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UC Davis UC Davis Previously Published Works UC Davis UC Davis Previously Published Works Title The oyster enigma variations: A hypothesis of microbial calcification Permalink https://escholarship.org/uc/item/8kn6h5dg Journal Paleobiology, 40(1) ISSN 0094-8373 Author Vermeij, GJ Publication Date 2014-12-01 DOI 10.1666/13002 Peer reviewed eScholarship.org Powered by the California Digital Library University of California The oyster enigma variations: a hypothesis of microbial calcification Author(s): Geerat J. Vermeij Source: Paleobiology, 40(1):1-13. 2013. Published By: The Paleontological Society DOI: http://dx.doi.org/10.1666/13002 URL: http://www.bioone.org/doi/full/10.1666/13002 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Paleobiology, 40(1), 2014, pp. 1–13 DOI: 10.1666/13002 The oyster enigma variations: a hypothesis of microbial calcification Geerat J. Vermeij Abstract.—Oysters, whose inner shell layer contains chambers, vesicles, and sometimes chalky deposits, often have extraordinarily thick shells of large size, prompting the idea that there is something unusual about the process of shell fPormation in these and similarly structured bivalves with the oyster syndrome. I propose the hypothesis that calcifying microbes, especially sulfate-reducing bacteria growing on organic substrates in fluid-filled shell-wall chambers, are responsible for shell calcification away from the shell-secreting mantle of the host bivalve. Other phenomena, including the formation of cameral deposits in fossil cephalopods, the cementation of molluscs and barnacles to hard substrata, the formation of a calcified intriticalx on the shell’s exterior, and cementation of objects by gastropods on the shell for camouflage, may also involve calcifying bacteria. Several lines of inquiry are suggested to test these hypotheses. Geerat J. Vermeij. Department of Geology, University of California, Davis, California 95616, U.S.A. E-mail: [email protected] Accepted: 9 July 2013 Published online: 27 September 2013 Introduction Chinzei 1986, 2013; Kirby 2001; Titschack et The British composer Edward Elgar (1857– al. 2010). 1934) could have been thinking about the The only bivalves rivaling oyster-like spe- cies in valve thickness are some taxa known or many bizarre, unexplained phenomena that inferred to harbor photosymbionts (fossil confront scientists when he wrote his Enigma megalodontids, alatoconchids, some Jurassic Variations. In the realm of evolutionary pinnids, an Eocene cardiid, and living tridac- biology, these phenomena often represent nine giant clams) as well as cool-temperate extreme variations on familiar themes that Permian bivalves of the Australian genera we claim to understand. Extremes can be Eurydesma and Myonia (Runnegar 1979; Ver- thought of either as the inevitable endpoints of meij 2013). Very large bivalves (length 200 mm a statistical distribution or as the outcomes of or more) with chemosymbionts (some sole- unusual circumstances or processes. Our myids, bathymodioline mytilids, vesicomyids, interpretation of extremes represents a tension Cretaceous myoconchids, and fossil Cenozoic between description and explanation, between lucinids) have thin to moderately thick shells what makes something possible and what (maximum thickness 28 mm in a Late Creta- propels it into existence. ceous species of the myoconchid Capsiconcha Among shell-bearing animals, one of those [see Kelly et al. 2000]). The same applies to enigmaticextremesisthevastsizeand very large bivalves that are known or pre- thickness of the shell of bivalves exhibiting sumed to lack symbionts, including some what I call the oyster syndrome, the condition living mytilids, pectinids, deep-sea limids, in which the inner layer of the shell contains pteriid pearl oysters, fossil Bakevelliidae and chambers, vesicles, and secondary mineral Isognomonidae, living pinnids, placunids, and precipitates referred to as chalky deposits or deep-burrowing mactrids, hiatellids, and pho- mocret (Malchus 1990). Oysters exceeding a ladomyids. In photosymbiotic bivalves, great shell height of 130 cm and a valve thickness of valve thickness may be enabled by a positive up to 10 cm are known from shallow-water feedback between calcification in the host and marine settings in many locations from the photosynthesis by the guests. An explanation Late Cretaceous (Cenomanian) onward (Ste- for exceptional thickness in bivalves with the phenson 1952; Sohl and Kauffman 1964; oyster syndrome must therefore focus on shell Ó 2014 The Paleontological Society. All rights reserved. 0094-8373/14/4001-0001/$1.00 2 GEERAT J. VERMEIJ calcification rather than on the production of other outstanding issues related to the geo- nonskeletal biomass. logical history of calcification. The aim of this Given that thick-shelled oysters are known unabashedly exploratory exercise is to awaken from open marine environments (Kirby 2001) interest by microbiologists in evolutionary as well as from dark unproductive caves and problems of great environmental importance deep-water rock walls (Hayami and Kase and not to test the hypothesis rigorously. 1992; Wisshak et al. 2009), the oyster syn- drome requires an explanation that does not Materials and Methods depend on the presence of photosymbionts. In order to document valve sizes and Moreover, as I shall show below, the oyster thicknesses of bivalves with and without the enigma and its variations extend to many oyster syndrome, I measured valve lengths other calcification-related phenomena as well. (longest linear dimensions) and thicknesses of An understanding of this enigma is therefore thick-shelled Late Cretaceous to Recent bi- of great interest in view of biomineralization valves at the Florida Museum of Natural processes in general and of the unparalleled History (abbreviated UF), and complemented rate of acidification (which interferes with these measurements with data from the calcification) in today’s ocean waters in taxonomic literature and my own collections. particular (Kump et al. 2009; Zeebe 2012). Particular attention was focused on oysters An understanding of any evolutionary (Ostreoidea), Spondylidae, Malleidae, Arci- enigma requires two complementary ap- dae, Chamidae, and Veneridae. For each proaches. One is an investigation of the species and site, I selected the individual with potential benefits of the phenomenon in the thickest valve. In addition, I surveyed question. This approach in turn entails the Miocene to Recent regional bivalve faunas identification of selective agents or agencies based on the taxonomic literature and my and knowledge of how they work to produce collections in order to ascertain where and the purported benefits. Complementing this when bivalves with the oyster syndrome were line of inquiry is an explanation of how the the thickest-shelled species in the assemblage. selected trait or benefit comes about phyloge- Taxonomic assignments for Cenozoic and netically, developmentally, physiologically, living oysters follow Harry (1985) and Bolton and mechanically. Without ignoring the first and Portell (2013). of these approaches, I emphasize the second, with the aim of proposing a hypothesis about The Oyster Syndrome how the unusual thickness and pattern of I define the oyster syndrome as the condi- calcification in bivalves with the oyster syn- tion in which the shell is porous and light- drome are achieved. weight thanks to the presence of vacuoles, In this speculative paper, I briefly review the chambers, vesicles, and sometimes chalky morphological peculiarities, phylogenetic and deposits (or mocret) in the inner layer of the geological distribution, and dimensions of shell wall. This condition is best exemplified bivalves with the oyster syndrome. I then by Late Triassic to Recent oysters (Ostreoidea) develop the hypothesis, first suggested but not (Harry 1985; Chinzei 1986, 1995, 2013; Mal- elaborated on by Chinzei and Seilacher (1993), chus 1990; Chinzei and Seilacher 1993; Car- that microbes housed inside the valves en- riker 1996; Hautmann 2001; Kirby 2001). hance calcification and make great size and In oysters that have them, chalky deposits valve thickness possible. Specifically, I argue may represent cases of calcification not direct- that sulfate-reducing bacteria, known to be ly controlled by the inner mantle surface. involved in calcification in other contexts, are Chalky deposits in the living oyster Crassostrea the responsible agents. I speculate that micro- virginica consist of bladelike structures orient- bial assistance in skeleton formation and ed perpendicular to the inner shell surface, cementation is widespread among sedentary where the blades are separated by
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