Implications of Climate-Induced Localised Extinction of Bull Kelp (Durvillaea amatheiae) for Holdfast Macrofauna

Round 1

Reviewer 1 Report

This paper describes animal communities associated with 57 holdfasts of the Australian bull kelp Durvillaea amatheia collected from six sites.  They find (a) large holdfast (= larger habitat), as expected is inhabited by more fauna, (b) community structures varied between sites (but not in simple way) and (c) fauna were overall generalist also found in adjacent habitats, like holdfasts from other kelp species. The results are discussed in a context of potential near-future range contraction of bull kelp and what this means for the fauna.

The paper is well written, data is, albeit ‘simple’, interesting and important to publish, and the analysis solid for this type of survey data. I recommend publication following a minor revisions.

First, the paper is ‘sold’ as a vital data-baseline paper to understand possible future changes particular associated with possible climate induced range contractions of bull kelp (no holdfast-fauna data exist for this species). I therefore argue that the authors should add their raw data to a data repository (with a doi – so that you still get cited if someone ever re-use your data).  The primary context of the paper (in the introduction and discussion) is that the presented data will be a baseline to understand future changes – but this baseline will only make sense if future studies can test their data against the data collected here.  In short, without a deposited dataset the context of the paper is ‘inadequate’.

L54. Add here that its an intertidal species inhabiting wave-exposed rocky reefs.

L72. Add a few more references to studies that have tested holdfast associated communities between different kelp species – e.g. 

Montie, S., & Thomsen, M. S. (2023). Facilitation of animals is stronger during summer marine heatwaves and around morphologically complex foundation species. Ecology and Evolution, 13(9), e10512.

Tuya, F., K. Larsen, and V. Platt. 2011. Patterns of abundance and assemblage structure of epifauna inhabiting two morphologically different kelp holdfasts. Hydrobiologia 658:373-382.

K92-94. Please add more details about the different sites to allow readers to understand possible site-effects – e.g. different temperatures, currents/waves, reef-sizes, sediments/turbidity?

Fig 1. Superimpose the know current distribution of bull kelp (how much more north and south does it go in AU?

L111. How did you get the holdfast off? With a crowbar or? And how did you collect the inverts/sediments after? Did you grab as many as you could see on the reef underneath the holdfast (after removed from the reef?)

L119. So, is this sediment only sediment contained within holdfast spaces – or also collected from the reef underneath the holdfast?

L133. Why did you pool nematoda and nemertea?  I agree many cryptic organisms should be pooled because its extremely difficult to identify them – but these two groups are relatively straightforward to tell apart – right? (e.g. rigid vs flexible structure).

L178. How many samples only contained 1 animal? (which seems a very low)

Table 2. Is this species per holdfast or in total for all holdfasts? If the latter, then mention that the site with lower sample size will have less taxa simply because less samples were collected.

Table 4. You don’t need 5-6 digits on R2 – 3-4 is more than enough.

Discussion somewhere. Are your holdfast sizes typical for adult bull kelp? They seem very small (table b1) with most <10 cm.  for most southern bull kelp species this would be juveniles/young kelp– and this would explain the relatively low biodiversity.

Discussion somewhere. Perhaps add a few lines about covariation between holdfast size and age – you don’t know if you have more animals in larger holdfasts because they are larger (more habitat) or older (more time for colonization).  

Author Response

Reviewer 1

This paper describes animal communities associated with 57 holdfasts of the Australian bull kelp Durvillaea amatheia collected from six sites.  They find (a) large holdfast (= larger habitat), as expected is inhabited by more fauna, (b) community structures varied between sites (but not in simple way) and (c) fauna were overall generalist also found in adjacent habitats, like holdfasts from other kelp species. The results are discussed in a context of potential near-future range contraction of bull kelp and what this means for the fauna.

The paper is well written, data is, albeit ‘simple’, interesting and important to publish, and the analysis solid for this type of survey data. I recommend publication following a minor revisions.

First, the paper is ‘sold’ as a vital data-baseline paper to understand possible future changes particular associated with possible climate induced range contractions of bull kelp (no holdfast-fauna data exist for this species). I therefore argue that the authors should add their raw data to a data repository (with a doi – so that you still get cited if someone ever re-use your data).  The primary context of the paper (in the introduction and discussion) is that the presented data will be a baseline to understand future changes – but this baseline will only make sense if future studies can test their data against the data collected here.  In short, without a deposited dataset the context of the paper is ‘inadequate’.

Response: We agree and have now deposited the dataset in the FigShare data repository at DOI: 10.6084/m9.figshare.25521670. We have clarified this in the “Data Availability Statement” at L402.

L54. Add here that its an intertidal species inhabiting wave-exposed rocky reefs.

Response: We agree and have modified the text at L56 so it now reads;

“It is an intertidal species inhabiting wave-exposed rocky reefs and is currently found along the mainland Australian coast from Aragunnu (36.59°S, 150.04°E) in New South Wales (NSW) to Wilson’s Promontory (39.06°S, 146.46°E) in Victoria [13,14].”

L72. Add a few more references to studies that have tested holdfast associated communities between different kelp species – e.g. 

Montie, S., & Thomsen, M. S. (2023). Facilitation of animals is stronger during summer marine heatwaves and around morphologically complex foundation species. Ecology and Evolution, 13(9), e10512.

Tuya, F., K. Larsen, and V. Platt. 2011. Patterns of abundance and assemblage structure of epifauna inhabiting two morphologically different kelp holdfasts. Hydrobiologia 658:373-382.

Response: We agree that this statement needs additional support and we have added the suggested references at L73.

L92-94. Please add more details about the different sites to allow readers to understand possible site-effects – e.g. different temperatures, currents/waves, reef-sizes, sediments/turbidity?

Response: To provide more information to readers about the locations sampled we have added average annual ocean temperatures at each location to Table 1 and have added more details about the locations to the text at L110-112 as follows;

“All sampling locations were on wave exposed intertidal rock platforms, with locations spanning a latitudinal gradient in sea surface temperatures of ~2.5C (Table 1)”

Fig 1. Superimpose the know current distribution of bull kelp (how much more north and south does it go in AU?

Response: We have superimposed a solid line on Figure 1 which shows the known current distribution of this species on mainland Australia (excluding Tasmania)

L111. How did you get the holdfast off? With a crowbar or? And how did you collect the inverts/sediments after? Did you grab as many as you could see on the reef underneath the holdfast (after removed from the reef?)

Response: Holdfasts were removed by sliding a broad-bladed scraper under the holdfasts. The holdfast was held on the scraper while being transferred to a sampling bag to prevent, as much as possible, any losses of fauna or sediment during sampling. Any sediment or fauna remaining on the rock after holdfast removal was also added to the sampling bag. This has been clarified in the text at L117-120 by stating;

“Holdfast removal was conducted using a broad-bladed scraper, which was held under the holdfast during transfer to the sampling bag to prevent, as much as possible, any loss of fauna or sediment during sampling. Any sediment or fauna remaining on the rock after holdfast removal was added to the sampling bag.”

L119. So, is this sediment only sediment contained within holdfast spaces – or also collected from the reef underneath the holdfast?

Response: This includes sediment collected from under the holdfast. This has been clarified in the text at L117-120 as detailed above.

L133. Why did you pool nematoda and nemertea?  I agree many cryptic organisms should be pooled because its extremely difficult to identify them – but these two groups are relatively straightforward to tell apart – right? (e.g. rigid vs flexible structure).

Response: Our apologies, this was poorly worded and has been mis-understood by the reviewer. We did not pool nematoda and nemertea together. Rather we separately pooled nematoda into one group and nemertea into a second group. We have clarified this in the text so that it now states at L141;

"Nematoda spp. and Nemertea spp. were pooled into two groups, one for each of these taxon”

L178. How many samples only contained 1 animal? (which seems a very low)

Response: The low count reflects the generally depauperate state of the assemblages found in D. amatheiae holdfasts. Four samples contained only a single animal, one at Aragunnu and three at Cape Conran. This has been clarified in the text at L152 by stating;

“Prior to analyses, samples with only a single animal in the whole sample (i.e. one sample at Aragunna and three at Cape Conran) were removed”

Table 2. Is this species per holdfast or in total for all holdfasts? If the latter, then mention that the site with lower sample size will have less taxa simply because less samples were collected.

Response: We have clarified that this is the total across all holdfasts sampled in the caption for Table 2, plus adding the total number of samples collected at each locations in brackets. We have also added a note at L223-224 that the species count for Merimbula may have been low as less samples were collected at this location, stating;

“It should be noted that lower numbers of species may have been recorded at Merimbula as less samples were collected at this location.”

Table 4. You don’t need 5-6 digits on R2 – 3-4 is more than enough.

Response: Agreed. We have edited Table 4 so that R squared is now shown to 3 decimal places.

Discussion somewhere. Are your holdfast sizes typical for adult bull kelp? They seem very small (table b1) with most <10 cm.  for most southern bull kelp species this would be juveniles/young kelp– and this would explain the relatively low biodiversity.

Response: Excellent point. The holdfasts collected were generally representative of the sizes previously reported (i.e. generally < 10 cm), but larger holdfasts were observed at the southern sites. We have elaborated on this point in the results at L191-193;

“The average diameters of collected holdfasts ranged from 37.5–130.0 mm, which is typical of D. amatheiae holdfasts which are generally < 10 cm in width [13], although larger holdfasts were observed in the field, particularly in Victoria (pers. obs.).”

We have highlighted that these holdfasts are small compared to some other species, and therefore may shelter lower macrofaunal diversity, stating at L320-323;

“It should be noted, however, that the size of the holdfasts examined for D. amatheiae (i.e. generally < 10 cm) was much lower than the size reported for D. antartica (up to 60cm [24]), which potentially contributed to the differences in holdfast macrofaunal richness recorded in these two studies.”

Discussion somewhere. Perhaps add a few lines about covariation between holdfast size and age – you don’t know if you have more animals in larger holdfasts because they are larger (more habitat) or older (more time for colonization).

Response: We have added some discussion points indicating that size and age are coupled, with increased diversity potentially due to greater age, stating at L347-354;

“It should be noted that holdfast size will generally increase with the age of the holdfast and it is difficult to disentangle whether larger holdfasts have greater species richness and abundance because they are larger, providing more habitat, or because they are older, which gives more time for colonization. Further research is needed to examine relationships between holdfast age and macrofaunal assemblages, however this would need a reliable method for aging D. amatheiae. Aging could potentially be achieved by counting growth rings in D. amatheiae stipes, as has been applied for aging of E. radiata [36].

Author Response File: Author Response.docx

Reviewer 2 Report

This work can be an interesting contribution to the knowledge of the possible hidden local extinctions due to climate change, especially, on a component of ecosystems that is so important, although often ignored, such as the seaweed macrofauna. The topic is properly introduced, references are relevant and the aims are well defined. However, there are some major concerns, mainly, some statistical analyses are incomplete and the results appear somewhat disordered.

Some observations or queries are as follows and I hope that these help to improve the study:

M&M

-. Were abundance data standardised by holdfast diameter or volume? And for all analyses or just for PERMANOVA?

-. Line 147: “mMDS” is “nMDS”. Similarly, in Figure 3 caption is “non-metric multidimensional scaling”.

-. Statistical analysis: this section should be re-ordered and re-written so that it follows the sequence as outlined in the Results. For example, the comparison with E. radiata fauna is at the end of M&M, however it is at the beginning of Results. I recommend combining all the sections related to data analysis.

-. “Comparison with Ecklonia radiata holdfast fauna”: How were the data compared? Nothing is shown in Results although it is mentioned in Discussion.

RESULTS

-. Lines 202-204: this sentence is Discussion.

-. PERMANOVA results are necessary, only p is not enough.

-. Section 3.4: maybe this section should go after the assemblages’ PERMANOVA and, especially, before of the models.

DISCUSSION

-. The discussion and conclusions seem appropriate, but, the discussion on the comparison with E. radiata should be supported by data analysis.

Author Response

Reviewer 2

This work can be an interesting contribution to the knowledge of the possible hidden local extinctions due to climate change, especially, on a component of ecosystems that is so important, although often ignored, such as the seaweed macrofauna. The topic is properly introduced, references are relevant and the aims are well defined. However, there are some major concerns, mainly, some statistical analyses are incomplete and the results appear somewhat disordered.

Some observations or queries are as follows and I hope that these help to improve the study:

M&M

-. Were abundance data standardised by holdfast diameter or volume? And for all analyses or just for PERMANOVA?

 Response:

Abundance data were standardised by holdfast diameter for the PERMANOVA analyses. This is stated in the methods at L168-170;

“PERMANOVA analyses were used to test for significant differences in species richness and total faunal abundance among locations, with data standardised by holdfast diameter to compensate for the effect of variations in holdfast sizes among locations.”

-. Line 147: “mMDS” is “nMDS”. Similarly, in Figure 3 caption is “non-metric multidimensional scaling”.

Response: No change made. The text is correct as the results are displayed using a metric MDS, hence the use of “mMDS” and “metric multidimensional scaling”. This is the recommended approach in the “Primer 7 user manual” for visualisation of bootstrap averaged 95% confidence intervals.

-. Statistical analysis: this section should be re-ordered and re-written so that it follows the sequence as outlined in the Results. For example, the comparison with E. radiata fauna is at the end of M&M, however it is at the beginning of Results. I recommend combining all the sections related to data analysis.

Response: Agreed. We have reordered the Materials and Methods section so that methods are described in the same order as results are presented. We have achieved this by moving the section describing methods for comparisons with E. radiata fauna up to section 2.5 (L144-149) so that it now precedes the section on statistical analysis methods. We have also combined the sections relating to data analysis into a single section (now 2.6) as suggested.

-. “Comparison with Ecklonia radiata holdfast fauna”: How were the data compared? Nothing is shown in Results although it is mentioned in Discussion.

Response: Species found in D. amatheiae holdfasts were compared against the species list for E. radiata holdfasts held by Steve D.A. Smith (pers. comm. 2023). This has been clarified in the text where we now state at L213-215;

“As far as could be determined, based on a comparison of the species found in D. amatheiae holdfasts against those found in previous research in E. radiata holdfasts (pers. comm. 2023 to SDAS), all taxa identified in D. amatheiae holdfasts also occur in E. radiata holdfasts within the region [29].”

RESULTS

-. Lines 202-204: this sentence is Discussion.

Response: This sentence has been retained in the results, but modified so that it now documents the findings of the comparison with E. radiata holdfast macrofaunal data in more detail, stating at L213-215.

“As far as could be determined, based on a comparison of the species found in D. amatheiae holdfasts against those found in previous research in E. radiata holdfasts (pers. comm. 2023 to SDAS), all taxa identified in D. amatheiae holdfasts also occur in E. radiata holdfasts within the region [29].”

-. PERMANOVA results are necessary, only p is not enough.

Response: These results have now been provided as Appendix C and are referenced in the text as Table C1 at L 219 for the initial test for differences among locations and Table C2 at L221 for the pairwise tests for differences among each pair of locations.

-. Section 3.4: maybe this section should go after the assemblages’ PERMANOVA and, especially, before of the models.

Response: We have shifted this section to 3.3 so that it now before the modelling section 3.4 as requested.

DISCUSSION

-. The discussion and conclusions seem appropriate, but, the discussion on the comparison with E. radiata should be supported by data analysis.

Response: We have provided more details on how the comparison with E. radiata was conducted at L213-215. This is detailed above in our responses to comments on the results section.

Author Response File: Author Response.docx