Fish carbonates - their nature and fate within the marine inorganic carbon cycle

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

This proposal is based on a fundamentally important and previously unexpected change to our understanding of the marine inorganic carbon cycle. It follows our recent revelation that calcium carbonates excreted by fish make a significant contribution but our current estimates vary over more than a 10-fold range (3 to 45 % of global marine carbonate). BACKGROUND: As humans burn more fossil fuels, atmospheric concentrations of the 'greenhouse gas' carbon dioxide (CO2) rise contributing to climate change. Atmospheric CO2 is in balance with CO2 dissolved in the oceans, in something referred to as the marine-atmospheric carbon cycle. Whatever happens to CO2 in the oceans, will ultimately have an effect on CO2 in the atmosphere, and hence can influence global climate. When CO2 dissolves in seawater, it forms bicarbonate ions. An important part of the marine-atmospheric carbon cycle is the reaction of this bicarbonate with seawater calcium to produce a solid precipitate of white calcium carbonate (the mineral found in limestone). These precipitates are very dense, and sink to the ocean bottom in a continuous 'rain' of white crystals. The rate at which they form and sink (or re-dissolve) is important in the marine carbon cycle. The majority of calcium carbonate is generated by marine life that promotes this reaction to make a hard protective 'shell'. The most famous organisms involved in this 'biogenic' calcification are corals. However, those thought to produce the most are actually microscopic phytoplankton called coccolithophores that live in the open ocean. Dense skeletons of these and other microscopic organisms are normally considered to be the only important source of marine carbonates. Scientists collect samples in deep ocean traps, to measure this carbonate 'rainfall' for use in computer models of the carbon cycle. We have recently discovered that marine fish also produce substantial amounts of precipitated calcium carbonate, but for a very different purpose. They produce it in their intestines, by drinking large volumes of seawater and actively promoting the reaction of seawater calcium with bicarbonate ions that are produced by their own metabolism. Fish then excrete the precipitated calcium carbonate into the surrounding seawater, where it probably mixes with all the better known (planktonic) sources. In fact, some tropical fish will excrete calcium carbonate equivalent to its own dry body weight every year! We have conservatively estimated that the contribution of fish may be up to 45% of the total global carbonate production. This novel discovery suggests that fish also contribute to the marine carbon cycle, but scientists who model this cycle have never previously taken this into account. Indeed, the unusual chemistry of fish carbonates (which are more soluble than carbonate from more traditional sources), may explain a phenomenon that has puzzled oceanographers for decades - the rapid dissolution of 'apparently insoluble' carbonates in the upper layers of the ocean. Our research is a multi-disciplinary project that for the first time aims to precisely model how much calcium carbonate is produced by marine fish under different environmental conditions and determine its fate within in our oceans. This will also help with predictions about how carbonate excretion by marine fish will be affected by future environmental changes, such as temperature and CO2. We predict that fish will become even more important in this regard in the future, whereas marine plankton will become less important. Thus a precise understanding of this fish contribution to the global marine carbon cycle is both a novel and environmentally important topic.

Publications

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Cooper CA (2014) Osmoregulatory bicarbonate secretion exploits H(+)-sensitive haemoglobins to autoregulate intestinal O2 delivery in euryhaline teleosts. in Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology

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Middlemiss KL (2016) Effects of seawater alkalinity on calcium and acid-base regulation in juvenile European lobster (Homarus gammarus) during a moult cycle. in Comparative biochemistry and physiology. Part A, Molecular & integrative physiology

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Perry CT (2011) Fish as major carbonate mud producers and missing components of the tropical carbonate factory. in Proceedings of the National Academy of Sciences of the United States of America

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Roberts CM (2017) Marine reserves can mitigate and promote adaptation to climate change. in Proceedings of the National Academy of Sciences of the United States of America

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Roderic Wilson (Author) (2011) A fishy tale - a missing part of the inorganic ocean carbon cycle in The Biochemist

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Schmitz O (2013) Animating the Carbon Cycle in Ecosystems

 
Description We are refining our estimates of the (unexpected) role of fish globally in the marine inorganic carbon cycle. Fish appear to be one of the major producers of calcium carbonate. This is a big surprise to most ocean scientists. We have also revealed some new insights to the unusual chemistry of carbonates produced by fish. This new understanding dramatically affects our understanding of how carbonates will behave in the oceans in terms of their sinking and dissolution rates.
Exploitation Route The Met Office will be taking the final outputs of our research (next year) and incorporating these into their models of the ocean carbon cycle.
Sectors Energy,Environment

 
Description AquaLeap: Innovation in Genetics and Breeding to Advance UK Aquaculture Production
Amount £1,700,000 (GBP)
Funding ID BB/S004300/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 01/2019 
End 12/2021
 
Description COST Short Term Scientific Mission (STSM)
Amount € 1,660 (EUR)
Funding ID COST-STSM-FA1004-11324 
Organisation European Cooperation in Science and Technology (COST) 
Sector Public
Country European Union (EU)
Start 08/2012 
End 08/2012
 
Description NERC Standard grant
Amount £461,688 (GBP)
Funding ID NE/K003143/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 08/2013 
End 07/2017
 
Description Mesopelagic fish carbonates (Atlantic) - Institute of Sea Fisheries, Hamburg 
Organisation University of Hamburg
Department Institute for Hydrobiology and Fisheries Science
Country Germany 
Sector Academic/University 
PI Contribution Samples of the gut contents of mesopelagic fish from the mid Atlantic (see below) were obtained from freshly thawed fish at Exeter. Otoliths were also be sampled together with organic tissue (white muscle) to provide comparison of the carbonate chemistry within otoliths and intestinal carbonates, and to compare stable isotopes signatures of C and O in future work. Dr. Erin Reardon processed the samples for analysis of the carbonate crystal structure and elemental composition (using ion chromatography, SEM and TEM with EDS analysis, and also XRD/FTIR for mineralogy). This was funded through an Exeter University Strategic Development Fund (SDF) grant.
Collaborator Contribution Through collaboration with Stephanie Czudaj, mesopelagic fish were sampled at a wide range of depths (surface to 1000 m deep) in the mid Atlantic by collaborators from Gran Canara during a multi-national research cruise project based in the Atlantic - "Migrants and Active Flux In the Atlantic ocean" in the early part of 2015. Samples were frozen to preserve gut carbonate content and then shipped on dry ice to Exeter once the ship returned to port.
Impact Data still being analysed. No outputs yet, but a NERC grant (Large or Standard) is anticipated. Also, this pilot data has contributed towards Rod Wilson being a joint applicant PI in a NERC Research Programme ("The Changing Arctic Ocean: implication for marine biology and biogeochemistry") grant led by Prof. Andrew Brierley (St. Andrews) on "Foodweb consequences In a changinG ARctic Ocean for plankton, predators and fisheries (FIGARO)". The total value of this grant is estimated to be £2.1M and the deadline for submission is mid March 2016.
Start Year 2014
 
Description Mesopelagic fish carbonates (Atlantic) - Universidad de Las Palmas de Gran Canaria and Institute of Sea Fisheries Hamburg 
Organisation University of Las Palmas de Gran Canaria
Department Institute of Oceanography
Country Spain 
Sector Academic/University 
PI Contribution Samples of the gut contents of mesopelagic fish from the mid Atlantic (see below) were obtained from freshly thawed fish at Exeter. Otoliths were also be sampled together with organic tissue (white muscle) to provide comparison of the carbonate chemistry within otoliths and intestinal carbonates, and to compare stable isotopes signatures of C and O in future work. Dr. Erin Reardon processed the samples for analysis of the carbonate crystal structure and elemental composition (using ion chromatography, SEM and TEM with EDS analysis, and also XRD/FTIR for mineralogy). This was funded through an Exeter University Strategic Development Fund (SDF) grant.
Collaborator Contribution Through collaboration with Prof. Santiago Hernández León (Instituto de Oceanografía, Universidad de Las Palmas de Gran Canaria), mesopelagic fish were sampled at a wide range of depths (surface to 1000 m deep) in the mid Atlantic by collaborators from Gran Canara during a multi-national research cruise project based in the Atlantic - "Migrants and Active Flux In the Atlantic ocean" in the early part of 2015. Samples were frozen to preserve gut carbonate content and then shipped on dry ice to Exeter once the ship returned to port.
Impact Data still being analysed. No outputs yet, but a NERC grant (Large or Standard) is anticipated. Also, this pilot data has contributed towards Rod Wilson being a joint applicant PI in a NERC Research Programme ("The Changing Arctic Ocean: implication for marine biology and biogeochemistry") grant led by Prof. Andrew Brierley (St. Andrews) on "Foodweb consequences In a changinG ARctic Ocean for plankton, predators and fisheries (FIGARO)". The total value of this grant is estimated to be £2.1M and the deadline for submission is mid March 2016.
Start Year 2014
 
Description Mesopelagic fish carbonates (Red Sea) - KAUST University, Saudi Arabia 
Organisation King Abdullah University of Science and Technology (KAUST)
Country Saudi Arabia 
Sector Academic/University 
PI Contribution Samples of the gut contents of mesopelagic fish from the Red Sea (see below) were obtained from freshly thawed fish at Exeter. Otoliths were also be sampled together with organic tissue (white muscle) to provide comparison of the carbonate chemistry within otoliths and intestinal carbonates, and to compare stable isotopes signatures of C and O in future work. Dr. Erin Reardon processed the samples for analysis of the carbonate crystal structure and elemental composition (using ion chromatography, SEM and TEM with EDS analysis, and also XRD/FTIR for mineralogy). This was funded through an Exeter University Strategic Development Fund (SDF) grant.
Collaborator Contribution Through collaboration with Drs. Fanny Debusserolles, Xabier Irigoien and Anders Rostad at KAUST, mesopelagic fish were sampled at maximum and minimum depths in the Red Sea by collaborators at KAUST using their ship facility. Samples were frozen to preserve gut carbonate content and then shipped on dry ice to Exeter.
Impact Data still being analysed. No outputs yet, but a NERC grant (Large or Standard) is anticipated. Also, this pilot data has contributed towards Rod Wilson being a joint applicant PI in a NERC Research Programme ("The Changing Arctic Ocean: implication for marine biology and biogeochemistry") grant led by Prof. Andrew Brierley (St. Andrews) on "Foodweb consequences In a changinG ARctic Ocean for plankton, predators and fisheries (FIGARO)". The total value of this grant is estimated to be £2.1M and the deadline for submission is mid March 2016.
Start Year 2014
 
Description Can Fish Fight Back? Carbonate Production in an Acidic Ocean 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact My talk was to a mixed audience of pubic, university personnel (undergrads, postgrads, researchers and academics) and local government environmental policy makers. This took place at the University of Washington, Seattle, USA. The talk was part of a series on "Ocean Acidification - Effects on Fisheries and Oceans". The impact of my talk was to spark a range of questions from all sectors of the audience and debate about the previously unrecognised role of fish in the global inorganic carbon cycle. This has far reaching implications for how we model the marine carbon cycle and climate predictions.

My talk and the debate afterwards resulted in many comments that the understanding and views of both scientists working on climate change and the carbon cycle in particular, as well as the general public, had been challenged by listening to the main messages of my talk. A video recording of my talk was available online following the free public seminar, so others were able to access this internationally.
Year(s) Of Engagement Activity 2011
URL http://depts.washington.edu/donbevan/2011/wilson.html
 
Description Can fish influence Earth's climate control? The surprising role of marine fish in the global carbon cycle 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach International
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact An invited talk to scientists and the media as part of the "Science with Impact" opening session at the Society for Experimental Biology conference in Salzburg, Austria, in July 2012. Debate and public/scientific discussion was the main result.

An invited plenary talk at the start of a scientific conference that was designed to engage the public, media, and policymakers/politicians in addition to the regular scientific community.
Year(s) Of Engagement Activity 2012
 
Description Fish carbonates: physiology, global production and impact on ocean chemistry 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Invited Seminar to a multi-disciplinary audience at Plymouth Marine Laboratories (PML). Before and after the talk I also had round table discussions with postgraduate and postdoctoral researchers as well as PIs at PML. This has resulted in a successful collaboration for one of my PhD student projects with staff at PML.

This has resulted in a successful collaboration for one of my PhD student projects with staff at PML.
Year(s) Of Engagement Activity 2012
 
Description From comparative physiology to global climate change 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Schools Outreach Activity - Guest Speaker at the Heads of Biology for Canford Schools (Devon, Cornwall, Somerset and Dorset A-level schools and colleges), held at Truro School, Cornwall on 12th June 2013. The talk was aimed at linking research to teaching in the A-level curriculum.

Southwest Schools Outreach Activity - Guest Speaker at the Heads of Biology for Canford Schools (Devon, Cornwall, Somerset and Dorset A-level schools and colleges), held at Truro School, Cornwall on 12th June 2013. The talk was aimed at linking research to education, and resulted in invitations to give further talks to senior school students in the region
Year(s) Of Engagement Activity 2013