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Inorganic Carbon OCB Workshop, Rutgers University 3-6th March 2019 “TowarDs a better understanding oF Fish contribution to carbon flux” FORMS OF CARBON - INORGANIC CARBON Gut production and excretion of calcium carbonate by marine fish Prof. Rod W. Wilson Biosciences, College of Life & Environmental Sciences [email protected] Marine Calcifiers (calcite or aragonite skeletons) coral reefs coralline algae …and now Fish BUT… coccolithophores Fish CaCO3 is not skeletal Pteropods Echinoderms(Bone is calcium phosphate) Photo by Peter Mumby, Exeter University foraminifera Modified from Dr. Toby Tyrell (NOC, Southampton) 1) Teleost Osmoregulation Physiology Seawater Ions (mM): (Why and How they do it…) Na+ ~ 470 Cl- ~ 550 2+ 2- Mg ~ 53 SO4 ~ 28 2+ Sea Water ~1050 mOsm/kg Ca ~ 10 K+ ~ 10 Salts H2O Blood ~330 mOsm/kg Compensatory Drinking (1-5 ml/kg/h) How? - Alkaline precipitation of ingested Ca2+ in the intestine - HCO3 secretion (intestinal cells) Ingestion of Ca2+ - rich seawater 2+ - Ca + 2HCO3 à CO2 + H2O + CaCO3 (and Mg2+) Excreted Intestinal Fluid Seawater CaCO3 pH 8.3-9.2 8.0-8.2 crystals - [HCO3 ] 30 to >100 mM 2 mM (and MgCO3) Pellets break down à high Mg calcite crystals (Perry et al., 2011 – PNAS; Salter et al., 2012,2014 – Sedimentology) Ellipsoidal Straw-bundle Dumbbell Semi-spheres Spheres < 1 µm 10-20 µm Great barracuda (Sphyraena barracuda) Body mass 13 kg ; 26 °C 50 ml tube Produced in 1 day Size-based Conservative estimate of fish CaCO3 production Macroecological = 40-110 million tonnes / year Model (Simon Jennings) (0.04-0.11 Pg CaCO3-C / year) = 3 to 15% of global CaCO3 production Less conservatively, but realistically = 3 x greater (9 to 45 %) Large Marine Ecosystems (LMEs) Model o In a warmer, higher CO2 future ocean (+ 4 C / 1000 µatm CO2) CaCO3 (Villy Christensen) Production (g m-2 year-1) Predict Fish CaCO3 Production will be > 70 % higher (Reardon, Cole, Stephens, Statton Taplin, & Wilson - in prep.) Wilson et al. (2009) Science 323: 359-362. Rapid dissolution of fish carbonates – may explain surface ocean chemistry phenomenon 0 (­ Total Alkalinity) 1 Fish Carbonates (High Mg calcites soluble at shallow depths?) 2 (Woosley et al (2012). J. Geophysical Sciences 117: C1048) Depth (km) Depth 3 CaCO + CO + H O è Ca2+ + 2HCO - Lysocline 3 2 2 3 (­ Total Alkalinity) (­ CaCO solubility) 4 3 Dissolution of carbonates at high Sedimentation pressure & low temperature 5 Wilson et al. (2009) Science 323: 359-362. BUT … Also evidence of fish carbonate preservation in sediments Cape Eleuthera Island The Bahamas - Warm - Shallow - Lots of fish ! Prof. Chris Perry (Geography, UoE) Ellipsoidal Fish carbonates in sediments of all 7 Bahamian habitats Dumbbells Bahamas Fish: 14 % of total CaCO3 mud production Splayed ellipsoidal Semi-spheres 70% contribution in some habitats (e.g. Mangroves) Perry et al. (2011) P.N.A.S. 108: 3865- Effect of Feeding on CaCO3 excretion rate: 1) Proportional to individual feeding rates 2) Mean rate is 10-fold higher than when starved 3) Substantial incorporation of precipitated phosphate 600 Juvenile sea bass 500 /kg/h) eq 400 300 (Sam Newbatt - PhD) 200 Excretion (µ Excretion 3 R² = 0.5917 100 CaCO 0 0 500 1000 1500 Food Consumption Rate (mg/kg/h) (Christine Stephens - PhD) Why does it matter? CaCO3 Dissolution ­ Alkalinity (Depth this occurs at important) Faecal CaCO3 content Phosphate Dissolution Sinking rate of faecal pellet ­ Nutrients (i.e. Organic C - POC) (Role in primary productivity?) Mesopelagic fish – Potential “Upward Alkalinity Pump” (­ Surface Alkalinity) Gut carbonates excreted near surface: 2+ - Ca + 2HCO3 ç CaCO3 + CO2 + H2O Production of gut carbonates at depth: (¯ Alkalinity at Depth) Diel Vertical Migration 2+ - Ca + 2HCO3 è CaCO3 + CO2 + H2O Roberts, C.M. et al. (2017). Marine reserves can Mitigate and proMote adaptation to cliMate change. P.N.A.S. doi: 10.1073/pnas.1701262114 20 species of mid-Atlantic mesopelagic teleost fish caught at 55 and 450 m Samples c/o Prof. Santiago Hernández León (Gran Canaria) & Dr. Stephanie Czudaj (Hamburg) Barbelled dragonfishes (Chauliodus sp.) All species had intestinal CaCO3 pellets Dr. Erin Reardon (Exeter) Giant hatchetfish, Argyropelecus gigas Acknowledgements EXETER: OUTSIDE EXETER: Prof. Chris Perry Martin Grosell (RSMAS, Miami, USA) Erin Reardon (PDRA) Frank Millero (RSMAS, Miami, USA) Jon Whittamore (PDRA) Simon Jennings (Cefas, UK) Chris Cooper (PDRA) Villy Christensen (UBC, Canada) Mike Salter (PDRA) Pat Walsh (Ottawa, Canada) NiCk Rogers (PhD student) Annabelle Oronti (CEI, Bahamas) Sam Newbatt (PhD student) Howard Jelks (US GeologiCal Survey, Gainesville, USA) Christine Stephens (PhD student) Stephen Crowley (Liverpool, UK) Louisa Taplin (MRes) Paul Halloran (UK Met OffiCe – now Exeter Geography) Chris Cobb (MSC) Ian Totterdell (UK Met OffiCe) JaCob Bill (MSc) Ben Booth (UK Met OffiCe) Jenna CorCoran (BSC) Jonathan Wilson (CIIMAR Porto & Wilfred Laurier, Canada) RebeCCa Crosta (BSC) Katie Statton (BSC) FUNDING: Jan Shears (TeCh) Grega Paull (ARC Manager) Jo Rabineau (TeCh) Kirsty Bolt (Tech) Eliane deBastos (TeCh) Karen Knapp (PhysiCs, X-Ray) Strategic Development Fund End Global Variation in Ocean Salinity http://aquarius.umaine.edu/cgi/gallery.htm Global Ocean Mean (35 psu) Effect of salinity on CaCO3 excretion Shanny Lipophrys pholis /kg/h) excretion 3 eq µ ( CaCO Measured: 30 35 40 Goldsinny wrasse Ctenolabrus rupestris 1.6 to 3.0 x ­ CaCO3 /kg/h) excretion excretion 3 eq µ (35 v. 40 psu) ( CaCO 30 35 40 Turbot Scopthalmus maximus /kg/h) excretion 3 eq µ ( CaCO (Christine Stephens – PhD work) 17 Two Ocean Carbon Cycles Organic Inorganic Carbon Pump Calcium Carbonate Pump CO2 CO2 Atmosphere 2+ - CO2 + H2O ® CH2O + O2 Ca + 2HCO3 ® CaCO3 + CO2 + H2O Surface OceanNet calcification reaction: 2+ - Ca + 2 HCO3 « CaCO3 + CO2 + H2O Confusion – Carbon sinK AND CO2 source! Calcite Soft & Aragonite Tissues Shells Deep Ocean 14,000 x 1018 g C 60,000 x 1018 g C (e.g. oil, coal etc.) (e.g. limestone, chalKs) Redrawn after Toby Tyrell (National Oceanography Centre, Southampton) 17 18 Two Ocean Carbon Cycles Organic Carbon Pump Inorganic Calcium Carbonate Pump CO2 CO2 Atmosphere 2+ - CO2 + H2O ® CH2O + O2 Ca + 2HCO3 ® CaCO3 + CO2 + H2O Surface Ocean 500-1000 years Calcite Soft & Aragonite Tissues Shells Deep Ocean 14,000 x 1018 g C 60,000 x 1018 g C (e.g. oil, coal etc.) (e.g. limestone, chalKs) Redrawn after Toby Tyrell (National Oceanography Centre, Southampton) 18 1) CaCO3 production rates by individual fish in laboratory: • increases exponentially with temperature • scales inversely with body size 3000 ) 1 - So smaller fish at warmer h 1 - 2500 temperatures produce the ) -1 most CaCO3 h -1 2000 mol C kg mol C µ mol C kg µ 1500 30 1000 25 20 Carbonate production production Carbonate ( 500 15 10 Carbonate Production ( 5 0 0 -2 0 2 4 log10 W (g) Log10 Body Mass (g) Normalized Total Alkalinity (µmol kg-1) 2280 2300 2320 2340 2360 0 Total alkalinity increases at much 500 shallower depths than predicted in Atlantic and Pacific oceans 1000 1500 Depth (m) 2000 Normalized total alkalinity of seawater as a function of depth for North Atlantic Waters (30 N and 23 E) 2500 Aragonite Saturation c/o Frank Millero, RSMAS, Miami, USA Expected Feely et al., Global Biogeochem. Cycles, 16, 1144 - (2002). 3000 Chung et al., Global Biogeochem. Cycles, 17, 1093 - (2003). doi: 10.1073/pnas.1701262114 21 Biogeochemical consequences of DSL depth variability Mesopelagic animals – Continuous Mesopelagic fish – Potential source of a novel ammonia excretion = novel role in N cycle “Upward Alkalinity Pump” (­ Surface Alkalinity) Gut carbonates excreted near surface (dissolution will enhance surface alkalinity): 2+ - Ca + 2HCO3 ç CaCO3 + CO2 + H2O (Wilson et al. 2009 – Science) + NH4 input from Diel Vertical Migrators Production of gut carbonates at depth: (¯ Alkalinity at Depth) Ammonia excretion (via gills) from diel vertical animal migration – previously overlooked role in anaerobic Migration Vertical Diel ammonium oxidation (Anammox) in deep ocean 2+ - Ca + 2HCO3 è CaCO3 + CO2 + H2O (Bianchi et al. 2014 – PNAS) High Pressures – Mesopelagic teleosts (0 to 1,000 m) Prof. Santiago Hernández León Dr. Stephanie Czudaj Instituto de Oceanografía y Cambio Global Institute of Sea Fisheries Universidad de Las Palmas de Gran Canaria Hamburg Spain Germany BIO Hesperides Cruise 2015 "Migrants and Active Flux In the Atlantic ocean" Fluid extracted from muscle of mesopelagic fish at 2 depths Epipelagic Zone Mesopelagic Zone (55 m depth) (450 m depth) (N = 8) (N = 38) [Na+] (mM) 91.7 ± 13.0 137.4 ± 9.0 P=0.032* [Cl-] (mM) 103.2 ± 14.1 159.7 ± 10.8 P=0.027* 3-4 individuals sampled from each of 10 species (order in parenthesis): Chauliodus cf. schmidti (Stomiiformes), Diaphus fragilis (Myctophiformes), Electron risso (Myctophiformes), Howella sherboni (Perciformes), Diretmus argenteus (Beryciformes), Ichthyococcus ovatus (Stomiiformes), Argyropelecus cf. sladeni (Stomiiformes), Argyropelecus affinis (Stomiiformes), Astronesthes cf. cyclophotus (Stomiiformes), cf. Bathylagus greyae (Clupeiformes) Effect of Temperature on CaCO3 excretion rate in marine fish Average Q10 for metabolic rate in fish = 1.83 (across 69 species, 0-30 °C) ClarKe & Johnson (1999) J. Anim. Ecol. 68, 893- Sheepshead Minnow Q10 = 6.40 (Cyprinodon variegatus) Common Goby Q10 = 4.49 (Pomatoschistus microps) Sea bass Q10 = 3.40 (Dicentrarchus labrax) European Flounder Q10 = 2.94 (Platichthys flesus) Turbot Q10 = 2.67 Scophthalmus maximus Shanny Q10 = 1.96 (Lipophrys pholis) (Reardon, Cole, Stephens, Statton Taplin, & Wilson - in prep.) Mean Q10 = 3.64 Elevated seawater CO2 increases gut CaCO3 excretion rate In a warmer and higher CO2 future ocean o (+ 4 C & 1000 µatm CO2) Predict gut CaCO3 to be > 70 % higher 2.50 (Reardon,3 Cole, Stephens, Statton Taplin, & Wilson - in prep.) 2.00 1.50 Mean reference (1.00-fold change) 1.00 = 47.1 ± 3.4 (µeq/kg/h) change in CaCO in change - Excretion Rate Rate Excretion 0.50 Fold 0.00 0 1000 2000 3000 4000 5000 Present Day Seawater CO2 (µatm) (400 µatm) (Cobb, Whittamore, Reardon, Rogers & Wilson - in prep.) Do all fish carbonates dissolve rapidly? 0 ? Sedimentation (­ Total Alkalinity) 1 Fish Carbonates (High Mg calcites soluble at shallow depths?) 2 (Woosley et al (2012).
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