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Review
Peer-Review Record

Thermal Effects on Ecological Traits of Salmonids

by Bror Jonsson
Reviewer 1:
Reviewer 2: Anonymous
Reviewer 3:
Submission received: 20 May 2023 / Revised: 22 June 2023 / Accepted: 23 June 2023 / Published: 25 June 2023
(This article belongs to the Special Issue Effect of Climate Change on Salmonid Fishes in Rivers)

Round 1

Reviewer 1 Report

The review paper is devoted to consideration potential effects of climate change and temperature as its most pronounced factor on ecological traits of salmonid fishes and their populations. The paper is divided into several sections, each focused on definite ecological traits (metabolic rates and aerobic scope, growth, adult size, reproductive and behavioural traits), reviewed data are discussed and potential for future research is delineated.

Doubtless this review paper will be of great interest for researchers studying effects of climate change on fish populations, and salmonids in particular. The paper is well prepared and structured, and includes the most thorough and contemporary data and considerations on the topic. It is quite difficult to propose anything useful for improving this manuscript, taking into account its high scientific level. The only one thing that I would recommend is adding some data regarding influence of temperature in early developmental stages on sex ratio in salmonids (see below). Please also see some minor specific comments below.

Specific comments

Lines 61-63 and Table 1. For what stages of development do these values applicable? Only for juveniles, as written in the lines 61-63? While different life stages can be different in thermal sensitivity, I suppose including data about life stage in the table capture can be valuable for readers.

Table 1, line 2. (65, 66, 187,188) should be changed to [65, 66, 187,188]

Table 1, line 5. “keye salmon” should be changed to “Sockeye salmon”.

Line 73.  (24) should be changed to [24]

Line 151. “stable temperature (15 ± 2.5 °C)” should be changed to “stable temperature (15 ± 0.5 °C)”

Line 200. (65,66] should be changed to [65,66].

Lines 288-290. It looks like references are needed here. Should they be added? Or these references are the same as in the next sentence?

Line 294. «llarge-scale» should be corrected.

Line 303. “Mprphotype” should be corrected.

Lines 303-307. There is also another interesting and relevant example of four sympatric forms of half-extinct Sevan trout, Salmo ischchan, from Lake Sevan (Armenia) (Levin et al., 2022). Their variation is also partly inherited, and they also differ in morphology and life histories. If interesting in more detail, please follow this link: https://doi.org/10.1016/j.ympev.2021.107346

Line 330: “with increasing in Japanese rivers” should be changed to “with increasing temperature in Japanese rivers”?

Lines 337 and below (5. Reproductive traits). I suppose that evidences of temperature effects on sex ratio in salmonids can be also relevant, and deserve to be added to this section. There is temperature-dependent sex inversion in early development of some salmonid species. If temperature can influence sex ratio in population, hence, it influences its reproductive potential. See, for example, Azuma et al., 2004, https://doi.org/10.1016/j.aquaculture.2003.11.023

Line 382. Is it a misprint there: «the juveniles migrates»?

Line 479. “Wheras” should be changed to “Whereas”.

Line 513. Is it a misprint there?: “The mechanisms involved in thermal plasticity is little investigated.”

Comments for author File: Comments.pdf

Author Response

Response to reviewers’ report: Author’s response in red

Reviewer #1

The review paper is devoted to consideration potential effects of climate change and temperature as its most pronounced factor on ecological traits of salmonid fishes and their populations. The paper is divided into several sections, each focused on definite ecological traits (metabolic rates and aerobic scope, growth, adult size, reproductive and behavioural traits), reviewed data are discussed and potential for future research is delineated.

Doubtless this review paper will be of great interest for researchers studying effects of climate change on fish populations, and salmonids in particular. The paper is well prepared and structured, and includes the most thorough and contemporary data and considerations on the topic. It is quite difficult to propose anything useful for improving this manuscript, taking into account its high scientific level. The only one thing that I would recommend is adding some data regarding influence of temperature in early developmental stages on sex ratio in salmonids (see below). Please also see some minor specific comments below.

 

Specific comments

Lines 61-63 and Table 1. For what stages of development do these values applicable? Only for juveniles, as written in the lines 61-63? While different life stages can be different in thermal sensitivity, I suppose including data about life stage in the table capture can be valuable for readers.

I inserted ‘juvenile in the table caption

Table 1, line 2. (65, 66, 187,188) should be changed to [65, 66, 187,188]

Corrected

Table 1, line 5. “keye salmon” should be changed to “Sockeye salmon”.

Corrected

Line 73.  (24) should be changed to [24]

Corrected

Line 151. “stable temperature (15 ± 2.5 °C)” should be changed to “stable temperature (15 ± 0.5 °C)”

Corrected

Line 200. (65,66] should be changed to [65,66].

Corrected

Lines 288-290. It looks like references are needed here. Should they be added? Or these references are the same as in the next sentence?

Same reference

Line 294. «llarge-scale» should be corrected.

Corrected

Line 303. “Mprphotype” should be corrected.

Corrected

Lines 303-307. There is also another interesting and relevant example of four sympatric forms of half-extinct Sevan trout, Salmo ischchan, from Lake Sevan (Armenia) (Levin et al., 2022). Their variation is also partly inherited, and they also differ in morphology and life histories. If interesting in more detail, please follow this link: https://doi.org/10.1016/j.ympev.2021.107346

Levin et al. 2022 inserted as a new reference [94]

Line 330: “with increasing in Japanese rivers” should be changed to “with increasing temperature in Japanese rivers”?

‘temperature’ is inserted

Lines 337 and below (5. Reproductive traits). I suppose that evidences of temperature effects on sex ratio in salmonids can be also relevant, and deserve to be added to this section. There is temperature-dependent sex inversion in early development of some salmonid species. If temperature can influence sex ratio in population, hence, it influences its reproductive potential. See, for example, Azuma et al., 2004, https://doi.org/10.1016/j.aquaculture.2003.11.023

Azuma et al. (2004) were experimentally able to change the sex of genetically female sockeye salmon to males by suddenly increasing the water temperature from 9 to 18 degrees C at the time of hatching. Many died, but among those that survived 87% changed to males, However, such a catastrophe will not occur under normal conditions in natural rivers, so I feel that it is too speculative to include it. As I wrote in Jonsson & Jonsson (2014), sex changes induced by a thermal shock is not considered a natural adaptation of the fish. Therefore, I have not included Azuma et al (2004) here.

Line 382. Is it a misprint there: «the juveniles migrates»?

Yes, corrected

Line 479. “Wheras” should be changed to “Whereas”.

Yes, corrected

Line 513. Is it a misprint there?: “The mechanisms involved in thermal plasticity is little investigated.”

Yes, corrected

Reviewer 2 Report

General comment

The MS is a review paper on the relationship between ecophysiological characteristics of salmonids and environmental thermal stress conditions. Apparently, one primary intent of the review is to understand the potential for this group of fish to adapt to global warming. However, this is not said clearly. Also, a significant and, in my opinion, a most interesting part of the review is dedicated to the consequences of thermal stress at early stages in fish. However, on the whole, the review's aims need to be better defined. A significant part of the review is dedicated to describing, in a very general way, basic concepts in the thermal physiology of animals (e.g. metabolic rate, aerobic scope, thermal tolerance, etc.), but their application to salmonids is only sometimes well-defined. The list of references is mostly correct and updated. The English usage is often incorrect, sentences are sometimes criptic and there is some misspelling. I find missing a description of the diversity in the ecophysiological characteristics of salmonids and the evolution of this group of fish.

Some detailed comments

Abstract

In the abstract, the aims and the major conclusion of the review are not clearly stated.

Main text

Line 36: Animal population or animal diversity? Global warming is not the only cause of animal diversity decline.

Line 41: “physiological reactions and ecological rates”: what exactly do these terms mean? Physiological reactions to environmental stress?

Line 44: Slamonids are not only present in freshwater.

Line 66: “Populations have limited ability”; It is the individual and not the population that has a limited ability to face thermal stress (or any stress); how this reflects the survival and distribution of populations and species should be described.

Line 103: “early temperature”; an ambiguous expression to indicate body temperature during early life stages.

Lines 109-110: the definition of MMR is confusing; nothing is wrong, but expressed confusingly.

Line 122-124: “these rates”; which rates? Can “competition” or “patrolling” be difined as rates? Optimal and critical temperatures are temperature-dependent in that they can be modified by long-term adaptation. A discussion on this point would be helpful.

Line 128: “SMR should be measured”. This sentence seems to be out of context here and maybe should be reported in the previous par.

Line 137: the concept of thermal window is not defined. "...response to past selection." Do you mean that Thermal windows are the result of evolutive adaptation? Please clarify.

Lines 145-146: the upper thermal limit is set in any case by the physiological limits in aerobic capacity; the point is that the thermal limits diversity among populations with different adaptative histories is likely the result of the adaptation in the aerobic capacity to different environmental temperature regimes.

Lines 177-: the concept of early programming needs to be clarified. What is the difference from the observations reported earlier in the paragraph?

Lines 183-: “The aerobic scope represents….”; this is a definition of aerobic scope that applies to all animals, not only juvenile fish.

Lines 201-208: this is a thermal tolerance range definition that appears a bit out of context here.

Lines 296-: "Because...": does this mean that the reduced nutrient transport from the ocean is due to the animals' small size?

Line 330: “migrant males decreased with increasing in Japanese rivers.”; increasing of what?

Line 351: a parenthesis is missing;

Discussion: This is not a proper discussion but a mix of recapitulation of some previous information and a deeper description of interindividual or transgenerational effects of thermal stress at early stages.

Sentences and paragraph construction are often incorrect or may generate confusion; examples are on lines 51, 74, 109, 136, 288, 296, 309.

Misspelling: "mprphotype", on line 303; “pejus” is mispelled "prejus" throughout the text.

 

Author Response

peer-review-29663415.v1.pdf

Submission Date

20 May 2023

Date of this review

09 Jun 2023 14:02:17

 

General comment

The MS is a review paper on the relationship between ecophysiological characteristics of salmonids and environmental thermal stress conditions. Apparently, one primary intent of the review is to understand the potential for this group of fish to adapt to global warming. However, this is not said clearly. Also, a significant and, in my opinion, a most interesting part of the review is dedicated to the consequences of thermal stress at early stages in fish. However, on the whole, the review's aims need to be better defined. A significant part of the review is dedicated to describing, in a very general way, basic concepts in the thermal physiology of animals (e.g. metabolic rate, aerobic scope, thermal tolerance, etc.), but their application to salmonids is only sometimes well-defined. The list of references is mostly correct and updated. The English usage is often incorrect, sentences are sometimes criptic and there is some misspelling. I find missing a description of the diversity in the ecophysiological characteristics of salmonids and the evolution of this group of fish.

Some detailed comments

Abstract

In the abstract, the aims and the major conclusion of the review are not clearly stated.

Aim and conclusion inserted

Main text

Line 36: Animal population or animal diversity? Global warming is not the only cause of animal diversity decline.

Correct, the text is changed to ‘The climate change is one of the reasons why animal populations decline,

Line 41: “physiological reactions and ecological rates”: what exactly do these terms mean? Physiological reactions to environmental stress?

Changed to ‘such as changes in biochemical reactions in the body and ecological traits such as growth, body size, age at maturity and behaviour’

Line 44: Slamonids are not only present in freshwater.

I understand that you mean ‘salmonid’, and yes, you are correct.

The text is changed to: ‘and as anadromous fish migrating in sea water’

Line 66: “Populations have limited ability”; It is the individual and not the population that has a limited ability to face thermal stress (or any stress); how this reflects the survival and distribution of populations and species should be described.

‘Populations’ is changed to ‘Individuals’

Line 103: “early temperature”; an ambiguous expression to indicate body temperature during early life stages.

Changed to ‘temperature during early life stages’

Lines 109-110: the definition of MMR is confusing; nothing is wrong, but expressed confusingly.

Changed to ‘MMR is the maximum rate of oxygen consumption that fish can achieve and use…’

Line 122-124: “these rates”; which rates? Can “competition” or “patrolling” be difined as rates? Optimal and critical temperatures are temperature-dependent in that they can be modified by long-term adaptation. A discussion on this point would be helpful.

‘Rates’ changed to ‘functions’.

Line 128: “SMR should be measured”. This sentence seems to be out of context here and maybe should be reported in the previous par.

Yes, thank you. The paragraph was moved forward

Line 137: the concept of thermal window is not defined. "...response to past selection." Do you mean that Thermal windows are the result of evolutive adaptation? Please clarify.

‘Thermal window’ is omitted

Lines 145-146: the upper thermal limit is set in any case by the physiological limits in aerobic capacity; the point is that the thermal limits diversity among populations with different adaptative histories is likely the result of the adaptation in the aerobic capacity to different environmental temperature regimes.

Thank you, changed to: The upper thermal limit is set by the physiological limits in aerobic capacity. Thermal limit diversity among populations with different adaptive histories is likely a result of adaptations in aerobic capacity to different environmental temperature regimes.

Lines 177-: the concept of early programming needs to be clarified. What is the difference from the observations reported earlier in the paragraph?

Changed to: Exposure to low temperatures at an early stage in life increases the temperature dependent SMR. Such an early programming of the metabolic rate has consequences for later growth, feeding and locomotor activity.

Lines 183-: “The aerobic scope represents….”; this is a definition of aerobic scope that applies to all animals, not only juvenile fish.

‘Juvenile fish’ changed to ‘organisms’

Lines 201-208: this is a thermal tolerance range definition that appears a bit out of context here.

Yes, you are right, the paragraph is moved to line 151.

Lines 296-: "Because...": does this mean that the reduced nutrient transport from the ocean is due to the animals' small size?

Yes, both smaller and fewer

Line 330: “migrant males decreased with increasing in Japanese rivers.”; increasing of what?

Temperature is inserted

Line 351: a parenthesis is missing;

Corrected

Discussion: This is not a proper discussion but a mix of recapitulation of some previous information and a deeper description of interindividual or transgenerational effects of thermal stress at early stages.

The discussion is improved.

Comments on the Quality of English Language

Sentences and paragraph construction are often incorrect or may generate confusion; examples are on lines 51, 74, 109, 136, 288, 296, 309.

Misspelling: "mprphotype", on line 303; “pejus” is mispelled "prejus" throughout the text.

Corrected

Reviewer 3 Report

The review is very well written and extensive; I have only some minor recommendations before acceptance for publication. Please add the author and date of every taxon at the first mention, including supraspecies levels (e.g., L44-45).

 

Author Response

Reviewer #3

The review is very well written and extensive; I have only some minor recommendations before acceptance for publication. Please add the author and date of every taxon at the first mention, including supraspecies levels (e.g., L44-45).

Thank you. Authors and years are included

Round 2

Reviewer 2 Report

The MS is significantly improved. I have only a few minor points to rise, mainly formal:
- The sentence on line 75 is still confusing: a population can go extinct because of the limits in the individual capacity to face thermal stress; I suggest: "Individuals have a limited ability to face thermal stress and adjust to rapidly changing temperature. Consequently, populations may decline, extirpate, or even go extinct when the climate changes quickly."
- The sentence on Lines 131-133 will be more precise if divided: "....body mass. Mass specific SMR declines...."
- Line 215: I am not convinced by using the term "programmed" for the results obtained by Alvarez et al. 2006. Which is the program, and what is programmed?

The quality of English is adequate.

Author Response

Response to reviewer #2

The sentence on line 75 is still confusing: a population can go extinct because of the limits in the individual capacity to face thermal stress; I suggest: "Individuals have a limited ability to face thermal stress and adjust to rapidly changing temperature. Consequently, populations may decline, extirpate, or even go extinct when the climate changes quickly."

Text changed as suggested
- The sentence on Lines 131-133 will be more precise if divided: "....body mass. Mass specific SMR declines...."

Sentence divided as suggested


  • - Line 215: I am not convinced by using the term "programmed" for the results obtained by Alvarez et al. 2006. Which is the program, and what is programmed?
  • Changed to 'influenced on'
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