Guest commentary from Jim Acker (GSFC/Adnet)
Research on the ocean carbonate cycle published in 2019 supports results from the 1980s – in contrast to many papers published since then.
During my graduate school education and research program in the 1980s, conducted at the Department of Marine Science (now the College of Oceanography) of the University of South Florida in St. Petersburg, I participated in research on the production (biogenic calcification) and fate of calcium carbonate (CaCO3) in the open waters of the northern Pacific ocean. There were two primary aspects of this research: one, to measure the sinking flux of biogenic materials in the water column of the Pacific Ocean, and two, to measure the dissolution rates of aragonite, a CaCO3 crystal structure (polymorph) formed by pteropods, under in situ conditions of temperature, pressure, and seawater chemistry.
Prior to this period, most estimates of the sinking flux of particles, organisms, and pieces of organisms had been made through the use of bottom-moored sediment traps deployed for weeks or months before recovery of their collected contents. Our research group, instead, used free-floating sediment traps attached to floats at the surface and deployed for very short periods of time, 24-36 hours. A primary reason for the free-floating method was that the sediment traps would move with the water currents at their deployment depth, reducing potential effects of current flow that might happen around a stationary moored trap. The free-floating traps were much bigger than moored traps, consisting of fiberglass cones about 4 meters high, with a capture area about a meter across.
To sum up, our research results were remarkably at odds with prior results. We found that pteropods dominated the sinking flux of biogenic CaCO3 at all depths deployed (100, 400, 900, and 2100 meters). The organisms to which the main mass of sinking CaCO3 had been previously attributed, sand-grain size foraminifera and microscopic coccolithophores (both composed of calcite), were minor constituents in our trap collections.
Aragonite is important because this crystal form is more soluble in seawater than calcite. So if the aragonite flux was much larger than the calcite flux, the standard concepts at that time regarding the formation and particularly dissolution of CaCO3 in the water column would be markedly changed. This is vital to characterize, because the absorption of increasing amounts of anthropogenic carbon dioxide (CO2) from the atmosphere causes ocean acidification, and this ongoing process would dissolve considerably more aragonite than calcite as the chemistry of the water column changed. My dissolution experiments also showed the likelihood of substantial dissolution of pteropod shells while they were sinking, especially in the north Pacific Ocean where corrosive waters occur at shallow depths (only hundreds of meters), compared to a couple of kilometers deep in the Atlantic. Up until then, most of the dissolution of biogenic CaCO3 had been thought to occur after the sinking particles reached the seafloor – out of reach of the immediate effects of ocean acidification.
So our results were published (Betzer et al. 1984 and Byrne et al. 1984), and were even accompanied by a commentary piece in Nature (“Surprise from the shallows” by Michael Whitfield of the Plymouth Marine Laboratory), in which he discussed how our results were fairly revolutionary. We found support for our results from papers by Robert Berner of Yale, in which he had postulated the aragonitic pteropods were likely to be an important component of the sinking flux of biogenic CaCO3. (Berner, R. A., 1977, Berner and Honjo 1981).
Thus, after getting my Ph.D., due to the historic impact of these papers in overturning cherished tenets of chemical oceanography, I had to consider offers from several prestigious oceanographic institutions. So I moved on to academic fame and tenured fortune.
About a year after our papers were published, a paper appeared criticizing our results (Harbison and Gilmer 1986), indicating that the biological behavior of pteropods, which are free-swimming zooplankton, could have caused “overtrapping” of the organisms. In addition to the possibility that they just swam into the trap, pteropods feed by creating a net of mucus that captures organic particles, and they reel in the net to ingest the particles. When disturbed, pteropods cut the net and sink. So the paper suggested that if they were disturbed by a trap floating underneath them, they would cut the net and sink into it. Thus, the derived suggestion for doing sediment trap collections of sinking biogenic CaCO3 was to basically toss out any possible swimmers and not measure them at all. With few exceptions, this has been the unwritten but accepted protocol of sediment trap measurements of sinking CaCO3 flux since the 1980s. Other papers generally supported these results, so estimates of both planktonic calcification and the global sinking CaCO3 flux were based on the mass of foraminifera and coccolithophores.
However, during the period between then and now, there were indications that this might not be quite right. In particular, accurate measurements of the alkalinity (mainly bicarbonate and carbonate ion concentration, and a little borate ion) of seawater globally, from depth to surface, indicated that there was probably a good amount of CaCO3 dissolution taking place at shallow depths, even shallower than the saturation horizons for calcite and aragonite. This was peculiar both because of calcite’s resistance to dissolution, and because estimates of planktonic mass just didn’t provide a lot of CaCO3. And it turns out that some pteropod species, especially the thin-shelled polar species Limacina helicina, are important prey species in the polar oceans, including for fish like herring and larval salmon. If there is enough of them to keep the fish fed, one would think that there is enough of them to have some effect on seawater chemistry when they sink and dissolve.
A couple of weeks ago, I was responding to a tweet about pteropods with a don’t-you-forget-about-us tweet citing our 1984 papers. I happened to look at the online version of the paper, which due to the wonders of technology now provided links to recently published papers citing it. I noticed that one of these papers, Buitenhuis et al., was published in 2019, so I took a look, expecting the citation of our work would be a polite afterthought. The “Plain Language Summary” is shown below.
“We show that pteropods contribute at least 33% to export of CaCO3 at 100m and up to 89% to pelagic calcification. This is in line with results by Betzer et al., 1984 and Byrne et al., 1984, and contradicts most of the work that has been published since then, which has tended to argue for the dominance of either coccolithophores or foraminifers. Pteropods precipitate CaCO3 in the crystal form of aragonite. This is more soluble than calcite, which is produced by coccolithophores and pelagic foraminifers. Thus, the ocean alkalinity cycle and associated buffer capacity for CO2 could be more sensitive to rising CO2 than has been suggested by existing Earth System Models, which only represent calcite.”Buitenhuis et al. (2019)
To put it mildly, I was intrigued. Actually, I jumped up and down in the hallway while pumping my fists and shouting. Fortunately it was late in the workday. I immediately emailed my co-major professor Robert Byrne, and in the grand tradition of triumphantly pithy statements, stated “We wuz RIGHT!” (He promised to tell my other major professor, Peter Betzer.)
So, what was done in this paper? Erik Buitenhuis of the Tyndall Centre for Climate Change Research and the University of East Anglia, and his co-authors, added the three main groups of planktonic calcifiers to a sophisticated biogeochemical model of the oceans. The model runs provided estimates of both the planktonic mass and the sinking fluxes resulting from it. So pteropods, essentially zeroed out before this, are suddenly responsible for nearly 90% of the total amount of open water CaCO3 formation the global surface waters. And more importantly, the sinking flux, where they were also zeroed out, now requires about 1/3 aragonite and 2/3 calcite, with aragonite the more soluble, and thus more sensitive, crystal form.
Three combined constraints – observations of pteropod biomass concentrations, pteropod growth rates, and aragonite production rates – meant that the model requires much more planktonic calcification overall than previous estimates, and also requires substantial dissolution shallower than the saturation horizon, where seawater is supersaturated with respect to CaCO3. Because it is undersaturated waters that are corrosive, you may wonder how that can happen. There are a couple of pathways – ingested prey can be dissolved in the guts of the predator, resulting in the excretion of highly alkaline fecal material, or when the organisms die, bacterial respiration will acidify the organic matter of the soft parts, essentially dissolving the shells from within. Also, pteropods vertically migrate, and in the polar Pacific, they can vertically migrate into undersaturated water, potentially causing shell damage such as that seen in Figure 2.
However, there is one other aspect to this whole story. While not accounting entirely for the alkalinity distribution in the oceans, measurements can get much closer to the models if pteropods are not excluded from sediment trap collections! There is support for this altered protocol, cited in the paper. I will also add, anecdotally, that we collected empty pteropod shells at the deeper depths of our trap deployments, including a pristine Clio pyramidata shell. This shell, which looks like a spaceship designed by Santiago Calatrava, has the same mass of a lot of foraminifera and a whole lot of coccolithophores. There was no reason, in my mind, to exclude the mass of empty pteropod shells from quantitative assessments.
Buitenhuis is currently working out the implications of this publication, particularly the impact on the oceanic alkalinity cycle and the global ocean sink for CO2. A greater mass of aragonite in surface waters and in the sinking flux could substantially change our understanding of the dynamics of the oceanic response to the effects of the absorbing more CO2. In fact, the pteropods may have bought us a little more time to react, if in the prophetic words of Michael Whitfield they “might act as a more rapid and effective sink for fossil-fuel CO2 than had been thought possible when attention was focussed on the dissolution of calcite from the ocean sediments”. Feedbacks of the changing alkalinity cycle can also affect the rate of ocean acidification, especially in shallower waters where acidification may detrimentally influence the life cycle of important seafood risotto constituents like crab and clams.
Which leaves us at the present. At the AGU Ocean Sciences meeting in San Diego, in February, there will be a couple of sessions about the carbonate cycle of the North Pacific Ocean. One of the chairpersons, Richard Feely of NOAA, was the principal investigator on the research cruises in the 1980s that I participated on (and a valued co-author, too). Though Erik Buitenhuis (who no longer flies due to his personal concerns about climate change) won’t be there, one of his co-authors, Nina Bednarsek, will be co-chairing these sessions and also giving a presentation prominently featuring pteropods, which have been the subject of much of her research.
I wish I could be there too. But thanks to these new research results, in essence, I think that my co-authors and I are already in attendance.
- P.R. Betzer, R.H. Byrne, J.G. Acker, C.S. Lewis, R.R. Jolley, and R.A. Feely, "The Oceanic Carbonate System: A Reassessment of Biogenic Controls", Science, vol. 226, pp. 1074-1077, 1984. http://dx.doi.org/10.1126/science.226.4678.1074
- R.H. Byrne, J.G. Acker, P.R. Betzer, R.A. Feely, and M.H. Cates, "Water column dissolution of aragonite in the Pacific Ocean", Nature, vol. 312, pp. 321-326, 1984. http://dx.doi.org/10.1038/312321a0
- R.A. Berner, "Sedimentation and Dissolution of Pteropods in the Ocean", The Fate of Fossil Fuel CO2 in the Oceans, pp. 243-260, 1977. http://dx.doi.org/10.1007/978-1-4899-5016-1_14
- R.A. Berner, and S. Honjo, "Pelagic Sedimentation of Aragonite: Its Geochemical Significance", Science, vol. 211, pp. 940-942, 1981. http://dx.doi.org/10.1126/science.211.4485.940
- G. Harbison, and R. Gilmer, "Effects of animal behavior on sediment trap collections: implications for the calculation of aragonite fluxes", Deep Sea Research Part A. Oceanographic Research Papers, vol. 33, pp. 1017-1024, 1986. http://dx.doi.org/10.1016/0198-0149(86)90027-0
- E.T. Buitenhuis, C. Le Quéré, N. Bednaršek, and R. Schiebel, "Large Contribution of Pteropods to Shallow CaCO 3 Export", Global Biogeochemical Cycles, vol. 33, pp. 458-468, 2019. http://dx.doi.org/10.1029/2018GB006110