Ocean acidification effects on Calanus

 Much recent research on zooplankton evaluates the effects of climate warming and of progressing carbonic acidification in both oceans and lakes. Oar Feet and Opal Teeth (OF&OT) summarizes the results of studies of copepod responses to century-scale acidity change (about -0.02 pH units per decade since 1985) as “reasonably resistant.” The book provided no review of that research, and one won’t fit in an “OarFeet.com” essay. However, I was attracted by a 2023 paper by David Fields, Jeff Runge, and eight colleagues: "A positive temperature-dependent effect of elevated CO₂ on growth and lipid accumulation in the planktonic copepod Calanus finmarchicus.”  Limnology and Oceanography 68: S87-S100. The title suggested that, for one copepod species at least, acidification could even be a good thing. For me the results also emphasize the accelerated patterns of copepod development and growth, a recurring source of interest for my career.

            Their study was experimental. They worked in April 2015 with those eight colleagues at Astevoll Research Station in SW Norway. Calanus finmarchicus were raised in all four combinations of 12° and 16°C with ~600 “ambient” and 1100 “high” matm pCO₂, each with three replicates. The lower pCO₂  water was from the adjacent fjord (pH 7.91); the more acidic (pH 7.64) was sustained by recurring additions of “stock” seawater sustained at still lower pH. Those were to represent present and possible end-21^st century atmospheric CO₂ levels. Recall that pH units are [-1 x logarithms of fractional concentrations]. Thus, reduction by ~0.27 pH units equals an increase of ~86% in H+ (hydrogen ion, as H₃CO₃  molarity), which is a lot. Those ions also convert some CO₃⁺⁺ (carbonate) to bicarbonate (HCO₃⁺). That is known to affect calcifying in molluscs, like pteropods, and corals more than for crustaceans (though not copepods, with no calcite or aragonite parts). Other crustacea may be able to harden their shells using bicarbonate.

            All treatment groups at Astevoll were held, with replete phytoplankton nutrition (>600 mg C L^-1) for all stages, in 40-liter tanks with slow, in- and out-filtered water replacement of 5 to 12 L per hour, assuring good oxygenation. Stocking was with 10,000 to 15,000 eggs per tank from field-collected females (same sources for all treatments, but many mothers, and staggered hatching times). Development (N1 to C6 adults) was assessed daily from samples counted for stage abundance. As fifth copepodites (C5) appeared, they were sorted into separate holding chambers. Many were measured and subsets weighed, oil sac volume quantified, and others were checked for oxygen consumption. The emphasis of checking newly molted specimens recognized that on molting from C4, the C5 weights would be minimal and lengths nearly final after drinking to expand to the C5 exoskeletons fully. Other C5s were then held separately and fed until their maturation molt.

Stage to stage development results were displayed in a graph I particularly like, their Figure 1, hence this essay. It is shown below. Every day of development to C5, the numbers-weighted estimates of the “running” mean stage number (N1=1, N2=2, …, C1-7, C2=8, … , C5=11) are plotted versus the age at which that culture’s mean stage was first reached. The temperature contrast is shown with orange shades (16ºC) and blue (12ºC) points. Variations between temperature and pCO₂ levels are represented by the scatter of shape-coded points around the impressively close polynomial lines. The graph represents stage-to-stage progress of copepod development started from eggs spawned by multiple females and over several days before (and then after) hatching. An older way of getting at the sequence of stage durations in copepod cultures is covered in OF&OT, pages 242-248, a method Runge et al. (2016) applied in an earlier paper. That was slick enough, but the new data plotting allows four different culture conditions, each replicated three times, all to fit in one eye-socking presentation:

Figure 1. From Fields et al (2023). Reproduction here is allowed by Open Access publication. As expected, development was faster at 16° than at 12°C. Symbols for pCO₂ levels all pack closely along the polynomial trend lines, which isn’t necessarily “expected,” but important to know. More details in text here.

 

After a couple of faster early molts (N1 to N2 to N3, when eating starts) intermolt intervals are roughly constant up to N6. That is, stage-to-stage molting of individuals (and of the whole culture in a bucket) is essentially “isochronal” (an old term long argued over). Averaged over all the buckets, constant average proportions of the stages are both added and later advanced by developmental progress. Early copepodites also develop in almost this explicitly “isochronal” fashion to C4, with the duration of stages longer than for nauplii. Biomass growth of stages before C5, if evaluated, was not reported in this paper.

Other work, see Figure 12.13 on OF&OT page 248 (borrow it from a library if you cannot afford the excessive price), which shows results from William Peterson for Calanus marshallae reared on replete rations at 10°C. In at least that species, probably all Calanus species, dry weight (DW) increases exponentially from N4 to C5. That is, each new stage adds new tissue equal to a constant fraction of biomass at the stage before. According to Peterson’s text, the overall rate was 0.73 mg DW added per µg DW from N4 to C5. Copepods grow impressively fast, probably attaining some fast-as-possible upper limit. There must be survival benefit to getting bigger fast. Very old data show that when food is limiting development proceeds anyway at nearly the fully-fed rates. Other old data show that actual food-limitation of Calanus growth in the ocean is uncommon.

 

What was the “positive temperature-dependent effect of elevated CO₂ on growth and lipid accumulation” mentioned in the paper’s title? That possibly positive effect was what drew me to the paper. The notice in the title is followed in the abstract by “The observations suggest that elevated pCO₂/lower pH in future oceans may have a beneficial effect [italics mine] on C. finmarchicus.” All the clearly identified effects of elevated pCO₂ were evident from data for C5 and females raised at 12ºC. Chapter 15 of OF&OT reviews diapause in C. finmarchicus. Major proportions of its stocks do enter diapause as C5 (some as C4 and C6 females) at temperatures around 11° or 12°C, departing for rest at various depths across the North Atlantic. So, 16°C would be very warm for catching C. finmarchicus. Nevertheless, it is interesting to know that development rate is not obviously affected at 16°C by pH as low as 7.64, which, barring serious action on global carbon emissions, is expected to be widely reached in temperate seas by 2100. 

The positive 12ºC results were for biomass (DW) and oil sac volumes of newly molted C5 and C6-females. Raised at either pH, neither stage was significantly longer at molt: C5 from lower pH had mean prosome lengths 2.0 vs higher 2.1 mm, and C6 2.4 vs 2.4 mm. However, those raised at lower pH were heavier:  somewhat for C5, 113 vs 94 µg dry weight with overlapping standard deviations. Similarly, for C6, dry weights were 221 vs. 175 µg. Measures of body carbon differed in the same directions. Mass in both treatments included the mass of wax secretion into the oil sacs (see a Neocalanus example of a calanid oil sac in OF&OT Fig. 1.2). So, the team also compared photo estimates of the oil sac volumes:    0.041 vs 0.029 mm³ comparing lower vs higher pH for C5; and 0.078 vs 0.056 mm³ for C6.

Mean oxygen consumption rates for C5 copepodites averaged ~1.8 O₂/L/hr/µg body carbon at 16º and 600 µatm pCO₂ and ~1.4 at 1100 µatm. At 12 ºC the difference was in the same direction, ~0.9 vs. ~0.6, at lower and higher pCO₂, respectively. Less oxygen uptake at colder temperatures is expected, as is finding more general metabolism above the normally inhabited range. Why doubling pCO₂ would reduce bulk metabolism (O₂ uptake down about a third) is a question, and available and reasonable hypotheses are reviewed by the authors. Invoking an OarFeet.com limit on essay length, I refer you to their Discussion. They also drew attention to lower metabolic costs possibly allowing the 41% greater C5 oil sac content at 12ºC and lower pCO₂.

The fatty acids of lipids extracted from both sexes were evaluated by author Michael Arts, but the results either are not presented separately, or a chunk of the caption explaining the results presented in Fig. 7 did not get printed. It is clear enough that (1) most of the specimens evaluated were close to the modal fatty acid ratios, while (2) some specimens from 12ºC varied from the modal bunch in different directions: relatively more of several 18-carbon fatty acids, with different double bond numbers at different positions, vs 16:0 fatty acids at high pCO₂, and less at low pCO₂. More cis-double bonds could reduce compressibility of oil sac wax, thus stabilizing buoyancy some better between the deep depths of diapause.

 Overall, if there is a benefit of greater pCO₂, it will have to compete with concern for seriously negative acidification effects on other marine life. Those are most obvious for aragonitic reef corals and pteropod shells that are particularly prone to dissolution by weak acid. The larval shells of many marine molluscs (snails, oysters, clams) are formed of aragonite, not the calcite of shells in later stages. Moreover, secretion of calcite shells depends in on abundant carbonate ion, and acidification converts substantial fractions of that to less directly useful bicarbonate. It is a great service from Fields, et al. to demonstrate the growth effects of acidification on marine copepods, which matter ecologically. It is a longer jump to call those “benefits.” What seems to me the most hopeful result of the warmer experiments is that C. finmarchicus, a high-temperate species, can develop completely at 16ºC and despite likely greater ocean acidity in the next century.

 

References:

Fields, D.M., J.A. Runge, C.R.S. Thompson, C.M.F. Durif, S. D. Shema, R.K. Bjelland, M. Niemisto, M.T. Arts, A. B. Skiftesvik, H.L. Browman (2023). TITLE IN TEXT. Limnology and Oceanography 68: S87-S100 (In a special L&O issue on ocean acidification.

Peterson, W.T. (1986) Development growth and survivorship of the copepod Calanus marshallae in the laboratory. Marine Ecology Progress Series 29: 61-72.

Runge, J.F., D.M. Fields, C.R.S. Thompson, S.D. Shema, R.K. Bjelland, C.M.F. Durif, A. B. Skiftesvik, H.I. Broman (2016). End of the century CO₂ concentrations do not have a negative effect on vital rate of Calanus finmarchicus, an ecologically critical planktonic species in North Atlantic ecosystems. ICES Journal of Marine Science 73: 937-850.