the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
| 05 Dec 2024
Decreasing foraminiferal flux in response to ongoing climate change in the Santa Barbara Basin, California
Abstract. The rapid response of foraminiferal assemblages to changing climate makes their shells an invaluable geological record of the past. However, the time frame over which foraminifera respond to climatic signals and the specific drivers influencing assemblage composition and abundance remain obscure. We focus on the impact of ongoing, anthropogenic climate change on planktic foraminifera in the California Current ecosystem, which would appear as a nearly instantaneous event in the sediment record. The Santa Barbara Basin sediment trap, located off the coast of California, USA since 1993, provides a 28-year record of particulate and foraminiferal flux to the basin’s seafloor. The sediment trap captures the superposition of the annual cycle of seasonal upwelling, Pacific multiannual El Niño-Southern Oscillation-driven temperature changes, and anthropogenically forced climate change. We present data on planktic foraminiferal flux collected between 2014–2021, at two-week intervals (164 samples, 60,006 individuals) and compare results to previously published data from 1993–1998. Consistent with previous studies, the most abundant species from 2014–2021 were Globigerina bulloides, Neogloboquadrina incompta, and Turborotalita quinqueloba, with peak fluxes occurring in the spring and summer. Lower fluxes and an increase in the abundance of N. incompta and subtropical species characterize the winter season. We find a 37.9 % decrease in total foraminiferal flux relative to the 1990s, primarily driven by a decrease in G. bulloides abundance. This decrease is accompanied by a 21.9 % overall reduction in calcium carbonate flux. We also find a decrease in the relative abundance of subtropical species (Globigerinoides ruber, Orbulina universa, Neogloboquadrina dutertrei) and their fluxes compared to the 1990s, contrary to expectations if assemblages and fluxes were to follow anthropogenic warming signals. We hypothesize that the observed decrease in subtropical species abundance and flux is likely related to an increase in acidification and in the timing and magnitude of upwelling along the California coast. The extremely rapid responses of foraminifera to ongoing changes in carbonate chemistry and temperature suggest that climate change is already having a meaningful impact on coastal carbon cycling. The observed decrease in particulate inorganic carbon (PIC) flux relative to particulate organic carbon (POC) flux may facilitate increased oceanic uptake of atmospheric CO2.
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RC1: 'Comment on egusphere-2024-3374', Anonymous Referee #1, 11 Jan 2025
Harvard et al. showed assemblages and fluxes of planktic foraminifers in sediment trap samples moored at Santa Barbara Basin in 2014-2021. Compared to data from 1993-1998, fluxes especially G. bulloides decreases. Contrary to the anthropogenic warming trend, relative abundances of subtroical species also decreases. Authors hypothesize widely acidified seawater in the upwelling is related to the foraminiferal changes. Hard work of authors provides a useful dataset to capture the rapid shift of foraminiferal assemblages and abundances in thirty years. Although the analyses are conventional methodology, the novelty of dataset showing the potential impact of environmental change is suitable for the scope of the journal.
I have following major comments.
First, assemblage analyses of foraminifer do not yield direct relationships between environmental parameters and fluxes or assemblages. As authors shown in Figs. 5 and 6 and table 2, related environmental factors to fluxes of the most abundant G. bulloides is unclear. In line 438-441, G.bulloides is an indicator of primary productivity but is negatively correlated to OC and opal, which are primary productivity indicators. And I consider that negative association between G. bulloides fluxes and pH means acidification may not negatively affect G. bulloides fluxes (I think this may be a descriptive problem).They appears to be a contradiction. Direct impact of acidification on foraminiferal fluxes is not confirmed by the results demonstrated in the manuscript. The statistical analysis does not confirm that acidification is related to the change of foraminiferal assemblages.
Authors do not compare fluctuation of environmental parameters and foraminiferal fluxes between 2014-2021 and 1993-1998. I understand this is difficult, but the drivers in the decline of foraminifer fluxes could not determined directly only by relationship environmental parameters and fluxes in 2014-2021. For example, because major species do not have symbionts and depend on feeding, is flux decreases related to the possibility of change of food in the basin? Therefore, I recommend that the authors make some revisions to clarify their study.
The followings is minor comments;
In manuscript, data of sinking particle components are missing. It is difficult to confirm the discussion and statistical analyses without the data.
Citation: https://doi.org/10.5194/egusphere-2024-3374-RC1 -
AC1: 'Reply on RC1', Emily Havard, 12 Feb 2025
We’d like to thank Reviewer 1 for their comments which we feel will allow us to improve and clarify our manuscript.
RC1: As authors shown in Figs. 5 and 6 and table 2, related environmental factors to fluxes of the most abundant G. bulloides is unclear. In line 438-441, G.bulloides is an indicator of primary productivity but is negatively correlated to OC and opal, which are primary productivity indicators. And I consider that negative association between G. bulloides fluxes and pH means acidification may not negatively affect G. bulloides fluxes (I think this may be a descriptive problem).
We have clarified the description of the relationships between G. bulloides and environmental parameters.
Proposed revision: “This species is further positively associated with surface dissolved oxygen which has many possible drivers, including primary productivity, the properties of upwelled waters, and seasonal currents (Fig. 6). However, Globigerina bulloides is negatively associated with environmental variables that are positively associated with upwelling (CUTI), including pH, organic carbon, nitrogen, and opal (Fig. 6). The negative association between G. bulloides and opal flux suggests that G. bulloides feeds on a variety of phytoplankton in SBB, rather than primarily on diatoms.”
RC1: Direct impact of acidification on foraminiferal fluxes is not confirmed by the results demonstrated in the manuscript. The statistical analysis does not confirm that acidification is related to the change of foraminiferal assemblages.
Acidification is a hypothesis presented as a possible explanation for the results that we see in our study. Given the co-linearities between environmental parameters, the complexity of this data set, and the paucity of carbonate chemistry for the 1993-1998 interval, no single parameter can statistically explain the assemblage change, nor would we expect this. However, we feel our hypothesis is supported by the observed increase in upwelling strength and duration between the two time periods as well as what is already understood about the ecology and susceptibility to acidification of these species. We will clarify that this remains a hypothesis in the body of the manuscript.
RC1: Authors do not compare fluctuation of environmental parameters and foraminiferal fluxes between 2014-2021 and 1993-1998. I understand this is difficult, but the drivers in the decline of foraminifer fluxes could not determined directly only by relationship environmental parameters and fluxes in 2014-2021.
This is correct. Unfortunately, some of the environmental data that we relied upon from 2014-2021 in SBB is spotty or non-existent between 1993-1998. Thus, we were unable to meaningfully compare environmental data from the two time periods. We explored long term trends in the available datasets of Coastal Upwelling Transport Index, foraminiferal flux, carbonate flux, organic carbon flux, and temperature, which form the basis of our hypothesis about acidification along with existing literature from the region. We used the environmental parameters from 2014-2021 to better understand the relationships between each species and seasonal environmental variability. A line will be added to the methods making explicit the lack of some environmental data from 1993-1998.
RC1: For example, because major species do not have symbionts and depend on feeding, is flux decreases related to the possibility of change of food in the basin?
This is a good point and certainly a possibility, but one we are unable to directly test this with our dataset. Existing knowledge about dietary preferences is vague and prey data is limited. Many of these species primarily feed on phytoplankton, and there has not been a major change in primary productivity (Catlett et al., 2021; Schiebel and Hemleben, 2017). More specific prey preferences remain poorly defined. As G. bulloides is known to be an opportunistic feeder, a change in food type is unlikely to affect them to an extent that would explain the decrease in flux we observe. A line will be added to the discussion raising the possibility of prey availability as a driver of assemblage change, though an unlikely primary driver in G. bulloides.
RC1: The followings is minor comments;
In manuscript, data of sinking particle components are missing. It is difficult to confirm the discussion and statistical analyses without the data.
Thank you for pointing this out. We will include particle flux data from the sediment trap in our supplement.
References
Catlett, D., Siegel, D. A., Simons, R. D., Guillocheau, N., Henderikx-Freitas, F., and Thomas, C. S.: Diagnosing seasonal to multi-decadal phytoplankton group dynamics in a highly productive coastal ecosystem, Prog Oceanogr, 197, 102637, https://doi.org/10.1016/J.POCEAN.2021.102637, 2021.
Schiebel, R. and Hemleben, C.: Planktic Foraminifers in the Modern Ocean, 2017.
Citation: https://doi.org/10.5194/egusphere-2024-3374-AC1
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AC1: 'Reply on RC1', Emily Havard, 12 Feb 2025
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RC2: 'Comment on egusphere-2024-3374', Anonymous Referee #2, 22 Jan 2025
The study of Harvard et al. uses a 28-year sediment trap record to investigate the impact of ongoing climate change on planktonic foraminiferal flux in the Santa Barbara Basin. The authors compare recent data to older records and find a significant decline in foraminiferal flux, particularly for Globigerina bulloides, alongside reduced calcium carbonate flux. They hypothesize that acidification and changes in upwelling dynamics are key drivers of these trends, highlighting the rapid response of foraminifera to environmental changes.
Firstly, I would like to thank the authors for providing this valuable long-term time series of planktonic foraminifera flux in the Santa Barbara Basin. This dataset represents an important environmental and ecological record, offering critical insights into the impacts of climate change on marine ecosystems.
If true, the decline in foraminifera shown here is alerting. However, one concern lies in the comparison between the 2014–2021 sediment trap data and the older dataset from 1993–1998. The study does not account for potential long-term changes in the size of planktonic foraminifera, which are thought to decrease due to warming/climate change (Deutsch et al., 2022) and especially during intensified upwelling (10.22541/au.171987328.88940417/v1). As the measurements are constrained to specimens larger than 125 microns, it is possible that smaller specimens, potentially more abundant over time, are passing through the sieve. This could artificially amplify the reported decline in abundance and flux. (Perhaps the fact that T. quinqueloba is a small species explains its flux consistency.) Addressing/discussing this aspect would strengthen the conclusions and provide a more accurate assessment of climate-driven changes in foraminiferal populations.
The authors emphasize ocean acidification as a major factor influencing planktonic foraminifera fluxes and abundances but focus only on its biotic effects. While basin waters are clearly acidifying due to anthropogenic emissions and intensified upwelling, the impact especially on living foraminifera remains debated (Leung et al., 2022). What is certain, however, is that acidification promotes post-mortem shell dissolution (unprotected shells), with significant carbonate loss occurring in the upper 300m (Kwon et al., 2024). Oxygen-rich waters can also intensify dissolution/acidification due to enhanced organic matter oxidation. A key concern is thus whether the observed decline in foraminiferal abundances in sediment trap data may instead reflect post-mortem dissolution of their shells in increasingly acidified waters. Smaller specimens, which are more prone to dissolution, may be disproportionately affected, especially given the potential long-term size reduction in planktonic foraminifera due to climate change. This raises the possibility that the decline in abundance is not solely a biological signal but also a taphonomic one. Greater clarity on how acidification influences both living populations and the preservation of their fossil remains would provide a more robust interpretation of these data.
Further on taphonomy, some specimens in Figure A1 appear slightly etched. Could those be resuspended material in the traps? Were any benthic specimens observed? This is a usual phenomenon is some sediment traps.
Minor
Methods: Please consider briefly explaining in the methods section what loadings and directions represent in Canonical Correlation Analysis to aid reader understanding.Lines 65-69: Partly true. Thinning can also be due to adaptation. Results indicate that salinity significantly influences pteropod distribution (Johnson et al., 2023), while their biomineralization is affected by salinity due to its role in buoyancy regulation (Manno et al., 2012). Similarly, calcification changes for buoyancy regulation have also been suggested for foraminifera (Zarkogiannis et al., 2019).
In a future submission please consider changing planktic to planktonic. The correct adjective form of plankton is planktonic. The adjectives of Greek nouns ending in -on get the suffix -ic in the end like plankton – planktonic, bion – bionic, lacon – laconic. This is different to nouns ending in -os, which lose the ending -os to the previous consonant by replacing it with -ic, like bentos – benthic, cosmos – cosmic or chronos – chronic.
References
Deutsch, C., Penn, J. L., Verberk, W. C. E. P., Inomura, K., Endress, M.-G., and Payne, J. L.: Impact of warming on aquatic body sizes explained by metabolic scaling from microbes to macrofauna, Proc. Nat. Acad. Sci., 119, e2201345119, 10.1073/pnas.2201345119, 2022.
Johnson, R., Manno, C., and Ziveri, P.: Shelled pteropod abundance and distribution across the Mediterranean Sea during spring, Prog. Oceanogr., 210, 102930, 10.1016/j.pocean.2022.102930, 2023.
Kwon, E. Y., Dunne, J. P., and Lee, K.: Biological export production controls upper ocean calcium carbonate dissolution and CO2 buffer capacity, Science Advances, 10, eadl0779, 10.1126/sciadv.adl0779, 2024.
Leung, J. Y. S., Zhang, S., and Connell, S. D.: Is Ocean Acidification Really a Threat to Marine Calcifiers? A Systematic Review and Meta-Analysis of 980+ Studies Spanning Two Decades, Small, 18, 2107407, 10.1002/smll.202107407, 2022.
Manno, C., Morata, N., and Primicerio, R.: Limacina retroversa's response to combined effects of ocean acidification and sea water freshening, Estuar. Coast. Shelf Sci., 113, 163-171, 10.1016/j.ecss.2012.07.019, 2012.
Zarkogiannis, S. D., Antonarakou, A., Tripati, A., Kontakiotis, G., Mortyn, P. G., Drinia, H., and Greaves, M.: Influence of surface ocean density on planktonic foraminifera calcification, Sci. Rep., 9, 533, 10.1038/s41598-018-36935-7, 2019.Citation: https://doi.org/10.5194/egusphere-2024-3374-RC2 -
AC2: 'Reply on RC2', Emily Havard, 12 Feb 2025
We thank Reviewer 2 for their thoughtful comments, especially regarding broadening the perspective of our manuscript to consider additional discussion points.
RC2: The study does not account for potential long-term changes in the size of planktonic foraminifera, which are thought to decrease due to warming/climate change (Deutsch et al., 2022) and especially during intensified upwelling (10.22541/au.171987328.88940417/v1). As the measurements are constrained to specimens larger than 125 microns, it is possible that smaller specimens, potentially more abundant over time, are passing through the sieve. This could artificially amplify the reported decline in abundance and flux. (Perhaps the fact that T. quinqueloba is a small species explains its flux consistency.) Addressing/discussing this aspect would strengthen the conclusions and provide a more accurate assessment of climate-driven changes in foraminiferal populations.
We agree that size of foraminifera is an important aspect to consider. The cutoff of 125 μm was chosen for consistency with studies from 1993-1998 (Kincaid et al. 2000; Black et al. 2001). As smaller foraminifera were not included from 1993-1998, a robust comparison would not have been possible for us. While we would not rule out that a change in size or calcification has cooccurred with assemblage change, we would not expect this to meaningfully impact our assemblage data. If decreasing foraminifera size were responsible for the observed decrease in flux, we would expect to see a decrease in abundance of the smallest species over time. We find the opposite: the fluxes of the two most common species small enough to straddle the 125 μm cutoff, T. quinqueloba and G. glutinata, remain consistent or slightly increase. The decrease in G. bulloides flux is the greatest contributor to the total flux decrease, and this species is consistently larger than 125 μm in Santa Barbara Basin.
In order to account for a potential change in particle size over time and other sources of carbonate to the seafloor, we include the total carbonate flux from the sediment trap, presented as g/m2/d rather than # of foraminifera/m2/day. Both total carbonate flux and foraminiferal flux decrease across the studied time period, but the broader conclusions about carbon cycling and PIC/POC are made using the total carbonate and total organic carbon flux data from the sediment trap.
RC2: The authors emphasize ocean acidification as a major factor influencing planktonic foraminifera fluxes and abundances but focus only on its biotic effects. While basin waters are clearly acidifying due to anthropogenic emissions and intensified upwelling, the impact especially on living foraminifera remains debated (Leung et al., 2022). What is certain, however, is that acidification promotes post-mortem shell dissolution (unprotected shells), with significant carbonate loss occurring in the upper 300m (Kwon et al., 2024). Oxygen-rich waters can also intensify dissolution/acidification due to enhanced organic matter oxidation. A key concern is thus whether the observed decline in foraminiferal abundances in sediment trap data may instead reflect post-mortem dissolution of their shells in increasingly acidified waters. Smaller specimens, which are more prone to dissolution, may be disproportionately affected, especially given the potential long-term size reduction in planktonic foraminifera due to climate change. This raises the possibility that the decline in abundance is not solely a biological signal but also a taphonomic one. Greater clarity on how acidification influences both living populations and the preservation of their fossil remains would provide a more robust interpretation of these data.
While this is an active area of research, many studies have explored the impacts of acidification on fossil and modern planktic foraminifera, though we note that there is more nuance in benthic foraminifera (especially larger symbiont-bearing species) (Davis et al., 2017; De Moel et al., 2009; Dong et al., 2022; Moy et al., 2009; Osborne et al., 2016; Pallacks et al., 2023). While we agree that taphonomy is an important topic in the context of foraminiferal assemblages, we feel this may be outside the scope of a study of exclusively modern material. However, the important points raised highlight the need for greater clarity in our methods. Based on their sinking speed, foraminifera in Santa Barbara Basin likely reach the sediment trap in 1-4 days (Takashi and Be, 1984). The sediment trap sits below the sill of the basin in anoxic/hypoxic conditions, and contains a borate buffered formalin solution where pH > 8. Thus, foraminifera shells are interacting with ambient seawater for only days. It is unlikely that entire tests in the relevant size range are dissolving before reaching the sediment trap. We would also note that increasing dissolution as described would be more likely to skew assemblages to larger species, which is not what was observed.
We have clarified the post-mortem preservation of the tests in the methods section, “Particles were preserved in a borate-buffered formalin solution (pH >8) as they reached the sediment trap, preventing interaction with the surrounding seawater. After trap recovery, samples were split, with a 1/16th split used for foraminiferal flux and species counts, excluding July-October 2015 and May-November 2020.”
RC2: Further on taphonomy, some specimens in Figure A1 appear slightly etched. Could those be resuspended material in the traps? Were any benthic specimens observed? This is a usual phenomenon is some sediment traps.
The inconsistencies in color and texture in Figure A1 are not etching, but residual organic sediment trap material attached to the tests. This is common in sediment trap samples. We did find a small number of benthics (< 0.5%) but no evidence of any major resuspension events or landslides. Such events have been described in similar sediment traps and basins like the 2008 sediment density flow in Cariaco Basin (Lorenzoni et al., 2012) and there is no evidence of anything similar at our site. We will include these points in our revised results.
Minor
RC2: Methods: Please consider briefly explaining in the methods section what loadings and directions represent in Canonical Correlation Analysis to aid reader understanding.We have added an explanation of the CCA loadings and directions to the methods section.
“Canonical Correlation Analysis (CCA) provided further analysis of the relationships between species and environmental data and was conducted using the ‘vegan’ package in RStudio (Oksanen et al., 2024; Posit Team, 2024). CCA loadings are the correlations between the canonical variables and environmental or species variables. For example, if a variable has a positive loading, it has a positive correlation with the canonical variable (CCA1 or CCA2) and is positively associated with other variables that have positive loadings on the same canonical variable.”
RC2: Lines 65-69: Partly true. Thinning can also be due to adaptation. Results indicate that salinity significantly influences pteropod distribution (Johnson et al., 2023), while their biomineralization is affected by salinity due to its role in buoyancy regulation (Manno et al., 2012). Similarly, calcification changes for buoyancy regulation have also been suggested for foraminifera (Zarkogiannis et al., 2019).
We have clarified these lines to acknowledge the array of environmental factors that influence pteropod distribution and shell formation in addition to carbonate chemistry and agree that reduced calcification could be adaptive.
“In addition to a variety of other environmental parameters such as salinity, oxygen, and temperature, pteropods are impacted by changes in carbonate chemistry (Bednaršek et al., 2019; Johnson et al., 2023; Mekkes et al., 2021). Modern (2016) pteropods, for example, produce thinner aragonite shells in the more acidic, nearshore upwelling zones of the California coast compared to offshore, due to a decrease in calcification (Mekkes et al., 2021). Foraminifera also calcify thinner shells in response to ocean acidification (De Moel et al., 2009; Moy et al., 2009; Osborne et al., 2016; Pallacks et al., 2023).”
RC2: In a future submission please consider changing planktic to planktonic.
Both terms are widely used, and the meaning is clear in either case (Emiliani 1991).
References
Black, D. E., Thunell, R. C., and Tappa, E. J.: Planktonic foraminiferal response to the 1997-1998 El Niño: A sediment-trap record from the Santa Barbara Basin. Geology, 1075 pp., 2001.
Davis, C. V., Rivest, E. B., Hill, T. M., Gaylord, B., Russell, A. D., and Sanford, E.: Ocean acidification compromises a planktic calcifier with implications for global carbon cycling, Sci Rep, 7, https://doi.org/10.1038/s41598-017-01530-9, 2017.
De Moel, H., Ganssen, G. M., Peeters, F. J. C., Jung, S. J. A., Kroon, D., Brummer, G. J. A., and Zeebe, R. E.: Planktic foraminiferal shell thinning in the Arabian Sea due to anthropogenic ocean acidification?, Biogeosciences, 2009.
Dong S, Lei Y, Bi H, Xu K, Li T, Jian Z. Biological Response of Planktic Foraminifera to Decline in Seawater pH. Biology, 11(1):98, https://doi.org/10.3390/biology11010098, 2022.
Emiliani C. Planktic/planktonic, nektic/nektonic, benthic/benthonic. Journal of Paleontology, 65(2):329-329, doi:10.1017/S0022336000020576, 1991.
Kincaid, E., Thunell, R. C., Le, J., Lange, C. B., Weinheimer, A. L., and Reid, F. M. H.: Planktonic foraminiferal fluxes in the Santa Barbara Basin: response to seasonal and interannual hydrographic changes, Deep-Sea Research II, 47, 1157–1176, 2000.
Lorenzoni, L., Benitez-Nelson, C. R., Thunell, R. C., Hollander, D., Varela, R., Astor, Y., Audemard, F. A., and Muller-Karger, F. E.: Potential role of event-driven sediment transport on sediment accumulation in the Cariaco Basin, Venezuela, Mar Geol, 307–310, 105–110, https://doi.org/10.1016/j.margeo.2011.12.009, 2012.
Moy, A. D., Howard, W. R., Bray, S. G., and Trull, T. W.: Reduced calcification in modern Southern Ocean planktonic foraminifera, Nat Geosci, 2, 276–280, https://doi.org/10.1038/ngeo460, 2009.
Osborne, E. B., Thunell, R. C., Marshall, B. J., Holm, J. A., Tappa, E. J., Benitez-Nelson, C., Cai, W. J., and Chen, B.: Calcification of the planktonic foraminifera Globigerina bulloides and carbonate ion concentration: Results from the Santa Barbara Basin, Paleoceanography, 31, 1083–1102, https://doi.org/10.1002/2016PA002933, 2016.
Pallacks, S., Ziveri, P., Schiebel, R., Vonhof, H., Rae, J. W. B., Littley, E., Garcia-Orellana, J., Langer, G., Grelaud, M., and Martrat, B.: Anthropogenic acidification of surface waters drives decreased biogenic calcification in the Mediterranean Sea, Commun Earth Environ, 4, https://doi.org/10.1038/s43247-023-00947-7, 2023.
Takashi, K. and Be, A. W. H.: Planktonic foraminifera: factors controlling sinking speeds, Deep Sea Research, 1984.
Citation: https://doi.org/10.5194/egusphere-2024-3374-AC2
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AC2: 'Reply on RC2', Emily Havard, 12 Feb 2025
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