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Article
Peer-Review Record

Recovery of Macrobenthic Food Web on Rocky Shores Following the Hebei Spirit Oil Spill as Revealed by C and N Stable Isotopes

Water 2022, 14(15), 2335; https://doi.org/10.3390/w14152335
by Hyun Je Park 1, Changseong Kim 2 and Chang-Keun Kang 2,*
Reviewer 1:
Reviewer 2:
Reviewer 3: Anonymous
Water 2022, 14(15), 2335; https://doi.org/10.3390/w14152335
Submission received: 27 June 2022 / Revised: 18 July 2022 / Accepted: 25 July 2022 / Published: 28 July 2022
(This article belongs to the Special Issue Application of Stable Isotopes in Marine Ecosystems)

Round 1

Reviewer 1 Report

 

This is a short, well-written paper that shows there is no significant difference in trophic structure, based upon stable carbon and nitrogen isotope composition of organisms in rocky intertidal habitats affected and unaffected by the Hebei Spirit oil spill in 2007. This study’s conclusions were supported by biotic sampling in 2013. The authors describe the results as supporting recovery from the oil spill, but on the other hand, there are no data available that show that the oil spill actually had an initial impact on food web trophic structure as determined using stable isotopes that has now been reversed. In fact, in a prior publication in Marine Pollution Bulletin, some of the same authors made essentially the same conclusion based upon sampling in 2009 and 2010 of a wider variety of organisms, including fish. As a result, I am not certain that this manuscript adds too many new insights. Since the authors correctly point out that oil is primarily degraded through bacterial metabolic pathways, an alternate explanation may be that stable isotopes are not a particularly robust methodology for following the impacts of an oil spill disturbance in a rocky intertidal ecosystem or foodweb.  Compared to a soft sediment ecosystem, deposit feeders have access to a much less vast sediment reservoir where weathered petrochemical contaminants might remain. Although the carbon isotope composition of the remaining oil would be expected to skew to less negative delta carbon-13 values, it would be helpful if a target composition of the oil could be provided for carbon isotopes.  However, in the process of natural remediation, the stable carbon isotope composition of the remaining petrochemical residues could be reasonably expected to become isotopically heavier as a result of preferential bacterial degradation of 12C relative to 13C. Thus it would become more challenging over time to identify unambiguously the presence of petrochemical source carbon in the food web.  So I think the authors might adjust tone some in the conclusions to acknowledge these limitations in their interpretations, although I don’t see any major flaws in the data or presentation. Standardization and methodology is well-described, and precision is within expected limits. Stating that the data are available from the author is also less than ideal and could be easily remedied by posting the raw data to an archive---much of the data are already tabulated in the text. As I mentioned, the paper is well-written and I have just a handful of editing suggestions/comments for the authors below.   

 

Line 12, 42. I think it would be preferable to use the official name of the country, the Republic of Korea, rather than South Korea.

 

Line 75-77. It is noteworthy if this is the first study of the Hebei oil spill using stable isotopes, although these approaches have been used in other oil spill impact studies and the difference between this study and the prior one published in Marine Pollution Bulletin should be specified.

 

Line 102, quadrat instead of quadrate. Quadrat is a noun and quadrate is an adjective.

Author Response

1. General comments

Comments and Suggestions for Authors

This is a short, well-written paper that shows there is no significant difference in trophic structure, based upon stable carbon and nitrogen isotope composition of organisms in rocky intertidal habitats affected and unaffected by the Hebei Spirit oil spill in 2007. This study’s conclusions were supported by biotic sampling in 2013. The authors describe the results as supporting recovery from the oil spill, but on the other hand, there are no data available that show that the oil spill actually had an initial impact on food web trophic structure as determined using stable isotopes that has now been reversed. In fact, in a prior publication in Marine Pollution Bulletin, some of the same authors made essentially the same conclusion based upon sampling in 2009 and 2010 of a wider variety of organisms, including fish. As a result, I am not certain that this manuscript adds too many new insights. Since the authors correctly point out that oil is primarily degraded through bacterial metabolic pathways, an alternate explanation may be that stable isotopes are not a particularly robust methodology for following the impacts of an oil spill disturbance in a rocky intertidal ecosystem or foodweb.  Compared to a soft sediment ecosystem, deposit feeders have access to a much less vast sediment reservoir where weathered petrochemical contaminants might remain. Although the carbon isotope composition of the remaining oil would be expected to skew to less negative delta carbon-13 values, it would be helpful if a target composition of the oil could be provided for carbon isotopes.  However, in the process of natural remediation, the stable carbon isotope composition of the remaining petrochemical residues could be reasonably expected to become isotopically heavier as a result of preferential bacterial degradation of 12C relative to 13C. Thus it would become more challenging over time to identify unambiguously the presence of petrochemical source carbon in the food web.  So I think the authors might adjust tone some in the conclusions to acknowledge these limitations in their interpretations, although I don’t see any major flaws in the data or presentation. Standardization and methodology is well-described, and precision is within expected limits. Stating that the data are available from the author is also less than ideal and could be easily remedied by posting the raw data to an archive---much of the data are already tabulated in the text. As I mentioned, the paper is well-written and I have just a handful of editing suggestions/comments for the authors below.

Response: Thanks for constructive comments. Accordingly, we have revised as suggested by the reviewer throughout the ms and described our responses one by one (see responses below). Above all, the originality of our study is the trophic recovery of macrobenthic food web in the rocky shore ecosystem impacted by the HSOS. We have represented the differences in macrobenthic food web structure between the rocky shore (our study) and soft-bottom (Han et al., 2015) habitats (see Figure 2).

2. Specific comments

- Line 12, 42. I think it would be preferable to use the official name of the country, the Republic of Korea, rather than South Korea.

Response: Thanks for comment. We have revised the phrase in the revised ms, accordingly.

- Line 75-77. It is noteworthy if this is the first study of the Hebei oil spill using stable isotopes, although these approaches have been used in other oil spill impact studies and the difference between this study and the prior one published in Marine Pollution Bulletin should be specified.

Response: As suggested by the reviewer, we have added the result of prior one published in Marine Pollution Bulletin (Han et al., 2015). Similar to our study, Han et al. (2015) found similar macrobenthic food web structure on soft-bottom sediments between the impacted area by the oil-spill and the reference area. The clear distinction between two studies is the study areas on habitat types of rocky shore and soft-bottom sediment, which definitely show different macrobenthic species compositions between two habitats (Lines 76–78).

- Line 102, quadrat instead of quadrate. Quadrat is a noun and quadrate is an adjective

Response: Thanks. We have deleted "e", accordingly.

 

Reviewer 2 Report

Generally, this is an interesting study. However, there exist lots of data on the HSOS, and this should be better integrated and used, and the new findings of this work should base on the previous findings. Thus, the results of the previous works need to be added, included and explained.

 

row 11: Put Hebei Spirit in italics.

Row 14: .... in 2 heavily oil-impacted and 1 non-impacted...

Row 18: ... have re-achieved...

Row 81: What does mean: ...12,547kL on...

Rows 82-83: Add GPS-coordinates of sampling sites.

Rows 90-92: What was the interpretation of the increase of the ecological indices over 1 year after the HSOS to reference values? On the one hand long-term changes are reported, on the other hand a rapid recovery had been found. Explain in more detail.

Figure 1. Add the sampling localities from Han et al., 2015. Add respective information in caption. Replace "oiled" by "oil-contaminated" or similar. Add demarkation line between North and South Korea.

Rows 139-140: either remove "approximately", or remove the last digit after the comma.

Table 2: Do you have an explanation for the high SD of d15N species No. 10?

Table 2 continued: Table headers do not fit with the table content.

Figure 2: Include the data of Han et al., 2015, (your reference 17) in this figure, or produce a separate figure which contains both data sets.

Row 214: replace oiled by oil-contaminated or similar.

Figure 3. Include the Han et al., 2015, data in the figure.

Rows 251-253: Remove the sentence, not necessary.

Rows 251-266: Add examples from literature where stable isotope analysis (C and N) evidenced the environmental changes caused by an oils spill.

Rows 279-280: Did this (decreased d13C-values) occur at the HSOS? Has it been described in the literature?

Author Response

- Generally, this is an interesting study. However, there exist lots of data on the HSOS, and this should be better integrated and used, and the new findings of this work should base on the previous findings. Thus, the results of the previous works need to be added, included and explained.

Response: Thanks for constructive comments. As suggested by the reviewer, we have added and have explained the previous result of soft intertidal macrobenthic food web investigated by Han et al., 2015 (Lines 76–78 and Figure 2).

- row 11: Put Hebei Spirit in italics.

Response: As indicated by the reviewer, we have changed these words in the revised ms.

- Row 14: .... in 2 heavily oil-impacted and 1 non-impacted...

Response: According to the reviewer's comment, we have modified this sentence in the revised ms.

- Row 18: ... have re-achieved...

Response: Agree. we have modified this word in the revised ms accordingly.

- Row 81: What does mean: ...12,547kL on...

Response: We made a mistake. We have removed the phrase in the revised ms.

- Rows 82-83: Add GPS-coordinates of sampling sites.

Response: As suggested by the reviewer, we have added GPS information on sampling sites in the revised ms (Lines 86–88).

- Rows 90-92: What was the interpretation of the increase of the ecological indices over 1 year after the HSOS to reference values? On the one hand long-term changes are reported, on the other hand a rapid recovery had been found. Explain in more detail.

Response: Jung et al. (2017) found that there were noticeable differences in the abundance of dominant species between the oil-impacted and natural sites during the first 5 years after the HSOS because of the proliferation of the Pacific oyster Crassostrea gigas and the high abundance of Lottia spp. and Odostomia aomori at oil-impacted site. Accordingly, the differences of ecological indices between the oil-impacted and natural areas may result from increased of some specific species at the oil-impacted sites. They suggested significant differences of macrobenthic communities between the polluted and control sites over the 6 years after the oil spill. We have represented the related information on macrobenthic communities (Discussion part) in the revised ms (Lines 346–351).

- Figure 1. Add the sampling localities from Han et al., 2015. Add respective information in caption. Replace "oiled" by "oil-contaminated" or similar. Add demarkation line between North and South Korea.

Response: As indicated by the reviewer, we have added the sampling sites from Han et al. 2015 and have modified the word and Figure 1 in the revised ms.

- Rows 139-140: either remove "approximately", or remove the last digit after the comma.

Response: We have removed the word in the revised ms accordingly

- Table 2: Do you have an explanation for the high SD of d15N species No. 10?

Response: We made a mistake. We have modified the SD value in the revised ms, accordingly.

- Table 2 continued: Table headers do not fit with the table content.

Response: Agree. We have modified the table line in the revised ms, accordingly.

- Figure 2: Include the data of Han et al., 2015, (your reference 17) in this figure, or produce a separate figure which contains both data sets.

Response: As suggested by the reviewer, we have added information on the results from Han et al. (2015) and have modified Figure 2 in the revised ms.

- Row 214: replace oiled by oil-contaminated or similar.

Response: As indicated by the reviewer, we have changed this word in the revised ms.

- Figure 3. Include the Han et al., 2015, data in the figure.

Response: As suggested by the reviewer, we have tried to include data from Han et al., 2015 in Figure 3. However, there were some problems since some feeding groups (e.g. suspension feeders) were short of published stable isotope data and sampling periods were at a different time or season. To our regret, therefore, we did not represent the isotopic niche comparisons of each feeding group from Han et al. (2015).

- Rows 251-253: Remove the sentence, not necessary.

Response: As suggested by the reviewer, we have removed the sentence in the revised ms.

- Rows 251-266: Add examples from literature where stable isotope analysis (C and N) evidenced the environmental changes caused by an oils spill.

Response: As suggested by the reviewer, we have added literature (Peterson, C.T.; Grubbs, R.D.; Mickle, A. An investigation of effects of the Deepwater Horizon oil spill on coastal fishes in the Florida big bend using fisher-independent surveys and stable isotope analysis. Southeastern Naturalist 2017) in the revised ms (Lines 264, 266).

- Rows 279-280: Did this (decreased d13C-values) occur at the HSOS? Has it been described in the literature?

Response: In the present study, we did not find the decrease by 1‰ to 4‰ in organic matter sources at the oil-impacted site. Graham et al. (2010) reported carbon depletion of organic matter (plankton size classes) in the oil-impacted areas.

Reviewer 3 Report

The study shows the impact of natural recovery of the microbenthic food web 4 years after the Hebei Spirit oil spill in the western coast of South Korea. Isotopic ratios of polluted and clean sites show no significant difference suggesting recovery. The study is novel and shown the long-term consequence of oil spill on the microbenthic environment and its resiliency.

 

 

Abstract:

 

Succinct and to the point. However, a major element that needs to be emphasised (missing in the abstract) for the readers is the temporal aspect i.e. 4 years post spillage.

 

Line 12: I would suggest adding “along Taean Peninsular on the western coast of Korea.

 

Introduction:

 

Line 63: Brackets around references

 

 

 

 

Materials and methods:

 

Line 80-97 : While the study sites are described as rocky shores it would have been valuable for the reader to have a picture from the sites where the samples were collected from to give an understanding of the topology of the location.

 

 

Results:

 

Table 2: Line 29 Why was Nereis heterocirrata included? Was there a reason for it?

 

Table 2. Continued: The columns seem to be misaligned.

 

Table 2 Continued. Line 33: Hima fratercula hypolia Why does it have an n =4 value but has missing mean and SD values in the Gurepo site?

 

Table 2 Continued Line 25 : Fix indent.

 

Figure 2: Line 216, 217 Ulva pertusa is represented as Ulva not UP in the figure. Sargassum thunbergii is represented as Sargassum not ST as mentioned in the description of the figure.

 

 

Discussion:

 

Line 344: Was this seen in any other species? Did you see significant change in species abundance and/or richness in Gurepo/Padori vs Yeonpo?

Author Response

- The study shows the impact of natural recovery of the microbenthic food web 4 years after the Hebei Spirit oil spill in the western coast of South Korea. Isotopic ratios of polluted and clean sites show no significant difference suggesting recovery. The study is novel and shown the long-term consequence of oil spill on the microbenthic environment and its resiliency.

Response: Thanks for constructive comments.

Abstract:

- Succinct and to the point. However, a major element that needs to be emphasised (missing in the abstract) for the readers is the temporal aspect i.e. 4 years post spillage.

Response: As indicated by the reviewer, we have inserted the phrase '4 years after the Hebei Spirit oil spill' in the revised ms.

- Line 12: I would suggest adding “along Taean Peninsular on the western coast of Korea.

Response: As suggested by the reviewer, we have changed the phrase into 'along Taean Peninsula on the western coast of Republic of Korea' in the revised ms.

Introduction:

- Line 63: Brackets around references

Response: As indicated by the reviewer, we have added the bracket in the revised ms.

Materials and methods:

- Line 80-97 : While the study sites are described as rocky shores it would have been valuable for the reader to have a picture from the sites where the samples were collected from to give an understanding of the topology of the location.

Response: As suggested by the reviewer, we have modified 'Figure 1' in the revised ms.

Results:

- Table 2: Line 29 Why was Nereis heterocirrata included? Was there a reason for it?

- Table 2. Continued: The columns seem to be misaligned.

- Table 2 Continued. Line 33: Hima fratercula hypolia Why does it have an n =4 value but has missing mean and SD values in the Gurepo site?

- Table 2 Continued Line 25 : Fix indent.

Response: We made mistakes in some parts. As indicated by the reviewer, we have modified the wrong parts of Table 2 in the revised ms.

- Figure 2: Line 216, 217 Ulva pertusa is represented as Ulva not UP in the figure. Sargassum thunbergii is represented as Sargassum not ST as mentioned in the description of the figure.

Response: As indicated by the reviewer, we have modified the abbreviation in the revised ms.

Discussion:

- Line 344: Was this seen in any other species? Did you see significant change in species abundance and/or richness in Gurepo/Padori vs Yeonpo?

Response: Jung et al. (2017) reported that the densities of Lottia spp. and Odostomia aomori were higher in polluted sites than those in control site. In addition, they found significant differences of rocky intertidal macrobenthic communities between polluted and control sites the five years after the HSOS, that densities of the most dominant species were higher in the control site than in polluted sites. Thus, as suggested by the reviewer, we have added such information in the revised ms (Lines 346–351).

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