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Contribution of Fish to the Marine Inorganic Carbon Cycle

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Science  16 Jan 2009:
Vol. 323, Issue 5912, pp. 359-362
DOI: 10.1126/science.1157972

Abstract

Oceanic production of calcium carbonate is conventionally attributed to marine plankton (coccolithophores and foraminifera). Here we report that marine fish produce precipitated carbonates within their intestines and excrete these at high rates. When combined with estimates of global fish biomass, this suggests that marine fish contribute 3 to 15% of total oceanic carbonate production. Fish carbonates have a higher magnesium content and solubility than traditional sources, yielding faster dissolution with depth. This may explain up to a quarter of the increase in titratable alkalinity within 1000 meters of the ocean surface, a controversial phenomenon that has puzzled oceanographers for decades. We also predict that fish carbonate production may rise in response to future environmental changes in carbon dioxide, and thus become an increasingly important component of the inorganic carbon cycle.

The inorganic half of the marine carbon cycle includes biogenic reaction of seawater calcium (Ca2+) with bicarbonate (HCO3), producing insoluble calcium carbonate (CaCO3) in the process of calcification (1): Math

The vast majority of oceanic calcification is by planktonic organisms (2). Coccolithophores are considered to be the major contributor, but foraminifera are also included in global carbonate budgets (3). Upon death, their carbonate “skeletons” are released and rapidly sink to deeper ocean layers. Based on observations and models, estimates of global production of new CaCO3 range from 0.7 to 1.4 Pg CaCO3-C year–1 (47) (Fig. 1).

Fig. 1.

A modified schematic diagram of ocean CaCO3 budget showing the potential contribution of high-magnesium calcite produced by marine teleost fish. The fish images represent teleosts from a wide range of species and habitats, because all teleosts (but not elasmobranchs) are thought to produce carbonates as part of their osmoregulatory strategy (813). All values except the fish production rate are previously published estimates for total global production or dissolution in the upper ocean (2, 57).

It is less widely known that all marine teleosts (bony fish) produce and excrete carbonate precipitates. Walsh et al. (8) originally suggested that this might be quantitatively significant on a large scale, an idea not previously considered within a global carbonate budget framework. Carbonate precipitates are excreted by fish via the intestine as a by-product of the osmoregulatory requirement to continuously drink calcium- and magnesium-rich seawater, and they are produced whether or not fish are feeding (9). As imbibed seawater passes through the intestine, it is alkalinized (to pH 8.5 to 9.2) along with substantial secretion of HCO3 ions, typically reaching 50 to 100 mM in gut fluid (811), well in excess of concentrations in seawater (∼2.5 mM). These conditions cause precipitation of imbibed Ca2+ (and some Mg2+) ions as insoluble carbonates (811). This process has physiological importance in facilitating water absorption by the gut (10), and it reduces calcium absorption, which secondarily protects the kidney by minimizing renal stone formation (12). Carbonate precipitates formed in the gut are excreted either within discrete mucus-coated tubes or pellets, or incorporated with feces when fish are feeding (810). The organic mucus-matrix is rapidly degraded in natural seawater, leaving only inorganic crystals of CaCO3 with high magnesium content (Mg:Ca ratio ranging from 10 to 33 mol %) (8) (fig. S1).

A striking visual indication of the high rate of carbonate production in marine fish is provided by x-rays of European flounder (Platichthys flesus) after acute transfer from fresh water (in which they do not produce carbonates) to seawater (Fig. 2). Accumulations of the precipitates (more x-ray opaque than some of the surrounding bones) can be seen forming inside the intestine within 3 hours of fish initiating drinking after transfer. Excreted carbonates have been collected and titrated to reveal production rates in the temperate European flounder and subtropical Gulf toadfish (Opsanus beta) ranging from 18 to 40 μmol C per kg of fish per hour (813). This range is explained by differences in metabolic rate, which are determined by body mass and temperature within a species, as well as by interspecific life-style differences. In aquatic organisms, mass-specific metabolism scales inversely with body size, increasing ∼1.6-fold with every 10-fold decrease in body mass, and increases exponentially with temperature typically by 1.83-fold for every 10°C rise (14). Thus, smaller fish at higher temperatures produce proportionally more carbonate per unit body mass (fig. S2).

Fig. 2.

Digital x-ray photographs of live European flounder (Platichthys flesus) showing formation of gut carbonates in unfed fish after transfer from fresh water to seawater. Note the absence of bones (apart from the overlying pectoral fin) over the abdominal area (bounded by dashed line) where the viscera (including intestine) are situated. (A) Flounder acclimated to fresh water for 1 week to allow clearance of previously produced carbonates from the intestine. (B) X-ray photo taken 3 hours after a freshwater flounder was transferred to seawater. In seawater, the fish rapidly initiates drinking and high rates of intestinal HCO3 secretion. This results in the formation of CaCO3 precipitates that form x-ray opaque structures within the intestine (indicated by solid white arrows). X-ray images were taken with Siemens multix-TOP x-ray equipment and a Konica regus computed radiography system.

To calculate the teleostean contribution to oceanic carbonate budgets requires knowledge of global marine fish biomass. We used two entirely independent models to describe the size composition and abundance of marine fish across the global oceans, one by using a size-based macro-ecological approach (15) and the other by using Ecopath software (16). The fish biomass estimates generated for each size-class and the relevant average local sea temperatures were then combined with individual fish carbonate excretion rates to predict global fish CaCO3 production ranging from 3.2 × 1012 to 8.9 × 1012 mol year–1 (0.04 to 0.11 Pg of CaCO3-C year–1). This range accounts for 2.7 to 15.4% of estimates for total global new CaCO3 production in the surface oceans.

Several potentially biasing assumptions are made in these calculations, but we adopted a conservative approach that, if anything, underestimates fish carbonate production. Adopting the more liberal of these realistic assumptions would yield estimates almost three times as high, i.e., 9 to 45% of total global new CaCO3 production (see Supporting Online Material for details of the above calculations and assumptions). Despite this conservatism, our estimate shows that fish are a major but previously unrecognized source of oceanic carbonate and contribute substantially to the marine inorganic carbon cycle (Fig. 1).

An important question following from this discovery is how the nature and fate of piscine carbonates compares with those from traditionally accepted sources. At the higher pressure and colder temperatures of the deep ocean, seawater becomes undersaturated with respect to CaCO3, leading to dissolution as it sinks, in a reversal of reaction 1; thus, the concentration of dissolved HCO3 and CO 2–3 increases with depth [measured as an increase in the total alkalinity (TA) of seawater]. Pelagic CaCO3 particles from traditional sources are predicted to dissolve once they reach the chemical lysoclines for either calcite (∼4300 and 750 m) or aragonite (∼1500 and 500 m), respectively, in the North Atlantic and Pacific Oceans (1, 1720). However, contrary to this view, recent carbonate budgets suggest that the majority (50 to 71%) of carbonates exported from surface waters dissolve at much shallower depths (4, 5, 21). This results in an increase in TA from ∼2400 μM to 2480 and 2500 μM at 1000-m depth, in the North Atlantic and Pacific oceans, respectively (1) (Fig. 3), a controversial phenomenon that has puzzled oceanographers for decades (7).

Fig. 3.

The normalized total alkalinity of seawater as a function of depth for North Atlantic Waters (30°N and 23°E) (18, 20).

The causes of CaCO3 dissolution above the lysocline (7) are subject to debate and have been attributed to (i) dissolution in zooplankton guts (2226); (ii) dissolution in microenvironments where bacterial oxidation of organic matter enhances this process (27); and (iii) dissolution of more soluble forms of CaCO3, including pteropods and high-magnesium calcite (28, 29). However, dissolution in copepod guts can account for only a small portion of the increase of TA (27). The sharp increase in TA in the Pacific indicates that a more soluble phase may be dissolving (28, 29), such as high-magnesium calcites that are twice as soluble as aragonite (30, 31). We suggest that a large portion of the increasing TA in surface waters is indeed related to the dissolution of high-magnesium calcites produced by fish. Given their high magnesium content (8) (fig. S1) and solubility, we predict that dissolution of piscine carbonates will make a major contribution (up to 26%) to the increase in TA in the shallower oceanic depths and helps at least partially explain this currently perplexing observation (7) (Fig. 3).

The above estimate is a global average for fish-derived carbonates and does not take into account the potential for regional hot spots of piscine carbonate production (figs. S4 and S5). Indeed, 50% of fish biomass is predicted to occur in only 17% of ocean area (15) (fig. S4). Furthermore, such hot spots are largely found over continental shelves and in upwellings where the water is mostly shallow (100 to 200 m deep). This raises the possibility that fish could be the major source of carbonate production in the surface ocean in these areas. Also, dissolution of fish carbonates at such shallow depths may not occur if the carbonates are buried within sediments. Thus, we suggest that the localized high production rates and fate of fish carbonates in some parts of the ocean (and correspondingly low production areas elsewhere) require further investigation. In addition, most carbonates collected in sediment traps cannot be visually identified and accurately assigned to traditional planktonic sources. Intriguingly, some of these collected carbonate particles strongly resemble those found in the intestines of marine fish (fig. S3). The Mg:Ca ratio of fish carbonates (10 to 33 mol %) overlaps with the range for the finest-sized fraction (<37 μm) of magnesian calcite particles collected in sediment traps in the Sargasso Sea (9 to 12 mol %) (32). At that time, this magnesian calcite phase of carbonate was assumed to originate from bryozoan skeletons attached to floating Sargassum. It is now tempting to suggest that fish may be the source of this carbonate phase.

So far, we have concentrated on production of carbonates, their excretion, and potential dissolution in the ocean, ignoring a subtle process that further links fish production and distribution to oceanic acid-base chemistry. HCO3 ions secreted by intestinal cells into the intestinal lumen of fish are derived largely from metabolic CO2 reacting with water within intestinal epithelial cells, under the catalytic influence of carbonic anhydrase (11). This reaction produces H+, which is exported into the blood and ultimately excreted into the external seawater via ion-transporting cells in the gills of fish (12, 13). Thus, there is an anatomical separation of, and physical distinction between, the acid and base components of this reaction and its excretory products; i.e., insoluble CaCO3 excreted via the gut, and dissolved H+ ions excreted via the gills. Furthermore, solid CaCO3 will rapidly sink and only redissolve at depth (raising TA at this point), whereas H+ ions excreted via the gills will remain in the surface ocean (decreasing TA). Regular vertical migrations of many pelagic fish species, often daily and over several hundred meters, may complicate interpretation of the expected acid-base effects, but the principle is worth noting.

Postindustrial oceanic acidification due to elevated atmospheric CO2 is now well recognized and is predicted to have major impacts on calcifying organisms (33), raising questions about how such future environmental changes may influence piscine global carbonate production. We predict that production of carbonate precipitates by fish will accelerate as a result of both increasing seawater temperatures and CO2 concentrations. First, metabolic rate increases exponentially with temperature in ectothermic fish, thus increasing metabolic CO2 production and intestinal carbonate excretion at the individual level (fig. S7). However, for communities, the model of Jennings et al. (15) suggests that community fish biomass will decrease with temperature (for a given rate of primary production) and that this will offset the accompanying increase in carbonate production owing to temperature effects on individual metabolism. Second, rising ambient levels of dissolved CO2 will cause a corresponding increase in CO2 partial pressures in the blood of fish (34, 35). In vitro studies show that increasing blood CO2 concentrations stimulate intestinal cells to produce more HCO3 (36), and thus intestinal excretion of precipitated carbonates is predicted to rise with ambient CO2. This contrasts with the commonly cited view that CaCO3 production rates decrease in calcifying marine plankton and corals as ambient CO2 increases [(2, 33); but see Supporting Online Material and (37)]. The biomineralization mechanisms in these organisms are not well understood (37) but are dependent upon the ambient concentrations of CO 2–3 or HCO3 in seawater, which change with pH as CO2 concentration increases (2). Distinct from this, fish use endogenous CO2 to produce HCO3 ions that rise to very high concentrations within the microenvironment of the gut lumen (typically 50 to 100 mM) (811). Thus, the contribution of fish to marine carbonate production seems likely to increase in the future and become an even more important component of the inorganic carbon cycle.

Supporting Online Material

www.sciencemag.org/cgi/content/full/323/5912/359/DC1

Materials and Methods

SOM Text

Figs. S1 to S6

Tables S1 and S2

References and Notes

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