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Review
Peer-Review Record

Reciprocal Role of Salamanders in Aquatic Energy Flow Pathways

Diversity 2020, 12(1), 32; https://doi.org/10.3390/d12010032
Reviewer 1: Anonymous
Reviewer 2: Anonymous
Reviewer 3: Anonymous
Diversity 2020, 12(1), 32; https://doi.org/10.3390/d12010032
Received: 19 November 2019 / Revised: 13 January 2020 / Accepted: 15 January 2020 / Published: 17 January 2020
(This article belongs to the Special Issue The Ecological Role of Salamanders as Predators and Prey)

Round 1

Reviewer 1 Report

In this review, Sanchez-Hernandez summarizes information about the role of salamanders as predators and prey in aquatic and terrestrial ecosystems. A great deal of research literature is cited and some interesting ideas are discussed, including some suggestions for future research. However, there are few new ideas or novel synthesis in this review. Much has been previously written the role of salamanders in the energy dynamics of ecosystems and how some, because of both aquatic and terrestrial life history stages, serve to couple energy and biomass of terrestrial and aquatic systems. Those same topics are covered here.

There are a number of grammatical errors that need correcting.

Here are just two examples; there are many more. Considerable editing is needed to make the manuscript acceptable.

Line 100 -  “apex predators have remarkably effects on lower trophic levels” It should be “apex predators have remarkable effects on lower trophic levels”

Line 125 – “Despite many salamander species develop defensive strategies…” It should be “Despite the fact that many salamander species develop defensive strategies…”

Some sentences did not make sense, at least to me. Perhaps grammatical errors make it difficult to understand the meaning.

For example:

Lines 107-109 – “However, the work by Atlas & Palen [50] is based on a multi-trophic modelling framework and empirical research under controlled (e.g. mesocosms) or natural conditions is required to be accepted as a general theory.”

Lines 115-116 – “In presence of apex predators (snake, otter and fish species), salamanders are profitable resource sources for higher trophic levels in the aquatic food chains and illustrate a good example about the energy and nutrient transfer from invertebrates up to apex predators (Figure 1).”

Lines 197-199 – “Larval ambystomatid salamander (marbled salamander and spotted salamanders) acquire most of their energy from copepods during early development, but from larval dipterans over ontogeny [36].”

Much of section 3.1 (Consumption of salamanders in higher trophic levels) is a simple listing of examples of salamanders serving as prey. This section would benefit from framing these examples as illustrating general principles.  

The figures as presented are not very useful. Figure 1 is a typical illustration of trophic levels. Figure 2 is simplistic and does not emphasize the three levels of aquatic-terrestrial coupling referred to in the text: (i) direct movement of salamanders between aquatic and terrestrial habitats (ii) consumption of salamanders by terrestrial predators and (iii) consumption of allochthonous food resources by salamanders.

Author Response

In this review, Sanchez-Hernandez summarizes information about the role of salamanders as predators and prey in aquatic and terrestrial ecosystems. A great deal of research literature is cited and some interesting ideas are discussed, including some suggestions for future research. However, there are few new ideas or novel synthesis in this review. Much has been previously written the role of salamanders in the energy dynamics of ecosystems and how some, because of both aquatic and terrestrial life history stages, serve to couple energy and biomass of terrestrial and aquatic systems. Those same topics are covered here.

RESPONSE: I thank the reviewer for the helpful feedback on the manuscript. In the revised version, I have paid more attention to underline new ideas to build future research. In addition, English style was revised by a by a native English-speaking colleague. Please note that I resubmitted the manuscript with the changes clearly highlighted using the "Track Changes" function in Microsoft Word as Sally Xia (Assistant Editor) suggested.

 

-There are a number of grammatical errors that need correcting.

RESPONSE: The revised manuscript has been checked by a native English-speaking colleague (A. Nunn, University of Hull).

 

-Here are just two examples; there are many more. Considerable editing is needed to make the manuscript acceptable.

Line 100 - “apex predators have remarkably effects on lower trophic levels” It should be “apex predators have remarkable effects on lower trophic levels”

RESPONSE: Revised as suggested.

 

-Line 125 – “Despite many salamander species develop defensive strategies…” It should be “Despite the fact that many salamander species develop defensive strategies…”

RESPONSE: Revised as suggested.

 

-Some sentences did not make sense, at least to me. Perhaps grammatical errors make it difficult to understand the meaning. For example:

Lines 107-109 – “However, the work by Atlas & Palen [50] is based on a multi-trophic modelling framework and empirical research under controlled (e.g. mesocosms) or natural conditions is required to be accepted as a general theory.”

RESPONSE: I have rewritten this sentence to improve readability.

 

-Lines 115-116 – “In presence of apex predators (snake, otter and fish species), salamanders are profitable resource sources for higher trophic levels in the aquatic food chains and illustrate a good example about the energy and nutrient transfer from invertebrates up to apex predators (Figure 1).”

RESPONSE: I have rewritten this sentence to improve readability.

 

-Lines 197-199 – “Larval ambystomatid salamander (marbled salamander and spotted salamanders) acquire most of their energy from copepods during early development, but from larval dipterans over ontogeny [36].”

RESPONSE: I have rewritten this sentence to improve readability.

 

-Much of section 3.1 (Consumption of salamanders in higher trophic levels) is a simple listing of examples of salamanders serving as prey. This section would benefit from framing these examples as illustrating general principles.

RESPONSE: Revised as suggested. Specifically, I have paid more attention to contextualise the importance of salamanders as prey in general principles (structure and function of communities and ecosystems; lines 231-237). Please also note that the concepts of cannibalism and intraguild predator that drive the structure and organization of some salamander assemblages is now better developed as suggested by reviewer 2.

 

-The figures as presented are not very useful. Figure 1 is a typical illustration of trophic levels. Figure 2 is simplistic and does not emphasize the three levels of aquatic-terrestrial coupling referred to in the text: (i) direct movement of salamanders between aquatic and terrestrial habitats (ii) consumption of salamanders by terrestrial predators and (iii) consumption of allochthonous food resources by salamanders.

RESPONSE: I agree with the reviewer that Figure 1 is a typical illustration of trophic levels, but it also provides to the reader information about predator-prey interactions and the key role of salamanders in aquatic systems (they are both predators and prey), which is the keystone of this review. I do believe this figure is helpful for readers to contextualise the key role of salamanders and was kept in the revised version. On the other hand, figure 2 is very simplistic and it does not include the three levels of aquatic-terrestrial coupling as the reviewer highlighted, and therefore was deleted in the revised version. Please note that reviewer 3 asked for a new figure, which is now included in the revised version.

Reviewer 2 Report

Overall, this manuscript has considerable promise. I think the topic would be of wide interest to a number of readers working in aquatic systems, food-web studies, and herpetology. However, I would not consider this a review paper - it is not thorough enough on the topic and does not provide a broad enough synthesis on predator-prey relationships. Rather, it highlights a select few studies on the topic, presents some interesting facts, and then has a few sentences that fail to present a cohesive and focused idea on the section topic. In addition, I think this manuscript is particularly biased towards studies conducted in Europe. Salamander diversity is higher in Eastern North America and a large number of studies have been conducted in this region, yet many of the foundational and important studies on this topic are not discussed.

Diet description section: The author makes statements but fails to follow up on them and explain them in more detail. For example, discuss the seasonal changes in diet for salamanders.

Also, while the author discusses diet in term of taxonomic descriptions, I think discussing their diet in terms of prey guilds or prey traits would make this section stronger as it can be generalized across multiple systems or species.

What general patterns emerge from studies that focus on salamander diets? This is a review paper and these patterns should be synthesized and described for the readers. The author is mostly cherry-picking a few studies and failing to discuss it in a broader perspective that would be of interest to a wide-readership.

Top-down control section: All of the example highlighted are from studies focused on larval salamanders or aquatic salamanders. The author should also highlight and discuss studies examining top-down control in adult, terrestrial species.

For example, see here:

Hickerson, C. A. M., Anthony, C. D., & Walton, B. M. (2017). Eastern Red-backed Salamanders regulate top-down effects in a temperate forest-floor community. Herpetologica, 73(3), 180-189.

Consumption of salamanders in higher trophic levels section: I found this section to be quite confusing and incomplete as there is a large section and amount of detail focused on mustelid predators and fish predators, yet the author briefly touches on predators that may consume salamanders more frequently (snakes) or ignores other important predator groups (other salamanders). Cannibalism and intraguild predator are important interactions that drive the structure and organization of some salamander assemblages, but this is completely ignored in this review. Below are just a fraction of the available literature on this topic.

Yurewicz, K. L. (2004). A growth/mortality trade-off in larval salamanders and the coexistence of intraguild predators and prey. Oecologia, 138(1), 102-111.

Gustafson, M. P. (1993). Intraguild predation among larval plethodontid salamanders: a field experiment in artificial stream pools. Oecologia, 96(2), 271-275.

Brodman, R. (1996). Effects of intraguild interactions on fitness and microhabitat use of larval Ambystoma salamanders. Copeia, 372-378.

Resetarits Jr, W. J. (1991). Ecological interactions among predators in experimental stream communities. Ecology, 72(5), 1782-1793.

Nyman, S., Wilkinson, R. F., & Hutcherson, J. E. (1993). Cannibalism and size relations in a cohort of larval ringed salamanders (Ambystoma annulatum). Journal of Herpetology, 78-84.

Wildy, E. L., Chivers, D. P., Kiesecker, J. M., & Blaustein, A. R. (2001). The effects of food level and conspecific density on biting and cannibalism in larval long-toed salamanders, Ambystoma macrodactylum. Oecologia, 128(2), 202-209.

Pfennig, D. W., Sherman, P. W., & Collins, J. P. (1994). Kin recognition and cannibalism in polyphenic salamanders. Behavioral Ecology, 5(2), 225-232.

Salamanders as energy subsides for higher trophic levels section: As with most of the manuscript, this section is just a checklist of prior studies on the topic and fails to meaningfully synthesize these patterns into a broader discussion and generalizable pattern.

Salamanders as promoters of aquatic-terrestrial coupling (lateral energy transfers) section: For the three levels that promote aquatic-terrestrial coupling by the author, why not discuss in detail studies that have supported these ideas? The author puts forth these ideas but fails to provide any evidence that salamanders actually fill these roles in their ecosystems by not discussing prior studies.

Conclusions: Again, I think this section needs to do a better job of synthesizing there patterns to a broad audience instead of selecting a few interesting studies to highlight. The paper as a whole fails to provide a cohesive message on the paper’s topic.

Author Response

Overall, this manuscript has considerable promise. I think the topic would be of wide interest to a number of readers working in aquatic systems, food-web studies, and herpetology. However, I would not consider this a review paper - it is not thorough enough on the topic and does not provide a broad enough synthesis on predator-prey relationships. Rather, it highlights a select few studies on the topic, presents some interesting facts, and then has a few sentences that fail to present a cohesive and focused idea on the section topic. In addition, I think this manuscript is particularly biased towards studies conducted in Europe. Salamander diversity is higher in Eastern North America and a large number of studies have been conducted in this region, yet many of the foundational and important studies on this topic are not discussed.

RESPONSE: I thank the reviewer for the constructive comments on the manuscript. In the revision, I have paid more attention to increase the geographical scope of this revision including more studies from North America as the reviewer suggested. It should be kept in mind that this review focus on aquatic systems and, and thus studies based on terrestrial species were avoid whenever possible. Please note that I resubmitted the manuscript with the changes clearly highlighted using the "Track Changes" function in Microsoft Word as Sally Xia (Assistant Editor) suggested.

 

-Diet description section: The author makes statements but fails to follow up on them and explain them in more detail. For example, discuss the seasonal changes in diet for salamanders.

RESPONSE: Revised as suggested. In the revised version, I paid more attention to discuss ontogenetic (lines 89-104) and seasonal (lines 105-120) diet changes as the reviewer suggested.

 

-Also, while the author discusses diet in term of taxonomic descriptions, I think discussing their diet in terms of prey guilds or prey traits would make this section stronger as it can be generalized across multiple systems or species.

RESPONSE: Revised as suggested. The reviewer raised an important comment about the way of describing the diet, which was included in the revised version (lines 79-89).

 

-What general patterns emerge from studies that focus on salamander diets? This is a review paper and these patterns should be synthesized and described for the readers. The author is mostly cherry-picking a few studies and failing to discuss it in a broader perspective that would be of interest to a wide-readership.

RESPONSE: Again, the reviewer brings a good point to the table. In the revised version, I have paid more attention to the take-home message about the general patterns in feeding of salamanders (lines 121-135).

 

-Top-down control section: All of the example highlighted are from studies focused on larval salamanders or aquatic salamanders. The author should also highlight and discuss studies examining top-down control in adult, terrestrial species. For example, see here:

Hickerson, C. A. M., Anthony, C. D., & Walton, B. M. (2017). Eastern Red-backed Salamanders regulate top-down effects in a temperate forest-floor community. Herpetologica, 73(3), 180-189.

RESPONSE: Revised as suggested. I thank the reviewer for the suggested paper, which is now included in the revised version. However, it is important to keep in mind that this review focus on aquatic energy flow pathways and terrestrial examples were intentionally skipped whenever possible.

 

-Consumption of salamanders in higher trophic levels section: I found this section to be quite confusing and incomplete as there is a large section and amount of detail focused on mustelid predators and fish predators, yet the author briefly touches on predators that may consume salamanders more frequently (snakes) or ignores other important predator groups (other salamanders). Cannibalism and intraguild predator are important interactions that drive the structure and organization of some salamander assemblages, but this is completely ignored in this review. Below are just a fraction of the available literature on this topic.

Yurewicz, K. L. (2004). A growth/mortality trade-off in larval salamanders and the coexistence of intraguild predators and prey. Oecologia, 138(1), 102-111.

Gustafson, M. P. (1993). Intraguild predation among larval plethodontid From another standing view todas lsalamanders: a field experiment in artificial stream pools. Oecologia, 96(2), 271-275.

Brodman, R. (1996). Effects of intraguild interactions on fitness and microhabitat use of larval Ambystoma salamanders. Copeia, 372-378.

Resetarits Jr, W. J. (1991). Ecological interactions among predators in experimental stream communities. Ecology, 72(5), 1782-1793.

Nyman, S., Wilkinson, R. F., & Hutcherson, J. E. (1993). Cannibalism and size relations in a cohort of larval ringed salamanders (Ambystoma annulatum). Journal of Herpetology, 78-84.

Wildy, E. L., Chivers, D. P., Kiesecker, J. M., & Blaustein, A. R. (2001). The effects of food level and conspecific density on biting and cannibalism in larval long-toed salamanders, Ambystoma macrodactylum. Oecologia, 128(2), 202-209.

Pfennig, D. W., Sherman, P. W., & Collins, J. P. (1994). Kin recognition and cannibalism in polyphenic salamanders. Behavioral Ecology, 5(2), 225-232.

RESPONSE: Revised as suggested. I have included a new paragraph top cover this important topic in the revised version (lines 256-278).

 

-Salamanders as energy subsides for higher trophic levels section: As with most of the manuscript, this section is just a checklist of prior studies on the topic and fails to meaningfully synthesize these patterns into a broader discussion and generalizable pattern.

RESPONSE: Revised as suggested. I paid more attention to put the history telling into a broader frame and generalizable pattern (lines 299-312 and 344-346).

 

-Salamanders as promoters of aquatic-terrestrial coupling (lateral energy transfers) section: For the three levels that promote aquatic-terrestrial coupling by the author, why not discuss in detail studies that have supported these ideas? The author puts forth these ideas but fails to provide any evidence that salamanders actually fill these roles in their ecosystems by not discussing prior studies.

RESPONSE: Revised as suggested. In the revised version I have integrated the ideas (three levels of aquatic-terrestrial coupling) with supporting literature (lines 361-377).

 

-Conclusions: Again, I think this section needs to do a better job of synthesizing there patterns to a broad audience instead of selecting a few interesting studies to highlight. The paper as a whole fails to provide a cohesive message on the paper’s topic.

RESPONSE: Revised as suggested. I paid more attention to highlight the take-home message contextualise it into a broader perspective.

Reviewer 3 Report

Sánchez-Hernández review

General comments:

Sánchez-Hernández did a good job integrating a lot of the literature on the role of salamanders in food webs and across ecosystem boundary flow of energy. The paper was well-written. I also study salamanders but am not as convinced that they are as important as the author implies, and wonder if the author may have cherry-picked articles that supported his ideas. The figures over-simplified some of the food web dynamics. If the author would incorporate more of the literature that found salamanders are not a keystone species, it would be a lot more believable. A figure summarizing the number of papers that supported vs. did not support the different roles (translocators of nutrients, source of nutrients to aquatic systems, trophic cascades, nutritious energy source for higher trophic levels, etc.) would be helpful for digesting the information. 

Specific comments:

In “salamanders as predators” I was surprised the author didn’t cite anything anything about intraguild predation among salamanders (see papers by Tom Anderson and Ray Semlitsch). They have also done some work on other predators of salamanders, including dragonfly nymphs and fish

L38 - remove “on”

L43 - “prey” not “preys”

L59 - “without movable accessory” is a little unclear. What about shell and caseless? Or some other better word choice.

L75 - by immature do you mean juvenile?

L82 - instead of “co-specimens” wouldn’t conspecifics be a better word?

L110 - Rowland et al. 2017 (Oecologia) and Anderson et al. 2017 (Oecologia) did not find evidence of trophic cascades with larval salamanders

L121 - I am confused about what the n = 69 vs. 89 means. Is that the number of salamander species and the number of predators?

Fig 1 - There are way more invertebrate predators of salamanders than this figure implies. Dragonfly nymphs, Dytisids, Notonectids, and many other species are documented as predators of the larval stage. Also why is there a salmon for the representative fish? I think a bluegill might be a better representation.

L169-170 - What do you mean by not massive? In almost all systems, the presence of fishes means that salamanders rarely make it to metamorphosis. Do you mean that salamanders are not a large component of fish diets?

L197-199 - I don’t necessarily agree with this. A lot of their energy come from Cladocerans, which are a better food source (higher in nutrients) than copepods

L225 - ‘Keystone’ is a strong word. Would energy transfer collapse without them?

L271-273 - This last sentence seems tacked on and not the point you want to end with. What are the overall conclusions you want people to take away?







Author Response

Sánchez-Hernández did a good job integrating a lot of the literature on the role of salamanders in food webs and across ecosystem boundary flow of energy. The paper was well-written. I also study salamanders but am not as convinced that they are as important as the author implies, and wonder if the author may have cherry-picked articles that supported his ideas. The figures over-simplified some of the food web dynamics. If the author would incorporate more of the literature that found salamanders are not a keystone species, it would be a lot more believable. A figure summarizing the number of papers that supported vs. did not support the different roles (translocators of nutrients, source of nutrients to aquatic systems, trophic cascades, nutritious energy source for higher trophic levels, etc.) would be helpful for digesting the information.

RESPONSE: I thank the reviewer for the constructive comments on the manuscript. In the revised version, I have paid more attention to underscore that salamanders not always function as a keystone species (e.g. lines 165-171). In addition, I have also included the requested figure with was used as take-home message in the Conclusion section. Please note that I resubmitted the manuscript with the changes clearly highlighted using the "Track Changes" function in Microsoft Word as Sally Xia (Assistant Editor) suggested.

 

Specific comments:

-In “salamanders as predators” I was surprised the author didn’t cite anything about intraguild predation among salamanders (see papers by Tom Anderson and Ray Semlitsch). They have also done some work on other predators of salamanders, including dragonfly nymphs and fish

RESPONSE: The reviewers brings a good point to the table, this was also suggested by reviewer 2. The concepts of cannibalism and intraguild predator that drive the structure and organization of some salamander assemblages are now better developed in lines 256-278. More specifically, I have included works by Tom Anderson and Ray Semlitsch (Journal of Animal Ecology 85:548–558; Journal of Zoology, 94:23–30) in addition to papers suggested by reviewer 2.

 

-L38 - remove “on”

RESPONSE: Revised as suggested.

 

-L43 - “prey” not “preys”

RESPONSE: Revised as suggested.

 

-L59 - “without movable accessory” is a little unclear. What about shell and caseless? Or some other better word choice.

RESPONSE: Revised as suggested. I changed “without movable accessory (cases/tubes)” with “without hard external structures (cases/shells)

 

-L75 - by immature do you mean juvenile?

RESPONSE: Revised as suggested. Yes, I meant juvenile.

 

-L82 - instead of “co-specimens” wouldn’t conspecifics be a better word?

RESPONSE: Revised as suggested.

 

-L110 - Rowland et al. 2017 (Oecologia) and Anderson et al. 2017 (Oecologia) did not find evidence of trophic cascades with larval salamanders

RESPONSE: Revised as suggested. I am very grateful for the suggested literature, which was included in the revised version.

 

-L121 - I am confused about what the n = 69 vs. 89 means. Is that the number of salamander species and the number of predators?

RESPONSE: Revised as suggested. I clarified this in the text to avoid misunderstandings (69 salamander species consumed by 89 predator species).

 

-Fig 1 - There are way more invertebrate predators of salamanders than this figure implies. Dragonfly nymphs, Dytisids, Notonectids, and many other species are documented as predators of the larval stage. Also why is there a salmon for the representative fish? I think a bluegill might be a better representation.

RESPONSE: Revised as suggested. I agree with the reviewer (there are way more invertebrate predators of salamanders than this figure implies), but I tried to keep the figure simple. In the revised version, I have included invertebrates feeding on larval stages. Additionally, I used a salmonid fish as representative fish because of its global distribution (please note that, for example, brown trout is indigenous to Europe, North Africa and western Asia but successfully introduced into at least 26 countries outside its native range including both North and South America). I kept the salmonid example, but I also included the centrarchid fish species (bluegill) as the reviewer suggested (see new figure 1).

 

-L169-170 - What do you mean by not massive? In almost all systems, the presence of fishes means that salamanders rarely make it to metamorphosis. Do you mean that salamanders are not a large component of fish diets?

RESPONSE: I have rewritten this part to clarify my point. That is, “It should be kept in mind that salamanders usually represent a small portion of fish stomach contents”.

 

-L197-199 - I don’t necessarily agree with this. A lot of their energy come from Cladocerans, which are a better food source (higher in nutrients) than copepods

RESPONSE: I agree with the reviewer. This statement is based on the work by Regester et al. (2008). In the revised version, I have included an additional statement to highlighting the importance of freshwater crustaceans other than copepods, such as isopods, cladocerans and amphipods (lines 314-316).

 

-L225 - ‘Keystone’ is a strong word. Would energy transfer collapse without them?

RESPONSE: Revised as suggested. I toned down the sentence just saying that “Salamanders can couple freshwater and terrestrial habitats through seasonal migrations (breeding adults) and emergences (metamorphosing larval)”.

 

-L271-273 - This last sentence seems tacked on and not the point you want to end with. What are the overall conclusions you want people to take away?

RESPONSE: Revised as suggested. I ended the paragraph with the take-home message.

Round 2

Reviewer 1 Report

This revised manuscript is much improved over the first draft, especially with regards to grammar and clarity. The author added new information in response to reviewer comments. However, I still find few new ideas or novel synthesis in this review. Many of the conclusions are simplistic and obvious, such as the point that salamanders are important as both consumers and prey in some ecosystems and the point that consumption of salamanders by apex predators may widely vary across large spatial scales.

I applaud the author for adding additional information about cannibalism and intraguild predation (lines 257-279) but the main point of this new information is lacking. What general themes emerge from cannibalism and intraguild predation ? How does this affect energy flow in the aquatic ecosystem? Does it alter the coupling with terrestrial ecosystems?

Figure 1 is an elementary illustration of trophic levels involving salamanders. I don’t think it adds anything to the discussion. The point of new Figure 2 is not clear and the figure is barely mentioned in the text. What does the Y axis represent (frequency of what)? What main point does this figure attempt to illustrate? Neither figure adds much to the paper.

There are some sentences that are unclear or do not make sense.

Examples of unclear statements include:

Line 231-234: “The above examples illustrate the importance of salamanders as intermediate consumers for many 232 vertebrate species and central players in energy and nutrient flow pathways from invertebrates up to 233 higher trophic levels, and thus for ecosystem functioning along multiple systems.” The above examples referred to in this statement actually discuss salamanders as prey, not as consumers.

Lines 286-288: “For example, the significance of salamander nutrient recycling is commonly variable in time and space (between 7 and 30% of stream nutrient), which is essential to understand dynamics in consumer-driven nutrient recycling [111].”

Lines 326-329: “This low frequency of occurrence, in line with the premise that this measurement does not provide any information about the abundance (numerical, biomass or volume) of prey categories [120], makes doubtful to conclude the importance of salamanders as energy resources for otter species compared to, for example, aquatic snakes [e.g. 76].”

Lines 369-371: “Thus, aquatic-terrestrial coupling needs to be contextualized as a dynamic phenomenon with frequent regime shifts in energy and nutrients translocations and recycling processes between freshwater and terrestrial ecosystems.”

Author Response

This revised manuscript is much improved over the first draft, especially with regards to grammar and clarity. The author added new information in response to reviewer comments. However, I still find few new ideas or novel synthesis in this review. Many of the conclusions are simplistic and obvious, such as the point that salamanders are important as both consumers and prey in some ecosystems and the point that consumption of salamanders by apex predators may widely vary across large spatial scales.

RESPONSE: I thank the reviewer for the constructive comments on the manuscript. In the revised version, I paid more attention to avoid simplistic and obvious conclusions. Thus, I re-wrote the sentence about the point that salamanders are important as both consumers and prey in the Discussion section. In addition, the sentence about the idea of spatial scales (“consumption of salamanders by apex predators may widely vary across large spatial scales”) was deleted.

 

-I applaud the author for adding additional information about cannibalism and intraguild predation (lines 257-279) but the main point of this new information is lacking. What general themes emerge from cannibalism and intraguild predation? How does this affect energy flow in the aquatic ecosystem? Does it alter the coupling with terrestrial ecosystems?

RESPONSE: The reviewer brings a good point to the table. In the revised version, the general themes emerging from cannibalism and intraguild predation were introduced on lines 273-285. Additionally, I extended the importance of cannibalism and intraguild predation on aquatic-terrestrial coupling (lines 357-365).

 

-Figure 1 is an elementary illustration of trophic levels involving salamanders. I don’t think it adds anything to the discussion. The point of new Figure 2 is not clear and the figure is barely mentioned in the text. What does the Y axis represent (frequency of what)? What main point does this figure attempt to illustrate? Neither figure adds much to the paper.

RESPONSE: I agree with the reviewer that the figure 1 doesn’t add anything to the discussion, instead it provides a clear example to show the point that salamanders are important as both consumers and prey in food-webs. I do believe this figure can be useful to readers in order to (i) contextualise the complex predator-prey interaction in which salamander are involved and (ii) show that aquatic and terrestrial systems are not isolated, but interconnected (aquatic-terrestrial coupling). Therefore, it was kept in the revised version. When it comes to the figure 2, please note that this figure was a specific request of reviewer 3 to summarise/conclude the number of papers supporting or refuting the potential importance of salamanders in the different roles. I agree with the reviewer 3 that this figure summarising the number of papers that supported vs. did not support the different roles can be helpful for digesting the information and thus used as take-home message in this study. I specified in the figure what the Y axis represents (i.e. frequency of occurrence (%) of papers).

 

-There are some sentences that are unclear or do not make sense. Examples of unclear statements include:

Line 231-234: “The above examples illustrate the importance of salamanders as intermediate consumers for many 232 vertebrate species and central players in energy and nutrient flow pathways from invertebrates up to 233 higher trophic levels, and thus for ecosystem functioning along multiple systems.” The above examples referred to in this statement actually discuss salamanders as prey, not as consumers.

RESPONSE: Revised as suggested. I changed “intermediate consumers” with “prey”, but also some minor edits in the writing (lines 231-232).

 

-Lines 286-288: “For example, the significance of salamander nutrient recycling is commonly variable in time and space (between 7 and 30% of stream nutrient), which is essential to understand dynamics in consumer-driven nutrient recycling [111].”

RESPONSE: Revised as suggested. This sentence was deleted to improve readability and avoid possible misunderstandings.

 

-Lines 326-329: “This low frequency of occurrence, in line with the premise that this measurement does not provide any information about the abundance (numerical, biomass or volume) of prey categories [120], makes doubtful to conclude the importance of salamanders as energy resources for otter species compared to, for example, aquatic snakes [e.g. 76].”

RESPONSE: Revised as suggested. I re-written this sentence to highlight that it is doubtful the use of literature sources only including frequency of occurrence to conclude the importance of salamanders as energy resources for otter species compared to papers reporting the abundance (numerical, biomass or volume) of prey categories (lines 330-334).

 

-Lines 369-371: “Thus, aquatic-terrestrial coupling needs to be contextualized as a dynamic phenomenon with frequent regime shifts in energy and nutrients translocations and recycling processes between freshwater and terrestrial ecosystems.”

RESPONSE: Revised as suggested. This sentence was deleted to improve readability and avoid possible misunderstandings.

Reviewer 2 Report

I think figure 2 is misleading as it seems like the author conducted an extensive literature review on the topic and these are the results from that review - I think it would mislead the readers as this review paper does not extensively review the literature on the topic. 

Author Response

-I think figure 2 is misleading as it seems like the author conducted an extensive literature review on the topic and these are the results from that review - I think it would mislead the readers as this review paper does not extensively review the literature on the topic.

RESPONSE: I thank the reviewer for the constructive comments on the figure 2. Please note that this figure was a specific request of reviewer 3. I utterly agree with the reviewer as this figure does not come from extensive literature review on the topic. Therefore, I included a caveat to point out that this figure only summarises the literature included in this article, but can be useful to summarise the number of papers supporting or refuting the potential importance of salamanders in the different roles (lines 435-440). This figure can be helpful for digesting the information and thus used as take-home message in this study.

Reviewer 3 Report

Thank you to the author for addressing all of my previous comments. The current version will be a great addition to the field. I have only minor comments:

L69: change ‘but’ to ‘and’

L283-285: This is confusing. Salamanders have a lower capacity for nutrient recycling than fish? Why? Because of nutrient content of salamanders vs. fish? Fish have more P-rich structures like scales, so I wouldn’t expect this.

L287: change to “nutrients”

I really like Figure 2!

Author Response

Thank you to the author for addressing all of my previous comments. The current version will be a great addition to the field. I have only minor comments:

RESPONSE: I thank the reviewer for the helpful feedback on the manuscript. In the revised version.

 

-L69: change ‘but’ to ‘and’

RESPONSE: Revised as suggested.

 

-L283-285: This is confusing. Salamanders have a lower capacity for nutrient recycling than fish? Why? Because of nutrient content of salamanders vs. fish? Fish have more P-rich structures like scales, so I wouldn’t expect this.

RESPONSE: Revised as suggested. I clarified why salamanders have a lower capacity for nutrient recycling than fish. That is, because excretion rates are higher in fish species (line 291).

 

-L287: change to “nutrients”

RESPONSE: Please note this sentence was deleted as consequence of comments from reviewer 1.

 

-I really like Figure 2!

RESPONSE: I really appreciate that the reviewer acknowledged the effort made in summarizing the number of papers that supported vs. did not support the different roles.

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