Abstract

We introduce an image cytometer (I-CYT) for the analysis of phytoplankton in fresh and marine water environments. A linear quantification of cell numbers was observed covering several orders of magnitude using cultures of Tetraselmis and Nannochloropsis measured by autofluorescence in a laboratory environment. We assessed the functionality of the system outside the laboratory by phytoplankton quantification of samples taken from a marine water environment (Dutch Wadden Sea, The Netherlands) and a fresh water environment (Lake Ijssel, The Netherlands). The I-CYT was also employed to study the effects of two ballast water treatment systems (BWTS), based on chlorine electrolysis and UV sterilization, with the analysis including the vitality of the phytoplankton. For comparative study and benchmarking of the I-CYT, a standard flow cytometer was used. Our results prove a limit of detection (LOD) of 10 cells/ml with an accuracy between 0.7 and 0.5 log, and a correlation of 88.29% in quantification and 96.21% in vitality, with respect to the flow cytometry results.

© 2017 Optical Society of America

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References

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  1. V. Kannan, “Globalization and Government Rugulations: Invasive Species Management in an Era of Interdependence,” J. Crit. Writ. 10, 8–12 (2015).
  2. J. Moreno-Andrés, L. Romero-Martínez, A. Acevedo-Merino, and E. Nebot, “Determining Disinfection Efficiency on E. Faecalis in Saltwater by Photolysis of H2O2: Implications for Ballast Water Treatment,” Chem. Eng. J. 283, 1339–1348 (2016).
    [Crossref]
  3. N. Bax, A. Williamson, M. Aguero, E. Gonzalez, and W. Geeves, “Marine Invasive Alien Species: A Threat to Global Biodiversity,” Mar. Policy 27(4), 313–323 (2003).
    [Crossref]
  4. H. Seebens, M. T. Gastner, and B. Blasius, “The risk of marine bioinvasion caused by global shipping,” Ecol. Lett. 16(6), 782–790 (2013).
    [Crossref] [PubMed]
  5. P. K. Dunstan and N. J. Bax, “Management of an Invasive Marine Species: Defining and Testing the Effectiveness of Ballast-Water Management Options Using Management Strategy Evaluation,” ICES J. Mar. Sci. 65(6), 841–850 (2008).
    [Crossref]
  6. IMO, “International Convention for the Control and Manangement Of Ship’s Ballast Water and Sediments” IMO Document BWM/CONF/36 no. February (2004): London:IMO.
  7. R. Rivas-Hermann, J. Köhler, and A. E. Scheepens, “Innovation in Product and Services in the Shipping Retrofit Industry: A Case Study of Ballast Water Treatment Systems,” J. Clean. Prod. 106, 443–454 (2015).
    [Crossref]
  8. P. P. Stehouwer, A. Buma, and L. Peperzak, “A comparison of six different ballast water treatment systems based on UV radiation, electrochlorination and chlorine dioxide,” Environ. Technol. 36(13), 2094–2104 (2015).
    [Crossref] [PubMed]
  9. L. Maranda, A. M. Cox, R. G. Campbell, and D. C. Smith, “Chlorine dioxide as a treatment for ballast water to control invasive species: shipboard testing,” Mar. Pollut. Bull. 75(1-2), 76–89 (2013).
    [Crossref] [PubMed]
  10. J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).
  11. S. Sanchez-Ferandin, F. Leroy, F. Y. Bouget, and F. Joux, “A new, sensitive marine microalgal recombinant biosensor using luminescence monitoring for toxicity testing of antifouling biocides,” Appl. Environ. Microbiol. 79(2), 631–638 (2013).
    [Crossref] [PubMed]
  12. J. Wollschläger, A. Nicolaus, K. H. Wiltshire, and K. Metfies, “Assessment of North Sea Phytoplankton via Molecular Sensing: A Method Evaluation,” J. Plankton Res. 36(3), 695–708 (2014).
    [Crossref]
  13. J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).
  14. J. P. Meneely, K. Campbell, C. Greef, M. J. Lochhead, and C. T. Elliott, “Development and Validation of an Ultrasensitive Fluorescence Planar Waveguide Biosensor for the Detection of Paralytic Shellfish Toxins in Marine Algae,” Biosensors and Bioelectronics 41, 691–697 (2013).
  15. J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
    [Crossref] [PubMed]
  16. M. J. W. Veldhuis and G. W. Kraay, “Application of Flow Cytometry in Marine Phytoplankton Research,” Current Applications and Future Perspectives 64(2), 121–134 (2000).
  17. U. Schreiber, “Chlorophyll Fluorescence : New Instruments for Special Applications,” Photosynth.: Mech. Eff. 5, 4253–4258 (1998).
  18. M. J. W. Veldhuis, F. Fuhr, J. P. Boon, and C. C. Ten Hallers-Tjabbers, “Treatment of Ballast Water ; How to Test a System with a Modular Concept?” Environ. Technol. 27, 909–921 (2006).
  19. M. A. O’Connell, B. A. Belanger, and P. D. Haaland, “Calibration and Assay Development Using the Four-Parameter Logistic Model,” Chemom. Intell. Lab. Syst. 20(2), 97–114 (1993).
    [Crossref]

2016 (1)

J. Moreno-Andrés, L. Romero-Martínez, A. Acevedo-Merino, and E. Nebot, “Determining Disinfection Efficiency on E. Faecalis in Saltwater by Photolysis of H2O2: Implications for Ballast Water Treatment,” Chem. Eng. J. 283, 1339–1348 (2016).
[Crossref]

2015 (4)

R. Rivas-Hermann, J. Köhler, and A. E. Scheepens, “Innovation in Product and Services in the Shipping Retrofit Industry: A Case Study of Ballast Water Treatment Systems,” J. Clean. Prod. 106, 443–454 (2015).
[Crossref]

P. P. Stehouwer, A. Buma, and L. Peperzak, “A comparison of six different ballast water treatment systems based on UV radiation, electrochlorination and chlorine dioxide,” Environ. Technol. 36(13), 2094–2104 (2015).
[Crossref] [PubMed]

V. Kannan, “Globalization and Government Rugulations: Invasive Species Management in an Era of Interdependence,” J. Crit. Writ. 10, 8–12 (2015).

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

2014 (1)

J. Wollschläger, A. Nicolaus, K. H. Wiltshire, and K. Metfies, “Assessment of North Sea Phytoplankton via Molecular Sensing: A Method Evaluation,” J. Plankton Res. 36(3), 695–708 (2014).
[Crossref]

2013 (4)

S. Sanchez-Ferandin, F. Leroy, F. Y. Bouget, and F. Joux, “A new, sensitive marine microalgal recombinant biosensor using luminescence monitoring for toxicity testing of antifouling biocides,” Appl. Environ. Microbiol. 79(2), 631–638 (2013).
[Crossref] [PubMed]

L. Maranda, A. M. Cox, R. G. Campbell, and D. C. Smith, “Chlorine dioxide as a treatment for ballast water to control invasive species: shipboard testing,” Mar. Pollut. Bull. 75(1-2), 76–89 (2013).
[Crossref] [PubMed]

H. Seebens, M. T. Gastner, and B. Blasius, “The risk of marine bioinvasion caused by global shipping,” Ecol. Lett. 16(6), 782–790 (2013).
[Crossref] [PubMed]

J. P. Meneely, K. Campbell, C. Greef, M. J. Lochhead, and C. T. Elliott, “Development and Validation of an Ultrasensitive Fluorescence Planar Waveguide Biosensor for the Detection of Paralytic Shellfish Toxins in Marine Algae,” Biosensors and Bioelectronics 41, 691–697 (2013).

2012 (2)

J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).

J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).

2008 (1)

P. K. Dunstan and N. J. Bax, “Management of an Invasive Marine Species: Defining and Testing the Effectiveness of Ballast-Water Management Options Using Management Strategy Evaluation,” ICES J. Mar. Sci. 65(6), 841–850 (2008).
[Crossref]

2006 (1)

M. J. W. Veldhuis, F. Fuhr, J. P. Boon, and C. C. Ten Hallers-Tjabbers, “Treatment of Ballast Water ; How to Test a System with a Modular Concept?” Environ. Technol. 27, 909–921 (2006).

2003 (1)

N. Bax, A. Williamson, M. Aguero, E. Gonzalez, and W. Geeves, “Marine Invasive Alien Species: A Threat to Global Biodiversity,” Mar. Policy 27(4), 313–323 (2003).
[Crossref]

2000 (1)

M. J. W. Veldhuis and G. W. Kraay, “Application of Flow Cytometry in Marine Phytoplankton Research,” Current Applications and Future Perspectives 64(2), 121–134 (2000).

1998 (1)

U. Schreiber, “Chlorophyll Fluorescence : New Instruments for Special Applications,” Photosynth.: Mech. Eff. 5, 4253–4258 (1998).

1993 (1)

M. A. O’Connell, B. A. Belanger, and P. D. Haaland, “Calibration and Assay Development Using the Four-Parameter Logistic Model,” Chemom. Intell. Lab. Syst. 20(2), 97–114 (1993).
[Crossref]

Acevedo-Merino, A.

J. Moreno-Andrés, L. Romero-Martínez, A. Acevedo-Merino, and E. Nebot, “Determining Disinfection Efficiency on E. Faecalis in Saltwater by Photolysis of H2O2: Implications for Ballast Water Treatment,” Chem. Eng. J. 283, 1339–1348 (2016).
[Crossref]

Aguero, M.

N. Bax, A. Williamson, M. Aguero, E. Gonzalez, and W. Geeves, “Marine Invasive Alien Species: A Threat to Global Biodiversity,” Mar. Policy 27(4), 313–323 (2003).
[Crossref]

Bax, N.

N. Bax, A. Williamson, M. Aguero, E. Gonzalez, and W. Geeves, “Marine Invasive Alien Species: A Threat to Global Biodiversity,” Mar. Policy 27(4), 313–323 (2003).
[Crossref]

Bax, N. J.

P. K. Dunstan and N. J. Bax, “Management of an Invasive Marine Species: Defining and Testing the Effectiveness of Ballast-Water Management Options Using Management Strategy Evaluation,” ICES J. Mar. Sci. 65(6), 841–850 (2008).
[Crossref]

Belanger, B. A.

M. A. O’Connell, B. A. Belanger, and P. D. Haaland, “Calibration and Assay Development Using the Four-Parameter Logistic Model,” Chemom. Intell. Lab. Syst. 20(2), 97–114 (1993).
[Crossref]

Blasius, B.

H. Seebens, M. T. Gastner, and B. Blasius, “The risk of marine bioinvasion caused by global shipping,” Ecol. Lett. 16(6), 782–790 (2013).
[Crossref] [PubMed]

Boon, J. P.

M. J. W. Veldhuis, F. Fuhr, J. P. Boon, and C. C. Ten Hallers-Tjabbers, “Treatment of Ballast Water ; How to Test a System with a Modular Concept?” Environ. Technol. 27, 909–921 (2006).

Bouget, F. Y.

S. Sanchez-Ferandin, F. Leroy, F. Y. Bouget, and F. Joux, “A new, sensitive marine microalgal recombinant biosensor using luminescence monitoring for toxicity testing of antifouling biocides,” Appl. Environ. Microbiol. 79(2), 631–638 (2013).
[Crossref] [PubMed]

Buma, A.

P. P. Stehouwer, A. Buma, and L. Peperzak, “A comparison of six different ballast water treatment systems based on UV radiation, electrochlorination and chlorine dioxide,” Environ. Technol. 36(13), 2094–2104 (2015).
[Crossref] [PubMed]

Campbell, K.

J. P. Meneely, K. Campbell, C. Greef, M. J. Lochhead, and C. T. Elliott, “Development and Validation of an Ultrasensitive Fluorescence Planar Waveguide Biosensor for the Detection of Paralytic Shellfish Toxins in Marine Algae,” Biosensors and Bioelectronics 41, 691–697 (2013).

Campbell, R. G.

L. Maranda, A. M. Cox, R. G. Campbell, and D. C. Smith, “Chlorine dioxide as a treatment for ballast water to control invasive species: shipboard testing,” Mar. Pollut. Bull. 75(1-2), 76–89 (2013).
[Crossref] [PubMed]

Catalan, V.

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

Cox, A. M.

L. Maranda, A. M. Cox, R. G. Campbell, and D. C. Smith, “Chlorine dioxide as a treatment for ballast water to control invasive species: shipboard testing,” Mar. Pollut. Bull. 75(1-2), 76–89 (2013).
[Crossref] [PubMed]

Dunstan, P. K.

P. K. Dunstan and N. J. Bax, “Management of an Invasive Marine Species: Defining and Testing the Effectiveness of Ballast-Water Management Options Using Management Strategy Evaluation,” ICES J. Mar. Sci. 65(6), 841–850 (2008).
[Crossref]

Elliott, C. T.

J. P. Meneely, K. Campbell, C. Greef, M. J. Lochhead, and C. T. Elliott, “Development and Validation of an Ultrasensitive Fluorescence Planar Waveguide Biosensor for the Detection of Paralytic Shellfish Toxins in Marine Algae,” Biosensors and Bioelectronics 41, 691–697 (2013).

Erickson, J. S.

J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).

J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).

Fuhr, F.

M. J. W. Veldhuis, F. Fuhr, J. P. Boon, and C. C. Ten Hallers-Tjabbers, “Treatment of Ballast Water ; How to Test a System with a Modular Concept?” Environ. Technol. 27, 909–921 (2006).

Gastner, M. T.

H. Seebens, M. T. Gastner, and B. Blasius, “The risk of marine bioinvasion caused by global shipping,” Ecol. Lett. 16(6), 782–790 (2013).
[Crossref] [PubMed]

Geeves, W.

N. Bax, A. Williamson, M. Aguero, E. Gonzalez, and W. Geeves, “Marine Invasive Alien Species: A Threat to Global Biodiversity,” Mar. Policy 27(4), 313–323 (2003).
[Crossref]

Golden, J. P.

J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).

J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).

Gonzalez, E.

N. Bax, A. Williamson, M. Aguero, E. Gonzalez, and W. Geeves, “Marine Invasive Alien Species: A Threat to Global Biodiversity,” Mar. Policy 27(4), 313–323 (2003).
[Crossref]

Greef, C.

J. P. Meneely, K. Campbell, C. Greef, M. J. Lochhead, and C. T. Elliott, “Development and Validation of an Ultrasensitive Fluorescence Planar Waveguide Biosensor for the Detection of Paralytic Shellfish Toxins in Marine Algae,” Biosensors and Bioelectronics 41, 691–697 (2013).

Haaland, P. D.

M. A. O’Connell, B. A. Belanger, and P. D. Haaland, “Calibration and Assay Development Using the Four-Parameter Logistic Model,” Chemom. Intell. Lab. Syst. 20(2), 97–114 (1993).
[Crossref]

Hashemi, N.

J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).

J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).

Jofre, M.

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

Joux, F.

S. Sanchez-Ferandin, F. Leroy, F. Y. Bouget, and F. Joux, “A new, sensitive marine microalgal recombinant biosensor using luminescence monitoring for toxicity testing of antifouling biocides,” Appl. Environ. Microbiol. 79(2), 631–638 (2013).
[Crossref] [PubMed]

Kannan, V.

V. Kannan, “Globalization and Government Rugulations: Invasive Species Management in an Era of Interdependence,” J. Crit. Writ. 10, 8–12 (2015).

Köhler, J.

R. Rivas-Hermann, J. Köhler, and A. E. Scheepens, “Innovation in Product and Services in the Shipping Retrofit Industry: A Case Study of Ballast Water Treatment Systems,” J. Clean. Prod. 106, 443–454 (2015).
[Crossref]

Kraay, G. W.

M. J. W. Veldhuis and G. W. Kraay, “Application of Flow Cytometry in Marine Phytoplankton Research,” Current Applications and Future Perspectives 64(2), 121–134 (2000).

Leroy, F.

S. Sanchez-Ferandin, F. Leroy, F. Y. Bouget, and F. Joux, “A new, sensitive marine microalgal recombinant biosensor using luminescence monitoring for toxicity testing of antifouling biocides,” Appl. Environ. Microbiol. 79(2), 631–638 (2013).
[Crossref] [PubMed]

Ligler, F. S.

J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).

J. P. Golden, N. Hashemi, J. S. Erickson, and F. S. Ligler, “A Microflow Cytometer for Optical Analysis of Phytoplankton,” Proc. SPIE 8212, 82120G (2012).

Lochhead, M. J.

J. P. Meneely, K. Campbell, C. Greef, M. J. Lochhead, and C. T. Elliott, “Development and Validation of an Ultrasensitive Fluorescence Planar Waveguide Biosensor for the Detection of Paralytic Shellfish Toxins in Marine Algae,” Biosensors and Bioelectronics 41, 691–697 (2013).

Maranda, L.

L. Maranda, A. M. Cox, R. G. Campbell, and D. C. Smith, “Chlorine dioxide as a treatment for ballast water to control invasive species: shipboard testing,” Mar. Pollut. Bull. 75(1-2), 76–89 (2013).
[Crossref] [PubMed]

Martínez, P.

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

Meneely, J. P.

J. P. Meneely, K. Campbell, C. Greef, M. J. Lochhead, and C. T. Elliott, “Development and Validation of an Ultrasensitive Fluorescence Planar Waveguide Biosensor for the Detection of Paralytic Shellfish Toxins in Marine Algae,” Biosensors and Bioelectronics 41, 691–697 (2013).

Metfies, K.

J. Wollschläger, A. Nicolaus, K. H. Wiltshire, and K. Metfies, “Assessment of North Sea Phytoplankton via Molecular Sensing: A Method Evaluation,” J. Plankton Res. 36(3), 695–708 (2014).
[Crossref]

Moreno-Andrés, J.

J. Moreno-Andrés, L. Romero-Martínez, A. Acevedo-Merino, and E. Nebot, “Determining Disinfection Efficiency on E. Faecalis in Saltwater by Photolysis of H2O2: Implications for Ballast Water Treatment,” Chem. Eng. J. 283, 1339–1348 (2016).
[Crossref]

Nebot, E.

J. Moreno-Andrés, L. Romero-Martínez, A. Acevedo-Merino, and E. Nebot, “Determining Disinfection Efficiency on E. Faecalis in Saltwater by Photolysis of H2O2: Implications for Ballast Water Treatment,” Chem. Eng. J. 283, 1339–1348 (2016).
[Crossref]

Nicolaus, A.

J. Wollschläger, A. Nicolaus, K. H. Wiltshire, and K. Metfies, “Assessment of North Sea Phytoplankton via Molecular Sensing: A Method Evaluation,” J. Plankton Res. 36(3), 695–708 (2014).
[Crossref]

O’Connell, M. A.

M. A. O’Connell, B. A. Belanger, and P. D. Haaland, “Calibration and Assay Development Using the Four-Parameter Logistic Model,” Chemom. Intell. Lab. Syst. 20(2), 97–114 (1993).
[Crossref]

Peperzak, L.

P. P. Stehouwer, A. Buma, and L. Peperzak, “A comparison of six different ballast water treatment systems based on UV radiation, electrochlorination and chlorine dioxide,” Environ. Technol. 36(13), 2094–2104 (2015).
[Crossref] [PubMed]

Pérez, J. M.

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

Pruneri, V.

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

Rivas-Hermann, R.

R. Rivas-Hermann, J. Köhler, and A. E. Scheepens, “Innovation in Product and Services in the Shipping Retrofit Industry: A Case Study of Ballast Water Treatment Systems,” J. Clean. Prod. 106, 443–454 (2015).
[Crossref]

Romero-Martínez, L.

J. Moreno-Andrés, L. Romero-Martínez, A. Acevedo-Merino, and E. Nebot, “Determining Disinfection Efficiency on E. Faecalis in Saltwater by Photolysis of H2O2: Implications for Ballast Water Treatment,” Chem. Eng. J. 283, 1339–1348 (2016).
[Crossref]

Sanchez-Ferandin, S.

S. Sanchez-Ferandin, F. Leroy, F. Y. Bouget, and F. Joux, “A new, sensitive marine microalgal recombinant biosensor using luminescence monitoring for toxicity testing of antifouling biocides,” Appl. Environ. Microbiol. 79(2), 631–638 (2013).
[Crossref] [PubMed]

Scheepens, A. E.

R. Rivas-Hermann, J. Köhler, and A. E. Scheepens, “Innovation in Product and Services in the Shipping Retrofit Industry: A Case Study of Ballast Water Treatment Systems,” J. Clean. Prod. 106, 443–454 (2015).
[Crossref]

Schreiber, U.

U. Schreiber, “Chlorophyll Fluorescence : New Instruments for Special Applications,” Photosynth.: Mech. Eff. 5, 4253–4258 (1998).

Seebens, H.

H. Seebens, M. T. Gastner, and B. Blasius, “The risk of marine bioinvasion caused by global shipping,” Ecol. Lett. 16(6), 782–790 (2013).
[Crossref] [PubMed]

Smith, D. C.

L. Maranda, A. M. Cox, R. G. Campbell, and D. C. Smith, “Chlorine dioxide as a treatment for ballast water to control invasive species: shipboard testing,” Mar. Pollut. Bull. 75(1-2), 76–89 (2013).
[Crossref] [PubMed]

Stehouwer, P. P.

P. P. Stehouwer, A. Buma, and L. Peperzak, “A comparison of six different ballast water treatment systems based on UV radiation, electrochlorination and chlorine dioxide,” Environ. Technol. 36(13), 2094–2104 (2015).
[Crossref] [PubMed]

Ten Hallers-Tjabbers, C. C.

M. J. W. Veldhuis, F. Fuhr, J. P. Boon, and C. C. Ten Hallers-Tjabbers, “Treatment of Ballast Water ; How to Test a System with a Modular Concept?” Environ. Technol. 27, 909–921 (2006).

Veldhuis, M. J. W.

M. J. W. Veldhuis, F. Fuhr, J. P. Boon, and C. C. Ten Hallers-Tjabbers, “Treatment of Ballast Water ; How to Test a System with a Modular Concept?” Environ. Technol. 27, 909–921 (2006).

M. J. W. Veldhuis and G. W. Kraay, “Application of Flow Cytometry in Marine Phytoplankton Research,” Current Applications and Future Perspectives 64(2), 121–134 (2000).

Williamson, A.

N. Bax, A. Williamson, M. Aguero, E. Gonzalez, and W. Geeves, “Marine Invasive Alien Species: A Threat to Global Biodiversity,” Mar. Policy 27(4), 313–323 (2003).
[Crossref]

Wiltshire, K. H.

J. Wollschläger, A. Nicolaus, K. H. Wiltshire, and K. Metfies, “Assessment of North Sea Phytoplankton via Molecular Sensing: A Method Evaluation,” J. Plankton Res. 36(3), 695–708 (2014).
[Crossref]

Wollschläger, J.

J. Wollschläger, A. Nicolaus, K. H. Wiltshire, and K. Metfies, “Assessment of North Sea Phytoplankton via Molecular Sensing: A Method Evaluation,” J. Plankton Res. 36(3), 695–708 (2014).
[Crossref]

Yáñez, M. A.

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

Analyst (Lond.) (1)

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
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Appl. Environ. Microbiol. (1)

S. Sanchez-Ferandin, F. Leroy, F. Y. Bouget, and F. Joux, “A new, sensitive marine microalgal recombinant biosensor using luminescence monitoring for toxicity testing of antifouling biocides,” Appl. Environ. Microbiol. 79(2), 631–638 (2013).
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Biosensors and Bioelectronics (1)

J. P. Meneely, K. Campbell, C. Greef, M. J. Lochhead, and C. T. Elliott, “Development and Validation of an Ultrasensitive Fluorescence Planar Waveguide Biosensor for the Detection of Paralytic Shellfish Toxins in Marine Algae,” Biosensors and Bioelectronics 41, 691–697 (2013).

Chem. Eng. J. (1)

J. Moreno-Andrés, L. Romero-Martínez, A. Acevedo-Merino, and E. Nebot, “Determining Disinfection Efficiency on E. Faecalis in Saltwater by Photolysis of H2O2: Implications for Ballast Water Treatment,” Chem. Eng. J. 283, 1339–1348 (2016).
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Chemom. Intell. Lab. Syst. (1)

M. A. O’Connell, B. A. Belanger, and P. D. Haaland, “Calibration and Assay Development Using the Four-Parameter Logistic Model,” Chemom. Intell. Lab. Syst. 20(2), 97–114 (1993).
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Environ. Technol. (2)

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Figures (6)

Fig. 1
Fig. 1

Schematic of the opto-mechanics. The system is composed of a light emitting diode (LED) light source, an optical lens for collimation, an optical filter to absorb the excitation pump and select two fluorescent emission channels centred at 512nm and 630nm, respectively, a parabolic mirror which acts as an optical transforming element to propagate the optical Fourier transform of the sample towards a microlens array, which spatially samples the incoming beam, and a CMOS image sensor array that captures the light sample to process.

Fig. 2
Fig. 2

Brightfield captures of a buffer sample (Fig. 2(a)) and a particulate sample (Fig. 2(b)) using the I-CYT. These images correspond to the formatted Fourier transform, which can in turn be analyzed for quantification of particles and size information. For the size determination, each lobe of the microlens is analyzed independently in terms of the spatial bandwidth product (SBP) of our optical system.

Fig. 3
Fig. 3

Results for the Tetraselmis and Nannochloropsis samples. Nannochloropsis results, with concentrations measured by the I-CYT from 3·103 cells/ml at a dilution from the stock of 10−3, to <10 cells/ml at a dilution from the stock of 10−7. Tetraselmis results, with concentrations measured by the I-CYT from 104 cells/ml at a dilution from the stock of 10−2, to <10 cells/ml at a dilution from the stock of 10−6. Both organisms were measured in two independent series, with each individual sample measured three times.

Fig. 4
Fig. 4

Concentration in [cells/ml] as measured by the proposed image cytometer and the reference flow cytometer. The two instruments show very similar results, with a deviation of 0.05 and 0.14 for the window below and above 10µm size, respectively.

Fig. 5
Fig. 5

Marine water samples measured before and after a BWTS of electrolysis by chlorine. The phytoplankton population was quantified in the two windows of interest; above (a) and below (b) the 10 µm threshold. The effect of the electrolysis by chlorine, reduces the phytoplankton population in both regions. This can be specially noted in samples 1 and 3, were the decrease in concentration is of one order of magnitude. In sample 2 the system has a lower impact, were it reduced the population in half an order of magnitude below the threshold and seem to stay the same above the threshold, where it shows a slight increase within the margin of 0.5 log deviation reported in the laboratory measurements.

Fig. 6
Fig. 6

Fresh water samples were tested before and after three different protocols of BWTS (electrolysis by chlorine, UV sterilization with 1 day holding, and UV sterilization with one day holding and a second UV exposure after holding). Both phytoplankton population and viability index were measured for the two windows of interest; above (a,c), and below (b,d) 10 µm size threshold. The samples were also measured with a gold reference flow cytometer. In terms of quantification, the image cytometer has correlation factors of 94.89% and 81.70% above and below the 10 µm size threshold, respectively; in terms of viability, the correlations are 92.43% and 100% above and below size threshold, respectively. The BWTS largely affect the phytoplankton population and viability as can be seen by the results obtained with both the image and flow cytometry platforms.

Tables (1)

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Table 1 Intra-assay and inter-assay deviation for both species at all concentrations measured.

Equations (2)

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Concentration[ cells ml ]=C· ( AD I CYT D ) 1/B
Vitality=1 F 0 F m

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