manuscript/f1000_revisions/marion_comments.md
In USEPA/Microcystinchla: Code, Data, and Manuscript for NLA, microcystin, Chl analysis
Overview: The manuscript/article addresses a critical question applicable to recreational and drinking water managers: Can we rapidly predict potentially harmful cyanobacteria blooms using traditional water quality methods? This question is likely to become more relevant according to the most current literature as blooms are expected to increase in frequency in the midst of a warming global climate facing more extreme storm and drought events 1-6. Using the rather large and nationally applicable National Lakes Assessment database for the United States, the authors demonstrate some of the strengths and weaknesses of using chlorophyll a as an indicator for at-risk conditions that could warrant management action or follow-up testing for cyanotoxins. The authors are also able to assign action levels or at least share possible action levels for management action using conditional probabilities. The strengths and weaknesses of selected probabilities are described using analyses similar to specificity and sensitivity in the form of accuracy and ‘avoiding type II errors’. The authors do not propose using chlorophyll a as a proxy to replace toxin measurement, but as a tool to help facilitate targeted monitoring of toxins during at-risk conditions.
Overall Comments: The article is meritorious in that it does provide a meaningful starting point for lakes with no phycocyanin measures and for providing a meaningful starting point for developing some semblance of an action level that could be employed by recreational water and drinking water managers concerned with cyanotoxins. The article does stand to improve significantly in some key areas, which are as follows:
(1) Additional discussion in methods related to the National Lakes Assessment
(2) Additional discussion needed on how the data were organized for data analysis
(3) Improved discussion needed on alternative indicators for cHABs and cyanotoxins not assessed in the NLA
(4) Consideration of region-specific criteria or limitations of national recommendations for chl a.
(5) Greater discussion on limitations of NLA and need for model validation/future studies.
(1) Additional discussion needed in methods related to the National Lakes Assessment:
The readership may not be aware of the U.S. NLA performed in 2007. The author(s) should clarify where samples were collected (nearshore or from the surface in the deeper waters). NLA chlorophyll a samples were take from the profundal zone rather than the littoral zone. The readership may also be interested in how many chl a samples were collected from each lake. Where were the microcystin-LR samples collected?
(2) Additional discussion needed on how the data were organized for data analysis:
Were these samples paired (collected at the same time from the same locale) or are these some type of aggregated value over a lake season? Describing this in the methods will really help for understanding the importance of this work. Paired results (MC-LR and Chl a from the same day) are much more impactful for demonstrating the rapid advantage of chl a compated to using results that are a seasonal average indicating that the hypereutrophic and eutrophic lakes (ones with the highest chl a) are also the ones that are most likely to have a cyanoHAB event sometime during the year.
(3) Improved discussion needed on alternative indicators for cHABs and cyanotoxins not assessed in the NLA: Brief mention is given to phycocyanin (one study), and the additional language (about phycocyanin not always being available for measure and when measured, it is for only measuring pigment and not toxins) is equally relevant for chl a. The same in vivo handheld fluorometers and continuous monitoring solutions available for chl a are now widely available for phycocyanin, often at the same cost as a rapid measure for chl a. Phycocyanin, like chl a, does not measure toxin either, but phycocyanin in many studies has outperformed chl a, and in some studies it has not (especially when toxin concentration is low). Historical records on PC are likely not as great as chlorophyll a. Overall, several studies on this topic have been produced in the last two to four years (see Zamyadi and Dorner’s work), with one study using phycocyanin to predict non-alcoholic liver disease presuming a relationship with cyanotoxins (Zhang et al. 2015)
(4) Consideration desired on region-specific criteria or limitations of national recommendations for chl a: With nearly 30% of the lakes in the temperate plains being coded as poor for chlorophyll a in the 2007 NLA, what impact would these conditional probabilities have on these lakes? Should the lake managers in this region be monitoring continuously all the time? What are the mean/median chlorophyll a levels for this part of the U.S? Regional variability may be really important and did the conditional probability approach take this into consideration or can it take it into consideration? Is there a way to evaluate if there are significant regional effects in the U.S? For nutrient standards in the U.S. and macroinvertebrate assessments, EPA has had to issue region-specific guidelines/criteria, etc. for some parameters.
(5) Greater discussion needed on limitations of NLA and need for model validation/future studies: The paper fails to address the limitations of the NLA – as a reader, I’m not aware of the limitations. I have much respect for the NLA, but I do have questions regarding the number of samples for each lake. Furthermore, a statement or two discussing the need to validate modeled data may be worthwhile. Is there a way to see if the probabilities actually align with the accuracy and type II error rates predicted by the conditional probability approach?
Abstract-Specific Comments: Near the bottom of the abstract, the units seem quite high for microcystins (g/L) rather than micrograms/L. The micro Greek symbol (mu) may have been lost during uploading.
Results Comments: (1) In discussing the lake exceedances of the various recommended levels by EPA, the addition of ‘drinking water’ is appropriate in my opinion. Although it is mentioned earlier in the methods, further providing the information in the results is helpful to a novice reader or a person just becoming familiar with drinking water regulations and guidelines, as the U.S. EPA child level may be presumed by a reader to be a level for recreation in a lake rather than a level associated with finished drinking water after water treatment. (2) “All lakes had reported chl a concentrations that exceeded detection limits” Does this mean that some were over range? Or does this mean that “All lakes had detectable levels of chl a”
Discussion Comments: The wedge pattern in figure 2 is not apparent in figure 2, however, the logic makes sense and is supported visually by the conditional probability plots in fig 1. If figure 2 could have two lines of best fit (similar to the way some researchers do for funnel plots on publication bias papers), it may be easier to see the wedge shape.
Climate Articles Highlighting Current Importance of Topic:
Harvell, C. D.; Kim, K.; Burkholder, J. M.; Colwell, R. R.; Epstein, P. R.; Grimes, D. J.; Hoffman, E. E.; Lipp,E. K.; Osterhaus, A. D. M. E.; Overstreet, R. M.; Porter, J. W.; Smith, G. W.; Vasta, G. R.Emerging marine diseases – climate links and anthropogenic factors Science 2000, 285, 1505– 1510
Peperzak, L.Climate change and harmful algal blooms in the North Sea Acta Oecol. 2003, 24, 139–144
Edwards, M.; Johns, D. G.; Leterme, S. C.; Svendsen, E.; Richardson, A. J.Regional climate change and harmful algal blooms in the northeast Atlantic Limnol. Oceanogr. 2006, 51 ( 2) 820– 829
Ye, C.; Shen, Z.; Zhang, T.; Feng, M.; Lei, Y.; Zhang, J.Long-term joint effect of nutrients and temperature increase on algal growth in Lake Taihu, China J Environ. Sci. 2011, 23 ( 2) 222– 227
Paerl, H. W.; Hall, N. S.; Calandrino, E. S.Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change Sci. Total Environ. 2011, 409, 1739– 1745
Davis, T. W.; Berry, D. L.; Boyer, G. L.; Gobler, C. J.The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms Harmful Algae 2009, 8, 715– 725
Articles on Phycocyanin and Toxin Indicators Ought to Be Considered:
Ahn, C.-Y.; Joung, S.-H.; Yoon, S.-K.; Oh, H.-M.Alternative alert system for cyanobacterial bloom, using phycocyanin as a level determinant J. Microbiol. 2007, 45 ( 2) 98– 104.
Makarewicz, J. C.; Boyer, G. L.; Lewis, T. .; Guenther, W.; Atkinson, J.; Arnold, M.Spatial and temporal distribution of the cyanotoxin microcystin-LR in the Lake Ontario ecosystem: Coastal embayments, rivers, nearshore and offshore, and upland lakes J. Great Lakes Res. 2009, 35, 83– 89.
Murby, A. L.Assessing spatial distributions of cyanobacteria and microcystins in N.H. lakes with implications for lake monitoring. Master’s Thesis. University of New Hampshire, 2009; p 89.
Lehman, E. M.Seasonal occurrence and toxicity of Microcystis in impoundments of the Huron River, Michigan, USA Water Res. 2007, 41, 795– 802
Lee C, Marion JW, Cheung M, Lee CS, Lee J. Associations among Human-Associated Fecal Contamination, Microcystis aeruginosa, and Microcystin at Lake Erie Beaches. International journal of environmental research and public health. 2015 Sep 11;12(9):11466-85.
Zamyadi A, Dorner S, Ndong M, Ellis D, Bolduc A, Bastien C, Prévost M. Application of in vivo measurements for the management of cyanobacteria breakthrough into drinking water treatment plants. Environmental Science: Processes & Impacts. 2014;16(2):313-23.
Zhang F, Lee J, Liang S, Shum CK. Cyanobacteria blooms and non-alcoholic liver disease: evidence from a county level ecological study in the United States. Environmental Health. 2015 May 7;14(1):41.
References
1. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus AD, Overstreet RM, Porter JW, Smith GW, Vasta GR: Emerging marine diseases--climate links and anthropogenic factors.Science. 1999; 285 (5433): 1505-10 PubMed Abstract
2. Peperzak L: Climate change and harmful algal blooms in the North Sea. Acta Oecologica. 2003; 24: S139-S144 Publisher Full Text
3. Edwards M, Johns D, Leterme S, Svendsen E, Richardson A: Regional climate change and harmful algal blooms in the northeast Atlantic. Limnology and Oceanography. 2006; 51 (2): 820-829 Publisher Full Text
4. Ye C, Shen Z, Zhang T, Fan M, Lei Y, Zhang J: Long-term joint effect of nutrients and temperature increase on algal growth in Lake Taihu, China.J Environ Sci (China). 2011; 23 (2): 222-7 PubMed Abstract
5. Paerl HW, Hall NS, Calandrino ES: Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change.Sci Total Environ. 2011; 409 (10): 1739-45 PubMed Abstract | Publisher Full Text
6. Davis T, Berry D, Boyer G, Gobler C: The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae. 2009; 8 (5): 715-725 Publisher Full Text
7. Ahn CY, Joung SH, Yoon SK, Oh HM: Alternative alert system for cyanobacterial bloom, using phycocyanin as a level determinant.J Microbiol. 2007; 45 (2): 98-104 PubMed Abstract
8. Makarewicz J, Boyer G, Lewis T, Guenther W, Atkinson J, Arnold M: Spatial and temporal distribution of the cyanotoxin microcystin-LR in the Lake Ontario ecosystem: Coastal embayments, rivers, nearshore and offshore, and upland lakes. Journal of Great Lakes Research. 2009; 35: 83-89 Publisher Full Text
9. Murlby AL: Assessing spatial distributions of cyanobacteria and microcystins in N.H. lakes with implications for lake monitoring. 2009; Master's Thesis (University of New Hampshire): 89
10. Lehman EM: Seasonal occurrence and toxicity of Microcystis in impoundments of the Huron River, Michigan, USA.Water Res. 2007; 41 (4): 795-802 PubMed Abstract | Publisher Full Text
11. Lee C, Marion JW, Cheung M, Lee CS, Lee J: Associations among Human-Associated Fecal Contamination, Microcystis aeruginosa, and Microcystin at Lake Erie Beaches.Int J Environ Res Public Health. 2015; 12 (9): 11466-85 PubMed Abstract | Publisher Full Text
12. Zamyadi A, Dorner S, Ndong M, Ellis D, Bolduc A, Bastien C, Prévost M: Application of in vivo measurements for the management of cyanobacteria breakthrough into drinking water treatment plants.Environ Sci Process Impacts. 2014; 16 (2): 313-23 PubMed Abstract | Publisher Full Text
13. Zhang F, Lee J, Liang S, Shum CK: Cyanobacteria blooms and non-alcoholic liver disease: evidence from a county level ecological study in the United States.Environ Health. 2015; 14: 41 PubMed Abstract | Publisher Full Text
USEPA/Microcystinchla documentation built on May 9, 2019, 5:23 p.m.
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Overview: The manuscript/article addresses a critical question applicable to recreational and drinking water managers: Can we rapidly predict potentially harmful cyanobacteria blooms using traditional water quality methods? This question is likely to become more relevant according to the most current literature as blooms are expected to increase in frequency in the midst of a warming global climate facing more extreme storm and drought events 1-6. Using the rather large and nationally applicable National Lakes Assessment database for the United States, the authors demonstrate some of the strengths and weaknesses of using chlorophyll a as an indicator for at-risk conditions that could warrant management action or follow-up testing for cyanotoxins. The authors are also able to assign action levels or at least share possible action levels for management action using conditional probabilities. The strengths and weaknesses of selected probabilities are described using analyses similar to specificity and sensitivity in the form of accuracy and ‘avoiding type II errors’. The authors do not propose using chlorophyll a as a proxy to replace toxin measurement, but as a tool to help facilitate targeted monitoring of toxins during at-risk conditions.
Overall Comments: The article is meritorious in that it does provide a meaningful starting point for lakes with no phycocyanin measures and for providing a meaningful starting point for developing some semblance of an action level that could be employed by recreational water and drinking water managers concerned with cyanotoxins. The article does stand to improve significantly in some key areas, which are as follows:
(1) Additional discussion in methods related to the National Lakes Assessment (2) Additional discussion needed on how the data were organized for data analysis (3) Improved discussion needed on alternative indicators for cHABs and cyanotoxins not assessed in the NLA (4) Consideration of region-specific criteria or limitations of national recommendations for chl a. (5) Greater discussion on limitations of NLA and need for model validation/future studies.
(1) Additional discussion needed in methods related to the National Lakes Assessment: The readership may not be aware of the U.S. NLA performed in 2007. The author(s) should clarify where samples were collected (nearshore or from the surface in the deeper waters). NLA chlorophyll a samples were take from the profundal zone rather than the littoral zone. The readership may also be interested in how many chl a samples were collected from each lake. Where were the microcystin-LR samples collected?
(2) Additional discussion needed on how the data were organized for data analysis: Were these samples paired (collected at the same time from the same locale) or are these some type of aggregated value over a lake season? Describing this in the methods will really help for understanding the importance of this work. Paired results (MC-LR and Chl a from the same day) are much more impactful for demonstrating the rapid advantage of chl a compated to using results that are a seasonal average indicating that the hypereutrophic and eutrophic lakes (ones with the highest chl a) are also the ones that are most likely to have a cyanoHAB event sometime during the year.
(3) Improved discussion needed on alternative indicators for cHABs and cyanotoxins not assessed in the NLA: Brief mention is given to phycocyanin (one study), and the additional language (about phycocyanin not always being available for measure and when measured, it is for only measuring pigment and not toxins) is equally relevant for chl a. The same in vivo handheld fluorometers and continuous monitoring solutions available for chl a are now widely available for phycocyanin, often at the same cost as a rapid measure for chl a. Phycocyanin, like chl a, does not measure toxin either, but phycocyanin in many studies has outperformed chl a, and in some studies it has not (especially when toxin concentration is low). Historical records on PC are likely not as great as chlorophyll a. Overall, several studies on this topic have been produced in the last two to four years (see Zamyadi and Dorner’s work), with one study using phycocyanin to predict non-alcoholic liver disease presuming a relationship with cyanotoxins (Zhang et al. 2015)
(4) Consideration desired on region-specific criteria or limitations of national recommendations for chl a: With nearly 30% of the lakes in the temperate plains being coded as poor for chlorophyll a in the 2007 NLA, what impact would these conditional probabilities have on these lakes? Should the lake managers in this region be monitoring continuously all the time? What are the mean/median chlorophyll a levels for this part of the U.S? Regional variability may be really important and did the conditional probability approach take this into consideration or can it take it into consideration? Is there a way to evaluate if there are significant regional effects in the U.S? For nutrient standards in the U.S. and macroinvertebrate assessments, EPA has had to issue region-specific guidelines/criteria, etc. for some parameters.
(5) Greater discussion needed on limitations of NLA and need for model validation/future studies: The paper fails to address the limitations of the NLA – as a reader, I’m not aware of the limitations. I have much respect for the NLA, but I do have questions regarding the number of samples for each lake. Furthermore, a statement or two discussing the need to validate modeled data may be worthwhile. Is there a way to see if the probabilities actually align with the accuracy and type II error rates predicted by the conditional probability approach?
Abstract-Specific Comments: Near the bottom of the abstract, the units seem quite high for microcystins (g/L) rather than micrograms/L. The micro Greek symbol (mu) may have been lost during uploading.
Results Comments: (1) In discussing the lake exceedances of the various recommended levels by EPA, the addition of ‘drinking water’ is appropriate in my opinion. Although it is mentioned earlier in the methods, further providing the information in the results is helpful to a novice reader or a person just becoming familiar with drinking water regulations and guidelines, as the U.S. EPA child level may be presumed by a reader to be a level for recreation in a lake rather than a level associated with finished drinking water after water treatment. (2) “All lakes had reported chl a concentrations that exceeded detection limits” Does this mean that some were over range? Or does this mean that “All lakes had detectable levels of chl a”
Discussion Comments: The wedge pattern in figure 2 is not apparent in figure 2, however, the logic makes sense and is supported visually by the conditional probability plots in fig 1. If figure 2 could have two lines of best fit (similar to the way some researchers do for funnel plots on publication bias papers), it may be easier to see the wedge shape.
Climate Articles Highlighting Current Importance of Topic: Harvell, C. D.; Kim, K.; Burkholder, J. M.; Colwell, R. R.; Epstein, P. R.; Grimes, D. J.; Hoffman, E. E.; Lipp,E. K.; Osterhaus, A. D. M. E.; Overstreet, R. M.; Porter, J. W.; Smith, G. W.; Vasta, G. R.Emerging marine diseases – climate links and anthropogenic factors Science 2000, 285, 1505– 1510
Peperzak, L.Climate change and harmful algal blooms in the North Sea Acta Oecol. 2003, 24, 139–144
Edwards, M.; Johns, D. G.; Leterme, S. C.; Svendsen, E.; Richardson, A. J.Regional climate change and harmful algal blooms in the northeast Atlantic Limnol. Oceanogr. 2006, 51 ( 2) 820– 829
Ye, C.; Shen, Z.; Zhang, T.; Feng, M.; Lei, Y.; Zhang, J.Long-term joint effect of nutrients and temperature increase on algal growth in Lake Taihu, China J Environ. Sci. 2011, 23 ( 2) 222– 227
Paerl, H. W.; Hall, N. S.; Calandrino, E. S.Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change Sci. Total Environ. 2011, 409, 1739– 1745
Davis, T. W.; Berry, D. L.; Boyer, G. L.; Gobler, C. J.The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms Harmful Algae 2009, 8, 715– 725
Articles on Phycocyanin and Toxin Indicators Ought to Be Considered:
Ahn, C.-Y.; Joung, S.-H.; Yoon, S.-K.; Oh, H.-M.Alternative alert system for cyanobacterial bloom, using phycocyanin as a level determinant J. Microbiol. 2007, 45 ( 2) 98– 104.
Makarewicz, J. C.; Boyer, G. L.; Lewis, T. .; Guenther, W.; Atkinson, J.; Arnold, M.Spatial and temporal distribution of the cyanotoxin microcystin-LR in the Lake Ontario ecosystem: Coastal embayments, rivers, nearshore and offshore, and upland lakes J. Great Lakes Res. 2009, 35, 83– 89.
Murby, A. L.Assessing spatial distributions of cyanobacteria and microcystins in N.H. lakes with implications for lake monitoring. Master’s Thesis. University of New Hampshire, 2009; p 89.
Lehman, E. M.Seasonal occurrence and toxicity of Microcystis in impoundments of the Huron River, Michigan, USA Water Res. 2007, 41, 795– 802
Lee C, Marion JW, Cheung M, Lee CS, Lee J. Associations among Human-Associated Fecal Contamination, Microcystis aeruginosa, and Microcystin at Lake Erie Beaches. International journal of environmental research and public health. 2015 Sep 11;12(9):11466-85.
Zamyadi A, Dorner S, Ndong M, Ellis D, Bolduc A, Bastien C, Prévost M. Application of in vivo measurements for the management of cyanobacteria breakthrough into drinking water treatment plants. Environmental Science: Processes & Impacts. 2014;16(2):313-23.
Zhang F, Lee J, Liang S, Shum CK. Cyanobacteria blooms and non-alcoholic liver disease: evidence from a county level ecological study in the United States. Environmental Health. 2015 May 7;14(1):41.
References 1. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus AD, Overstreet RM, Porter JW, Smith GW, Vasta GR: Emerging marine diseases--climate links and anthropogenic factors.Science. 1999; 285 (5433): 1505-10 PubMed Abstract 2. Peperzak L: Climate change and harmful algal blooms in the North Sea. Acta Oecologica. 2003; 24: S139-S144 Publisher Full Text 3. Edwards M, Johns D, Leterme S, Svendsen E, Richardson A: Regional climate change and harmful algal blooms in the northeast Atlantic. Limnology and Oceanography. 2006; 51 (2): 820-829 Publisher Full Text 4. Ye C, Shen Z, Zhang T, Fan M, Lei Y, Zhang J: Long-term joint effect of nutrients and temperature increase on algal growth in Lake Taihu, China.J Environ Sci (China). 2011; 23 (2): 222-7 PubMed Abstract 5. Paerl HW, Hall NS, Calandrino ES: Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change.Sci Total Environ. 2011; 409 (10): 1739-45 PubMed Abstract | Publisher Full Text 6. Davis T, Berry D, Boyer G, Gobler C: The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae. 2009; 8 (5): 715-725 Publisher Full Text 7. Ahn CY, Joung SH, Yoon SK, Oh HM: Alternative alert system for cyanobacterial bloom, using phycocyanin as a level determinant.J Microbiol. 2007; 45 (2): 98-104 PubMed Abstract 8. Makarewicz J, Boyer G, Lewis T, Guenther W, Atkinson J, Arnold M: Spatial and temporal distribution of the cyanotoxin microcystin-LR in the Lake Ontario ecosystem: Coastal embayments, rivers, nearshore and offshore, and upland lakes. Journal of Great Lakes Research. 2009; 35: 83-89 Publisher Full Text 9. Murlby AL: Assessing spatial distributions of cyanobacteria and microcystins in N.H. lakes with implications for lake monitoring. 2009; Master's Thesis (University of New Hampshire): 89 10. Lehman EM: Seasonal occurrence and toxicity of Microcystis in impoundments of the Huron River, Michigan, USA.Water Res. 2007; 41 (4): 795-802 PubMed Abstract | Publisher Full Text 11. Lee C, Marion JW, Cheung M, Lee CS, Lee J: Associations among Human-Associated Fecal Contamination, Microcystis aeruginosa, and Microcystin at Lake Erie Beaches.Int J Environ Res Public Health. 2015; 12 (9): 11466-85 PubMed Abstract | Publisher Full Text 12. Zamyadi A, Dorner S, Ndong M, Ellis D, Bolduc A, Bastien C, Prévost M: Application of in vivo measurements for the management of cyanobacteria breakthrough into drinking water treatment plants.Environ Sci Process Impacts. 2014; 16 (2): 313-23 PubMed Abstract | Publisher Full Text 13. Zhang F, Lee J, Liang S, Shum CK: Cyanobacteria blooms and non-alcoholic liver disease: evidence from a county level ecological study in the United States.Environ Health. 2015; 14: 41 PubMed Abstract | Publisher Full Text
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