Skip to main content
SpringerLink
Log in

Long-term continuous mismatch between grazing cues and real grazing losses causes attenuation of induced morphological defense in Scenedesmus

  • Research
  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

For the freshwater phytoplankton Scenedesmus, morphological defense induced by infochemicals released from grazers (such as Daphnia) is considered to be a defensive strategy. In this study, we investigated the response of Scenedesmus obliquus to long-term repeated grazing infochemicals exposure, with two stimulation intervals (short period of 4 days and long period of 7 days per round). Results demonstrated that the defensive response of S. obliquus gradually degenerated with periodically repeated exposure to Daphnia infochemicals and the degeneration rate was positively correlated with stimulation frequency, that is, shorter intervals caused a faster decrease in average algal colony size. According to nonlinear regression fitting, a harmonic oscillator function with exponential attenuation could be applied to illustrate S. obliquus morph changes, with which the growth rate was positively correlated. Our study suggests that the optimal defensive colony size in S. obliquus might depend on trade-offs between its anti-grazing defense and other functions. This insight contributes to the understanding of algal inducible defense mechanism, serving as a complement to the optimal defense theory. Additionally, long-term periodic grazing threats without causing concrete damage may disrupt feedback mechanisms and real biomass loss is assumed to be an important precondition for sustaining enduring defensive phenotypes.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 7

Similar content being viewed by others

Data availability

Data are available from the authors upon reasonable request.

References

  • Agrawal AA (1998) Algal defense, grazers, and their interactions in aquatic trophic cascades. Acta Oecol 19:331–337

    Article  Google Scholar 

  • Brown ER, Kubanek J (2020) Harmful alga trades off growth and toxicity in response to cues from dead phytoplankton. Limnol Oceanogr 65:1723–1733

    Article  CAS  Google Scholar 

  • Chen H, Zhang Y, He C, Wang Q (2014) Ca2+ signal transduction related to neutral lipid synthesis in an oil-producing green alga Chlorella sp. C2. Plant Cell Physiol 55:634–644

    Article  CAS  PubMed  Google Scholar 

  • Conrath U, Thulke O, Katz V, Schwindling S, Kohler A (2001) Priming as a mechanism in induced systemic resistance of plants. Eur J Plant Pathol 107:113–119

    Article  CAS  Google Scholar 

  • Fadzly N, Burns KC (2010) Hiding from the ghost of herbivory past: Evidence for crypsis in an insular tree species. Int J Plant Sci 171:828–833

    Article  Google Scholar 

  • Gagliano M, Renton M, Depczynski M, Mancuso S (2014) Experience teaches plants to learn faster and forget slower in environments where it matters. Oecologia 175:63–72

    Article  PubMed  Google Scholar 

  • Grønning J, Kiørboe T (2020) Diatom defence: Grazer induction and cost of shell-thickening. Funct Ecol 34:1790–1801

    Article  Google Scholar 

  • Gross S, Kourtchenko O, Rajala T, Andersson B, Fernandez L, Blomberg A, Godhe A (2017) Optimization of a high-throughput phenotyping method for chain-forming phytoplankton species. Limnol Oceanogr Methods 16:57–67

    Article  Google Scholar 

  • Haavisto F, Jormalainen V (2019) Water-borne defence induction of a rockweed in the wild. Funct Ecol 33:786–797

    Article  Google Scholar 

  • Hahn M, Moore E, Höfle M (2000) Role of microcolony formation in the protistan grazing defense of the aquatic bacterium Pseudomonas sp. Microb Ecol 39:175–185

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hoverman JT, Relyea RA (2012) The long-term impacts of predators on prey: Inducible defenses, population dynamics, and indirect effects. Oikos 121:1219–1230

    Article  Google Scholar 

  • Huang Y, Cui G, Li B, Zhu X, Yang Z (2017) Elevated atmospheric CO2 enhances grazer-induced morphological defense in the freshwater green alga Scenedesmus obliquus. Limnol Oceanogr 63:1004–1014

    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 

  • Huntzinger M, Karban R, Young TP, Palmer TM (2004) Relaxation of induced indirect defenses of Acacias following exclusion of mammalian herbivores. Ecology 85:609–614

    Article  Google Scholar 

  • Jia XH, Pan YQ, Zhu XX (2023) Salinization and heavy metal cadmium impair growth but have contrasting effects on defensive colony formation of Scenedesmus obliquus. Sci Total Environ 862:160693

    Article  CAS  PubMed  Google Scholar 

  • Joseph E, Kaycey P, Glanzman DL (2010) Long-term habituation of the gill-withdrawal reflex in Aplysia requires gene transcription, calcineurin and L-type voltage-gated calcium channels. Front Behav Neurosci 4:181

    Google Scholar 

  • Lampert W, Rothhaupt KO, von Elert E (1994) Chemical induction of colony formation in a green alga (Scenedesmus acutus) by grazers (Daphnia). Limnol Oceanogr 39:1543–1550

    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. Ann Limnol - Int J Limnol 39:85–101

    Article  Google Scholar 

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

    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  PubMed  Google Scholar 

  • Lürling M, Van Donk E, Beekman-Lukassen W (2000) Algal concentration affects grazer-induced colony formation in Scenedesmus. Verh Int Verein Limnol 27:2124–2127

    Google Scholar 

  • Matulich KL, Carroll IT, Cardinale BJ (2009) Priority effects: initial densities alter exponential growth rates of competing species. In: 94th Ecological Society of America Annual Meeting, Albuquerque, NM, USA

  • Mirouze M, Paszkowski J (2011) Epigenetic contribution to stress adaptation in plants. Curr Opin Plant Biol 14:267–274

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell DR, Fey SB, Cottingham KL (2013) Nutrient availability influences kairomone-induced defenses in Scenedesmus acutus (Chlorophyceae). J Plankton Res 35:191–200

    Article  CAS  Google Scholar 

  • Park G, Dam H (2021) Cell-growth gene expression reveals a direct fitness cost of grazer-induced toxin production in red tide dinoflagellate prey. Proc R Soc B 288:2480

    Article  Google Scholar 

  • Park G, Norton L, Avery D, Dam HG (2023) Grazers modify the dinoflagellate relationship between toxin production and cell growth. Harmful Algae 126:102439

    Article  CAS  PubMed  Google Scholar 

  • Perisse E, Raymond-Delpech V, Néant I, Matsumoto Y, Leclerc C, Moreau M, Sandoz JC (2009) Early calcium increase triggers the formation of olfactory long-term memory in honeybees. BMC Biol 7:30

    Article  PubMed  PubMed Central  Google Scholar 

  • Reynolds CS (2006) Ecology of phytoplankton. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Roccuzzo S, Couto N, Karunakaran E, Kapoore RV, Butler TO, Mukherjee J, Hansson EM, Beckerman AP, Pandhal J (2020) Metabolic insights into infochemicals induced colony formation and flocculation in Scenedesmus subspicatus unraveled by quantitative proteomics. Front Microbiol 11:792

    Article  PubMed  PubMed Central  Google Scholar 

  • Rzymski P, Klimaszyk P, Jurczak T, Poniedziałek B (2020) Oxidative stress, programmed cell death and microcystin release in Microcystis aeruginosa in response to Daphnia grazers. Front Microbiol 11:1201

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun YF, Zhang XX, Zhang L, Huang Y, Yang Z, Montagnes D (2020) UVB radiation suppresses antigrazer morphological defense in Scenedesmus obliquus by inhibiting algal growth and carbohydrate-regulated gene expression. Environ Sci Technol 54:4495–4503

    Article  CAS  PubMed  Google Scholar 

  • Tollrian R, Duggen S, Weiss LC, Laforsch C, Kopp M (2015) Density-dependent adjustment of inducible defenses. Sci Rep 5:12736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Van Holthoon FL (2004) Isolation and identification of kairomone(s) in the Daphnia-scenedesmus system. Dissertation, Wageningen University

  • Verschoor AM, Bekmezci OK, Van Donk E, Vijverberg J (2009) The ghost of herbivory past: Slow defence relaxation in the chlorophyte Scenedesmus obliquus. J Limnol 68:327–335

    Article  Google Scholar 

  • Via S, Gomulkiewicz R, Jong GD, Scheiner SM, Schlichting CD, Tienderen PHV (1995) Adaptive phenotypic plasticity: Consensus and controversy. Trends Ecol Evol 10:212–217

    Article  CAS  PubMed  Google Scholar 

  • Wheeler GL, Brownlee C (2008) Ca signalling in plants and green algae – changing channels. Trends Plant Sci 13:506–514

    Article  CAS  PubMed  Google Scholar 

  • Wiackowski K, Starońska A (1999) The effect of predator and prey density on the induced defence of a ciliate. Funct Ecol 13:59–65

    Article  Google Scholar 

  • Yang Z, Kong FX, Shi XL, Xing P, Zhang M (2007) Effects of Daphnia-associated infochemicals on the morphology, polysaccharides content and PSII-efficiency in Scenedesmus obliquus. Int Rev Hydrobiol 92:618–625

    Article  Google Scholar 

  • Zachleder V, Bišová K, Vítová M, Kubín Š, Hendrychová J (2002) Variety of cell cycle patterns in the alga Scenedesmus quadricauda (Chlorophyta) as revealed by application of illumination regimes and inhibitors. Eur J Phycol 37:361–371

    Article  Google Scholar 

  • Zangerl AR, Rutledge CE (1996) The probability of attack and patterns of constitutive and induced defense - a test of optimal defense theory. Am Nat 147:599–608

    Article  Google Scholar 

  • Zhu XX, Nan H, Chen Q, Wu Z, Wu X, Yuan H, Zhou Y (2015a) Potential grazing intensity directly determines the extent of grazer-induced colony formation in Scenedesmus obliquus. Biochem Syst Ecol 61:271–277

    Article  CAS  Google Scholar 

  • Zhu XX, Sun YF, Zhang L, Wang J, Gu L, Huang Y, Yang Z (2021) Multi-omics reveal the pathways involved in induced defensive colony formation of Tetradesmus obliquus in response to Daphnia grazing cues. Limnol Oceanogr 66:1819–1831

    Article  CAS  Google Scholar 

  • Zhu XX, Wang J, Chen Q, Chen G, Huang Y, Yang Z (2016) Costs and trade-offs of grazer-induced defenses in Scenedesmus under deficient resource. Sci Rep 6:22594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu XX, 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  PubMed  Google Scholar 

  • Zhu XX, Wang J, Lu Y, Chen Q, Yang Z (2015b) Grazer-induced morphological defense in Scenedesmus obliquus is affected by competition against Microcystis aeruginosa. Sci Rep 5:12743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Ran Wang for the collaboration in modelling.

Funding

This study was supported by the National Natural Science Foundation of China (32101290, 32271626) and Natural Science Foundation of Jiangsu Province (BK20210364).

Author information

Authors and Affiliations

  1. Jiangsu Key Laboratory for Biodiversity and Biotechnology, School of Biological Sciences, Nanjing Normal University, 1 Wenyuan Road, Nanjing, 210023, China

    Xuexia Zhu, Yunfei Sun, Yuan Huang, Jun Wang & Zhou Yang

  2. College of Animal Science and Technology, Yangzhou University, Yangzhou, 225009, China

    Xuexia Zhu & Jun Wang

Authors
  1. Xuexia Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yunfei Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuan Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhou Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Z.Y. conceptualized and designed the experiment together with X.Z. Experiments were conducted by X.Z., Y.S., and J.W. Data analyses were performance by X.Z., H.Y., J.W., and Z.Y. The first draft of the manuscript was written by X.Z. and improved by Z.Y. All authors have read the final version of the article.

Corresponding authors

Correspondence to Jun Wang or Zhou Yang.

Ethics declarations

Competing interests

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.

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

Zhu, X., Sun, Y., Huang, Y. et al. Long-term continuous mismatch between grazing cues and real grazing losses causes attenuation of induced morphological defense in Scenedesmus. J Appl Phycol 36, 1353–1362 (2024). https://doi.org/10.1007/s10811-023-03174-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-023-03174-x

Keywords

Search

Navigation