Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

By mimicking the info-chemicals emitted by grazers, the common anionic surfactant sodium dodecyl sulfate (SDS) can induce colony formation in the green algal genus Scenedesmus at environmentally relevant concentrations. The morphometric effects can hinder the feeding efficiency of grazers, reducing energy flow along the pelagic food chain from Scenedesmus to consumers. Despite this potential ecological risk, few studies exist on whether the SDS-triggered induction of colonies is common in other species of the family Scenedesmaceae. Here, we investigated the effects of SDS on the growth and morphology of three species of Scenedesmaceae (Desmodesmus subspicatus, Scenedesmus acutus, and Tetradesmus dimorphus) and on the clearance rates of Daphnia galeata grazing on the SDS-induced colonies. SDS triggered colony formation in all algal species at concentrations nonlethal to them (0.1–10 mg L−1) in 72 h; however, the induction levels of colony formation were generally lower than for those in the Daphnia culture medium. We also found that the SDS-induced colonial algae reduced D. galeata clearance rates. Our results highlight the potential effect of SDS on the Daphnia–Scenedesmaceae system by triggering the morphological response of Scenedesmaceae at concentrations below those that exert toxicity. Such disruptive effects of pollutants on predator–prey interactions should be considered within the framework of ecological risk assessments.

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

Similar content being viewed by others

References

  • Aomura K, Ashidate N, Aisawa T, Fujita M, Goto K, Hasebe K, Hikime S, Ikehata A, Kawamura S, Kimura M et al (1981) Mizu no Bunseki. The Japan Society for Analytical Chemistry, Hokkaido, Kagaku-Dojin, Kyoto, pp 374–378

    Google Scholar 

  • Arenzon A, Pinto RF, Colombo P, Raya-Rodriguez MT (2003) Assessment of the freshwater annual fish Cynopoecilus melanotaenia as a toxicity test organism using three reference substances. Environ Toxicol Chem 22(9):2188–2190

    Article  CAS  Google Scholar 

  • Bondi CA, Marks JL, Wroblewski LB, Raatikainen HS, Lenox SR, Gebhardt KE (2015) Human and environmental toxicity of sodium lauryl sulfate (SLS): evidence for safe use in household cleaning products. Environ Health Insights 9:EHI-31765

    Article  Google Scholar 

  • Boyd RS (2010) Heavy metal pollutants and chemical ecology: exploring new frontiers. J Chem Ecol 36(1):46–58

    Article  CAS  Google Scholar 

  • Bulus Rossini GD, Ronco AE (1996) Acute toxicity bioassay using Daphnia obtusa as a test organism. Environ Toxicol Water Qual 11(3):255–258

    Article  CAS  Google Scholar 

  • Chawla G, Viswanathan PN, Devi S (1987) Biochemical studies on the toxicity of linear alkylbenzene sulphonate to Scenedesmus quadricauda in culture. Environ Exp Bot 27(3):311–323

    Article  CAS  Google Scholar 

  • Gerritsen J, Porter KG (1982) The role of surface chemistry in filter feeding by zooplankton. Science 216:1225–1227

    Article  CAS  Google Scholar 

  • Ha K, Jang MH, Takamura N (2004) Colony formation in planktonic algae induced by zooplankton culture media filtrate. J Freshw Ecol 19(1):9–16

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hemmer MJ, Barron MG, Greene RM (2010). Comparative toxicity of Louisiana sweet crude oil (LSC) and chemically dispersed LSC to two Gulf of Mexico aquatic test species. USEPA Dispersed Oil Toxicity Testing

  • Hessen DO, Van Donk E (1993) Morphological changes in Scenedesmus induced by substances released from Daphnia. Arch Hydrobiol 127:129–140

    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(2):625–634

    Article  Google Scholar 

  • Jackson M, Eadsforth C, Schowanek D, Delfosse T, Riddle A, Budgen N (2016) Comprehensive review of several surfactants in marine environments: fate and ecotoxicity. Environ Toxicol Chem 35(5):1077–1086

    Article  CAS  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(1):147–159

    Article  CAS  Google Scholar 

  • Lewis MA (1990) Chronic toxicities of surfactants and detergent builders to algae: a review and risk assessment. Ecotoxicol Environ Saf 20(2):123–140

    Article  CAS  Google Scholar 

  • Liwarska-Bizukojc E, Miksch K, Malachowska-Jutsz A, Kalka J (2005) Acute toxicity and genotoxicity of five selected anionic and nonionic surfactants. Chemosphere 58(9):1249–1253

    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 (2006) Effects of a surfactant (FFD-6) on Scenedesmus morphology and growth under different nutrient conditions. Chemosphere 62:1351–1358

    Article  Google Scholar 

  • Lürling M (2012). Infodisruption: pollutants interfering with the natural chemical information conveyance in aquatic systems. Brönmark C, Hansson LA (Eds.), Chemical Ecology in Aquatic Systems, Oxford University Press, New York, 250–271.

  • Lürling M, Beekman W (2002) Extractable substances (anionic surfactants) from membrane filters induce morphological changes in the green alga Scenedesmus obliquus (Chlorophyceae). Environ Toxicol Chem 21(6):1213–1218

    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(3):432–437

    Article  Google Scholar 

  • Lürling M, Van Donk E (2000) Grazer-induced colony formation in Scenedesmus: are there costs to being colonial? Oikos 88(1):111–118

    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(8):1881–1889

    Article  Google Scholar 

  • Mariani L, De Pascale D, Faraponova O, Tornambè A, Sarni A, Giuliani S, Ruggiero G, Onorati F, Magaletti E (2006) The use of a test battery in marine ecotoxicology: the acute toxicity of sodium dodecyl sulfate. Environ Toxicol 21(4):373–379

    Article  CAS  Google Scholar 

  • Marker AFH, Nusch EA, Rai H, Riemann B (1980) The measurement of photosynthetic pigments in freshwaters and standardization of methods: conclusions and recommendations. Archiv Für Hydrobiologie Beihefte Ergebnisse Der Limnologie 14:91–106

    CAS  Google Scholar 

  • Martínez-Jerónimo F, García-González R (1994) Effect of food concentration on the chronic toxicity of sodium dodecyl sulphate to Daphnia magna. J Aquat Ecosyst Health 3(4):247–253

    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 

  • Organisation for Economic Co-operation and Development (OECD) (2011). OECD guidelines for testing of chemicals, no. 201: Freshwater Alga and Cyanobacteria, Growth Inhibition Test. OECD, Paris

  • Reátegui-Zirena EG, Whatley A, Chu-Koo F, Stewart PM (2013) Acute toxicity testing of crude oil using Piaractus brachypomus, and Pimephales promelas. Int J Environ Protection 3(12):1

    Google Scholar 

  • Rebello S, Asok AK, Mundayoor S, Jisha MS (2014) Surfactants: toxicity, remediation and green surfactants. Environ Chem Lett 12(2):275–287

    Article  CAS  Google Scholar 

  • Ritz C, Cedergreen N, Jensen JE, Streibig JC (2006) Relative potency in nonsimilar dose–response curves. Weed Sci 54:407–412

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Shedd TR, Widder MW, Toussaint MW, Sunkel MC, Hull E (1999) Evaluation of the annual killifish Nothobranchius guentheri as a tool for rapid acute toxicity screening. Environ Toxicol Chem 18(10):2258–2261

    CAS  Google Scholar 

  • Van Donk E (2007) Chemical information transfer in freshwater plankton. Ecol Inform 2(2):112–120

    Article  Google Scholar 

  • Van Donk E, Peacor S, Grosser K, Domis LNDS, 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 91–105

  • Verschoor AM, Vos M, Van Der Stap I (2004) Inducible defences prevent strong population fluctuations in bi- and tritrophic food chains. Ecol Lett 7(12):1143–1148

    Article  Google Scholar 

  • Wheeler MW, Park RM, Bailer AJ (2006) Comparing median lethal concentration values using confidence interval overlap or ratio tests. Environ Toxicol Chem 25:1441–1444

    Article  CAS  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(28):4765–4767

    Article  CAS  Google Scholar 

  • Yasumoto K, Nishigami A, Kasai F, Kusumi T, Ooi T (2006) Isolation and absolute configuration determination of aliphatic sulfates as the Daphnia kairomones inducing morphological defense of a phytoplankton. Chem Pharm Bull 54:271–274

    Article  CAS  Google Scholar 

  • Yasumoto K, Nishigami A, Aoi H, Tsuchihashi C, Kasai F, Kusumi T, Ooi T (2008a) Isolation and absolute configuration determination of aliphatic sulfates as the Daphnia kairomones inducing morphological defense of a phytoplankton—Part 2. Chem Pharm Bull 56:129–132

    Article  CAS  Google Scholar 

  • Yasumoto K, Nishigami A, Aoi H, Tsuchihashi C, Kasai F, Kusumi T, Ooi T (2008b) Isolation of new aliphatic sulfates and sulfamate as the Daphnia kairomones inducing morphological change of a phytoplankton Scenedesmus gutwinskii. Chem Pharm Bull 56:133–136

    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 Roy Soc B Biol Sci 278(1704):458–463

    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 

  • Zhu X, Wang Z, Sun Y, Gu L, Zhang L, Wang J, Huang Y, Yang Z (2020) Surfactants at environmentally relevant concentrations interfere the inducible defense of Scenedesmus obliquus and the implications for ecological risk assessment. Environ Pollut 261:114131

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by a Grant-in-Aid for Japan Society for the Promotion of Sciences (JSPS) fellows (Grant No. JP20J11681). We thank Natalie Kim, PhD, from Edanz Group (https://en-author-services.edanz.com/ac) for editing a draft of this manuscript.

Author information

Authors and Affiliations

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

    Yusuke Oda

  2. Department of Environmental and Civil Engineering, Toyama Prefectural University, Imizu, Toyama, Japan

    Masaki Sakamoto

  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. Masaki Sakamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuichi Miyabara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yusuke Oda.

Ethics declarations

Conflict of interest

The authors declare they have no conflict of interests in relation to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oda, Y., Sakamoto, M. & Miyabara, Y. 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 (2022). https://doi.org/10.1007/s00244-021-00890-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-021-00890-8

Search

Navigation