Determining how biotic and abiotic variables affect the shell condition and parameters of <i>Heliconoides inflatus</i> pteropods from a sediment trap in the Cariaco Basin

Abstract

Abstract. Pteropods have been nicknamed the “canary in the coal mine” for ocean acidification because they are predicted to be among the first organisms to be affected by changing ocean chemistry. This is due to their fragile, aragonitic shells and high abundances in polar and subpolar regions where the impacts of ocean acidification are most pronounced. For pteropods to be used most effectively as indicators of ocean acidification, the biotic and abiotic factors influencing their shell formation and dissolution in the modern ocean need to be quantified and understood. Here, we measured the shell condition (i.e., the degree to which a shell has dissolved) and shell characteristics, including size, number of whorls, shell thickness, and shell volume (i.e., amount of shell material) of nearly 50 specimens of the pteropod species Heliconoides inflatus sampled from a sediment trap in the Cariaco Basin, Venezuela, over an 11-month period. The shell condition of pteropods from sediment traps has the potential to be altered at three stages: (1) when the organisms are live in the water column associated with ocean acidification, (2) when organisms are dead in the water column associated with biotic decay of organic matter and/or abiotic dissolution associated with ocean acidification, and (3) when organisms are in the closed sediment trap cup associated with abiotic alteration by the preservation solution. Shell condition was assessed using two methods: the Limacina Dissolution Index (LDX) and the opacity method. The opacity method was found to capture changes in shell condition only in the early stages of dissolution, whereas the LDX recorded dissolution changes over a much larger range. Because the water in the Cariaco Basin is supersaturated with respect to aragonite year-round, we assume no dissolution occurred during life, and there is no evidence that shell condition deteriorated with the length of time in the sediment trap. Light microscope and scanning electron microscope (SEM) images show the majority of alteration happened to dead pteropods while in the water column associated with the decay of organic matter. The most altered shells occurred in samples collected in September and October when water temperatures were warmest and when the amount of organic matter degradation, both within the shells of dead specimens and in the water column, was likely to have been the greatest. The hydrographic and chemical properties of the Cariaco Basin vary seasonally due to the movement of the Intertropical Convergence Zone (ITCZ). Shells of H. inflatus varied in size, number of whorls, and thickness throughout the year. There was not a strong correlation between the number of whorls and the shell diameter, suggesting that shell growth is plastic. H. inflatus formed shells that were 40 % thicker and 20 % larger in diameter during nutrient-rich, upwelling times when food supply was abundant, indicating that shell growth in this aragonite-supersaturated basin is controlled by food availability. This study produces a baseline dataset of the variability in shell characteristics of H. inflatus pteropods in the Cariaco Basin and documents the controls on alteration of specimens captured via sediment traps. The methodology outlined for assessing shell parameters establishes a protocol for generating similar baseline records for pteropod populations globally.

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

“…Notably, we collected the thinnest shells at the onshore station with the highest chlorophyll fluorescence (station 99). This is in contrast to previous studies, which reported that increased food availability enhanced calcification in bivalves 38 and pteropods 27 , 39 , 40 . During spring, at the onset of the upwelling season, phytoplankton blooms in the productive waters of the CCE are commonly found close to shore and are often patchy 41 .…”

“…For instance, comparison of historical (from 1921) and modern samples of the pteropod Styliola subula demonstrated that shells had become thinner with a decrease in pH in the Mediteranean Sea 26 . Shell thickness has thus been proposed as a useful indicator of the effect of environmental change across various temporal scales 26 , 27 .…”

“…Here, we examine the variability in net calcification of L. helicina pteropods along the upwelling gradients of the CCE, characterized by a combination of parameters, including low pH and Ω Ar , low temperature, low oxygen and high p CO 2 . We measured shell thickness of 80 individuals as a proxy of net calcification using micron-scale computed tomography (micro-CT), a high-resolution X-ray technique that provides detailed 3D information on the shell 25 – 27 . In addition, the extent of dissolution on the outer surface of the same shells was examined through Scanning Electron Microscopy (SEM) to assess to what extent dissolution level impacts shell thickness.…”

Current and future ocean chemistry negatively impacts calcification in predatory planktonic snails

“…Similar trends have been found in other calcifying organisms, including pteropods 43 , corals 44,45 and the early benthic stages of the bivalve mollusc Mytilus edulis 46 . The pteropod Heliconoides inflatus was found to produce shells that were 40% thicker and 20% larger in diameter during periods of naturally high nutrient concentrations in the Cariaco basin (compared to specimens sampled during oligotrophic conditions) 43 . A review of OA studies on calcifying marine organisms found that an intermediate or high food supply increased the resistance to low pH for growth and calcification 47 .…”

Using the Stable Isotopic Composition of Heliconoides inflatus Pteropod Shells to Determine Calcification Depth in the Cariaco Basin

“…Sediment trap samples were collected every 2 weeks, supplemented by measurements of hydrography and water chemistry on monthly oceanographic cruises. The planktic foraminifera from the CARIACO timeseries have been used extensively to study seasonal and interannual population changes, and changes in the isotopic composition, temperature, and carbonate concentration of seawater (e.g., Black et al, 2001;Tedesco and Thunell, 2003;Tedesco et al, 2007;McConnell et al, 2009;Marshall et al, 2013Marshall et al, , 2015Davis et al, 2019), however, there has only been one study on pteropods from the Cariaco Basin (Oakes and Sessa, 2020). The wealth of samples, hydrographic measurements, and previous studies of calcareous plankton, makes the Cariaco Basin the ideal place to develop pteropods as oceanographic proxies.…”