Article | Open | Published:

Phase heterogeneity in carbonate production by marine fish influences their roles in sediment generation and the inorganic carbon cycle

Scientific Reportsvolume 7, Article number: 765 (2017) | Download Citation


Marine teleost fish are important carbonate producers in neritic and oceanic settings. However, the fates of the diverse carbonate phases (i.e., mineral and amorphous forms of CaCO3) they produce, and their roles in sediment production and marine inorganic carbon cycling, remain poorly understood. Here we quantify the carbonate phases produced by 22 Bahamian fish species and integrate these data with regional fish biomass data from The Bahamas to generate a novel platform-scale production model that resolves these phases. Overall carbonate phase proportions, ordered by decreasing phase stability, are: ~20% calcite, ~6% aragonite, ~60% high-Mg calcite, and ~14% amorphous carbonate. We predict that these phases undergo differing fates, with at least ~14% (amorphous carbonate) likely dissolving rapidly. Results further indicate that fisheries exploitation in The Bahamas has potentially reduced fish carbonate production by up to 58% in certain habitats, whilst also driving a deviation from natural phase proportions. These findings have evident implications for understanding sedimentary processes in shallow warm-water carbonate provinces. We further speculate that marked phase heterogeneity may be a hitherto unrecognised feature of fish carbonates across a wide range of neritic and oceanic settings, with potentially major implications for understanding their role in global marine inorganic carbon cycling.


Marine bony fish have recently been identified as a globally important source of marine calcium carbonate1. Thus, alongside coccolithophores, foraminifera, and pteropods in oceanic settings, and benthic organisms (such as corals, coralline algae, and echinoderms) and microbial calcification in neritic environments2,3,4,5,6,7, they are now recognised as playing a potentially key role in the marine inorganic carbon cycle1, 8, 9. Whilst the bicarbonate transport mechanisms which drive the formation of carbonates in the piscine intestine are now reasonably well understood10, 11, and progress has been made in understanding their potential sedimentary significance in shallow warm-water settings12,13,14, the cycling of these carbonates through the marine inorganic carbon system remains poorly understood. This, however, is a significant issue given that: (i) the inorganic carbon cycle, together with the organic carbon cycle, strongly regulates oceanic carbon distribution; and (ii) the contribution to this inorganic carbon cycle by fish is evidently significant: highly conservative modelled estimates suggest they produce 3–15% of global marine carbonates, with less conservative criteria suggesting up to 45%1. It is thus important that the role of marine teleosts in the carbon cycle is properly understood and appropriately integrated within ocean carbon models.

Conventional understanding of the inorganic carbon cycle holds that carbonate precipitation takes place primarily in the euphotic zone of oceanic settings, where coccolithophores, foraminifera (calcite) and pteropods (aragonite) are thought to be the major sources, with smaller contributions of aragonite and high-Mg calcite within neritic environments5, 6. The net effect of this precipitation can be described by the following reversible reaction:

C a 2 + +2HC O 3 CaC O 3 +C O 2 + H 2 O

Calcification thereby contributes CO2 (some of which may be taken up by net organic production) to surface waters and lowers alkalinity, with ~0.6 mol of CO2 effectively being generated for each one mole of CaCO3 precipitated15, whilst carbonate dissolution reverses this process. Calcite and aragonite are stable under most surface water conditions, with dissolution theoretically proceeding only below their saturation horizons at depths greater than ~0.5–4.5 km (depending on carbonate phase and geographic region)16. Thus, the fate of most carbonates should either be accumulation as sediment if deposited above their respective saturation horizons, or dissolution in deeper ocean settings; surface water alkalinity remaining depleted in either case. In this context, initial assumptions that fish carbonates are composed entirely of high Mg-calcite (HMC; 5–25 mol% MgCO3) and very high Mg-calcite (VHMC; >25 mol% MgCO3) formed the basis of a hypothesis wherein they strongly influence alkalinity–depth profiles in the ocean1. This is because the solubilities of these metastable carbonate phases exceed those of aragonite (except where MgCO3 content is less than ~12 mol%) and calcite17, 18, implying that their corresponding saturation horizons are located at shallower depths. Accordingly, this hypothesis invokes fish carbonates–as the only known high-solubility carbonate phases significant to marine carbonate production in oceanic settings–as a unique source of alkalinity in the upper water column that can at least partially explain a widespread positive alkalinity anomaly at depths of ~1000 m1, 8.

In shallow marine settings HMC often forms a significant component of accumulated carbonate sediments19,20,21, with fish now seen as a potentially important source of fine-grained carbonate mud (<63 µm)11,12,13. However, several recent studies have demonstrated that fish carbonates produced in shallow water habitats of sub-tropical regions actually occur in a remarkably diverse range of phases. In addition to HMC and VHMC, these include low-Mg calcite (LMC; 0–5 mol% MgCO3), aragonite, and amorphous calcium and magnesium-rich carbonate (ACMC)12, 13, 22. If established solubility relationships for these phases apply (i.e., in order of decreasing solubility: ACMC > VHMC > HMC > aragonite > LMC; solubility in calcites being positively correlated with MgCO3 content19, 23), fish-derived carbonate solubilities thus span two orders of magnitude, suggesting they will have markedly different post-excretion fates. This implies that their roles in carbonate sediment cycling and inorganic carbon cycling in these neritic environments, and potentially also in oceanic settings if phase heterogeneity applies universally, will strongly depend on what phases are being produced and in what ratios. However, a lack of quantitative data regarding the relative abundances of carbonate phases produced by different fish species and communities–both in neritic and oceanic settings–severely limits our capacity to understand the nature of these roles. Developing such an understanding may be important not only for modelling the role of fish in past, present and future sedimentary scenarios, but also for predicting the oceanic response to rising levels of atmospheric CO2, and potentially for informing decisions on how fish stocks should be managed as a carbon-regulating service9, 24 in the face the challenges such as climate change mitigation.

Here we utilise attenuated total reflectance Fourier transform infrared (ATR-FTIR) spectroscopy to provide the first quantification of precipitate phases produced by a range of Caribbean fish species. This methodology provides additional capability over previously used X-ray diffraction (XRD) techniques1, 12, 13 to enable the presence of both amorphous and crystalline carbonate phases to be determined. Results are combined with morphological and compositional data to facilitate an assessment of the abundances of different phases produced by each species. We then combine these data with production rate data and regional fish census data from a range of habitats in shallow-water areas of the extensive banks of carbonate sediment that form The Bahamas (i.e., the Bahamian platform) to model fish carbonate production with respect to different carbonate phases. Because precipitation products vary among fish species12, 13, this model not only estimates phase abundances at an archipelago scale; it also models variations according to fish species assemblage and, thus, habitat. Furthermore, census data from sites within marine reserves provide a proxy for quasi-historical conditions (i.e., before anthropogenic disturbance) and facilitate production comparisons between modern degraded reefs and historical ‘pristine’ reefs. The outcomes of this work are considered with respect to their implications for the fate and sedimentary significance of fish-derived carbonates in shallow-water regions of tropical and sub-tropical carbonate provinces, and their potential relevance to the inorganic carbon cycle in wider ocean settings.


Phase characterisation and relative abundances

ATR-FTIR spectra indicate that carbonates excreted by most of the 22 Caribbean fish species sampled are dominated by calcitic phases, with those from some species also generating minor aragonite peaks (Fig. 1). These results are in good agreement with those from previous XRD analyses12, 13. However, the additional presence of ACMC, in some cases as the dominant phase, is confirmed for samples from seven species, as indicated by distinctive ν1 and ν2 peak positions, broader and weaker ν2 peaks than those generated by crystalline phases, and the absence of well-defined ν4 peaks (Fig. 1–spectrum d). Monohydrocalcite (CaCO3·H2O) and brucite (Mg[OH]2)–phases not previously reported as being produced by fish–are also identified (Fig. 1–spectra c, e), albeit as minor components (<1.5% of total excreted precipitates).

Figure 1
Figure 1

ATR-FTIR spectra and morphological properties for the main forms of fish-derived carbonate. Spectra indicate the following phases: a–calcite (as produced here by Lutjanus apodus); b–calcite + aragonite (as produced by Sparisoma chrysopterum); c–calcite + ACMC, hydrated + brucite (as produced by Platybelone argalus); d–ACMC, hydrated (as produced by Albula vulpes); e–monohydrocalcite (as produced by Sphoeroides testudineus). Spectra for any given phase are generally similar among species. Vertical bands through spectra: grey = absorption bands associated with carbonate phases, where ν1–ν4 represent different vibrational modes in the CO3 2− ion; blue = absorption bands associated with hydrated (ACMC and monohydrocalcite) and hydroxide (brucite) phases, where vibrations are assigned to O-H stretching and H-O-H bending. SEM images show typical morphotypes for each phase; letter symbols indicating morphotype (see key). Scale bars (bottom centre of each image) represent 2 µm.

In addition to phase identifications and assignments, FTIR data yield information on several other aspects of fish-derived carbonates that may provide useful insights to precipitation processes and post-excretion fates. Firstly, strong hydration peaks are generated by all fish-derived carbonates containing ACMC (Fig. 1). These spectra, consistent with those generated elsewhere for fish-derived ACMC22, indicate that it is a strongly hydrated phase. Hydration peaks are also generated by samples in which (V)HMC is dominant, albeit they are much weaker than those associated with ACMC and monohydrocalcite (Fig. 1). However, they are nearly always stronger than equivalent peaks generated by other biogenic calcites and aragonites we have analysed (Supplementary Fig. 1). Since hydrated amorphous and crystalline carbonates are thought likely to be more soluble than their anhydrous forms23, 25, these findings may be of some significance to understanding their post-excretion fates.

Secondly, Politi et al.26 used the ratio of the intensities between carbonate ν2 and ν4 absorption bands (out-of-plane and in-plane bending modes for the CO3 2− ion, respectively; Fig. 1) as a proxy for crystallinity in calcites; lower values being indicative of higher degrees of crystallinity. This ratio is consistently higher in fish-derived (V)HMC ellipsoids (range 7.4–13.2) than in sedimentary HMC foraminifera tests (range 4.2–5.0; Supplementary Fig. 1), which suggests they have a low degree of crystallinity compared to at least some sedimentary HMC and implies that they may be less resistant to dissolution27. Ascertaining the relative degree of crystallinity in other fish-derived calcites, however, is hampered by overlapping FTIR peaks resulting from the presence of multiple calcite phases.

Estimates of phase abundance by family, based on SEM assessments informed by these new FTIR data coupled with single-crystal compositional data and existing XRD data12, 13, are presented in Table 1, with complete estimates for phases and morphotypes by species presented in Supplementary Tables 1 and 2. Precipitates from eight teleost families (of 15 investigated) are dominated by HMC and VHMC, with those from a further four families being dominated by LMC, and two families by ACMC. The latter phase also accounts for ≥10% of precipitates excreted by fishes from four other families. Of the subsidiary phases, aragonite is the most abundant, being produced by 12 of 15 families and frequently accounting for 5–10% of excreted products. Conversely, monohydrocalcite is produced by only three families, whereas brucite, although present in the carbonates produced by most families, typically accounts for 1% of products. Averaging these abundance estimates yields an ‘other family’ category (Table 1), which effectively represents the average phase proportions for all fish families. These proportions were applied to all families seen during fish surveys for which carbonates have not been characterised.

Table 1 Estimated volumetric abundances of the various precipitate phases produced by 22 fish species from 15 families

Production modelling

Platform-wide production in generalised habitats

Production values per habitat type (Table 2) show that carbonate production by fish is highest (per unit area) in reefal, hard bottom, and fringing mangrove habitats; production patterns being generally similar to those of Perry et al.12, but with considerably higher values reflecting the application of an activity scaling factor (after Wilson et al.1) to yield more realistic outputs. Otherwise, differences that reflect our updating of the production rate–fish body mass relationship (after Perry et al.12), and the inclusion of additional census data from reefal and hard bottom sites, are minor. However, incorporating our family-specific phase abundance data (Table 1) within this production model provides the first estimates for the total volumes of each phase produced in these habitats, and across the entire platform. Outputs indicate that HMC (specifically that with >15 mol% MgCO3) and VHMC–hereafter collectively referred to as (V)HMC–are the dominant phases produced platform-wide (~57% of total production), but also that LMC and ACMC account for significant proportions (~19 and ~13%, respectively). Other phases, however, are generally scarce; platform-wide production totals comprising ~6% aragonite, ~3% HMC (5–15 mol% MgCO3), and <1.5% each of monohydrocalcite and brucite (Table 2 and Fig. 2).

Table 2 Carbonate production (105 kg·yr−1) by fish in shallow-water habitats of The Bahamas.

Figure 2
Figure 2

Phase proportions modelled for different habitat types. Fish carbonate phases shown as a proportion of total production in each of seven generalised habitats within The Bahamas, and as a proportion of area-weighted average production across the entire shallow platform area. Right-hand axes show mean (±s.e.m.) production rates. For each habitat type, n is the number of fish biomass survey sites. Data from Orbicella reefs are used to represent phase proportions for generalised reefal habitats, although proportions from Acropora reefs and patch reefs may be somewhat different (see Fig. 4).

Modelled outputs further indicate that differences in fish densities and species assemblage among habitats result in substantial differences in the relative proportions of carbonate phases produced (Figs 2 and 3). These differences are most striking when comparing (V)HMC with ACMC; reefal and hard bottom habitats tend to yield high proportions of (V)HMC (~58–63% combined production), and low proportions of ACMC (~9–12%), whereas substrates dominated by bare sand or seagrass yield relatively lower proportions of (V)HMC (~28–40%) and higher proportions of ACMC (~18–34%). Likewise, bare sand and seagrass meadows tend to yield higher proportions of LMC (~26–28%) than reefal and hard bottom habitats (~18–19%). Production in fringing mangroves is disparate from all of these habitats; ~92% of total production comprising (V)HMC, with other phases each contributing <3%.

Figure 3
Figure 3

Mapping of production model results. Panels show a section of the shallow platform region adjacent to the eastern shoreline of Andros Island, The Bahamas, detailing: (a) habitat distribution; (b) overall fish carbonate production rates (g·m−2·yr−1); and (c) production of ACMC as a proportion of total fish carbonate production in each habitat. Note that wide expanses of habitat in which ACMC accounts for >20% of total production are those in which overall production rate is very low. Scale bar in panel (b) represents 10 km. Maps were created by the authors in the software package ERDAS Imagine 8.3 (

Sub-habitat comparisons and marine reserve effects

Within broad habitat types (Table 2), carbonate production by fishes varies among sub-habitats defined using a higher-resolution classification scheme (Supplementary Tables 3). For example, the relatively coral-rich habitats forming generalised ‘reef’ habitats–Orbicella sp. (formerly Montastraea) reefs, Acropora sp. reefs, and spur-and-groove forereefs–yield production rate means spanning 4.8–7.3 g·m−2·yr−1 (Table 2 and Fig. 4). In contrast, patch reefs, which are abundant in The Bahamas but omitted from ‘reef’ habitat areal extent estimates, return a higher mean rate of 9.7 g·m−2·yr−1; a consequence of the concentration of fish biomass into small reef patches surrounded by lagoonal habitats. Generalised ‘hard bottom’ habitats (macroalgal and gorgonian plains) yield mean production rates of 1.7 g·m−2·yr−1 (Fig. 4), whereas less common hard bottom habitats typically yield lower rates (mean 0.1–1.4 g·m−2·yr−1; Table 2); only hard bottom areas characterised by relatively high habitat structure return a higher mean production rate (16.7 g·m−2·yr−1). As with generalised habitats, differences in fish community structure among these sub-habitats yield different proportions of carbonate phases (Fig. 4). For example, ACMC is generated in considerably higher proportions on Orbicella reefs and spur-and-groove forereefs (~11–13%) than on patch reefs and Acropora reefs (~4–5%).

Figure 4
Figure 4

Production charts for sub-habitats within reefal and hard bottom habitat types. Insets show production rates (±s.e.m.) by fish in discrete habitats of (a) ‘reefal’ and (b) ‘hard bottom’ habitat types. Main charts show the different phases as a proportion of total production in each habitat type. Shading in each of the main charts indicates sub-habitat types as delineated in the corresponding insets. Numbers in parentheses (insets) refer to the number of fish biomass surveys conducted in each habitat type.

A critical caveat to these outputs is that they derive from unprotected areas. Thus, fishing pressure has almost certainly diminished overall production rates and potentially, through selective fish extraction, changed natural ratios of phase productivity. To test the impact of fishing pressure we compared production values from unprotected habitats with those from corresponding habitats (specifically, Orbicella reefs and macroalgal/gorgonian plains) in a no-take marine reserve (Exuma Cays Land and Sea Park; ECLSP); outputs from the latter being taken as a proxy for historical production in unfished (more ‘pristine’) habitats. Unsurprisingly, removal of fishing pressure (enforced by warden patrols since 1986) has resulted in significantly higher fish species diversity on Orbicella reefs in the ECLSP, which support a significantly higher biomass of commercially important large-bodied serranids (23.75 g·m−2 inside ECLSP vs. up to 7.93 outside)28, 29. Additionally, higher biomass of large serranids and lutjanids in ECLSP hard bottom habitats is a potential reserve effect29.

The impact of these effects on fish carbonate production (Fig. 5) is significant: mean production rates are ~140% higher on Orbicella reefs inside the ECLSP than outside (11.40 g·m−2·yr−1 vs. 4.75; one-tailed Mann-Whitney: P = 0.009), and 109% higher on macroalgal/gorgonian plains (3.45 g·m−2·yr−1 vs. 1.65; one-tailed Mann-Whitney: P = 0.033). If comparable effects are applicable across all reefal habitat types, production rates for generalised reefs (6.19 g·m−2·yr−1 in unprotected areas; Table 2) could be as high as 14.85 g·m−2·yr−1. These results suggest that removal of fishing pressure from reefal and hard bottom habitats across the entire platform could yield production outputs 54% higher than current models indicate (22.1 × 106 kg·yr−1 vs. 14.3 × 106; Table 2), and this value could be even higher if similar effects apply for other habitats. However, effects are probably most pronounced in reefal and hard bottom habitats because these are favoured by many commercially important fishes30, biomass increases of which are one of the greatest benefits of no-take reserves29, 31.

Figure 5
Figure 5

Marine reserve effects on fish carbonate production. Insets show production rates (±s.e.m.) by fish in (a) ‘reefal’ and (b) ‘hard bottom’ habitat types inside and outside of the Exuma Cays Land and Sea Park (ECLSP). In both habitat types the difference between sites inside and outside ECLSP is significant (one-tailed Mann-Whitney: P < 0.05). Main charts show the different phases as a proportion of total production in each habitat type. Shading in each of the main charts corresponds with that shown in each of the insets. Numbers in parentheses (insets) refer to the number of fish biomass surveys conducted within each habitat type.

Comparison of data from corresponding habitats inside and outside the ECLSP further indicate major differences in the proportions of phases produced. Specifically, (V)HMC is produced in higher proportions within the ECLSP for both reefal (76.2 vs. 60.0%) and hard bottom (84.4 vs. 58.5%) habitats, with correspondingly lower proportions of LMC, aragonite, and ACMC (Fig. 5). These differences reflect greater abundance and biomass of commercially important (V)HMC-producing families (e.g., Serranidae) within the reserve; selective removal of these families outside the reserve having driven a deviation from normal natural phase proportions. Thus, phase proportions produced over historical timescales will likely have been somewhat different to those modelled for present-day Bahamian settings; a finding that should be used to inform future fisheries management decisions.


New analysis of fish-derived carbonates using FTIR spectroscopy identified a wide range of carbonate and associated phases produced by 22 Caribbean marine fish species. Whilst several of these phases (LMC, HMC, VHMC, aragonite, and ACMC) were identified as common precipitates in previous studies12, 13, 22, these new spectroscopic data coupled with novel phase proportion estimates reveal a hitherto unrecognised significance of ACMC and LMC; both are produced in unexpectedly high proportions, and ACMC is produced by more species than previously thought. Monohydrocalcite and brucite are also recognised for the first time in fish-derived precipitates, albeit typically as minor phases (Table 2). Integration of these new data within production models for shallow habitats in The Bahamas generates platform-wide phase quantifications that yield high proportions of LMC, (V)HMC, and ACMC, and low proportions of aragonite, monohydrocalcite, and brucite. In addition, these models allow us to explore among-habitat variations in phase proportions as a consequence of differences in fish species assemblage.

Based on this model, sedimentologists assessing the genetic origins of sediments in contemporary tropical and sub-tropical shallow platform settings might expect evidence for fish-derived carbonates to differ according to depositional habitat (Figs 2 and 3; Table 2). However, several caveats apply: i) evidence for fish carbonates in modern sediments may be obscured by rapid post-depositional alteration or dissolution13–a subject of ongoing research; and ii) distribution patterns may be modified by post-excretion sediment transport mechanisms, which may preferentially remove mud-sized (<63 µm) sediments (including most fish carbonates14) from higher-energy production sites (i.e., reefal and hard bottom habitats), ultimately transporting them either to mud-dominated sediments of lower-energy platform interiors32, or to deeper waters off-platform14, 33. These uncertainties aside, understanding patterns of fish carbonate production among different fish communities is important for predicting their overall contribution to mud-sized sediment production in tropical and sub-tropical shallow-water carbonate platforms. For example, high production rates associated with reefal, hard bottom, and mangrove habitats means that, even though their collective areal extent covers only 3.2% of shallow platform area of The Bahamas, they generate 63% of the platform-wide fish carbonate production budget (Table 2), resulting in a platform-wide phase proportion signature dominated by (V)HMC (Fig. 2).

The significance of these findings is perhaps best highlighted by extending them across shallow warm-water carbonate provinces beyond The Bahamas, on the assumption that similar production rates and phase proportions apply (albeit with the caveat that fish community structure and biomass are likely to vary among these provinces). This is because the habitat configuration of the Bahamian platform is actually somewhat atypical among shallow warm-water carbonate provinces, particularly with respect to habitats that support high fish biomass concentrations (reefs, hard bottoms, and fringing mangroves): whereas these account for only 3.2% of the total shallow platform area in The Bahamas, they account for 22.9% in the Florida Keys; this being the next smallest proportion in our assessment of other provinces (Table 3). Across other provinces these habitats occupy even higher proportions of the shallow water area, reaching up to 86% at the Northern Line Islands site of Palmyra Atoll. Accordingly, we would predict that the significance of fish carbonate mud to platform-wide production totals is likely to be considerably greater in many of these shallow-water carbonate provinces than in The Bahamas.

Table 3 Fish carbonate contributions to platform-wide mud production as a function of benthic habitat configuration

To test this prediction, we applied our habitat-specific production rate estimates from The Bahamas across a number of other global localities (Table 3), with inherent caveats as stated above. This current best-estimate approach suggests that platform-averaged production rates from test regions are typically in the range 0.61–3.68 g·m−2·yr−1, compared with 0.13 g·m−2·yr−1 in The Bahamas. If a Bahamian mud production budget12 involving other carbonate sources is also broadly applicable across these provinces, fish carbonates will typically account for 1.3–7.3% of total carbonate mud production, compared with 0.2% in The Bahamas. Given the magnitude of these differences in production totals, one might also expect these contrasting habitat configurations to yield different platform-wide phase proportions. However, as alluded to above, platform-wide phase proportions in The Bahamas are effectively an average of phase proportions generated in reefs and hard bottoms (Fig. 2); such is the dominance of these habitats in terms of fish carbonate generation there. Consequently, increasing their proportional extent, even dramatically, has only a small effect on platform-wide phase proportions, typically manifested as (V)HMC totals up to ~62% (cf. 57% in The Bahamas) and ACMC totals down to ~10% (cf. 13% in The Bahamas).

It is important to bear in mind that these calculations are based on model outputs for overfished settings. Adjusting habitat-specific rates in our test regions to those estimated from our marine reserve data (Fig. 5), we find that platform-averaged rates approximating fish carbonate production over historical (and perhaps geological) timescales in these provinces could have been in the range 1.30–8.64 g·m−2·yr−1 (2.7–15.7% total carbonate mud production; Table 3). Furthermore, these historical estimates are likely conservative, since data from other regions suggest that the capacity for many no-take marine reserves to restore fish biomass to truly pristine states may be limited by their restricted size and proximity to overfished areas. Indeed, the highest documented biomass concentrations of reef-associated fishes are from large and isolated marine reserves (e.g., the Chagos Archipelago) that perhaps best approximate true ‘wilderness’ settings34 and could potentially yield fish carbonate production rates far higher than those estimated here.

A major implication of the diverse range of fish carbonate phases is that they likely have differing post-excretion fates. This is a particularly important outcome since it can provide insights to the nature of fish carbonate contribution to sedimentary processes in shallow water settings through consideration of the relative abundance and solubility potential of each phase. Solubility measurements involving VHMC ellipsoids produced by the gulf toadfish (Opsanus beta) indicate they are nearly twice as soluble as aragonite, with results being broadly comparable with other types of sedimentary HMC8. It is therefore reasonable to assume that fish-derived precipitates have solubilities comparable with those of similar phases precipitated via other biogenic (where data are available) or abiotic processes, although factors such as the low degree of crystallinity, relatively higher water contents, and small crystal size of some fish-derived carbonates (e.g., VHMC ellipsoids), may further influence their solubilities19, 27. Whilst this approach is complicated by considerable disparity among published Mg-calcite solubility relationships19, we follow the approach of Morse et al.35 by considering two relationships for Mg-calcites: (1) the ‘best fit’ biogenic relationship17, 18; and (2) the ‘Plummer and Mackenzie’ relationship36, 37.

On the basis of solubility orders determined using these relationships (Fig. 6), the post-excretion fates of fish-derived carbonates in surface seawater can be predicted if DIC-system parameters, and thus CaCO3 saturation states (Ω), are known. ‘Normal’ surface seawater around The Bahamas is characterised by elevated alkalinity38, with Ωcalcite ≈ 6 and Ωaragonite ≈ 4, whereas poorly circulating waters overlying platform interiors can have depleted alkalinities and correspondingly lower saturation states (Ωcalcite ≈ 4 and Ωaragonite ≈ 2)39. Thus, predicting the fate of some fish carbonate phases is straightforward: LMC and aragonite should be stable under all surface seawater scenarios in The Bahamas, whereas monohydrocalcite, ACMC, and brucite should be unstable. Of these unstable phases, monohydrocalcite probably dehydrates and transforms to more stable phases under surface seawater conditions40, 41. Amorphous carbonates can undergo similar transformations25, although available evidence suggests that fish-derived ACMC undergoes rapid (hours to days) dissolution22, whilst brucite likely follows a similar fate17, 42.

Figure 6
Figure 6

Likely solubility orders of fish carbonate phases and their theoretical fates in different surface seawater scenarios in The Bahamas. Solubility orders (left) are based on existing data for similar phases of biogenic (where available) and synthetic origins. Differences between the columns reflect a disparity in published solubility data for HMC. Data are from: 1) Morse and Mackenzie19 (and references therein); 2) Hull and Turnball64; 3) Walter and Morse17; 4) Brečević and Nielsen23 and Clarkson et al.65. Phases below the dashed line are thermodynamically unstable (Ω < 1) under normal surface seawater (SSW) conditions in The Bahamas. Based on these solubility data, a plot of CaCO3 ion concentration product (ICP; i.e. [Ca2+][CO3 2−]) for seawater (practical salinity 35; temperature 25 °C; ρCO2 400 µatm) versus total alkalinity illustrates the predicted stabilities of these phases relative to SSW in The Bahamas (right; modified after Morse et al.35 with the kind permission of Elsevier). ICP values for normal and platform interior (Inner GBB) waters are plotted (solid circles) along with equilibrium ICP values for relevant carbonate phases (dashed lines; Ω = 1); these phases being more stable the further their equilibrium ICP values are below seawater ICP. Uncertainties regarding brucite and ACMC solubilities are discussed in Supplementary Note 1, but available data suggest both phases are highly unstable in SSW.

The fate of (V)HMC, however, is more problematic to predict, in part because of uncertainty regarding solubility curves, but also because their fates will vary depending on where they are deposited (Fig. 6). For example, employing the ‘Plummer and Mackenzie’ solubility curve, HMC containing less than ~19 mol% MgCO3 should be stable in ‘normal’ seawater, whereas the equivalent threshold composition in poorly circulating platform interior waters could be as low as ~11 mol% MgCO3. These compositional thresholds are higher when using the ‘best fit’ biogenic curve, but the same principle applies. In either case, some fish-derived (V)HMC will be thermodynamically unstable at surface seawater conditions, although this does not necessarily mean it will dissolve. Rapid dissolution of reagent-grade calcite43 of comparable grain size to fish-derived carbonates requires Ωcalcite < 0.8. If a similar rule applies for fish-derived (V)HMC, low dissolution rates in waters where Ω(V)HMC = 0.8–1.0 could be overridden by the rate at which original grains alter to more stable forms, as has been shown to proceed very rapidly (months) in algal-derived HMC44. Thus, the fates of fish-derived (V)HMC in these platform settings remain somewhat uncertain, but their high MgCO3 contents mean they likely represent some of the least stable carbonate phases in tropical and sub-tropical carbonate platform settings, and are probably ‘early responders’ where dissolution is concerned.

Integration of these predicted fates in our production model yields a first-order estimate of the proportion of fish-derived carbonate that is thermodynamically unstable at surface seawater conditions in The Bahamas. On a platform-wide scale, ~29% of fish-derived carbonate (LMC, aragonite, and HMC with 5–15 mol% MgCO3; Table 2) should be stable at surface conditions, whereas ~14% (ACMC and brucite) may rapidly dissolve. The fate of (V)HMC (the remaining ~57%) is less certain: the ‘best fit’ biogenic solubility relationship suggests most will be stable in normal surface seawater, whereas the ‘Plummer and Mackenzie’ relationship suggests most will be thermodynamically unstable (Fig. 6).

Clearly further experimental work on the preservation and dissolution pathways of fish-derived carbonate phases is required to overcome these theoretical prediction issues, but our findings may nevertheless serve as a guide to further work that will help to constrain the production and cycling of fish-derived carbonates on a wider global scale. In particular, these findings provide strong evidence for a marked phase diversity in fish carbonate products occurring at a local scale, and it is reasonable to speculate that similar patterns may be replicated at the global scale. It is well beyond the scope of this study to attempt to model global scale phase proportions, as that would at least require additional phase production datasets from pelagic and cool-water fish groups–which are currently sparse at best. However, it is worth illustrating the potential implications that phase diversity in fish carbonates could have at the global scale. This is a highly relevant issue because fish have recently, and on the assumption that they produce only (V)HMC, been invoked as having a major role in the cycling of inorganic carbon in the upper 1 km of the oceans1, 8. Using our Bahamian dataset to populate an entirely conceptual oceanic model (Fig. 7), however, it is evident that dissolution of fish carbonates potentially occurs over a much greater depth range than initially hypothesised, and that their role in the marine inorganic carbon cycle could be considerably more complex and diverse than previously thought.

Figure 7
Figure 7

Conceptual model of the fish carbonate contribution to marine inorganic carbon cycling. Arrows represent major sources of CaCO3 production (blue); CaCO3 deposition as sediment (purple); and CaCO3 dissolution (pink). Predicted dissolution depths are for a North Atlantic scenario, where ASH and CSH are aragonite and calcite saturation horizons (Ω = 1), respectively (Feely et al.16). Assuming phase proportions of total fish CaCO3 production reflect those estimated for most shallow-water habitats in The Bahamas, ~57–72% (ACMC and (V)HMC) is predicted to dissolve in the upper water column, accounting for 4–19% of total upper water column dissolution. This contribution will be greater (7–25%) if total production is more similar to that in Bahamian mangrove habitats (94% ACMC and (V)HMC), and even more significant if less conservative estimates of global fish carbonate production are used. Fish carbonate production estimates are from Wilson et al.1; total carbonate production, deposition, and dissolution estimates are from Feely et al.16 and Milliman et al.66. Figure is modified after Wilson et al.1 with the kind permission of The American Association for the Advancement of Science.

Constraining the role of fish carbonates in the wider oceanic setting is particularly important, not only because of the apparent magnitude of their contribution to the inorganic carbon cycle1, but because of the potential for this role to change in the future. In part, changes could relate to rising levels of atmospheric CO2 and subsequent elevations in surface seawater temperatures and pCO2, both of which are predicted to stimulate increased carbonate production rates at the level of individual fish1, albeit effects remain to be fully quantified45. Such a response would contrast with that predicted for many other calcifying organisms under elevated pCO2 46, and it is possible that fish will contribute an increasingly large proportion of total marine carbonate under future climate change scenarios. However, such a change is potentially being offset by dramatic global declines in fish biomass due to recent and ongoing fishing pressures47. Furthermore, associated shifts in fish species composition could, as we see at the local scale here, drive a shift in overall fish carbonate phase proportions.

Our findings thus highlight that, in addition to these potential future changes in the magnitude of the fish carbonate contribution to inorganic carbon cycling, the nature of this contribution remains poorly understood due to a paucity of carbonate phase data, and is subject to change in response to shifting proportions of these carbonate phases. Since the inorganic carbon cycle controls the distribution of alkalinity throughout the oceans16, all of these issues could have implications for future climate through their potential effects on the capacity of the surface ocean to buffer increases in atmospheric CO2. Thus, there is a pressing need for additional data that will help to quantify phase proportions across a wider range of fish communities in different global marine settings. Models that incorporate such data will then underpin further work aimed at quantifying the role of fish in past, present, and future cycling of inorganic carbon across global scales, potentially with consequences for future fisheries management as a carbon-regulating service9.


Carbonate collections

Gut carbonate samples were collected from 22 fish species common to the Caribbean using aquaria facilities at the Cape Eleuthera Institute, Eleuthera Island, The Bahamas. Sampling was conducted in November 2009, July 2010, and in May and December 2011, thus encompassing the full range of seasonal temperature fluctuations. Fish were held in natural seawater at local ambient surface conditions (salinity in the range 36–37 on the practical salinity scale; temperature in the range 25–30 °C); all water having first passed through a 1 µm filter to ensure no external particles could be ingested by the fish. Food was withheld throughout the study to ensure that sample material comprised only gut-produced carbonates. To further facilitate sample purity, carbonate pellets were collected only after fish were held for an initial 48 hour period to ensure their guts were completely voided of other materials. Excreted carbonate pellets were then recovered from tank floors using disposable 10 mL Pasteur pipettes, typically at 24 hr intervals, before being cleaned with sodium hypochlorite (commercial bleach), rinsed with distilled water, and dried at 50 °C, following procedures recommended for the preparation of naturally occurring carbonates48. Animal collection and holding was conducted under approval by The Bahamas Department of Marine Resources and in accordance with animal care guidelines set out in UK Home Office Project Licence PPL 30/2735.

Tank floor recovery is a widely adopted approach to sampling piscine gut carbonates8, 12,13,14, 22, 45 but other methods include direct sampling from the intestinal tract (following animal euthanasia)8, 22, 45 and collection in a surgically attached rectal sac45. Direct sampling from the intestine was unsuitable here for two reasons. Firstly, animal euthanasia precludes the possibility of measuring carbonate production rates. Secondly, the stages involved in gut carbonate precipitation are poorly understood but it is possible that fish carbonates, like many other biogenic carbonates25, form via an amorphous precursor. The possibility then arises that precipitates are dominated by ACMC in the foregut but become increasingly more crystalline as they ‘mature’ towards the hindgut, as has been documented in at least one instance elsewhere22. Direct intestinal sampling thus has the potential to yield misleading compositional and mineralogical data. The rectal sac approach, which allows excreted solids and fluids to accumulate in isolation from surrounding seawater, is an excellent means of controlling for post-excretion processes affecting precipitates (e.g., dissolution) in experiments involving different seawater treatments22. However, for the purposes of this study it is problematic because the interval between excretion and retrieval of precipitates effectively represents an artificial lengthening of the time for which they are in contact with gut fluids, thus potentially prolonging precipitation and crystallisation processes. Consequently, this approach might also yield misleading mineralogical and compositional data.

Collection of excreted carbonates from tank floors is therefore the only sampling strategy in which we can be confident that products are representative of those entering the marine environment. A limitation of this approach, however, is that exposure of carbonates to seawater introduces the possibility of sample loss through dissolution; an issue likely to be most pronounced for ACMC, which can dissolve very rapidly in seawater22. For this reason, samples thought to contain ACMC (e.g., those produced by labrids and pomacentrids) were omitted from production rate determinations. For all other carbonate types (e.g., HMC ellipsoids, LMC spheres), we observed no differences in phase proportions or particle properties (morphology, composition, and phase) when comparing freshly excreted samples with those collected within 24 hrs of excretion by the same individual fish. This observation suggests these carbonate types undergo limited or no change within the first 24 hrs of seawater exposure.

It is further necessary to point out that fasting of study animals will have lowered their metabolic rates and potentially affected gut fluid composition, thus raising the possibility that samples collected during the study were not representative of fish carbonates produced under normal natural circumstances. However, gut carbonates excreted alongside faecal matter have been shown to be similar to those produced during periods of fasting13. Furthermore, samples produced by fasting barramundi (Lates calcarifer) are identical to those produced by the same individuals after a controlled diet of prawn flesh (n = 4) or squid flesh (n = 4) was introduced (Supplementary Fig. 2). Thus, available data suggest that carbonates produced by fasting fish are similar to those produced under normal natural circumstances, although further work on this subject is necessary.

Carbonate characterisation and phase abundance estimates

ATR-FTIR analyses were performed at a resolution of 2 cm−1 using a Nicolet 380 FTIR spectrometer coupled with a Thermo Scientific SMART iTR ATR sampler equipped with a diamond reflecting cell, with final spectra obtained by the co-addition of 32 repeated scans. Analyses were performed on at least three powdered sub-samples (each comprising 2–3 pellets) per species to ensure representative spectra were obtained. Identification of the carbonate phases was achieved through reference to an extensive spectral database (Supplementary Tables 4– 6). Additionally, some samples were analysed using transmission FTIR spectroscopy in order to better resolve peaks at low wavenumbers (<600 cm−1). Powdered CaCO3 pellets were homogenised with KBr and pressed into transparent discs (~0.5 mm thick) which were then analysed with a Nicolet FTIR spectrometer using analytical settings as described for ATR-FTIR spectroscopy.

Although FTIR spectroscopy is effective at discriminating between discrete carbonate phases, we found it unreliable for determining MgCO3 contents in fish-derived carbonates, despite the existence of a published relationship between ν4 (in-plane bending mode) peak position and MgCO3 content in well crystallised biogenic Mg calcites49. It is possible that this relationship does not hold for fish-derived Mg calcites due to their low degree of crystallinity (see Results). Consequently, where spectra indicate the presence of calcite, this may refer to any of LMC, HMC, or VHMC; more specific identification only being possible through acquisition of compositional and/or XRD data.

Samples were characterised with respect to morphology and chemical composition using scanning electron microscopy (SEM) and energy-dispersive X-ray spectroscopy (EDX) within a Zeiss Supra 40VP field emission gun system with integrated Oxford Instruments ISIS EDX detector. A minimum of 10 EDX scans were performed in discrete regions of each of at least 5 (and up to 30) pellets per fish species, incorporating all particle morphotypes known to be produced by each. Because the spatial resolution of these scans exceeds the size of many of the subject particles, scans were only performed if subject particles were surrounded by similar particles, or if they were of sufficient size to overcome this issue. Detailed results concerning MgCO3 contents determined using this approach are presented elsewhere13. Briefly, variability in MgCO3 content within species is most pronounced when comparing different particle morphotypes. For example, sample- and species-specific MgCO3 contents are typically higher in micron-scale ellipsoids (e.g., typically ~25–35 mol%) than they are in ~20 µm dumbbells (e.g., typically ~5–15 mol%). In addition, within some particle morphotypes there can be considerable variability among samples produced by any given fish species (e.g., 1 S.D. can be as large as 9 mol% MgCO3) and even within samples produced by individual fish, with the greatest variability being seen in ACMC (nanospheres and material lacking any definable morphology) and VHMC (ellipsoids). It is worth mentioning here that controls on Mg2+ incorporation in calcites generally can be complex and wide-ranging, but a positive correlation between MgCO3 content and temperature is frequently reported50. However, we found no significant differences in the MgCO3 contents of each particle morphotype when comparing samples obtained in winter (SST ≈ 25 °C) with those obtained from the same fish species in summer (SST ≈ 30 °C), suggesting that seasonal SST fluctuations in The Bahamas are insufficient to influence gut carbonate magnesium contents.

Compositional and morphological data were then combined with FTIR data to facilitate assignment of carbonate phases (i.e., calcite categorised by mol% MgCO3 content, aragonite, monohydrocalcite, ACMC, or brucite) to each morphotype. In some samples the presence of a single mineral phase (as indicated by FTIR data) meant assignment of phase to morphotype was straightforward. However, many samples comprised multiple phases and it was then necessary to differentiate morphotypes on the basis of magnesium and strontium contents (using morphotype-specific compositional data from EDX spectroscopy) before assigning phases in accordance with published phase–composition relationships51, 52. Variability of MgCO3 content within morphotypes was generally not problematic in this regard because it was most pronounced in ACMC and VHMC, both of which are defined by a broad range of MgCO3 contents (i.e., no specified limits in ACMC and >25 mol% in VHMC). Where MgCO3 contents did span two or more phase categories (e.g., VHMC and HMC with 15–25 mol% MgCO3), we apportioned a relative abundance to each based on the average spread of MgCO3 contents for the species concerned. This approach was performed for samples produced by 16 fish species, and morphotype phases were generally consistent among these (e.g., all monocrystalline ellipsoids were VHMC or HMC). Samples from an additional 6 species were of insufficient size for FTIR and XRD analyses, so phases were assigned using only morphological and compositional data on the assumption that morphotype phases are consistent among all fish species (compositional data support this assumption). Following phase assignments, >30 pellets from each species were examined using SEM to facilitate visual estimation of the volumetric abundances of all morphotypes, and thus phases.

Finally, we extrapolate our abundance estimates across entire fish families by averaging the totals for species within each family tested. The validity of this approach is substantiated by a pattern emerging from published data13 and our ongoing work that indicates strong intra-family consistency in precipitation products. For example, of nine lutjanid species we have tested, all predominantly produce (V)HMC ellipsoids, and of eleven labrid species tested, all produce ACMC with subsidiary LMC. Precipitation products are similarly consistent for all families (n = 13) in which multiple species have been tested, these including serranids (n = 10), pomacentrids (n = 3), and scorpaenids (n = 4).

Production rates and modelling

Production rates were determined using carbonates excreted over known time (typically 24–48 hours) by fish of known mass. The mass of excreted carbonates was determined from cleaned dried samples either by weighing, or by acid-base titration using 0.02 M HCl and 0.02 M NaOH; the amount of acid required to dissolve the entire sample being used to calculate the number of moles of (Ca,Mg)CO3 in the original sample. Results were then converted to weight values (accounting for known ratios of MgCO3 to CaCO3), which typically differed from direct weight measurement values by <2%.

Measured production rates, however, are highly conservative because they are derived from starved and inactive fish (inactivity being a consequence of confinement). The cumulative effect of these experimental conditions will have been to lower metabolic rates and thus ultimately to lower carbonate production rates1. Estimates of scaling factors that account for the difference between normal metabolic rates and those depressed through removal of feeding and physical activity are in the range 2.5–3.453; the lowest of these values being employed elsewhere1 to conservatively adjust measured fish carbonate production rates to more practical real-world values. We follow this approach in order to generate realistic estimates of fish carbonate production rate in The Bahamas.

Production calibration data were then analysed by regressing production rates against log-transformed values of fish biomass and a quadratic term for log biomass to account for any potential curvilinear relationships. Fish family was included as a random factor, so analyses used mixed-effects linear models in the nlme package54 in R statistical software55. In addition to the data from fish families measured empirically, the model included an ‘other’ family, parameterised as the mean biomass and production rate of all other families. This additional family category allowed the model to be used to predict production rates by fishes from all other families where species-level data were unavailable. Models were fitted using the procedure outlined by Crawley56. Briefly, a maximal model was fitted including all factors. Least significant terms were then removed in turn, and after each term was removed models were compared to ensure that term removal did not lead to a significant increase in deviance or Akaike information criterion (AIC). Terms were removed until the model contained only significant terms or removal of any non-significant terms caused a significant increase in deviance or AIC (minimal adequate model; see Supplementary Methods 1).

Data for fish abundances across The Bahamas are described in detail elsewhere57, so are only briefly described here. Data were collected from replicate sites in all major hard- and soft-bottom habitats found around each of nine islands: Abaco, Andros, Bimini, Conception, Eleuthera, Grand Bahama, Lee Stocking, San Salvador, and the Turks and Caicos, and from sites in and around the Exuma Cays Land and Sea Park (ECLSP). Sites were selected from seven generalised habitats of known areal extent, as delineated by Perry et al.12, of which ‘reefs’ and ‘hard bottoms’ are further sub-divided on the basis of ecology and/or geomorphology–see Supplementary Table 3 for classification scheme. At each site, all but nocturnal (e.g., Apogonidae) and cryptic (e.g., Clinidae and Gobiidae) fish species were surveyed using discrete group visual fish census58. The exclusion of data on cryptic species may mean that our overall rate estimates are somewhat conservative. However, the extent of underestimation may be limited given that small cryptic fish species not seen during visual surveys in a different reef system, although abundant, reportedly account for only 1% of total biomass59. Species were divided into three groups and density and size (to nearest cm) estimated along belt transects. Transect size and number was optimized through the use of data from equivalent surveys within the Caribbean60.

The calibration model was then used to generate species- or family-specific production rates for every teleost fish seen during field surveys. Firstly, data on fish lengths were converted to biomass using allometric relationships61, and these biomasses were used to generate production estimates from the model. The family-specific mean phase proportions (including variations of MgCO3 content in calcites) were then used to separate the total carbonate production per fish into production values of each phase per fish. Estimates for the entire fish assemblage seen on each transect were then summed and averaged across transects to produce an estimate of mean production per transect for each fish group. All values were standardised to production per 200 m2, and mean production per 200 m2 for each of the three fish groups were summed to provide production estimates for the entire assemblage per site. Since multiple sites were surveyed per habitat type, data were averaged to generate mean production rates of each morphotype and phase in each habitat type.

Additional information

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.


  1. 1.

    Wilson, R. W. et al. Contribution of fish to the marine inorganic carbon cycle. Science 323, 359–362 (2009).

  2. 2.

    Fabry, V. J. Shell growth rates of pteropod and heteropod molluscs and aragonite production in the open ocean: Implications for the marine carbonate system. J. Mar. Res. 48, 209–222 (1990).

  3. 3.

    Milliman, J. D. Production and accumulation of calcium carbonate in the ocean: budget of a nonsteady state. Global Biogeochem. Cycles 7, 927–957 (1993).

  4. 4.

    Schiebel, R. Planktic foraminiferal sedimentation and the marine calcite budget. Globl Biogeochem. Cycles 16, 1065, doi:10.1029/2001GB001459 (2002).

  5. 5.

    Iglesias-Rodriguez, D. et al. Progress made in the study of the ocean’s calcium carbonate budget. Eos 83, 365–375 (2002).

  6. 6.

    Lebrato, M. et al. Global contribution of echinoderms to the marine carbon cycle: CaCO3 budget and benthic compartments. Ecol. Monogr. 80, 441–467 (2010).

  7. 7.

    Yates, K. K. & Robbins, L. L. Geological perspectives of global climate change (eds Gerhard, L. C., Harrison, W. E. & Hanson, B. M.) Ch. 14, 267–283 (AAPG, 2001).

  8. 8.

    Woosley, R. J., Millero, F. J. & Grosell, M. The solubility of fish-produced high magnesium calcite in seawater. J. Geophys. Res. 117, C04018 (2012).

  9. 9.

    Lutz, S. J. & Martin, A. H. Fish Carbon: Exploring Marine Vertebrate Carbon Services (GRID-Arendal, Arendal, 2014).

  10. 10.

    Wilson, R. W., Wilson, J. M. & Grosell, M. Intestinal base secretion by marine teleost fish–why and how? Biochim. Biophys. Acta 1566, 182–193 (2002).

  11. 11.

    Grosell, M. Intestinal anion exchange in marine teleosts is involved in osmoregulation and contribute to the oceanic inorganic carbon cycle. Acta Physiol. 202, 421–434 (2011).

  12. 12.

    Perry, C. T. et al. Fish as major carbonate mud producers and missing components of the tropical carbonate factory. Proc. Natl. Acad. Sci. USA 108, 3865–3869 (2011).

  13. 13.

    Salter, M. A., Perry, C. T. & Wilson, R. W. Production of mud-grade carbonates by marine fish: crystalline products and their sedimentary significance. Sedimentology 59, 2172–2198 (2012).

  14. 14.

    Salter, M. A., Perry, C. T. & Wilson, R. W. Size fraction analysis of fish-derived carbonates in shallow sub-tropical marine environments and a potentially unrecognised origin for peloidal carbonates. Sed. Geol. 314, 17–30 (2014).

  15. 15.

    Ware, J. R., Smith, S. V. & Reaka-Kudla, M. J. Coral reefs: sources or sinks of atmospheric CO2? Coral Reefs 11, 127–130 (1992).

  16. 16.

    Feely, R. A. et al. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305, 362–366 (2004).

  17. 17.

    Walter, L. M. & Morse, J. W. Magnesian calcite stabilities: a re-evaluation. Geochim. Cosmochim. Acta 48, 1059–1069 (1984).

  18. 18.

    Bischoff, W. D., Mackenzie, F. T. & Bishop, F. C. Stabilities of synthetic magnesian calcites in aqueous solution: comparison with biogenic materials. Geochim. Cosmochim. Acta 51, 1413–1423 (1987).

  19. 19.

    Morse, J. W. & Mackenzie, F. T. Geochemistry of Sedimentary Carbonates (Elsevier, Amsterdam, 1990).

  20. 20.

    Matthews, R. K. Genesis of recent lime mud in Southern British Honduras. J. Sed. Pet. 36, 428–454 (1966).

  21. 21.

    Gischler, E., Dietrich, S., Harris, D., Webster, J. M. & Ginsburg, R. N. A comparative study of modern carbonate mud in reefs and carbonate platforms: Mostly biogenic, some precipitated. Sed. Geol. 292, 36–55 (2013).

  22. 22.

    Foran, E., Weiner, S. & Fine, M. Biogenic fish-gut calcium carbonate is a stable amorphous phase in the gilt-head seabream, Sparus aurata. Sci. Rep. 3, article no. 1700 (2013).

  23. 23.

    Brečević, L. & Nielsen, A. E. Solubility of amorphous calcium carbonate. J. Cryst. Growth 98, 504–510 (1989).

  24. 24.

    Jennings, S. & Wilson, R. W. Fishing impacts on the marine inorganic carbon cycle. J. Appl. Ecol. 46, 976–982 (2009).

  25. 25.

    Radha, A. V., Forbes, T. Z., Killian, C. E., Gilbert, P. U. P. A. & Navrotsky, A. Transformation and crystallization energetics of synthetic and biogenic amorphous calcium carbonate. Proc. Natl. Acad. Sci. USA 107, 16438–16443 (2010).

  26. 26.

    Politi, Y., Arad, T., Klein, E., Weiner, S. & Addadi, L. Sea urchin spine calcite forms via a transient amorphous calcium carbonate phase. Science 306, 1161–1164 (2004).

  27. 27.

    Bonneau, M.-C. et al. Variations isotopiques (oxygène et carbone) et cristallographiques chez les espèces actuelles de Foraminifères planctoniques en function de la profondeur de dépôt. Bull. Soc. Géol. France 7, 791–793 (1980).

  28. 28.

    Mumby, P. J. et al. Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311, 98–101 (2006).

  29. 29.

    Harborne, A. R. et al. Reserve effects and natural variation in coral reef communities. J. Appl. Ecol. 45, 1010–1018 (2008).

  30. 30.

    Sluka, R. et al. Density, species and size distribution of groupers (Serranidae) in three habitats at Elbow Reef, Florida Keys. Bull. Mar. Sci. 62, 219–228 (1998).

  31. 31.

    Côté, I. M., Mosqueira, I. & Reynolds, J. D. Effects of marine reserve characteristics on the protection of fish populations: a meta-analysis. J. Fish. Biol. 59, 178–189 (2001).

  32. 32.

    Purdy, E. G. Recent calcium carbonate facies of the Great Bahama Bank. 2. Sedimentary Facies. J. Geol. 71, 472–497 (1963).

  33. 33.

    Wilber, R. J., Milliman, J. D. & Halley, R. B. Accumulation of bank-top sediment on the western slope of the Great Bahama Bank: rapid progradation of a carbonate megabank. Geology 18, 970–974 (1990).

  34. 34.

    Graham, N. A. J. & McClanahan, T. R. The last call for marine wilderness? Bioscience 63, 397–402 (2013).

  35. 35.

    Morse, J. W., Andersson, A. J. & Mackenzie, F. T. Initial responses of carbonate-rich shelf sediments to rising atmospheric ρCO2 and “ocean acidification”: Role of high Mg-calcites. Geochim. Cosmochim. Acta 70, 5814–5830 (2006).

  36. 36.

    Plummer, L. N. & Mackenzie, F. T. Predicting mineral solubility from rate data; application to dissolution of magnesian calcites. Am. J. Sci. 274, 61–83 (1974).

  37. 37.

    Thorstenson, D. C. & Plummer, L. N. Equilibrium criteria for two component solids reacting with fixed composition in an aqueous phase-example: the magnesian calcites. Am. J. Sci. 277, 1203–1233 (1977).

  38. 38.

    Lee, K. et al. Global relationships of total alkalinity with salinity and temperature in surface waters of the world’s oceans. Geophys. Res. Lett. 33, L19605, doi:10.1029/2006GL027207 (2006).

  39. 39.

    Morse, J. W., Millero, F. J., Thurmond, V., Brown, E. & Ostlund, H. G. The chemistry of Grand Bahama Bank waters: After 18 years another look. J. Geophys. Res. 89, 3604–3614 (1984).

  40. 40.

    Taylor, G. F. The occurrence of monohydrocalcite in two small lakes in the southeast of South Australia. Am. Mineral. 60, 690–697 (1975).

  41. 41.

    Munemoto, T. & Fukushi, K. Transformation kinetics of monohydrocalcite to aragonite in aqueous solutions. J. Mineral. Petrol. Sci. 103, 345–349 (2008).

  42. 42.

    Nothdurft, L. D. et al. Brucite microbialites in living coral skeletons: Indicators of extreme microenvironments in shallow-marine settings. Geology 33, 169–172 (2005).

  43. 43.

    Keir, R. S. The dissolution kinetics of biogenic calcium carbonates in seawater. Geochim. Cosmochim. Acta 44, 241–252 (1980).

  44. 44.

    Patterson, W. P. & Walter, L. M. Syndepositional diagenesis of modern platform carbonates: Evidence from isotopic and minor element data. Geology 22, 885–888 (1994).

  45. 45.

    Heuer, R. M. et al. Changes to intestinal transport physiology and carbonate production at various CO2 levels in a marine teleost, the Gulf toadfish (Opsanus beta). Physiol. Biochem. Zool. 89, 402–416 (2016).

  46. 46.

    Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).

  47. 47.

    Christensen, V. et al. A century of fish biomass decline in the ocean. Mar. Ecol. Prog. Ser. 512, 155–166 (2014).

  48. 48.

    Gaffey, S. J. & Bronnimann, C. E. Effects of bleaching on organic and mineral phases in biogenic carbonates. J. Sed. Pet. 63, 752–754 (1993).

  49. 49.

    Böttcher, M. E., Gehlken, P.-L. & Steele, D. F. Characterisation of inorganic and biogenic magnesian calcites by Fourier Transform infrared spectroscopy. Solid State Ionics 101, 1379–1385 (1997).

  50. 50.

    Wasylenki, L. E., Dove, P. M. & De Yoreo, J. J. Effects of temperature and transport conditions on calcite growth in the presence of Mg2+: implication for paleothermometry. Geochim. Cosmochim. Acta 69, 4227–4236 (2005).

  51. 51.

    Mucci, A. & Morse, J. W. The incorporation of Mg2+ and Sr2+ into calcite overgrowths: Influences of growth rate and solution composition. Geochim. Cosmochim. Acta 47, 217–233 (1983).

  52. 52.

    Carpenter, S. J. & Lohmann, K. C. Sr/Mg ratios of modern marine calcite: Empirical indicators of ocean chemistry and precipitation rate. Geochim. Cosmochim. Acta 56, 1837–1849 (1992).

  53. 53.

    Kerr, S. R. Estimating the energy budgets of actively predatory fishes. Can. J. Fish. Aquat. Sci. 39, 371–379 (1982).

  54. 54.

    Pinheiro, J. C., Bates, D., DebRoy, S., Sarkar, D. & R Core Team nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–113 (Vienna, Austria: R Development Core Team, 2013).

  55. 55.

    R Development Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing (Vienna, Austria, 2008).

  56. 56.

    Crawley, M. J. The R Book (John Wiley & Sons Ltd., Chichester, England, 2007).

  57. 57.

    Harborne, A. R. et al. Tropical coastal habitats as surrogates of fish community structure, grazing, and fisheries value. Ecol. Appl. 18, 1689–1701 (2008).

  58. 58.

    Greene, L. E. & Alevizon, W. S. Comparative accuracies of visual assessment methods for coral reef fishes. Bull. Mar. Sci. 44, 899–912 (1989).

  59. 59.

    Ackerman, J. L. & Bellwood, D. R. Reef fish assemblages: a re-evaluation using enclosed rotenone stations. Mar. Ecol. Prog. Ser. 206, 227–237 (2000).

  60. 60.

    Mumby, P. J. et al. Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427, 533–536 (2004).

  61. 61.

    Froese, R. & Pauly, D. Fish Base. World Wide Web electronic publication: (2013).

  62. 62.

    Bruckner, A. et al. Khaled bin Sultan Living Oceans Foundation Atlas of Saudi Arabian Red Sea Marine Habitats (Panoramic Press, Phoenix, AZ, 2012).

  63. 63.

    Monaco, M. E. et al. National Summary of NOAA’s Shallow-water Benthic Habitat Mapping of U.S. Coral Reef Ecosystems. NOAA Technical Memorandum NOS NCCOS 122. Prepared by the NCCOS Center for Coastal Monitoring and Assessment Biogeography Branch (Silver Spring, MD, 2012).

  64. 64.

    Hull, H. & Turnball, A. G. A thermochemical study of monohydrocalcite. Geochim. Cosmochim. Acta 87, 685–694 (1973).

  65. 65.

    Clarkson, J. R., Price, T. J. & Adams, C. J. Role of metastable phases in the spontaneous precipitation of calcium carbonate. J. Chem. Soc. 88, 243–249 (1992).

  66. 66.

    Milliman, J. D. et al. Biologically mediated dissolution of calcium carbonate above the chemical lysocline? Deep Sea Res. Part I 46, 1653–1669 (1999).

Download references


M.A.S., C.T.P., and R.W.W. acknowledge financial support from the UK National Environmental Research Council (NERC) through grants NE/K003143/1 and NE/G010617/1. A.R.H. was funded through NERC fellowship NE/F015704/1, and by the Australian Research Council (ARC) through fellowship DE120102459. We thank Annabelle Brooks and Aaron Shultz (Cape Eleuthera Institute, Bahamas) for their invaluable assistance with fieldwork. This is contribution #XX of the Marine Education and Research Center in the Institute for Water and Environment at Florida International University.

Author information


  1. Geography, College of Life and Environmental Sciences, University of Exeter, Amory Building, Rennes Drive, Exeter, EX4 4RJ, UK

    • Michael A. Salter
    •  & Chris T. Perry
  2. Department of Biological Sciences, Florida International University, North Miami, Florida, 33181, USA

    • Alastair R. Harborne
  3. Marine Spatial Ecology Laboratory and Australian Research Council Centre of Excellence for Coral Reef Studies, School of Biological Sciences, Goddard Building, The University of Queensland, Brisbane, QLD 4072, Australia

    • Alastair R. Harborne
  4. Biosciences, College of Life and Environmental Sciences, University of Exeter, Geoffrey Pope Building, Stocker Road, Exeter, EX4 4QD, UK

    • Rod W. Wilson


  1. Search for Michael A. Salter in:

  2. Search for Alastair R. Harborne in:

  3. Search for Chris T. Perry in:

  4. Search for Rod W. Wilson in:


Research was initiated by C.T.P. and R.W.W., and this study was conceived through discussion between C.T.P., M.A.S., and A.R.H. Collection and analysis of fish carbonates was performed by M.A.S., C.T.P., and R.W.W. Fish biomass modelling and habitat mapping was performed by A.R.H., who calibrated the CaCO3 production rates to generate model outputs. M.A.S. analysed the model and wrote the manuscript. C.T.P., A.R.H., and R.W.W. all contributed to the manuscript.

Competing Interests

The authors declare that they have no competing interests.

Corresponding author

Correspondence to Michael A. Salter.

Electronic supplementary material

About this article

Publication history






By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.