Low planktic foraminiferal diversity and abundance observed in a spring 2013 west–east Mediterranean Sea plankton tow transect

Mallo, Miguel; Ziveri, Patrizia; Mortyn, P. Graham; Schiebel, Ralf; Grelaud, Michael

doi:https://doi.org/10.5194/bg-14-2245-2017

Articles | Volume 14, issue 9

https://doi.org/10.5194/bg-14-2245-2017

© Author(s) 2017. This work is distributed under
the Creative Commons Attribution 3.0 License.

https://doi.org/10.5194/bg-14-2245-2017

© Author(s) 2017. This work is distributed under
the Creative Commons Attribution 3.0 License.

Articles | Volume 14, issue 9

Research article

|

04 May 2017

Research article |

| 04 May 2017

Low planktic foraminiferal diversity and abundance observed in a spring 2013 west–east Mediterranean Sea plankton tow transect

Miguel Mallo, Patrizia Ziveri, P. Graham Mortyn, Ralf Schiebel, and Michael Grelaud

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Final revised paper (published on 04 May 2017)
Supplement to the final revised paper
Preprint (discussion started on 14 Jul 2016)
Supplement to the preprint

Interactive discussion

Status: closed

AC: Author comment | RC: Referee comment | SC: Short comment | EC: Editor comment

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RC1: 'Review of Mallo et al', Anonymous Referee #1, 18 Jul 2016
- AC1: 'Response to Reviewer Comments- Referee #1', Patrizia Ziveri, 14 Oct 2016
  - AC2: 'Response to Reviewer Comments- Referee #1', Patrizia Ziveri, 14 Oct 2016
RC2: 'Review of Mallo et al.', Manuel Weinkauf, 29 Jul 2016
- AC5: 'Response to M. F. G. Weinkauf Referee #2 Comments', Patrizia Ziveri, 14 Oct 2016
RC3: 'Review of MS No.: bg-2016-266', Anonymous Referee #3, 03 Aug 2016
- AC3: 'Response to Reviewer Comments- Referee #3', Patrizia Ziveri, 14 Oct 2016

Peer-review completion

AR: Author's response | RR: Referee report | ED: Editor decision

ED: Reconsider after major revisions (17 Oct 2016) by Markus Kienast

AR by Patrizia Ziveri on behalf of the Authors (28 Nov 2016) Author's response Manuscript

ED: Referee Nomination & Report Request started (03 Dec 2016) by Markus Kienast

RR by Anonymous Referee #1 (09 Dec 2016)

Suggestions for revision or reasons for rejection

This is my second review of Mallo et al. ‘Low planktic foraminiferal diversity 1 and abundance observed in a spring 2013 West-East Mediterranean Sea plankton tow transect’. The authors analysed the data in a new way (PCA) and thoroughly changed the manuscript. As such it has improved considerably. However, it is still a difficult read (partly because the distribution of planktonic foraminifera is not an easy/straightforward issue), and I sometimes lost track while reading it, or simply couldn’t follow the conclusions. It would be good if the authors try to streamline the manuscript a bit more and make sure that the most important messages are not lost. In addition to many small comments I also still have some bigger issues that need to be clarified before I can recommend publication.

Statistical analyses:
While reading the ms I get repeatedly the impression that the authors relate foraminifera abundance or area density to a single environmental parameter (e.g. L276-283, L286-287, L613, these are just some examples). How did they distinguish between the influence of covarying environmental parameters? (and how is that possible by doing a PCA on the environmental parameters?). They have used the PCA to describe the variability in the environmental parameters and plotted the foraminifera data in the PCA space. These plots go some way towards a meaningful statistical analysis, but it is still hard to see (and impossible to quantify) the correlations to which the authors repeatedly refer.
It would make more sense to then use the PCA scores and see how these correlate (in a scatter plot) with the abundance or area density. Better still would be to use CCA to take both the environmental and the foraminiferal data into account.

Lunar cycles:
In response to my previous comment, the authors write:
We are aware that lunar cycle can influence the distribution of foraminifera. However, in our study the lunar day influence on the total absolute abundances (REV Fig. 2) was negligible.
First of all, it is unclear to me how that is evident from Fig. 2 (map of sample locations with chlorophyll-a concentration as background), so please explain. Also, I think this should be part of the manuscript, even a negative result is important and show that lunar paced abundance variability was at least considered as a possible mechanism. Moreover, was the influence of a lunar cycle on area density checked? It seems to me that this parameter would be extremely sensitive to the ontogenetic stage of the organism.

Area to long axis relationship:
In response to my previous comment, the authors write:
Size and mass of foraminifers relationship does not start at the origin. The proloculus of planktic foraminifera measures between 15-30 m in average, and has a certain calcite mass, which has so far not been determined (see Hemleben et al., 1989). We will use the power fit in the three species treated in Fig. S4 of the original manuscript for consistency reasons.

I’m happy to see that the species are treated consistently, but disagree with assertion that the curves – which are apparently interpreted as growth curves - should not go through origin. That is physically impossible.
As to the interpretation that these relationships reflect growth patterns, it seems that the relationships reflect regional differences in size, rather than ontogeny (Fig. S2). Do the authors think that they sampled shells at different ontogenetic stages at different locations (synchronized reproduction?)? It would be good if they commented on this. Also, were juvenile O. universa (without the spherical chamber) recognized/found?

Minor comments:
L16: it would be good to mention here the reason why are density was investigated.
L49: perhaps delete ‘source’ and mention the influence of temperature on seasonal abundance variability (Jonkers and Kučera, 2015; Zaric et al., 2005).
L67-69: I don’t quite understand this sentence about the different temperature and salinity ranges for water masses (and doubt that Be and Tolderlund is the right citation for that); please clarify.
L81: is it Gulf of Lion or of Lions?
L83: the terms distribution and daily fluxes are confusing to me, sediment traps do not provide daily fluxes, but integrate the flux over a certain time interval. Perhaps leaving distribution and daily out is better.
L85-87: this sentence is also unclear to me. Sediment traps provide information about the export flux of shells, not an abundance that is directly comparable to measurements from plankton nets. And if there is a correlation (or relationship?) between flux and nutrient supply (why nutrients? Forams don’t rely on nutrients) and water column conditions, then how does this work (which direction)?
L106-108: it would be good if the authors explicitly stated what SNW or area density can be used for, i.e. say that it may tell something about calcification intensity.
L112: add a space between spring and 2013. There are more cases where the space is missing between words (I guess because of the many changes in the document), please double check.
L138: is there really a longitudinal increase in insolation?
L146: add ‘s’ after become.
L165-167: please reword this sentence.
L175: replace PO4 and NO3 with PO43- and NO3- throughout the manuscript.
L186-187: Can you please reword this sentence, it is unclear to me what has been done.
L190: I guess the last statement about the exclusion of tests with attached organic matter only applies to the size/weight analyses, or not? If not, then please explain the reason why.
L191: consider changing ‘under optical microscopy.’ to ‘using optical microscopy.’
L218: I think the figure order needs to be updated, Fig. 7 should not appear before Fig. 3.
L248: space after ‘Overall,’.
L277: is food availability estimated/inferred from the fluorescence, make this explicit because food availability is not directly in the PCA? Perhaps this is unneeded, but it is important to realise that foraminifera rely on food, not on nutrients. But again, why do a PCA and then discuss individual environmental parameters and not use the scores?
L286-287: it would be helpful if the authors indicate the station number(s) in the text. Also, please explain how this correlation is evident from this plot.
L334: to what degree is the large IQR due to the low n?
L374-375: this statement should be part of the results.
L398: reword. Sediment traps provide shell flux.
L401: not Mediterranean studies (even though all the authors were from countries bordering the Med). Rigual-Hernandez analysed the >150 micron fraction, not the 63-150.
L408: the comparison with R-H is appropriate. This study is not from the Alboran Sea as is suggested here. Better compare to the other sediment trap studies from the Alboran Sea.
L410-411: I still think one cannot and should not extrapolate a few observations spread over several decades to suggest a trend. Moreover, ‘in the Mediterranean’ (L410) should be replaced with ‘this study’ and the ‘trend of changing conditions’ is a very vague description of what is happening to temperature and salinity and water mass mixing. If the authors insist on leaving this speculative statement in the ms they should at least analyse this properly (i.e. take the counted number of shell into account, calculate a rarefaction curve etc) and explain what and how the Med is changing and suggest a mechanism how this can affect species diversity.
L413: I somehow missed where it is discussed how ‘the ecology and distribution of planktic foraminifera’ could change due to these changing conditions. Please explain and provide evidence that the ecology is really changing (and what is meant with that).
L430: add a reference.
L433-434: reword ‘characterized by its wide temperature range’.
L440-442: the comparison with Cifelli doesn’t make sense here: L437-440 compare the Atlantic with the western Med, Cifelli compares western and eastern Med. The sentence is also very long and complicated, please reword.
L449: please add station numbers.
L454: reword ‘as due to….’
L455-456: May is not the month when G. ruber fluxes are highest in the Gulf of Lions or the Alboran Sea (it’s perhaps the month when total shell fluxes are highest).
L483-485: add reference and what is the rational behind the link between seasonal and spatial distribution?
495-496: I don’t understand this sentence. How does it match and why is bulloides mentioned?
L501-502: reword, it cannot be ‘In accordance with Cifelli’ and ‘whereas in our study’.
L506: replace ‘all the transect’ with ‘the whole transect’.
L509: what characteristic of bulloides correlates with fluorescence peaks (its abundance, relative abundance) and if it really correlates, then show the scatter plot.
L513: faster reproduction, how would that work? I know that Barcena et al say this, but struggle to grasp it. Where is the evidence? Reproductive success may be higher, population growth too, but faster reproduction?
L517: replace ‘higher’ with ‘larger’.
L524: water ‘column’ stratification.
L525: ‘being more present’: there seems to be a word missing.
L537: foraminiferal prey? Or fluorescence/chl a?
L541: planktonic foraminifera rely on food, not on nutrient, availability.
L544: reword ‘… was found ubiquitous…’
L547: there is an abundance peak of O. universa at station 16, so I don’t understand this sentence.
L552: ‘quite ubiquitous’ is very vague.
L639: misnumbered? Fig. S4a.
L640: suitable conditions?
L652: ‘effect of limited alimentation on calcification’. What is meant exactly? And I assume this only holds for bulloides?
L654-655: reword.
L660: the samples were collected in May 2013
L663: that looks more like the average and standard deviation than like a range.
L674: ‘rather balanced’ – what does that mean?
L679: ‘trophic conditions and food availability’ – what is the difference? And how is that clear from the analyses?

Jonkers, L., and Kučera, M.: Global analysis of seasonality in the shell flux of extant planktonic Foraminifera, Biogeosciences, 12, 2207-2226, 10.5194/bg-12-2207-2015, 2015.
Zaric, S., Donner, B., Fischer, G., Mulitza, S., and Wefer, G.: Sensitivity of planktic foraminifera to sea surface temperature and export production as derived from sediment trap data, Marine Micropaleontology, 55, 75-105, 2005.

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RR by Anonymous Referee #3 (12 Dec 2016)

Suggestions for revision or reasons for rejection

Dear
Biogeosciences Editorial Board

I hereby you receive my second report on the MS " Low planktic foraminiferal diversity and abundance observed in a spring 2013 West-East Mediterranean Sea transect” by Mallo et al.

After the first run of reviewer procedure, this version of the manuscript is ready for publication. The authors included in this version of the manuscript most of the suggestion of the previous reviewer and the PCA analysis, suggested by all the previous reviewers, clearly supports the interpretation of data. The manuscript results properly constructed and all figures are representative and useful for this version of the manuscript.

Minor comments:
Line 109: delete the double point
Line 171: delete the double parenthesis
Line 227: delete double parenthesis close to (without sac)). Substitute the parenthesis before G. ruber with bracket. Substitute the parenthesis after O. universa with a bracket. Delete the parenthesis after Figure 7.
Line 248: please let space between words Overall,higher
Line 383: I would like only to make a small comment concerning the differences for the occurrence of G. elongatus. It is important to take in account that the time interval covered by the 2 cm of sediment analysed by Thunell (1978) is variable between some centuries to one or two millennia. This issue is important to consider because of recently Margaritelli et al (2016), in the central Tyrrhenian Sea fossil record, found G. elongatus over the last 4 millennia and the last specimens of this species are recorded in the last two centuries.
Line 392: I would like to suggest to add more references concerning sedimentary cores. The manuscript is focused on living forams so that I would like to see references also concerning the last millennia (i.e., Margaritelli et al., 2016 or others).
Line 401: Pujol & Vergraud-Grazzini 1995 and not 1998
Paragraph 4.2: In this paragraph, the authors discuss the Figure 6, but the previous paragraph is mainly focused on figure 7. Is it possible to find a solution? It is enough anomalous.
Line 480: please let space between words Pujol & Vergraud-Grazzini (1995),In winter
Line 610: please let space between words G. ruber (white)is only

All the best
Fabrizio Lirer

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RR by Manuel Weinkauf (16 Dec 2016)

ED: Reconsider after major revisions (20 Dec 2016) by Markus Kienast

AR by Patrizia Ziveri on behalf of the Authors (01 Feb 2017)

ED: Referee Nomination & Report Request started (13 Feb 2017) by Markus Kienast

RR by Anonymous Referee #1 (16 Feb 2017)

Suggestions for revision or reasons for rejection

Please find my third review of the manuscript by Mallo et al. In general, the manuscript has improved further and now reads considerably better than the previous versions. The authors also satisfyingly respond to the comments I raised earlier, but in many cases, do not include their response in the manuscript. This holds particularly true for the issue I raised on the possibility of lunar periodicity on abundance and area density, but my other major comments are also not fully addressed in the ms. So, I’m afraid that a few minor changes are still necessary before the paper can be accepted for publication.

I welcome the new plots showing the PCA factor scores vs. abundance and delta-a in the rebuttal. It’s good to see the results included in table form in the ms, but I suggest the plots should be made available in the supplementary materials too. Visual information always work better than dry text. And the explanation of the variation in abundance is after all the most important topic of this manuscript.
In reply to my previous comment, the authors agree that the abundance of foraminifera is ‘usually not related to a unique environmental parameter’. This was exactly my point and it is good to see that we’re on the same page regarding this point. However, I think the authors should make this clearer in the manuscript and consistently use the results of the PCA. For instance, in L284 and L292 the PCA axis 1 is further reduced and suggested to reflect only food availability, whereas one cannot distinguish between food and temperature because they are correlated. Moreover, the results of the PCA are not even mentioned in the discussion. This leaves me with the feeling that it was just added to the manuscript to satisfy the reviewers, but not really taken into account in new, or more careful interpretation of the data. This should be addressed in a revised version.

Then the second point about the lunar periodicity. Again, I’m happy the see the data and to see what the authors actually did. Apart from a fundamental issue with this analysis, I really wonder why this is not part of the manuscript. I asked for it twice and the authors fail to convince me that there is a reason not to include it in some way in the manuscript. In fact, their response is more or less fine, carefully worded at least. However, more fundamentally, why would any parameter by linearly related to the lunar day? Wouldn’t one expect some kind of cyclic pattern (e.g. Bijma et al., 1994)? And why treat all species together? Some species may not show any cycles, some may have two, rather than one per lunar month, the phasing may differ, etc. Lumping them together may obscure any trend and the authors therefore fail to convince that there really is no influence of a lunar cycle. So, I think this still needs to be addressed in the paper, irrespective of whether there is any detectable influence of a lunar cycle or not.

Area-long axis relationships: I questioned whether these reflect growth and I am not convinced by the authors’ reply. They state themselves that there are regional differences in size. If one would interpret this as regional differences in growth (juveniles in one area, adults in another) then there is of course no problem (but this would point to some kind of synchronisation of ontogeny), but I don’t think that this is what the authors mean. Perhaps they need to explain better, or refrain from suggesting that these curves reflect ontogenetic growth.

In the revised version the authors frequently mention the influence of thermal stratification on the abundance/distribution of foraminifera. While this may be true – especially via the proposed links to food availability – it makes me wonder why stratification was not taken into account in the PCA. If the authors think stratification is such an important environmental parameter, then I think they should.

Changing ecology (L404): I think I commented on this before. To me changing ecology means that the habitat preferences of the individual species change (e.g. that a warm-water species adapts and becomes a cold-water species). I don’t think this is what the authors want to suggest (they provide no evidence for it in any case) and suggest that they rephrase.

Minor points:

L487: add space after Atlantic

L496: add space after concentration

L506: add space after it

L511: word missing?

L541-542: main species where it is rare? Perhaps reword to make clearer what is meant here.

L571-572: if delta-a of O. universa would be related to food availability too, wouldn’t one then expect a clear west-east gradient?

Bijma, J., Hemleben, C., Wellnitz, K., 1994. Lunar-influenced carbonate flux of the planktic foraminifer Globigerinoides sacculifer (Brady) from the central Red Sea. Deep Sea Research Part I: Oceanographic Research Papers 41, 511-530.

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RR by Manuel Weinkauf (17 Feb 2017)

ED: Publish subject to minor revisions (Editor review) (21 Feb 2017) by Markus Kienast

AR by Patrizia Ziveri on behalf of the Authors (07 Mar 2017) Author's response Manuscript

ED: Publish as is (12 Mar 2017) by Markus Kienast

AR by Patrizia Ziveri on behalf of the Authors (14 Mar 2017) Manuscript

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Short summary

Single-celled living calcareous planktic foraminifera data across the Mediterranean Sea suggest that stratification of the surface water column, food availability, temperature, and seawater carbonate chemistry are the main factors controlling their distribution and mass. Increasing temperature, salinity, surface ocean stratification, and trophic conditions could be the causes of reduced abundance, diversity and species-specific changes in calcification in planktic foraminifera.