Article https://doi.org/10.1038/s41467-023-36177-w Pelagic calcium carbonate production and shallow dissolution in the North Pacific Ocean Received: 23 August 2020 Patrizia Ziveri 1,2,3,13 , William Robert Gray 4,5,13 , Griselda Anglada-Ortiz1,6, Clara Manno7, Michael Grelaud 1, Alessandro Incarbona 8, Accepted: 18 January 2023 James William Buchanan Rae 5, Adam V. Subhas9, Sven Pallacks 1, Angelicque White 10, Jess F. Adkins 11 & William Berelson12 Check for updates 1234567890():,; 1234567890():,; Planktonic calcifying organisms play a key role in regulating ocean carbonate chemistry and atmospheric CO2. Surprisingly, references to the absolute and relative contribution of these organisms to calcium carbonate production are lacking. Here we report quantification of pelagic calcium carbonate produc- tion in the North Pacific, providing new insights on the contribution of the three main planktonic calcifying groups. Our results show that coccolitho- phores dominate the living calcium carbonate (CaCO3) standing stock, with coccolithophore calcite comprising ~90% of total CaCO3 production, and pteropods and foraminifera playing a secondary role. We show that pelagic CaCO3 production is higher than the sinking flux of CaCO3 at 150 and 200 m at ocean stations ALOHA and PAPA, implying that a large portion of pelagic calcium carbonate is remineralised within the photic zone; this extensive shallow dissolution explains the apparent discrepancy between previous estimates of CaCO3 production derived from satellite observations/biogeo- chemical modeling versus estimates from shallow sediment traps. We suggest future changes in the CaCO3 cycle and its impact on atmospheric CO2 will largely depend on how the poorly-understood processes that determine whether CaCO3 is remineralised in the photic zone or exported to depth respond to anthropogenic warming and acidification. The marine calcium carbonate (CaCO3) cycle is a key component of the quantify total CaCO3 pelagic production10–12 and the contribution of global carbon cycle, and is intimately related to atmospheric CO2 specific calcifying plankton groups. However, the relative contribution (ref. 1). The formation of CaCO3 in the ocean is a process largely con- of the main calcifying taxa to total CaCO3 pelagic production has not trolled by the biological calcification of marine organisms2. Planktonic yet been directly quantified. calcifying organisms at the base of the food web (from primary pro- There is large uncertainty in total pelagic CaCO3 production, ducers to zooplankton) have played a key role since the Mesozoic3, via with current estimates varying between 0.7–4.7 Pg C yr−1 processes including regulation of surface water alkalinity, ballasting of (0.6−3.9×1014 mol CaCO3 yr−1)7,10–13. In general, estimates based on organic matter and alkalinity export, and establishment of a pelagic satellite observations or modeling of ecosystems/carbonate chem- carbonate buffer capable of influencing major CO2 change4–6. istry in the surface ocean suggest higher CaCO3 production10,12,13 Since the seminal work of Milliman7–9 on the production and whereas estimates based on export from the production layer typi- accumulation of CaCO3 in the ocean, several studies have aimed to cally report lower values7,8,11. A full list of affiliations appears at the end of the paper. e-mail: Patrizia.Ziveri@uab.cat; william.gray@lsce.ipsl.fr Nature Communications | (2023)14:805 1 Article https://doi.org/10.1038/s41467-023-36177-w There is also uncertainty on the make-up of pelagic CaCO3 pro- PIC August climatology mg m−3 duction by different groups. Mainly based on sediment trap export 60 100 fluxes and sediment data, there is a general understanding that coc- St.6.5 colithophores (single-celled haptophytes inhabiting the photic zone, 50 St.5 PAPA performing photosynthesis and producing calcite) and planktonic St.4.5 St.4 Lat (°N) foraminifera (single-celled marine eukaryotes producing calcite) each 40 St.3.5 contribute ~50% to the global pelagic CaCO3 production and St.3 10 St.2.5 30 sedimentation8,14–16. However, more recent papers have highlighted St.2 the potential of shelled pteropods (specialized free-swimming pelagic St.1 ALOHA 20 sea snails producing aragonite) as an important component of pelagic CaCO3 production13,17,18. Other taxa such as heteropods (holoplank- 10 1 tonic gastropods with aragonite shells, Pterotracheoidea) may also –180 –160 –140 –120 Lon (°E) contribute to a lesser degree. These planktonic calcifying taxa have specific mechanisms of Fig. 1 | Satellite PIC and location map. August satellite-derived Particular Inor- biogenic calcification, and associated differences in vulnerability to ganic Carbon97 (PIC; mg CaCO3 m-3) climatology (2002-2017) and location of C- ocean acidification19,20 with their shell solubility depending on their DisK-IV stations (black crosses) and long-term sediment trap studies (orange/pink specific polymorph mineralogy and Mg content21–23. In addition, crosses). Large black crosses show the location of Niskin bottle rosette, plankton planktonic calcifiers exhibit a large range of particulate inorganic tow, and floating sediment trap sampling sites at C-DisK-IV stations. Small black carbon to particulate organic carbon ratios (PIC/POC)18,24,25, which crosses show sites with additional plankton tow sampling only at C-DisK-IV stations. influences the integrated carbon export rain ratio, an important Note the logarithmic scale. term for carbon cycling in the oceans and atmospheric CO21,26. Furthermore, and as we discuss later, the association of PIC and POC together within calcifying organisms may play a critical role in Results and discussion driving CaCO3 dissolution above the saturation horizon27. However, North Pacific CaCO3 standing stocks despite the importance of pelagic calcification to the marine carbon The total CaCO3 standing stock is lower in the nutrient-poor and less cycle, key questions remain about pelagic CaCO3 production rates, productive subtropical gyre (~560–900 mg m-2; note here and standing stocks, and export fluxes. Most importantly, it is critical to throughout we refer to mg of CaCO3, unless specified otherwise), and determine the contributions of different planktonic calcifying strongly increases into the nutrient-rich and productive subpolar gyre groups to pelagic calcification, the proportion of aragonite versus (~1700–4500 mg m−2 total) (Figs. 2 and 3a, Table S3), reflecting the calcite, and the magnitude of CaCO3 production compared to major ecological shift across the North Pacific, from low-CaCO3 pro- export. duction in the oligotrophic subtropics, to high-CaCO3 production in The North Pacific Ocean is a key region for understanding the the subpolar region32,35. We find that coccolithophores dominate the role of pelagic calcifiers in the global CaCO3 budget, due to its large CaCO3 producing standing stock at all stations, demonstrating a mean volume and the wide range of biogeochemical conditions from contribution of ~79% (with a range of 62–96% across all sites) to the the subtropical to subpolar gyres. In addition, the waters of the total CaCO3 standing stocks. Pteropods contribute ~14% (3–29% North Pacific are some of the most undersaturated in the global range), followed by foraminifera (~6% mean, 0.1–22% range), and het- ocean with respect to calcite and aragonite, and thus calcifying eropods (~1%, 0–2%). Calcite from coccolithophores and foraminifera organisms in the region are most at risk of future ocean acidification is thus the most abundant mineral, constituting ~86% of the standing driven by anthropogenic CO2 emissions28,29. Although there are stock (71–96%), with aragonite making up ~14% of the standing studies of the relative distribution of pelagic calcifiers in the North stock (4–30%). Pacific30,31, estimates of their relative contribution to CaCO3 stand- The coccosphere CaCO3 standing stock depth profiles follow the ing stock and production rates are severely lacking. The discovery overall chlorophyll fluorescence, albeit with the scaling between of excess alkalinity above the saturation horizon in the North Pacific fluorescence and coccosphere CaCO3 varying between stations, (Fig. 2, has sparked debate about the role of different pelagic calcifiers and Fig. S1), indicating a substantial contribution by haptophytes/cocco- their contribution to the alkalinity budget above the thermo- lithophores to the total standing stock of photosynthetic algae dynamic saturation horizon23,32,33. production36. We observe a shallowing of the chlorophyll maximum We conducted a research cruise from subtropical to subpolar depth and coccolithophore CaCO3 standing stock maximum from North Pacific waters in which we assessed the pelagic living CaCO3 subtropical to subpolar stations (Fig. 2). standing stock. We targeted the main planktonic calcifiers at five Our estimates of living coccolithophore CaCO3 standing stocks survey stations, from Honolulu, Hawaii, to Seward, Alaska, (Fig. 1, range from 0.13 mg m-3 at 175 m (St. 1) in the subtropical gyre to Tables S1 and S2). We deployed plankton nets to sample calcifying 110 mg m-3 at 30 m (St. 5) in the subpolar gyre, with depth-integrated zooplankton and rosettes of Niskin bottles to target calcifying estimates from 753 mg m-2 to 3048 mg m-2 at the same stations, phytoplankton. In addition, four intermediate planktonic towing respectively (Fig. 2b, c, Tables S2 and S3). Our results support previous stations were sampled and integrated into the overall data set work in the North Pacific based on coccolithophore cell concentration, (Fig. 1, Tables S1, S2). Coccolithophores, foraminifera, pteropods, which showed that their biomass is highest at high latitudes, and heteropods were quantified and the CaCO3 biomass was esti- decreasing in temperate and subtropical regions30 (Fig. S8). The sub- mated, providing the first overall picture of the total CaCO3 living polar and transitional North Pacific Ocean is also known as a region of standing stock (i.e. inventory), and the relative contribution of sustained seasonal E. huxleyi (the most abundant and cosmopolitan the main calcite and aragonite planktonic producers in the pro- coccolithophore species) blooms37 with an estimated maximum ductive upper ocean. Using estimates of turnover time for each satellite-derived PIC concentration of ~0.8 mmol m−3 (CaCO3 of group we estimate annual production (Methods), and compare this 80 mg m-3) in August/September (note, satellite PIC is limited to to aragonite and calcite biomineral export out of the surface ocean retrievals over the first optical depth of satellite data, ~10 m). There is a to 100 and 200 m water depth estimated using floating sediment remarkable agreement between our estimated values of coccolitho- traps deployed during the time of sampling34 and historical time phore CaCO3 from the shallowest sampled water depth (~5 m, i.e. the series in the region. surface CaCO3 concentration) and satellite-derived PIC concentrations Nature Communications | (2023)14:805 2 Article https://doi.org/10.1038/s41467-023-36177-w Fluorescence (mg/m3) CaCO3 (mg m3) CaCO3 (mg m3) Omega 0.0 1.0 2.0 3.0 0 5 10 15 0 20 40 60 80 100 0 1 2 3 4 5 6 0 a b c d 50 100 Depth (m) 150 transition zone/ subtropical gyre subpolar gyre 200 St.1 St.2 250 St.3 St.4 coccospheres St.5 coccoliths 300 calcite 0.00 0.05 0.10 0.15 0.0 0.4 0.8 1.2 aragonite (mmol m ) 3 (mmol m ) 3 Fig. 2 | Coccolithophore standing stock vertical profiles. a chlorophyll fluorescence. Coccosphere, and coccolith CaCO3 from C-DisK-IV stations (b) 1 and 2 and, (c) 3, 4, and 5. Note the different x axis range on panels (b) and (c). d Omega calcite and aragonite at the five stations. (Figs. S2 and S3), which are mostly tuned to capture coccolithophore Our pteropod CaCO3 concentrations range from 0.2–8.6 mg m-3 PIC. This supports the high correlation between satellite-derived PIC (Fig. 3a). We find good agreement between our estimates of pteropod and measured PIC surface water concentrations suggested by Balch CaCO3 standing and North Pacific sites in the MAREDAT database17 and others;10,38 however as previously noted38 and discussed later, (Methods; Fig. 3), which show a typical concentration of 0.5 (0.2–1.1, much of the coccolith PIC production can occur below the depth of the 68% CI) mg m-3. Despite our pteropod CaCO3 standing stock results optical retrieval, particularly in the subtropics where the production being similar to/higher than previous estimates from the North Pacific/ layer deepens. North Atlantic, our values are lower than the proposed 23.17 mg CaCO3 We also quantify the CaCO3 contribution of loose coccoliths m-3 global-mean value of shelled pteropod CaCO3 standing stock (calcite plates extruded to the cell surface forming the coccosphere; concentration18. However, our analysis shows that this global dataset is Fig. 2b; Table S5). Coccoliths are shed into the surrounding waters heavily skewed (Skewness = 13.3, where a value above one indicates a following death and breakup of the coccosphere, or produced con- skewed dataset), with the median pteropod biomass value reported18 tinuously by some species38–40. We found that loose coccolith CaCO3 being around three orders of magnitude smaller than the reported can contribute significantly to the total CaCO3 standing stock in the mean. As such the global-mean value is not a useful descriptor of this productive photic layer, with maximum values of 44 and 64 mg m-3 in data compilation18. Our analysis shows typical pteropod CaCO3 bio- E. huxleyi blooms at Stations 3 and 5 (Fig. S3). Our results show loose mass globally is 0.3 (0.08–0.9, 68% CI) mg m-3 in the upper 250 m and coccolith distribution is tied to the distribution of intact coccospheres 0.2 (0.07–0.8, 68% CI) mg m-3 in the upper 1000 m (Methods; Sup- and PIC, as observed in previous studies10,38. We note that our cocco- plemental Fig. S6), two orders of magnitude lower than the global- lithophore living standing stock estimates (used to calculate CaCO3 mean value reported by ref. 18, and in line with our results from the production rate) only include whole coccosphere cells, and excludes North Pacific. loose coccoliths. Our vertically integrated pteropod CaCO3 standing stocks range Our pteropod standing stock concentrations in the subpolar gyre between ~64–111 mg m-2 in subtropical gyre and between range from 109–802 ind. m-3, broadly within the published range of the ~215–1306 mg CaCO3 m-2 in the subpolar gyre (Fig. 3; Table S3; Fig. S5). pteropod standing stocks in the northwestern Pacific (e.g.; 41,42, Fig. 3; We find good agreement between our estimates and the vertically Table S3; Fig. S5) and the Gulf of Alaska43,44, although pteropods show a integrated pteropod CaCO3 standing stock calculated from North significant seasonal and inter-annual variability in the coastal habitats Pacific sites in the MAREDAT database17 (Methods; Fig. 4), which show of the Gulf of Alaska43,44. The recent study of Bednaršek et al.45 found a typical value of 121 (50–270, 68%) mg m-2, with our estimates thus that the abundance of pteropods collected in May 2015 in the subpolar being slightly higher. gyre and Gulf of Alaska was (42–423 ind m-2), around two orders of Our heteropod standing stock concentrations range from 5–40 magnitude lower than our abundances observed in August 2017 in the ind. m-3 and 0.01–0.1 mg CaCO3 m-3, and their presence is limited to same region (Stations 4–6, Table S3) and previous studies43. This dif- the subtropics and transition zone. Although previous estimates of ference in abundance may relate to seasonal and inter-annual varia- heteropod standing stocks are extremely scarce, comparison to bility in this region, and/or the use of larger mesh size in their study previous abundances from a latitudinal Atlantic Ocean transect (200–335 µm)45, which could have resulted in an underrepresentation confirmed that heteropods almost exclusively inhabit warm waters of the small size pteropod (juvenile) fraction. Our estimates from the and the recorded maximum of 0.7 ind. m-3 (ref. 46) is lower than our subtropical gyre (22–391 ind. m-3) (Table S3) are similar to previous estimates in the North Pacific. Our vertically integrated heteropod estimates for this region and are higher than values observed across CaCO3 standing stocks range from 3-35 mg CaCO3 m-2; heteropods the Atlantic Ocean46. thus contribute between 3–12% of the total aragonite standing stock Nature Communications | (2023)14:805 3 Article https://doi.org/10.1038/s41467-023-36177-w STG TZ SPG CaCO3 standing stock (mg m2) 5000 a 50 30 b ptero hetero 25 turnover time (days) 4000 foram 40 m2 ) cocco 20 3000 total 30 15 (mmol 2000 20 10 1000 10 5 0 0 0 ro o o m 1 2 3 4 5 cc er te ra co pt he fo station annual CaCO3 production (mol m2 yr) daily CaCO3 production (mg m2 day) STG TZ SPG STG TZ SPG 3500 August c 35 5 seasonally d 3000 2017 30 adjusted 4 m2 day) 2500 25 2000 20 3 1500 15 (mmol 2 1000 10 1 500 5 0 0 0 1 2 3 4 5 1 2 3 4 5 station station Fig. 3 | Standing stock and production by pelagic calcifiers. a living CaCO3 estimate. Error bars for the standing stock (a) and production (c, d) by individual standing stock b turnover time of calcifying taxa used to calculate production from taxon represent the 95% CI (Methods). STG, TZ, and SPG represent subtropical standing stock (the range represented by the bar length is applied with a flat gyre, transition zone, and subpolar gyre, respectively. Purple bands on panels probability distribution in our error propagation) c CaCO3 production per day a, c, and d show 68% range of pteropod standing stock and daily/annual production (August 2017) d CaCO3 annual production corrected for seasonal bias using calculated using the MAREDAT database (Methods). The blue stars on panel d show satellite-derived PIC/chlorophyll97,104 and zooplankton seasonality estimates (all the estimates of total production calculated with in-situ pH and fCO2 measure- data and metadata are publicly available at hahana.soest.hawaii.edu/hot/hot-dogs/ ments at Ocean Station PAPA (ref. 57, light blue), and estimates of production in the interface.html). The total CaCO3 production is shown by the violin plots in panels subpolar North Pacific calculated using the seasonal cycle of alkalinity and dis- (c) and (d), where the probability density of the estimate is represented by the solved inorganic carbon (ref. 12, dark blue). STG, TZ, and SPG represent subtropical thickness of the shaded area and the grey lines show the 68% and 95% confidence gyre, transition zone, and subpolar gyre, respectively. interval (CI); note the non-normal distribution with the high-tail on the upper in the subtropics and transition zone, but are absent from the sub- relatively quickly after death47,49, and the individuals sampled con- polar region. tained cytoplasm/soft tissue (Methods). For coccolithophores this Our estimates of integrated foraminiferal CaCO3 standing stock assumption is valid as we only consider intact coccospheres, which range from 9–37 mg m-2 in the subtropical gyre to 182–404 mg m-2 in disaggregate quickly upon death into the component coccoliths50, and the subpolar gyre. Although previous estimates of foraminiferal is supported by the fact that the peaks of coccolithophore CaCO3 standing stock in the North Pacific are scarce, our estimates of the match the peaks in chlorophyll fluorescence (Fig. 2). We include the integrated vertical standing stock of the number of foraminifera from caveat that our approach assumes the living standing stock is in the subtropical gyre/transition zone sites are similar to, or slightly approximate steady state. higher, than previous estimates of the integrated vertical standing Given that coccolithophores have a shorter turnover time stock from the subtropical gyre/transition zone in the western North (1.5–10 days) than the other calcifying groups (Methods, Pacific31,47 (Figs. S4, 5). Our estimates of the vertically integrated Table 1, Fig. 3b) and dominate the CaCO3 standing stock, they account standing stock of the number of foraminifera in the subpolar North for ~86% (67–97%) of total CaCO3 annual production across the sites. Pacific (190,000–250,000 ind. m-2) are generally higher than the esti- Pteropods contribute ~10% to total production (2–17%), heteropods mates of Taylor et al.31, which ranged up to ~80,000 ind. m-2, although ~0.3% (0–1%), and foraminifera contribute ~2% (0.02–9%). As such, 89% such high values are not unprecedented, with previous estimates of of the CaCO3 production is calcite (70–97%), with the remainder being the vertically integrated standing stock from the North Atlantic ran- aragonite (Fig. 3c). ging up to ~390,000 ind. m-2 ref. 48. Given the large seasonality of PIC production51,52 (Fig. S7), we estimate annual CaCO3 production correcting for seasonal bias Pelagic CaCO3 production (Methods, Table S6). Our seasonally corrected annual CaCO3 produc- We calculate CaCO3 production rate by dividing our measurements of tion estimates range from 0.2–0.4 mol m-2 yr-1 in the subtropical gyre, a the living CaCO3 standing stock by estimates of the turnover time (i.e. similar range or slightly lower than the estimate of the production rate typical life span) of each group (Methods, Fig. 3b). Our approach of 0.7 mol m-2 yr-1 in the subtropical/tropical Atlantic53, although in assumes all of the organisms within the standing stock are living; this is good agreement with the global mean estimate of 0.4 mol m-2 yr-1 valid for foraminifera, pteropods, and heteropods as individuals sink (ref. 10, Fig. 3d). Our estimates from the transition zone and the Nature Communications | (2023)14:805 4 Article https://doi.org/10.1038/s41467-023-36177-w a Pteropods 0 - 250 m CaCO3 biomass 0.02 2.0 (mmol/m3) 1.5 (mg/m3) 0.01 1.0 0.5 0.00 0.0 MAREDAT CDisk-4 0.30 0.30 probability density (frac. tot.) probability density (frac. tot.) P 32 P 50 P 68 P max P 32 P 50 P 68 P max 0.25 0.09 0.22 0.49 0.03 0.25 0.19 0.47 1.05 0.19 0.20 0.20 0.15 0.15 0.10 0.10 0.05 0.05 b c 0.00 0.00 0 1 2 3 4 5 0 2 4 6 8 10 C biomass (mg/m3) CaCO3 biomass (mg/m3) 0 0.2 0.4 0.6 0.8 0.1 (mmol/m3) 0.30 0.5 probability density (frac. tot.) probability density (frac. tot.) P 32 P 50 P 68 P max P 32 P 50 P 68 P max 0.25 49 117 262 48 5 12 26 4 0.4 0.20 0.3 0.15 0.2 0.10 0.05 0.1 d e 0.00 0.0 0 200 600 1000 0 50 100 200 integrated CaCO3 standing stock (mg/m2) daily CaCO3 production (mg/m2/day) 0 2 4 6 8 10 0 1 2 (mmol/m2) (mmol/m2/day) Fig. 4 | Pteropod CaCO3 biomass estimates. a Pteropod CaCO3 biomass estimated comprehensive MAREDAT database17,18 (Methods). Red shading indicates 32–68% from the MAREDAT database17 and measured in this study; note, maximum values confidence interval range. Red values show the 32nd, 50th, 68th percentiles; extend above 2 mg m-3. Probability density of pteropod (b) Carbon biomass (c) orange value shows the value with the highest probability (all values given in mg). CaCO3 biomass (d) Integrated CaCO3 standing stock (e) daily CaCO3 production Note the distributions are highly skewed. calculated using samples in the upper 250 m of the North Pacific from the productive subpolar gyre are higher (0.9–1.0 mol m-2 yr-1) than production in the subtropics, as well as the thickness of the cocco- this global average even at the 95% confidence interval (Fig. 3d); lithophore productive layer (Fig. 2) from the upper ~175 m in the however, they agree well with the estimate of production calculated subtropics to the upper ~75 m in subpolar region, which will bias the with in-situ pH and fCO2 measurements at Ocean Station PAPA satellite-derived PIC estimates to lower values38. For Stations through (1.2 mol m−2 yr-1; ref. 54), and estimates of production in the 1–4 surface PIC is below 10 mg m- 3 (both at the time of sampling and subpolar North Pacific calculated using the seasonal cycle of alkalinity in the annual mean climatology), yet we observe a depth integrated and dissolved inorganic carbon (0.9 ± 0.1 mol m-2 yr-1; ref. 12). seasonally corrected production of 0.2–1 mol m-2 yr-1 at these sites To explore the implications of our estimates of CaCO3 produc- (Table S6). Note, this surface PIC value is very similar to the threshold tion for global production, we use a global climatology of satellite- proposed by Balch et al.38 (0.13 mmol m-3/ 13 mg m-3) between derived PIC (Fig. S7). While there is a high correlation between surface-dominated and depth-dominated CaCO3 production satellite PIC and our estimates of surface PIC concentration (Fig. S2a; regimes. Similar low surface PIC regimes (with annual surface PIC of ref. 38), our results indicate depth integrated CaCO3 production is <10 mg m-3) represent 87% of the surface of the ocean (Fig. S8); thus, only twice as high in the nutrient-rich subpolar gyre than the assuming similar rates of CaCO3 production as the seasonally cor- nutrient-poor subtropical gyre, smaller than the range expected from rected production rates at Stations 1–4 globally puts a minimum the satellite PIC (CaCO3) estimates, which suggest PIC concentrations estimate (assuming the remaining 13% of the ocean with higher sur- ~6–7 times higher in the subpolar region compared to the subtropics. face PIC will have higher depth integrated production) for total This difference likely reflects the deeper (coccolithophore) CaCO3 global CaCO3 production of ~2.2×1014 mol yr-1 (2.6 Pg C yr-1), that is Nature Communications | (2023)14:805 5 Article https://doi.org/10.1038/s41467-023-36177-w Table 1 | Ratio of Particular Inorganic carbon (PIC) to Particular Organic Carbon (POC) and turnover time (life span) for the calcifying taxon Group PIC:POC ratio PIC:POC references Turnover time (days) Turnover time references Coccolithophores 0.19–2.08a ref. 98 and references therein 0.6–10 days (0.1–1.5 cell divisions per day) ref. 59 and references therein Pteropods 0.20–0.56b ref. 18,99 5–16 ref. 13,58,100 Heteropods 0.28–0.45 This study 5–16 ref. 13,58,100 101 102,103 c Planktonic foraminifera 3–6 ref. and references therein; ref. 14–28 ref. 78 and references therein a C. leptoporus, E. huxleyi, C. pelagicus subsp. braarudii, G. oceanica, S. apsteinii, H. carteri, S. pulchra, U. sibogae. b Limaciniidae and Cavoliniidae families. c excludes deeper dwelling species with longer turnover times, however, these comprise only a very minor component of the assemblages30,31. 0.8×1014 mol yr-1 using the production rate at Station 1 and 3.6×1014 review by Gafar et al.25 which ranged from 0.19 to 2.30 and much lower mol yr-1 using the production rate at Station 3. than the value 0.52 they used for pteropods, which is itself about two To make a first-order approximation of the impact of deepening times higher than the estimates of Bednaršek et al.18 (Table 1). Sec- CaCO3 production on global CaCO3 production we use a simple lin- ondly, they assume a similar turnover time for (single-celled) cocco- ear regression of total CaCO3 production at our sites against satellite lithophores and (complex) pteropods, contrary to the available PIC (CaCO3) (Fig. S2), with the deepening of production primarily estimates from the literature57–60 (Table 1). Finally, within their calcu- manifesting as a non-zero intercept (note the high variability in the lation they assume all CaCO3 dissolving above the calcite saturation intercept coming from the changing production regimes from Sta- horizon is aragonite, an assumption which is likely to exaggerate ara- tions 1 to 4 despite the low surface PIC at all Stations). We then apply gonite production; as we discuss below, previous studies52,61,27 and our this relationship to global satellite PIC climatology (Fig. S8). We results indicate substantial dissolution of coccolithophore calcite include the caveat that 1) this assumes the bias caused by the dee- above the calcite saturation horizon (which we attribute to respiration- pening of CaCO3 production in the subtropics scales with surface PIC driven dissolution and dissolution within the guts of grazers) such that in a similar way globally38, and 2) the regression in Fig. S2 is driven by this assumption is likely to be invalid. one station with high surface PIC (Station 5). While crude, this approach allows us to make a first-order approximation of the impact CaCO3 sinking and export fluxes versus production of deepening CaCO3 production on global CaCO3 production. Our estimate of 3.1×1014 mol CaCO3 yr-1 global pelagic CaCO3 produc- Applying the relationship between total production and satellite PIC tion is ~30 – 300 times larger than required to meet the 0.8 1012 - (Table S7) to the global mean surface satellite-derived PIC climatol- 1.1×1013mol CaCO3 buried in deep sea sediments each year8,11,62–64 and ogy (Fig. S8), and integrating globally (weighting by area) results in a balance the riverine of input of alkalinity to maintain steady-state, total CaCO3 production of 3.1×1014 mol yr-1 (3.7 Pg C yr-1) globally. This reaffirming previous findings that most of the CaCO3 produced in the estimate is similar to, although toward the upper end, of previous surface ocean is dissolved and recycled within the ocean interior (e.g., estimates of total pelagic calcification based on satellites, upper ref. 8). More surprisingly, at several stations our estimates of CaCO3 water column measurements, seasonal alkalinity changes, and eco- production are larger than the export fluxes at 100 to 200 m water system modeling which range from 0.9–3.9×1014 mol CaCO3 yr-1 depth in floating sediment trap deployed during the plankton (1.1–4.7 Pg C yr-1)10,12,13,28,32,55. However, as previously noted by sampling34, and our production estimates at Stations 1 and 5 are higher others10,13 this estimate is considerably higher than estimates of glo- than the long running shallow sediment traps at Station ALOHA65 and bal mean CaCO3 export flux from the upper ocean which ranges from Ocean Station PAPA64,66,67) (Fig. 5). While the discrepancy observed 0.5–0.6×1014 mol yr-1 (0.6–0.7 Pg C yr-1; refs. 7,8). with the floating traps deployed during the sampling interval (in place While our estimate of the total amount of CaCO3 produced agrees for ~72 hrs) may be explained by a decoupling of CaCO3 production well with that of Buitenhuis et al.13, there is a large discrepancy between and natural mortality/sinking of pteropods, and coccolith aggregation, our results and those of Buitenhuis et al.13 in terms of the dominant such that there could be a time lag between production at the surface CaCO3 polymorph produced. We find CaCO3 production is dominated and export through the water column, this time lag cannot explain the by calcitic coccolithophores, however, their results suggested pelagic discrepancy observed with the long running sediment traps at Ocean CaCO3 production is mainly driven by aragonite pteropods with coc- Station PAPA and Station ALOHA. Our results show an annual pro- colithophores and foraminifera playing a minor role. duction of 0.4 (0.2-2.1, 95% CI) and 0.9 (0.5-3.8) mol CaCO3 m-2 yr-1 at Given the discrepancy with the results of Buitenhuis et al.13 and the Stations 1 and 5, which is ~5 times higher than the annual export of 0.08 limited temporal interval of our sampling and the potential for and 0.16 mol CaCO3 m-2 yr-1 at 150 m depth at ALOHA and 200 m at large temporal variability of pteropod abundances43, we also calculate PAPA (Fig. 5c, d). We reiterate that previous estimates of annual CaCO3 pteropod CaCO3 biomass and production in the North Pacific using the production at PAPA station based on seasonal cycle of seawater car- comprehensive MAREDAT database18, which has excellent spatial and bonate chemistry support our production value12,54,57. seasonal sampling distribution in the North Pacific (Methods, Fig. 4). This disparity between the amount of CaCO3 produced, and the This results in a typical pteropod CaCO3 biomass in the upper 250 m of amount of CaCO3 that is exported out of the photic zone, suggests that the North Pacific of 0.5 mg m-3 (0.2–1, 32–68% CI; note the dataset is a large portion (~80%) of the total CaCO3 produced in the photic zone highly skewed, Fig. S6), a vertically integrated pteropod CaCO3 bio- is never exported, and is instead remineralised in situ; that is, only mass of 122 mg m-2 (50–269, 32–68% CI), and a pteropod CaCO3 pro- ~20% of the total CaCO3 produced is exported from the photic zone. duction rate of 12 mg m-2 day-1 (5–27, 32–68% CI). The results calculated Bishop & Wood52 suggested up to 92% of the total CaCO3 produced using the MAREDAT database are thus in good agreement with the dissolved within the upper 500 m in the subpolar North Pacific. In situ estimates calculated using the samples collected during our own remineralisation of such a high fraction of the CaCO3 that is produced cruise (Fig. 3). We propose the discrepancy with the results of Bui- within the photic zone explains the previous discrepancy between tenhuis et al.13 instead comes from three other factors: Firstly, their higher estimates of global CaCO3 production based on satellites, upper model parametrization uses a fixed PIC/POC ratio of 0.1 ref. 56 for water column measurements, seasonal alkalinity changes, and eco- coccolithophores; this value is substantially lower than the published system modeling (which all estimate the total amount of CaCO3 Nature Communications | (2023)14:805 6 Article https://doi.org/10.1038/s41467-023-36177-w Fig. 5 | Pelagic CaCO3 production versus sinking fluxes. a total CaCO3 production dashed line shows the depth of aragonite saturation horizon (calculated from versus sinking flux in the floating traps deployed at 100 m and 200 m during the GLODAPv2105 and orange dotted line shows depth of deepest floating trap. Pro- plankton sampling at all stations (PIC concentrations not available at 200 m depth duction in all panels is produced during the time of sampling (August 2017) i.e. it is for stations 1 and 3)34 b Station 1/ALOHA 65 c Station 5/PAPA;64 turquoise star not corrected for seasonal bias. Error bars for the total production (a, b, c) and represents production estimate at PAPA from ref. 54 based on the seasonally cycle of fraction aragonite of production (d) represent the 95% CI (Methods) See legend in in-situ pH and fCO2 d fraction aragonite in production and sinking flux in the panel a for square symbols in panels (c, d, e). STG, TZ, and SPG represent sub- floating traps deployed during the plankton sampling as a function of latitude; red tropical gyre, transition zone, and subpolar gyre, respectively. produced)10,13,28 and lower estimates of CaCO3 based on export pro- from the inside out (as well as making them a more attractive food duction (such as sediment traps below the photic zone)7,8. source to grazers). Although the degree to which this could drive total Shallow remineralisation of pteropods is suggested by the frac- dissolution of whole pteropod shells is still uncertain70, widespread tion of aragonite present in the shallow traps versus the production dissolution of coccolithophore CaCO3 within the upper water column ratio, with the fraction of aragonite in the shallow traps decreasing has been observed during bloom events (e.g., ref. 71). Furthermore, northwards as the aragonite saturation horizon shoals, while the coccolithophores (which constitute by far the largest fraction of fraction produced increases (Fig. 4e); the highest fraction aragonite CaCO3 produced) disintegrate into individual coccoliths after death produced is at Station 5, where we also observe the lowest fraction in (this can be seen in the coccolith standing stocks in Fig. 2), and must the shallow traps, and the aragonite saturation horizon shoals to above sink by forming aggregates (e.g. marine snow). In situ micro-electrode the depth of the shallow trap (<200 m). This dissolution pattern in measurements demonstrate a large pH drop with marine-snow during living pteropod communities in the Gulf of Alaska has been observed respiration72, which would drive further micro-environmental under- recently by Bednaršek et al.45 However, our results indicate that not saturation and CaCO3 dissolution27. In addition, shallow sediment traps only aragonitic pteropod and heteropods dissolve13, but also a large indicate coupling of PIC and POC remineralisation from 100 m to amount of coccolithophore calcite. Our findings thus require CaCO3 200 m depth in the North Pacific34. dissolution above the calcite/aragonite saturation horizon throughout Although the processes by which coccolithophore CaCO3 dis- the North Pacific27. Tracers of excess alkalinity support widespread solves in supersaturated waters remain uncertain, some insight may be shallow dissolution, far above the calcite and aragonite saturation gained from the residence time of loose coccolith CaCO3 within the horizons, throughout the global ocean23,27. production layer; dividing the loose coccolith CaCO3 standing stocks The large amount of CaCO3 dissolution above the calcite/arago- (Fig. 2) by the estimated whole coccosphere CaCO3 production rate at nite saturation horizon may be driven by multiple mechanisms, each station gives an approximate coccolith CaCO3 residence time on including localized undersaturation within the microenvironment the order of several days to a couple of weeks. Given the requirement driven by the remineralisation of organic matter, as well as dissolution of coccoliths to sink by aggregation and fecal pellets73, the export and within the guts of grazers and predators23,33,45,68,69. Both pteropods and dissolution of coccolithophore calcite may occur in discrete events, coccolithophores contain a large fraction of organic carbon (Table 1), possibly associated with episodes of high organic carbon production the respiration of which after their death can promote dissolution and grazing, rather than sinking as a steady rain, in agreement with Nature Communications | (2023)14:805 7 Article https://doi.org/10.1038/s41467-023-36177-w previous suggestions based on seasonal export production in sedi- through the water column. The maximum depth was determined from ment trap studies (e.g., refs. 4,50). While our results suggest that a large the fluorescence profile of the preceding CTD cast, and was selected to portion of coccolithophore CaCO3 is remineralised in the photic zone, ensure the net sampling captured well below the base of the chlor- the very high rate of production means a substantial amount is still ophyll maximum and ranged from 150 m in the most northerly sub- exported4,5, and incorporated within sediments14. polar sites to 300 m in the subtropical region (Tables S1, S2). The Foraminifera comprise ~20% of the total CaCO3 flux in a sediment volume of water represented by each net tow sample was calculated by trap at 3800 m at Station PAPA;74 however, our results show they multiplying the net area by the distance traveled as determined by a consist of only ~4% of the total annual CaCO3 standing stock, and ~1% of flowmeter. For the vertically integrated values, the integration is car- the total annual CaCO3 production at Station 5. Due to their mass and ried out from the surface to the maximum depth of the tow. low organic carbon content24,75 (Table 1), foraminifera sink quickly After collection, samples were preserved in a 4% formalin seawater after death50, have a low self-dissolution potential, and are thus effi- solution, buffered to a pH of ~8.1 with hexamethylenetetramine73. cient exporters of CaCO3 out of the photic zone. Thunell & Honjo74 Samples were split with a Folsom splitter or a McLane rotary splitter found the August flux of foraminiferal calcite in a sediment trap at (splitting error <4%). Large pteropods and heteropods (>1 mm) were 3800 m at Station PAPA ranged from 2−6 mg m-2 day-1. Our for- picked and quantified before splitting. Half of the split sample was aminiferal calcite production estimate at Station 5 is 9 mg m-2 day-1, transferred into ethanol solution in the laboratory for the analysis of suggesting foraminiferal calcite is efficiently exported into the deep pteropods and heteropods. ocean. Foraminifera thus play an important role in CaCO3 export and Water samples from rosettes of Niskin bottles equipped with CTD sedimentation, despite their low contribution to total production; (Sea-Bird SBE 9) were collected at different depths throughout the estimates of CaCO3 in sediments suggest a ~50/50 ratio of cocco- photic zone and including the chlorophyll maximum depth. lithophores/foraminifera13 versus the ~90/2 production ratio we observe. Quantification of calcifying plankton community standing stock While much attention has been given to decreasing calcification and biomass under ocean acidification19,76 our results indicate a decoupling of All foraminifera were wet picked from the sample splits, divided into CaCO3 production and export (Fig. 5). As such, future changes in the groups greater and less than 125 µm, counted, and weighed with a high processes driving shallow dissolution, and the ability to export CaCO3 precision microbalance. We assume the mass of organic matter is out of the photic zone may play an equally important role in deter- negligible since dry cytoplasm has no statistically significant effect on mining the future response of the CaCO3 cycle and its effects on the the weight of tests > 150 μm24,75. Empty tests made up a negligible marine carbon cycle under anthropogenic climate change. Changes in component of the standing stock, typically comprising <2% of the total grazing, particle aggregation, the PIC/POC ratio of the aggregates, or standing stock. Replicate picking and weighing of splits gave a typical the relative abundance of foraminifera to coccolithophores/pter- reproducibility of ±4% (1σ). Foraminiferal assemblages from these opods, could lead to large changes in the amount of CaCO3 exported samples were previously reported31. from the surface ocean and thus the cycle of alkalinity. The PIC/POC Pteropods and heteropods were quantified and shell diameter ratio of coccolithophores has been demonstrated to decrease with was measured using a Leica Z16 AP0 binocular light microscope at increasing CO2 (ref. 25); if the dissolution of coccolithophore CaCO3 20−100×. Pteropods and heteropods were identified and grouped within the photic zone is in part related to the degree of calcification respectively in three (Cavoliniidae, Cymbuliidae, Limacinidae) and two and/or the remineralisation of organic carbon contained within the (Atlantidae, Carinidae) families. soft tissue of the calcifying organisms, this decrease in the PIC/POC of CaCO3 biomass (B) was estimated as follows: CaCO3 (mg) = PIC coccolithophores may lead to a negative feedback with CO2, with (mg) ×8.33 (assuming that all inorganic carbon is in the form of increased dissolution (and thus reduced export of alkalinity) out of the CaCO3), where the constant 8.33 represents the molecular mass ratio surface ocean acting to buffer rising atmospheric CO2. Given the of carbon to CaCO3 and PIC is the Particulate Inorganic Carbon79. To potential importance of CaCO3 export in driving changes in alkalinity estimate PIC we used the PIC/POC ratio of 0.27:0.73 calculated on and atmospheric CO2, and the large uncertainties in our current pteropods by Bednaršek et al.18, where POC is the Particulate Organic understanding, future work should focus on understanding the pro- Carbon (POC) representing the soft tissue of the organisms. POC was cesses by which CaCO3 is either dissolved within the photic zone or estimated by converting Wet Weight (WW, mg) to Dry Weight (DW, exported to depth. mg) using80 equation DW = WW × 0.28. DW was subsequently trans- formed to POC using the conversion factor POC = DW × 0.25 Methods following81. WW and/or DW were calculated from the shell length Sample collection (L, mm) using equations based on the different shell shape: ref. 80,82,83. Samples were collected along a transect from Hawaii to Alaska during August 2017 as part of the CDisK-IV (KM1712) cruise on R/V Kilo Moana Cavoliniidae, WW = 0:2152 × L2:293 , ð1Þ (Fig. 1). The five stations along the transect were designed to sample subtropical, transition zone, and subpolar waters. A rosette of Niskin bottles equipped with CTD (conductivity, temperature, depth) and Carinidae, WW = 0:0888 × L2:161 , ð2Þ other sensors for coccolithophore and biogeochemical parameters and a vertically integrated plankton tow were collected at each station. Further plankton tows were conducted at four additional intermediate Limacinidae, DW = 0:1365 × L1:501 , ð3Þ stations (Supplementary material). A 0.5 m diameter net with 90 µm mesh size was used throughout; For Cymbulidae, we generated the following equation DW = based on previous work this mesh size should provide a good estimate (0.0392 × L)−0.003 from the measurement of shell (mm) and DW of of both pteropod18,77 and foraminiferal78 biomass. The sampling strat- 67 individuals. egy was designed to capture an integrated sample of all foraminifera, For Atlantidae we generated the following equation pteropods, and heteropods from juveniles to adults living throughout CaCO3 = 0.769e0,0023L (R2 = 0.885) from the measurement of shell the upper water column. The net was towed from the surface down to a length (mm) and CaCO3 biomass (mg) of 85 individuals. For the mea- specified maximum depth within the water column, and then back to surement of CaCO3 biomass heteropods were heated to 550 °C for 5 h the surface in a continuous manner following an oblique trajectory to eliminate organic matter content and the ashes (representing the Nature Communications | (2023)14:805 8 Article https://doi.org/10.1038/s41467-023-36177-w remains of the shells) weighed using a Toledo microbalance. The ash production using a flat probability distribution i.e. for foraminifera weight can be considered an indirect estimate of CaCO3 content84. there is equal chance of the average lifespan being 10 days as it is Between 2.1 and 6.0 liters of seawater were filtered onto Millipore 30 days (this highly conservative approach thus results in larger total cellulose acetate membranes, with 0.45 µm of pore size and 47 mm of uncertainties in production rate). The production (mg m-2 day-1) is then diameter, for coccolithophore analysis. Filters were oven dried at given as the CaCO3 standing stock (in mg m-2) divided by the turnover 40 °C and stored in plastic petri dishes. A portion of each filter was time (days), mounted on a glass slide and analyzed by a polarized LEICA DM6000 1 light microscope at 1000× magnification along radial transects whose CaCO3 production ðmg m2 day Þ area was between 0.35 and 3.14 mm2. Cell concentrations per liter of ð5Þ = CaCO3 standing stockðmg m2 Þ=turnover timeðdaysÞ seawater were estimated as follows: Our approach assumes that all of the organisms we sampled are Coccolithophore concentration ðnumber=LÞ = ðF × CÞ=ðA × VÞ ð4Þ living. This assumption is valid for foraminifera and pteropods as they sink individually, and relatively quickly upon death. For coccolitho- where F is the effective filtration area (mm2), C is the number of coc- phores this assumption is valid as we only consider intact cocco- cospheres, V is the filtered seawater volume (L) and A is the investi- spheres, which mostly disaggregate quickly upon death. Annual gated filter area (mm2). estimates were then calculated by multiplying the daily estimates by Taxa were identified following taxonomic concepts for living 365 accounting for the seasonal bias at the time of sampling using PIC/ coccolithophores by ref. 85,86. To estimate the CaCO3 contribution by chlorophyll_a/zooplankton time series (see below). coccolithophore assemblages in each sample, we carried out the The data and R code to perform the calculation of CaCO3 pro- transformation of coccospheres in number of coccoliths, following the duction including error propagation and seasonal bias correction (see estimates by ref. 87, and then we adopted the coccolith mass estimates below) is available at https://doi.org/10.5281/zenodo.7458132. by88. The coccolith mass of Noëlaerhabdaceae also took into account the estimates by ref. 89 considering different mass for E. huxleyi calci- Correction of production for seasonality and interannual fication degree. variability The estimate of coccosphere calcite was further complemented To account for seasonal/inter-annual bias (or specifically, the bias at by the individual coccolith (detached from the coccosphere) calcite the time of sampling compared to mean annual production) we use concentration quantified by microscopy along radial transects of 0.32 satellite-derived PIC (CaCO3) to correct the coccolithophore pro- mm2, and subsequent mass estimates as described above. duction estimates (Fig. S7). The rationale behind this is that although The integrated total living coccolithophore calcite standing stock satellites only capture coccolithophore PIC concentrations in the was obtained considering the first shallow sampling depth to a depth upper few meters of the water column, the relative seasonal/inter- equal to 1% of the fluorescence peak. In St1 it ranges from 6 m to 180 m, annual changes at the surface should broadly reflect the relative Station 2 5–215 m, Staction 3 5–135 m; Staction 4 5–130 m, Staction 5: depth integrated seasonal/inter-annual changes in production at 5–130 m. To estimate the total annual coccolithophore calcite pro- depth10,38. We assess the validity of using satellite-derived PIC by duction we consider only the coccosphere calcite (number of calcify- regressing satellite-derived PIC (CaCO3) estimates during August ing cells). Uncertainty in the coccolith CaCO3 standing stock estimates 2017 against the surface values of coccolithophore CaCO3 (Fig. S1). is typically ±9% (1σ). Our surface (~5 m depth) estimates of coccolithophore CaCO3 standing stock show a strong correlation with satellite PIC (CaCO3) From concentration to annual production during August 2017. For each site the seasonal bias factor is calcu- We converted the measured CaCO3 concentrations (i.e. CaCO3 standing lated as satellite PIC during August 2017)/satellite mean annual PIC stock, CaCO3 biomass) into production rate, using estimates of the (2009–2019). Annual mean coccolithophore production is then turnover time for each group (that is, the typical lifespan of an indivi- given as depth integrated coccolithophore CaCO3 production during dual; Table 1): for foraminifera we used a range of 10–30 days90–93, August 2017 × 1/seasonal bias factor. As a sensitivity experiment, we noting that more slowly reproducing deep-dwelling species make up repeated this exercise using satellite-derived chlorophyll (see below) only a very small fraction of the assemblages in our tows31. For pter- instead of PIC, which results in larger estimates of annual CaCO3 opods and heteropods we used a range of 5–16 days (although we note production than using PIC. their lifespan may be much longer than this94). Pteropods and hetero- Unlike coccolithophores, we have no way to directly measure pod turnover time was calculated as turnover time (days) =1/G, where G changes in foraminiferal CaCO3 production through time. Instead, we is the average instantaneous growth rates expressed as mg Ca depos- use satellite-derived Chlorophyll A (chlor_a) to correct the for- ited (on mg Ca shell)−1 day−1 ref. 57,58. We assume that growth rates do not aminiferal production estimates for seasonal/interannual changes vary with shell size; this approximation is supported by a previous (Fig. S9). The rationale here is that the seasonal flux of foraminifera in study77, who found no significant difference in the shell growth rates of the North Pacific has been shown to follow primary production31,74, small and large sizes of any of the four pteropod species the author such that we can use relative changes in chlorophyll through time at examined. each site to correct the foraminiferal production estimates. For each For coccolithophores we used a range of 0.1–1.5 cell division day−1 site the seasonal bias factor is calculated as chlor_a during August (1.5–10 days) (Table 1). This range is derived from laboratory field 2017)/mean annual chlor_a (2002–2019). Annual mean foraminiferal estimates and simulated by a generalized coccolithophore model for production is then given as foraminiferal CaCO3 production during equatorial to North Pacific Ocean59. We are aware that cell growth August 2017 × 1/seasonal bias factor. phase differs for small cells with few coccoliths produced during Again, as we have no way to directly measure changes in exponential growth phase (normal, rapid division) and larger cells with pteropod/heteropod CaCO3 production through time, for het- more coccoliths produced during early stationary phase (slowed cell eropods and pteropods we refer to the long-term zooplankton division). data set from ocean stations ALOHA and PAPA to correct pteropod Given the large range in the turnover rate of coccolithophores, and heteropod CaCO3 production for seasonality. The rational foraminifera, pteropoda, and heteropoda, we apply a probabilistic here is that the seasonal changes in pteropod/heteropod abun- approach to determine the production rate and propagate the dance should broadly follow the seasonal changes in zooplankton uncertainties in turnover time through to our estimates of total abundance57. We note, that unlike the satellite PIC and chlorophyll Nature Communications | (2023)14:805 9 Article https://doi.org/10.1038/s41467-023-36177-w estimates used for coccolithophores and foraminifera, this 250 m, or 0.04 mg m-3, considering all data in the upper 1000 m method is not able to account for interannual variability, and only (Fig. S6). These values are three orders of magnitude smaller than the adjusts for the seasonal trend. Based on the multidecadal data set mean pteropod CaCO3 biomass value reported by ref. 18. of total zooplankton biomass at St. PAPA66,67 and St. ALOHA (all data and metadata are publicly available at hahana.soest.ha- Global satellite-derived PIC waii.edu/hot/hot-dogs/interface.html) the mean zooplankton In order to extrapolate the implications of our CaCO3 production biomass in the summer is respectively 2 and 1.2 times greater than estimates globally, we utilize a global climatology of satellite PIC the mean annual zooplankton biomass. We extrapolate these (CaCO3) (Fig. S8;97). Our results indicate satellite PIC (MODIS CaCO3) values of seasonal bias to each of our sites using latitude. We estimates in the subtropical gyre are biased low compared to vertically assume undetectable seasonal variation in pteropod growth rates. integrated CaCO3 production, due to the deeper (mainly coccolitho- If growth rates of pteropods could slightly decrease with tem- phore) CaCO3 production depth and the thickness of the coccolitho- perature, the annual production of aragonite would be less. Given phore productive layer (Fig. 2). To account for this bias in the CaCO3 the large assumptions within our method of correcting the pter- estimates we use a simple regression of total CaCO3 production at our opod and heteropod production data for seasonal variability, and sites against satellite CaCO3, the possibility of large temporal variability in pteropod abundances43, we also calculate annual pteropod CaCO3 produc- annual production CaCO3 ðmol m2 yrÞ = 0:65 + 0:03 tion using the comprehensive pteropod biomass compilation of ð6Þ × satellite PIC ðmg m3 Þ Bednaršek et al.18 (see below), which has excellent spatial and temporal sampling in the North Pacific (below). R2 = 0.71, p < 0.05, standard error = 0.3 mol m2 yr-1 (Fig. S2; Table S8). The deepening of production manifests as the non-zero Pteropod biomass and production estimated from MAREDAT intercept. Note this relationship is driven by one station with high Given the discrepancy observed with previous estimates of pteropod surface PIC (Station 5). Applying the relationship between total pro- CaCO3 production13 and the sparse spatial and temporal resolution of duction and satellite PIC (Fig. S2, Table S8) to the global mean surface our net-tow sampling, which unlike the coccolithophore data, cannot satellite derived PIC climatology (Fig. S7, Table S8), and integrating be independently verified using satellite data, we also estimate globally (weighting by area) results in a total CaCO3 production of pteropod CaCO3 biomass and production in the North Pacific using 3.1 1014 mol yr-1 (3.7 Pg C yr-1) globally, with the large caveat that this the MAREDAT database17. The database has excellent spatial and assumes the bias caused by the deepening of production away from temporal coverage of pteropod sampling within the North Pacific the high latitudes scales with surface PIC similarly globally. While we (Fig. 5). Similar to Bednaršek et al.18, we find no significant trends in acknowledge this approach is very crude, it nevertheless provides us biomass by latitude or time of year, so we perform our analysis using with a first-order approximation of total global production of CaCO3 all samples spanning the entire North Pacific basin and for all months. implied by our results. The MODIS PIC data are available from NASA We take all estimates of pteropod carbon biomass (reported in the Goddard Space Flight Center, Ocean Ecology Laboratory, Ocean Biol- database as mg C m-3) from the upper 250 m of the water column, ogy Processing Group97. which we consider as the production layer, with the vast majority of pteropod biomass found within the upper 200m18,95. This results in Floating sediment trap deployments 1793 discrete observations. We include zero values (120 samples, <7% The methods and data for the floating sediment traps are given in total) and remove 3σ outliers (16 samples, <1% total). Including these Dong et al.34 To summarize, at Stations 1–5 (Fig. 1) an array of surface- outliers results in unstable Gaussian Kernal densities (see below). We tethered sediment traps was deployed on a single line; one at 100 m calculate the CaCO3 biomass as the carbon biomass multiplied by the and the other at 200 m depth. Traps were deployed as free-floating fraction PIC (fPIC), using PIC:POC estimates given in Table 1. We then arrays for 52 to 78 h. The traps were polycarbonate particle interceptor integrate the standing stock over the production layer, and calculate tubes (PIT) that were 70 cm long, 10 cm diameter (12 tubes per trap) the production by diving by the turnover time (Table 1) in the same with funnels inserted to guide particles into a Falcon tube attached to manner as for the C-Disk-IV samples. We calculate the uncertainties the end of the funnel. Falcon tubes were pre-filled with HgCl2 poison in via Bootstrapping of the dataset, propagating the uncertainty in brine solutions to inhibit diffusive loss of poison during deployment. PIC:POC and turnover time using Monte-Carlo simulation, using a The poison-brine solution was made from seawater collected at 150 m highly-conservative flat probability distribution for both. Using with NaCl added to increase the salinity by ∼5, and sodium borate was a different depth range for the production layer (i.e. 0–1000 m) has a added to increase alkalinity by ∼2000 μM (US JGOFS protocol). Sam- negligible effect on our results. ples from six arbitrarily-chosen tubes among the 12 tubes at the same We estimate the probability of pteropod carbon and CaCO3 bio- depth were combined and ‘swimmers’ were manually picked out. The mass in the upper 250 m, integrated CaCO3 biomass, and CaCO3 pro- samples were then filtered onto a pre-weighed glass fiber filter duction rate using truncated kernal density:96 this approach truncates (Whatman glass microfiber filters, Grade GF/F, 1825–047) and, after the densities below zero, up-weighting the values that are closest to being returned to the lab, were reweighed to calculate sinking mass zero, and thus deals better with the highly-skewed dataset containing flux. The solid materials on the filters were then collected and analyzed zero values. with XRD for mineralogy (aragonite/calcite), and with the Picarro for In the North Pacific we find a typical CaCO3 biomass in upper PIC and total C. We refer the reader to Table 1 in ref. 34 for the values 250 m of 0.5 mg m-3 (0.2–1, 32–68% range), vertically integrated CaCO3 aragonite/calcite ratios and fluxes. biomass in upper 250 m of 122 mg m-2 (50–269, 32–68% range), daily CaCO3 production of 12 mg m-2 day-1 (5–27, 32-68% range). Data availability Expanding our analyzes the global dataset of ref. 18 (i.e. not only The data are given in Tables S1-6 in Supplementary Information and are the North Pacific subset described above) we find the global dataset is available on Pangaea (https://doi.org/10.1594/PANGAEA.948508). heavily skewed (Skewness = 13.3; a value above 1 is considered Skewed), such that the mean value reported by ref. 18 is not a useful Code availability statistic to describe the dataset. 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Nature Communications | (2023)14:805 13 Article https://doi.org/10.1038/s41467-023-36177-w 1 Universitat Autònoma de Barcelona, Institute of Environmental Science and Technology, Barcelona, Spain. 2Catalan Institution for Research and Advanced Studies (ICREA), Barcelona, Spain. 3Universitat Autònoma de Barcelona, BABVE Department, Barcelona, Spain. 4Laboratoire des Sciences du Climat et de l’Environnement (LSCE/IPSL), Université Paris-Saclay, Gif-sur-Yvette, France. 5University of St Andrews, School of Earth and Environmental Sciences, St Andrews, United Kingdom. 6Centre for Arctic Gas Hydrate, Environment and Climate (CAGE), Department of Geosciences, UiT The Arctic University of Norway, Tromsø, Norway. 7British Antarctic Survey, Natural Environmental Research Council, Cambridge, United Kingdom. 8Università di Palermo, Diparti- mento di Scienze della Terra e del Mare, Palermo, Italy. 9Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA. 10School of Ocean and Earth Science and Technology, Department of Oceanography, University of Hawai’i at Manoa, Honolulu, USA. 11 Department of Geology and Planetary Sciences, Linde Center for Global Environmental Science, California Institute of Technology, Pasadena, CA, USA. 12 University of Southern California, Department of Earth Sciences, Los Angeles, CA, USA. 13These authors contributed equally: Patrizia Ziveri, William Robert Gray. e-mail: Patrizia.Ziveri@uab.cat; william.gray@lsce.ipsl.fr Nature Communications | (2023)14:805 14