Carbonate deposits in marine fish intestines: A new source of biomineralization

Walsh, Patrick J.; Blackwelder, Patricia; Gill, Kenneth A.; Danulat, Eva; Mommsen, Thomas P.

doi:10.4319/lo.1991.36.6.1227

Cited by 92 publications

(75 citation statements)

References 9 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…It is also the case that numerous in vitro studies have grown crystals with very similar morphologies through both synthetic inorganic and organically-induced precipitation, but that those showing the greatest similarity to fish carbonates were also bacterially mediated (28,29). This observation raises some fundamental questions about the potential role of microbial activity in mediating carbonate precipitation and growth within the intestines of marine teleost fish, even though antibiotic treatment was previously 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 are hypo-saline with respect to normal seawater (approximately one third of ambient seawater) and this, alongside observed differences in pH, Ca 2þ , Mg 2þ , HCO 3 − , and CO 3 2− levels longitudinally within the intestines of temperate fish species (23), indicates that these carbonates are formed under conditions with a distinctive chemistry compared to other marine calcifiers.…”

Section: Resultsmentioning

confidence: 79%

“…In these shallow marine environments carbonate production rates are typically high and preservation potential is good because of high carbonate saturation states in the overlying waters. The process by which fish precipitate carbonate crystals within their guts has been documented in some detail (19)(20)(21)(22) and occurs within the teleosts (bony fish) that dominate the marine fish fauna. Briefly, precipitation occurs as a by-product of the osmoregulatory requirement of teleosts to continuously drink Ca-and Mg-rich seawater.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Fish as major carbonate mud producers and missing components of the tropical carbonate factory

Perry

Salter

Harborne

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

119

View full text Add to dashboard Cite

Carbonate mud is a major constituent of recent marine carbonate sediments and of ancient limestones, which contain unique records of changes in ocean chemistry and climate shifts in the geological past. However, the origin of carbonate mud is controversial and often problematic to resolve. Here we show that tropical marine fish produce and excrete various forms of precipitated (nonskeletal) calcium carbonate from their guts ("low" and "high" Mg-calcite and aragonite), but that very fine-grained (mostly <2 μm) high Mgcalcite crystallites (i.e., >4 mole % MgCO 3 ) are their dominant excretory product. Crystallites from fish are morphologically diverse and species-specific, but all are unique relative to previously known biogenic and abiotic sources of carbonate within open marine systems. Using site specific fish biomass and carbonate excretion rate data we estimate that fish produce ∼6.1 × 10 6 kg CaCO 3 ∕year across the Bahamian archipelago, all as mud-grade (the <63 μm fraction) carbonate and thus as a potential sediment constituent. Estimated contributions from fish to total carbonate mud production average ∼14% overall, and exceed 70% in specific habitats. Critically, we also document the widespread presence of these distinctive fish-derived carbonates in the finest sediment fractions from all habitat types in the Bahamas, demonstrating that these carbonates have direct relevance to contemporary carbonate sediment budgets. Fish thus represent a hitherto unrecognized but significant source of fine-grained carbonate sediment, the discovery of which has direct application to the conceptual ideas of how marine carbonate factories function both today and in the past. marine teleost | fish intestine | carbonate production M arine carbonates contain unique records of changes in ocean chemistry, biogeochemical cycling, and benthic and pelagic ecology (1), and therefore provide vital information on climate shifts in the geological past. A distinctive and often volumetrically important component of these sediments is carbonate mud (the <63 μm sediment fraction). However, the origins of both aragonitic and Mg-calcite carbonate muds remains a topic of long-standing debate (2, 3). Indeed, where attempts have been made to quantify sources of the fine sediment fraction a high proportion remains of unknown origin (e.g., up to 40% in Bahamian sediments and between 28 and 36% in Belize lagoon sediments) (4, 5). This problem arises in part because, with the exception of inorganic carbonate precipitation (e.g., the carbonate "whiting" controversy) (3, 6-8), the processes of carbonate mud production necessarily invoke the degradation of larger bioclasts (skeletal fragments of marine organisms) to produce mud-grade carbonate, and/or grain recrystallization to produce high Mg-calcite muds (9-11). Thus attempts to determine primary mud sources and production budgets are often hampered because of grain obliteration. The mineralogical composition of the mud fraction of modern tropical carbonate sediment is also very variable between s...

show abstract

Section: Resultsmentioning

confidence: 79%

mentioning

confidence: 99%

Fish as major carbonate mud producers and missing components of the tropical carbonate factory

Perry

Salter

Harborne

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

119

View full text Add to dashboard Cite

show abstract

“…In agreement with Shehadeh and Gordon (Shehadeh and Gordon, 1969), Walsh and co-workers concluded from their investigation of the gulf toadfish that the source of total CO 2 found in the intestinal lumen of toadfish was most likely endogenous, and further, that intestinal epithelial respiration was the likely source of CO 2 . This latter suggestion was not empirically tested until much later (see 'Mechanisms of intestinal anion exchange' section below), but was supported by the high density of mitochondria observed in the intestinal epithelial cells (Walsh et al, 1991), indicating a high level of CO 2 production.…”

Section: Anion Exchangementioning

confidence: 99%

“…Subsequently, evidence for an apical, DIDS sensitive Cl -/HCO 3 -exchange process in the seawater acclimated eel intestine (Ando and Subramanyam, 1990) further supported a role for anion exchange in intestinal Cl -absorption. Also supporting the role for intestinal anion exchange in osmoregulation were observations of rectal secretion of solid carbonate pellets (see 'Alkaline precipitation' section below) in gulf toadfish held in 100% seawater but not in 25% seawater (hypo-osmotic) (Walsh et al, 1991). In agreement with Shehadeh and Gordon (Shehadeh and Gordon, 1969), Walsh and co-workers concluded from their investigation of the gulf toadfish that the source of total CO 2 found in the intestinal lumen of toadfish was most likely endogenous, and further, that intestinal epithelial respiration was the likely source of CO 2 .…”

Section: Anion Exchangementioning

confidence: 99%

Intestinal anion exchange in marine fish osmoregulation

Grosell

2006

Journal of Experimental Biology

230

211

View full text Add to dashboard Cite

Osmoregulation in marine fishThree distinct strategies for maintaining salt and water balance have evolved in fishes inhabiting the marine environments. (1) Osmoconformity/ionoconformity is found in the strictly marine agnathan hagfishes, which do not appear to regulate osmotic pressure and concentrations of main osmolytes to a great extent in seawater (Morris, 1958). (2) Osmoconformity and ionoregulation are seen in marine elasmobranchs (Hazon et al., 2003) and in the lobe-finned coelacanth (Griffith et al., 1974), which maintains plasma osmolality at or slightly above that of the surrounding seawater but NaCl concentrations at approximately d of ambient levels. (3) The most common strategy is osmoregulation, found in all teleosts (Marshall and Grosell, 2005) and marine lampreys (Morris, 1958), achieved by the regulation of the main extracellular electrolyte (Na + and Cl -) levels at approximately d of full strength seawater. Under steady state conditions at constant salinities, hagfish, elasmobranchs and coelacanths presumably do not need to drink to maintain water balance. It was shown, however, that the unavoidable renal and extra-renal fluid loss to the hypertonic marine environment in hypo-osmoregulating fish was compensated for by ingestion of seawater with subsequent water absorption across the gastro-intestinal tract (Smith, 1930). More recently, it was demonstrated that even the osmoconforming elasmobranchs display transient drinking when exposed to elevated ambient salinity, and evidence for components of the rennin-angiotensin system (RAS), even in the elasmobranchs (Anderson et al., 2002;Hazon et al., 2003) and hagfish (Cobb et al., 2004) as well as in lamprey (Brown et al., 2005), continues to accumulate. The drinking reflex is at least in part controlled by RAS and it thus appears that the ability to regulate ingestion of seawater and thereby the magnitude of intestinal fluid absorption is an ancestral osmoregulatory trait among fishes.The ingestion and processing of the imbibed seawater for osmoregulatory purposes have, at least in teleost fish, received much attention for three quarters of a century since the first classic studies by Smith published in 1930(Smith, 1930. It is now well established that an initial desalinization of the ingested seawater occurs in the esophagus, which absorbs Na + and Cl -through both passive and active transport pathways, Despite early reports, dating back three quarters of a century, of high total CO 2 concentrations in the intestinal fluids of marine teleost fishes, only the past decade has provided some insight into the functional significance of this phenomenon. It is now being recognized that intestinal anion exchange is responsible for high luminal HCO 3 -and CO 3 2-concentrations while at the same time contributing substantially to intestinal Cl -and thereby water absorption, which is vital for marine fish osmoregulation. In species examined to date, the majority of HCO 3 -secreted by the apical anion exchange process is derived from hydration of metabolic ...

show abstract

“…The substrates calcium and/or magnesium are in high concentration in the intestinal lumen (i.e. ingested seawater) and, in addition, epithelial bicarbonate secretion creates alkaline conditions (Faggio et al, 2011;Fuentes et al, 2010b;Grosell, 2011;Kurita et al, 2008;Walsh et al, 1991;Wilson and Grosell, 2003;Wilson et al, 2009;Wilson et al, 2002). Thus, secreted bicarbonate immobilizes divalent ions in the form of carbonate aggregates, reduces fluid osmolality, and ultimately favours osmotic water absorption.…”

Section: Introductionmentioning

confidence: 99%