Off-Flavors in Aquacultured Fish: Origins and Implications for Consumers
, Paloma N. N. Freitas 1,2,†, Juliana P. Souza 1,2, Thalita M. Oliveira 1,2, Isabella Brites 1,2 and Ernani Pinto 1,3,*Round 1
Reviewer 1 Report
Thank you for selecting an important subject for a MS. However, the MS did not really contain new information and some key aspects were missing. It seems that this subject was unfamiliar to the authors and many typically used terms in the field were replaced by unsuitable ones. I stronly suggest a thorough editing and adding the most recent information before the MS can be published.
More detailed comments can be found below.
14 remove phosphate
Although phosphate content has been studied, decreased phosphate content
does not lead to decreased off-flavor problems.
20 remove in the future
It should currently too.
Keywords
Replace fish cage with a better keyword. Fish cage was not mentioned at all in the text.
Intro
31-32 Add references to these statements.
35 bioaccumulated
40-41 Rephrase the sentence.
46-52 Does this apply globally? You might want to add if this applies to
northern or southern hemisphere or both.
59 geosmin is often abbreviated GSM
73-74 GSM is semi-volatile
82 In 1969, it was identified that GSM and MIB cause these flavors but
the muddy off-flavor was reported already in the 1930´s.
83-86 You should add that in some countries ,consumers can accept fish
with certain amount of off-flavor while in others they are not.
92 at low levels
95 typically this means sensory analysis =tasting
3
116 Headspace solid-phase microextraction (HS-SPME)
Actually SPME is often a labor-intensive method which requires
expensive consumables. Not suitable for everyone.
118 Shake bar-> stir bar
167-168 gills are the main route, then intestinal tract and skin. Add
a reference here.
166 hydrophobic -> lipophilic
176-177 coumpound clearance -> depuration
179 Remove usually. Usually the sensory threshold in salmonids is at
0.7-0.9 µg/kg and only rarely 0.25 µg/kg has been
reported (Robertson et al. 2005).
5
198 TiO2 subsript 2
211 There are other factors as well, eg. water temperature, flow rate
etc. Add them with references.
211-226
Lindholm-Lehto et al. used European whitefish, not tilapia. Correct this.
cleaning out-> depuration
247 In that study it took 16 days but in that study circulation water
was mixed with clean water leading to longer depuration time. This
cannot be genralized. Rephrase.
Author Response
Dear Dr. Esteban,
We thank the Editor and reviewers for pointing out some important modifications needed in our revision.
All comments from referees are well directed and have been of help to us in revising and improving our article. I am uploading in the MDPI - Fishes website a new version of our manuscript, considering all referees’ queries and comments. The revision has been modified to accommodate questions and suggestions of the referees, as detailed on the response on the accompanying sheets.
I hope that it will be satisfactory to be accepted for publication.
All my best and I will be looking forward to hearing from you.
Yours Sincerely,
Ernani Pinto and Jéssica Moretto
Reviewer 1:
Thank you for selecting an important subject for a MS. However, the MS did not really contain new information and some key aspects were missing. It seems that this subject was unfamiliar to the authors and many typically used terms in the field were replaced by unsuitable ones. I stronly suggest a thorough editing and adding the most recent information before the MS can be published.
Author’s answer: We thank referee #1 comments. We agree with all suggestions and below we answered all queries. As suggested, the changes have been made and marked in yellow.
More detailed comments can be found below.
14 remove phosphate. Although phosphate content has been studied, decreased phosphate content does not lead to decreased off-flavor problems. 20 remove in the future It should currently too.
Author’s answer: Thank you for the comments. We replace the phosphate with phosphorus, due to many studies describe that the presence of phosphorus and nitrogen in water favors episodes of cyanobacterial blooms, which produce off-flavors as secondary metabolites. In other words, reducing the episodes of cyanobacteria and other phytoplankton blooms, consequently, reduces the production of off-flavors. As suggested, in the future was removed.
Jing Li, Lars-Anders Hansson and Kenneth M. Persson. Nutrient Control to Prevent the Occurrence of Cyanobacterial Blooms in a Eutrophic Lake in Southern Sweden, Used for Drinking Water Supply. Water 2018, 10(7), 919; https://doi.org/10.3390/w10070919
Vanderley, R.F., Ger, K.A., Becker, V. et al. Abiotic factors driving cyanobacterial biomass and composition under perennial bloom conditions in tropical latitudes. Hydrobiologia, 2021, 848, 943–960. https://doi.org/10.1007/s10750-020-04504-7
Royer, T.V. Stoichiometry of nitrogen, phosphorus, and silica loads in the Mississippi-Atchafalaya River basin reveals spatial and temporal patterns in risk for cyanobacterial blooms. Limnol Oceanogr, 2020, 65: 325-335. https://doi.org/10.1002/lno.11300
Keywords
Replace fish cage with a better keyword. Fish cage was not mentioned at all in the text.
Author’s answer: We replace the Fish cage with bioaccumulation.
Intro 31-32 Add references to these statements.
Author’s answer: the references 1 and 2 were added.
- Van Rijn, J. The Potential for Integrated Biological Treatment Systems in Recirculating Fish Culture—A Review. 338 Aquaculture 1996, 139, 181–201, https://doi.org/10.1016/0044-8486(95)01151-X. 339
- Gutierrez-Wing, M.T.; Malone, R.F. Biological Filters in Aquaculture: Trends and Research Directions for Freshwater 340 and Marine Applications. Aquacultural Engineering 2006, 34, 163–171, https://doi.org/10.1016/j.aquaeng.2005.08.003
35 bioaccumulated.
Author’s answer: As suggested, it was corrected.
40-41 Rephrase the sentence.
Author’s answer: As suggested, the sentence was rewritten to “These metabolites are a major concern in a wide range of environments as they make end products undesirable.”
46-52 Does this apply globally? You might want to add if this applies to northern or southern hemisphere or both.
Author’s answer: Yes, it does. Several studies have shown the climate change and other factors increase the incidence of cyanobacteria blooms worldwide, for example, we cite studies below.
Gophen, M. Climate Change-Enhanced Cyanobacteria Domination in Lake Kinneret: A Retrospective Overview. Water 2021, 13, 163. https://doi.org/10.3390/w13020163
Paerl, Hans W., et al. "Mitigating a global expansion of toxic cyanobacterial blooms: confounding effects and challenges posed by climate change." Marine and Freshwater Research 71.5 (2019): 579-592.
Havens, Karl E., et al. "Dynamics of cyanobacteria blooms are linked to the hydrology of shallow Florida lakes and provide insight into possible impacts of climate change." Hydrobiologia 829.1 (2019): 43-59.
59 geosmin is often abbreviated GSM
Author’s answer: We thank the reviewer for this observation. However, the explanation for using GEO was based on the work of Churro et al. (2020) in which they mention that the molecular basis of geosmin production is the geosmin synthase gene (geoA), normally the abbreviation of the compound and the gene is the same. However, both terms (GEO and GSM) can be used. In order to standardized for the readers, we kept as GEO in the entire revision.
Churro, C., Semedo-Aguiar, A. P., Silva, A. D., Pereira-Leal, J. B., & Leite, R. B. (2020). A novel cyanobacterial geosmin producer, revising Geo A distribution and dispersion patterns in Bacteria. Scientific reports, 10(1), 1-18.
73-74 GSM is semi-volatile
Author’s answer: As suggested, it was corrected.
82 In 1969, it was identified that GSM and MIB cause these flavors but the muddy off-flavor was reported already in the 1930´s.
Author’s answer: We are grateful for this observation. As suggested, we made the necessary corrections and marked it in yellow.
83-86 You should add that in some countries, consumers can accept fish with certain amount of off-flavor while in others they are not.
Author’s answer: As suggested, we added this information to the text and it’s highlighted in yellow.
92 at low levels 95 typically this means sensory analysis = tasting
Author’s answer: as suggested, it was corrected.
116 Headspace solid-phase microextraction (HS-SPME). Actually, SPME is often a labor-intensive method which requires expensive consumables. Not suitable for everyone.
Author’s answer: The SPME method offers some important advantages. Speed and simplicity, single-step extraction, reducing sample preparation time by 70%. Versatility, featuring selectivity of different available analytes, adaptable to any HPLC or GC system, easy mechanization/automation. Efficient and economical, it uses practically no solvents, in addition to allowing, on average, more than 50 extractions per fiber. Relatively low operating cost, commercial devices for your application are considerably reusable (Watson et al., 2000; Pawliszyn, 1997).
Watson SB, Brownlee B, Satchwill T, Hargesheimer EE (2000) Quantitative analysis of trace levels of geosmin and MIB in source and drinking water using headspace SPME. Water Research 34: 2818-2828.
Pawliszyn J (1997) Solid phase microextraction: Theory and practice. New York; Toronto: J. Wiley.
118 Shake bar-> stir bar
Author’s answer: As suggested, it’s done and is highlighted in yellow.
167-168 gills are the main route, then intestinal tract and skin. Add a reference here.
Author’s answer: As suggested, the reference was added: Howgate P. Tainting of farmed fish by geosmin and 2-methyl-iso-borneol: a review of sensory aspects and of uptake/depuration. Aquaculture. 2004; 234:155–181. Doi: 10.1016/j.aquaculture.2003.09.032.
166 hydrophobic -> lipophilic
Author’s answer: As suggested, hydrophobic was replaced with lipophilic and it is highlighted in yellow.
176-177 compound clearance -> depuration
Author’s answer: As suggested, it’s done and highlighted in yellow.
179 Remove usually. Usually, the sensory threshold in salmonids is at 0.7-0.9 µg/kg and only rarely 0.25 µg/kg has been reported (Robertson et al. 2005).
Author’s answer: As suggested, we made changes to the text and added the cited reference.
198 TiO2 subscript 2
Author’s answer: As suggested, it’s done.
211 There are other factors as well, eg. Water temperature, flow rate etc. Add them with references.
Author’s answer: As suggested, we have added other examples of factors, as well as their appropriate references.
211-226 Lindholm-Lehto et al. used European whitefish, not tilapia. Correct this. Cleaning out-> depuration
Author’s answer: As suggested, it’s done and highlighted in yellow.
247 In that study it took 16 days but in that study circulation water was mixed with clean water leading to longer depuration time. This cannot be generalized. Rephrase.
Author’s answer: As suggested, we rewrote this part in the text.
Reviewer 2 Report
- This article has been improved since the first round of review, but still has some deficiencies. The authors have not definitively clarified the exact focus and/or have included sections that create confusion in that regard. In some instances the focus appears to be off-flavor in RAS (abstract and Section 1 Intro), but in other areas the article drifts to discussion of ponds and outdoor systems. This must be improved. Perhaps clarification in the title, whether the article intends to generally cover off-flavor in freshwater fish produced in aquaculture settings or specific production systems such as RAS? Improved focus would then need to be addressed accordingly throughout the article.
- Next the Intro. (Section 1) is very short and seems focused on RAS. Even then if the focal point is RAS, the description is not accurate or thorough enough. This section requires clarification towards the focus of the review and should be more than a few paragraphs regardless of the decided focus.
- There are still some inaccuracies and inadequate word choices used in various sections of the article. Note that I will mention some specific instances below, but have not pointed out all areas that could be improved via word choice or sentence structure. There is also an inappropriate use of one-sentence paragraphs.
- Line 118 - I believe their is a typo, "shake" bar should be "stir" bar
- One page 5 the term "fish pulp" is used. I am not familiar with this terminology and it is likely not the best word choice
- Line 234-235 - Fish species should be noted as part of this sentence
- Line 239-242 - Please check the references. One of these articles did not report a profound temperature effect as was implied by your text.
- Line 256 - Use of the term scrubbing in context to the Davidson et al. article. I am familiar with this article and don't believe these authors ever used the term "scrubbing" in the paper. Please improve word choice.
- Line 260 - Effect of off-flavors on "wildlife" - The term wildlife is certainly poor word choice in this instance as the article discusses off-flavor in captively propagated domestic fish.
- The conclusions were very basic and insufficient
Author Response
Dear Dr. Esteban,
We thank the Editor and reviewers for pointing out some important modifications needed in our revision.
All comments from referees are well directed and have been of help to us in revising and improving our article. I am uploading in the MDPI - Fishes website a new version of our manuscript, considering all referees’ queries and comments. The revision has been modified to accommodate questions and suggestions of the referees, as detailed on the response on the accompanying sheets.
I hope that it will be satisfactory to be accepted for publication.
All my best and I will be looking forward to hearing from you.
Yours Sincerely,
Ernani Pinto and Jessica Moretto
Reviewer 2:
This article has been improved since the first round of review, but still has some deficiencies. The authors have not definitively clarified the exact focus and/or have included sections that create confusion in that regard. In some instances, the focus appears to be off-flavor in RAS (abstract and Section 1 Intro), but in other areas the article drifts to discussion of ponds and outdoor systems. This must be improved. Perhaps clarification in the title, whether the article intends to generally cover off-flavor in freshwater fish produced in aquaculture settings or specific production systems such as RAS? Improved focus would then need to be addressed accordingly throughout the article.
Author’s answer: Thank you for all comments, the manuscript has been revised to accommodate questions and suggestions of the referee.
As suggested, the title was modified to Off-flavors in aquaculture fish: origins and implications for consumers.
As the manuscript is intended to cover off-flavors in freshwater fish produced in aquaculture environments, modifications were made throughout the manuscript, mainly in the introduction.
Next the Intro. (Section 1) is very short and seems focused on RAS. Even then if the focal point is RAS, the description is not accurate or thorough enough. This section requires clarification towards the focus of the review and should be more than a few paragraphs regardless of the decided focus.
There are still some inaccuracies and inadequate word choices used in various sections of the article. Note that I will mention some specific instances below but have not pointed out all areas that could be improved via word choice or sentence structure. There is also an inappropriate use of one-sentence paragraphs.
Author’s answer: Thank you for all comments, they were important to improve the manuscript.
In order to improve the introduction, more comprehensive information on aquaculture has been added to the text. In addition, to clarify the focus of our study, the following sentence was added: Therefore, the general objective of this review is to aggregate information about the main TOCs produced by cyanobacteria and other phytoplankton, how these compounds affect aquaculture, fish consumption and commercialization, and what are the main detection and purification methods. All changes are marked in yellow.
Line 118 - I believe their is a typo, "shake" bar should be "stir" bar
Author’s answer: Thank you for all comments, as suggested shake was changed to stir.
One page 5 the term "fish pulp" is used. I am not familiar with this terminology, and it is likely not the best word choice.
Author’s answer: As suggested fish pulp was changed to fish meat.
Line 234-235 - Fish species should be noted as part of this sentence
Author’s answer: As suggested, fish species (channel catfish) was added and marked in yellow.
Line 239-242 - Please check the references. One of these articles did not report a profound temperature effect as was implied by your text.
Author’s answer: As suggested, the reference 67 was deleted.
Line 256 - Use of the term scrubbing in context to the Davidson et al. article. I am familiar with this article and don't believe these authors ever used the term "scrubbing" in the paper. Please improve word choice.
Author’s answer: As suggested, scrubbing was replaced with cleaning.
Line 260 - Effect of off-flavors on "wildlife" - The term wildlife is certainly poor word choice in this instance as the article discusses off-flavor in captively propagated domestic fish.
Author’s answer: As suggested, wildlife was deleted.
The conclusions were very basic and insufficient
Author’s answer: As suggested, the conclusions were rewritten.
Reviewer 3 Report
Composition and structure of the review manuscript is well designed and contains the most important tasks related to the topic of off-flavors in aquatic environment. This topic has still actuality due to occurrence of off-flavors in fish reared in RAS or pond systems.
However, there are some issues in the paper that needs further revision work.
Abstract
LINE 23 please make more general or give all the species mentioned in the review
- Off-flavor compounds in the environment: an overview
LINE 89 are missing the scientific names of fish species
- Transfer of off-flavor compounds, bioaccumulation in fish, and toxicity
LINE 162-164 wrong conclusions, please rewrite it
„According to Papp et al. [63], lower concentrations of GEO were found in the fillet of carnivorous catfish (Clarias gariepinus) than in herbivorous carp (Ctenopharyngodon idella), both plankton-feeding”
In the above mentioned article: “GSM was always lower in fillets of carnivorous African catfish (C. gariepinus) and herbivorous grass carp (C. idella) than in species with other feeding habits in the same aquatic system….Geosmin concentrations were usually higher in the fillets of bottom-feeding omnivorous common carp (C. carpio) than those found in all species with other feeding habits in the same aquatic system….. “
Please complete and edit the next references:
18,41,42, 46, 50, 52, 53, 58, 99
Comments for author File: 
Comments.pdf
Author Response
Dear Dr. Esteban,
We thank the Editor and reviewers for pointing out some important modifications needed in our revision.
All comments from referees are well directed and have been of help to us in revising and improving our article. I am uploading in the MDPI - Fishes website a new version of our manuscript, considering all referees’ queries and comments. The revision has been modified to accommodate questions and suggestions of the referees, as detailed on the response on the accompanying sheets.
I hope that it will be satisfactory to be accepted for publication.
All my best and I will be looking forward to hearing from you.
Yours Sincerely,
Ernani Pinto and Jéssica Moretto
Reviewer 3:
Composition and structure of the review manuscript is well designed and contains the most important tasks related to the topic of off-flavors in aquatic environment. This topic has still actuality due to occurrence of off-flavors in fish reared in RAS or pond systems.
However, there are some issues in the paper that needs further revision work.
Abstract
LINE 23 please make more general or give all the species mentioned in the review
Author’s answer: As suggested, we have generalized the sentence, and this is marked in yellow in the text.
- Off-flavor compounds in the environment: an overview
LINE 89 are missing the scientific names of fish species
Author’s answer: As suggested, the scientific names were added and marked in yellow.
- Transfer of off-flavor compounds, bioaccumulation in fish, and toxicity
LINE 162-164 wrong conclusions, please rewrite it.
According to Papp et al. [63], lower concentrations of GEO were found in the fillet of carnivorous catfish (Clarias gariepinus) than in herbivorous carp (Ctenopharyngodon idella), both plankton-feeding”
In the above mentioned article: “GSM was always lower in fillets of carnivorous African catfish (C. gariepinus) and herbivorous grass carp (C. idella) than in species with other feeding habits in the same aquatic system….Geosmin concentrations were usually higher in the fillets of bottom-feeding omnivorous common carp (C. carpio) than those found in all species with other feeding habits in the same aquatic system….. “
Author’s answer: As suggested, it was rewritten and marked in yellow.
According to Papp et al. [63], insignificant levels of MIB were found in five important fish species cultivated in Hungarian aquaculture, the planktivorous silver carp (Hypophthalmichthys molitrix), the herbivorous carp (Ctenopharyngodon idella), the omnivorous common carp (Cyprinus carpio), the omnivorous tilapia (Oreochromis niloticus) and the carnivorous African catfish (Clarias), but the highest concentrations of GSM were found in the bottom-feeding common carp fillet, being higher than in the silver carp or African catfish.
Please complete and edit the next references:
18,41,42, 46, 50, 52, 53, 58, 99
Author’s answer: As suggested, the references were edited and marked in yellow.
NOTE: the number of references was changed due to text modifications requested by other referees.
Round 2
Reviewer 1 Report
The authors have made corrections and modifications according to reviewers´ suggestions. In my opinion, the manuscript can be published in Fishes.
Author Response
To: Prof. Dr. Joyce Chen
Assigned Editor
Dear Dr. Chen,
We thank the Editor and reviewers for pointing out some important modifications needed in our revision.
All comments from referees were previously answered. I am uploading in the MDPI - Fishes website a new version of our manuscript without highlights.
I hope that it will be satisfactory to be accepted for publication.
All my best and I will be looking forward to hearing from you.
Yours Sincerely,
Dr. Jéssica Ap. Moretto Dr. Ernani Pinto
Post-doctoral Researcher Full Professor
University of São Paulo University of São Paulo
Reviewer 1:
The authors have made corrections and modifications according to reviewers´ suggestions. In my opinion, the manuscript can be published in Fishes.
Authors answered: Thank you for the comment. A new version without highlights was uploaded.
Reviewer 2: No comments. Answers were given in the first-round revision.
Reviewer 3: No comments. Answers were given in the first-round revision.
