Global database of ratios of particulate organic carbon to thorium-234 in the ocean: Improving estimates of the biological carbon pump

The ocean’s biological carbon pump (BCP) plays a major role in the global carbon cycle. A fraction of the photosynthetically fixed organic carbon produced in surface waters is exported below the sunlit layer as settling particles (e.g., marine snow). Since the seminal works on the BCP, global estimates of the global strength of the BCP have improved but large uncertainties remain (from 5 to 20 GtCyr−1 exported below the euphotic zone or mixed-layer depth). The 234Th technique is widely used to measure the downward export of particulate organic carbon (POC). This technique has the advantage of allowing a downward flux to be determined by integrating the deficit of 234Th in the upper water column and coupling it to the POC/234Th ratio in sinking particles. However, the factors controlling the regional, temporal, and depth variations of POC/234Th ratios are poorly understood. We present a database of 9318 measurements of the POC/234Th ratio in the ocean, from the surface down to > 5500 m, sampled on three size fractions (∼> 0.7 μm, ∼ 1–50 μm, ∼> 50 μm), collected with in situ pumps and bottles, and also from bulk particles collected with sediment traps. The dataset is archived in the data repository PANGAEA® under https://doi.org/10.1594/PANGAEA.911424 (Puigcorbé, 2019). The samples presented in this dataset were collected between 1989 and 2018, and the data have been obtained from published papers and open datasets available online. Unpublished data have also been included. Multiple measurements can be found in most of the open ocean provinces. However, there is an uneven distribution of the data, with some areas highly sampled (e.g., China Sea, Bermuda Atlantic Time Series station) compared to some others that are not well represented, such as the southeastern Atlantic, the south Pacific, and the south Indian oceans. Some coastal areas, although in a much smaller number, are also included in this global compilation. Globally, based on different depth horizons and climate zones, the median POC/234Th ratios have a wide range, from 0.6 to 18 μmoldpm−1. Published by Copernicus Publications. 1268 V. Puigcorbé et al.: Global database of oceanic POC/234Th ratios


Introduction
The vertical export of photosynthetically produced particulate organic carbon, from the surface waters to the deep ocean (i.e., biological carbon pump; Eppley and Peterson, 1979), has a strong impact in the global carbon cycle. Through this process, the ocean stores carbon dioxide (CO 2 ) away from the atmosphere and buffers the global climate system (Kwon et al., 2009). Indeed, estimates suggest that atmospheric CO 2 levels would be 200 ppm higher than current concentrations without the biological carbon pump (Parekh et al., 2006). However, quantifying the magnitude of the biological carbon pump at both the regional and global scales is challenging and current assessments vary widely, with estimates ranging from 5 to 20 Gt C yr −1 being exported below the euphotic zone or the mixed-layer depth (Guidi et al., 2015;Henson et al., 2011;Laws et al., 2011).
Here we focus on the use of radioisotopes, specifically, 234 Th. The 234 Th approach allows us to quantify an export flux from (i) a water profile of 234 Th to obtain its deficit relative to 238 U combined with (ii) an estimate of the ratio of POC concentration to 234 Th activity (POC/Th ratio) in sinking matter (Buesseler et al., 1992). In reviewing POC/Th ratio variability using the data available at the time, Buesseler et al. (2006) found that the POC/Th ratios (i) increase or remain constant with increasing particle size and (ii) decrease with depth. Regionally, the POC/Th ratios vary largely between oceanic provinces and regimes (Puigcorbé et al., 2017a). The study of the biogeochemical behavior of 234 Th with regards to marine particles has received significant attention (Maiti et al., 2010;Le Moigne et al., 2013c;Puigcorbé et al., 2015;Rosengard et al., 2015;Santschi et al., 2006), and the availability of 234 Th-related data has been enhanced thanks to international and national programs such as GEOTRACES (Mawji et al., 2015;Schlitzer et al., 2018), JGOFS (Joint Global Ocean Flux Study) (Buesseler et al., 1998(Buesseler et al., , 1995, or VERTIGO (Buesseler et al., 2008b), yet the factors controlling the variations in the POC/Th ratio as a function of region, time, particle size and type, and water column depth remain poorly understood. Assessing the influence of such factors on the POC/Th ratios will contribute to improve our modeling efforts and our capacity to predict the export and fate of the organic carbon produced in the surface layers. Indeed, the necessity to constrain the variability of the POC/Th was discussed and considered a priority at the tech-nical meeting "The Application of Radionuclides in Studies of the Carbon Cycle and the Impact of Ocean Acidification" held at the International Atomic Energy Agency (IAEA) Environment Laboratories in Monaco in October 2016 . Therefore, we compiled a database that comprises 9318 POC/Th ratios collected between 1989 and 2018 covering most oceanic provinces at depths ranging from 0 to > 5500 m. The particles were collected using collection bottles (i.e., Niskin), in situ pumps, or sediment traps, and they include bulk and size fractionated samples. This database significantly increases the pool of POC/Th ratio data available at the time of Buesseler et al. (2006) and enables us to test the influence of various factors on the variability of POC/Th ratios. Among other information, the influence of biogeochemical characteristics of the area (e.g., nutrient concentrations) together with the surface productivity levels, phytoplankton compositions, and zooplankton abundance could be examined through satellites products and/or global databases (e.g., Buitenhuis et al., 2013;Moriarty and O'Brien, 2013).

The 234 Th approach
The short-lived radionuclide thorium-234 ( 234 Th, t 1/2 = 24.1 d) is widely used to estimate the magnitude of POC that escapes the upper ocean layers (e.g., the euphotic zone) (Waples et al., 2006). 234 Th is the decay product of uranium-238 ( 238 U, t 1/2 = 4.47 × 10 9 yr). While uranium is conservative and proportional to salinity in well-oxygenated seawater (Chen et al., 1986;Ku et al., 1977;Owens et al., 2011), thorium is not soluble in seawater and it is scavenged by particles as they form and/or sink along the water column. As a consequence, a radioactive disequilibrium between 238 U and 234 Th can be observed, mainly in the upper layers of the water column, which at first approximation, is proportional to the numbers of particles exported and hence can be used to estimate particle and elemental export fluxes.
A one-box scavenging model (see review by Savoye et al., 2006, and references therein) is commonly applied to calculate 234 Th export rates. Steady-state (SS) or non-steady-state (NSS) conditions are assumed depending on the conditions at the sampling time and the possibility to reoccupy locations within an adequate timescale. Le Moigne et al. (2013b) reported 234 Th fluxes from both types of models in their database with flux integration depths spanning from the surface down to 300 m, although the most common integration depths were between 100 and 150 m. The choice of export depth when using the 234 Th technique is not trivial. Rosengard et al. (2015) provide recommendations to the various manners of choosing the export depth in order to integrate the 234 Th fluxes. Once the 234 Th export flux is estimated, it is multiplied by the ratio of POC to particulate 234 Th activ-ity in sinking particles to obtain the POC flux. The sinking particles from which the ratio is measured should, ideally, be collected at the depth where the export has been estimated and represent the pool of particles that are driving the export of organic carbon.

2.2
The crux of the 234 Th approach: POC/Th ratios of sinking particles The determination of the POC/Th ratio has been historically attained by assuming that sinking carbon is driven by large particles, generally >50 µm in size (researchers also use 51, 53, or 70 µm, depending on the mesh supplier) whereas organic carbon within small particles is assumed to remain suspended and therefore not contribute to the export flux (Bishop et al., 1977;Fowler and Knauer, 1986). However, recent studies have shown that small particles can be significant players in the particle export and should not be disregarded (Alonso-González et al., 2010;Durkin et al., 2015;Le Gland et al., 2019;Puigcorbé et al., 2015;Richardson, 2019), particularly in oligotrophic regions. The most common methods to obtain the particulate fraction to measure the POC/Th ratio are (i) in situ pumps (ISPs), which can allow for sampling different particle sizes; (ii) collection bottles (CBs) such as Niskin bottles, providing bulk particles, i.e., > 0.7 or 1 µm particles; (iii) sediment traps (STs); and although less common (iv) marine snow catchers. In some instances various methods have been used in combination (Cai et al., 2010;Maiti et al., 2016;Puigcorbé et al., 2015). Different sampling devices have been shown to provide differences in POC/Th ratios, usually within a factor of 2 to 4 . The differences can be related to the collection of different particle pools and/or the enhanced presence of swimmers. STs collect sinking particles and may suffer from hydrodynamic discrimination and undersample slow-sinking particles (Gustafsson et al., 2004). CBs sample both sinking and suspended particles similar to ISPs. ISPs filter large volumes of water and have been suggested to potentially undersample some of the fast-sinking particles (Lepore et al., 2009) and sample neutrally buoyant C-rich aggregates (i.e., non-sinking but with high POC/Th ratios) (Lalande et al., 2008). Biases due to washout of large particles when using ISPs (Bishop et al., 2012) or aggregate collapse induced by their high cross-filter pressure (Gardner et al., 2003) may further enhance these differences. The presence of swimmers can also be an important bias of POC/Th ratios when not thoroughly removed, since they skew measurements towards higher values because of their high POC proportion compared to 234 Th (Buesseler et al., 1994;Coale, 1990).

POC/ 234 Th ratio variability
Despite the significant body of literature available on POC/Th ratios, more than 10 years after the review by Bues-seler et al. (2006) we still cannot explain the variability of the POC/Th ratios with depth, time, particle type and size, or sinking velocity easily or at a global level. Changes with size and depth have been the most extensively examined. The relation between POC/Th ratio and particle size has been assessed before, with results suggesting that there is not a direct relationship. Previous studies have reported increasing ratios with increasing particle size Buesseler et al., 1998;Cochran et al., 2000), which has been interpreted as an effect of the volume-to-surface area ratio of the particles, due to 234 Th being surface bound whereas C would be contained within the particles ). Yet, a number of studies have reported the opposite trend (i.e., decreasing ratio with increasing particle size; Bacon et al., 1996;Planchon et al., 2013;Puigcorbé et al., 2015) or no clear change with size Lepore et al., 2009;Speicher et al., 2006). Depth is another factor that has been considered when assessing the variability of POC/Th, since particles are produced in the surface layer and are remineralized on their transit along the water column (Martin et al., 1987). POC/Th ratios have been found to be attenuated with depth (Jacquet et al., 2011;Planchon et al., 2015;Puigcorbé et al., 2015). This is due to (in no order or importance) decreasing autotrophic production with increasing water depth, preferential C loss compared to 234 Th through remineralization processes, changes in superficial binding ligands along the water column, and/or scavenging of 234 Th during particle sinking resulting in enhanced particulate 234 Th activities Rutgers van der Loeff et al., 2002), leading to significant variability in the attenuation rates. Theoretically, high sinking velocities may limit the variations in POC/Th ratios with depth, owing to shorter residence times limiting the impacts of biotic and abiotic processes. However, using specifically designed STs that segregate particles according to their in situ sinking velocities, Szlosek et al. (2009) observed no consistent trend between POC/Th ratios and sinking velocities.
The truth is that numerous processes can impact the POC/Th ratios apart from particle size or depth, such as particle composition or aggregation-disaggregation processes mediated by physical or biological activity (Buesseler and Boyd, 2009;Burd et al., 2010;Maiti et al., 2010;Szlosek et al., 2009), which adds a level of complexity to the prediction of their variability in the ocean. Yet, due to the significance of the POC/Th ratios for the accuracy of the 234 Th flux method, the effort should be made to constrain the factors that will impact its variability, and a number of environmental and biogeochemical parameters can be assessed with that goal at a global scale. Among others, surface productivity, phytoplankton composition, zooplankton abundance, mixed-layer depth, dust inputs to the surface ocean, and ice cover Mahowald et al., 2009;Moriarty and O'Brien, 2013) are all poten-1270 V. Puigcorbé et al.: Global database of oceanic POC/ 234 Th ratios tial candidates to test their global patterns against POC/Th ratio variability.

Data classification
Our dataset is archived in the data repository PANGAEA ® (http://www.pangaea.de), https://doi.org/10.1594/PANGAEA.911424 (Puigcorbé, 2019). Latitude, longitude, and sampling dates are reported. When dates of the individual stations were not reported in the original publications, we allocated the midpoint of the sampling period as the sampling date. The same was done when the specific sampling coordinates were not available (see details in the comments related to the dataset; https://doi.org/10.1594/PANGAEA.902103; Puigcorbé, 2019). The database consists of 9318 measurements of POC/Th ratios in the ocean. Particles were collected using in situ pumps (ISPs), water collection bottles (CBs), and sediment traps (STs). We refer to "bulk" (BU) for particles sampled using CBs and ISPs with a pore size filter of 0.2-1 µm. For this group of samples, particles > 0.7 µm were collected using GFF filters and > 1 µm using QMA filters. In some particular cases other types of filters, with a different pore size (e.g., 0.2, 0.45, or 0.6 µm) might have been used (see database for details). Hereafter, we use > 1 µm for the bulk particles. We refer to "small particles" (SPs) for particles usually collected using ISPs on a 1-50 µm mesh size and "large particles" (LPs) for particles usually collected using ISPs on mesh size > 50 µm (see details on other size ranges also used in the database). Finally, some POC/Th ratios were measured in sinking particles sampled using sediment traps (STs). Figure 1 shows the global distribution of POC/Th ratios grouped by these four categories: BU, LP, SP, and ST. The POC/Th ratios were obtained from particles collected at various depths from the surface to > 5500 m (Fig. 2). All the information on locations, dates, depth, size fractions/device (BU, SP, LP, and ST), and references is included as metadata in the online database and presented in Table 1.
Our database covers POC/Th measurements sampled between 1989 and 2018, including unpublished data from our laboratories or graciously made available to us by colleagues and data available in online databases. Figure 3 shows the number of POC/Th measurements available per year. In the years 1997, 2004, 2005, 2008, 2010, 2011, and 2013, the number of POC/Th measurements was > 500. This highlights dedicated carbon export programs such as the Joint Global Ocean Flux Study (JGOFS) (Buesseler et al., 1998(Buesseler et al., , 1992(Buesseler et al., , 1995Murray et al., 1996Murray et al., , 2005, the VER-TIGO (Vertical Transport in the Global Ocean) voyages in the Pacific Ocean (Buesseler et al., 2008b), and the GEO-TRACES program (Mawji et al., 2015;Schlitzer et al., 2018), as well as the maintained effort of the time series stations (Kawakami et al., 2004(Kawakami et al., , 2010(Kawakami et al., , 2015Kawakami and Honda, 2007). Sampling effort also varied depending on the month of the year (Fig. 3b), with late spring-summer months being the most highly sampled in both hemispheres. The Northern Hemisphere has been largely sampled in September, May, and June (49, 10, and 5 times more data than in the Southern Hemisphere, respectively), whereas the Southern Hemisphere has been more sampled in December and February (5 and 4 times more data than in the Northern Hemisphere, respectively), with no data available for the months of July and August and only five data points in September (austral winter). For the rest of the months, the Northern Hemisphere presents 1.4-1.8 times more data than the Southern Hemisphere. In the equatorial region (taken as the latitudes between −10 and 10 • N) major sampling efforts took place in May, with no data collected in January and just eight data points available from December. The monthly distribution is, therefore, globally biased towards the warmer and more productive seasons, leaving the winter months largely undersampled, particularly in the Southern Hemisphere.

Global variability: climate zones and depth horizons
The global variability of POC/Th ratios looking at six different depths horizons (50, 100, 200, 500, 1000, and > 1000 m) and grouped by climatic zones (polar > 66.5 • , subpolar 66.5-50 • , temperate 50-35 • , subtropical 35-23.5 • , and tropical 23.5 • N-23.5 • S) is presented in Fig. 4. A PERMANOVA analysis was conducted to examine the data, and the results indicate that all the depth horizons defined here were significantly different (p < 0.05). Significant differences were also found between climatic zones, except between the temperate and subtropical zones and between the subtropical and the tropical zones, when considering all the data together. Statistical differences between zones within a certain depth range are shown in Fig. 4.
In general, we observe a reduction in POC/Th ratios with depth, previously reported by others , and likely mainly due to the remineralization of carbon along the water column. The decrease is particularly marked in the upper 200 m, where biological processes affecting the ratios are more intense, and then it smoothes below that depth horizon as the strength of these processes is more limited below the euphotic zone. It is worth noticing that some studies, particularly in coastal areas, presented extremely large POC/Th ratios (> 100 µmol dpm −1 , not included in Fig. 4). These high ratios are not always discussed in the publications, but the presence of live zooplankton Savoye et al., 2008;Trull et al., 2008), especially in BU, ST, and LP fractions, when not picked out can be the cause for those high values and should be considered with caution.
Regarding the climate zones, there is significant variability, but, in general, large POC/Th ratios occur more often in productive and high-latitude regions relative to low-latitude Table 1. Sampling year; area; number of samples for large particles (LPs), small particles (SPs), bulk (BU) particles, and particles collected with sediment traps (STs); and reference of studies used in the database. Note the following references refer to data published in several papers: Stukel et al. CCE refers to data published in Stukel et al. (2011Stukel et al. ( , 2015Stukel et al. ( , 2017Stukel et al. ( , 2019; Stukel et al. CRD refers to data from Stukel et al. (2015Stukel et al. ( , 2016. Buesseler JGOFS dataset Arabian Sea refers to data published in Buesseler et al. (1998) and also available at https: //www.bco-dmo.org/project/2043 (last access: 3 June 2020). Buesseler JGOFS dataset Southern Ocean refers to data published in Buesseler et al. (2001) and also available at https://www.bco-dmo.org/project/2044 (last access: 3 June 2020). Kawakami North Pacific time series data are available at http://www.jamstec.go.jp/res/ress/kawakami/234Th.html (last access: 3 June 2020) and have also been published in Kawakami (2009), Kawakami et al. (2004Kawakami et al. ( , 2010Kawakami et al. ( , 2015, Kawakami and Honda (2007), and Yang et al. (2004). Further details regarding particle size specifications or sampling device can be found in the database file https://doi.org/10.1594/PANGAEA.902103.

Sampling year
Area LP SP ST BU Reference/investigator n n n n
High POC/Th ratios are usually associated with the presence of large phytoplankton groups, such as diatoms, which are dominant in high-latitude areas with no nutrient limitations, or where zooplankton populations are large and there is a significant input of fecal pellets, which should also have high POC/Th ratios. Low ratios, on the other hand, are commonly observed in warm oligotrophic areas where productivity is limited and the main phytoplanktonic groups are picoplankton . Exceptions do exist, but they are usually found in coastal areas where other factors could be influencing the planktonic community (e.g., seasonal upwelling, continental influence, river inputs).

Contributing to global POC export estimates
The 234 Th approach has been used to derive an export model at the global scale that uses sea surface temperatures and net primary productivity from satellite products (Henson et al., 2011). The parametrization for this model has large uncertainties in the cold regions (low sea surface temperature), which lead to a reduced estimate of the global biological carbon pump (∼ 5 Gt C yr −1 ) compared to other satellitederived export models (9-13 Gt C yr −1 ; Dunne et al., 2007;Laws et al., 2011). A recent study by Puigcorbé et al. (2017a) estimated POC export fluxes in the North Atlantic using in situ data for the 234 Th method and compared it to three different satellite-derived export models: Dunne et al. (2007), Henson et al. (2011), andLaws et al. (2011). The conclusion was that, overall, the geographical trends were captured by all the approaches, but the absolute values between them   could reach important discrepancies. In that study, the authors advised a revision of the parametrization of the models going beyond sea surface temperatures in order to adjust to specific ocean bioregions. This database sets a strong background to develop that parametrization and contribute to similar modeling efforts to constrain the global carbon export fluxes as done by Henson et al. (2011).

Significant gaps and recommendations
This database provides the global POC/Th ratios sampled from all the oceans up until 2018. The sampling coverage is significant but it is not evenly distributed. Areas such as the China Sea, Arabian Sea, northwestern Mediterranean Sea, central Pacific, and high latitudes of the Atlantic Ocean are well represented, whereas other areas, such as the olig-otrophic gyres, west Pacific, or the Southern Ocean, present important gaps. The data are not evenly distributed between seasons either, with most of the sampling taking place during spring and summer in both hemispheres, which is also when the export fluxes are expected to be larger. High seasonality in undersampled areas could potentially bias our global view of the POC/Th ratios and have an impact on the Th-derived carbon export flux estimates. It would be beneficial for future efforts to obtain data for those undersampled areas with high seasonality to better characterize the expected variability in the ratios within those areas and to cover a larger span of seasons in order to better understand the seasonality of POC/Th and thus be able to translate it more accurately to the global POC export estimates.

Conclusion
Here we provide a global database of 9318 estimates of POC/Th ratios collected between 1989 and 2018 at various depths from below the surface to > 5500 m using in situ pumps, collection bottles, and sediment traps. The observed pattern of POC/Th ratios reflects a decrease with depth and a link with the latitude, with higher ratios usually observed in high-latitude areas. Some noteworthy gaps in the dataset are the Benguela system, the Mauritanian upwelling, the western and south Pacific, and the southern Indian Ocean. The fall-winter months in both hemispheres are also underrepresented. The temporal and spatial undersampling of some areas could bias the global view of the POC/Th ratios. Despite the gaps, this database is the largest compilation POC/Th ratios to date and could be used to better understand the factors controlling the variation in ratios on a global scale. This will help revise and provide improved estimates of the ocean's biological carbon pump.
Author contributions. VP and FACLM compiled the dataset and prepared and reviewed the manuscript. All the authors contributed to the review of the manuscript.
Competing interests. The authors declare that they have no conflict of interest.

Acknowledgements.
We are very grateful to all of those who have provided data for this global database, especially to those authors who have provided unpublished data to make this database as complete as possible. We would also like to thank Elena Ceballos and Sian McNamara who helped during the preparation of the database. We also thank Daniela Ransby, from the PAN-GAEA Data Archiving & Publication team, for her support and efficiency during the data submission process. Viena Puigcorbé received funding from the School of Science at Edith Cowan University to compile the dataset and facilitate the collaboration with Frédéric A. C. Le Moigne (G1003879). This work is contributing to the ICTA "Unit of Excellence" (MinECo, MDM2015-0552). Thanks also to the Radioecology Laboratory of the IAEA for hosting the technical meeting "The Application of Radionuclides in Studies of the Carbon Cycle and the Impact of Ocean Acidification", and in particular to Stephanie Morris and all the participants for the fruitful discussions.
Financial support. This research has been supported by the Edith Cowan University (grant no. G1003879).
Review statement. This paper was edited by David Carlson and reviewed by Erin Black and one anonymous referee.