Calcification generates protons for nutrient and bicarbonate uptake

EARTIHCIENCE

Earth-Science Reviews 42 ( 1997) 95- 117

Calcification generates protons for nutrient and bicarbonate uptake T.A. McConnaughey

a, J.F. Whelan b

a Marine Research. Biosphere 2 Center, Highway 77, PO Box 689, Oracle, AZ 85623 USA b U.S.G.S., Box 2.5046, MS 963, Denuer, CO 802250046

USA

Received 21 February 1996; accepted 12 July 1996

Abstract The biosphere’s great carbonate deposits, from caliche soils to deep-sea carbonate oozes, precipitate largely as by-products of autotrophic nutrient acquisition physiologies. Protons constitute the critical link: Calcification generates protons, which plants and photosynthetic symbioses use to assimilate bicarbonate and nutrients. A calcium ATPase-based “tram” mechanism underlies most biological calcification. This permits high calcium carbonate supersaturations and rapid carbonate precipitation. The competitive advantages of calcification become especially apparent in light and nutrient-deficient alkaline environ-

ments. Calcareous plants often dominate the lower euphotic zone in both the benthos and the plankton. Geographically and seasonally, massive calcification concentrates in nutrient-deficient environments including alkaline soils, coral reefs, cyanobacterial overrated. Ke~wordst

mats and coccolithophorid

calcium;

carbonate;

bicarbonate;

blooms.

proton; acid

Structural

Calcification creates two types of product, minerals and protons: + CaCO, + H+

(1)

Calcareous skeletons support and protect the soft parts of many organisms. Proton secretion is less obvious, but plays major roles in the photosynthetic assimilation of bicarbonate (Walker et al., 1980; Lucas and Berry, 1985) and in nutrient acquisition (Kochian, 1991; Raven, 199 1). This review explores how calcareous plants and photosynthetic symbioses couple calcification to carbon and nutrient assimila0012-8252/97/$29&l Copyright PII SOOl2-8252(96)00036-O

uses for calcareous

skeletons

are sometimes

; calcareous; nutrient; reef

1. Introduction

Ca2+ + HCO;

and defensive

tion, and postulates that such uses of calcification account for much of the massive carbonate accumulation which occurs in alkaline environments ranging from desert soils to coral reefs. The photosynthetic uses of calcification are easy to appreciate. Bicarbonate is the most abundant carbon source in alkaline waters, but is inaccessible without a source of protons: H++ HCO;

+ CH,O + 0,

(2)

Diffusion from ambient waters can supply protons, but the photosynthetic organism is then bathed in an alkaline, CO,-depleted micro-environment, which inhibits photosynthesis. By discharging the

0 1997 Elsevier Science B.V. All rights reserved.

protons from calcification into their boundary layers, calcareous plants and symbioses can maintain or even elevate CO, concentrations despite photosynthetic CO> uptake. This increases carboxylation efficiencies, and helps them to cope with conditions such as low light levels, when photosynthetic efficiencies are at a premium. Adding reactions I and 2, one obtains a 1: 1 ratio of calcification to photosynthesis (C/P): Ca” + 2HCO;~ + CaCO, + CH ,O + O?

(3)

Such ratios are common in aquatic plants and algae-invertebrate symbioses (Goreau, 1963; Paasche, 1964). Reaction 3 does not consume or produce H’ or CO,. so it affects solution pH and P co2 less than calcification or photosynthesis individually. This becomes important to biospheric chemical regulation. The importance of proton secretion to nutrient uptake is best documented in terrestrial plants. Acidification leaches nutrient elements from soil minerals and promotes the uptake of PO:- (Frossard et al., 1994), NH,’ (Kronzucker et al., 1996) and K+ (Schachtman and Schroeder, 1994). It also stimulates the reduction of NO, @anti et al., 1995). and transition metals (Landsberg, 1986; Rabotti and Zocchi, 19941, whose divalent cations are more stable and assimilable in acidic solution. Despite the importance of acid secretion to nutrient acquisition. proton sources have been generally overlooked. Calcification appears to be important however, judging from the prevalence of root calcification in soils of high acid neutralizing capacity (Jaillard et al.. 199 1). Nutrient-depleted waters also host many outstandingly calcareous communities. These include coral reefs (Muscatine and D’Elia, 19781, cyanobacterial mats (Paerl et al., 1993) and summertime coccolithophorid blooms (Brown and Yoder, 1994). Calcareous organisms seldom appear to prefer nutrient depletion (Atkinson et al., 1995), but rather they presumably cope with such conditions better than do non-calcareous organisms. In some cases nutrient shortage even appears to stimulate calcification (Paasche and Brubak, 1994) while nutrient additions suppress calcification (Kinsey and Davies, 1979; Smith, 1979; Kinsey, 1988; Risk and Sammarco. 1991).

Calcification by aquatic photoautotrophs poses a “chicken and egg” dilemma: Does photosynthesis elevate carbonate ion activity (2HCO; -+ CH,O + O2 + CO_:-) and cause calcification, or does calcification counteract CO, depletion (2HCO.T + Ca’+ + CaCO, + CO, + H,O) and thereby stimulate photosynthesis’? Cis and tram models (Fig. 1) express this more explicitly. Cis calcification (Fig. IA) occurs on the same side of the organism as photosynthetic carbon uptake. due to alkalinization of the water. Photosynthetic rates, aquatic chemistry and diffusion within the boundary layer surrounding the organism determine CaCO, supersaturation levels and calcification rates. Cis calcification would be expected only in illuminated photoautotrophs. Truns calcification (Fig. 1B) occurs away from the site of carbon uptake, due to ion transport through the organism. The speeds and energetics of the ion

A. “Cis” Calcification 2 HCOj

Cat+

HCO; *CO,

B. “Trans”

+ OH-

Calcification Ca++

2HCO; boundary layer

Acidic surface

I

Ca++

2H’ + PHCO,

1

+

2C0,

+ 2&O

Fig. I. Cis and truns calcification mechanisms. Photosynthetic alkalinization of the water causes cis calcification, while ATP powered Ca2+/2H+ exchange, catalyzed by the enzyme Ca’+ ATPase drives fran.7 calcification.

T.A. McConnaughey,

J.F. Whelan/Earth-Science

pumps determine ion concentrations, CaCO, supersaturation levels, and calcification rates. Controlling the ion pumps allows the organism to control calcification. Truns calcification does not require photosynthesis, but the protons generated during calcification will convert HCO; to CO, when they are discharged into ambient waters, and this may stimulate photosynthesis. Root calcification raises similar issues. Calcification may occur when the transpiring plant draws soil water into its roots, but excludes Ca2+ (Fig. 2A). Alternatively, some plants apparently calcify within the vacuoles of root cortical cells (Fig. 2B). The resulting protons may contribute to nutrient acquisition physiologies which involve proton secretion. Calcification physiology is however poorly understood Mann(Lowenstam and Weiner, 1989; Mann et

A. Evapotranspiration concentretes ions around roots, causing calcifiiation

B. Calcification by ro(>t cortical ceils generates protons for nutrient absorption

MnO (N Ht) Clay

iontransport into cell vacuole

Reviews 42 (1997) 95-l 17

91

al., 1989; McConnaughey, 1989~; Simkiss and Wilbur, 1989). The identities and properties of ion transporters have rarely been unambiguously demonstrated, and mineral supersaturation levels never accurately determined. Analogy and chemical modeling must therefore supplement the observed biochemistry and physiology. Analogy begins with observations. Calcareous aquatic plants such as Potamogeton pump protons from the upper (calcified) to the lower (non-calcified) surfaces of their leaves (e.g. Prins et al., 1982). By analogy, proton pumping can be suspected across the calcifying epithelium of corals. Photosynthetic and non-photosynthetic corals probably share the same calcification mechanism (Marshall, 19961, so photosynthesis probably isn’t directly involved in coral calcification. Again by analogy, photosynthesis might not cause calcification in Potamogeton either. Chemical modeling may begin with the C/P ratio and the requirements for high CaCO, supersaturations. Both cis and truns calcification models can be drawn so that they appear to yield 1: 1 C/P ratios (Fig. 11, but more detailed chemical models are needed to determine what is actually likely, and how supersaturated the calcifying solutions will become. The motivations for calcification need to be addressed. Some calcification may occur as an incidental consequence of photosynthesis, transpiration, or other processes. Calcification also creates structures which contribute to support and defense. Finally, the protons from calcification can be useful for carbon and nutrient acquisition. The multiple causes and uses for calcification complicate the search for simple answers. The calcification mechanism largely determines its uses. With cis calcification, hydroxyl ions produced as a consequence of photosynthesis strip H+ from HCO;, but no proton secretion actually occurs. In contrast, trans calcification generates a stream of protons which are potentially available for bicarbonate and nutrient absorption.

2. Calcification physiology Fig. 2. Soil and root calcification. (A) Evapotranspiration and ion exclusion by the plant concentrate ions around the plant roots, causing calcification. (B) Active calcification within root cortical cells generates protons for nutrient uptake.

Cis calcz$kation results from photosynthetic alkalinization of the water. It is most likely to occur near

the plant surface where the carbon assimilation occurs, and alkalinization is most intense. The dissolved carbonate system responds in interesting ways to various combinations of photosynthesis and calcification (Fig. 3A). Alkalinization and CaCO, supersaturations [fi = {Ca’+}{CO~-J/K,,], where brackets denote ion activities and K,,, is the CaCO, solubility product) are of course strongest when photosynthesis is strongest, and calcification weakest. Equal amounts of photosynthesis and calci-

0A

1

1

.6

0

.7

B

,

a31

Calcification to Photosynthesis Ratio Fig. 3. Effects of photosynthesis and calcification on aquatic chemistry. (A) Contours of pH (dashed lines), PC0 (solid lines) and calcite saturation state (dotted lines, with shaiing) in fresh water subjected to various amounts of calcification (on X axis) and photosynthesis (Y axis). A 1: I ratio of calcification to photosynthesis (C/P) forms a diagonal through the figure. Several aquatic plants in Williams Lake, Minnesota display approximately I: I C/P ratios when incubated in calcium supplemented lakewater. (B) Calcite saturation state (in multiples of ambient) at the surface of a plant in seawater. Calculations are appropriate for the cis calcification model, with assumed P,,, levels at leaf surface of 35 and 100 ppm. Note that the calcite sa&ration state at the leaf surface never reaches very high values, and that the degree 01 calcite saturation decreases as C/P increases

fication (C/P = I, along a diagonal), allow carbon to be withdrawn without much change in pH or CO, concentrations, especially in fresh water. Likewise. f2 changes little for a I:1 C/P ratio. This might appear to explain the prevalence of 1: 1 C/P ratios in calcareous aquatic autotrophs, and support the cis model. That success is illusory however, because biological calcification is often quite rapid, and requires more than just maintenance of ambient CaCO, supersaturations. This is best appreciated by remembering that abiological calcification from ambient waters is generally much slower than biological calcification (McConnaughey et al., 1994). The shortcomings of (*is calcification become more apparent when the dissolved carbonate system is modeled as series of coupled diffusion equations for all chemical species within the fluid boundary layer surrounding an aquatic plant. As CO, uptake proceeds. CO:- and OH- accumulate in the boundary layer, and begin to diffuse away. This reduces the amount of calcification which can occur. Diffusion models cannot simultaneously yield high surface CO:- concentrations (and therefore high CaCO, supersaturations and calcification rates), and high C/P ratios (Fig. 3B). This cis mechanism requires net carbon uptake. It therefore does not apply to most animals, or to plants such as Chum, where calcification demonstrably occurs in different places than most carbon uptake (McConnaughey, 1991). Cis calcification does not involve ion transport through the organism. Therefore it does not apply to coccolithophorids, where calcification occurs within intracellular vesicles, or to Chcrru, where active H’ and Ca2’ transport underlie calcification physiology (McConnaughey and Falk, 1991). Cis calcification offers no insight into why some aquatic plants calcify and others do not. Tram culcification: Like soap bubbles, cells enclose their contents within lipid-rich membranes. Small, lipid soluble molecules such as CO, easily cross the membranes (Gutknecht et al., 19771, while ionized and polar molecules such as HCO,, CO:-, CB’+, H’, and most biochemicals do not. Molecular gates and pumps on the membrane control the movement of such molecules, chemically differentiating inside (cytosol) from outside. Plants and animals generally maintain cytosolic Ca2’ at sub-micromolar

T.A. McConnaughey,

J.F. Whelan/Earth-Science

activities (e.g. Evered and Whelan, 19861, i.e. lo3 to lo4 times below environmental Ca*+ activities. Membrane-bounded cellular compartments may however have higher Ca*+ activities. All non-pathological calcification therefore occurs either within membrane bound internal compartments or outside of the cell membrane. An evolutionarily ancient and ubiquitous class of enzymes known as Ca2+ ATPases are largely responsible for ejecting Cazf from the cytosol (Song and Fambrough, 1994). Ca*+ ATPases use the energy of adenosine triphosphate (ATP) hydrolysis to exchange internal Ca2+ for external protons (Niggli et al., 1982; Dixon and Haynes, 1989). Depending on the system, the energy from one ATP energizes either a Ca2+/2H+ or 2Ca2+/4H+ exchange. Mammalian Ca2+ ATPases are best known, and constitute the most abundant enzymes on muscle cell membranes. Plant Ca *+ ATPases have also attracted some attention, and also exchange Ca*+ for protons (Rasi-Caldogno et al., 1987). Ca” ATPases have been implicated in calcification by numerous plants and animals, as discussed later. Ca2+ ATPase is easily incorporated into calcification models. Directional Ca2+ pumping from the cell creates a Ca*+-rich, alkaline extracellular solution (Fig. 1B). CO, diffuses across the membrane into this fluid, ionizes, and precipitates: (Ca2+ + CO, + H,O + CaCO, + 2Hf). The protons so generated are removed by further Ca*+/2H+ exchange. This model can be applied extracellularly, between an epithelial layer and a shell, and intracellularly within membrane-bound vesicles (Fig. lB, 2B, 5, 7). The energy (E) needed to power Ca2+/2Hf exchange increases with the trans-membrane Ca2+ and H+ activity gradients (McConnaughey and Falk, 1991): E = 2.3RT[ a(pCa,

- pCai) - b(pH,

- pH,)] (4)

where R is the gas constant, T is Kelvin temperature, a and b are the numbers of Ca2+ and H+ ions transported per cycle across the membrane, and subscripts i and o denote inside (cytosol) and outside. pCa = -log{Ca*+), analogous to the definition of pH. The thermodynamic limits for ATP-driven Ca2+/2H+ exchange against the cytosol yield a line in (pCa, pH) space having a slope of a/b = l/2,

Reuiews 42 (1997) 95-117

99

11

10

9

PH a

pCa = -log{Ca) Fig. 4. Thermodynamic limits for Ca2+/2Hf exchange (against the cytosol), and approximate CaCO, supersaturations (a - I) estimated from Ht. Ca2+, and CO, concentrations. The pH data for the alkaline surface of Chara, collected in carbon-free solutions, are compatible with ATP driven Ca2+/2H+ exchange. Many animals probably use the more economical 2Ca2+/4H+ exchange. For this construction, CO, concentrations and CaCO, supersaturations are assumed to be in equilibrium with the atmosphere (360 ppm CO, ).

separated from the cytosol by the energy equivalent of ATP hydrolysis, about 50-60 KJ/mol (Fig. 4). (pCa, pH) combinations at the calcified surface of the alga Chara sometimes approach the thermodynamic limit for ATP-driven Ca2+/2H+ exchange (Fig. 4). pH values around 10.7 are observed in specialized media (McConnaughey and Falk, 1991), and pH values greater than 10.4 develop in more normal media for both Chara and other aquatic plants (e.g. Prins et al., 1982). CO, diffuses across the calcifying membrane, and ionizes to produce HCO; and CO:- concentrations as determined by local pH: [HCO;] = K,[CO,]/{H+} and [CO:-] = K,K,[CO,]/(H’}* (at chemical equilibrium). K, and K, are the first and second apparent ionization constants of CO,. CO:- therefore concentrates on the alkaline side of the membrane as described by the ratio: [CO:?],/[CO:-]i

= ({H+Ii/IH+J,)2 (5)

100

TA. McConnuughey.

J.F. Whelm/

A membrane proton gradient of 2-3 pH units, like that within the alkaline calcifying zones of Chara, can theoretically concentrate CO:by a factor of IO4 to 106. Ca2+/2H+ exchange alkalinizes the calcifying solution by 2 pH units for each 1 unit change in pCa. Because CO:- concentrations increase by a factor of 100 for each unit of pH increase (Eq. 5). the Ht pumping associated with Ca’ ‘/2Hc exchange increases the CaCO, saturation state of the calcifying solution more than does the addition of CaZi. Isopleths of equal CaCO, supersaturation in (pCa, pH) space have a slope of l/2, paralleling the thermodynamic limits for Ca’+/2H’ exchange (Fig. 4). CaCO, supersaturations as high as 10’ are theoretically possible (for a Ca’+/2H+: 1ATP stoichiometry, at atmospheric Pco, levels of 350 ppm). due mostly to elevation of pH and therefore CO: ~. Significant supersaturations are also possible for 2Ca2+/4H+: 1ATP stoichiometry, especially if tissue CO, levels exceed ambient. The site of tram calcification can be enclosed within membrane bound vesicles (as with coccolithophorids), or between the cell and extracellular precipitates (Chara and corals) (Figs. 5 and 7). Complete isolation is apparently rare, as evidenced by the skeletal incorporation of diverse chemicals and particles in coral skeletons (McConnaughey, 1989a) and the sensitivity of coccolithophorid calcification to organophosphate calcification inhibitors (Sekino and Shiraiwa, 1994.) Experiments with proton buffers and phosphate nevertheless indicate substantial isolation of the extracellular calcification site in Charu (McConnaughey, 1991). Diffusion of OH and CO:from the calcification site therefore do not lower the C/P ratio in truns-calcifying plants as much as would be expected for cis calcification. The calculations of aquatic chemistry presented in Fig. 3A apply to the bulk fluids surrounding the calcareous organism, but not to the immediate site of calcification, which is more alkaline and supersaturated, or to the site of proton discharge. 2.1. Case studies 2. I. 1. Aquatic plants Bischoff (1828) observed alternating calcareous and non-calcareous zones along the giant cells of

Earth-Science

Ruiews

42 (1997) 95-117

“Tram” Calcification

Coccolithophorid Fig. 5. Trc1n.s calcification models applied to Chum, coccolithophorid\, and coralline algae. Two versions of the tram model are illustrated for Churn: (Left). electrophoretic H+ uptake at the calcifying surface deprotonates HCO; and causes CaCO, precipitation. (Right), Ca’+ ATPase catalyzed Ca’+/2H+ exchange at the alkaline surface creates a Ca’%ich. alkaline fluid which absorbs CO, from the cell and precipitates CaCO,. In either case, rhe protons-taken up at the alkaline surface are expelled at the acidic surface, where they promote HCO; assimilation. The Ca” ATPase model is then applied to coccolithophorids (C) and coralline algae CD).

Chat-u (Fig. 5), and Charles Darwin reputedly used pH dyes to reveal separate alkaline and acidic surfaces on certain aquatic vascular plants (R. Wetzel. pers. commun.). This pH differentiation develops under illumination but continues under dim light, and in alkaline buffer solutions lacking DIC, and therefore does not depend on photosynthesis (McConnaughey and Falk, 1991). The cis model offers no explanation for acidic surfaces, or for the alkaline surfaces in DIC-free media, while the tram model does. Chura takes up carbon mainly along its noncalcified acidic surfaces, and uses this carbon for both photosynthesis and calcification (McCon-

T.A. McConnaughey, J.F. Whelan/ Earth-Science Retiiews 42 (1997) 95-117

naughey, I99 1; Fig. 6A). Aquatic angiosperms such as Potamogeton apparently function analogously, with acidification of the lower leaf surface, and alkalinization and calcification above (e.g. Prins et al., 1982; Staal et al., 1989). Proton uptake at the alkaline surfaces of these plants was originally attributed to electrophoretic proton movement across the membrane electrical gradient (Fig. 5A). The Ca2+ ATPase mode1 (Fig. 5B) predicts several things more accurately however, including thermodynamics, anticorrelations between Ca2+ and H+ activities at the calcifying surface, and inhibition of Hf uptake by chemicals which disrupt Ca*+ transport (McConnaughey and Falk, 199 I). It also offers more realistic explanations for the 1:l C/P ratios commonly observed under mildly alkaline, Ca*+-rich conditions,

_I

:;:..

I

..+

/@

/6.‘-

in acidic zone

.

.

zo/c

,f.:’ 2 20.,-‘5:. :.1$-t: ..;-::a.:.* ..,. ._::~;;,;;r+.r .:::.... \ ,.::: rl:::i:::.::’ uM CO2

??

’

’

8a

L

PH

’

I

*

9

1

4

10

Fig. 6. Experiments with the giant-celled alga Chara. (A) Carbon14 uptake for both calcification and photosynthesis in Chara occurs mainly in the acidic (non-calcified) pericellular zones. (B) Calcification to photosynthesis ratio as a function of solution pH. Dashed curves based on diffusion model applied to acidic surfaces. Best tits were obtained for assumed CO, concentrations > 20 FM at the acidic surfaces.

101

the use of CO, from inside the cell in extracellular calcification (Fig. 6A), and the strong kinetic depletions of 180 and 13C in many biological carbonates (McConnaughey, 1989a, b). Coccolithophorid calcification occurs within membrane-bound internal vesicles (Klaveness, 1976; Winter and Siesser, 1994). The algae presumably pump Ca*+ into the coccolith vesicles (and pump protons out) using Ca*+ ATPase (Fig. 5C). Coccolithophorids exhibit high Ca*+ dependent ATPase activities (Okazaki et al., 1984; Wainwright et al., 1992; Kwon and Gonzalez, 1994) and genetic sequences coding for probable P-type Ca*+ ATPase have been isolated (Song and Fambrough, manuscript.) These Ca* + ATPases apparently pump Ca*+ into “calcosome” vesicles (Song and Fambrough, 19951, which discharge their contents into larger coccolith producing vesicles. Van der Wal et al. (1985) suggested that Ca*+ in these vesicles may greatly exceed ambient concentrations. Because calcification occurs within intracellular vesicles while carbon uptake occurs at the outer surface, a cis calcification mechanism appears highly improbable. Coccolithophorids often exhibit C/P ratios near 1:l (Sikes et al., 1980; Brownlee et al., 1994; Paasche and Brubak, 1994; Westbroek et al., 1994a; Winter and Siesser, 1994). Photosynthesis in highly calcareous coccolithophorids is relatively insensitive to 0, and molecular CO, concentrations (Nielsen, 1995; Israel and Gonzalez, 1996). Oxygen insensitivity has also been noted in corals (Muscatine, 1980; Goiran et al., 1996). This is consistent with CO, enrichment of the extracellular boundary layer, made possible by secreting the protons derived from calcification. Many coralline algae likewise calcify within extracellular pockets sandwiched between adjoining cells (Fig. 5D) (Borowitzka, 1983). They presumably take up carbon along the cellular surfaces facing ambient seawater, so that cis calcification again appears unlikely. Mori et al. (1996) reported that a Ca*+ activated H+ translocating ATPase contributes to calcification in Seratacardia. 2.1.2. Photosymbiotic animals Photosynthetic corals, foraminifera and clams probably calcify by the same mechanisms as their non-photosynthetic relatives, which obviously do not

use cis mechanisms. Ca’+ ATPase or Ca’ ’ transport through the coral cells (which probably implies ejection from the cell by Ca’+ ATPase) has been associated with calcification in non-symbiotic corals (Kingsley and Watabe, 1984, 1985; Allemand and Grillo. 1992; Marshall, 1996) as well as symbiotic corals (Isa et al., 1980; Ip et al.. 1991; Al-Moghrabi et al., 1996; TambuttC et al., 1996) and foraminifera (Kuile et al., 1989a). If the invertebrate host calcifies faster when illuminated (e.g. Barnes and Crossland, 1978; Chalker and Taylor, 1978). then presumably it regulates calcification to stimulate the algal symbionts. Symbiotic corals can be “fooled” into rapid calcification in the dark by increasing oxygen levels (Rinkevich and Loya, 1984). Prior exposure to light sometimes enhances calcification almost as much as concurrent exposure (Roth et al.. 1982). Photosynthetic foraminifera likewise calcify at normal lightenhanced rates when photosynthetic carbon fixation is blocked by low concentrations of the herbicide DCMU (Erez, 1983). Low DCMU concentrations block photosystem II (which is required for carbon fixation) while photosystem I can continue to make ATP through cyclic photophosphorylation (Fedke, 1982). Hence ATP availability appears to be more important than carbon fixation for calcification in algae-invertebrate symbioses. Calcification may also be concentrated away from the most photosynthetic parts of an organism. Coral symbionts inhabit cells lining the internal gastrovascular system (coelenteron), mainly on the oral (top) side, while calcification occurs across the basal epithelium from the coelenteron (Johnston, 1980) (Fig. 7B). Branching and foliose corals calcify most rapidly in their apical regions (Fig. 7A), which have high respiration rates and ATP levels but few symbionts (Fang et al., 1983; Gladfelter et al., 1989). Giant clams similarly calcify from the mantle epithelium. while their algal symbionts inhabit a complex tubular system derived from the gut, which lacks any direct contact with the shell (Norton et al., 1992). Corals probably discharge the protons generated through calcification into the coelenteron, so symbiotic algae living within adjacent endodermal cells have easy access to the resulting CO,. This CO, source gains additional significance because corals often close their mouths during the daytime. Branch-

Rapid calcification

Fig.

7.

Spatial

relationships

between

synthesis in corals. (A) Calcification

calcification

and photo-

at branch tips creates CO?-

rich water which may be transported by cilliary currents to more photosynthetic lateral polyps. (B) Calcification discharges protons into the coelenteron, producing CO? which is used by symbiotic algae (dots) inside the cells of the adjacent oral epithelium.

ing and foliose corals may use cilliary currents to bring CO,-rich waters from the branch tips to more photosynthetic lateral tissues (Fig. 7A). Gladfelter ( 1982) emphasized the prominence of the axial canal, and detected inward cilliary currents at the branch tip (Gladfelter, 1983). Similarly, giant clams discharge the protons from calcification into hemolymph fluids. which ultimately deliver CO, to the symbionts. The symbiotic dinoflagellates of corals and giant clams meanwhile appear to utilize a form the enzyme Rubisco which requires high CO, levels for photosynthesis (Rowan et al.. 1996.) 2.1..3. Cvunnbucteria Many cyanobacteria calcify (Golubic, 1973; Whitton and Potts, 1982), and show photosynthetic characteristics such as low sensitivity to ambient CO, and 0, levels (e.g. Espie et al., 1991: Beer et al.. 1992) similar to those seen in calcareous aquatic eukaryotes. These features suggest a similar physiology. As with eukaryotic plants, the photosynthetic characteristics have previously been interpreted in terms of active carbon transport however, while calcification has been attributed to a cis mechanism (Robbins and Blackwelder, 1992). Prokaryotes lack many components of eukaryotic Ca’ + physiology. They nevertheless appear to regu-

T.A. McConnaughey, J.F. Whelan/ Earth-Science Reciews 42 (1997) 95-117

late internal Ca*+ in an analogous manner (Smith, 1988), possess electroneutral calcium-proton exchanging ATPases (Driessen and Konings, 1986), and often show evidence of cellular localization, asymmetry or polarization (e.g. Sherman et al., 1994). Ogawa and Kaplan (1987) observed a pH and HCO; dependent, light induced acidification of the medium by Anacystis nidulans, under conditions of photosynthetic inhibition, and a 1: 1 correspondence between H+ extrusion and HCO; uptake. CO, ionization within alkaline internal reservoirs may have provided the proton source, and would also account for inorganic carbon concentration within cyanobacteria (Kaplan et al., 1991). Merz et al. (1993) detected acidic zones between the cyanobacterium Scytonema and its calcified outer sheath. Calcification therefore appeared to involve proton export. Perhaps the cyanobacterium calcifies internally, exports (membrane coated?) CaCO, particles within the membranous “s” layer, and discharges protons into its environment to assimilate HCO;. Merz (1992) and others have also reported approximately 1: 1 ratios of cyanobacterial calcification to photosynthesis under field conditions, a stoichiometry which suggests a rrans-calcification mechanism.

3. The photosynthetic utilization of bicarbonate Calcareous aquatic plants and symbioses use the protons from calcification to convert HCO, to CO,, for photosynthesis. Exactly how proton secretion couples to carbon uptake is however unclear (Lucas and Berry, 1985). CO, or HCO; may be actively taken up across the plasma membrane in co-transport with protons. Alternatively, HCO, may be protonated to CO, within the extracellular environment (sometimes catalyzed by carbonic anhydrase) and absorbed by simple diffusion through the membrane (Staal et al., 1989). Modeling suggests that acidification of the boundary layer surrounding the cell raises CO, concentrations to levels well above those of ambient waters (Walker et al., 1980; Prins et al., 1982), and far higher than calculated CO, concentrations within the diffusive boundary layers surrounding non-calcareous aquatic plants. Therefore it is unclear why cal-

103

careous plants would need active HCO; uptake. Diffusion also plays somewhat opposite roles in calcareous and non-calcareous plants. In non-calcareous plants, the slow diffusion of CO, and H+ equivalents toward the plant restricts photosynthesis, while in calcareous plants, the slow diffusion of CO, and H+ from the acidic surfaces enhances photosynthesis. 3. I. Stoichiometry Calcareous plants and symbioses often display ratios of calcification to photosynthesis (C/P> near 1 (Table 1). This ratio is not carved in stone. In acidic or Ca2+-depleted waters, C/P ratios approach zero, while calcification in the dark yields, at least temporarily, infinite C/P ratios. C/P = 1 instead represents an optimization under mildly alkaline conditions, in which the plant or symbiosis relies heavily on the protons from calcification to convert HCO; to CO,, for photosynthesis. In Char-a, C/P increases sigmoidally with pH (Fig. 6B), but approximates 1 between pH 8 and 9 (McConnaughey, 199 1) This pH dependence is consistent with control by diffusion of carbon species and proton buffers toward the acidic surface, where carbon uptake occurs. Bicarbonate is the principle carbon species and proton acceptor under mildly alkaline conditions, giving rise to the 1:l C/P ratio: Alkaline

surfaces CO, + H,O + Ca2+

+ CaCO, + 2H+ Acidic surfaces 2H++

(6) 2HCOT + 2C0,

+ 2H,O (7)

Chloroplasts Net: 2HCO;

CO, + H,O -+ CH,O + 0, + Ca*+ + CaCO, + CH,O + 0,

(8) (9)

HCO, rather than CO, diffuses toward the plant, so photosynthesis is relatively independent of solution CO, concentrations (Nimer et al., 1994; Nielsen, 1995; Israel and Gonzalez, 1996). Various biochemical and morphological specializations increase CO, acquisition efficiencies in aquatic plants and symbioses. At the acidic surfaces, these include complex membrane invaginations, elevated carbonic anhydrase activities, and concentrations of active chloroplasts (e.g. Price et al., 1985;

T.A. McConnaughr\;

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J. F. Whrlan / Earth-Science

Table I Calcification and photosynthesis in aquatic plants and algae-invertebrate symbioses. C/P is the molar ratio of calcification to photosynthesis, usually measured under full illumination near pH 8, often quoting the upper range of observed values. L/D is the ratio of calcification in the light compared to dark (or when relatively high DCMU concentrations inhibit photosynthesis) C/P

Organism

L/D

Ref.

Cyanobacteria

0% I .OIO (DCMU)

Scytclnemcl Swechocwtis

-I

I 2

Coccolitbophorids Emiliania huxleyi Cricosphaera

carterae

Umbilicosphaera Pleurochrysis

sibo

sp. (HC)

-1 -I 0.6

- 0.5

2 --t IO > lo’? > IO - 5

3-14 3, 4 5 IS

( > IO)

16-18 I9 20-23 24 IX, 25

Macrophytic algae Chara spp. Corallina 0fficinnli.s

Halimeda spp (35 calcareous algae) Aquatic vascular plants symbioses (foram) Archaias angulatus (foram) Amphisorus hempri. (foram) Aphistegina lobif. (foram) Heterostigina dep. (foram) Operculina ammono. (foram) Borealis schlumbe. (foram) Acropora cewicor. (coral) Montastrea annula. (coral) focillopora evdou. (coral) Tridacna gigas (clam) Hippopus hippopus (clam)

-I 0.97 0.4-0.6 -I -1

3+ IO l-4 0.3-2.5

Algae-invertebrate Sorites marginalis

- I - I - I -I - 1 - I - 0.5 0.8-4.7 - I 0.3-l 0.2-0.4 0.3-o.‘)

26 27 22 (DCMU) 2X. 29 4-X (DCMU) 28.29 28 24 I2 2X 28 23.30 2.5-13. I

2-o

23.30.3I 32 33 33

References: (I) Merz. 1992. (2) Yates and Robbins. 1994. (3) Sikes et al., 1980. (4) Ariovich and Pienaar, 1979. (5) Balch et al.. 1992. (6) Paasche, 1964. (7) Nimer and Merrett, 1992. (8) Nimer and Merrett, 1993. (9) Paasche and Brubak, 1994. (IO) Nielsen. 1995. (I 1) Paasche, 1964. (12) Maraiion et al., 1996. (13) Dong et al., 1993. (14) Linschooten et al., 1991. (IS) Israel and Gonzalez. 1996. (16) McConnaughey, 1991. (17) McConnaughey and Falk, 1991. (18) McConnaughey et al., 1994. (19) Pentecost, 1978. (20) Jensen et al., 1985. (21) Stark et al., 1969. (22) Borowitzka and Larkum, 1976a,b,c,d. (23) Delgado and Lapointe. 1994. (24) Goreau, 1963. (25) McConnaughey, 1994. (26) Duguay. 1983. (27) Duguay and Taylor, 1978. (28) Kuile and Erez. 1987. (29) Kuile et al., 1989a,b. (30) Chalker and Taylor, 1978. (3 1) Barnes and Taylor, 1973. (32) Davies, 1984. (33) Klumpp and Griffiths. 1994. Cited reports were shamelessly distilled for this summary. Certain caveats, restrictions, limitations, addendums, and exclusions may apply.

Rrrkws

42 (1997)

Y5- I I7

Bisson et al., 1991). The probable roles of the internal cavities and cilliary currents in corals were discussed above.

High pericellular CO, concentrations potentially increase both photosynthetic rate and quantum efficiency. Rate (~1) enhancement follows directly from Michaelis kinetics, 11= V/( KM/c + I), where V is the maximum rate of photosynthesis which the plant can sustain, c is substrate concentration, and K, is the half saturation constant for photosynthesis, estimated at lo-20 p,M CO, in Chara (Smith and Walker, 1980) and 40-50 FM CO, for the coccolithophorid Pleuruchtysis (Israel and Gonzalez, 1996). By increasing u, the plant increases the ratio of carbon fixation to available light, or quantum efficiency. Rate enhancement may be most important when light and nutrients are abundant, while quantum efficiency may be most important under low light. Smith and Walker (1980) extended the kinetic analysis to include the limitations of diffusion through the boundary layer, using the Hill-Whittingham equation: (K,P+cP+V) _ [ ( K, P + cP + V)’ - 4rPV]““)

(‘0)

where P = D/Z is the permeability of the diffusive layer, 2 is its thickness and D is molecular diffusivity of the substrate. Calcareous plants essentially replace diffusion of the relatively rare molecules CO, and H+ (including H+ equivalents), whose concentrations are likely to be in the micromolar range, with diffusion of the abundant molecules HCO; and Ca’+, whose concentrations are often in the millimolar range. C/P is relatively insensitive to solution Ca’+ concentrations, above 0.5 mM (Fig. 8) (McConnaughey and Falk, 1991). This derives from the isolation of the calcifying region, whose chemistry depends mostly on ion transport across the cell membrane. The plant must however obtain Ca’+ by diffusion from solution, and Ca2+ supply becomes rate limiting at concentrations below about 0.5 mM.

T.A. McConnaughey, J. F. Whelan/Earth-Science

8

C$

$ 5

: ; :

E

A

7 $

Chara Calcification (scaled to photosynthesis)

;5

* Emiliania photosynthesis

;

(Paasche, 1964) OLA 0

r” =1

0 Myriophyllum photosynthesis (Steeman Nielsen, 1947) I

I

1

2

105

10

aA ( ’ 0 Chara photosynthesis S 50 9 -- - Hill & Whittingham kinetics 2 ; E

Reviews 42 (1997) 95-1 I7

0 I

3 Calcium (mM)

Calcified I 4

Decalcified I 5

6

Fig. 8. Ca2+ diffusion toward the cell limits photosynthesis in Chara co), Emiliania ( * , after Paasche, 1964) and Myriophyllum (squares, after Steeman Nielsen, 1947). Curve fit to Chara photosynthesis (except points for 0.0 and 0.1 mh4 Ca2+) calculated using Hill-Whittingham kinetics. Chara calcification data scaled to photosynthesis. Inset: Ca2+ complexed with citrate stimulates photosynthesis at low and constant solution Ca2+ activities. This suggests that Ca 2+ diffusion, not thermodynamic activity, accounts for photosynthetic stimulation at low solution Ca2+ concentrations.

For comparison, HCO, diffusion usually limits photosynthesis at concentrations below about 1 mM (Smith and Walker, 1980). The 1:2 ratio of limiting Ca2+ to HCO; concentrations reflects the proportions in which these molecules are used (reaction 9). Seawater contains about 10 mM Ca’+, so Ca*+ limitation is never likely in the oceans. Alkaline fresh waters often contain less than 0.4 mM Ca2+ however, so Ca *+ limitation is quite possible. When solution Ca2+ levels limit photosynthesis, the calcareous plant probably behaves much like any non-calcareous plant, and depends on the diffusion toward the plant of CO, and proton equivalents (carried mainly by OH- and CO:efflux). The plant may also cycle protons from its alkaline to its acidic surfaces with little net calcification, relying on the modest Ca2+ supplies from solution, dissolution of old carbonate encrustations, or internal supplies to keep the cycle going. From Fig. 8 it appears that Ca*+ insufficiency reduces the rate of photosynthesis in various aquatic plants by about half. A similar photosynthetic inhibition occurs in corals, incubated

in Ca*+ free artificial 1996).

seawater (Al-Moghrabi

et al.,

4. Calcification and nutrient assimilation In both terrestrial and aquatic systems, the protons generated through calcification appear to contribute to nutrient assimilation. 4.1. Terrestrial plants Many plants (calcifuges) require high fertilization to grow in limestone-rich soils and other alkaline soils of high acid neutralizing capacity (Tyler, 1994; Susin et al., 1996). Acid secretion by the roots plays an important role in nutrient assimilation in such soils (Kochian, 19911, and root calcification appears to be fairly common (Jaillard, 1987; Jaillard et al., 1991). Therefore it appears reasonable to associate these phenomena. Land plants “mine” most of the elements they need from soils using an acid leach process (e.g.

T.A. McConnuughr,v.

106

J.F.

Whelm

/ Eurth-Scrmcr

Raven, 199 1; Kochian, I99 I ). Leachable nutrients include P, N, K, Mg, Fe, Mn and others. Some illustrative acid leaching reactions include: -+3(H?P01)

6H++ Ca,F(PO,),

+F

+SCa” 0))

H++ NH: (Clayy

) -NH:

+H+(Clay

2H’+

-+ 2K++

KAl,Si,O,,,(OH),

3KAlSi,O,

+ 6Si01 6Hf+

Mg,Si,O,(OH),

+ 3Mg”+

)

t 12)

( ‘3) 2Si0,

+ .5H,O ( 14)

8H++ 4FeOOH + CH,O + 4Fe”

+ CO, + 7Hz0 (15)

4H’+

2Mn0,

+ CH,O -+ 2Mn’ ’ + CO, + 3H,O ( ‘6)

Soil acidification sometimes aids nutrient uptake as well. NO; uptake (McClure et al., 1990; RuizCristin and Briskin, 1991; Santi et al., 1995), high affinity K + uptake (Schachtman and Schroeder, 1994) and H,PO; uptake (McIntosh and Oliver. 1994) evidently occur through H’ cotransport. and are therefore stimulated by extracellular acidification. Many plants evidently take up ammonia primarily as NH: (e.g. Kronzucker et al., 1996), so soil acidification would aid uptake as well as leaching from alkaline soils. Most plants assimilate divalent transition metals such as Fe” and Mn’ + more readily than higher oxidation states, and acidification stabilizes these reduced forms. Proton secretion also stimulates root Fe3+ reductase activity in various plants (Grusak and Pezeshgi, 1996; Susin et al.. 1996).

Proton secretion usually concentrates in a region somewhat behind the root tip (Fig. 2B), giving rise to characteristic pH and electrical zonation analogous to the electrochemical banding of calcareous aquatic plants (Raven, 1991, 1992). Deficiencies of iron (Landsberg, 1986; Rabotti and Zocchi, 1994), nitrogen (Raven et al., 1990) and phosphate (Muchhal and Raghothama, 1995), as well as the appearance of NOj @anti et al.. 1995) induce intense H+ secretion and often accumulation of polyvalent organic acids in a small zone behind the root tips. Deficiency of

Hwirw.~

42

f I9971

95-I

I7

phosphate (and perhaps other nutrients) also induces Ca?’ ATPase production by the root (Muchhal and Raghothama. 1995). Carbonate precipitation presumably increases proton production. Plants resort to root calcification mainly when growing on alkaline soils of high acid neutralizing capacity. Calcification concentrates within root cortical cells (Fig. 2B), sometimes nearly filling them (Jaillard, 1987). Root tips. a central channel through the root (stele), and the outer cell layer (rhizoderm) remain uncalcified. Much of the root volume may become calcified. Calcite grains often retain exquisite cellular detail, suggesting for example undulations of the tonoplast (vacuole membrane). Calcification of root cell vacuoles implies an interesting reversal of their normally acidic condition. Ca’+ transport into the vacuole has been thought to occur through passive Ca”‘/2H+ exchange (Schumaker and Sze, 1985; see Fig. 41, although Ca’+ ATPase has also been suggested as the main Ca” carrier (Gavin et al.. 1993; Pfeiffer and Hager, 1993). Muchhal and Raghothama ( 1995) observed increased Ca’ ’ ATPase activity during phosphate deficiency. so it is likely that whether or not Ca’+ transport into the vacuole is normally passive, it becomes ATP coupled under nutrient starvation. Fig. 2B illustrates some likely relations between vacuolar calcification, acid secretion, and nutrient absorption. Soil fungi including mycorrhizal symbionts also accelerate mineral decomposition and contribute to soil calcification, including precipitation of calcium oxalates (Graustein et al., 1977; Pohlman and McCoil, 1988; Drever and Vance. 1993). Oxalate secretion enhances nutrient absorbtion by the root complex through chelation effects (Fox and Comerford, 1992; Pate, 1994) as well as through proton generation. Root calcification therefore involves more than transpiration-driven ion accumulation around a root. Transpiration should cause calcification mainly within rhizosphere soils and within the cell walls of root cells, away from the zones of acid secretion. Root calcification in contrast apparently concentrates in the vacuoles of cortical cells, within the zones of acid secretion. Acid secretion near the root tips meanwhile redissolves old soil carbonates and encourages opal (SiOz) precipitation.

T.A. McConnaughey, J.F. Whelan/Earth-Science

4.1.2. Soil carbonates Ross and Delaney (1977) observed massive CaCO, accumulation in the roots of a nitrogen starved forage legume. Reeves (1976) and Esteban and Klappa (1983) identified calcified roots as important components in many soils, and described developmental sequences for pedogenic calcification. Jaillard (1987) and Jaillard et al. (1991) presented light and electron micrographs of living and dead calcified roots, and thought it probable that most filamentous soil carbonates (“microcodium”) derive from vascular plants. These low Mg calcites comprised about a quarter of the soil mass in some sites in southern France. Alkaline soils in the deserts of southern Nevada host many examples of calcified (and silicified) roots (Fig. 9). These fossils sometimes retain considerable detail of plant structure, and sometimes provide reasonably closed systems for isotopic (U/Th, 14C) dating (Paces et al., 1994). Soil calcification generally produces sub-horizontal calcrete layers, but vertical deposits also form where faults focus downward penetration of meteoric waters and roots (Fig. 9B, C). Such deposits have played an interesting role in the debate over paleoclimate and hydrological stabil-

Reviews 42 (1997) 95-117

107

ity of the proposed Yucca Mountain repository for high-level radioactive wastes (Stuckless et al., 1991). Although considerably less massive than marine carbonates, soil carbonates contain about as much carbon as the atmosphere (Schlesinger, 19851, and are significant factors in desert hydrology and plant nutrition. 4.2. Aquatic plants and symbioses Coral reefs flourish in tropical regions of chronic nutrient shortage. Both free living calcareous reef algae (Littler et al., 1988; Delgado and Lapointe, 1994) and algae-invertebrate symbioses (Muscatine and D’Elia, 1978; Cook et al., 1994; Rees et al., 1994; Fitt et al., 1995; McAuley and Smith, 1995) tend to take up nutrients mainly during the daytime, when calcification is concentrated. Corals also appear to reduce calcification when nutrients are abundant (Kinsey and Davies, 1979; Smith, 1979; Kinsey, 1988; Risk and Sammarco, 1991). Planktonic blooms of coccolithophorid algae typically develop during summer, after diatoms and other non-calcareous algae have reduced nutrient concentrations (including iron) to low levels (Wal et al., 1985, 1995; Balch et al., 1992; Bleijswijk et al.,

Fig. 9. Calcified roots and soil carbonates in southern Nevada. (A) Calcified roots in sandy soils at Busted Butte. (B) Erosional gully exposing sub-horizontal paleosol layers and fault zone rich in calcified roots, Busted Butte. (Cl Massive indurated siliceous calcrete exposed at Trench 14, Bow Ridge Fault, Yucca Mountain.

1994; Brown and Yoder, 1994; Kristiansen et al.. 1994). Coccolithophorids are comparatively resistant to shortages of phosphate (Riegman et al.. 1992) and iron (Muggli and Harrison, 19961, and may increase calcification (at least relative to other metabolic processes), even in the dark, when nutrients become depleted (Linschooten et al.. 1991; Bleijswijk et al., 1994; Paasche and Brubak, 1994; Wal et al., 1995). Phacorus, a calcareous freshwater analog of coccolithophorids, also tends to bloom late in the growing season, when nutrients are depleted (Huber-Pestalozzi, 196 1; Thomas, 1980). Planktonic cyanobacteria tend to proliferate late in the growing season, especially in oligotrophic hard water lakes (Pick, 1991) and nutrient-deficient seawater (Robbins and Blackwelder, 1992; Estrada et al., 1993). Cyanobacterial mats are likewise especially prominent in oligotrophic environments (Whitton and Potts, 1982; Paerl et al., 1993, 1994).

5. Structural and defensive uses for carbonates Hay et al. (1994) noted that calcareous algae proliferated long before macrofaunal herbivores evolved. Algal calcification therefore did not arise as a defense against herbivores, although plants have since adapted calcification to defensive needs. Carbonates have three notable properties which consumers might dislike: physical hardness, acid neutralizing capacity, and displacement of nutritious components of the food by carbonates. The deterrent properties of carbonates have been partially tested by adding CaCO, (and likewise silica) to synthetic foods (Table 2). CaCO, additions in excess of 50% dry weight often reduce consumption, especially by feeding generalists, although the deterrent effects are often modest. Pennings and Svedberg (1993) for example found that one species of sea urchin slightly disliked particulate aragonite (but accepted powdered calcite), others didn’t care, or even preferred CaCO, augmented foods. Structural benefits appear minimal in calcareous freshwater macrophytes such as Charu and Potamogeton, which grow without calcifying in acidic or Ca*+-depleted water. Chum sometimes becomes weighted down by its encrustations. The upper calcareous leaf surface of Potamogeton readily sheds

Table 2 Consumer responses to dietary carbonate and silica. Herbivore responses are scored from -2 (strong rejection) to +2 (strong preference for) calcite (Cal) aragonite (Ara) and silica (Sil) additions Herbivores Urchins: Il. unlillurum

Echinomrtrcr.sp. Dicrdemasetosum Mespilia globulus

Cal

0, - I +I +I 0

Ara

Sil

Reference

1 0

2

-1 -1

2 2

Molluscs:

Dolubellr auriculoriu

-I

3

Fish: Parrotfishes Damselfishes Surgeonfishes Natural fish populations

0 -1 -1 - 2

4 4 5

C)mudusu jilosu

-I

1

Predators Natural fish populations Natural fish populations Natural fish populations Natural fish populations Natural fish populations Natural fish populations Snail Cyphomu uenrilina Sea stars

- I - 1 - 1 - 2 0 - 1 0

1

Crustaceans:

0

6 7

8 9 IO II 10 11

References: 1= Hay et al., 1994; 2 = Pennings and Svedberg, 1993; 3 = Pennings and Paul, 1992; 4 = Schupp and Paul, 1994: 5 = Meyer and Paul, 1995; 6 = Chanas and Pawlik, 1995; 7 = Harvell et al., 1988; 8 = Harvell and Fenical, 1989; 9 =Van Alstyne et al., 1992; 10 = Van Alstyne and Paul, 1992; 11 = Slattery and McClintock, 1995.

carbonates, suggesting that the plant tries to avoid carbonate accumulation. Calcification was not mentioned as a factor affecting invertebrate herbivory by Jacobsen and Sand-Jensen (1995). Coccolithophorids sometimes dump their scales and swim around naked, suggesting that they can dispense with both the armor and the skeleton (Balch et al., 1993). Alternatively, they may continue calcifying after they are completely covered with coccoliths, suggesting that calcification offers important benefits beyond structure and protection. Calanoid copepods have mildly alkaline guts (Pond et al.,

T.A. McConnaughey, J. F. Whelan/Earth-Science

19951, and readily feed on coccolithophorids (Harris, 1994; Wal et al., 1995). Sikes and Wilbur (1982) concluded that coccoliths offer little protection against grazers, and coccolith accumulation sometimes even increases susceptibility to grazing by increasing cell size (P. van der Wal, pers. commun., 1996). A recent review of copepod diets (Kleppel, 1993) did not mention rejection of coccolithophorids. Suspended calcite likewise did not reduce grazing rates by freshwater copepods, and had only slight effects on cladocera (Vanderploeg et al., 1987.) Symbiotic corals continue calcifying long after they have built suitable skeletons. They sometimes accumulate skeletal heaps several meters high, but inhabit only the top few millimeters. The skeleton occurs underneath the tissue layer, so it would appear to offer minimal protection against predators such as sea stars, urchins, and snails. It may however deter biting predators such as parrot fishes. Under stressful conditions the coral polyps sometimes abandon their skeletons, suggesting that corals, like anemonies, can dispense at least temporarily with both the support and protection offered by the skeleton. Some of the symbiotic tridacnid giant clams cannot close their shells completely, suggesting that their massive shells are not just defensive in nature. Such anecdotal evidence suggests that calcareous plants and symbioses usually derive substantial benefits from calcification, in addition to any structural and defensive benefits from skeletal carbonates.

6. Environmental

controls on calcification

6.1. Ca2’ and CO,

In fresh waters, Ca2+ concentrations are often too low to support much calcification, or pH is outside of the optimal range for HCO; utilization. But where aquatic chemistry is suitable, calcification can contribute substantially to plant and ecosystem productivity. In Williams Lake, Minnesota, most of the important submersed macrophytes begin calcifying in late spring (Fig. lo), about the time that free CO, levels drop below atmospheric values, and calcify in approximately 1: 1 ratios to photosynthesis when sufficient Ca2+ is available (Fig. 3A). About l/3 of the

Reviews 42 (1997) 95-1 I7

109

“JFMAMJJASOND MONTH

Fig. 10. Seasonal distribution of calcification and photosynthesis in Williams Lake, Minnesota. Photosynthesis is subdivided into components using CO, and HCO; as substrate. Protons generated through calcification make most of the photosynthetic HCO, assimilation possible.

total plant production in the lake depends on proton generation through calcification, despite sub-optimal Ca2+ levels and substantial summertime Ca*+ depletion (McConnaughey et al., 1994). Calcareous plants and photosynthetic symbioses truly dominate in many alkaline low light and low nutrient conditions. Preference for such conditions usually appears no more likely than preference for CO, depletion, but rather the calcareous autotrophs presumably cope with these adversities better than do their non-calcareous competitors. Light and nutrient deprivation seldom occur together however. Therefore, in a particular environment, calcification in its role as a proton generator is likely to help mainly with one problem or the other. 6.2. Nutrients Coral reefs develop in tropical regions of chronic nutrient shortage, and planktonic blooms of coccolithophorids typically develop during summer, after diatoms and other non-calcareous algae have reduced nutrient concentrations (including iron) to low levels. Coccolithophorids may be the world’s most important calcifiers (Westbroek et al., 1994b), and their

blooms can be visible from space (Ackleson et al.. 1988; Balch et al., 1991; Brown and Yoder, 1994). Freshwater calcareous planktonic algae such as cyanobacteria and Phacorus likewise tend to proliferate late in the growing season and in hard water, oligotrophic systems (Huber-Pestalozzi. 196 1: Thomas, 1980; Pick, 199 1). When nutrients become abundant, non-calcareous plants tend to take over, both in polluted tropical environments (Steven and Larkum, 1993; Miller, 1996) and in seasonally eutrophic extratropical regions. Opportunistic fleshy algae may either outcompete the calcareous forms directly, or change community structure in ways which harm the calcareoua forms.

6.3. Lighf Charles Darwin (1842) observed that coral reefs grow actively only in shallow tropical waters. Light attenuation with depth presumably accounts for the concentration of calcification within the euphotic zone. The tendency for calcification to show a subsurface maximum (Barnes and Taylor, 1973; Baker and Weber, 1975) may reflect an increasing need to calcify as light falls off with depth. The dark of the extratropical winter probably excludes most longlived sessile photosynthetic organisms from high latitudes. Temperate zone plants from kelps to trees shut down or die back during the winter. and corals may be less able to do this. Calcareous macrophytic algae dominate the bottom of the euphotic zone in both the oceans (Aggegian and Abbott, 1985; Blair and Norris, 1988; Littler et al., 1985, 1988) and in fresh waters (Schwarz et al., 1996). Coccolithophorids and cyanobacteria likewise tend to dominate the deep plankton in both the oceans (Estrada et al., 1993: Ikeya et al., 1994) and fresh waters (Pick and Agbeti, 199 1). High quantum efficiencies may help them to survive the lower euphotic zone. Balch et al. (1992) suggested that C/P ratios increase with depth, and in comparing highly and lightly calcareous varieties of coccolithophorids, Nielsen ( 1995) and Israel and Gonzalez (1996) reported that highly calcareous coccolithophorids grew faster and had higher photosynthetic efficiencies at low light levels.

7. Geochemistry Even under the conditions of CaCO, supersaturation which exist in many lakes and marine surface waters, biological calcification often far outpaces non-biological calcification. This mainly reflects the ability of a truns calcification mechanism to attain high CaCO, supersaturations. Rapid calcification creates a convenient source of protons, which are useful for such purposes as converting HCO; to CO?. and for assimilating inorganic nutrients. Plants and photosynthetic symbioses account for much of the carbonate which accumulates as reefs and deep-sea oozes (Milliman, 1974; Morse and Mackenzie, 1990). This is known mainly from textural analyses, although biological carbonates can also be distinguished from inorganically precipitated carbonates on the basis of isotopic (Gonzalez and Lohman, 1985; McConnaughey, 1989b) and chemical (Carpenter and Lohmann, 1992) properties. Since the onset of biological calcification, most of the carbon in the biosphere has been converted into carbonates (Fig. 11). Reaction 3 leads in principle to equimolar accumulations of CaCO,, CH,O and O?. Such stoichiometries are often observed in short term single species incubations, and sometimes in highly calcareous reef environments during the daytime (Smith, 1973; Kinsey, 1985; Crossland et al., 199 1; Gattuso et al., 1993). Global inventories of organic carbon and oxygen fall short of carbonate accumulations however, illustrating that carbonates tend to preserve better, and that numerous additional reac-

Global Carbon Reservoirs

(10’~ moles c) 0 o 0

Biomass .04 Atmosphere .06 Dead .31

n

Ocean DIC

10 Fuels

2.8

.5

Box volumes proportionalto quantityof carbon Fig. 1 I. Global carbon reservoirs, after Lasaga et al. (1985).

The

bar graphs within the carbonate box provides some sense of when carbonates were precipitated, and their mineralogies.

T.A. McConnaughey, J. F. Whelan/Earth-Science

tions contribute to the chemical evolution of the biosphere. Global net (production minus destruction) C/P ratios may change with time. Global net C/P ratios might increase, for example, in response to deglacial sea level rise (Opdyke and Walker, 1992). Over geologic time, changing net C/P ratios appear to have influenced atmospheric CO, levels and therefore global heat budgets (Bemer, 1991). Carbonate production has obvious homeostatic attributes, such as the tendency for plant C/P ratios to increase with pH, but little is actually known about how such factors contribute to global carbon cycles. Nor is it known how much more supersaturated the oceans might be, or whether Pco,values would be significantly lower, if biological calcification were not so important. The use of calcification as a proton generator potentially influences global geochemistry in additional, subtle ways that are not obviously tied to carbonates or carbon dioxide. For example, to the extent that calcification allows aquatic plants to colonize low light and low nutrient environments, calcification may intensify the nutrient depletion which occurs in surface waters, and deepen the nutrient-depleted zones. On land, proton secretion by plant roots accelerates the weathering of silicate minerals (Hinsiger et al., 1992; Drever and Vance, 1993; Drever, 1994), which form the bulk of continental crust. The importance of root calcification to proton secretion and to mineral weathering remains completely unknown. In alkaline soils of high acid neutralizing capacity, root calcification may however be significant both to plant nutrition and soil development.

8. Summary A Ca*+ ATPase-based tram calcification mechanism seems to apply widely among plants and animals. This physiology allows organisms to attain high CaCO, supersaturations and therefore high rates of calcification. Autotrophs inhabiting alkaline environments often turn to calcification as a convenient proton generator. Terrestrial plants sometimes use root calcification to generate protons needed to solubilize and absorb soil nutrients. Aquatic plants and

Reuiews 42 (1997) 95-l 17

111

algae-invertebrate symbioses use the protons to assimilate HCO;, and probably also several inorganic nutrient elements. The resulting marls and reefs accumulate more or less where they would be expected on the basis of benefit to photosynthesis and nutrient acquisition, and constitute the biosphere’s largest carbon reservoirs.

References Ackleson, S., Balch, W.M. and Holligan, P.M., 1988. White waters of the Gulf of Maine. Oceanology, 1: 18-22. Aggegian, C.R. and Abbott, LA., 1985. Deep-water macroalgal communities: a comparison between Penguin Bank, Hawaii and Johnston Atoll. In: Proc. 5th lnt. Coral Reef Congr., Tahiti, pp. 47-5 I. Allemand, D. and Grille, M.C., 1992. Biocalcification mechanism in gorgonians - 45Ca uptake and deposition by the Mediterranean red coral Corallium rubrum. J. Exp. Zool., 262: 237246. Al-Moghrabi, S., Goiran, C., Allemand, D., Speziale, N. and Jaubert, J., 1996. Inorganic carbon uptake for photosyntheis by the symbiotic coral-dinoflagellate association. II. Mechanisms for bicarbonate uptake. J. Exp. Mar. Biol. Ecol., 199: 227-248. Ariovich, D. and Pienaar, R.N., 1979. The role of light in the incorporation and utilization of Ca*+ ions by Hymenomonas carterae. (Braarud et Fagerl.) Braarud (Prymnesiophyceae). Br. Phycol. J., 14: 17-24. Atkinson, M.J., Carlson, B. and Crow, G.L., 1995. Coral growth in high-nutrient, low-pH seawater: a case study of corals cultured at the Waikiki Aquarium, Honolulu, Hawaii. Coral Reefs, 14: 215-223. Baker, P.A. and Weber, J.N., 1975. Coral growth rate: variation with depth. Earth Planet. Sci. Lett., 27: 57-61. BaJch, W.M., Holligan, P.M., Ackleson, S.G. and Voss, K.J., 1991. Biological and optical properties of mesoscale coccolithophorid blooms in the Gulf of Maine. Limnol. Oceanogr., 36: 629-643. Balch, W.M., Holligan, P.M. and Kilpatrick, K.A., 1992. Calcification, photosynthesis, and growth in the bloom-forming cocEmiliania huxleyi. Continental Shelf Res., 12: colithophore, 1353-1374. Balch, W.M., Kilpatrick, K., Holligan, P.M. and Cucci, T., 1993. Coccolith production and detachment by Emiliania huxleyi (Prymnesiophyceae). J. Phycol., 29: 566-575. Barnes, D.J. and Crossland, C.J., 1978. Diurnal productivity and apparent “C-calcification in the staghom coral, Acropora acuminara. Comp. B&hem. Physiol., 59A: 133-138. Barnes, D.J. and Taylor, D.L., 1973. In situ studies of calcification and photosynthetic carbon fixation in the coral Monfasrrea annualaris. Helgol. Wiss. Meeresunters., 24: 284-291. Beer, S., Spencer. W.E. and Bowes, G., 1992. HCO; use and evidence for a carbon concentrating process in the mat-forming cyanophyte Lyngbya birgei G.M. Smith. Aquat. Bot., 42: 159-171.

II2

T.A. McConnaughey

J.F. Whelan /Eurth-Science

Bemer, R.A., 199 I. A model for atmospheric CO? over phanerozoic time. Am. J. Sci., 291: 339-376. Bischoff, G.W., 1828. Die kryptogamischen Gewachse mit besonderer Beriicksigtigung der Flora Deutschlands und der Schweiz, organographisch, anatomisch, physiologisch, und systematisch. J.L. Schrag, Numberg. Bisson, M.A., Sigel, A., Chau, R., Gelsomino, S.A. and Herdic, S.L., 1991. Distribution of Charasomes in Chow: Banding pattern and effect of photosynthetic inhibitors. Aust. J. Plant Physiol., 18: 8 l-93. Blair, S.M. and Norris. J.N.. 1988. The deep-water species of Halimeda Lamouroux (Halimedaceae, Chlorophytal from San Salvador Island, Bahamas: species composition, distribution and depth records. Coral Reefs, 6: 227-236. Borowitzka, M.A., 1983. Calcium carbonate deposition by reel algae: Morphological and physiological aspects. In: D.J. Barnes (Editor), Perspectives on Coral Reefs. Brian Clouston, Manuka, pp. 16-28. Borowitzka, M.A. and Ldrkum, A.W.D., 1976a. b, c, d. Calcification in the green alga Halimeda. J. Exp. Bot.. 27: 27-51. 864-878, 879-893, 894-907. Brown, C.W. and Yoder, J.A., 1994. Coccolithophorid blooms in the global ocean. J. Geophys. Res., 99tC4): 7467-7482. Brownlee, C., Nimer, N., Dong, L. and Merrett, M., 1994. Cellular regulation during calcification in Emiliania huxleyi. In: J. Green and B. Leadbeater (Editors), The Haptophyte Algae. Clarendon Press, Oxford, pp. 133-148. Carpenter, S.J. and Lohmann, K.C., 1992. Sr/Mg ratios of modem marine calcite: empirical indicators of ocean chemistry and precipitation rate. Geochim. Cosmochim. Acta, 56: 18371849. Chalker, B.E. and Taylor, D.L., 1978. Rhythmic variations in calcification and photosynthesis associated with the coral Acropora ceruicornis (Lamarck). Proc. R. Sot. London, 8201: 179- 189. Chanas, B. and Pawlik, J.R.. 1995. Defenses of Caribbean sponges against predatory reef fish. II. Spicules, tissue toughness, and nutritional quality. Mar. Ecol. Prog. Ser., 127: 195-21 I. Cook, C.B., Muller-Parker, G. and Orlandini, CD., 1994. Ammonium enhancement of dark carbon fixation and nitrogen limitation in zooxanghellae symbiotic with reef corals Mudrack mirabilis and Montastrea annularis. Mar. Biol., 118: 157- 165. Crossland, C.J., Hatcher, B.G. and Smith, S.V., 1991. Role of coral reefs in global ocean production. Coral Reefs, 10: 55-63. Darwin, C., 1842. The Structure and Distribution of Coral Reefs. Smith, Elder and Co., 214 pp. Davies, P.S., 1984. The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouri. Coral Reefs, 2: 181-186. Delgado, 0. and Lapointe, B.E., 1994. Nutrient-limited productivity of calcareous versus fleshy macroalgae in a eutrophic, carbonate-rich tropical marine environment. Coral Reefs, 13: 151-159. Dixon, D.A. and Haynes, D.H., 1989. Cal+ pumping ATPase of cardiac sarcolemma is insensitive to membrane potential produced by K+ and Cl- gradients but requires a source of counter-transportable H+. J. Membrane Biol., 112: 169-183. Dong, L.F., Nimer, N.A., Okus, E. and Merrett. M.M.. 1993.

Rec,iews 42 (1997) 95-l

I7

Dissolved inorganic carbon utilization in relation to calcite prpoduction in Emiliania huxleyi (Lohmann) Kamptner. New Phytol., 123: 679-684. Drever, J.I., 1994. The effect of land plants on weathering rates of silicate minerals. Geochim. Cosmochim. Acta, 58: 2325-2332. Drever. J.I. and Vance, G.F.. 1993. Role of soil organic acids in mineral weathering processes. Chapter 6. In: E.D. Pittman and M.D. Lewan (Editors), Organic Acids in Geological Processes. Springer, Berlin, pp. 138- 161. Driessen, A.J.M. and Konings, W.N., 1986. Calcium transport in membrane vesicles of Streptococcus cremoris. Eur. J. Biochem., 159: 149-155. Duguay, L.E., 1983. Comparative laboratory and field studies on calcification and carbon fixation in foraminiferal-algal associations. J. Foram. Res., 13: 252-261. Duguay, L.E. and Taylor, D.L., 1978. Primary production and calcification by the soritid foramifer Archaias angulatus. J. Protozool.. 25: 356-361. Erez, J.. 1983. Calcification rates, photosynthesis, and light in planktonic foraminifera. In: P. Westbroek and E.W. de Jong (Editors), Biomineralization and Biological Metal Accumulation. Reidel, Dordrecht, pp. 307-312. Espie, G.S., Miller, A.G. and Canvin, D.T., 1991. High affinity transport of COT in the cyanobacterium Synechococcus UTEX 625. Plant Physiol., 97: 943-953. Esteban, M. and Klappa, C.F., 1983. Subaerial exposure environment. Chapter I. In: P.A. Scholle, D.G. Bebout and C.H. Moore (Editors), Carbonate Depositional Environments. Am. Assoc. Petrol. Geol. Mem., 33: l-54. Estrada. M., Marrast, C., Latasa, M., Berdalet, E., Delgado, M. and Riera. T., 1993. Variability of deep chlorophyll maximum characteristics in the Northwestern Mediterranean. Mar. Ecol. Prog. Ser., 92: 289-300. Evered, D. and Whelan, J. (Editors), 1986. Calcium and the Cell. Wiley, Chichester. Fang, L-S., Chen, Y.-W. and Chen, C.-S., 1983. Why does the white tip of stony coral grow so fast without zooxanthellae’? Mar. Biol., 103: 359-363. Fedke, C., 1982. Biochemistry and Physiology of Herbicide Action. Springer, Berlin, 202 pp. Fitt. W.K., Rees, T.A.V. and Yellowlees, D., 1995. Relationship between pH and the availability of dissolved inorganic nitrogen in the zooxanthella-giant clam symbiosis. Limnol. Oceanogr., 40: 976-982. Fox, T.R. and Comerford, B.B., 1992. Influence of oxalate loading on phosphorus and aluminum solubility in spodosols. Soil Sci. Sot. Am. J., 56: 290-294. Frossard, E., Brossard, M., Hedley, M.J. and Metherell, A., 1994. Reactions controlling the cycling of P in soils. In: H. Tiessen (Editor), Phosphorous in the Global Environment, Ch. 7. Wiley, Chichester, pp. 121-140. Gattuso, J.-P., Pichon, M., Delesalle, B. and Frankignoulle, M.. 1993. Community metabolism and air-sea CO, fluxes in a coral reef ecosystem (Moorea, French Polynesia). Mar. Ecol. Prog. Ser.. 96: 259-267. Gavin. O., Pilet, P.-E. and Chanson, A., 1993. Tonoplast localization of a calmodulin-stimulated Ca2+ pump from maize roots. Plant Sci., 92: 143- 150.

T.A. McConnaughey, .I.F. Whelan/Earth-Science Gladfelter, E.H., 1982. Skeletal development in Acropora ceruicorks: I. Patterns of calcium carbonate accretion in the axial corallite. Coral Reefs, 1: 45-51. Gladfelter, E.H., 1983. Circulation of fluids in the gastrovascular system of the reef coral Acropora cemicornis. Biol. Bull., 165: 619-636. Gladfelter, E.H., Michel, G. and Sanfelici, A., 1989. Metabolic gradients along a branch of the reef coral Acropora palmata. Bull. Mar. Sci., 44: 1166-l 173. Goiran, C., Al-Moghrabi, S., Allemand, D. and Jaubert, J., 1996. Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellate association, I. Photosynthetic pertormantes of symbionts and dependence on sea water bicarbonate. J. Exp. Mar. Biol. Ecol., 199: 207-225. Golubic, S., 1973. The relationship between blue-green algae and carbonate deposits. In: N.G. Carr and B.A. Whitton (Editors), The Biology of Blue-Green Algae. Botanical Monographs, 9, ch. 21. Blackwell, Oxford, 434-472. Gonzalez, L.A. and Lohman, K.C., 1985. Carbon and oxygen isotopic composition of Holocene reefal carbonates. Geology 13: 811-814. Goreau, T.F., 1963. Calcium carbonate deposition by coralline algae and corals in relation to their roles as reef-builders. Ann. N.N. Acad. Sci., 107: 127-167. Graustein, W.C., Cromack, K. Jr. and Sollins, P., 1977. Calcium oxalate: Occurrence in soils and effect on nutrient and geochemical cycles. Science, 198: 1252-1254. Grusak, M.A. and Pezeshgi, S., 1996. Shoot-to-root signal transmission regulates root Fe(II1) reductase activity in the dgl mutant of pea. Plant Physiol., 110: 329-334. Gutknecht, J., Bisson, M.A. and Tosteson, F.C., 1977. Diffusion of carbon dioxide through lipid bilayer membranes. Effects of carbonic anhydrase, bicarbonate, and unstirred layers. J. Gen. Physiol., 69: 779-794. Harris, R.P., 1994. Zooplankton grazing on the coccolithophore Emiliania huxleyi and its role in inorganic carbon flux. Mar. Biol., 119: 431-439. Harvell, C.D., Fenical, W. and Greene, C.H., 1988. Chemical and structural defenses of Caribbean gorgonians (Pseudopterogorgia spp. ). I. Development of an in situ feeding assay. Mar. Ecol. Prog. Ser., 49: 287-294. Harvell, C.D. and Fenical, W., 1989. Chemical and structural defenses of Caribbean gorgonians (Pseudopterogorgia spp. 1: Intracolony localization of defense. Limnol. Oceanogr., 34: 382-389. Hay, M.E., Kappel, Q.E. and Fenical, W., 1994. Synergisms in plant defenses against herbivores: Interactions of chemistry, calcification, and plant quality. Ecology, 75: 1714- 1726. Hinsiger, P., Jaillard, B. and Dufey, J.E., 1992. Rapid weathering of a trioctahedral mica by roots of ryegrass. Soil Sci. Sot. Am. J., 56: 977-982. Huber-Pestalozzi, G., 1961. Das Phytoplankton des Sligwassers. Systematik und Biologie. 5. Teil Chlorophyceae (Griinalgen). Schweizerbart’sche Verlagsbuchhandlung, Stuttgart. Ikeya, T., Ohki, K. Takahashi, M. and Fujita, Y., 1994. Photosynthetic characteristics of marine Synechococcus spp. with special reference to light environments near the bottom of the euphotic zone in the open ocean. Mar. Biol., 118: 215-221.

Reciews 42 (1997) 95-l 17

113

Ip, Y.K., Lim, A.L.L. and Lim, R.W.L. (1991). Some properties of calcium-activated adenosine triphosphatase from the hermatypic coral Galaxea fasciculuris.Mar. Biol., 111: 19 1- 197. Isa, Y., Norikatsu, I. and Yamazato, K., 1980. Evidence for the occurrence of Ca*+ dependent adenosine triphosphatase in a hermatypic coral, Acropora hebes, Dana. In: Proc. 4th Int. Coral Reef Symp. Manilla, pp. 99-106. Israel, A.A. and Gonzalez, E.L., 1996. Photosynthesis and inorganic carbon utilization in Pleurochrysis sp. (Haptophyta), a coccolithophorid alga. Mar. Ecol. Prog. Ser., in press. Jacobsen, D. and Sand-Jensen, K., 1995. Variability of invertebrate herbivory on the submerged macrophyte Potamogeton perfoliatus. Freshwater Biol., 34: 357-365. Jaillard, B., 1987. Les Structures Rhizomorphes Calcaires: Modele de Reorganisation des Mineraux du Sol par les Racines. These, Univ. Sci. Tech. Languedoc, Montpellier, 220 pp. Jaillard, B., Guyon, A. and Maurin, A.F., 1991. Structure and composition of calcified roots, and their identification in calcareous soils. Geoderma, 50: 197-210. Jensen, P.R., Gibson, R.A., Littler, M.M. and Littler, D.S., 1985. Photosynthesis and calcification in four deep-water Hulimeda species (chlorophyceae, Caulerpales). Deep-Sea Res., 32: 45 l-464. Johnston, I.S., 1980. The ultrastructure of skeletogenesis in hermatypic corals. Int. Rev. Cytol., 67: 171-214. Kaplan, A., Schwarz, R., Lieman-Hurwitz, J. and Reinhold, L., 1991. Physiological and molecular aspects of the inorganic carbon-concentrating mechanism in cyanobacteria. Plant Physiol., 97: 851-855. Kingsley, R.J. and Watabe, N., 1984. Calcium uptake in the Gorgonian Leptogorgia uirgulata. The effects of ATPase inhibitors. Comp. Biochem. Physiol., 79A: 487-491. Kingsley, R.J. and Watabe, N., 1985. Ca-ATPase localization and inhibition in the gorgonian kptogorgia oirguluta (Lamarck) (Coelenterata: Gorgonaceal. J. Exp. Mar. Biol. Ecol., 93: 157-167. Kinsey, D.W., 1985. Metabolism, calcification, and carbon production. System level studies. In: Proc. 5th Int. Coral Reef Congr., 4: 363-377. Kinsey, D.W., 1988. Coral reef system response to some natural and anthropogenic stresses. Galaxea, 7: 113-128. Kinsey, D.W. and Davies, P.J., 1979. Effects of elevated nitrogen and phosphorus on a coral reef. Limnol. Oceanogr., 24: 935940. Klaveness, D., 1976. Emilianiu huxleyi (Lehman) Hay and Mohler. 3. Mineral deposition and the origin of the matrix during coccolith formation. Protistologica, 12: 217-224. Kleppel, G.S., 1993. On the diets of calanoid copepods. Mar. Ecol. Prog. Ser., 99: 183-195. Klumpp, D.W. and Griftiths, C.L., 1994. Contributions of phototrophic and heterotrophic nutrition to the metabolic and growth requirements of four species of giant clam (Tridacnidae). Mar. Ecol. Prog. Ser., 115: 103-115. Kochian, L.V., 1991. Mechanisms of micronutrient uptake and translocation in plants. In: J.J. Mortvedt (Editor), Micronutrients in Agriculture. Soil Science Society of America, Madison WI, pp. 229-296, Kristiansen, S., Thingstad, T.F., van der Wal, P., Farbrot, T. and

I I4

T.A. McCmnnughey.

J.F. Whelm / Eurth-kimcr

Skjoldal, F., 1994. An Emilimi hunlrvi dominated bloom beneath the brackish layer of the Samnangerljord, western Norway. Importance of hydrography and nutrients. Sarsia, 79: 357-368. Kronzucker, H.J., Siddiqi. M.Y. and Glass, A.D.M.. 1996. Kinetics of NH: influx in spruce. Plant Physiol., I IO: 773-779. Kuile, B. Ter and Erez. J., 1987. Uptake of inorgnic carbon and internal carbon cycling in symbiont-bearing benthonic foraminifera. Mar. Biol., 94: 499-509. Kuile, B. Ter, Erez, J. and Padan. E.. 1989a. Mechanisms for the uptake of inorganic carbon by two species of symbiont-bearing foraminifera. Mar. Biol., 103: 24 I-25 I. Kuile, B. Ter. Erez, J. and Padan. E.. 1989b. Competition foiinorganic carbon between photosynthesis and calcificatton in the symbiont-bearing foraminifer Amphistegina lohifeni. Mar. Biol., 103: 253-259. Kwon. D.-K. and Gonzalez, E.L., 1994. Localization of Ca’+stimulated ATPase in the coccolith-producing compartment ot cells of Pleurochrysis sp. (Prymnesiophyceae). J. Phycol.. 30: 689-695. Landsberg, E.-C., 1986. Function of rhizodermal transfer cells in the Fe stress response mechanism of Cupsicunt clnnuum L. Plant Physiol., 82: 5 I I-S 17. Lasaga, A.C., Berner, R.A. and Garre1s.R.M.. 1985. An improved geochemical model of atmospheric CO? fluctuations over the past 100 million years. In: E.T. Sundquist and W.S. Broecker (Editors), The Carbon Cycle and Atmospheric CO:: Natural Variations Archaen to Present. Geophys. Monogr.. 32. Am. Geophys. Union, Washington, D.C., pp. 397-41 I. Linschooten, C.H., van Bleijswijk, J.D.L.. Emburg, P.R., de Vrind, J.P.M., Kempers. ES., Westbroek, P. and de Vrind-de Jong. E.W.. 1991. Role of light-dark cycle and medium composition huxkw on the production of coccoliths by Emikrniu (Haptophyceaeb J. Phycol., 27: 82-86. Littler. M.M., Littler, D.S., Blair, S.M. and Norris, J.N., 1985. Deepest known plant discovered on an uncharted seamount. Science, 227: 57-59. Littler. M.M., Littler, D.S. and Lapointe, B., 1988. A comparison of nutrient- and light-limited photosynthesis in psammophytic versus epilithic forms of H&n& (Caulerpales, Halimedaceae) from the Bahamas. Coral Reefs, 6: 219-225. Lowenstam, H.A. and Weiner, S., 1989. On Biomineralization. Oxford University Press, 324 pp. Lucas, W.J. and Berry. J.A. (Editors), 1985. Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms. American Society of Plant Physiologists. Rockville Md. Mann, S., Webb, J. and Williams. R.J. 1989. Biomineralization: Chemical and Biochemical Perspectives. VCH Press, 541 pp. Maraiion, E., Femandez, E.. Haris, R.P. and Harbour, D.S.. 1996. Effects of the diatom-Emilianiu huxleG succession on photosynthesis, calcification, and carbon metabolism by size-fractionated phytoplankton. Hydrobiologia, 3 17: 189- 199. Marshall. A.T., 1996. Calcification in hermatypic and ahermatypic corals. Science, 27 1: 637-639. McAuley, P.J. and Smith. V.J., 1995. Effect of die1 photoperiod on nitrogen metabolism of cultured and symbiotic zooxanthellae. Mar. Biol., 123: 145152.

Rrc~irws 42 (IYY7)

YS-I I7

McClure. P.R.. Kochian. L.V., Spanswick, R.M. and Schaff. J.E.. 1990. Evidence for cotransport of nitrate and protons in maize roots. Measurement of NO, and Ht fluxes with ion-selective microelectrodes. Plant Physiol., 93: 290-294. McConnaughey, T.A., 1989a. b. “C and “0 isotopic disequilibrium in biological carbonates. 1. Patterns. II. In vitro simulatton of kinetic isotope effects. Geochim. Cosmochim. Acta. S3: 151-162. 163-171. McConnaughey. T.A.. 1989~. Biomineralization mechanisms. In: R.E. Crick (Editor), Origin, Evolution, and Modern Aspects of Biomineralization in Plants and Animals. Plenum, New York. pp. 57-73. McConnaughey, T.A., 1991. Calcification in Chum cordlirxr: CO, hydroxylation generates protons for bicarbonate assimilation. Limnol. Oceanogr., 36: 619-628. McConnaughey. T.A., 1994. Calcification, photosynthesis, and global carbon cycles. In: F. Doumenge (Editor). Past and Present Biomineralization Proceses. Mu&e Oceanographique. Monaco, pp. l37- 162. McConnaughey. T.A. and Falk. R.H., 1991. Calcium-proton exchange during algal calcification. Biol. Bull. Mar. Biol. Lab.. Woods Hole, Mass., 180: 185-195. McConnaughey, T.A.. Labaugh. J.W.. Rosenberry, D.O., Striegl. R.G.. Reddy. M.M.. Schuster, P.F. and Carter, V., 1994. Carbon budget for a groundwater-fed lake: Calcification supports summer photosynthesis. Limnol. Oceanogr., 39: 13191332. McIntosh. CA. and Oliver, D.J., 1994. The phosphate transporter from pea mitochondria. Plant Physiol., 105: 47-52. Merl. M.U.E., 1992. The biology of carbonate precipitation by cyanobacteria. Facies, 26: 81-102. Merz, M.U.E., Schlue. W.-R. and Zankl, H., 1993. pH-measurcments in the sheath of calcifying filamentous cyanobacteria. Biomineralization 93, Program and Abstracts, #45, p. 48. Musee Octanographique, Monaco. Meyer, K.D. and Paul, V.J.. 1995. Variation in secondary metabolite and aragonite concentrations in the tropical green seaweed Nronzeris mnualtu: effects on herbivory by fishes. Mar. Biol.. 122: 537-545. Miller, S., 1996. Carolina, the keys, and coral reef research. Geotimes. Apr. 1996: 24-27. Milliman. J.D., 1974. Recent Sedimentary Carbonates. I. Marine Carbonates. Springer, Berlin, 375 pp. Mori. I.C., Sate. G. and Okazaki, M.. (manuscript, 1996). Proton transport by Ca’+-ATPase associated with the plasma membrane from a calcareous alga seratacardia maxima (Corallinaceae, Rhodophyta). Submitted to J. Jap. Sot. Phycology. Morse. J.W. and Mackenzie, F.T., 1990. Geochemistry of Sedimentary Carbonates. Elsevier. Amsterdam, 707 pp. Muchhal, U. and Raghothama, K.G., 1995. Phosphate starvation induced changes in the expression of tomato Ca*+ ATPase. Plant Physiol.. 108: 112. Muggli, D.L. and Harrison, P.J., 1996. Effects of nitrogen source on the physiology and metal nutrition of Emiliania hux/e,vi grown under different iron and light conditions. Mar. Ecol. Prog. Ser., 130: 2555267. Muscatine, L., 1980. Productivity of aooxanthellae. In: P.G.

T.A. McConnaughey, J.F. Whelan/Earth-Science Falkowski (Editor), Primary Productivity in the Sea. Plenum, New York, pp. 381-402. Muscatine, L. and D’Elia, C.F., 1978. The uptake, retention, and release of ammonium by reef corals. Limnol. Oceanogr., 23: 725-734. Nielsen, M.V., 1995. Photosynthetic characteristics of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae) exposed to elevated concentrations of dissolved inorganic carbon. .I. Phycol., 31: 715-719. Niggli, V.E., Sigel, E. and Carafoli, E., 1982. The purified Ca2+ pump of the human erythrocyte membranes catalyzes an electroneutral Ca2+ -H* exchange in reconstituted liposomal systems. J. Biol. Chem., 257: 2350-2356. Nimer, N.A. and Merrett, M.J., 1992. Calcification and utilization Emiliania huxleyi of inorganic carbon by the coccolithophorid Lohmann. New Phytol., 121: 173-177. Nimer, N.A. and Merrett, M.J., 1993. Calcification rate in Emiliania huxleyi Lohmann in response to light, nitrate, and availability of inorganic carbon. New Phytol., 123: 673-677. Nimer, N.A., Brownlee, C. and Merrett, M.J., 1994. Carbon dioxide availability, intracellular pH and growth rate of the coccolithophore Emiliania huxleyi. Mar. Ecol. Prog. Ser., 109: 257-262. Norton, J.H., Shepherd, M.A., Long, H.M. and Fitt, W.K., 1992. The zooxanthellar tubular system in the giant clam. Biol. Bull., 183: 503-506. Ogawa, T. and Kaplan, A., 1987. The stoichiometry between CO, and H’ fluxes involved in the transport of inorganic carbon in cyanobacteria. Plant Physiol., 83: 888-891. Okazaki, M., Fujii, M., Usuda, Y. and Furuya, K., 1984. Soluble Caz+ ATPase and its possible role in calcification in the coccolithophorid Cricosphaera roscoffensis var. Haptonemofera (Haptophyta). Bot. Mar., 27: 363-369. Opdyke, B.N. and walker, J.C.G., 1992. Return of the coral reef hypothesis: Basin to shelf partitioning of Ca CO, and its effects on CO,. Geology, 20: 733-736. Paasche, E., 1964. A tracer study of the inorganic carbon uptake during coccolith formation and photosynthesis in the coccolithophorid Cocco&hus huxleyi. Plant Physiol., Suppl. III: 5-82. Paasche, E. and Brubak, S. (1994). Enhanced calcification in the coccolithophorid Emiliania huxleyi (Haptophyceae) under phosphorous limitation. Phycologia, 33: 324-330. Paces, J.B., Mahan, S.A., Kwak, L., Neymark, L.A., McConnaughey, T.A. and Bush, C.A., 1994. Preliminary Age Estimates for Late Pleistocene Ground-water Discharge Deposits near Yucca Mountain, Nevada. U.S. Geol. Surv. Open File Rep., 94-703. Paerl, H.W., Bebout, B.M., Joye, S.B. and Des Marais, D.J., 1993. Microscale characterization of disolved organic matter production and uptake in marine microbial mat communities. Limnol. Oceanogr., 38: 1150-1161. Paerl, H.,W., Bebout, B.M., Currin, C.A., Fitzpatrick. M.W. and Pinckney, J.L., 1994. Nitrogen fixation dynamics in microbial mats. In: L.J. Stal and P. Caumette (Editors), Microbial Mats. Springer, Berlin, pp. 325-337.

Reviews 42 (1997) 95-117

115

Pate, J.S., 1994. The mycorrhizal association: just one of many nutrient acquiring specializations in natural ecosystems. Plant Soil, 159: I- 10. Pennings, S.C. and Paul, V.J., 1992. Effect of plant toughness, calcification, and chemistry on herbivory by Dolabella auricularia. Ecology, 73: 16061619. Pennings, S.C. and Svedberg, J., 1993. Does CaCO, in food deter feeding by sea urchins? Mar. Ecol. Prog. Ser., 101: 163-167. Pentecost, A., 1978. Calcification and photosynthesis in Corallina oficinalis L. using the 14C02 method. Br. Phycol. J., 13: 383-390. Pfeiffer, W. and Hager, A., 1993. A Ca+‘-ATPase and a Mg*+/H+ antiporter are present on tonoplast membranes from roots of Zea maize L. Planta, 191: 377-385. Pick, F.R., 1991. The abundance and composition of freshwater picocyanobacteria in relation to light penetration. Limnol. Oceanogr., 36: 1457-1462. Pick, F.R. and Agbeti, M., 1991. The seasonal dynamics and composition of photosynthetic picoplankton communities in temperate lakes in Ontario, Canada. Int. Rev. Ges. Hydrobiol., 76: 565-580. Pohlman, A.A. and McCall, J.G., 1988. Soluble organics from forest litter and their role in metal dissolution. Soil Sci. Sot. Am. J., 52: 265-271. Pond, D.W., Harris, R.P. and Brownlee, C., 1995. A microinjection technique using a pa-sensitive dye to determine the gut pH of Calanus helgolandicus. Mar. Biol., 123: 75-79. Price, G.D., Badger, M.R., Bassett, M.E. and Whitecross, MI., 1985. Involvement of plasmalemmasomes and carbonic anhydrase in photosynthetic utilization of bicarbonate in Chara corallina. Aust. J. Plant Physiol., 12: 241-256. Prim, H.B.A., Snel, J.F.H., Zanstra, P.E. and Helder, R.J.. 1982. The mechanism of bicarbonate assimilation by the polar leaves at the leaf of Potamogeton and Elodea. CO, concentrations surface. Plant Cell Environ., 5: 208-214. Rabotti, G. and Zocchi, G., 1994. Plasma membrane-bound H+ATPase and reductase activities in Fe-deficient cucumber roots. Physiol. Plant, 90: 775-785. Rasi-Caldogno, F., Pugliarello, M.C. and de Michelis, MI., 1987. The Ca2+ transport ATPase of plant plasma membrane catalyzes a nH+/Ca’+ exchange. Plant Physiol., 83: 994-1000. Raven, J.A., 1991. Terrestrial rhizophytes and H+ currents circulating over at least a millimetre: an obligate relationship? New Phytol., 117: 177-185. Raven, J.A., 1992. Hf extrusion and organic-acid synthesis in N,-fixing symbioses involving vascular plants. New Phytol., 114: 369-389. Raven, J.A., Franco,A.A., de Jesus, E.L. and Jacob Neto, J., 1990. H+ extrusion and organic acid synthesis in N,-fixing symbiosis involving vascular plants. New Phytol., 114: 369-389. Rees, T.A.V., Fitt, W.K. and Yellowlees, D., 1994. Host glutamine synthetase activities in the giant clam-zooxanthellae symbiosis: effects of clam size, elevated ammonia and continuous darkness. Mar. Biol., 118: 681-685. Reeves, CC. Jr., 1976. Caliche. Estacado Books, Lubbock, TX, 233 pp.

116

T.A. McConnaughr~.

.I.F. Whrlun / Earth-Science Keriews 42 ( 19971 YS- 117

Riegman, R.. Noordeloos, A.A.M. and Cadte, G.C., 1992. Phaeocystis blooms and eutrophication of the continental zones oi the North Sea. Mar. Biol., I 12: 479-484. Rinkevich, B. and Loya. Y., 1984. Does light enhance calcification in hermatypic corals? Mar. Biol., 80: l-6. Risk, M.J. and Sammarco. P.W. (199 I ). Cross-shelf trends in skeletal density of the massive coral Porites lobaru from the Great Barrier Reef. Mar. Ecol. Prop. Ser.. 69: 195-200. Robbins, L,L. and Blackwelder, P.L., 1992. Biochemical and ultrastructural evidence for the origin of whitings: a biologically induced calcium carbonate precipitation mechanism, Geology, 20: 464-468. Ross, W.D. and Delaney, R.H.. 1977. Massive accumulation of calcium carbonate and its relation to nitrogen fixation of sainfoin. Agronomy J.. 69: 242-246. Roth, A.A., Clausen, CD.. Yahiku. P.Y.. Clausen, V.E. and Cox. W., 1982. Some effects of light on coral growth. Pac. Sci.. 36: 65-8 I. Rowan, R., Whitney, S.M., Fowler, A. and Yellowlees, D.. 1996. Rubisco in marine symbiotic dinofiagellates: Form II enzyme5 in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell, 8: 539-553. Ruiz-Cristin, J. and Briskin, D.P.. 1991. Characterization of a H+/NO; symport associated with plasma membrane vesicles of Maize roots using ‘hCIO, as a radiotracer analog. Arch. Biochem. Biophys., 285: 74-82. Santi. S., Locci, G., Pinton, R.. Cesco, S. and Veranini. Z., 1995. Plasma membrane H’-ATPase in Maize roots induced for NO, uptake. Plant Physiol., 109: l277- 1283. Schachtman, D.A. and Schroeder, J.I., 1994. Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature, 370: 655-658. Schlesinger, W.H.. 1985. The formation of caliche soils of the Mojave Desert, California. Geochim. Cosmochim. Acta. 49: 57-66. Schumaker, K.S. and Sze, H.. 1985. A Ca’ ’/H+ antiport system driven by the proton electrochemical gradient of a tonoplast H+ -ATPase from oat roots. Plant Physiol.. 79: I 1 I I - I I 17. Schupp, P.J. and Paul, V.J.. 1994. Calcium carbonate and secondary metabolites in tropical seaweeds: variable effects on herbivorous fishes. Ecology. 75: 1 172-I 185. Schwarz, A-M.. Hawes. 1. And Howard-Williams. C.. 1996. The role of photosynthesis/light relationships in determining lower depth limits of Characeae in South Island. New Zealand lakes. Freshwater Biol., 35: 69-80. Sekino, K. and Shiraiwa. Y.. 1994. Accumulation and utilization of dissolved inorganic carbon by a marine unicellular coccolithophorid Emiliania huxleyi. Plant Cell Physiol., 35: 353-36 I. Sherman, D.M., Troyan. T.A. and Sherman. L.A., 1994. Localization of membrane proteins in the cyanobacterium Syrchocmcus sp. PCC7942. Plant Physiol.. 106: 25 l-262. Sikes, C.S. and Wilbur, K.M. (1982). Functions of coccolith formation. Limnol. Oceanogr., 27: 18-26. Sikes, C.S.. Roer, R.D. and Wilbur, K.M., 1980. Photosynthesis and coccolith formation: Inorganic carbon sources and net inorganic reaction of deposition. Limnol. Oceanogr., 25: 24% 261.

Simkiss. K. and Wilbur, K.M.. 1989. Biomineralization. Academic Press, New York. Slattery, M. and McClintock, J.B., 1995. Population structure and feeding deterrence in three shallow-water antarctic soft corals. Mar. Biol., 122: 461-470. Smith, F.A. and Walker. N.A.. 1980. Photosynthesis by aquatic plants: Effects of unstirred layers in relation to assimilation of CO? and HCO; and to carbon isotope discrimination. New Phytol., 86: 245-259. Smith, R.J.. 1988. Calcium-mediated regulation in the cyanobacteria? In: L.J. Rogers and J.R. Gallon (Editors), Biochemistry of the Algae and Cyanobacteria. Clarendon Press, Oxford, pp. 185-199. Smith, S.V., 1973. Carbon dioxide dynamics: a record of organic carbon production, respiration, and calcification in the Eniwetok reef flat community. Limnol. Oceanogr., 18: 106-120. Smith, S.V., 1979. Effects of elevated nitrogen and phosphorus on coral reef growth. Limnol. Oceanogr.. 24: 935-240. Song. Y. and Fambrough, D., 1994. Molecular evolution of the calcium-transporting ATPases. Sot. Gen. Physiol. Ser., 49: 27 l-284. Song. Y. and Fdmbrough. D., 1995. Calcosomes, coccolithosome\. and calcium pumps: towards a synthesis for coccolithogenesis. In: European Commission Conference on Carbon Cycle, European Union, Emilianiu huxkyi and the Oceanic Carbon Cycle. The Natural History Museum, London. Song. Y. and Fambrough, D. (manuscript). Molecular identification of a P-type intracellular calcium ATPase in a cocclithopore: implications for cellular calcification and molecular evolution. Staal. M., Elzenga. J.T.M. and Prim, H.B.A., 1989. “C fixation hy leaves and leaf cell protoplasts of the submerged aquatic angiosperm Potamogeton lucuns:carbon dioxide or bicarbonate? Plant Physiol., 90: 103S- 1040. Stark. L.M.. Almodovar, L. and Krauss, R.W., 1969. Factors affecting the rate of calcification in Halimedrr opuntiu CL.) Lamouroux and Halimedo discoidea Decaisne. J. Phycol.. 5: 305-312. Steeman Nielsen, E., 1947. Photosynthesis of aquatic plants with special reference to carbon sources. Dansk Ark, 12: l-71. Steven. A. and Larkum, T., 1993. ENCORE: the effect of nutrient enrichment on coral reefs. Search, 24: 2 16-219. Stuckless. J.S., Peterman, Z.E. and Muhs, D.R., 1991. U and Sr isotopes in groundwater and calcite, Yucca Mountain, Nevada: evidence against upwelling water. Science. 254: 55 l-554. Suain, S.. Abadia, A., GonzBlez-Reyes. J.A., Lucena, J.J. and Abadia. J.. 1996. The pH requirement for in vivo activity 01 the iron deficiency-induced “turbo” ferric chelate reductase. Plant Physiol., 110: I1 I-123. Tambutt& E., Allemand, D., Mueller, E. and Jaubert, J.. 1996. A compartmental approach to the mechanism of calcification in hermatypic corals. J. Exp. Biol., 199: in press. Thomas, E.A.. 1980. Die Sauerstoffverh’iiltnisse im Ziirichsee und ihre Beeinflussung durch biologische und metereologische Faktoren. Bern. Bot. Ges., 468: 174- 175. Tyler. G.. 1994. A new approach to understanding the calcifuge hahit of planta. Ann. Bat.. 73: 327-370.

T.A. McConnaughey, J. F. Whelan /Earth-Science Van Alstyne, K.L. and Paul, V.J., 1992. Chemical and structural defenses in the sea fan Gorgonia uentalina: effects against generalist and specialist predators. Coral Reefs, 11: 155-159. Van Alstyne, K.L., Wylie, C.R., Paul, V.J. and Meyer, K., 1992. Antipredator defenses in tropical Pacific soft corals (Coelenterata: Alcynonacea). I. Sclerites as defenses against generalist carnivorous fishes. Biol. Bull., 182: 231-240. Bleijswijk, J.D.L. van, Kempers, R.S., Veldhuis, M.J. and Westbrook, P., 1994. Cell and growth characteristics of types A and B of Emiliania huxleyi (Prymnesiophyceael as determined by flow cytometry and chemical analysis. J. Phycol., 30: 230-241. Vanderploeg, H.A. Eadie, B.J., Leibig, J.R., Tarapchak, S.J., Glover, R.M., 1987. Contributions of calcite to the particle-size spectrum of Lake Michigan seston and its interactions with the plankton. Can. J. Fish. Aquat. Sci., 44: 1898-1914. Wal, P. van der, de Bruijn, W. and Westbroek, P., 1985. Cytochemical and X-ray microanalysis studies of intracellular calcium pools in scale-bearing cells of the coccolithophorid Emiliania huxleyi. Protoplasma, 124: l-9. Wal, P. van der, Kempers, R.S. and Veldhuis, M.J.W., 1995. Production and downward flux of organic matter and calcite in a North Sea bloom of the coccolithophore Emiliania huxleyi. Mar. Ecol. Prog. Ser., 126: 247-265. Wainwright, I.M., Kwon, D.-K. and Gonzalez, E., 1992. Isolation and Characterization of golgi from Coccolithus pelagicus (Prymnesiophyceae). J. Phycol., 28: 643-348. Walker, N.A., Smith, F.A. and Cathers, I.R., 1980. Bicarbonate assimilation by fresh-water charophytes and higher plants: I. Membrane transport of bicarbonate ions is not proven. J. Membrane Biol., 57: 51-58. Westbroek, P., van Hinte, J., Brummer, B.-J., Veldhuis, M., Brownlee, C., Green, J., Harris, R. and Heimdal, B., 1994a. Emiliania huxleyi as a key to biosphere-geosphere interactions In: J. Green and B. Leadbeater (Editors), The Haptophyte? Algae. Clarendon Press, Oxford, pp. 32 l-334.

Reviews 42 (1997) 95-117

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Westbroek, P., Buddemeier, B., Coleman, M., Kok, D.J., Fautin, D. and Stal, L., 1994b. Strategies for the study of climate forcing by calcification. In: F. Doumenge (Editor), Past and Present Biomineralization Processes. Musee OcBanographique, Monaco, pp. 37-60. Whitton, B.A. and Potts, M., 1982. Marine litoral. In: N.G. Carr and B.A. Whitton (Editors), The Biology of Cyanobacteria. Blackwell, Oxford, pp. 515-542. Winter, A. and Siesser, W., 1994. Coccolithophores. Cambridge University Press, 342 pp. Yates, K.K. and Robbins, L.L., 1994. Experimental evidence for a CaCO, precipitation mechanism for marine Synechocystis. In: D. Allemand and J.-P. Cuif (Editors), Biomineralization 93. Proc. 7th Int. Biomineralization Symp. Bull. Inst. Oceanogr., Monaco, 14.

Ted McConnaughey’s interest in carbonates began innocently enough. While extracting isotopic records of El Niiio from Galapagos corals under the capable guidance of Prof. Minze Stuiver, he rediscovered that coral skeletons do not precipitate in isotopic equilibrium with ambient waters. He reasoned that the carbonates precipitate rapidly from molecular CO,, and carried this obsession into postdoctoral studies at the University of California Davis and Marine Biological Laboratory in Woods Hole. He subsequently joined the U.S. Geological Survey where, among other things, he studied carbonate precipitation in the Nevada desert with Joe Whelan. At the invitation of Prof. Wallace Broecker of Lamont-Doherty Earth Observatory, Columbia University, he now leads the marine ecophysiology team at the Biosphere 2 Center.