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. 2021 Jan 18;11(1):1731.
doi: 10.1038/s41598-021-81131-9.

Pteropods make thinner shells in the upwelling region of the California Current Ecosystem

Lisette Mekkes  1   2 , Willem Renema  3   4 , Nina Bednaršek  5   6 , Simone R Alin  7 , Richard A Feely  7 , Jef Huisman  4 , Peter Roessingh  4 , Katja T C A Peijnenburg  8   9
Affiliations

Pteropods make thinner shells in the upwelling region of the California Current Ecosystem

Lisette Mekkes et al. Sci Rep. .

Abstract

Shelled pteropods are widely regarded as bioindicators for ocean acidification, because their fragile aragonite shells are susceptible to increasing ocean acidity. While short-term incubations have demonstrated that pteropod calcification is negatively impacted by ocean acidification, we know little about net calcification in response to varying ocean conditions in natural populations. Here, we examine in situ calcification of Limacina helicina pteropods collected from the California Current Ecosystem, a coastal upwelling system with strong spatial gradients in ocean carbonate chemistry, dissolved oxygen and temperature. Depth-averaged pH ranged from 8.03 in warmer offshore waters to 7.77 in cold CO2-rich waters nearshore. Based on high-resolution micro-CT technology, we showed that shell thickness declined by ~ 37% along the upwelling gradient from offshore to nearshore water. Dissolution marks covered only ~ 2% of the shell surface area and were not associated with the observed variation in shell thickness. We thus infer that pteropods make thinner shells where upwelling brings more acidified and colder waters to the surface. Probably the thinner shells do not result from enhanced dissolution, but are due to a decline in calcification. Reduced calcification of pteropods is likely to have major ecological and biogeochemical implications for the cycling of calcium carbonate in the oceans.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Aragonite saturation along the northern California Current Ecosystem. (a) Map representing the aragonite saturation horizon, defined as the depth at which ΩAr = 1, between May 28th and June 7th of 2016. Waters with ΩAr < 1 are considered undersaturated. Limacina helicina pteropods were sampled from 11 stations, indicated by open and closed symbols for offshore and nearshore stations, respectively. (b–d) Depth distributions of (b) ΩAr, (c) pHT, and (d) temperature (°C), along the offshore-onshore gradient from locations A to B indicated on the map. Each dot in (b–d) indicates a sampling point, and stations 80 and 84 are indicated by vertical lines. Undersaturated conditions (ΩAr < 1) come close to the surface in nearshore waters and deepen offshore.
Figure 2
Figure 2
Relationships among ocean variables and average shell thickness of L. helicina pteropods. (a) Principal Component Analysis (PCA) based on aragonite saturation (ΩAr), pCO2, pH, temperature (Temp), oxygen (O2) and chlorophyll fluorescence. The numbers within the plot represent the sampling stations used for analyses. Circles indicate stations with strong upwelling conditions nearshore (grey), and with less intense upwelling conditions offshore (white), see also Fig. 1. PC1 explains 83.0% of the variation among stations, and essentially reflects the offshore-onshore gradient driven by coastal upwelling. PC2 explains 11.9% of the variation, and is largely driven by variation in chlorophyll fluorescence. (b) Average shell thickness decreased significantly with PC1, associated with the upwelling gradient (principal component regression: y =  − 0.595 PC1 + 10.671; R2 = 0.487, N = 11, p = 0.010). (c) Average shell thickness did not vary significantly with PC2, associated with chlorophyll fluorescence (principal component regression: R2 =  − 0.058, N = 11, p = 0.519). Each dot in (b,c) represents the mean ± SD of average shell thickness calculated over all 6–8 individuals per station. PC axes in the biplot (a) were scaled according to Gabriel (1971), whereas PC axes in (b,c) are unscaled.
Figure 3
Figure 3
Variation in shell thickness measured by micro-CT scans of two Limacina helicina specimens. (a) A thick shell sampled offshore (station 101). (b) A thin shell sampled onshore (station 99). Coloring indicates shell thickness, with brighter colors for thicker areas. (c,d) Frequency distribution of shell thickness of the two specimens. These frequency distributions were used to calculate average thickness per shell.
Figure 4
Figure 4
Shell images obtained by light microscopy, micro-CT and scanning electron microscopy (SEM) of eight Limacina helicina specimens illustrating the variability in our data set. (a) Specimens with a thick shell (upper row) and a thin shell (lower row) without dissolution marks. (b) Specimens with a thick shell and a thin shell showing marks of initial dissolution (Type I), with pitting at the inner whorl (indicated by arrows). (c) Specimens with a thick shell and a thin shell with Type II marks of dissolution penetrating the aragonite structure. (d) Specimens with a thick shell and a thin shell with Type III dissolution, characterized by deep damage on the outer shell surface. All images in the same row are of the same specimen.
Figure 5
Figure 5
Percentage surface area with dissolution marks (%) and average shell thickness of the individual shells. Each dot represents an individual pteropod shell analyzed for both average shell thickness and dissolution marks. Circles indicate individuals from nearshore stations with strong upwelling conditions (grey), and offshore stations with less intense upwelling conditions (white). See Fig. 4 for examples of dissolution marks, Fig. S5 for specific graphs of the three different dissolution types, and Fig. S8 for an illustration of the calculation method.
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