the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
| 31 Jul 2024
Effects of photosymbiosis and related processes on planktic foraminifera-bound nitrogen isotopes in South Atlantic sediments
Abstract. Foraminifera often form symbiotic relationships with photosynthetic algae, providing a host environment and inorganic nutrients in exchange for photosynthetic organic matter from the algal symbiont. To date, the history of this relationship has been studied in paleoceanographic records with the oxygen and carbon stable isotopes of foraminiferal calcite. More recently, photosymbiotic activity has been observed to impact the nitrogen isotope ratio (δ15N) of foraminiferal tissue and the organic matter incorporated into foraminiferal tests. Dinoflagellate symbiont-bearing species appear to be lower in δ15N than symbiont-barren species and more similar to their feeding sources, likely due to their retention of low-δ15N metabolic ammonium and thus a weaker amplitude for the “trophic enrichment factor,” the δ15N increase per trophic level that is widely observed in food webs. We report new glacial/interglacial foraminifera-bound δ15N (FB-δ15N) data from Deep Sea Drilling Program Site 516, located in the subtropical South Atlantic gyre, which contains multiple foraminifera species at adequately high abundance for inter-species comparison of foraminiferal nitrogen, carbon, and oxygen isotopes over a full glacial cycle. Our data show a conserved δ15N difference of 3–5 ‰ between dinoflagellate-bearing species and the other species, qualitatively consistent with, but greater in amplitude than, the δ15N difference observed in previous modern ocean and core-top studies. We propose that this greater amplitude is the result of lateral transport of symbiont-barren species into the South Atlantic subtropical gyre, which appears to represent a small region of low thermocline nitrate δ15N surrounded by regions with higher thermocline nitrate δ15N. The data point to FB-δ15N as the best available proxy for dinoflagellate symbiosis. However, they also suggest caution in regions with strong gradients, where species from contrasting environments occur in a single sediment sample.
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RC1: 'Comment on egusphere-2024-2291', Rocco Gennari, 05 Sep 2024
Dear Authors and Editor,
I found the manuscript entitled "Effects of photosymbiosis and related processes on planktic foraminifera-bound nitrogen isotopes in South Atlantic sediments" by Auderset et al. very interesting as it shed light on potential bias in using the FB-∂15N in particular oceanographic areas. The manuscript also explain clearly how this method has the potential to discern among different type of symbiont hosted in foraminifera and non symbiont-bearing foraminifera. The manuscript is well written and clearly present data and discuss them. I just found several unclear aspect in some sentences, figures or references to figures, which were highlighted as comment or insert in the attached PDF. For this reasons I think that after the review of the authors the manuscript could be ready for publication, depending on the comments of other reviewers and of the editor.
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RC2: 'Comment on egusphere-2024-2291', Anonymous Referee #2, 09 Sep 2024
General comments:
The manuscript entitled “Effects of photosymbiosis and related processes on planktic foraminifera-bound nitrogen isotopes in South Atlantic sediments” by Auderset et al. reported the species-specific FB-δ15N from sediment core samples together with test δ13C and δ18O, which is important to validate the utility of FB-δ15N to detect fossil foraminiferal photosymbiosis. They found consistently lower FB-δ15N on dinoflagellate-bearing foraminifera than non-dinoflagellate/non-symbiotic species. They also discussed the offset between the dinoflagellate-bearing species’ FB-δ15N and others, especially an exceptionally high offset in DSDP Site 516 compared to the global compilation of FB-δ15N. They proposed the possible influence of regional differences in nitrate δ15N. This study is important to gain our understanding of the FB-δ15N proxy as a tool to detect fossil photosymbiosis, and as a tool to reconstruct past N cycling. This study presents invaluable information on FB-δ15N, which will fuel future studies in this field.
The manuscript is overall well-written, and carefully discussed with adequate data sets. However, some statistical representations seem incorrect, and some discussions need to be reformulated. The paper would be more improved if the following points are fully considered.
Specific comments:
1. Size-specific δ13C
I would recommend not to use R2 as a metric of the strength of relationships. In the first place, R2 is not a “regression coefficient (L206)” but a “coefficient of determination”, a measure of the proportion of the variance in the dependent variable that is explained by the independent variables in the regression model (goodness-of-fit). Regression coefficient is a slope in a linear regression model. I assume the authors intended to say “correlation coefficient (normally denoted by r)” in this sentence. Please report the r and p-value together in Table S1. In addition, R2 for G. bulloides (R2 =1.00) is meaningless since it is the result of two-point linear regression (n=2). It can be omitted or the sample size should be shown in the same table.
I would like to confirm the largest size class of each species. 400um is large enough for G. ruber but may be still in the juvenile stage for species like G. siphonifera which often reaches 800um in maximum length. For example, Bornemann and Norris (2007) measured size-specific δ13C of modern species, and they used 13 size fractions ranging from 75um to 800um. Having this in mind, the size range from 250um to 400um (or 425um?) used in this study seems too narrow to detect size trends. I won’t argue that more size fraction is needed, but caution needs to be paid in the discussion. Please present the largest size class for each species in the sample so that the readers can determine whether the specimens are juvenile or adult/gametogenic stage.
In terms of G. siphonifera’s size-δ13C trend, an experimental study by Bijma et al. (1998) is helpful to understand the phenomenon. In their study, G. siphonifera type II showed steeper slope than type I. Also, they proposed that effective utilization of the host’s respired CO2 by symbionts inside the test may reduce the effect of δ13C increase of surrounding microenvironmental seawater DIC. This phenomenon is supported by the recent experimental study by Takagi et al. (2022) which focused on symbiont photosynthesis.
2. Size-specific δ18O
At L212-L217, the authors describe the size-specific δ18O trend with the regression parameters like the size-specific δ13C discussion, but I don’t see any clear correlation between test size and δ18O based on Fig. S3. I think this part should be fully rewritten.
3. Supplementary discussion
I suggest including supplementary discussion, especially “Influence of depth habitat on carbonate δ13C and δ18O”, in the main text. The reason why there is very little difference in δ13C between dinoflagellate-bearing species and non-symbiotic G. truncatulinoides is not clear from the current discussion in the main text alone (L271-272), but the depth profile of δ13CDIC gives reasonable interpretation.
4. FB-δ15N of G. siphonifera
In 4.3, the authors discuss the factors explaining the high values of FB-δ15N of G. siphonifera from the viewpoint of symbiont digestion. Please check the ontogenetic dynamics of G. siphonifera chlorophyll content in Takagi et al. (2016, Marine Micropaleontology). Based on that study, the peak chlorophyll content of G. siphonifera was always observed before the final chamber formation (or even earlier). At the time of final chamber formation, the largest or second-largest chamber consisting of the majority of calcite mass, the chlorophyll content gets very low, which seems to support the authors’ discussion. Alternatively, I think there is a possibility that the physiology of algae (or interaction between the host and the symbionts) may differ between dinoflagellate-symbiont and others. According to Uhle et al. (1999), FB-δ15N can vary tremendously based on the source and pathways of nitrogen within the host-symbiont system (from NO3- diffusion or from recycled NH4+ pool). Uhle et al. (1999) demonstrated the importance of the NH4+ pool for dinoflagellate-symbiosis, but it may not be the case for pelagophytes. If the non-dinoflagellate symbiont can uptake nitrate from environmental seawater enough efficiently, the recycled NH4+ pool may be not so important and the remaining nitrogen is supplied by diets. Although there are many unknowns, physiological differences should exist between dinoflagellate (relatively large in size, ~10um) and pelagophyte (~1-2um) to some extent. In any case, I believe such physiological differences may also affect the FB-δ15N differences and so should be considered.
5. Discussion on lateral transport
The authors discuss the possibility of lateral transport of G. bulloides and G. siphonifera from outside of the gyre based on the nitrate δ15N profile of the North Atlantic. First, I would like to know whether the difference in δ15N between the inside and outside of such a gyre can be generalized. The example the author showed is of the North Atlantic, with δ15N difference of 2–3‰. Is this the only example that can be referred to? If the authors want to assume the same mechanism in the DSDP Site 516, I believe at least multiple examples (examples of δ15N difference between inside and outside gyre, regardless of the region) are needed. Please be very careful when applying a specific phenomenon to your case. Without adequate generalization, discussion sounds opportunistic. Next, I wonder if it is possible to transport specific species. If their lateral transport hypothesis is true, why not for the other species? Lateral transport is a physical process, so I imagine that there should be no selectivity if they share the same habitat. In addition, I wonder if the amount of laterally transported specimens can exceed over the local population. Based on the authors’ argument, I understand that they assume most of the specimens of G. bulloides and G. siphonifera are from outside of the gyre (2–3‰ difference is directly reflected in the foraminifera). Unless the amount of the transported specimens is large enough, a mixture of the local population and transported specimens makes the resultant FB-δ15N deviation more subtle. In my impression, discussing lateral transport is fine, but the tone needs to be down.
6. Geochemical proxy for photosymbiosis
I believe FB-δ15N has great potential as a useful tool to distinguish fossil foraminiferal photosymbiosis. As with size-specific δ13C, not all tools are perfect, but their combination will enhance our understanding of the phenomenon. I would like to encourage the authors to emphasize the potential of this proxy. Specifically, the FB-δ15N differs from δ13C-based reconstructions of photosymbiosis in that it can differentiate symbiont species (dinoflagellate or not), which is a great advantage in reconstructing photosymbiotic partnership through evolutionary timescales. I understand that the manuscript addresses important aspects of the limitation of the proxy or points to be aware of, but the more positive argument for the usefulness of this proxy would make this paper more appealing.
Technical corrections
Text overall: The style of in text references need to be checked. There are many parentheses within parentheses, and sometimes only one side parenthesis. Please check the journal format and correct them.
L91: …by feeding on foraminiferal feeding on algal cells.
by foraminiferal feeding on algal cells
L95: shell or test
Please keep consistent wording.
L97: …(Spero et al., 1991). Period is missing.
L108: planktonic foraminifera
In this paper, the author uses “planktic” instead of “planktonic” in the title. Please keep it consistent.
L156–165: In this paragraph, both chemical names and chemical formula are used. I suggest to use chemical formula consistently (nitrate in L156→NO3-, nitrite in L161→NO2-).
L167: 250-400μm size fraction
Specimens for FB-δ15N were picked from 250-425μm size fraction (L131). I suppose 400 may be 425, since the largest fraction is >400μm (L172).
L183: The title of this section is the same as the previous one. Probably something like “Age model”?
L217-218: This paragraph can be deleted since the discussion and related figure are all completed in supplementary materials.
L246: 4.2…carbon isotopes in DSDP Site 516 ---> at DSDP Site 516 (for consistency to 4.1)
L294: foraminifer --> foraminifera (for consistency)
L312: G. menardi --> G. menardii
L325, 329: Please correct the spell of “dinoflagellate”.
L353: PON --> need to represent abbreviation (particulate organic matter) or unify the term to PN which is used in the text prior to this.
Caption of Fig. 2: G. siphoniphera (typo) ---> G. siphonifera
Fig. 2d: The δ13C of benthic stack cannot be seen clearly because of overlap. There appears to be no discussion on this profile, so it may be removed. In addition, the caption says “benthic stack of South Atlantic cores at shallow depths (Lisiecki et al., 2008)”, but the one I found in the reference paper was for shallow North Atlantic sites. Is it correct?
Fig.4c: The labels of the vertical arrows should be reversed (higher δ13C should be higher photosynthesis).
Caption of Fig. 4: Distinction --> distinction
Fig. 5: The category of G. hirsuta here is “chrysophyte or pelagophyte symbionts”, but I think this should be symbiont-barren. Although Gastrich (1987) reported chrysophyte from this species, later on Hemleben et al. (1989) further analyzed this species and concluded that algae in this species should be prey. The other related paper to the authors study also categorize G. hirsuta to symbiont-barren (see Smart et al. 2018 for example). Likewise, please show the reference for G. tumida symbionts. I don’t know whether this species has been investigated for symbiosis.
Fig. 9: “(‰)” is not necessary
Caption of Fig. 9: “dinoflagellate hosting foraminifera” ---> “dinoflagellate-bearing foraminifera” is better for consistency.
Supplementary material 1st page, 1st section: …compilation (Fig. S2 b,c,e) ---> Fig.S3
Supplementary material 2nd page, 2nd row: G. ruber and G. siphonifera δ13C seem to be higher than T. sacculifer… ---> lower (or more depleted)
Caption of Fig. S2, S3: “(d) G. bulloides, … and (f) G. truncatulinoides” ---> Opposite. (d) is G. truncatulinoides and (f) is G. bulloides.
Table S1: G.Siphonifera (typo) --> G. siphonifera
Citation: https://doi.org/10.5194/egusphere-2024-2291-RC2
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