# On Einer Steemann Nielsen's 1952 "The Use of Radio-active Carbon (C14) for measuring Organic Production in the Sea"

John R Dolan

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John R Dolan. On Einer Steemann Nielsen's 1952 "The Use of Radio-active Carbon (C14) for measuring Organic Production in the Sea". ICES Journal of Marine Science, 2025, 82, 10.1093/icesjms/fsaf041. hal-05020303

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# On Einer Steemann Nielsen's 1952 "The Use of Radio-active Carbon (C¹⁴) for measuring Organic Production in the Sea"

John R. Dolan*

Laboratoire d'Océanographie de Villefranche-sur-Mer, Sorbonne Université CNRS UMR 7073, Station Zoologique, 181, Chemin du Lazaret, 06230 Villefranche-sur-Mer, France

*Corresponding author. Laboratoire d'Océanographie de Villefranche-sur-Mer, Sorbonne Université CNRS UMR 7073, Station Zoologique, 181, Chemin du Lazaret, 06230 Villefranche-sur-Mer, France. E-mail: john.dolan@imev-mer.fr

## Abstract

Einer Steemann Nielsen's 1952 methods paper describing the use of C¹⁴ to measure photosynthesis in the journal now known as the *ICES Journal of Marine Research* was a landmark publication. It is still regularly cited today. Here, in a brief account, the story of Einer Steemann Nielsen (1907–1989), and his major publication is given, along with evidence of its enduring value.

**Keywords:** primary production; phytoplankton; history of science

One might think a method introduced 73 years ago, involving manipulating a radioactive isotope, is likely enjoying a well-deserved retirement, perhaps replaced in day-to-day work with an electronic device of some sort. However, much like the Secchi Disk that dates from 1864 (see Wernard 2010), some methods have proved to be timeless, and the use of C¹⁴ to measure primary production is one such method. Here, first the life and work of Einer Steemann Neilsen (1907–1989) are briefly reviewed, with a special focus on his diverse contributions to the journal now known as the *ICES Journal of Marine Science*. The biographical and bibliographic sketch is based largely on the account by Søndergaard 2002 (which includes a complete Steemann Nielsen bibliography), and is followed by a close look at his 1952 landmark publication and finally the evidence of its enduring value to the scientific community.

Einer Steemann Nielsen was born on June 13th in 1907. He studied at the University of Copenhagen beginning in 1925, completing a masters in botany in 1931 and obtaining his Ph.D. in 1934. Unknown to most of us is that he began his career as a phytoplankton taxonomist. His first publication was a description of new species of diatoms, a dinoflagellate, and a chlorophyte from the Indian Ocean (Steemann Nielsen 1931), and his Ph.D. thesis was on dinoflagellates of the genus *Ceratium* (Steeman Nielsen 1934), both based mostly on samples he gathered himself during part of the Dana Expedition of 1928–1930 around the world. Steemann Nielsen's first scientific job was as a research assistant at the Plankton Laboratory at the Danish Commission for Fisheries and Sea Research in 1934, and shortly after he also held a post as a research assistant at the Royal Danish School of Pharmacy. He was made Professor of Botany at the Royal Danish School of Pharmacy in 1944 and remained there until 1969, when he became a professor at the University of Copenhagen. Steeman Nielsen was

active in scientific organizations. In the late 1940s he was a founding member and served as secretary of the *Societas Physiologiae Platarum Scandinavica*, and in the 1950s was also quite active in ICES. Steemann Nielsen was a familiar face at ICES meetings; he chaired the Plankton Committee and organized a meeting in 1957 on measurements of marine primary production (Rozwadowski 2002) and was a co-author of a report on the meeting (Ruther et al. 1958). Steemann Nielsen retired in 1977, at the age of 70. He then withdrew completely from science and devoted himself to studies of the paintings and stained glass windows of the churches of Europe. Steemann Nielsen passed away on April 17, 1989.

Steemann Nielsen's early contributions to the *Journal du Conseil*, now known as the *ICES Journal of Marine Science*, concerned the quantification of the standing stocks of phytoplankton (Steemann Nielsen 1933, 1938), zooplankton (Steemann Nielsen 1935a, 1939), and the relationships between the concentrations of the two groups (Steemann 1937). In his subsequent work during the 1940s, Steemann Nielsen worked mostly on the physiology of macroalgae and phytoplankton. Steemann Nielsen's next contribution (other than an obituary of Ove Paulsen) to the *Journal du Conseil* was his detailed description of the use of C¹⁴ to measure the primary production of phytoplankton (Steemann Nielsen 1952). It remains today, curiously unclear what prompted Steemann Nielsen's turn towards measuring rates of primary production, and in particular the use of C¹⁴ (Søndergaard 2002). However, according to the account of Barber and Hilting (2002) and that of Marra (2019), he was simply the right person in the right place, because in Copenhagen, C¹⁴ isotope labeling was used to study the products of photosynthesis in the post-WW2 years. In Barber and Hilting's words, "*Steemann Nielsen had the insight that the radiotracer methodology could be used to quantify a bulk ecological process such as primary production.*" At the
<figure><img src="image_2.png" /><figcaption>**Figure 1.** The left panel shows Steemann Nielsen (wearing white shoes) holding the water sampler aboard the *Galathea* (image from Søndergaard 2002, with permission). The middle panel shows the glass sampler in a teak frame used to obtain water samples without any contact with metals. The right panel shows the illuminated rotating disk device used to incubate samples inoculated with $C^{14}$. The middle and right images are from Steemann Nielsen (1956), out of copyright.</figcaption></figure>

time, primary production was most often quantified using the light bottle/dark bottle technique, first published in English in 1927, in the ICES publication, *Rapports et Procès-verbaux des Réunions* (Gaarder and Gran 1927). Rates of photosynthesis are estimated based on increases in the oxygen concentration in bottles in ambient light (light bottles) due to photosynthesis, corrected for oxygen consumption due to respiration, estimated by declines in oxygen in opaque bottles (dark bottles), in the absence of photosynthesis. Steemann Nielsen actually had extensive experience with the technique (Steemann Nielsen 1932, 1935b, 1940, 1951a), and he realized that the method was inappropriate, likely too insensitive, for use in oligotrophic waters (Steemann Nielsen 1956). In any case, an opportunity presented itself to allow Steemann Nielsen to attempt to measure production in oligotrophic waters by participating in the Galathea Deep Sea Expedition (1950–1952). It was organized in the late 1940s (Spärck 1956), and eventually given the primary goal of sampling abyssal depths (Bruun 1956), most often found in oligotrophic waters. By the spring of 1950, Steemann Nielsen had worked out the protocol and developed the devices to be used aboard the *Galathea* (Fig. 1) for the determination of primary productivity measurements.

Steemann Nielsen's $C^{14}$ method paper appeared in the August 1952 issue of the *Journal du Conseil* (Fig. 2). Oddly, results of measurements of primary production made aboard the *Galathea* first appeared over a year earlier, in a letter published in *Nature* in April of 1951, dated March 17th, thus well before the complete description of the $C^{14}$ method appeared. The *Nature* letter included only a cursory description of his method, preceded by the statement “A full description will shortly be published elsewhere.” (Steemann Nielsen 1951b). It is possible that the 1952 *Journal du Conseil* article was already in press when the 1951 *Nature* letter appeared as it is not cited in his 1952 article. Steemann Nielsen's $C^{14}$ method paper (Steemann Nielsen 1952) gave very detailed instructions. Including, for example, the setup of glassware, preparation of stock solutions, type of filters to be used, and directions concerning the

use of a “Geiger-Müller” counter tube to measure the radioactivity of the processed filters. With regard to field procedures, it was specified that water samples should be collected using an all-glass sampler, of the type shown here in Fig. 1, and said in the $C^{14}$ method paper, as described in “Aabye Jensen and Steemann Nielsen 1952.” However, the article was given in the “Literature” without a year as “In preparation,” and it actually appeared in the January 1953 issue of the *Journal du Conseil* (Aabye Jensen and Steemann Nielsen 1953). Thus, the complete methods and materials used to generate the primary production data reported in the *Nature* letter of April 1951 were not available until early 1953!

Steemann Nielsen's 1951 letter in *Nature* and the $C^{14}$ method paper in the *Journal du Conseil* strongly criticized the existing estimates of primary production in the oligotrophic open ocean made by Gordon Riley in the Sargasso Sea using the light bottle/dark bottle technique (Riley 1939) as overestimating primary production by a factor of 10. According to Steemann Nielsen, photosynthetic production of $O_2$ is greatly overestimated in light-exposed bottles because bacterial respiration of $O_2$ is suppressed due to the bactericidal effects of UV light penetration. Riley attempted to defend his estimates but he admitted, “*Although the attack on the oxygen method seems as empty as it is violent, it is immediately apparent that the new C¹⁴ technique is superior in sensitivity and accuracy*” (Riley 1953). In Steemann Nielsen's next article in the *Journal du Conseil* “On organic production in the Oceans” (Steemann Nielsen 1954), he fully quoted Riley's admission. Although it was soon shown that the bactericidal effects of UV light penetration in glass bottles incubated *in situ* below a few cm from the surface are negligible (Vaccaro and Ryther 1954), the $C^{14}$ method rapidly gained acceptance. It actually became somewhat of an industry with the creation of the non-profit enterprise “The International Agency for ¹⁴C Determination,” under the honorary supervision of Steemann Nielsen, which sold “ready to use” ampoules of $C^{14}$ and also processed filters, providing estimates of carbon assimilation rates (Anon. 1958a, Steemann Nielsen 1959). The agency was financed in
<figure><img src="image_3.png" /><figcaption>**Figure 2.** Steemann Nielsen's landmark paper appeared in August of 1952 in issue 2 of volume 18 of the publication entitled (reading from top to bottom of the cover) "*Conseil Permanent International pour l'Exploration de la Mer, Journal du Conseil*," the present day *ICES Journal of Marine Science*. The official name of the journal at the time was *Journal du Conseil International pour l'Exploration de la Mer* (Anderson 2024). Citations to the paper are remarkably heterogeneous. For example, as authored by Steemann-Nielsen (Engstrom et al. 2000) or Nielsen, S.E. (Pierrella Karlusich et al. 2020) and as published in "J. Cons." (Banse 2002a), "J. Cons. Int. Mer" (Jugnia et al. 2000), and "Cons. Perm. Int. Explor. Mer" (Turley et al. 2000).</figcaption></figure>

part by UNESCO, a tribute to its international nature. (Anon. 1958b).

While the C¹⁴ uptake method is today most commonly employed (e.g. Milligan et al. 2015), it should be noted that the light/dark bottle technique and the C¹⁴ method coexisted for quite some time and indeed still coexist. Steemann Nielsen gave detailed recommendations on the protocols for both techniques in his article "Experimental methods for measuring organic production in the sea" in *Rapports et Procès-verbaux des Réunions* (Steemann Nielsen 1958). As late as 2007, the light/dark bottle and C¹⁴ rates were still being compared (Gazeau et al. 2007).

With the wide employment of the C¹⁴ method, it became "*undoubtedly, the most controversial topic between the 1960s and the 1980s in biological oceanography...*" (Mills 1989). This was because a multitude of confounding factors and

potential artifacts became known (see Petersen 1980). These were findings such as the effects of bottle volumes, incubation time, the variable phenomenon of excretion of fixed carbon as dissolved organic matter by phytoplankton, rapidly assimilated by heterotrophic prokaryotes, and the importance of primary productivity by very small taxa of phytoplankton, poorly retained by commonly used filters. Such findings called into question the relationship between C¹⁴ retained on filters and gross or net primary production. Some of the potential problems and needed refinements to the technique were reported on in ICES serials (e.g. Berge 1958, Wolfe and Schelske 1967, Goldman 1968). Nonetheless, C¹⁴ estimates of primary production have become a "core measurement" in large international oceanographic programs such as the 1987–2003 Joint Global Ocean Flux Study (see Knap et al. 1994).
<figure><img src="image_4.png" /><figcaption>**Figure 3.** Cumulative number of citations to Steemann Nielsen's (1952) paper on the C¹⁴ method, with time, based on citation data using Google Scholar and Clarivate Web of Science. For both platforms, searches were conduction for citations to the article title "The use of radio-active carbon (C14) for measuring organic production in the sea," which returns citations regardless of the name of the author or the name of the journal, both of which have been cited in various manners (see Fig. 2 legend). Total citations to the paper from the Web of Science number 1845 and 3096 according to Google Scholar.</figcaption></figure>

Strong opinions on the utility of the C¹⁴ method resurfaced in 2002 with the 50th anniversary of method's introduction in a remarkable series of letters published in the *Limnology and Oceanography Bulletin*. The first, entitled "Should we continue to measure ¹⁴C-uptake by phytoplankton for another 50 years?" by Karl Banse argued that in of itself, C¹⁴ uptake is not easily converted to rates of cell growth rates or biomass production that are needed to estimate primary production (Banse 2002b). The first reply by Tim Parsons, was that the method provides rates of photosynthesis, and knowledge of temporal or geographical variability of the rates is quite valuable (Parsons 2002). The second was by Evelyn and Barry Sherr and can be summarized as stating that our knowledge of marine photosynthesis and loss process is largely insufficient and does not allow abandoning measuring rates of photosynthesis (Sherr and Sherr 2002). A reply in the form an article from John Marra was that carbon assimilation does correlate with new biomass production, and perhaps most importantly, "... we should continue to measure ¹⁴C-uptake in the future as an important component of temporal change in the ocean" (Mara 2003). Echoing Mara's point, Louis Hobson's letter pointed out that "the principal use of ¹⁴C-uptake measurements during the past 50 years was to assess spatial and temporal variations in primary production. I believe that there will be a continuing need for these measurements in oceanic environments, particularly at this time of increasing CO₂ levels" (Hobson 2003). Banse answered that temporal changes may be best assessed using satellite-detected changes in photosynthetic pigment concentrations (Banse 2003), oddly ignoring the fact that satellite-based measures of chlorophyll concentration were already used to map rates of photosynthesis based in large part on C¹⁴ data (e.g. Behrenfeld and Falkowski 1997). The exchanges between Banse and Mara were followed by a letter from Algird Moigis on Mara's reply concerning possibly large effects of grazers in incubations (Moigis 2004). It was answered by Mara, saying that grazer effects in small incubation volumes are likely not important in all places and times (Mara 2004).

The utility of the C¹⁴ technique was ardently defended 50 years after its introduction, and I, for one, predict that its 100th anniversary, in <30 years from now, will be celebrated. This is because, while problems with the method still exist, e.g. the discrepancies between incubations *in situ* and using incubators (Larsson et al. 2021), it is still very widely used today. Clear evidence of the utility of Steemann Nielsen's 1952 article is obvious by a simple consideration of citation data. The 1952 paper has been very well cited throughout the years, and it continues to be well-cited today (Fig. 3). In 2024 alone, it was cited 34 times according to Web of Science data and 51 times according to Google Scholar (data retrieved on January 30, 2025). Total citations to the paper according to the Web of Science number 1845 and 3096 according to Google Scholar. Note that Google Scholar includes citations not only in journals but also in reports, books, and theses. It is then arguably a more inclusive measure of use of a publication than the Web of Science data.

To put the citation numbers of Steemann Nielsen's paper in perspective, they can be compared to another "highly cited" paper, the one spotlighted by Sathyendranath et al. (2015) in the pages of this journal: Sverdrup's "On the conditions for the vernal blooming of phytoplankton" (Sverdrup 1953). In the landmark paper, Sverdrup introduced the critical depth hypothesis linking water column structure to the development of blooms of phytoplankton. It was published about the same time and in the same journal as Steemann Nielsen's C¹⁴ paper. According to Google Scholar, Sverdrup's paper has been cited 2813 times in the period 1953–2024, and was cited 85 times in 2024, figures quite comparable to the citation data for Steemann Nielsen's C¹⁴ publication, given above. Here I posit that both Steemann Nielsen's 1952 and Sverdrup's 1953 paper, should be recognized as outstanding contributions of the *ICES Journal of Marine Science*, well deserving of recognition!

## Acknowledgments

Patrick Kociolek kindly supplied a copy of Steemann Nielsen's 1931 paper. The librarians of the ICES Secretariat very helpfully scanned and posted copies of articles in *Rapports et Procès-verbaux des Réunions* in the ICES digital library. The comments of the three reviewers resulted in great improvements. I am sincerely grateful for their efforts.

## Author contributions

John Dolan is solely responsible for all errors of fact, omission, and interpretation.

*Conflict of interest:* None declared.

## Data availability

Citation numbers by year (WoS and Google Scholar) are available upon request.

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Handling Editor: Howard Browman