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Fish As Major Carbonate Mud Producers and Missing Components of the Tropical Carbonate Factory

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Fish As Major Carbonate Mud Producers and Missing Components of the Tropical Carbonate Factory Fish as major carbonate mud producers and missing components of the tropical carbonate factory Chris T. Perrya,1, Michael A. Saltera, Alastair R. Harborneb, Stephen F. Crowleyc, Howard L. Jelksd, and Rod W. Wilsonb,1 aSchool of Science and the Environment, Manchester Metropolitan University, Chester Street, Manchester M1 5GD, United Kingdom; bBiosciences, College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4PS, United Kingdom; cDepartment of Earth and Ocean Sciences, University of Liverpool, 4 Brownlow Street, Liverpool L69 3GP, United Kingdom; and dUS Geological Survey, 7920 North West 71st Street, Gainesville, FL 32653 Edited* by George N. Somero, Stanford University, Pacific Grove, CA, and approved January 6, 2011 (received for review November 2, 2010) Carbonate mud is a major constituent of recent marine carbonate nite and Mg-calcite mud-grade carbonate occur and thus budget- sediments and of ancient limestones, which contain unique records ary considerations need to accommodate production from a of changes in ocean chemistry and climate shifts in the geological range of potential sources. This issue has important geo-environ- past. However, the origin of carbonate mud is controversial and mental implications because carbonate muds are major constitu- often problematic to resolve. Here we show that tropical marine ents of limestones and are volumetrically important in most fish produce and excrete various forms of precipitated (nonskele- modern shallow marine carbonate environments (17). Further- tal) calcium carbonate from their guts (“low” and “high” Mg-calcite more, the presence of Mg-calcite muds in marine carbonates is and aragonite), but that very fine-grained (mostly <2 μm) high Mg- considered critical to preserving primary sediment textures and > calcite crystallites (i.e., 4 mole % MgCO3) are their dominant ex- fabrics (15), thus influencing sediment porosity and permeability cretory product. Crystallites from fish are morphologically diverse which are of critical importance to fluid flow in limestone and species-specific, but all are unique relative to previously known sequences. Mud production in ancient limestones has proven par- biogenic and abiotic sources of carbonate within open marine ticularly perplexing because evidence is often lacking for the pre- systems. Using site specific fish biomass and carbonate excretion sence of species that are regarded as key modern mud producers ∼ × 6 ∕ rate data we estimate that fish produce 6.1 10 kg CaCO3 year (especially the calcareous green algae) (18). across the Bahamian archipelago, all as mud-grade (the <63 μm Recent observations of carbonate crystals growing within, and fraction) carbonate and thus as a potential sediment constituent. being continually excreted from, the intestines of temperate fish Estimated contributions from fish to total carbonate mud produc- species (19) lead us to speculate that such crystals could represent tion average ∼14% overall, and exceed 70% in specific habitats. a hitherto unrecognized source of mud-grade carbonate in shal- Critically, we also document the widespread presence of these dis- low tropical marine environments. In these shallow marine envir- tinctive fish-derived carbonates in the finest sediment fractions onments carbonate production rates are typically high and from all habitat types in the Bahamas, demonstrating that these preservation potential is good because of high carbonate satura- carbonates have direct relevance to contemporary carbonate tion states in the overlying waters. The process by which fish pre- sediment budgets. Fish thus represent a hitherto unrecognized cipitate carbonate crystals within their guts has been documented – but significant source of fine-grained carbonate sediment, the in some detail (19 22) and occurs within the teleosts (bony fish) discovery of which has direct application to the conceptual ideas that dominate the marine fish fauna. Briefly, precipitation occurs of how marine carbonate factories function both today and in as a by-product of the osmoregulatory requirement of teleosts the past. to continuously drink Ca- and Mg-rich seawater. Subsequent intestinal bicarbonate secretion generates exceptionally high con- − – marine teleost ∣ fish intestine ∣ carbonate production centrations of HCO3 (50 100 mM) and very high pH values (up to 9.2) which leads to the alkaline precipitation of calcium arine carbonates contain unique records of changes in and magnesium within ingested seawater as insoluble carbonates along the intestine (19–24; Fig. 1). Carbonate precipitation is ocean chemistry, biogeochemical cycling, and benthic and M believed to occur within the mucus that is secreted along the en- pelagic ecology (1), and therefore provide vital information tire length of the intestinal lumen (21, 23, 24), and carbonates are on climate shifts in the geological past. A distinctive and often subsequently excreted within mucus-coated pellets. Following volumetrically important component of these sediments is carbo- their excretion the rapid degradation of the organic mucus matrix nate mud (the <63 μm sediment fraction). However, the origins is assumed to release inorganic crystals into the water column of both aragonitic and Mg-calcite carbonate muds remains a topic (19). Whilst the physiological processes driving fish carbonate GEOLOGY of long-standing debate (2, 3). Indeed, where attempts have been production are thus increasingly well understood, the morpholo- made to quantify sources of the fine sediment fraction a high pro- gical characteristics of such carbonates and their sedimentologi- portion remains of unknown origin (e.g., up to 40% in Bahamian cal significance have never been considered. sediments and between 28 and 36% in Belize lagoon sediments) (4, 5). This problem arises in part because, with the exception of Results and Discussion inorganic carbonate precipitation (e.g., the carbonate “whiting” In order to study the morphological and compositional character- controversy) (3, 6–8), the processes of carbonate mud production istics of carbonates produced by tropical marine fish, carbo- necessarily invoke the degradation of larger bioclasts (skeletal fragments of marine organisms) to produce mud-grade carbo- PHYSIOLOGY nate, and/or grain recrystallization to produce high Mg-calcite Author contributions: C.T.P. and R.W.W. designed research; C.T.P., M.A.S., A.R.H., and – R.W.W. performed research; H.L.J. contributed new reagents/analytic tools; C.T.P., muds (9 11). Thus attempts to determine primary mud sources M.A.S., A.R.H., S.F.C., and R.W.W. analyzed data; and C.T.P., M.A.S., A.R.H., S.F.C., and and production budgets are often hampered because of grain R.W.W. wrote the paper. obliteration. The mineralogical composition of the mud fraction The authors declare no conflict of interest. of modern tropical carbonate sediment is also very variable *This Direct Submission article had a prearranged editor. between settings: in some environments the finest sediment frac- 1To whom correspondence may be addressed. E-mail: [email protected] or r.w.wilson@ tions are predominantly aragonite (12, 13), but high Mg-calcite ex.ac.uk. can account for in excess of 40% of the mud fraction in many This article contains supporting information online at www.pnas.org/lookup/suppl/ settings (14–16). Ultimately variable admixtures of both arago- doi:10.1073/pnas.1015895108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1015895108 PNAS ∣ March 8, 2011 ∣ vol. 108 ∣ no. 10 ∣ 3865–3869 Downloaded by guest on September 24, 2021 Fig. 1. Fish carbonate production and precipitation products. Schematic diagram illustrating the processes associated with carbonate precipitation within the intestines of fish and the dominant crystallite morphologies iden- tified in this study to be produced by tropical fish species. nate samples were obtained from 11 common fish species (see SI Appendix) collected from shallow water sites on the Eleuthera Bank, Bahamas (SI Appendix: Fig. S1). This area was selected for study as it combines warm, shallow waters that are supersaturated with respect to CaCO3, and comprises a range of typical carbo- nate platform sedimentary environments. The mucus-coated Fig. 2. Common morphologies of tropical fish-produced carbonate precipi- pellets excreted from fish guts that contain the carbonate preci- tates. (A) Type 1—Ellipsoidal crystallites (size range: <0.25 to 3 μm long); (B)Type2—Straw-bundle crystallites (size range: 1–3 μm long); (C)Type3 pitates vary in shape and size with fish species (SI Appendix: — – μ Fig. S2), but subsequent degradation of the organic mucus phase Polycrystalline dumbbell-shaped aggregates (size range: typically 1 3 m long, but large examples to ∼10–15 μm also occur); (D) Type 4—Polycrystal- in the laboratory, through dilute hypochlorite treatments (see line spheroidal aggregates (size range: <10 to 30 μm diameter). Occur both as SI Appendix), releases inorganic carbonate pellets up to 2 mm discrete spheres and as multilobate aggregations of spheres; (E) Large poly- in size. Each pellet comprises huge numbers of individual crystal- crystalline aggregates with a semisphere morphology (size range: ∼5 to lites and polycrystalline precipitates (in most cases estimated at ∼30 μm diameter); (F) Elongate rod-like crystallites which often occur as >106 per pellet; SI Appendix: Fig. S2), along with an amorphous intergrown bundles of crystallites (size range: 2–3 μm long); (G) Splayed ∼2 μ “matrix” of finer (<0.25 μm) carbonate. When
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