Skip to main content
SpringerLink
Log in

A perspective on the current status of approaches for early detection of microalgal grazing

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

Abstract

Consumption of microalgae, as prey, by predatory zooplankton is a major ecological process in aquatic environments. The presence of predators in large-scale cultivation, such as in open ponds, results in a devastating loss of microalgal biomass, often referred to as a “pond crash.” Reported biomass losses of 20–30% due to predator invasion in open cultivation systems is one of the bottlenecks in achieving a desired economically viable system. Many commercial scale algal cultivation setups have reported clearance of prey within 2–5 days after detection of predators. Knowledge of how to monitor and manage algal pests is limited. Research to date is largely driven towards the development of predator mitigation strategies, whereas monitoring is mainly limited to traditional (direct) methods such as microscopy- and oligonucleotide-based screening. Use of online and real-time measures for in situ estimation of microalgal grazing is sparsely reported. We suggest that more knowledge about microalgal grazing at the pond level is required for the development of indirect screening measures, based on unique features of microalgal prey and predator interactions, to enable online monitoring. This article systematically reviews the current status of available methods, both at laboratory and field level, for early detection of microalgal grazing.

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

Similar content being viewed by others

References

  • Bartley ML, Boeing WJ, Corcoran AA, Holguin FO, Schaub T (2013) Effects of salinity on growth and lipid accumulation of biofuel microalga Nannochloropsis salina and invading organisms. Biomass Bioenergy 54:83–88

    CAS  Google Scholar 

  • Bilanovic D, Andargatchew A, Kroeger T, Shelef G (2009) Freshwater and marine microalgae sequestering of CO2 at different C and N concentrations – response surface methodology analysis. Energy Convers Manag 50:262–267

    CAS  Google Scholar 

  • Borowitzka MA (1999) Commercial production of microalgae: ponds, tanks, tubes and fermenters. J Biotechnol 70:313–321

    CAS  Google Scholar 

  • Borowitzka MA (2013) Energy from microalgae: a short history. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy. Springer, Dordrecht, pp 1–15

    Google Scholar 

  • Borowitzka MA, Moheimani NR (2013) Open pond culture systems. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy. Springer, Dordrecht, pp 133–152

  • Bravo I, Figueroa R (2014) Towards an ecological understanding of dinoflagellate cyst functions. Microorganisms 2:11–32

    PubMed  PubMed Central  Google Scholar 

  • Brussaard CP (2004) Viral control of phytoplankton populations—a review. J Eukaryot Microbiol 51:125–138

    PubMed  Google Scholar 

  • Carney LT, Lane TW (2014) Parasites in algae mass culture. Front Microbiol 5:278–286

    PubMed  PubMed Central  Google Scholar 

  • Carney LT, Reinsch SS, Lane PD, Solberg OD, Jansen LS, Williams KP, Trent JD, Lane TW (2014) Microbiome analysis of a microalgal mass culture growing in municipal wastewater in a prototype OMEGA photobioreactor. Algal Res 4:52–61

    Google Scholar 

  • Carney LT, Wilkenfeld JS, Lane PD, Solberg OD, Fuqua ZB, Cornelius NG, Gillespie S, Williams KP, Samocha TM, Lane TW (2016) Pond crash forensics: presumptive identification of pond crash agents by next generation sequencing in replicate raceway mass cultures of Nannochloropsis salina. Algal Res 17:341–347

    Google Scholar 

  • Collins AM, Jones HD, McBride RC, Behnke C, Timlin JA (2014) Host cell pigmentation in Scenedesmus dimorphus as a beacon for nascent parasite infection. Biotechnol Bioeng 111:1748–1757

    CAS  PubMed  Google Scholar 

  • Crofts AR (1967) Amine uncoupling of energy transfer in chloroplasts. I. Relation to ammonium ion uptake. J Biol Chem 242:3352–3359

    CAS  PubMed  Google Scholar 

  • Dagenais-Bellefeuille S, Morse D (2013) Putting the N in dinoflagellates. Front Microbiol 4:369–683

    PubMed  PubMed Central  Google Scholar 

  • Damiani MC, Leonardi PI, Pieroni OI, Cáceres EJ (2006) Ultrastructure of the cyst wall of Haematococcus pluvialis (Chlorophyceae): wall development and behaviour during cyst germination. Phycologia 45:616–623

    Google Scholar 

  • Davis R, Markham J, Kinchin C, Grundl N, Tan EC, Humbird D (2016) Process design and economics for the production of algal biomass: algal biomass production in open pond systems and processing through dewatering for downstream conversion. Laboratory NREL, Golden, Colorado. NREL/TP-5100-64772 pp 1–112

  • Dawidziuk A, Popiel D, Luboinska M, Grzebyk M, Wisniewski M, Koczyk G (2017) Assessing contamination of microalgal astaxanthin producer Haematococcus cultures with high-resolution melting curve analysis. Microb Genet 58:277–285

    CAS  Google Scholar 

  • Day JG, Thomas NJ, Achilles-Day UE, Leakey RJ (2012) Early detection of protozoan grazers in algal biofuel cultures. Bioresour Technol 114:715–719

    CAS  PubMed  Google Scholar 

  • Day JG, Gong Y, Hu Q (2017) Microzooplanktonic grazers – a potentially devastating threat to the commercial success of microalgal mass culture. Algal Res 27:356–365

    Google Scholar 

  • Dean AP, Nicholson JM, Sigee DC (2012) Changing patterns of carbon allocation in lake phytoplankton: an FTIR analysis. Hydrobiologia 684:109–127

    CAS  Google Scholar 

  • Deglint JL, Jin C, Wong A (2018) Investigating the automatic classification of algae using fusion of spectral and morphological characteristics of algae via deep residual learning. https://arxiv.org/abs/1810.10889

  • Deore P, Beardall J, Noronha S (2020a) Non-photochemical quenching, a non-invasive probe for monitoring microalgal grazing: influence of grazing-mediated total ammonia-nitrogen. Appl Phycol 1:32–43

    Google Scholar 

  • Deore P, Karthikaichamy A, Beardall J, Noronha S (2020b) Non-photochemical quenching, a non-invasive probe for monitoring microalgal grazing: an early indicator of predation by Oxyrrhis marina and Euplotes sp. Appl Phycol 1:20–31

    Google Scholar 

  • Di Caprio F (2020) Methods to quantify biological contaminants in microalgae cultures. Algal Res 49:101943

    Google Scholar 

  • Ding Y, Peng X, Wang Z, Wen X, Geng Y, Zhang D, Li Y (2018) Occurrence and characterization of an epibiotic parasite in cultures of oleaginous microalga Graesiella sp. WBG-1. J Appl Phycol 30:819–830

    CAS  Google Scholar 

  • Ferrell J, Sarisky-Reed V (2010) National algal biofuels technology roadmap. U.S. Department of Energy Biomass program, Maryland, USA. DOE/EE-03324329 pp 1–124.

  • Flynn KJ, Kenny P, Mitra A (2017) Minimising losses to predation during microalgae cultivation. J Appl Phycol 29:1829–1840

    PubMed  PubMed Central  Google Scholar 

  • Fott B (1967) Phlyctidium scenedesmi spec. nova, a new chytrid destroying mass cultures of algae. Z Allgem Mikrobiol 7:97–102

    CAS  Google Scholar 

  • Fulbright SP, Dean MK, Wardle G, Lammers PJ, Chisholm S (2014) Molecular diagnostics for monitoring contaminants in algal cultivation. Algal Res 4:41–51

    Google Scholar 

  • Fundel B, Stich H, Schmid H, Maier G (1998) Can phaeopigments be used as markers for Daphnia grazing in Lake Constance. J Plankton Res 20:1449–1462

    Google Scholar 

  • Gachon CM, Sime-Ngando T, Strittmatter M, Chambouvet A, Kim GH (2010) Algal diseases: spotlight on a black box. Trends Plant Sci 15:633–640

    CAS  PubMed  Google Scholar 

  • Ganuza E, Sellers CE, Bennett BW, Lyons EM, Carney LT (2016) A novel treatment protects Chlorella at commercial scale from the predatory bacterium Vampirovibrio chlorellavorus. Front Microbiol 7:848–861

    PubMed  PubMed Central  Google Scholar 

  • Gerphagnon M, Latour D, Colombet J, Sime-Ngando T (2013) A double staining method using SYTOX green and calcofluor white for studying fungal parasites of phytoplankton. Appl Environ Microbiol 79:3943–3951

    CAS  PubMed  PubMed Central  Google Scholar 

  • Giordano M, Ratti S, Domenighini A, Vogt F (2009) Spectroscopic classification of 14 different microalga species: first steps towards spectroscopic measurement of phytoplankton biodiversity. Plant Ecol Divers 2:155–164

    Google Scholar 

  • Guo F, Kainz M, Sheldon F, Bunn S (2016) The importance of high-quality algal food sources in stream food webs - current status and future perspectives. Freshw Biol 61:815–831

    CAS  Google Scholar 

  • Gutman J, Zarka A, Boussiba S (2009) The host-range of Paraphysoderma sedebokerensis, a chytrid that infects Haematococcus pluvialis. Eur J Phycol 44:509–514

  • Hansen PJ, BjØrnsen PK, Hansen BW (2000) Zooplankton grazing and growth: scaling within the 2–2,000-μm body size range. Limnol Oceanogr 45:1891–1891

    Google Scholar 

  • Havlik I, Reardon KF, Ünal M, Lindner P, Prediger A, Babitzky A, Beutel S, Scheper T (2013) Monitoring of microalgal cultivations with on-line, flow-through microscopy. Algal Res 2:253–257

    Google Scholar 

  • Jeffrey LCW (2011) The occurrence of ergosterol and (22E,24R)-24-ethylcholesta-5,7,22-trien-3β-ol in the unicellular chlorophyte Dunaliella tertiolecta. Can J Chem 57:2569–2571

    Google Scholar 

  • Kansiz M, Heraud P, Wood B, Burden F, Beardall J, McNaughton D (1999) Fourier transform infrared microspectroscopy and chemometrics as a tool for the discrimination of cyanobacterial strains. Phytochemistry 52:407–417

    CAS  Google Scholar 

  • Karuppasamy S, Musale AS, Soni B, Bhadra B, Gujarathi N, Sundaram M, Sapre A, Dasgupta S, Kumar C (2018) Integrated grazer management mediated by chemicals for sustainable cultivation of algae in open ponds. Algal Res 35:439–448

    Google Scholar 

  • Knoshaug EP, Wolfrum E, Laurens LM, Harmon VL, Dempster TA, McGowen J (2018) Unified field studies of the algae testbed public-private partnership as the benchmark for algae agronomics. Sci Data 5:180267–180277

    PubMed  PubMed Central  Google Scholar 

  • Lammers PJ, Huesemann M, Boeing W, Anderson DB, Arnold RG, Bai X, Bhole M, Brhanavan Y, Brown L, Brown J (2017) Review of the cultivation program within the National Alliance for Advanced Biofuels and Bioproducts. Algal Res 22:166–186

    Google Scholar 

  • Lane T, Poorey K, Geng H, Curtis DJ, Carney LT (2016) Algal crop protection strategies and technologies. Sandia National Laboratory, Livermore, United States. SAND2016-8236C

  • Ma M, Yuan D, He Y, Park M, Gong Y, Hu Q (2017) Effective control of Poterioochromonas malhamensis in pilot-scale culture of Chlorella sorokiniana GT-1 by maintaining CO2-mediated low culture pH. Algal Res 26:436–444

    Google Scholar 

  • Ma M, Gong Y, Hu Q (2018) Identification and feeding characteristics of the mixotrophic flagellate Poterioochromonas malhamensis, a microalgal predator isolated from outdoor massive Chlorella culture. Algal Res 29:142–153

    Google Scholar 

  • Maes D, Reichardt TA, Jensen TJ, Dempster TA, McGowen JA, Poorey K, Hipple T, Lane T, Timlin JA (2018) Spectroradiometric detection of competitors and predators in algal ponds. Sandia National Laboratory, Albuquerque,United States. SAND2018-6164C

  • Mansour MP, Volkman JK, Jackson AE, Blackburn SI (2002) The fatty acid and sterol composition of five marine dinoflagellates. J Phycol 35:710–720

    Google Scholar 

  • McBride RC, Lopez S, Meenach S, Burnett M, Lee PA, Nohilly F, Behnke C (2014) Contamination management in low cost open algae ponds for biofuels production. Ind Biotechnol 10:221–227

    Google Scholar 

  • McGowen J, Knoshaug EP, Laurens LM, Dempster TA, Pienkos PT, Wolfrum E, Harmon VL (2017) The Algae Testbed Public-Private Partnership (ATP3) framework; establishment of a national network of testbed sites to support sustainable algae production. Algal Res 25:168–177

    Google Scholar 

  • Montagna PA (1995) Rates of metazoan meiofaunal microbivory: a review. Vie et Milieu 45:1–10

    Google Scholar 

  • Moreno-Garrido I, Cañavate JP (2001) Assessing chemical compounds for controlling predator ciliates in outdoor mass cultures of the green algae Dunaliella salina. Aquac Eng 24:107–114

    Google Scholar 

  • Müller P, Li X, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

  • Murphy TE, Macon K, Berberoglu H (2013) Rapid algal culture diagnostics for open ponds using multispectral image analysis. Biotechnol Prog 30:233–240

    PubMed  Google Scholar 

  • Natchimuthu S, Chinnaraj P, Parthasarathy S, Senthil K (2013) Automatic identification of algal community from microscopic images. Bioinf Biol Insights 7:327–334

    Google Scholar 

  • Park S-H, Steichen SA, Li X, Ogden K, Brown JK (2019) Association of Vampirovibrio chlorellavorus with decline and death of Chlorella sorokiniana in outdoor reactors. J Appl Phycol 31:1131–1142

    CAS  Google Scholar 

  • Post FJ, Borowitzka LJ, Borowitzka MA, Mackay B, Moulton T (1983) The protozoa of a Western Australian hypersaline lagoon. Hydrobiologia 105:95–113

    Google Scholar 

  • Poulton NJ, Martin JL (2010) Imaging flow cytometry for quantitative phytoplankton analysis-FlowCAM. In: Karlson B, Cusack C, Bresnan E (eds) Microscopic and molecular methods for quantitative phytoplankton analysis. UNESCO, Paris, pp 47–53

    Google Scholar 

  • Rasconi S, Jobard M, Jouve L, Sime-Ngando T (2009) Use of calcofluor white for detection, identification, and quantification of phytoplanktonic fungal parasites. Appl Environ Microbiol 75:2545–2553

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ratti S, Knoll AH, Giordano M (2013) Grazers and phytoplankton growth in the oceans: an experimental and evolutionary perspective. PLoS One 8:e77349

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reese KL, Fisher CL, Lane PD, Jaryenneh JD, Moorman MW, Jones AD, Frank M, Lane TW (2019) Chemical profiling of volatile organic compounds in the headspace of algal cultures as early biomarkers of algal pond crashes. Sci Rep 9:1–10

    CAS  Google Scholar 

  • Reichardt TA, Collins AM, McBride RC, Behnke CA, Timlin JA (2014) Spectroradiometric monitoring for open outdoor culturing of algae and cyanobacteria. Appl Opt 53:31–45

    Google Scholar 

  • Reichardt TA, Maes D, Jensen T, Dempster TA, McGowen JA, Poorey K, Curtis DJ, Lane TW, Timlin J (2020) Spectroradiometric monitoring of competitor diatoms and the grazer Poteriochromonas in algal cultures. Algal Res 51:102020

    Google Scholar 

  • Richardson JW, Johnson MD, Zhang X, Zemke P, Chen W, Hu Q (2014) A financial assessment of two alternative cultivation systems and their contributions to algae biofuel economic viability. Algal Res 4:96–104

    Google Scholar 

  • Richmond A (ed) (2004) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Science Ltd, Oxford

  • Rogers JN, Rosenberg JN, Guzman BJ, Oh VH, Mimbela LE, Ghassemi A, Betenbaugh MJ, Oyler GA, Donohue MD (2014) A critical analysis of paddlewheel-driven raceway ponds for algal biofuel production at commercial scales. Algal Res 4:76–88

    Google Scholar 

  • Ruiz J, Olivieri G, de Vree J, Bosma R, Willems P, Reith J, Eppink M, Kleinegris D, Wijffels R, Barbosa M (2016) Towards industrial products from microalgae. Energy Environ Sci 9:3036–3043

    Google Scholar 

  • Samantaray A, Yang B, Dietz JE, Min BC (2018) Algae detection using computer vision and deep learning. https://arxiv.org/abs/1811.10847

  • Sandnes JM, Ringstad T, Wenner D, Heyerdahl PH, Kallqvist T, Gislerød HR (2006) Real-time monitoring and automatic density control of large-scale microalgal cultures using near infrared (NIR) optical density sensors. J Biotechnol 122:209–215

    CAS  PubMed  Google Scholar 

  • Schroeder DC, Oke J, Hall M, Malin G, Wilson WH (2003) Virus succession observed during an Emiliania huxleyi bloom. Appl Environ Microbiol 69:2484–2490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smith VH, Foster BL, Grover JP, Holt RD, Leibold MA, deNoyelles F (2005) Phytoplankton species richness scales consistently from laboratory microcosms to the world's oceans. Proc Natl Acad Sci 102:4393–4396

    CAS  PubMed  Google Scholar 

  • Steedman HF (ed) (1976) Zooplankton fixation and preservation. UNESCO, Paris

    Google Scholar 

  • Steichen S (2016) Tracking an algal predator: monitoring the dynamics of Vampirovibrio chlorellavorus in outdoor culture. MSc Thesis, The University of Arizona, USA 66 pp

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, United States

    Google Scholar 

  • Strittmatter M, Guerra T, Silva J, Gachon CMM (2016) A new flagellated dispersion stage in Paraphysoderma sedebokerense, a pathogen of Haematococcus pluvialis. J Appl Phycol 28:1553–1558

    CAS  PubMed  Google Scholar 

  • Sudhakar K, Premalatha M (2015) Characterization of micro Aalgal biomass through FTIR/TGA /CHN Aanalysis: application to Scenedesmus sp. Energy Sources A 37:2330–2337

    Google Scholar 

  • Urabe J, Kyle M, Makino W, Yoshida T, Andersen T, Elser JJ (2002) Reduced light increases herbivore production due to stoichiometric effects of light/nutrient balance. Ecology 83:619–627

    Google Scholar 

  • Wang H, Zhang W, Chen L, Wang J, Liu T (2013) The contamination and control of biological pollutants in mass cultivation of microalgae. Bioresour Technol 128:745–750

    CAS  PubMed  Google Scholar 

  • Wang Y, Castillo-Keller M, Eustance E, Sommerfeld M (2017) Early detection and quantification of zooplankton grazers in algal cultures by FlowCAM. Algal Res 21:98–102

    Google Scholar 

  • Wang Y, Gong Y, Dai L, Sommerfeld M, Zhang C, Hu Q (2018) Identification of harmful protozoa in outdoor cultivation of Chlorella and the use of ultrasonication to control contamination. Algal Res 31:298–310

    Google Scholar 

Download references

Funding

Research by the authors was funded by Reliance Industries Limited, Mumbai, India and IITB-Monash Research Academy, Mumbai, India. (Fund code–IMURA0303)

Author information

Authors and Affiliations

  1. IITB-Monash Research Academy, Mumbai, 400076, India

    Pranali Deore

  2. School of Biological Sciences, Monash University, Clayton, 3800, Australia

    Pranali Deore & John Beardall

  3. Department of Chemical Engineering, Indian Institute of Technology Bombay, Mumbai, 400076, India

    Pranali Deore & Santosh Noronha

Authors
  1. Pranali Deore
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John Beardall
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Santosh Noronha
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Pranali Deore conceptualized and prepared manuscript. John Berdall corrected, improved, and critically reviewed the manuscript. Santosh Noronha critically reviewed and corrected the manuscript.

Corresponding author

Correspondence to Santosh Noronha.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deore, P., Beardall, J. & Noronha, S. A perspective on the current status of approaches for early detection of microalgal grazing. J Appl Phycol 32, 3723–3733 (2020). https://doi.org/10.1007/s10811-020-02241-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-020-02241-x

Keywords

Search

Navigation