Bosmina by colony formation of Desmodesmus subspicatus triggered by sodium octyl sulfate

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

There are growing concerns that several aquatic contaminants can indirectly alter biological interactions by inhibiting the adaptive phenotypic plasticity of organisms, even at nonlethal concentrations. In Scenedesmaceae, a family of green algae, many chemicals interfere with defensive colony formation against grazers (i.e., through induced or limited coloniality). Although several studies have demonstrated that the effects of coloniality can limit the feeding capacity of Daphnia spp., grazing inhibition in other zooplankton species is not well understood. In this study, we examined the influence of sodium octyl sulfate (SOS) on the growth and morphology of Desmodesmus subspicatus and on the feeding rates of three cladoceran species (Daphnia galeata, Bosmina longirostris, and Bosmina fatalis) feeding on SOS-induced colonies under factorial conditions of different food levels and grazer ages. SOS remarkably induced colony formation with no observed effect on growth in D. subspicatus. D. galeata and B. fatalis showed a remarkable reduction in feeding rates when they fed on colonial D. subspicatus, whereas no significant effect of the prey morphotype was found on the feeding rates of B. longirostris. Microscopic observations of algal morphology after being grazed showed that each species can consume colonial prey depending on food level and age. Comparisons of the inhibition ratio of feeding among the three cladocerans revealed that Daphnia was more sensitive to prey coloniality compared with Bosmina. Our findings provide specific insights into the effects of chemically interfered colony formation on population dynamics and community structures.

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

Data availability

Data are available as supplemental.

References

  • Aomura K, Ashidate N, Aisawa T, et al. (1981) Mizu no Bunseki (in Japanese). The Japan Society for Analytical Chemistry, Hokkaido, Japan

  • Bennice CO, Conroy JD, Culver DA (2009) Decreasing trophic efficiency in cool-water aquaculture ponds: size-selective predation removes large prey. Aquac Res 40:582–589

    Article  Google Scholar 

  • Bleiwas AH, Stokes PM (1985) Collection of large and small food particles by Bosmina1. Limnol Oceanogr 30:1090–1092

    Article  Google Scholar 

  • Boyd RS (2010) Heavy metal pollutants and chemical ecology: exploring new frontiers. J Chem Ecol 36:46–58

    Article  CAS  Google Scholar 

  • Burns CW (1995) Effects of crowding and different food levels on growth and reproductive investment of Daphnia. Oecologia 101:234–244

    Article  Google Scholar 

  • Chang KH, Hanazato T (2003) Seasonal and spatial distribution of two Bosmina species (B. longirostris and B. fatalis) in Lake Suwa, Japan: its relation to the predator Leptodora. Limnology 4:0047–0052

    Article  CAS  Google Scholar 

  • Colina M, Calliari D, Carballo C, Kruk C (2016) A trait-based approach to summarize zooplankton–phytoplankton interactions in freshwaters. Hydrobiologia 767:221–233

    Article  CAS  Google Scholar 

  • DeMott WR (1982) Feeding selectivities and relative ingestion rates of Daphnia and Bosmina1. Limnol Oceanogr 27:518–527

    Article  Google Scholar 

  • DeMott WR, Kerfoot WC (1982) Competition among cladocerans: nature of the interaction between Bosmina and Daphnia. Ecology 63:1949–1966

    Article  Google Scholar 

  • Detmer TM, Wahl DH (2019) Trophic cascade strength is influenced by size frequency distribution of primary consumers and size-selective predation: examined with mesocosms and modeling. Aquat Sci 81:1–11

    Article  CAS  Google Scholar 

  • Geller W, Müller H (1981) The filtration apparatus of Cladocera: filter mesh-sizes and their implications on food selectivity. Oecologia 49:316–321

    Article  Google Scholar 

  • Gophen M, Geller W (1984) Filter mesh size and food particle uptake by Daphnia. Oecologia 64:408–412

    Article  Google Scholar 

  • Ha K, Jang MH, Takamura N (2004) Colony formation in planktonic algae induced by zooplankton culture media filtrate. J Freshw Ecol 19:9–16

    Article  Google Scholar 

  • Hanazato T (1995) Combined effect of the insecticide carbaryl and the Chaoborus kairomone on helmet development in Daphnia ambigua. Hydrobiologia 310:95–100

    Article  CAS  Google Scholar 

  • Hanazato T (1998) Response of a zooplankton community to insecticide application in experimental ponds: a review and the implications of the effects of chemicals on the structure and functioning of freshwater communities. Environ Pollut 101:361–373

    Article  CAS  Google Scholar 

  • Hanazato T (2001) Pesticide effects on freshwater zooplankton: an ecological perspective. Environ Pollut 112:1–10

    Article  CAS  Google Scholar 

  • Hanazato T, Arakawa T, Sakuma M, Chang KH, Okino T (2001) Zooplankton community in Lake Suwa: community structure and its role in the ecosystem. Jpn J Limnol 62:151–167

    Article  CAS  Google Scholar 

  • Hanazato T, Dodson SI (1995) Synergistic effects of low oxygen concentration, predator kairomone, and a pesticide on the cladoceran Daphnia pulex. Limnol Oceanogr 40:700–709

    Article  CAS  Google Scholar 

  • Hanazato T, Yasuno M (1987) Experimental studies on competition between Bosmina longirostris and Bosmina fatalis. Hydrobiologia 154:189–199

    Article  Google Scholar 

  • Haney JF, Hall DJ (1973) Sugar-coated Daphnia: a preservation technique for Cladocera1. Limnol Oceanogr 18:331–333

    Article  Google Scholar 

  • Helgen JC (1987) Feeding rate inhibition in crowded Daphnia pulex. Hydrobiologia 154:113–119

    Article  Google Scholar 

  • Hessen DO (1985) Filtering structures and particle size selection in coexisting Cladocera. Oecologia 66:368–372

    Article  Google Scholar 

  • Hessen DO, Van Donk E (1993) Morphological changes in Scenedesmus induced by substances released from Daphnia. Arch Hydrobiol 127:129–129

    Article  Google Scholar 

  • Huang Y, Nan H, Zhu X, Li B, Zhang Z, Yang Z (2016) Waterborne copper impairs grazer-induced colony formation and photosynthetic efficiency in Scenedesmus obliquus. Limnol Oceanogr 61:625–634

    Article  Google Scholar 

  • Kilham SS, Kreeger DA, Lynn SG, Goulden CE, Herrera L (1998) COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377:147–159

    Article  CAS  Google Scholar 

  • Korosi JB, Paterson AM, DeSellas AM, Smol JP (2010) A comparison of pre-industrial and present-day changes in Bosmina and Daphnia size structure from soft-water Ontario lakes. Can J Fish Aquat Sci 67:754–762

    Article  Google Scholar 

  • Kruk C, Huszar VLM, Peeters ETHM, Bonilla S, Costa L, Lürling M, Reynolds CS, Scheffer M (2010) A morphological classification capturing functional variation in phytoplankton. Freshw Biol 55:614–627

    Article  Google Scholar 

  • Labenia JS, Baldwin DH, French BL, Davis JW, Scholz NL (2007) Behavioral impairment and increased predation mortality in cutthroat trout exposed to carbaryl. Mar Ecol Prog Ser 329:1–11

    Article  CAS  Google Scholar 

  • Lürling M (2003) Phenotypic plasticity in the green algae Desmodesmus and Scenedesmus with special reference to the induction of defensive morphology. Annales de Limnologie Int J Limnol 39:85–101

    Article  Google Scholar 

  • Lürling M, De Lange HJ, Peeters E (2011) Effects of an anionic surfactant (FFD-6) on the energy and information flow between a primary producer (Scenedesmus obliquus) and a consumer (Daphnia magna). Ecotoxicology 20:1881–1889

    Article  Google Scholar 

  • Lürling M, Scheffer M (2007) Info-disruption: pollution and the transfer of chemical information between organisms. Trends Ecol Evol 22:374–379

    Article  Google Scholar 

  • Lürling M, Van Donk E (1996) Zooplankton-induced unicell-colony transformation in Scenedesmus acutus and its effect on growth of herbivore Daphnia. Oecologia 108:432–437

    Article  Google Scholar 

  • Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692

    Article  Google Scholar 

  • Nevalainen L, Ketola M, Korosi JB, Manca M, Kurmayer R, Koinig KA, Psenner R, Luoto TP (2014) Zooplankton (Cladocera) species turnover and long-term decline of Daphnia in two high mountain lakes in the Austrian Alps. Hydrobiologia 722:75–91

    Article  CAS  Google Scholar 

  • Oda Y, Sakamoto M, Miyabara Y (2022) Colony formation in three species of the family Scenedesmaceae (Desmodesmus subspicatus, Scenedesmus acutus, Tetradesmus dimorphus) exposed to sodium dodecyl sulfate and its interference with grazing of Daphnia galeata. Arch Environ Contam Toxicol 82:37–47

    Article  CAS  Google Scholar 

  • Oh HJ, Oda Y, Ha JY, Nagata T, Hanazato T, Miyabara Y, Sakamoto M, Chang KH (2019) Responses of daphnids and other zooplankton populations to massive fish kill in Lake Suwa. Ecol Res 34:856–863

    Article  Google Scholar 

  • Pan Y, Dong J, Wan L, Sun S, MacIsaac HJ, Drouillard KG, Chang X (2020) Norfloxacin pollution alters species composition and stability of plankton communities. J Hazard Mater 385:121625

    Article  CAS  Google Scholar 

  • Pan Y, Liu C, Li F, Zhou C, Yan S, Dong J, Li T, Duan C (2017) Norfloxacin disrupts Daphnia magna-induced colony formation in Scenedesmus quadricauda and facilitates grazing. Ecol Eng 102:255–261

    Article  Google Scholar 

  • Porter KG, Feig YS, Vetter EF (1983) Morphology, flow regimes, and filtering rates of Daphnia, Ceriodaphnia, and Bosmina fed natural bacteria. Oecologia 58:156–163

    Article  Google Scholar 

  • Ritz C, Strebig JC, Ritz MC (2016) Package ‘drc.’ Creative Commons, Mountain View, CA

  • Sakamoto M, Nagata T, Ha JY, Kimijima S, Hanazato T, Chang KH (2015) Inducible defenses as factor determining trophic pathways in a food web. Hydrobiologia 743:15–25

    Article  Google Scholar 

  • Schulz KL, Sterner RW (1999) Phytoplankton phosphorus limitation and food quality for Bosmina. Limnol Oceanogr 44:1549–1556

    Article  CAS  Google Scholar 

  • Scheffer M, Rinaldi S, Kuznetsov YA, Van Nes EH (1997) Seasonal dynamics of Daphnia and algae explained as a periodically forced predator-prey system. Oikos 80:519–532

    Article  Google Scholar 

  • Sommer U, Sommer F, Santer B, Zöllner E, Jürgens K, Jamieson C, Boersma M, Gocke K (2003) Daphnia versus copepod impact on summer phytoplankton: functional compensation at both trophic levels. Oecologia 135:639–647

    Article  Google Scholar 

  • Urabe J (1991) Effect of food concentration on the carbon balance of Bosmina longirostris (Crustacea: Cladocera). Freshw Biol 26:57–68

    Article  Google Scholar 

  • Van Donk E, Peacor S, Grosser K, Senerpont Domis LND, Lürling M (2016) Pharmaceuticals may disrupt natural chemical information flows and species interactions in aquatic systems: ideas and perspectives on a hidden global change. Rev Environ Contam Toxicol 23:91–105

    Google Scholar 

  • Verschoor AM, Vos M, Van Der Stap I (2004) Inducible defences prevent strong population fluctuations in bi- and tritrophic food chains. Ecol Lett 7:1143–1148

    Article  Google Scholar 

  • Yasumoto K, Nishigami A, Yasumoto M, Kasai F, Okada Y, Kusumi T, Ooi T (2005) Aliphatic sulfates released from Daphnia induce morphological defense of phytoplankton: isolation and synthesis of kairomones. Tetrahedron Lett 46:4765–4767

    Article  CAS  Google Scholar 

  • Yokota K, Sterner RW (2011) Trade-offs limiting the evolution of coloniality: ecological displacement rates used to measure small costs. Proc R Soc B Biol Sci 278:458–463

    Article  Google Scholar 

  • Wan L, Long Y, Hui J, Zhang H, Hou Z, Tan J, Pan Y, Sun S (2020) Effect of norfloxacin on algae–cladoceran grazer–larval damselfly food chains: algal morphology-mediated trophic cascades. Chemosphere 256:127166

    Article  CAS  Google Scholar 

  • Wei W, Zhang K, Shi Q (2021) Complete mitochondrial genome of Bosmina fatalis (Cladocera: Bosminidae) and its phylogenetic analysis. Mitochondrial DNA Part B 6:2567–2568

    Article  Google Scholar 

  • Wu X, Zhang J, Qin B, Cui G, Yang Z (2013) Grazer density-dependent response of induced colony formation of Scenedesmus obliquus to grazing-associated infochemicals. Biochem Syst. Ecology 50:286–292

    CAS  Google Scholar 

  • Zhu X, Sun Y, Zhang X, Heng H, Nan H, Zhang L, Huang Y, Yang Z (2016) Herbicides interfere with antigrazer defenses in Scenedesmus obliquus. Chemosphere 162:243–251

    Article  CAS  Google Scholar 

  • Zhu X, Wang Y, Hou X, Kong Q, Sun Y, Wang J, Huang Y, Yang Z (2019) High temperature promotes the inhibition effect of Zn2+ on inducible defense of Scenedesmus obliquus. Chemosphere 216:203–212

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by a Grant-in-Aid from the Japan Society for the Promotion of Sciences (JSPS) (Grant No. JP20J11681). We thank Dr. Masaki Sakamoto for providing helpful comments on the drafting of the manuscript.

Author information

Authors and Affiliations

  1. Department of Science and Technology, Shinshu University, Matsumoto, Nagano, Japan

    Yusuke Oda

  2. Center for Health and Environmental Risk Research, National Institute for Environmental Studies, Tsukuba, Ibaraki, Japan

    Yusuke Oda

  3. Suwa Hydrobiological Station, Faculty of Science, Shinshu University, Suwa, Nagano, Japan

    Yuichi Miyabara

  4. Institute of Mountain Science, Shinshu University, Minamiminowa, Nagano, Japan

    Yuichi Miyabara

Authors
  1. Yusuke Oda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuichi Miyabara
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YO, YM conceived the study, YO designed the study, YO carried out the experiment, YO analyzed the data; YO, YM wrote the manuscript, and all authors edited the manuscript.

Corresponding author

Correspondence to Yusuke Oda.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oda, Y., Miyabara, Y. Grazing inhibition in Daphnia and Bosmina by colony formation of Desmodesmus subspicatus triggered by sodium octyl sulfate. Ecotoxicology 32, 884–894 (2023). https://doi.org/10.1007/s10646-023-02694-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-023-02694-z

Keywords

Search

Navigation