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Effect of Temperature and Salinity on Shell Growth in Estuaries


1. Introduction to Shell Growth

Many groups of marine organisms produce shells or calcified skeletons, and while these calcium carbonate structures are relied on for a bevy of specialized defensive and structural purposes their deposition is largely influenced by physical and chemical characteristics of the water in which these organisms live. Estuaries expose their inhabitants to a wide array of quickly changing physical conditions, exaggerating differences in physical and chemical properties of the water in these dynamic habitats. Estuaries have large variation in salinity (S), ranging from entirely fresh water upstream to fully marine water at the ocean boundary. Estuarine systems also experience daily, tidal and seasonal swings in temperature (T), which affects many of the chemical characteristics of the water as well as the metabolic and calcifying processes of shell-producing organisms. T & S affect the carbonate balance of the water, influencing carbonate equilibrium, calcium carbonate solubility and the saturation states of calcite and aragonite. Tidal influences and shallow waters ensure that estuarine organisms experience wide variations in T, S and other aspects of water chemistry, making this habitat ideal for studies of the influence of changing physical and chemical conditions on processes such as shell deposition. Changing conditions in estuaries and coastal regions is especially important since around 50% of global calcification and 90% of fish catch occurs in these locations.[1]

Many calcifying organisms are in the Phylum Mollusca, including the bivalves, cephalopods, chitons, and gastropods, among others, but cnidarians like corals, echinoderms like sea urchins, and arthropods such as barnacles produce shells in coastal ecosystems as well. Most of these groups are benthic organisms, either attached to (barnacles, corals) or moving around on (urchins, gastropods) or in (bivalves) hard or soft substrates on the bottom of the estuary. However, pelagic species in the phyla Foraminifera and Radiolaria produce ornate CaCO3 skeletons as well. Many benthic mollusks have planktonic larvae called veligers that also produce calcareous shells, and these larvae are particularly vulnerable to changes in water chemistry since their shells are so thin that small changes could have a large impact on their fitness (Fig. 1a)

File:D:\DOCs\Old Uconn\Old classes\Biogeochemistry Fa12\paper\Figures
Figure 1a. Mussel veliger larvae with transparent calcareous shell (Courtesy aquaculturehub.org)

. Some holoplankton (planktonic adults and larvae) have calcareous skeletons as well, and are even more susceptible to unfavorable shell deposition conditions since they spend their entire lives in the water column (Fig. 1b).

There are several variations in calcium carbonate (CaCO3) skeletons, including the calcium carbonate species calcite and aragonite, as well as other elements that can become incorporated into the mineral matrix, altering its properties (Table 1). Calcite is a hexagonal form of CaCO3 that is softer and less dense than aragonite, which has a rhombic form.[2][3] Calcite is the more stable form of CaCO3 and is less soluble in water under standard T and pressure than aragonite, with a solubility product constant (Ksp) of 10-8.48 compared to 10-8.28 for aragonite.[4] This means that a greater proportion of aragonite will dissolve in water, producing calcium (Ca2+) and carbonate (CO32-) ions. The amount of magnesium (Mg) incorporated into the mineral matrix during calcium carbonate deposition can also alter the properties of the shell, as magnesium inhibits calcium deposition by inhibiting nucleation of calcite and aragonite.[5] [6] [7] Skeletons with significant amounts of magnesium incorporated into the matrix (greater than 12%) are more soluble, so the presence of this mineral can negatively impact shell durability, which is why some organisms remove Mg from the water during the calcification process.[8][9]

Food availability can alter shell growth patterns, as can chemical cues from predators, which cause clams,[10] snails[11] and oysters[12] to produce thicker shells. There are costs to producing thicker shells, including the energetic expense of calcification, limits on somatic growth, and reduced growth rates in terms of shell length.[13][14][15] In order to minimize the significant energetic expense of shell formation, several calcifying species reduce shell production by producing porous shells or spines and ridges as more economical forms of predator defense.

T & S also affect shell growth by altering organismal processes including metabolism and shell Mg incorporation as well as water chemistry in terms of calcium carbonate solubility, CaCO3 saturation state, ion pairing, alkalinity and carbonate equilibrium.[16][17][18] This is especially relevant in estuaries, which have S ranging from 0 to 35 and other water properties such as T and nutrient composition vary widely as well during the transition between fresh river water and saline ocean water. Acidity (pH) and carbonate saturation states also reach extremes in estuarine systems, making these habitats a natural testing ground for the impacts of chemical changes on calcification of shelled organisms.[19][20][21]


2. Carbonate and Shell Deposition

Calcification rates are largely related to the amount of available carbonate (CO32-) ions in the water, and this is linked to the relative amounts of (and reactions between) different types of carbonate. Carbon dioxide from the atmosphere and from respiration of animals in estuarine and marine environments quickly reacts in water to form carbonic acid, H2CO3. Carbonic acid then dissociates into bicarbonate (HCO3-) and releases hydrogen ions, and the equilibrium constant for this equation is referred to as K1. Bicarbonate dissociates into carbonate (CO32-), releasing another hydrogen ion (H+), with an equilibrium constant known as K2.[22][23] The equilibrium constants refer to the ratio of products to reactants produced in these reactions, so the constants K1 and K2 govern the relative amounts of the different carbonate species in the water.

H2CO3 ↔ H+ + HCO3- K1 = ([H+] x [HCO3-]) / [H2CO3] HCO3- ↔ H+ + CO32- K2 = ([H+] x [CO32-]) / [HCO3-]

Since alkalinity, or acid-buffering capacity, of the water is regulated by the number of hydrogen ions that a cation can accept, carbonate (can accept 2 H+) and bicarbonate (can accept 1 H+) are the principle components of alkalinity in estuarine and marine systems. Since acidic conditions promote shell dissolution, the alkalinity of the water is positively correlated with shell deposition, especially in estuarine regions that experience broad swings in pH.[24] Based on the carbonate equilibrium equations, an increase in K2 leads to higher levels of available carbonate and a potential increase in calcification rates as a result. The values for K1 and K2 can be influenced by several different physical factors, including T, S and pressure, so organisms in different habitats can encounter different equilibrium conditions. Many of these same factors influence solubility of calcium carbonate, with the solubility product constant Ksp expressed as the concentration of dissolved calcium and carbonate ions at equilibrium: Ksp = [Ca2+][CO32-]. Therefore, increases in Ksp based on differences in T or pressure or increases in the apparent solubility constant K’sp as a result of S or pH changes means that calcium carbonate is more soluble.[25] Increased solubility of CaCO3 makes shell deposition more difficult, so has a negative impact on the calcification process.

The saturation state of calcium carbonate also has a strong influence on shell deposition, with calcification only occurring when the water is saturated or supersaturated with CaCO3, based on the formula: Ω = [CO32-][Ca2+] / K’sp.[26] Higher saturation states mean higher concentrations of carbonate and calcium relative to the solubility of calcium carbonate, favoring shell deposition. The two forms of CaCO3 have different saturation states, with the more soluble aragonite displaying a lower saturation state than calcite. Since aragonite is more soluble than calcite and solubility increases with pressure, the depth at which the ocean is undersaturated with aragonite (aragonite compensation depth) is shallower than the depth at which it is undersaturated with calcite (calcite comp. depth). As a result, aragonite-based organisms live in shallower environments.[27] Figure 2 shows the relationship between aragonite saturation state and calcification rate for a coral species with an aragonite skeleton, indicating that calcification rate does not change much with saturation levels above 300%.[28] Since saturation state can be affected by both solubility and carbonate ion concentrations, it can be strongly impacted by environmental factors such as T & S.


3. Effect of Temperature on Calcification

Water temperatures (T) vary widely on a seasonal basis in polar and temperate habitats, inducing metabolic changes in organisms exposed to these conditions. Seasonal T swings are even more drastic in estuaries than in the open ocean due to the large surface area of shallow water as well as the differential T of ocean and river water. During the summer, rivers are often warmer than the ocean, so there is a gradient of decreasing T towards the ocean in an estuary. This switches in the winter, with ocean waters being much warmer than river water, producing the opposite T gradient. T is changing on a larger time scale as well, with predicted T changes slowly increasing both freshwater and marine water sources (though at variable rates), further enhancing the impact that T has on shell deposition processes in estuarine environments.[29]

Temperature has a strong effect on the solubility product constants for both calcite and aragonite, with an approximately 20% decrease in K’sp from 0 to 25 °C as shown in Table 2.[30][31] The lower solubility constants for calcite and aragonite with elevated T have a positive impact on calcium carbonate precipitation and deposition, making it easier for calcifying organisms to produce shells in water with lower solubility of calcium carbonate.[32][33] T can also influence the calcite: aragonite ratios, as aragonite precipitation rates are more strongly tied to T, with aragonite precipitation dominating above 6 °C (Fig. 3).

T also has a large impact on saturation state of calcium carbonate species, as the level of disequilibrium (degree of saturation) strongly influences reaction rates.[34] Comeau et al. [35] point out that cold locations such as the Arctic show the most dramatic decreases in aragonite saturation state (Ω) associated with climate change. This particularly affects pteropods since they have thin aragonite shells and are the dominant planktonic species in cold Arctic waters.[36] Figure 4 shows the positive correlation between T and calcite saturation state for the eastern oyster Crassostrea virginica, which produces a shell primarily composed of calcite. While oysters are benthic and use calcite instead of aragonite (like pteropods), there is still a clear increase in both calcite saturation level and oyster calcification rate at the higher T treatments (Fig. 4).[37]

In addition to impacting the solubility and saturation state of calcite and aragonite, T can alter the composition of shell or calcified skeletons, especially influencing the incorporation of magnesium (Mg) into the mineral matrix.[38] Magnesium content of carbonate skeletons (as MgCO3) increases with T, explaining a third of the variation in sea star Mg:Ca ratios.[39] This is important because when more than 8-12% of a calcite-dominated skeleton is composed of MgCO3, the shell material is more soluble than aragonite.[40] As a result of the positive correlation between T and Mg content, organisms that live in colder environments such as the deep sea and high latitudes have a lower percentage of MgCO3 incorporated into their shells. [41] Even small T changes such as those predicted under global warming scenarios can influence Mg:Ca ratios, as the foraminiferan Ammonia tepida increases its Mg:Ca ratio 4-5% per degree of T elevation.[42] This response is not limited to animals or open ocean species, since crustose coralline algae also increase their incorporation of magnesium and therefore their solubility at elevated T.[43]

Between the effect that T has on Mg:Ca ratios as well as on solubility and saturation state of calcite and aragonite, it is clear that short- or long-term T variations can influence the deposition of calcium carbonate by altering seawater chemistry. The impact that these T-induced chemical changes have on shell deposition has been repeatedly demonstrated for a wide array of organisms that inhabit estuarine and coastal systems, highlighting the cumulative effect of all T-influenced factors. The blue mussel Mytilus edulis is a major space occupier on hard substrates on the east coast of North America and west coast of Europe, and the calcification rate of this species increases up to five times with rising T (Fig. 5).[44] Eastern oysters and crustose coralline algae have also been shown to increase their calcification rates with elevated T, though this can have varied effects on the morphology of the organism.[45]

Schone et al. (2006) found that the barnacle Chthamalus fissus and mussel Mytella guyanensi showed faster shell elongation rates at higher T, with over 50% of this variability in shell growth explained by T changes. However, the cowry (type of snail) Cypraea annulus displayed a positive correlation between sea surface temperature (SST) and the thickness of the callus, the outer surface of juvenile shells (Fig. 6).[46] The intertidal snail Nucella lapillus also develops thicker shells in warmer climates, likely due to constraints on calcification in cold water.[47] Pelecypod clams show higher growth rates and produce thicker shells, more spines, and more shell ornamentation at warmer, low latitude locations, again highlighting the enhancement of calcification as a result of warmer water and the corresponding chemical changes.[48]

The short-term changes in calcification rate and shell growth described by the aforementioned studies are based on experimental T elevation or latitudinal thermal gradients, but long-term T trends can also affect shell growth. Sclerochronology can reconstruct historical T data from growth increments in shells of many calcifying organisms based on differential growth rates at different T.[49] This can even be done with fossil shells, enabling researchers to establish that clams such as Phacosoma balticum and Ruditapes philippinarum grew the fastest during times of warmer climate (Fig. 7).[50][51]


4. Effect of Salinity on Calcification

Salinity (S) varies even more widely than temperature (T) in estuaries, with S ranging from zero to 35, often over relatively short distances. Even organisms in the same location experience broad swings in S with the tides, exposing them to very different water masses with chemical properties that provide varying levels of support for calcification processes. Even within a single estuary, an individual species can be exposed to differing shell deposition conditions, resulting in varied growth patterns due to changes in water chemistry and resultant calcification rates.

Salinity displays a positive correlation with Mg:Ca ratios, though shows only about half as much influence as T (Fig. 8).[52][53] S in some systems can account for about 25% of the variation in Mg:Ca ratios, with 32% explained by T, but these S induced changes in shell MgCO3 incorporation are not due to differences in available Mg.[54] Instead, in planktonic foraminiferans, changes in S could hinder the internal mechanisms of Mg removal prior to calcification.[55] Foraminiferans are thought to produce calcification vacuoles that transport pockets of seawater to the calcification site and alter the makeup of the seawater and remove Mg, a process that may be interrupted by high levels of S.[56] S can also affect solubility of CaCO3, as shown by the following formulas relating T & S to K’sp, the apparent solubility product constant for CaCO3.[57]

K’sp(calcite) = (0.1614 + .05225 S – 0.0063 T) x 10-6 K’sp(aragonite) = (0.5115 + .05225 S – 0.0063 T) x 10-6

These equations show that T displays a negative relationship with K’sp, while S shows a positive relationship with K’sp (calcite & aragonite). The slopes of these lines are the same, with only the intercept changing for the different carbonate species, highlighting that at standard T and pressure, aragonite is more soluble than calcite. Mucci presented more complex equations relating S & T to K’sp (Table 3), but the same general pattern appears (Fig. 9).[58]

The increasing solubility of CaCO3 with S indicates that organisms in more marine environments would have difficulty depositing shell material if this factor was the only one influencing shell formation. Apparent solubility product is tied to S because of the ionic strength of the solution and the formation of cation-carbonate ion pairs that lower the amount of carbonate ions that are available in the water.[59] This equates to the removal of the products from the equation for the dissolution of CaCO3 in water (CaCO3 ↔ Ca2+ + CO32-), which facilitates the forward reaction and favors the dissolution of calcium carbonate. This results in an apparent solubility product for CaCO3 that is 193 times higher in 35‰ seawater than in distilled water.[60]

S has a different effect on the saturation state of calcite and aragonite, causing increases in these values and in calcium concentrations with higher S, favoring the precipitation of calcium carbonate (Fig. 10).[61] Both alkalinity, or acid buffering capacity, and CaCO3 saturation state increase with S, which may help estuarine organisms to overcome fluctuations in pH that could otherwise negatively impact shell formation.[62] [63] However, river waters in some estuaries are oversaturated with calcium carbonate, while mixed estuarine water is undersaturated due to low pH resulting from respiration.[64] Highly eutrophic estuaries support high amounts of planktonic and benthic animals that consume oxygen and produce carbon dioxide, which lowers the pH of estuarine waters and the amount of free carbonate.[65] Therefore, even though higher S can cause increased saturation states of calcite and aragonite, there are many other factors that interact in this system to influence the shell deposition of estuarine organisms.

All of these aspects of shell deposition are affected by S in different ways, so it is useful to examine the overall impact that S has on calcification rates and shell formation in estuarine organisms, especially in conjunction with T, which also affects calcification. Fish bones and scales are heavily calcified, and these parts of Arctic fish are about half as calcified (27% inorganic material) as those from fish in temperate (33%) and tropical (50%) environments.[66] The benthic blue mussel Mytilus edulis also displayed an increase in calcification rate with S, showing calcification rates up to 5 times higher at 37‰ than 15‰ (Fig. 11).[67]

For oysters in Chesapeake Bay, S does not have an influence on calcification at high T (30°C), but does significantly increase calcification at cooler T (20°C).[68] In the crustose coralline algae Phymatolithon calcareum, T & S showed an additive effect, as both of these factors increased the overall calcification rate of this encrusting alga (Fig. 12).[69] The gross effect of S on calcification is largely a positive one, as evidenced by the positive impact of S on calcification rates in diverse groups of species. This is likely a result of the increased alkalinity and calcium carbonate saturation states with S, which combine to decrease free hydrogen ions and increase free carbonate ions in the water.[70] Higher alkalinity in marine waters is especially important since carbon dioxide produced via respiration in estuaries can lower pH, which decreases saturation states of calcite and aragonite and can cause CaCO3 dissolution.[71] Because of lower S in fresher parts of estuaries, alkalinity is lower, increasing the susceptibility of estuarine organisms to calcium carbonate dissolution due to low pH. Increases in S and T can counteract the negative impact of pH on calcification rates, as they elevate calcite and aragonite saturation states and generally facilitate more favorable conditions for shell growth.


5. Future changes in Estuarine Shell Formation

Shell growth and calcification rate are the cumulative outcome of the impacts of T & S on water chemistry and organismal processes such as metabolism and respiration. It has been established that T & S influence the balance of the carbonate equilibrium, the solubility and saturation state of calcite and aragonite, as well as the amount of magnesium that gets incorporated into the mineral matrix of the shell. All of these factors combine to produce net calcification rates that are observed under different physical and environmental conditions. Organisms from many phyla produce calcium carbonate skeletons (Table 1), so organismal processes vary widely, but the effect of physical conditions on water chemistry impacts all calcifying organisms.[72] Since these conditions are dynamic in estuaries, they serve as an ideal test environment to draw conclusions about future shifts in calcification rates based on changes in water chemistry with climate change.

With changing climate, precipitation is predicted to increase in many areas, resulting in higher river discharge into estuarine environments.[73] In large estuaries such as the Chesapeake Bay, this could result in a large-scale decrease in S over hundreds of square kilometers of habitats and cause a decrease in alkalinity and CaCO3 saturation states, reducing calcification rates in affected habitats (Table 4).[74] Lower alkalinity and increased nutrient availability from runoff will increase biological activity, producing carbon dioxide and thus lowering the pH of these environments.[75][76] This could be exacerbated by pollution that could make estuarine environments even more eutrophic, negatively impacting shell growth since more acidic conditions favor shell dissolution (Table 4). However, this may be mitigated by increased T due to global warming, since elevated T result in lower solubility and higher saturation states for calcite and aragonite, facilitating CaCO3 precipitation and shell formation (Table 4).[77][78] Therefore, if organisms are able to adapt or acclimate to increased T in terms of physiology, the higher T water will be more conducive to shell production than current water T, at least in temperate regions.

The limiting factor in shell deposition may be saturation state, especially for aragonite, which is a more soluble and less stable form of CaCO3 than calcite. In 1998, the average global aragonite saturation state was 390%, a range commonly experienced since the last glacial period and a percentage above which calcification rates plateaued.[79] However, there is a precipitous drop in calcification rate with aragonite saturation state dropping below 380%, with a three-fold decrease in calcification accompanying a drop to 98% saturation. By 2100, pCO2 of 560 and pH drop to 7.93 (global ocean average) will reduce the saturation state to 293%, which is unlikely to cause calcification decreases. The following 100-200 years may see pCO2 increase to 1000, pH drop to 7.71, and aragonite saturation state drop to 192, which would result in a 14% drop in calcification rate based on this alone.[80] This could be exacerbated by low S from higher precipitation in estuaries, but could also be mitigated by increased T which could increase calcification rates. The interaction between pH, T & S in estuaries and in the world ocean will drive calcification rates and determine future species assemblages based on susceptibility to this change.

One problem with counting on increased T to counteract effects of acidification on calcification rate is the relationship between T and Mg:Ca ratios, as higher T result in higher amounts of magnesium incorporated into the shell matrix.[81][82][83] Shells with higher Mg:Ca ratios are more soluble, so even organisms with primarily calcite (less soluble than aragonite) skeletons may be heavily impacted by future conditions.



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