Amphiboreality and Distribution of Snailfishes (Cottiformes: Liparidae) in the Arctic and the North Atlantic
Round 1
Reviewer 1 Report
This is an interesting Ms on relevant aspects on the trans-Arctic migrations of the northern fish fauna using as an example the family Liparidae. The Ms/review is well organized and I have no particular comments on specific aspects that might be considered for a revision of the present layout and contents. The only minor aspect and from a very personal perspective is the fact that I find the reading a bit too "dense and heavy" but this might be expected from such an investigation. Thus, I consider that the Ms might be accepted in the present form.
Author Response
I express my deep gratitude to the reviewers, whose comments helped me to improve the manuscript.
Response to Reviewer 1 Comments
Point 1: This is an interesting Ms on relevant aspects on the trans-Arctic migrations of the northern fish fauna using as an example the family Liparidae. The Ms/review is well organized and I have no particular comments on specific aspects that might be considered for a revision of the present layout and contents. The only minor aspect and from a very personal perspective is the fact that I find the reading a bit too "dense and heavy" but this might be expected from such an investigation. Thus, I consider that the Ms might be accepted in the present form.
Response 1: I am grateful for your work in reviewing my manuscript, and appreciate your positive feedback. The manuscript has been edited to improve clarity and better understanding of the text.
Reviewer 2 Report
Dear Author, I have just few minor remarks:
- I think it would be good, for visual presentation, to include a distribution graph or some of the migration paths you mention in the Introduction, at least for the most important groups of fish.
- Some genera and subgenera in tables are not written in italic; please, correct this.
- Table 4 is not clearly presented; 2 for the first genus vs 4 columns for the second genus - what do they present (those different columns)?
Author Response
Response to Reviewer 2 Comments
Point 1: I think it would be good, for visual presentation, to include a distribution graph or some of the migration paths you mention in the Introduction, at least for the most important groups of fish.
Response 1: Dear Reviewer, I appreciated much for your helpful comment. Four figures (Figs 1-4) with distribution of species-groups added.
Point 2: Some genera and subgenera in tables are not written in italic; please, correct this.
Response 2: I have checked all Latin names in the manuscript, including the tables, and change if they are not in Italics.
Point 3: Table 4 is not clearly presented; 2 for the first genus vs 4 columns for the second genus - what do they present (those different columns)?
Response 3: Table 4 has been clarified: in the headings of columns 3 and 4 and in the footnote: There are no species with the indicated characters in the first subgenus (columns 3 and 4).
Reviewer 3 Report
The present manuscript is a review of the amphiboreal concept in Liparidae based on two core pieces of information: (1) the species composition of each region of interest (Arctic, North Pacific, North Atlantic), and (2) inference of relationships among species based on morphological similarity. The family Liparidae is of significant evolutionary and biogeographic interest, in part because it is one of the high-latitude fish groups found to have one of the highest speciation rates across marine fishes. I think this review is an important step forward towards understanding the biogeography of the clade. I do not think a model-based biogeographic analysis such as using BioGeoBEARS is within reach at the moment, pending a more robust time-calibrated phylogeny of Liparidae.
My biggest criticism is this: The morphological similarity of species is used to infer relationships and therefore possible dispersal routes. That is fine; however, we also have a well-sampled molecular phylogeny of Liparidae (Orr et al. 2019). A more comprehensive review would discuss whether relationships appear similar or different using morphology or molecules, and how any discrepancies change the interpretation of dispersal routes for the relevant sister species pairs or species clusters. Right now, the Orr et al. paper is cited only in passing (lines 198, 248). I would like to see molecular relationships tied in throughout the "Results" section.
I have smaller suggestions below:
line 51: "Lycodes Polaris" Polaris should be lowercase.
line 52: Please provide a clear definition of the amphiboreal concept as early as possible in the text for readers who are not familiar.
Lines 86–88: it is not clear why dispersal from Pacific to Atlantic should be favored compared to the reverse.
Please be aware throughout the manuscript that "fishes" should be used instead of "fish" when referring to multiple species (i.e. "Liparid fish" on line 152 should be "Liparid fishes")
Author Response
Response to Reviewer 3 Comments
Point 1: The MS is quite long in some parts (introduction) and requires some revision to be clearer (especially in material and methods. Please find all the comments and suggestions in the pdf attached.
Response 1: Thank you very much for your time, your comments helped a lot to make the MS more clear. The introduction is shortened as much as possible without distorting the content. The Material and methods have been supplemented. Corrections were done to make the text clearer. The text with corrections and the clean text are attached as separate files.
I tried to follow all your comments along the text, and provide answers to them point-by-point below.
Point 2: Line 44-45: “The degree of their penetration into the Arctic varies.”
Comment: Please, use more appropriate term
Response 2: The sentence is changed to the following: “The boundaries of their distribution in the Arctic are different”.
Point 3: Lines 95-111.
Comment: Please, shorten this part and give just a short summary.
Response 3: I made it as short as I could. The text with corrections and clean text are below.
The text with corrections is as follows:
Usually two periods of different-time migrations through the Bering Strait region are accepted, Pliocene and post-glacial [2,5,6,10,11,13,15,16-23]. In general, the history of migrations can be summarized as follows. 1. The results of Pliocene migrations through the Bering Strait, which was open at the end of the Miocene ca. 5.32 Ma [24], were well-specified amphiboreal species or even genera. The dispersal proceeded both along the coasts of Siberia and or through the American Arctic, which led to the formation of different species on both sides of the Atlantic Ocean in boreal waters. The direction of migrations of oligohaline marine species towards the Atlantic took place mostly along the coasts of northern Canada. Migrations of more euryhaline species (Petromyzontidae, Osmeridae, Pleuronectidae) took place mostly along the Asian coasts desalinated by river runoff. Thus, different boreal species emerged on both sides of the Atlantic. Fewer groups migrated in the opposite (Atlantic – Pacific) direction (Clupeidae, Gadidae). The advantage of the Pacific-Atlantic direction is explained due to the greater species abundance of the older Pacific fauna compared to the Atlantic.2. During the Ice age, the ice sheets occupied the Eurasian shelf for at least four times: during in the Late Saalian (>140 ka), the Early Weichselian (100–80 ka), the Middle Weichselian (60–50 ka) and the Late Weichselian (25–15 ka) [25], Glaciers covering a huge area from the modern British Isles to Severnaya Zemlya [26]. The Bering Land Bridge existed, closing the passage from the Pacific Ocean to the Arctic [27]. The boreal fauna, which occupied earlier a vast range from the North Atlantic to the eastern Arctic, have become extinct in the areas of glaciations, or retreated. Cold-water fauna began to form in the region of the Siberian shelf. In the Atlantic, the boreal fauna retreated to the southern latitudes, and some species could penetrate to the Mediterranean Sea and even to the southern hemisphere (sandlances Gymnammodytes). Partly, Several elements could have been preserved in refugia. Some other species , some other may have escape from the glaciers to bathyal depth. F and further speciation of isolated populations could lead to the formation of the endemic Arctic species, including the bathyal ones.
- The postglacial migrations were associated with postglacial climatic optimum and boreal transgression, when the Bering Strait was open (since 11 cal ka BP) and the climate was warmer than today [13,27–29]. This led to the wide distribution of shelf Pacific fish species into the Arctic, which did not have time to noticeably separate themselves from the Bering Sea populations there. 4. At present, the temperature of the waters in the Arctic is lower than before [30,31]. The most warm-loving fishes of the boreal fauna did not survive in the regions of central Siberia, where the most severe climatic conditions were established [32] (Nazarkin, 1992). Interrupted (amphiboreal) ranges of some species were formed, as the populations of migrants did not have time to separate taxonomically from the Pacific populations.
Clean text is as follows:
Usually two periods of different-time migrations through the Bering Strait region are accepted, Pliocene and post-glacial [2,5,6,10,11,13,15,16-23]. The results of Pliocene migrations through the Bering Strait, which was open at the end of the Miocene ca. 5.32 Ma [24], were well-specified amphiboreal species or even genera. The dispersal proceeded along the coasts of Siberia or through the American Arctic. The desalination-resistant species (Petromyzontidae, Osmeridae, Pleuronectidae) probably migrated along the Asian coast influenced by the flow of the great rivers. This may explain the deriving of different amphiboreal groups of species on both sides of the Atlantic.
The Pacific-Atlantic migration of the fauna prevailed, only a few groups (Clupeidae, Gadidae) migrated in the opposite direction, from the Atlantic to the Pacific. The advantage of the first direction is explained by the greater species abundance of the older Pacific fauna compared to the Atlantic one.
During the Ice age, the ice sheets occupied the Eurasian shelf for at least four times: in the Late Saalian (>140 ka), the Early Weichselian (100–80 ka), the Middle Weichselian (60–50 ka) and the Late Weichselian (25–15 ka) [25]. The largest glaciers covered a huge area from the modern British Isles to Severnaya Zemlya [26]. The Bering Land Bridge existed, closing the passage from the Pacific Ocean to the Arctic [27]. The boreal fauna, which occupied earlier a vast range from the North Atlantic to the eastern Arctic, have become extinct in the glaciated areas. A few elements could have been preserved in free-of-ice refugia; some other may have escape from the glaciers to bathyal depth. Cold-water fauna began to form in the cool region of the glacier-free Siberian shelf and in periglacial freshwaters. In the Atlantic, the boreal fauna retreated southward; some species could disperse that time to the Mediterranean Sea and even to the southern hemisphere (sandlances Gymnammodytes). Further evolutionary processes in separated populations may have led to the formation of new species, including the bathyal ones. The interglacial migrations may have occurred more than once, which explains the varying degree of morphological and genetic differentiation between amphiboreal taxa or populations.
Postglacial migrations were associated with the period of the postglacial climatic optimum and the boreal transgression when the Bering Strait opened (starting from 11 cal ka BP) [13,27-29]. The Pacific shelf species, which were able to spread widely in the Arctic, have not had time since that period to noticeably separate from the Bering Sea populations. Species with wide ranges (Pacific boreal-arctic species) appeared. At present, when the climate in the Siberian region has become harsher than before [30,31], the most thermophilic fish have not survived there [32], and interrupted ranges of some species have formed.
Point 4: Line 156: The main aim of this review is to consider if this concept is applicable …
Comment: give the full concept here
Response 4: This has been changed to: “The main aim of this review is to consider if the amphiboreal concept is applicable … “
Point 5: Lines 155-156: The main aim of this review is to consider if this concept is applicable to explaining the modern ranges of northern Liparidae.
Comment: The aim is one of the most important part of a paper and should be clear and clearly states the scope and starting hypothesis. Please revise
Response 5: This has been changed to: “The idea was to analyze the issue in a broad way, covering all the species of each genus present in northern waters. To do this, it is necessary to present the species composition of snailfish living in the Arctic and the boreal Atlantic. Then one should consider each genus of the family from these regions, whether they contain amphiboreal species or groups. This will allow us to discuss whether the probable ways of distribution and speciation of representatives of these taxa fit into the context of the amphiboreal concept”.
Point 6:. Lines 162 The review is based on liparid materials from the Arctic and adjacent areas, studied by the author for over 30 years.
Comment: Liparidae specimens collected … over many years of practical studies in taxonomy and related disciplines.
Response 6: This has been changed to: Liparidae specimens collected the Arctic and adjacent areas over many years of practical studies in taxonomy and related disciplines.
Point 7:. Lines 162-165
The review is based on liparid materials from the Arctic and adjacent areas, studied 162
by the author for over 30 years. Specimens of all Arctic genera, involved in the consider- 163
ation, were studied: Liparis, Careproctus, Paraliparis, Rhodichthys and Psednos [35-43]. Ma- 164
terials of liparid species related to the theme were also researched [44-48 and others]
Comment: you can also add some details about the location and availability of the analyzed materials
Response 7: The table with the volume of processed material is added (Table 1).
Table 1. Volume of processed material of fishes of the family Liparidae, number
|
Genera |
Species |
Specimens |
Stations/Lots |
Radiograms |
|
Liparis |
55 |
1555 |
525 |
359 |
|
Careproctus |
27 |
549 |
192 |
142 |
|
Paraliparis |
67 |
229 |
140 |
183 |
|
Psednos |
32 |
42 |
39 |
45 |
|
Rhodichthys |
2 |
7 |
5 |
6 |
|
Total: |
182 |
2382 |
901 |
734 |
Point 8:. Lines 173-174: The species of Careproctus of the Southern Ocean were analyzed in connection with the editing the manuscript [6].
Comment: not clear
Response 8: : It changed to: The species of Careproctus of the Southern Ocean were analyzed in connection with the assistance of Anatole Andriashev in the preparation of his monograph on Liparid fishes of the Southern Ocean [60], as well as in the descriptions of C. paxtoni [61], when 10 southern species were studied for comparisons.
Point 9:. Lines 176-190:
The borders of the Arctic region are considered within the biogeographic boundaries 176
substantiated earlier [62,63]. The area covers the Arctic shelves, the Central Arctic Basin 177
and the polar basins north of the Greenland–Iceland–Faroe Ridge, which delimits the 178
Polar and Atlantic basins. The Faroe Trench, connected to the Norway Basin is included 179
to the Arctic.
Morphological characters. The head pore formula (e.g. 2−5−7− …
Comment: The methodologies in this form is quite confused. Some explanation about the methodologies should be provided before to pass to the list of characters that were used.
Response 9: : The text is expanded:
Methodology. To show the background, a brief overview of the family Liparidae is made, and the species composition of snailfishes is listed 1) for the Arctic, 2) for the boreal Atlantic. Then snailfishes of the genus Liparis are analyzed for the presence of amphiboreal species or groups. The same is done for Careproctus and other genera. This made it possible to discuss whether the probable ways of distribution and speciation of representatives of these taxa fit into the context of the amphiboreal concept.
Point 10: Line 632. The data presented in the article allow us to hope that it provides a broad panorama of the complex events
Comment: change to: aim to provide a wide background
Response 10: The change is accepted: The data presented in the article aim to provide a wide background of the complex events.
Point 11:. Line 635. We used the traditional way of analyzing our materials collected over many years of…
Comment: what do you meand for traditional?
Response 11: We used the comparative methods of analyzing our materials collected over many years of Liparid studies…
Reviewer 4 Report
This MS worth interest because reports a detailed review of the distribution of Snailfishes in the Arctic and the North Atlantic. This topic is really important and still less studied and it is fully within the topics of the journal.
Although this, the MS is quite long in some parts (introduction) and requires some revision to be clearer (especially in material and methods. Please find all the comments and suggestions in the pdf attached.
Comments for author File: 
Comments.pdf
Author Response
I express my deep gratitude to the reviewers, whose comments helped me to improve the manuscript.
Response to Reviewer 4 Comments
Minor comments are the first.
Point 1: Line 51: "Lycodes Polaris" Polaris should be lowercase.
Response 1: This has been changed to: "Lycodes polaris"
Point 2: line 52: Please provide a clear definition of the amphiboreal concept as early as possible in the text for readers who are not familiar.
Response 2: The definition of the term “amphiboreal” is included in the fourth paragraph on the Introduction (the revised version)
“The third group includes a number of amphiboreal taxa of Pacific origin, which in the boreal Atlantic have taxonomically separated to the rank of species or even genera. Amphiboreal (from the Greek amphi - around, on both sides) means - existing in the boreal regions of the Atlantic and Pacific oceans. In total, there are up to several dozen amphiboreal groups of fishes and invertebrates [3,6,10]”.
Point 3: Lines 86–88: The advantage of the Pacific-Atlantic direction is explained due to the greater species abundance of the older Pacific fauna compared to the Atlantic.
Comment: It is not clear why dispersal from Pacific to Atlantic should be favored compared to the reverse.
Response 3: The text is changed to: “The advantage of the Pacific-Atlantic direction is explained by the greater species abundance of the more ancient Pacific fauna compared to the Atlantic, since statistically, the richer the fauna is in species, the more of them can settle through the opened strait. Another reason may lie in the prevailing direction of the currents”.
Point 4: Please be aware throughout the manuscript that "fishes" should be used instead of "fish" when referring to multiple species (i.e. "Liparid fish" on line 152 should be "Liparid fishes")
Response 4: The whole text has been checked to correct this error.
Point 5: My biggest criticism is this: The morphological similarity of species is used to infer relationships and therefore possible dispersal routes. That is fine; however, we also have a well-sampled molecular phylogeny of Liparidae (Orr et al. 2019). A more comprehensive review would discuss whether relationships appear similar or different using morphology or molecules, and how any discrepancies change the interpretation of dispersal routes for the relevant sister species pairs or species clusters. Right now, the Orr et al. paper is cited only in passing (lines 198, 248). I would like to see molecular relationships tied in throughout the "Results" section.
Response 5: Your remark taken into account. A few additions are inserted. Please, see the attached file for detailes
Author Response File: 
Author Response.docx
Round 2
Reviewer 4 Report
The author has revised the MS and it can be now accepted
Author Response
I am grateful for your work in reviewing my manuscript, and appreciate your positive feedback.
