Effects of seawater Mg²⁺/Ca²⁺ ratio and diet on the biomineralization and growth of sea urchins and the relevance of fossil echinoderms to paleoenvironmental reconstructions

Abstract

It has been argued that skeletal Mg/Ca ratio in echinoderms is mostly governed by Mg 2+ and Ca 2+ concentrations in the ambient seawater. Accordingly, well-preserved fossil echinoderms were used to reconstruct Phanerozoic seawater Mg 2+ /Ca 2+ ratio. However, Mg/Ca ratio in echinoderm skeleton can be affected by a number of environmental and physiological factors, the effects of which are still poorly understood. Notably, experimental data supporting the applicability of echinoderms in paleoenvironmental reconstructions remain limited. Here, we investigated the effect of ambient Mg 2+ /Ca 2+ seawater ratio and diet on skeletal Mg/Ca ratio and growth rate in two echinoid species (Psammechinus miliaris and Prionocidaris baculosa). Sea urchins were tagged with manganese and then cultured in different Mg 2+ /Ca 2+ conditions to simulate fluctuations in the Mg 2+ /Ca 2+ seawater ratios in the Phanerozoic. Simultaneously, they were fed on a diet containing different amounts of magnesium. Our results show that the skeletal Mg/Ca ratio in both species varied not only between ossicle types but also between different types of stereom within a single ossicle. Importantly, the skeletal Mg/Ca ratio in both species decreased proportionally with decreasing seawater Mg 2+ /Ca 2+ ratio. However, sea urchins feeding on Mg-enriched diet produced a skeleton with a higher Mg/Ca ratio. We also found that although incubation in lower ambient Mg 2+ /Ca 2+ ratio did not affect echinoid respiration rates, it led to a decrease or inhibition of their growth. Overall, these results demonstrate that although skeletal Mg/Ca ratios in echinoderms can be largely determined by seawater chemistry, the type of diet may also influence skeletal geochemistry, which imposes constraints on the application of fossil echinoderms as a reliable proxy. The accuracy of paleoseawater Mg 2+ /Ca 2+ calculations is further limited by the fact that Mg partition coefficients vary significantly at different scales (between species, specimens feeding on different types of food, different ossicle types, and stereom types within a single ossicle).

Impact of seawater Mg2+/Ca2+ on Mg/Ca of asterozoan skeleton – Evidence from culturing and the fossil record

“…Decreased magnesium concentration in sea water also affects the expression of skeletogenic genes (Martino et al, 2019) and magnesium concentration in the sea urchin tooth skeleton has an effect on the mechanical properties of calcite (Ma et al, 2008(Ma et al, , 2009. Low ambient Mg 2+ /Ca 2+ is also known to slow down calcification rates in sea urchins (Prionocidaris baculosa and Psammechinus miliaris; Kołbuk et al, 2020). Magnesium deprivation was expected to be also harmful for other echinoderms, including asterozoans.…”

“…Although the seawater composition has the prevalent role in echinoderm biomineralization, the ultimate skeletal Mg/Ca ratio is a result of a complex interplay between environmental and physiological factors. In echinoids, the Mg/Ca ratio in the stereom differs on several organizational levels, e.g., between orders, families, species, or on an individual scale (i.e., significant variation is detected between different ossicles within a single specimen or even within one ossicle; see Discussion in Gorzelak et al 2013;Kołbuk et al, 2020). Other echinoderm classes, such as asteroids and ophiuroids, also display a wide range of Mg/Ca ratios, on higher taxonomic levels such as orders and families (Weber, 1969); additional variation can also occur between species (Duquette et al, 2018) from similar environmental conditions.…”

“…Firstly, the specimens were labeled with manganese. Despite being widely used in biomineralization studies (e.g., Hawkes et al, 1996;Barbin et al, 2008;Lartaud et al, 2010), manganese only recently gained attention as a reliable labeling tool for echinoderms (Gorzelak et al, 2017;Kołbuk et al, 2020). Nonetheless, its efficiency in tagging asterozoan skeletons has not yet been determined.…”

“…To date, studies investigating the effect of seawater Mg 2+ /Ca 2+ on the skeletal Mg/Ca in echinoderms focused on sea urchins. It has been experimentally shown that under lowered Mg 2+ /Ca 2+ ratio certain species of echinoids (including cidaroids: Eucidaris tribuloides, Prionocidaris baculosa, and euechinoids: Paracentrotus lividus, Psammechinus miliaris) produce skeleton with decreased Mg/Ca ratio (Ries, 2004;Kołbuk et al, 2019Kołbuk et al, , 2020.…”

“…Accordingly, it has been suggested that Mg/Ca ratio in well-preserved fossil echinoderms constitutes a reliable proxy for the seawater composition (Mg 2+ /Ca 2+ ratio) in the Phanerozoic era (Dickson, 2002(Dickson, , 2004Ries, 2004;Hasiuk and Lohmann, 2010). However, experimental studies on some sea urchins showed that magnesium in their skeletons can also originate from diet (Asnaghi et al, 2014;Kołbuk et al, 2019Kołbuk et al, , 2020, imposing constraints on the application of fossil echinoderms as a reliable paleoseawater Mg 2+ /Ca 2+ proxy. Furthermore, the skeletal Mg/Ca ratio in echinoderms can be also affected by temperature, salinity (Chave, 1954;Weber, 1969Weber, , 1973Borremans et al, 2009;Hermans et al, 2010) and physiological (vital) effects (Hermans et al, 2011).…”