Effect of Depth across a Latitudinal Gradient in the Structure of Rhodolith Seabeds and Associated Biota across the Eastern Atlantic Ocean

Round 1

Reviewer 1 Report

I read with lot of interest your work. This study represents an important contribute to the scarce literature dealing with rhodolith beds. In particular, it addresses important topics on many Eastern Atlantic rhodolith beds characterized by different environmental conditions to understand how depth influenced the structure (size and shape) of rhodoliths and the associated flora and fauna.

I have added below some specific comments and suggestions that in my opinion would improve the quality of the manuscript.

 

 

 

Line 65: Please use the term “coralline algae” or “rhodolith-forming species” instead of “rhodolith beds”, that are the whole habitat/community

 

Line 70 is not very clear. Knowledge about what? Ecosystem functions provided by ecosystem engineers? If so, I disagree. There are plenty of ecological studies based on depth gradients. Please reformulate

 

Line 82: “and a lower and deeper sublittoral”…. please be consistent with the previous points and add under what current.

 

Line 92-94: Please add more references, the only one reported it is not sufficient. At least add one for each listed ecological role

 

Line 97: the period at the end of the sentence is missing

 

Line 98-105: There are worth mentioning studies on Mediterranean rhodolith beds, that occur almost exclusively at elevated water depths (below 40 m), that correlate the influence of water depth, water energy and light to rhodolith abundance, size and morphology. Please see: Bracchi et al. 2019 “A resilient deep-water rhodolith bed off the egadi archipelago (mediterranean sea) and its actuopaleontological significance”; Rendina et al. 2020 “Distribution and Characterization of Deep Rhodolith Beds off the Campania Coast (SW Italy, Mediterranean Sea)”; Basso 1998 “Deep rhodolith distribution in the Pontian Islands, Italy: A model for the paleoecology of a temperate sea”.

 

Line 175: I would put Table S1 in the main text instead of the supplementary materials. Indeed, it would be important to have a look at “shallow”, “intermediate” and “deep” depths of each site while reading the article to follow the graphs, results and discussion

 

Line 292: Did you think about make a section and look at the nucleus (if there is a visible one) of the rhodolith nodules to see if/how it affects the whole rhodolith size and morphology? The nucleus (biogenic or not) has a key role influencing the algal growth and it is worth mentioning that

 

Line 300: the term “greater” depth is misleading, I understood the opposite (deeper). Please simply use “shallower”

 

Lines 302-304: Please see and cite more important studies, such as: Littler et al. 1991, Steller and Foster 1995, Riul et al. 2009, Bahia et al. 2010.

 

Line 319: Please change “on” the bottom with “at” the bottom

 

Author Response

I read with lot of interest your work. This study represents an important contribute to the scarce literature dealing with rhodolith beds. In particular, it addresses important topics on many Eastern Atlantic rhodolith beds characterized by different environmental conditions to understand how depth influenced the structure (size and shape) of rhodoliths and the associated flora and fauna.

I have added below some specific comments and suggestions that in my opinion would improve the quality of the manuscript.

We greatly appreciate the interest and the encouraging comments of the reviewer. In the response to the reviewers, to facilitate the location of the changes generated based on their suggestions, we wrote the number of lines in the version with the track changes corrector. 

 

Line 65: Please use the term “coralline algae” or “rhodolith-forming species” instead of “rhodolith beds”, that are the whole habitat/community

Amended. We modified in the text “rhodolith beds” for “coralline algae”. Now, L. 65-66.

Line 70 is not very clear. Knowledge about what? Ecosystem functions provided by ecosystem engineers? If so, I disagree. There are plenty of ecological studies based on depth gradients. Please reformulate

We have specified examples of ecological functions that ecosystems engineers can provide, such as the provision of habitat or nursery for other species (Now, L. 72).

On the other hand, we consider that the studies dealing with ecological variability along vertical scales are comparatively sparse than studies of local or latitudinal variation (See Otero-Ferrer et al. (2020). Effect of depth and seasonality on the functioning of rhodolith seabeds. Estuarine, Coastal and Shelf Science, 235, 106579.) For this reason, we maintained the emphasis on the smaller number of studies conducted for ecosystem engineers (e.g., seagrasses, kelp, rhodolith seabeds) combining the comparison across vertical gradients (e.g., depth) with horizontal scale (e.g., Latitude).

Line 82: “and a lower and deeper sublittoral”…. please be consistent with the previous points and add under what current.

 Amended. We added the level of turbulence for the depth strata that the reviewer indicated. Now, L. 83-84.

Line 92-94: Please add more references, the only one reported it is not sufficient. At least add one for each listed ecological role

 We added two new references to support the mentioned ecological functions. Now, L. 96-97.

Reference number 33 (See Navarro-Mayoral et al. (2020). Spatio-temporal variability of amphipod assemblages associated with rhodolith seabeds. Marine and Freshwater Research, 72(1), 76-83.) highlights the role of rhodoliths as habitat for macroinvertebrates.

Reference number 32 (See Fredericq et al. (2019). The critical importance of rhodoliths in the life cycle completion of both macro-and microalgae, and as holobionts for the establishment and maintenance of marine biodiversity. Frontiers in Marine Science, 5, 502.) to support their role as 'seed banks' for the life history stages of micro- and macroalgae.

Reference number 31 (see Schubert et al. (2022) Rhodolith Physiology Across the Atlantic: Towards a Better Mechanistic Understanding of Intra-and Interspecific Differences. Front. Mar Sci 2022, 9, 921639) deals with the role of rhodoliths in the carbon cycle through the CO2 sequestration for the formation of their structures.

Line 97: the period at the end of the sentence is missing

 Amended. Now, L. 100.

Line 98-105: There are worth mentioning studies on Mediterranean rhodolith beds, that occur almost exclusively at elevated water depths (below 40 m), that correlate the influence of water depth, water energy and light to rhodolith abundance, size and morphology. Please see: Bracchi et al. 2019 “A resilient deep-water rhodolith bed off the egadi archipelago (mediterranean sea) and its actuo paleontological significance”; Rendina et al. 2020 “Distribution and Characterization of Deep Rhodolith Beds off the Campania Coast (SW Italy, Mediterranean Sea)”; Basso 1998 “Deep rhodolith distribution in the Pontian Islands, Italy: A model for the paleoecology of a temperate sea”.

We added two references suggested by the reviewer for the Mediterranean Sea that that contrast the same pattern of bathymetric distribution of deep rhodolith seabeds in the Atlantic Ocean, considereing environmental factors (Rendina et al., 2020 and Bracchi et al., 2019).

Moreover, we added other reference that highlights the special conditions of the Mediterranean, since rhodoliths are found in very shallow waters (i.e., 5-10 meters). (See: Georgiadis et al., (2009). Coralligène formations in the eastern Mediterranean Sea: Morphology, distribution, mapping and relation to fisheries in the southern Aegean Sea (Greece) based on high-resolution acoustics. Journal of experimental marine biology and ecology, 368(1), 44-58.)

Now, L. 110-116

 

Line 175: I would put Table S1 in the main text instead of the supplementary materials. Indeed, it would be important to have a look at “shallow”, “intermediate” and “deep” depths of each site while reading the article to follow the graphs, results and discussion

 We transferred Table S1 from the supplementary material and have incorporated it into the manuscript, specifically in section "2.2. Sampling design and collection of samples" of material and methods, where we explain the different regions and depths sampled.

Thus, changes have also been made to the number and order of tables in the manuscript (i.e., Table 2 is now Table 3) and in the supplementary material (Table S2 is now S1, S3 is now S2, S4 is now S3, S5 is now S4, S6 is now S5, and S7 is now S6).

Line 292: Did you think about make a section and look at the nucleus (if there is a visible one) of the rhodolith nodules to see if/how it affects the whole rhodolith size and morphology? The nucleus (biogenic or not) has a key role influencing the algal growth and it is worth mentioning that

In the case of Brittany and Galicia, the rhodoliths do not have a nucleus, while in the other regions (Gran Canaria, Madeira and Isla Principe) it was not possible to verify the existence of a nucleus in the rhodolith nodules. Therefore, since the characterization of the nucleus was not one of the objectives of the study, we cannot include a section for results. However, since as the reviewer indicates, the nucleus affects the morphology and growth of the rhodoliths, we have included it in the discussion in section ‘4.1. Rhodolith attributes’. Now, L. 337-341.

Line 300: the term “greater” depth is misleading, I understood the opposite (deeper). Please simply use “shallower”

We modified the concept "greater" depths, since as the reviewer indicates it can be confusing. We changed it to the term "intermediate" instead of "shallower", since we are referring to a depth between the layer superficial and the deep. Now, L. 331.

Lines 302-304: Please see and cite more important studies, such as: Littler et al. 1991, Steller and Foster 1995, Riul et al. 2009, Bahia et al. 2010.

 We cited the study of Steller and Foster (1995) and Bahia et al., 2010, that were already on our reference list. Moreover, we added a new reference, the study of Littler et al., 1991 (Littler, M. M., Littler, D. S., & Hanisak, M. D. (1991). Deep-water rhodolith distribution, productivity, and growth history at sites of formation and subsequent degradation.Journal of experimental marine biology and ecology, 150(2), 163-182.) Now, L. 335.

 

Line 319: Please change “on” the bottom with “at” the bottom

Amended. Now L. 355

Author Response File: Author Response.pdf

Reviewer 2 Report

The manuscript analyses depth and latitude effects on the characteristics of some atlantic rhodolith beds. The topic is very interesting also because rhodolith beds represents an important habitat poorly known. The introduction section is very interesting and well written; methods and results are described with some small inaccuracies that I reported in the attached revised manuscript. furthermore some little notes are highlighted in the discussion

Comments for author File: Comments.zip

Author Response

Review 2

 

Supplementary material

 

Table S1. Are these the replicates 25x25? Why number of replicates are different in the three depth strata? Please explain here or in the M&M section

 

Table S1 was moved to the manuscript, now being Table 2, at the request of the first reviewer.

 

The numbers of the three depths stratum (i.e., shallow, intermediate and depth) are not the number of replicas, it is referred to the depth at which the rhodolith seabeds was found at each region. For example, the shallowest rhodolith seabeds sampled in Brittany was found at 2 meters, while in Madeira it was found at 16 meters. We clarified this in the Table legend to avoid confusion. (Table 2. Date, location (region, site, latitude and longitude) and depth (meters) that corresponded to each region. The depth of each stratum (i.e., shallow, intermediate and depth) varied for each region, where the rhodolith seabeds presented different bathymetric ranges)

This is already explained in the M&M apparatus ‘2.3. Sampling design and collection of samples’ in L. 183-195.

 

Manuscript

 

 

29. 29. beds are not engineers rather rhodolith as organisms are engineers

 

We decided to maintain 'rhodolith seabeds' as an 'ecosystem engineer' concept, since it is the set of rhodoliths on the bottom that generate structurally complex habitats that harbor distinctive assemblages of highly diverse fauna and flora.

In this way, several authors include the seabed within the concept of "ecosystem engineers", understanding that ecosystem engineering functions occur in an extensive bed of rhodoliths on the seabed. Some of the studies that included 'seabed' are:

Rebelo, A. C., Martín-González, E., Melo, C., Johnson, M., González-Rodríguez, A., Galindo, I., ... & Rasser, M. W. (2022). Rhodolith beds and their onshore transport in Fuerteventura Island (Canary Archipelago, Spain). Frontiers in Marine Science, 9.

Teichert, S. (2013). Rhodoliths (Corallinales, Rhodophyta) as a biosedimentary system in arctic environments (Svalbard Archipelago, Norway). Friedrich-Alexander-Universitaet Erlangen-Nuernberg (Germany).

Tuya, F. (2020). Structure and Biodiversity of Rhodolith Seabeds: A Special Issue. Diversity, 12(8), 300.

Navarro-Mayoral, S., Fernandez-Gonzalez, V., Otero-Ferrer, F., & Tuya, F. (2020). Spatio-temporal variability of amphipod assemblages associated with rhodolith seabeds. Marine and Freshwater Research, 72(1), 76-83.

Otero-Ferrer, F., Mannarà, E., Cosme, M., Falace, A., Montiel-Nelson, J. A., Espino, F., ... & Tuya, F. (2019). Early-faunal colonization patterns of discrete habitat units: A case study with rhodolith-associated vagile macrofauna. Estuarine, Coastal and Shelf Science, 218, 9-22.

The same occurs for other ecosystem engineers such as seagrass, where the studies cited the name of the specific species (e.g., Posidonia oceanica) or seagrasses in general followed by 'meadows' to refer to the ecosystem engineers:

Brun, F. G., van Zetten, E., Cacabelos, E., & Bouma, T. J. (2009). Role of two contrasting ecosystem engineers (Zostera noltii and Cymodocea nodosa) on the food intake rate of Cerastoderma edule. Helgoland Marine Research, 63(1), 19-25.

Eriksson, B. K., van der Heide, T., van de Koppel, J., Piersma, T., van der Veer, H. W., & Olff, H. (2010). Major changes in the ecology of the Wadden Sea: human impacts, ecosystem engineering and sediment dynamics. Ecosystems, 13(5), 752-764.

 

89. 89. As already written in the comment below, I think that ecosystem engineers are the rhodolith as "organism that..."see line 63-65 and not rhodolith seabeds, could you please revise it in the manuscript?

 

See previous response to comment of comments “L. 29. beds are not engineers rather rhodolith as organisms are engineers”

Figure 2. I would change symbols to make the interpretation of the figure easier, i,e. in the map with all the sampling sites, the five regions should be marked with squares and furthermore I would move the fig 1d down to better see all the map

 

We have moved figure 1d to the lower left to better visualize the entire map as suggested by the reviewer. In the general map, we marked the 5 regions with a square, transparent and with the outline of the color assigned to each region (that is, red for Britany, yellow for Galicia, blue for Madeira, green for Gran Canaria and purple for Isla Principe).

 

 

 

 

 

Table 1. I have found this table a little bit confusing: letters in the first row are ok but letters in the other rows are useless and confusing, I would mark the presence of the specie in a region with a cross/thich; furthermore what are the numbers reported as apex? are the references ? I would delete them and report them in some other ways, for example in the caption " see references 41.43.44... for the species distribution"

Lastly, please revise all the references some of these are not correct(i.e. 41 does not report species distribution in Galicia, Madeira and Gran Canaria)

 

We followed the reviewer's suggestions and we used 'X' to mark the presence of the rhodolith species in the regions. However, we kept the references in superscript letters, since putting it in the title of the table would make it difficult to read since there are many species per region. To make reading easier we left a reference by species.

 

158. 158. I don't understand the usefulness of this section. First of all, how Sea Surface temperature is related to a deep habitat as maerl bed? Secondly SST and PAR show seasonal changes and it is difficult relate them as mean value with maerl bed sampled in different periods of the year. Lastly "environmental context" is not in any way related and discussed in the remaining part of the manuscript

We agree with the reviewer, and we deleted this section (environmental context) in material and methods and in results. In a first moment, due to the wide latitudinal gradient covered by our study, we found it interesting to show surface temperature data and Sea Surface Photosynthetically Available Radiation (PAR) data. Although these variables change seasonally, these data can be useful in a spatial context like ours (i.e., from high latitudes to the tropics). However, as the reviewer indicates, the sampling times were different for the five regions, so the data for these environmental variables cannot be comparable and we deleted.

169. 169. why do you cite fig 2 here? fig 2 reports results

We removed figure 2 from this part.

170. 170. please see comments on the supplementary file

See our previous answer to comments on the supplementary file.

 

172. 172. what are the depth range in each depth stratum? I suggest to write them

The depths for each stratum (i.e., shallow, intermediate and depth) vary depending on the region (i.e., Britanny, Galicia, Madeira, Gran Canaria and Isla Principe), since the bathymetric distribution range in which rhodolites are found it is not the same. Therefore, we included the reference to Table 2 (before Table S1) in which the specific depths for each stratum and for each region are shown so that the reader can consult it.

200. 198-200. taxonomic identification of the macrofauna is not reported in the result section: I suggest to delete this part or to report it in the result section even as supplementary table

We modified the macrofauna section of ‘2.3. Samples processing' indicated by the reviewer to avoid confusion. Now. L 218-225.

We specified that the macrofauna was classified only at the phylum level, and we removed the part that could make understand that fauna was identified at other taxonomic levels such as order, genus or species. We keep this section in M&M, since it is necessary to explain how the macrofauna samples that appear in the results and discussion of this study were processed.

218. 218. please see the comment of the paragraph 2.2

We agree with the reviewer, and we deleted this section in material and methods (environmental context) and in results. Due to the wide latitudinal gradient covered by our study, we found it interesting to show surface temperature data and surface photosynthetic radiation (PAR) data. Although these variables change seasonally, these data can be useful in a spacial context like ours. In our study, we tested how rhodolith communities (associated flora and fauna) change across different latitudes, without considering the part of seasonal variation. However, as the reviewer indicates, the sampling times were different for the five regions, so the data for these environmental variables cannot be comparable and we deleted.

L.227. all references to the tables do not match

All figures and results tables corrected following the reviewer's suggestions.

229. 229. Fig 2 table S2

In the previous version, in L. 229, we referred to Fig. 3 and Table S3 and the reviewer asks us to change it to Fig 2 and Table S2.

• Figure

We kept Figure 3, since in L. 229 (now. L 249-250) we described how the size of rhodoliths consistently differed among depth strata across regions. Figure 3 is a box plot that shows the mean diameter (mm) of the rhodoliths in each depth stratum (Sh: Shallow; Int: Intermediate and Dp: Deep) and region. The Figure 2 is only the reference map of the sampled regions and did not show any results on the size of the rhodoliths.

• Table

We corrected the number of the Table. Instead of putting Table S2 as indicated by the reviewer, we put Table S1, since when moving the first table of the supplementary material (at the suggestion of the first reviewer) to the manuscript, the order of the tables has changed. In this way, Table S1 is the previous table S2.

 

231. 231. Fig 2

Amended. Fig. 3 now Fig. 2

252. 252. I think that the results on epiflora abundance have been affected by different sampling seasons. Please comment this in the discussion section

Done. We incorporated a paragraph on the seasonal and latitudinal variability experienced by the epiflora associated with rhodolith seabeds. L, 396-404.

254. 254. numbers of tables and figures are not corresponding along the paragraph

The sentence in line 254 says the following: 'The epiphytic macroalgal biomass (g per kg of rhodolith) varied among regions across the latitudinal gradient' and we cited Fig. 5 and Table S5.  

The figure and table of L. 254 (now L. 279) are correct. Figure 5 shows the "total biomasses of epiphytic macroalgae (dry weight) in each depth stratum (Sh: Shallow; Int: Intermediate and Dp: Deep) and regions" and table S5 (now Table S4) shows the statistical differences of the amount of epiphytes between depths along the different latitudes.

265. 264-265. What does it mean? Please explain better

It is an error in the legend, since the boxplots are not bar graphs, and the standard error is not represented. We removed it from the legend of the graph and from the other graphs in the manuscript where it appears.

277. 273-277. this is not completely true, please revise it

We modified this part of the results, since, as indicated by the reviewer, the pattern described by regions was not entirely correct. Now, L. 297-304

381. 381. What other taxonomical groups were found?

We corrected this sentence to avoid confusion and to fit it our results, since in our study the epifauna was classified only at the phylum level. Now, L. 425-427

387. 387. you refer to the results of the manuscript or to literature, it is not clear

We referred to the results obtained in our study. We clarified in the manuscript to avoid confusion. Now, L. 431-432

402. 401-402. please add some references to support this sentence

The last paragraph (L.444-447) summarizes the conclusions obtained in our study, so we cannot add any reference.

Ref. 26. please add Journal name

Amended. Now ref. 26

Ref. 46. Add page numbers

Amended. Now ref. 51                                                

Ref. 48. Add journal name

Amended. Now ref. 53

Ref. 53. Please add journal

Amended. Now. Ref 124

Ref. 54. Change in italics

Amended. Now ref. 69

Ref.58. change in italics

Amended. Now ref. 63

Ref. 64. Please add journal name

Amended. Now ref. 58

Ref 70. Add journal name

Amended. Now ref. 75

Ref. 81. Please add journal name

Amended. Now ref. 88

Ref. 110. Add journal name

Amended. Now ref. 118

 

Author Response File: Author Response.pdf