Seasonal variation in physiology and shell condition of the pteropod Limacina retroversa in the Gulf of Maine relative to life cycle and carbonate chemistry

Abstract

Natural cycles in the seawater partial pressure of carbon dioxide (CO2) in the Gulf of Maine, which vary from ~250-550 µatm seasonally, provide an opportunity to observe how the life cycle and phenology of the shelled pteropod Limacina retroversa responds to changing food, temperature and carbonate chemistry conditions. Distributional, hydrographic, and physiological sampling suggest that pteropod populations are located in the upper portion of the water column (0-150 m) with a maximum abundance above 50 m, allowing them to generally avoid aragonite undersaturation. Gene expression and shell condition measurements show, however, that the population already experiences biomineralization stress in the winter months even when aragonite is slightly oversaturated, reinforcing the usefulness of this organism as a bio-indicator for pelagic ecosystem response to ocean acidification. There appear to be two reproductive events per year with one pulse timed to coincide with the spring bloom, the period with highest respiration rate, fluorescence, and pH, and a second more extended pulse in the late summer and fall. During the fall there is evidence of lipid storage for overwintering, allowing the second generation to survive the period of low food and aragonite saturation state. Based on these observations we predict that in the future pteropods will likely be most vulnerable to changing CO2 regionally during the fall reproductive event when CO2 concentration already naturally rises and there is the added stress of generating lipid stores.

Effects of Ocean Acidification on Calcification of the Sub-Antarctic Pteropod Limacina retroversa

“…Here, geneexpression analysis showed that genes linked to calcification were upregulated, presumably to counter a further reduction of the calcification rate. A similar finding was recorded for natural populations of North Atlantic L. retroversa, where lower shell condition and upregulation of biomineralization genes was found in response to seasonally lower Ar state (Maas et al, 2020). Hence, lower shell weight of sub-Antarctic L. retroversa in near-future conditions likely indicates that the organisms are less able to maintain calcification rates when exposed to more acidified conditions.…”

“…The first generation is produced in austral spring, when a rapid increase in size is essential to reach fertility and produce offspring for the second generation in late summer (Dadon and de Cidre, 1992;Seibel et al, 2007). The same applies to L. retroversa in the Gulf of Maine, where the phytoplankton spring bloom is thought to enable rapid growth of the juvenile pteropods (Maas et al, 2020). We mimicked a scenario of high food abundance in our experiments, by successfully feeding the incubated pteropods with microalgae (as shown by bright-green stomach contents and mucous webs) and all pteropods were still swimming lively after 3 days.…”

The impacts of past, present and future ocean chemistry on predatory planktonic snails

“…If atlantids reach reproductive maturity in approximately 116 days, this could allow for more than one generation per year. This is comparable to the shelled pteropods, which are thought to live for approximately 1-2 years and may produce two generations of offspring per year in the Southern Ocean [96,97], and in more temperate waters [98]. During specimen collection in the South Atlantic Ocean for the present study, small juvenile and large adult specimens were present in the same location at the same time, supporting this inference.…”

Sea butterflies in a pickle: Reliable biomarkers and seasonal sensitivity of pteropods to ocean acidification in the Gulf of Maine

“…Pteropod shells are made of a more soluble calcium carbonate compound (aragonite) than the form used by most planktonic species, and are impacted at a higher saturation state (ΩAr =1.5) than would be predicted from pure chemical equilibrium (ΩAr =1.0), the point at which aragonite is predicted to dissolve (Bednarsek et al, 2019), suggesting that their shell condition could serve as an "early warning" of OA impacts for other shelled species. Natural phenology and seasonal cycles have, however, been demonstrated to influence phenotypic responses of thecosomes to OA (León et al, 2020;Maas et al, 2020), confounding and potentially obscuring the correlations between saturation state and the gene expression, respiration, and shell condition of these potential bioindicators. A metanalysis of the response metrics was only able to find consensus on thresholds of response (Bednarsek et al, 2019), rather than develop consistent predictive relationships between saturation state and a response variable.…”