Fish as major carbonate mud producers and missingcomponents of the tropical carbonate factoryChris T. Perrya,1, Michael A. Saltera, Alastair R. Harborneb, Stephen F. Crowleyc, Howard L. Jelksd, and Rod W. Wilsonb,1

aSchool of Science and the Environment, Manchester Metropolitan University, Chester Street, Manchester M1 5GD, United Kingdom; bBiosciences, Collegeof Life and Environmental Sciences, University of Exeter, Exeter EX4 4PS, United Kingdom; cDepartment of Earth and Ocean Sciences, University ofLiverpool, 4 Brownlow Street, Liverpool L69 3GP, United Kingdom; and dUS Geological Survey, 7920 North West 71st Street, Gainesville, FL 32653

Edited* by George N. Somero, Stanford University, Pacific Grove, CA, and approved January 6, 2011 (received for review November 2, 2010)

Carbonate mud is a major constituent of recent marine carbonatesediments and of ancient limestones, which contain unique recordsof changes in ocean chemistry and climate shifts in the geologicalpast. However, the origin of carbonate mud is controversial andoften problematic to resolve. Here we show that tropical marinefish produce and excrete various forms of precipitated (nonskele-tal) calcium carbonate from their guts (“low” and “high”Mg-calciteand aragonite), but that very fine-grained (mostly <2 μm) highMg-calcite crystallites (i.e., >4 mole % MgCO3) are their dominant ex-cretory product. Crystallites from fish are morphologically diverseand species-specific, but all are unique relative to previously knownbiogenic and abiotic sources of carbonate within open marinesystems. Using site specific fish biomass and carbonate excretionrate data we estimate that fish produce ∼6.1 × 106 kg CaCO3∕yearacross the Bahamian archipelago, all as mud-grade (the <63 μmfraction) carbonate and thus as a potential sediment constituent.Estimated contributions from fish to total carbonate mud produc-tion average ∼14% overall, and exceed 70% in specific habitats.Critically, we also document the widespread presence of these dis-tinctive fish-derived carbonates in the finest sediment fractionsfrom all habitat types in the Bahamas, demonstrating that thesecarbonates have direct relevance to contemporary carbonatesediment budgets. Fish thus represent a hitherto unrecognizedbut significant source of fine-grained carbonate sediment, thediscovery of which has direct application to the conceptual ideasof how marine carbonate factories function both today and inthe past.

marine teleost ∣ fish intestine ∣ carbonate production

Marine carbonates contain unique records of changes inocean chemistry, biogeochemical cycling, and benthic and

pelagic ecology (1), and therefore provide vital informationon climate shifts in the geological past. A distinctive and oftenvolumetrically important component of these sediments is carbo-nate mud (the <63 μm sediment fraction). However, the originsof both aragonitic andMg-calcite carbonate muds remains a topicof long-standing debate (2, 3). Indeed, where attempts have beenmade to quantify sources of the fine sediment fraction a high pro-portion remains of unknown origin (e.g., up to 40% in Bahamiansediments and between 28 and 36% in Belize lagoon sediments)(4, 5). This problem arises in part because, with the exception ofinorganic carbonate precipitation (e.g., the carbonate “whiting”controversy) (3, 6–8), the processes of carbonate mud productionnecessarily invoke the degradation of larger bioclasts (skeletalfragments of marine organisms) to produce mud-grade carbo-nate, and/or grain recrystallization to produce high Mg-calcitemuds (9–11). Thus attempts to determine primary mud sourcesand production budgets are often hampered because of grainobliteration. The mineralogical composition of the mud fractionof modern tropical carbonate sediment is also very variablebetween settings: in some environments the finest sediment frac-tions are predominantly aragonite (12, 13), but high Mg-calcitecan account for in excess of 40% of the mud fraction in manysettings (14–16). Ultimately variable admixtures of both arago-

nite and Mg-calcite mud-grade carbonate occur and thus budget-ary considerations need to accommodate production from arange of potential sources. This issue has important geo-environ-mental implications because carbonate muds are major constitu-ents of limestones and are volumetrically important in mostmodern shallow marine carbonate environments (17). Further-more, the presence of Mg-calcite muds in marine carbonates isconsidered critical to preserving primary sediment textures andfabrics (15), thus influencing sediment porosity and permeabilitywhich are of critical importance to fluid flow in limestonesequences. Mud production in ancient limestones has proven par-ticularly perplexing because evidence is often lacking for the pre-sence of species that are regarded as key modern mud producers(especially the calcareous green algae) (18).

Recent observations of carbonate crystals growing within, andbeing continually excreted from, the intestines of temperate fishspecies (19) lead us to speculate that such crystals could representa hitherto unrecognized source of mud-grade carbonate in shal-low tropical marine environments. In these shallow marine envir-onments carbonate production rates are typically high andpreservation potential is good because of high carbonate satura-tion states in the overlying waters. The process by which fish pre-cipitate carbonate crystals within their guts has been documentedin some detail (19–22) and occurs within the teleosts (bony fish)that dominate the marine fish fauna. Briefly, precipitation occursas a by-product of the osmoregulatory requirement of teleoststo continuously drink Ca- and Mg-rich seawater. Subsequentintestinal bicarbonate secretion generates exceptionally high con-centrations of HCO3

− (50–100 mM) and very high pH values(up to 9.2) which leads to the alkaline precipitation of calciumand magnesium within ingested seawater as insoluble carbonatesalong the intestine (19–24; Fig. 1). Carbonate precipitation isbelieved to occur within the mucus that is secreted along the en-tire length of the intestinal lumen (21, 23, 24), and carbonates aresubsequently excreted within mucus-coated pellets. Followingtheir excretion the rapid degradation of the organic mucus matrixis assumed to release inorganic crystals into the water column(19). Whilst the physiological processes driving fish carbonateproduction are thus increasingly well understood, the morpholo-gical characteristics of such carbonates and their sedimentologi-cal significance have never been considered.

Results and DiscussionIn order to study the morphological and compositional character-istics of carbonates produced by tropical marine fish, carbo-

Author contributions: C.T.P. and R.W.W. designed research; C.T.P., M.A.S., A.R.H., andR.W.W. performed research; H.L.J. contributed new reagents/analytic tools; C.T.P.,M.A.S., A.R.H., S.F.C., and R.W.W. analyzed data; and C.T.P., M.A.S., A.R.H., S.F.C., andR.W.W. wrote the paper.

The authors declare no conflict of interest.

*This Direct Submission article had a prearranged editor.1To whom correspondence may be addressed. E-mail: c.t.perry@mmu.ac.uk or r.w.wilson@ex.ac.uk.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1015895108/-/DCSupplemental.

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nate samples were obtained from 11 common fish species (seeSI Appendix) collected from shallow water sites on the EleutheraBank, Bahamas (SI Appendix: Fig. S1). This area was selected forstudy as it combines warm, shallow waters that are supersaturatedwith respect to CaCO3, and comprises a range of typical carbo-nate platform sedimentary environments. The mucus-coatedpellets excreted from fish guts that contain the carbonate preci-pitates vary in shape and size with fish species (SI Appendix:Fig. S2), but subsequent degradation of the organic mucus phasein the laboratory, through dilute hypochlorite treatments (seeSI Appendix), releases inorganic carbonate pellets up to 2 mmin size. Each pellet comprises huge numbers of individual crystal-lites and polycrystalline precipitates (in most cases estimated at>106 per pellet; SI Appendix: Fig. S2), along with an amorphous“matrix” of finer (<0.25 μm) carbonate. When subjected to evengentle ultrasonic agitation, rapid pellet disaggregation occurs, re-sulting in the release of large volumes of fine-grained crystallites(SI Appendix: Fig. S3).

Different fish species produce different types of pellet(in terms of size, shape, and density of precipitate packing) thatconsist of crystallites and polycrystalline aggregates of varyingsize and morphology (Fig. 1 and SI Appendix: Figs. S4–S14),although most are <2 μm in size. Despite the differences be-tween species, four particularly common morphologies occurfrom the range of fish examined: ellipsoidal; straw bundle-shaped; dumbbell-shaped; and spheroidal (Fig. 2 A–D). In addi-tion, several less common morphologies occur including: (i) semi-spherical polycrystalline aggregates (Fig. 2E); (ii) polycrystallineaggregates that are rod-like (Fig. 2F), or form intertwinedcrosses; and (iii) “splayed ellipsoids” (Fig. 2G). These crystallitemorphologies are highly distinctive and fundamentally differfrom those associated with all known biogenic and abiotic sourcesof carbonate within tropical marine carbonate systems, includingthe basic crystal structures that build the skeletons of commontropical carbonate sediment producing species (10, 11). Thisobservation alone has major significance from the perspectiveof establishing the origins of marine carbonate muds.

High Mg-calcite (i.e., >4 mole% MgCO3) is the dominantcarbonate phase precipitated by these tropical fish species.This finding is confirmed in X-ray diffraction (XRD) analysisof bulk samples from a range of the fish examined (SI Appendix:Fig. S15 A and B), and in energy dispersion X-ray microanalysis(EDX) of the dominant crystallite morphologies produced byeach fish species (Fig. 3 and SI Appendix: Figs. S4–S14 ). XRDanalyses also indicates that some fish species precipitate “low”(i.e., <4 mole% MgCO3) Mg-calcite phases along with smallvolumes (typically less than a few %) of aragonite (SI Appendix:Fig.S15 A and B). Of particular interest is that recently excretedsamples (collected with 24 h) from all fish species predominantlycomprise “high” Mg-calcite phases, with average MgCO3 con-tents ranging from 18–39 mol% dependant on species (Fig. 3).These Mg levels are considerably higher than those from othercarbonate producers at comparable latitudes (Fig. 3), and arealso well above the average MgCO3 content of both tropicalmarine carbonate sediments (13.5 mol% MgCO3) and naturallyoccurring marine inorganic Mg-calcite cements (11.9 mole%MgCO3) (26). However, as we discuss below, our preliminary

Fig. 1. Fish carbonate production and precipitation products. Schematicdiagram illustrating the processes associated with carbonate precipitationwithin the intestines of fish and the dominant crystallite morphologies iden-tified in this study to be produced by tropical fish species.

Fig. 2. Common morphologies of tropical fish-produced carbonate precipi-tates. (A) Type 1—Ellipsoidal crystallites (size range: <0.25 to 3 μm long);(B) Type 2—Straw-bundle crystallites (size range: 1–3 μm long); (C) Type 3—Polycrystalline dumbbell-shaped aggregates (size range: typically 1–3 μmlong, but large examples to ∼10–15 μm also occur); (D) Type 4—Polycrystal-line spheroidal aggregates (size range: <10 to 30 μmdiameter). Occur both asdiscrete spheres and as multilobate aggregations of spheres; (E) Large poly-crystalline aggregates with a semisphere morphology (size range: ∼5 to∼30 μm diameter); (F) Elongate rod-like crystallites which often occur asintergrown bundles of crystallites (size range: 2–3 μm long); (G) Splayedellipsoidal crystallites (size range ∼2 μm long and narrow towards their term-inal points).

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data indicate that recrystallization of fish carbonates to a lowerMg-calcite state seems to occur subsequent to their excretion inthe natural marine environment (a key point in relation to thepreservation potential of fish carbonates).

A crude relationship is observed between crystal formand mole fraction of MgCO3. Samples with the highest averageMgCO3 contents (means ranging from33.7 to 39.6mol%MgCO3)being dominated by small (1–2 μm) ellipsoidal and dumbbellmorphology crystallites, while samples with lower MgCO3 con-tents (means range from 18.6 to 23.1 mol % MgCO3) are domi-nated by larger (10–20 μm) spheroids (Fig. 3). We speculate thatthis variability may reflect a progressive reduction in the MgCO3

content of crystallites as they grow larger and/or as the crystalliteforms evolve during growth. These ideas remain to be tested.

The unusual occurrence of the observed crystal forms andthe precipitation of crystals outside normal stability ranges ofMg-calcite, raises a number of questions about controls on car-bonate precipitation inside the guts of fish and how stable thesecarbonate forms are once excreted. To our knowledge such crys-tallite forms have not previously been described within openmarine systems, the only similar crystals having been describedfrom natural marine environments deriving from intertidal mi-crobial mats, where dumbbell-, rod- and sphere-type morpholo-gies have been identified as bacterially-mediated precipitates(27). It is also the case that numerous in vitro studies have growncrystals with very similar morphologies through both syntheticinorganic and organically-induced precipitation, but that thoseshowing the greatest similarity to fish carbonates were also bac-terially mediated (28, 29). This observation raises some funda-mental questions about the potential role of microbial activityin mediating carbonate precipitation and growth within the intes-tines of marine teleost fish, even though antibiotic treatment waspreviously shown to have no obvious effect, at least quantitatively,on total gut carbonate production in one species of marine fish(20). However, it is also the case that fish intestinal fluids arehypo-saline with respect to normal seawater (approximately onethird of ambient seawater) and this, alongside observed differ-ences in pH, Ca2þ, Mg2þ, HCO3

−, and CO32− levels longitudin-

ally within the intestines of temperate fish species (23), indicatesthat these carbonates are formed under conditions with a distinc-tive chemistry compared to other marine calcifiers.

While both the high MgCO3 content and the crystallitemorphologies observed distinguish these fish carbonates from

those previously documented in tropical marine environments,two significant questions arise that are pertinent to the wider sig-nificance of fish crystal production in the tropics. First, how muchtotal carbonate do tropical fish produce? And second, how sig-nificant is this carbonate in the context of carbonate mud produc-tion? To address the first question, we measured fish body massand carbonate excretion rates in 11 different Bahamas fish spe-cies (see SI Appendix). Average production rates vary betweenspecies and range from ∼10 × g CaCO3∕kg fish/year in barracu-da (Sphyraena barracuda) to >80 × g CaCO3∕kg fish/year inschoolmaster (Lutjanes apodus). However, production rates arestrongly dependent upon body mass (scaling similarly to meta-bolic rate—see SI Appendix: Fig. S16 for further details), such thatsmaller fish produce relatively more carbonate on a mass-specificbasis (see SI Appendix). By combining this production rate datawith habitat-specific fish biomass data from sites around theBahamas and with the measured area of each habitat, it is thenpossible to scale our data to consider fish carbonate productionrates at regional spatial scales (see SI Appendix). On this basiswe estimate that fish produce ∼6.1 × 106 kg CaCO3 across theBahamian archipelago each year (an area of ∼111;577 km2).Major contributions from fish derive from gorgonian-hardgroundhabitats (∼2.3 × 106 kg CaCO3 year−1) and medium-density sea-grass beds (∼1.2 × 106 kg CaCO3 year−1) reflecting the largeareas these habitats cover, but the highest rates per unit areaoccur in reef habitats and within mangrove-fringed embay-ments, reflecting much higher densities of fish biomass (Fig. 4).It is important to point out, however, that these figures are likelyto be highly conservative because: (i) the habitat mapping doesnot delineate individual patch reefs across the sand and seagrassdominated platform environments, but which are focal points ofhigh fish biomass in these areas; and (ii) because our calculationsare based primarily on fish biomass data from areas that areoutside marine reserves (i.e., our surveyed areas are significantlyreduced by fishing). Within reef and gorgonian-hardground ha-bitats, for example, fish-derived carbonate production increasesby 202% and 139% respectively, when biomass data from onlythose sites inside marine reserves are used, and even higherrates would be expected under historical “pristine” ecologicalconditions (30).

To address the question about contributions to mud produc-tion, we compared our measures of fish carbonate productionagainst regional estimates of mud production for different plat-form top habitats (see SI Appendix). On this basis, we estimate

Fig. 3. Comparison of mole% MgCO3 of fish-derived carbonates and skele-tal Mg-calcite producing benthic organisms. Latitudinal data for skeletalbenthic organisms (white circles) from Chave (25). Fish-derived data fromEleuthera at 25° N plotted as average MgCO3 contents (þ∕ − 1 s:d:) (blackcircles) based on EDX analysis (n ¼ 50 analyses per fish) of dominant crystal-lite morphologies observed in each species. Samples are grouped based onthe dominant crystal morphology associated with each fish species.

Fig. 4. Estimates of fish carbonate production across the Bahamian archipe-lago. Summary diagram showing estimated volumes of carbonate (millionskg CaCO3∕yr) produced in different habitats across the Bahamas. Productionvolume estimates are based on measured fish body mass and carbonateexcretion data, combined with known habitat-specific fish biomass datafor the region (see SI Appendix: Methods).

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that fish contribute an average ∼14% to total estimated carbonatemud production across the Bahamian archipelago each year,although contributions vary markedly between habitats. Relativecontributions are, for example, very low (<1%) across the plat-form top seagrass and algal meadow habitats where mud produc-tion derives predominantly from calcareous epiphytes, calcareousalgal breakdown, and/or inorganic (“whiting”) precipitation. Incontrast, the contribution from fish is much higher in hardground(∼25%) and in fringing mangrove habitats (∼70%), reflecting thegreater fish biomass in these environments. Contributions to mudproduction in reef habitats average ∼2.6%, but are much higher(∼6%) if equivalent fish biomass data from marine reservesis used.

The archipelago-wide estimates from the Great Bahama Banksuggest that fish produce carbonate at sufficient rates to influenceshallow marine carbonate sediment budgets and consequentlytheir role in carbonate mud production requires serious consid-eration. Whilst the mud fraction on the Great Bahama Bank ispredominantly aragonite, derived mainly from algal breakdownor carbonate “whitings” (see refs. 2, 7, 8 for discussions), between10 and 32% is high Mg-calcite (15) and thus fish provide a viableexplanation for the origin of a major portion of this type of sedi-ment. Furthermore, the Mg-calcite content of the mud fractionof sediments from many other sites is even higher: in southernBelize ∼45% (16); in Florida 50–75% (14); and in northern Belize70–90% (9)—the proportion increasing in the <20 μm fraction.It is therefore highly significant that analysis of the finest grain-size fractions from sediment samples recovered from sites acrossthe Eleuthera Bank (see SI Appendix) all contain carbonate crys-tallites that are morphologically identical to those collected fromfish in our experiments (Fig. 5 and SI Appendix: Fig. S17). Thiscritical observation provides clear evidence that fish carbonatesdo accumulate in modern sedimentary environments and do notsimply dissolve immediately postexcretion, despite their highMgCO3 content at the point of release (31, 32). Preliminary dataalso indicate that the fish crystals observed within surface sedi-ments, despite remaining morphologically similar to the freshlyexcreted carbonates (Fig. 5 and SI Appendix: Fig. S17), havealready recrystallized to more stable high Mg-calcite forms(∼7–13 mole% MgCO3). Thus recrystallized fish carbonatesare comparable in their chemical composition to many other bio-genic high Mg-calcite grains (26), indicating that they shouldhave good preservation potential within the adjacent sedimentaryenvironments.

It is also the case that fish carbonates represent a unique directsource of high Mg-calcite mud-grade carbonate i.e., a sourcewhose production is not dependent upon postmortem grain dis-aggregation or bioclast breakdown and recrystallization, as neces-sarily invoked to explain the production of Mg-calcite mud fromother sources (9–11)—see ref. 33 for possible submarine precipi-tation sources. Further work is clearly required to elucidate thepathways from the release of fish carbonate crystals to theirdeposition and early diagenesis within marine sediments, andto quantify fish crystal abundances in the finest (<20 μm) frac-tions of carbonate platform and shelf sediments. However, thedata presented clearly demonstrate that fish carbonates repre-sent a primary source of high Mg-calcite mud-grade carbonate,and that these carbonates are produced in sufficient quantitiesto have direct relevance to tropical carbonate sediment budgetswithin the Holocene (last 12,000 years). Furthermore, given thatbony marine fish probably evolved as early as the Ordovician(488–444 Million years) (34) and that “modern” reef fish assem-blages have existed since at least the Eocene (56–34 Millionyears) (35) the implications for addressing some of the majorunknowns about the provenance of carbonate muds in the geo-logic record are considerable.

Materials and MethodsData. We measured rates of carbonate production and examined the mor-phological and chemical composition of carbonate precipitates in 11 speciesof tropical fish (SI Appendix: Table S1) collected from the shallow waterenvironments around Eleuthera, The Bahamas (24° 50′N, 76° 20′ W). Follow-ing collection fish were held in holding tanks provided with flow-throughfiltered seawater without feeding for 48 h prior to collections starting(see SI Appendix). Mucus pellets produced by the fish were collected at 24 hintervals and subjected to replicate distilled water rinses and treatments insequential 3 h treatments with excess sodium hypochlorite (5.25% by mass;commercial bleach) in order to disaggregate the organic component ofthe mucus pellets from the carbonate crystals. Samples were then filteredand dried prior to morphological and chemical analysis (see SI Appendix),with a subset of the cleaned inorganic crystals used to determine carbonateproduction rates per unit of time.

Fig. 5. Crystallites in the fine-sediment fractions from a range of modernenvironments across the Eleuthera Bank, Bahamas. (A) Discrete dumbbellmorphology crystallites from reefal environments (15 m water depth);(B) Splayed ellipsoidal morphology crystallites from reefal environments(15 m water depth); (C) Cluster of ellipsoidal morphology crystallites fromshallow mangrove-fringed coastal inlet site

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Analysis. We used Scanning ElectronMicroscopy (SEM), EDX, and XRD to exam-ine the morphological and chemical characteristics of the carbonate crystallitesproduced byeach fish species. Carbonate production rates per unit of timeweredetermined by titration using the double titration method (see SI Appendix).In order to scale measured fish carbonate production rate data to habitatscales across The Bahamas we integrated recent Geographical InformationSystems (GIS)-derived data on the areal extent of different habitat types fromThe Bahamas with habitat-specific fish biomass data, supplemented with dataon cryptic species densities in comparablemarine habitats from sites in St. Croix,US Virgin Islands. Rates of mud-grade carbonate production per unit area byfish, as measured in this study, were compared against published rates of pro-duction fromother known carbonatemudproducers in TheBahamas, includingproduction by calcareous algae, seagrass epiphytes and carbonate whitings.

ACKNOWLEDGMENTS. We acknowledge the support of staff at the CapeEleuthera Institute, especially Annabelle Oronti, Karla Cosgriff, AaronShultz, and Thiago Soligo. The Bahamian seagrass and mangrove habitatswere mapped by Damaris Torres and colleagues at the University of SouthFlorida under a contract from The Nature Conservancy. Ian Elliott preparedthe Bahamas habitat map. Fish data were collected under the NationalScience Foundation Bahamas Bicomplexity Project. Peter Mumby, CraigDahlgren, William Smith-Vaniz, and Luiz Rocha conducted some of the fishcensuses. This work was supported by the Natural Environment ResearchCouncil (Grant NE/G010617/1 to C.T.P and R.W.W) and Biotechnologyand Biological Sciences Research Council (Grants BB/D005108/1 and BB/F009364/1 to R.W.W.). A.R.H. was funded by Natural Environment ResearchCouncil Fellowship NE/F015704/1.

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