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Risk and Resilience: Variations in Magnesium in Echinoid Skeletal Calcite

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Risk and Resilience: Variations in Magnesium in Echinoid Skeletal Calcite Vol. 561: 1–16, 2016 MARINE ECOLOGY PROGRESS SERIES Published December 15 doi: 10.3354/meps11908 Mar Ecol Prog Ser OPENPEN ACCESSCCESS FEATURE ARTICLE Risk and resilience: variations in magnesium in echinoid skeletal calcite Abigail M. Smith1,*, Dana E. Clark1,4, Miles D. Lamare1, David J. Winter2,5, Maria Byrne3 1Department of Marine Science, University of Otago, PO Box 56, Dunedin 9054, New Zealand 2Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand 3University of Sydney, New South Wales 2006, Australia 4Present address: Cawthron Institute, Private Bag 2, Nelson 7042, New Zealand 5Present address: Institute of Fundamental Sciences, Massey University, Private Bag 11 222, Palmerston North 4442, New Zealand ABSTRACT: Echinoids have high-magnesium (Mg) calcite endoskeletons that may be vulnerable to CO2- driven ocean acidification. Amalgamated data for echinoid species from a range of environments and life-history stages allowed characterization of the factors controlling Mg content in their skeletons. Pub- lished measurements of Mg in calcite (N = 261), sup- plemented by new X-ray diffractometry data (N = 382), produced a database including 8 orders, 23 families and 73 species (~7% of the ~1000 known extant spe- cies), spanning latitudes 77° S to 72° N, and including 9 skeletal elements or life stages. Mean (± SD) skeletal carbonate mineralogy in the Echinoidea is 7.5 ± 3.23 Magnesian calcite skeletons of the New Zealand endemic wt% MgCO3 in calcite (range: 1.5−16.4 wt%, N = 643). sea urchin Evechinus choloroticus may be vulnerable to Variation in Mg within individuals was small (SD = ocean acidification. 0.4−0.9 wt% MgCO3). We found significant differ- Photo: Chris Cornelisen, Cawthron Institute ences among skeletal elements: jaw demi-pyramids were the highest in Mg, whereas tests, teeth and spines were intermediate in Mg, but generally higher than larvae. Higher taxa have consistent mineralogical INTRODUCTION patterns, with orders in particular showing Mg related to first appearance in the fossil record. Latitude was a Ocean acidification, the result of ocean uptake of good proxy for sea-surface temperature (SST), although increasing pCO2 (Raven et al. 2005, IPCC 2014), is incorporating SST where available produced a slightly decreasing the saturation state of calcium carbonate, better model. Mg content varied with latitude; higher which, in many marine invertebrates, makes the pro- Mg content in warmer waters may reflect increased duction and maintenance of calcified structures more metabolic and growth rates. Although the skeletons of difficult (e.g. Orr et al. 2005). The effects of ocean some adult urchins may be partially resistant to ocean acidification on calcium carbonate saturation state acidification, larvae and some species may prove to be vulnerable to lowered pH, resulting in ecosystem will vary with depth and location, but general predic- changes in coastal marine environments. tions are for a 2- to 4-fold increase in both calcite and aragonite solubility in sea surface waters this cen- KEY WORDS: Carbonate mineralogy · Echinoidea · tury, with the aragonite saturation horizon (below Larvae · Skeletal morphology · Urchins · Ocean which aragonite can be expected to dissolve) reach- acidification ing the surface in at least the Southern Ocean by © The authors 2016. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 2 Mar Ecol Prog Ser 561: 1–16, 2016 ≈2050 (Orr et al. 2005, Fabry et al. 2008). Under- Although the skeleton of echinoderms is calcitic, its standing the response of marine calcifiers, in particu- solubility is closer to that of aragonite than pure lar their ability to make their skeletons and shells, to calcite (Dubois 2014). The solubility of Mg-calcite this major and rapid environ mental change requires increases with increasing Mg content, with calcite an understanding of skeletal carbonate mineralogy containing more than approximately 12 wt% MgCO3 across a range of phyla and at various life-history being more soluble than aragonite (Walter & Morse stages. 1984, Bischoff et al. 1987, Morse et al. 2006, Anders- Among these major marine calcifiers are those in son et al. 2008). Given the high Mg2+ content of the the phylum Echinodermata, with approximately 7000 sea urchin skeleton, the high solubility of the mineral known extant species and 13 000 extinct species, and form (Andersson et al. 2008) and the dominance of including the Class Echinoidea (sea urchins) with skeleton in the body wall, sea urchins are likely to be about 1000 known extant species distributed in the particularly vulnerable to the effects of ocean acid - world’s oceans (Kroh & Mooi 2011). Echinoids are ification. This is especially so for species in high- ecologically important marine invertebrates and are latitude and deep-sea environments because they considered to be the most important group of con- already inhabit seawater that is only slightly super- sumers living in shallow water (Steneck 2013). Lar- saturated with respect to the carbonate phase they val, juvenile and adult echinoids have an endoskele- secrete (Andersson et al. 2008, but see Dubois 2014). ton of calcite (CaCO3) produced by the mesoderm As ocean pH progressively declines, high-latitude and usually covered by the epidermis, with the calcifiers are increasingly vulnerable as concurrent exception of the spines of urchins in the order ocean warming will likely prevent them moving Cidaroida (Dubois 2014). The teeth are also directly toward the lower latitudes. Marine calcifiers that exposed to surrounding sea water and may contain deposit stable carbonate minerals such as calcite and the highest levels of magnesium (Mg) (Wang et al. low-Mg calcite may become increasingly dominant 1997). The skeleton is laid down as stereom, in a 3- (Andersson et al. 2008); this also applies to taxa (e.g. dimensional rhombohedral mesh-like calcite lattice sea stars) that are less calcified. Here we investigated (with more or less Mg substitution) with individual factors that may influence skeletal carbonate miner- elements being crystalline, a skeletal form unique to alogy, including water temperature, water chemistry, the Echinodermata that has its maximum develop- phylogeny and natural genotypic variation. ment in the Echinoidea (Smith 1980, Dubois & Chen We examined the skeletal mineralogy of sea urchins 1989, Cavey & Märkel 1994). Production, growth and from a broad range of latitudes, from 77° S to 72° N. In maintenance of this mesodermal skeleton is the a comprehensive literature review and incorporating result of intricate and detailed biochemical pathways new data from the Northern and Southern Hemi- (Wilt 1999, Matranga et al. 2013). Calcified skeletal sphere, we collated the mineralogy of 73 echinoid elements of adult echinoids include test plates, jaw species in 23 of the 50 currently recognized echinoid components (including teeth and pyramids) and families (Smith & Kroh 2011). Previous sampling ef- spines, both primary and secondary. The feeding forts had been concentrated in the Northern Hemi- echinopluteus larvae of most echinoids have a basket- sphere, and we address this gap by generating data shaped endoskeleton supporting the body and arm for specimens from the Southern Hemisphere. In ad- rods that support the larval arms (Emlet 1988, Kinjo dition, while a number of mineralogical studies have et al. 2006), which can be simple or fenestrated cal- been published on echinoids (Clarke & Wheeler 1922, cite rods, with the latter being more robust (Kinjo et Chave 1954, Pilkey & Hower 1960, Raup 1966, Weber al. 2006). 1969, Sumich & McCauley 1972, Bischoff et al. 1983, The skeletal elements of most echinoids are com- McClintock et al. 2011), lack of replication reported posed of Mg-calcite (≈3 to 16 wt% MgCO3; Chave means the variability in the measurements with and 1952, 1954, Raup 1966), where Mg2+ is substituted for between individuals cannot be assessed. For more Ca2+ during calcification. The Mg content of Mg- than half of the species studied (58%), apparently calcite varies with latitude in some marine calcifiers, only 1 specimen was examined. For 4 species, we including echinoderms (Chave 1954, Andersson et al. determined the mineralogy within individuals and 2008, McClintock et al. 2011, Lebrato et al. 2013). This among multiple individuals. We assimilated data from trend has been attributed to differences in growth body skeletal elements for species from a range of rate, carbonate saturation state and sea temperature environments and life-history stages, to characterize (e.g. Mackenzie et al. 1983, Andersson et al. 2008, their mineralogy and evaluate the factors controlling Hermans et al. 2010), all of which may be related. Mg content in their skeletons. Smith et al.: Mg in echinoid skeletal calcite 3 METHODS ternal standard halite peak, and then a machine- specific calibration for determining Mg content was A comprehensive literature review showed that 56 applied: y = 30x − 882, where y = wt% MgCO3 in cal- species (261 measurements) from (mostly) the North- cite and x = calcite peak position in °2θ (after Gray ern Hemisphere have had mineralogy measured and & Smith 2004). reported (Table S1 in Supplement 1 at www. int- res.com/articles/suppl/m561p001_supp1.pdf); where units varied, they were standardised to wt% MgCO3. Phylogenetic
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