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Fate of calcifying tropical symbiont-bearing large benthic foraminifera: living sands in a changing ocean.

Introduction

Marine environments worldwide are experiencing an unprecedented change due to anthropogenic impacts of increased greenhouse gasses released into the atmosphere that are altering the physical and chemical properties of oceans worldwide (Orr et al., 2005; Hoegh-Guldberg et al., 2007; Doney et al., 2012; IPCC, 2013). Recent studies document increasing concerns as to the persistence of marine organisms, and in particular calcifiers, in an ocean increasing in acidity and temperature (Doney et al., 2012). Ocean uptake of atmospheric C[O.sub.2] alters seawater carbonate chemistry, leading to more acidic conditions (lower pH) and lower saturation states ([OMEGA]) for calcium carbonate minerals (Orr et al., 2005). The rate of pH change is 30 to 100 times faster than in the geological past (Zeebe and Ridgwell, 2011; Honisch et al., 2012). Surface ocean pH has decreased 0.1 pH units since preindustrial times (equivalent to a 30% increase in [H.sup.+] ions), and the most recent forecast suggests that pH will further decrease by 0.3 units by the end of this century (Representative Concentration Pathway [RCP] 8.5; IPCC, 2013). In addition, oceans are predicted to warm by 2.6-4.8[degrees]C under the same projection by the end of the century, with a likely mean increase of 3.7[degrees]C (IPCC, 2013), causing increased physiological demands on organisms, with marine calcifiers being particularly vulnerable (Kelly and Hoffman, 2013; Kroeker et al., 2013). To date, most marine species appear to respond negatively to increased temperature and acidification (Kroeker et al., 2013), with multi-stressor studies indicating significant additive effects (Byrne and Przeslawski, 2013; Harvey et al., 2013). However, some studies have shown that moderate warming can ameliorate or reduce the negative effects of increased acidification on calcifiers in the early life-history stages (Byrne, 2011; Byrne et al., 2013).

Foraminifera are protozoans abundant worldwide in marine ecosystems. This taxon emerged in the Cambrian explosion (~500Ma) and has persisted through multiple mass extinctions (Culver, 1991). The number of extant species is estimated to be greater than 10,000 (Vickerman, 1992), and composes approximately one-eighth of the Kingdom Protoctista (Hammond, 1995). Foraminifera comprises four subclasses, delineated by the composition of their tests. These include the allogromiid (test composed of organic materials), agglutinated (test composed of particles from the surrounding environment), calcareous (test composed of calcium carbonate), and siliceous (test compound of silica) (Sen Gupta, 1999). Calcareous foraminifera are further divided into hyaline (porous CaC[O.sub.3] test composed of interlocking microcrystals) and porcelaneous (non-porous CaC[O.sub.3] test composed of randomly arranged rods) forms.

From a global carbon cycle perspective, calcareous foraminifera play an important role in carbon sequestration through their calcification biology and the net flux of their tests into deep-ocean sediments and shallow-water carbonate sandy habitats (Langer et al., 1997; Langer, 2008). Although much of the global carbonate production of foraminifera is contributed by planktonic species (Langer, 2008), large benthic foraminifera (LBFs) are important in coral reefs, where they play a major role in production of carbonate sands essential for beach maintenance of low-lying sand cays (e.g., Yamano et al., 2000; Fujita et al., 2009). These organisms contribute about 5% of annual shallow-water carbonate production in coral reef environments (Langer, 2008). The carbonate sediments produced by LBFs are also crucial for buffering daily pH changes in lagoons through increased local alkalinity associated with test dissolution (Yamamoto et al., 2012). The tests of calcareous LBFs are composed of high-magnesium calcite (~70-250 mmol Mg/Ca; Raja et al., 2005), the mineral form considered to be most sensitive to ocean acidification (Morse et al., 2006; Yamamoto el al., 2012).

While living, many tropical LBFs form symbioses with a range of marine algae including dinoflagellates, diatoms, red algae (rhodophytes), green algae (chlorophytes), and cyanobacteria (Lee, 2006). Specifically, tropical LBFs that are important for carbonate production host dinoflagellates (some soritids), diatoms (calcarinids, amphistiginids, alveolinids, and nummulitids), and rhodophytes (some soritids; see table 1 in Ziegler and Uthicke, 2011). Within these groups, the symbioses formed in single LBF species exhibit a large genetic diversity of dinoflagellates (Pochon et al., 2007; Momigliano and Uthicke, 2013). On a reef scale, symbionts within the LBF holobiont contribute to primary production through photosynthesis and organic carbon production. For instance, LBFs can account for up to 10% of organic carbon production on reef crest communities (Smith and Wiebe, 1977; Fujita and Fujimura, 2008).

Recent meta-analyses have highlighted the vulnerability of marine calcifiers to ocean acidification, reflecting the relationship between carbonate saturation state of seawater and calcification (e.g., Harvey et al., 2013; Kroeker et al., 2013). Symbiont-bearing LBFs secrete high-magnesium calcite tests (Raja et al., 2005), the solubility of which can exceed that of aragonite produced by reef corals at a similar seawater pC[O.sub.2] level (Morse et al., 2006). Therefore, tropical reef foraminifers with high-magnesium calcite shells may be the "first responders" among reef calcifying organisms to the decreasing saturation state of seawater caused by ocean acidification (Fujita et al., 2011; Yamamoto et al., 2012). In addition, as thermotolerance is an important factor controlling species biogeography and persistence (Bozinovic et al., 2011; Sunday et al., 2012), the persistence of all common coral reef species, such as LBFs in a warming environment, are of great concern (Hoegh-Guldberg, 2011; Pandolfi et al 2011).

This review presents a synthesis of research on the effects of the global change stressors ocean warming and acidification on LBF calcification and holobiont physiology. In addition, carbonate production by LBFs on tropical coral reefs is summarized to provide context with respect to their contribution to calcification on tropical reefs. Other factors of anthropogenic stress (turbidity, UV light, eutrophication, heavy metals, etc.) have been shown to influence growth rate and calcification in LBFs, and are reviewed by Reymond et al. (2012). Lastly, we synthesize results of previous studies by performing a meta-analysis to better predict impacts of changing climate on the potential future persistence of this important group of organisms. These data will provide insight into the contribution of LBFs in carbonate production and how this may be affected in a changing ocean, with important applications to understanding how reef systems may respond to global change.

Materials and Methods

To assess the impact of projected ocean warming and acidification conditions, 18 publications of experimental studies on tropical symbiont-bearing LBFs were compiled for this meta-analysis (see Appendixes 1-3 for details and raw data). As in recent meta-analyses, an unweighted analysis was performed using previous methods of log-transformed response ratio (LnRR; e.g., Kroeker et al., 2013). In this analysis, data for the ambient treatments of the experiment were compared with a "treatment" group, to determine response ratios as a measure of the impact compared to the control. Negative LnRR values represent negative impacts and positive ones indicate positive responses. Thus, a LnRR of 1 is equivalent to an increase of about 170% in the variable measured. The RCP 8.5 scenario for projected ocean warming and acidification by the end of the century was used as the benchmark for the "treatment" group (IPCC, 2013). The projections for 2100 are a warming of +4[degrees]C, and a decrease of 0.3 pH units/940 ppm (IPCC, 2013). In cases where multiple response variables were measured for the same experiment, similar metrics (e.g., growth and size) were included only once.

Effects of Ocean Acidification on LBFs

Methodology of ocean acidification response studies

The impacts of ocean acidification on LBFs have been investigated in laboratory culture and field studies. For laboratory studies, seawater carbonate chemistry and pH was adjusted either by (1) addition of acid (HCl) and base (NaOH) (ter Kuile et al., 1989; Kuroyanagi et al., 2009), (2) bubbling C[O.sub.2]-enriched air through seawater (Fujita et al., 2011; Hikami et al., 2011; Sinutok et al., 2011; Uthicke and Fabricius, 2012; Vogel and Uthicke, 2012; Reymond et al., 2013), or (3) controlling atmospheric pC[O.sub.2] directly in an incubator (McIntyre-Wressnig et al., 2013). Of these approaches, bubbling C[O.sub.2]-enriched air through seawater is the best proxy for naturally occurring ocean acidification, which changes dissolved inorganic carbon at constant total alkalinity (Schulz et al., 2009). Culturing experiments using stable ocean acidification conditions have merits for testing the effects of different carbonate chemistry; however, the conditions are unrealistic in most cases, as they do not reflect the temporal (daily and seasonal) variation in environmental variables (e.g., light and temperature).

Field studies on the effects of ocean acidification on LBF communities have been undertaken at areas close to volcanic C[O.sub.2] seeps, where pC[O.sub.2] and other carbonate chemistry measures are used as proxies for future ocean conditions projected to occur during this century (Uthicke and Fabricius, 2012; Uthicke et al., 2013). Although field studies can provide insights into the responses of LBF species to acidification under natural conditions, these responses may also be influenced by other environmental variables in addition to C[O.sub.2] gradients. In particular, effects of other volcanic gases (e.g., H2S) should be checked in seep areas. As these are open systems, other factors such as the source population of propagules may also influence observed trends.

Calcification

Contrasting results have been documented for the calcification of LBFs maintained in ocean acidification conditions. Most laboratory (ter Kuile et al., 1989; Kuroyanagi et al., 2009; Sinutok et al., 2011; Reymond et al., 2013) and field (Uthicke and Fabricius, 2012) studies report decreasing calcification for porcelaneous foraminifera that have dinoflagellate symbionts (e.g., Marginopora sp.; Fig. 1A). Kuroyanagi et al (2009) reared asexually produced individuals of Marginopora (Amphisorus) kudakajimensis under lower [pH.sub.NBS] conditions (7.7, 7.9, 8.2, 8.3) over a 10-week incubation. In that study, calcification measured as the change in shell weight and diameter was generally reduced at low pH (pH 7.7/980 ppm). In contrast, Vogel and Uthicke (2012) showed increasing calcification and growth rates (measured as % daily increase of surface area) of Marginopora vertebralis in higher pC[O.sub.2] seawater (1169 and 1662 ppm/[pH.sub.Total] 7.79 and 7.66).

Hyaline foraminiferans that have diatom symbionts either do not exhibit a response (e.g., growth/calcification) to incubation in ocean acidification conditions or exhibit increased growth (Fujita et al., 2011; Hikami et al., 2011; Glas et al., 2012; Vogel and Uthicke, 2012; Mclntyre-Wressnig et al., 2013). In pC[O.sub.2] levels ranging from 300 to 1000 [micro]atm ([pH.sub.Total] 8.17-7.76), calcification of Baculogypsina sphaerulata and Calcarina gaudichaudii, measured as growth of asexually reproduced juveniles, increased with elevated pC[O.sub.2] (Fujita et al., 2011; Hikami et al., 2011). However, no effect on calcification was observed in Amphistegina spp. and Heterostegina depressa in broader and more extreme pC[O.sub.2] ranges (Glas et al., 2012; Vogel and Uthicke, 2012; McIntyre-Wressnig et al., 2013). These contrasting experimental results may be due to differences in species genotypes, pC[O.sub.2] ranges examined, culture duration, experimental conditions such as light and temperature, or different methods used to measure calcification. Thus, to gain comparable data there is a need for protocols, culturing conditions, and measurement methods to be consistent among researchers, as noted for echinoderms (Byrne, 2012).

Dissolution

In ocean acidification conditions, growth and dissolution of foraminiferal shells may occur simultaneously. Sinutok et al (2011) reported that after exposure to lower pH seawater (-0.2 pH units compared to ambient), test weights of M. vertebralis decreased compared with those before exposure, indicating partial dissolution of shells. However, it should be noted that dissolution was observed by Sinutok et al (2011) even in control conditions. A study of Amphistegina gibbosa reported dissolution of test surfaces of living individuals in seawater with pC[O.sub.2] of 2000 ppmv ([pH.sub.Total] ~7.5), seen by scanning electron microscopy (McIntyre-Wressnig et al., 2013). Shell surfaces of Amphistegina sp. also dissolved in seawater with less extreme conditions (pC[O.sub.2] 444 [micro]atm; Uthicke et al., 2013). Shell surfaces of hyaline foraminifers (e.g., calcarinids) are covered with a thin membrane of ectoplasm that provides an organic layer protecting the CaC[O.sub.3] test from changes in seawater chemistry (Erez, 2003). On the other hand, porcelaneous foraminifera lack an ectoplasm layer, exposing the calcium carbonate shells to seawater conditions. These cytological differences between hyaline and porcelaneous forms suggest that porcelaneous foraminifers are more vulnerable to dissolution in lower pC[O.sub.2] (higher pH) seawater than are hyaline foraminifers.

Photosynthesis

How photosynthetic parameters (e.g., chlorophyll a, symbiont density) will respond to future ocean acidification scenarios is an important consideration, as the health of the symbiont is directly related to the health of the LBF. There are contrasting findings on the effects of ocean acidification on photosynthesis of LBFs with algal symbionts (Fig. 1B). In general., gross photosynthesis (oxygen production) rates of M. vertebralis increased up to 90% with increasing pC[O.sub.2] (lowering pH) in volcanic C[O.sub.2] seep sites (Uthicke and Fabricius, 2012). In laboratory results, however, photosynthesis rates of M. vertebralis decreased at lower pH (Sinutok et al., 2011; Reymond et al., 2013). As a marker of symbiont health, maximum photochemical efficiency (Fv/Fm), measured by pulse amplitude modulation fluorescence, which measures the efficiency of charge separation of electrons in Photosystem II, is often used (Enriquez and Borowitzka, 2009). Previous studies have all found decreased Fv/Fm values, symbiont density, and chlorophyll contents in ocean acidification conditions (Sinutok et al., 2011; Reymond et al., 2013), suggesting inactivation of photosynthesis of the symbiont. For M. vertebralis, exposure to low pH seawater ([pH.sub.Total] 7.66) produced no significant differences in gross photosynthesis and respiration rates among different acidified seawaters (Vogel and Uthicke, 2012). Since no significant differences were observed in maximum quantum yield, chlorophyll a contents, and other photosynthetic properties, the authors concluded that acidified seawater did not affect photosynthetic activity of symbionts (Vogel and Uthicke, 2012). Microsensor studies of [O.sub.2] and pH microenvironments over shell surfaces of foraminifers (M. vertebralis, Amphistegina radiata, H. depressa, Peneroplis sp.) demonstrated that photosynthesis increased pH on shell surfaces, but this increase was insufficient to compensate for decreases in ambient seawater pH (Glas et al., 2012). Although symbiont photosynthesis changes pH on the shell surfaces, it may also activate cellular metabolism. Investigating nutrient and carbon cycling between foraminifers and symbionts using C/N ratio (Uthicke et al., 2012) and isotope tracers in acidified seawater would shed light on this issue.

Key issues unsolved: contrasting calcification responses between hyaline and porcelaneous taxa

Previous studies indicate that calcification responses of LBF species cultured in ocean acidification conditions differ between hyaline taxa with diatom symbionts and porcelaneous taxa with dinoflagellate symbionts (Fig. 1). Calcification is either enhanced or does not change for hyaline species and generally decreases for porcelaneous species (Fig. 1A). The mechanism behind this contrasting result could be due to differences in (1) the carbonate species used for calcification (ter Kuile, 1991), (2) the type of symbionts (Lee, 2006), and (3) the degree of nutritional dependence upon symbionts (Lee et al., 1991). To distinguish between these effects, comparing LBLs reared in ocean acidification conditions and in chemically manipulated seawater, in which bicarbonate ion concentration varies under a constant carbonate ion concentration, would be useful. Lor instance, Hikami et al (2011), using these techniques, concluded that carbonate ion affected growth of Amphisorus hemprichii (porcelaneous foraminifer), while the C[O.sub.2] ion had a greater influence on C. gaudichaudii (hyaline foraminifer. The contrasting responses of these two foraminiferal genera to acidification may reflect different sensitivities to these carbonate species (C[O.sub.3.sup.2-] vs. C[O.sub.2]) and the type of symbiotic algae (diatom vs. dinoflagellate). Calcification of porcelaneous taxa may decrease in acidification conditions because more C[O.sub.2] in seawater decreases the concentration of the main carbonate ion used for calcification (ter Kuile, 1991). In addition, porcelaneous Foraminifera are not nutritionally dependent upon symbiont photosynthesis (Lee et al., 1991) even if symbiont photosynthesis is enhanced by high pC[O.sub.2] seawater (Glas et al., 2012; Uthicke and Fabricius, 2012). Calcification of hyaline taxa may be enhanced by ocean acidification conditions because this taxon is nutritionally dependent on symbiont photosynthesis (Lee et al., 1991), which may be enhanced by higher C[O.sub.2] (Lujita et al., 2011; Hikami et al., 2011). Since the majority of hyaline species host diatom symbionts whereas most porcelaneous LBF species associate with dinoflagellate symbionts, the investigation of Alveolinella, a porcelaneous foraminifer with diatom symbionts, may provide important insights into the mechanism underlying different calcification responses between the two taxa. In addition, species-specific differences in Mg/Ca concentrations (affecting solubility of the CaC[O.sub.3] test) in LBF tests may also contribute to differences observed (Raja et al., 2005).

Ocean Warming

Although physiological stress due to increased temperatures often results in bleaching of LBFs (e.g., Schmidt et al., 2011), the cellular mechanism of bleaching in the context of warming oceans is not well understood. Corals, which also form symbioses with marine algae, offer an interesting parallel to LBFs. In corals, increased temperature can compromise photosynthesis by the algal symbiont (e.g., Iglesias-Prieto et al., 1992; Jones et al., 1998; Warner et al., 1999), leading to increased production of reactive oxygen species (Lesser, 1997). This in turn causes a disassociation of the symbiont and host (bleaching) and in extreme cases, host mortality (Gates, 1990; Hoegh-Guldberg, 1999). Although photoinhibition due to thermal stress is well documented for corals (reviewed in Smith et al., 2005), less is known about how other marine symbioses, such as the foraminiferan-algae association, will respond to increased temperature in the context of climatic change. Varied responses in the LBF-algal symbiosis to increased temperature are reported in several studies (e.g., Schmidt et al., 2011; van Dam et al., 2012), and may be influenced by symbiont type, as suggested above for ocean acidification studies.

Although calcification was not measured in the studies listed in Table 1, changes in LBF growth are used as a proxy for calcification. As LBF shells are composed nearly entirely of calcium carbonate and relatively little organic matter, shell growth/reduction provides a good indicator of calcification responses. To date, the impacts of increased temperature on the growth of LBFs have been investigated in both short- and long-term time frames. To properly account for experimental duration, which has been shown to influence the physiology and motility of LBFs (Schmidt et ai, 2011), studies on the impact of increased temperatures were separated into two types: short (5 hours-6 days) and long (3 weeks-6 weeks).

Short-term experimental findings (5 hours-6 days)

Physiological responses of LBFs in short-term increased temperature experiments provide insights into how these organisms will respond to ocean warming and pulses of warming in the environment (Table 1; Fig. 1C, D). From an ecological perspective, LBFs appear to be adapted to conditions experienced in situ (+2-6[degrees]C above ambient), as documented by a heat-shock experiment with B. sphaerulata (diatom-bearing) from the intertidal, resulting in a 50% reduction of the RuBisCO protein (photosynthetic rate-limiting enzyme) at +8[degrees]C above ambient (Doo et al., 2012b). For that study, the upper thermal limit reflects extreme conditions normally experienced in situ, as determined by temperature data collected at the site. Similarly, studies with other intertidal species indicate adaptive mechanisms to short-term heat stress but less resilience to longer thermal stress (Stillman, 2003). Thus, it seems likely that the physiological responses of LBFs to increased temperature depend on the habitat conditions they are adapted to. To date, only two thermotolerance experiments have been performed to assess colder water responses of LBFs. In the first experiment, two species of diatom-bearing LBFs, Amphistegina madagascariensis and A. radiata, exhibited an optimal range of -4 to +6[degrees]C with respect to ambient conditions, with a significant decrease in movement outside this thermal window (Zmiri et al., 1974). Recently, the thermotolerance ranges of three common reef species (B. sphaerulata, C. gaudichaudii, and A. kudakajimensis) on Okinawa, Japan, were determined over an experimental range of 5-45[degrees]C (Fujita et al., 2014). In that study, optimal photosynthesis and respiration was observed at about 5[degrees]C greater than mean seawater temperature for all species, reflecting acclimation to life in thermally variable environments (Fujita et al., 2014). While understanding the impacts of increased temperature on LBFs is important, research on cold-temperature tolerance is also needed to discern impacts of natural physiological changes in context with the dynamic environment in some LBF habitats (e.g., Doo et al., 2012b).

Two studies investigating the effects of increased temperature on LBFs have measured the Fv/Fm response for a wide suite of common LBFs along the Great Barrier Reef (GBR), Australia, in response to short-term warming (Schmidt et al., 2011; van Dam et al., 2012). In those studies, warming for 4-6 days caused a decrease in Fv/Fm values by symbionts in diatom-bearing Calcarina tnayori, C. hispida, Alveolinella quoyi, Amphistegina radiata, and dinoflagellate-bearing M. vertebralis (Schmidt et al., 2011; van Dam et al., 2012). Interestingly, no changes in Fv/Fm were observed in rhodophyte-bearing Peneroplis planatus and diatom-bearing H. depressa in response to elevated thermal stress (Schmidt et al., 2011; van Dam et al., 2012). While the majority of LBF species investigated in short-term increased temperature conditions exhibited decreases in physiological health (as measured by Fv/Fm), several species (e.g., P. planatus and H. depressa), appeared more tolerant to thermal stress (Schmidt et al., 2011; van Dam et al., 2012). Thus, it appears that some LBF species are more resilient to heat stress than others.

Longer-term experimental findings (3-6 weeks)

Long-term studies on the effects of increased temperature on LBFs have been performed on only five species (see below), and in all cases, negative effects are reported (Fig. 1C, D). Decreased growth and, in extreme cases, dissolution was observed in M. vertebralis incubated at 32[degrees]C (+6[degrees]C above ambient) for 3 weeks (Doo et al., 2012a). Decreased oxygen production was observed with elevated temperatures (+4[degrees]C above ambient) for M. vertebralis after longer-term exposure (Uthicke and Fabricius, 2012). Amphistegina gibbosa cultured in elevated temperatures (+12[degrees]C above ambient) for 5 weeks bleached, although these effects were also attributed to UV effects (Talge and Hallock, 2003). Amphistegina radiata also exhibited decreased growth at +5[degrees]C above ambient (Schmidt et al., 2011).

Our meta-analysis indicates that long-term exposure to increased temperature has deleterious effects on the health of photosymbionts in LBFs (Fig. 1C, D). Amphistegina radiata, C. mayori, and H. depressa incubated at elevated temperatures (5[degrees]C above ambient) for 4 weeks all experienced significant decreases in Fv/Fm values (Schmidt et al., 2011). This presents an interesting contrast to the results of short-term (up to 6 days) experiments, in which H. depressa was tolerant to heat stress but was not able to withstand long-term stress (Schmidt et al., 2011). Schmidt et al. (2011) documented that the duration of heat stress is also important to the physiological health of LBFs. All LBFs incubated in long-term warming experiments exhibited reduced calcification and photosymbiont health (Fig. 1C, D).

Field observations of warming impacts

While experimental incubation in aquaria is crucial to our understanding of LBF responses to future warming, there remains a concern about whether these organisms respond differently in nature. In this context, laboratory-based experiments paired with field sampling of population dynamics would aid in our understanding of natural population oscillations. Natural seasonal oscillations in LBF population density are well documented (see the following section on Carbonate Contribution of LBFs). Seasonal effects on calcification rate indicated that calcification in M. vertebralis is significantly higher in winter (Reymond et al., 2011), while bleaching in A. gibbosa does not change with increased summer temperatures (Hallock et al., 1995). Atnphistegina radiata exposed for >5 weeks in several experiments in winter and summer on the GBR showed reduced growth during warmer summer temperatures (Uthicke and Altenrath, 2010). However, re-analysis of these data indicated that this may not be just a temperature effect, but one likely to be influenced by increased nutrients associated with runoff of land-based nutrients in the summer (S. Uthicke, unpub. data). In the same study, H. depressa also grew more slowly in summer in response to a small increase in ambient temperatures (as above, re-analysis of data).

A significant shortcoming of field observations is the difficulty in discerning which physical variable or variables causes the response observed. As seen in a study on Sorites dominicensis, bleaching was observed at temperatures 3[degrees]C above ambient; however, there were also possible influences of freshwater input and desiccation at the field site (Richardson, 2009). In addition, information gleaned from summer/winter comparisons are accompanied by changes in additional factors (e.g., differences in day length) that vary alongside temperature.

Insights of Multiple-Stressor Experiments on LBF Physiology

While the oceans are simultaneously warming and acidifying, there remains a large gap in experimental data on how LBFs may respond to simultaneous exposure to multiple stressors. To date, only two studies have investigated the effect of future ocean acidification and thermal stress on tropical LBFs (Sinutok et al., 2011; Schmidt et al., 2014). In these studies, the simultaneous exposure of warming and acidification caused decreased growth, reduced Fv/Fm values, decreased chlorophyll, and decreased calcite crystal size in M. vertebralis (Sinutok et al., 2011; Schmidt et al., 2014). However, in Sinutok et al. (2011), the Fv/Fm and chlorophyll values were low even under control conditions, indicating that the LBFs may have had compromised health. Schmidt et al. (2014) also observed a greater deleterious effect of temperature (3[degrees]C above ambient) than of acidification (decrease of 0.2 pH units) for survivorship, growth, and photosynthesis in two common LBF species (M. vertebralis and H. depressa).

Interactions between multiple anthropogenic stressors can provide interesting insights into how LBFs will respond in a multi-stressor ocean, highlighting the possibility of mitigation of some negative climate change effects. A study by Reymond et al. (2013) documents a diminishing of the negative effects of ocean acidification with moderate increases in nutrient in the foraminiferan Marginopora rossi. This is the first study to document a non-additive effect of multiple climate change stressors in LBFs, and further work is needed across different species and stressors. A crucial area for research is understanding the interactive effects of ocean warming and acidification on LBFs, as these two ocean change stressors are among the greatest of worldwide concern (Schmidt et al., 2014).

Carbonate Contribution of LBFs to Coral Reef Sediments and Potential Alteration of Reef Carbonate Budgets due to Climate Change

Although single-species experimental studies are important to our understanding of how LBFs may be impacted by changing climate, there remains a lack of understanding of how these organisms contribute to reef carbonate budgets. This is a major gap in knowledge needed to predict how the role of LBFs in coral reef ecosystems may change in the future. While carbonate sediment production on tropical coral reefs is largely attributed to fragmented coral skeletons, LBFs are primary sources of calcareous sediment production in many reef systems (Vila-Concejo et al., 2013). Several qualitative studies document the large contribution of benthic foraminiferan tests in carbonate sands of the central GBR (Scoffin and Tudhope, 1985). Recent work on the carbonate budget on coral reefs has indicated that LBFs are likely the missing component in most reef-scale estimates of calcification (Hamylton et al., 2013). The importance of LBFs is especially noted in low-lying islands in the south Pacific such as Tuvalu, which are completely reliant on these organisms for replenishment of beach sands (Collen, 1996).

At the global scale, LBFs contribute approximately 4.8% to reef-scale carbonate budgets (Langer et al., 1997; Langer, 2008). The majority of calcification occurs on reef flats, with certain studies documenting that production of LBF calcium carbonate (CaC[O.sub.3]) in the Majuro Atoll is up to 10,000 g [m.sup.-2] [y.sup.-1] (Fujita et al., 2009), with a world-wide average of 230 g [m.sup.-2] [y.sup.-1] (Langer et al., 1997). At Green Island, GBR, up to 30% of CaC[O.sub.3] formed is composed of LBF tests (Yamano et al., 2000; Table 2). Other emergent reef platforms have smaller contributions of LBFs ranging from 2% to 8% in studies of reef systems across the Indo-Pacific (Venec-Peyre, 1991; Harney and Fletcher, 2003; Hart and Kench, 2007). Reefs in Palau have been documented to produce an excess of 3000 g [m.sup.-2] [y.sup.-1] CaC[O.sub.3] (Hallock, 1981), while at a high-latitude reef at Sesoko Island, Japan, production is 560 g [m.sup.-2] [y.sup.-1] (Hohenegger, 2006). Foraminifera that live as epiphytes on algal-dominated reef platforms along the GBR produce a large amount of CaC[O.sub.3], with LBF production at One Tree Reef estimated to be 3000 g [m.sup.-2] [y.sup.-1] (Doo et al., 2012a), and at Raine Island Reef to be 1800 g [m.sup.-2] [y.sup.-1] (Dawson et al., in press). Estimates of carbonate production by LBFs that reside on lagoonal sediments are lower than those on fore-reefs, with the worldwide average being 30.4 g [m.sup.-2] [y.sup.-1] (Langer et al., 1997). Only three studies have assessed yearly production of LBFs in lagoons, and these estimates range from 70 to 1020 g [m.sup.-2] [y.sup.-1] (Hallock, 1981; Fujita et al., 2009; Hohenegger, 2006).

It is clear that changing climate has the potential to significantly impact the calcification biology of LBFs. In this context, a better understanding of the contribution of LBFS to a reef-scale carbonate budget and how this may change with future climate change scenarios is needed (Resig, 2004). From a population standpoint, localized extinction and range extensions are predicted in this "do or die" global change scenario (Poloczanska et al., 2013). Although range expansion and migration to more suitable temperatures as a mechanism for LBF species persistence has been modeled for Amphestigina sp. (Langer et al., 2013), habitat suitability is likely to be a limiting factor, as identified for tropical echinoderms (Hardy et al., 2014; Lamare et al., 2014).

Conclusions

In the multi-stressor marine environment in which LBFs reside, other factors not reviewed here such as UV, salinity, and pollution will also affect the persistence of this important taxon (Reymond et al., 2012). A recent meta-analysis documents a varied, but largely negative effect of changing oceans on marine calcifiers (Kroeker et al., 2013). Although our review reveals a general negative trend on LBF health in response to ocean warming and acidification, the small number of empirical studies published to date emphasizes the need for further work on LBFs and, in particular, multi-stressor studies. Furthermore, certain groups of LBFs appear more resilient than others. While controlled laboratory studies are essential for our understanding of physiological responses to climate change, our ability to predict marine organisms' responses lies within understanding the adaptive capacity in LBFs. This includes understanding the effects of phenotypic plasticity to tolerate stress and genetic capability to evolve in a changing ocean (Munday et al., 2013).

Many issues remain that impede our full understanding of how LBFs will respond to changing climatic conditions, in particular, the following:

1. The potential interactive effects of multiple climate change stressors (in particular warming and acidification) of LBFs.

2. Whether differences in the calcification response of a species to warming and acidification are due to differences in calcification mechanisms between porcelaneous and hyaline taxa or are related to symbiont types.

3. Incorporation of the relationship between habitat and thermal history of LBFs into resilience measurements.

4. The contribution of LBFs to reef-scale carbonate production.

5. What additional parameters can he used to monitor both host and symbiont compartments. Multiple techniques are available to assess photosymbiont health (e.g., Fv/Fm and chl-a), but few exist for the host alone.

6. Use of surveys of molecular variation (e.g., varied gene expression in response to stress), to aid in mechanism-focused questions.

Abbreviations: GBR, Great Barrier Reef; LBF, large benthic foraminifera; LnRR, log-transformed response ratio; RCP, Representative Concentration Pathway.

Appendix 1

Studies that were included in the meta-analysis. A. Ocean
acidification effects on calcification. B. Ocean acidification
effects on photobiology. C. Ocean warming effects on calcification.
D. Ocean warming effects on photobiology. All studies were compiled
using IPCC 2013 Representative concentration Pathway 8.5 scenarios
of estimates of ocean warming (+4[degrees]C), and acidification
(-0.3 pH unit or 960 ppm).

  Shell Wall                                                   Control
    Type *           Foraminifera        Measurements Made      Mean

A. OCEAN ACIDIFICATION EFFECTS ON CALCIFICATION

Hyaline          Amphistegina gibbosa   Growth rate (%          0.350
                                        surface area)

                 Amphistegina radiata   Growth rate (%          0.175
                                        surface area
                                        [d.sup.-1])

                 Baculogypsina          Final shell weight     16.260
                 sphaerulatci           (alpha population)

                 Baculogypsina          Final shell weight     14.580
                 sphaerulatci           (beta population)

                 Baculogypsina          Final diameter         298.000
                 sphaerulata            (alpha population)

                 Baculogypsina          Final diameter (beta   283.500
                 sphaerulata            population)

                 Calcarina              Final shell weight     40.855
                 gaudichaudii           (alpha population)

                 Calcarina              Final shell weight     39.660
                 gaudichaudii           (beta population)

                 Calcarina              Final diameter         358.250
                 gaudichaudii           (alpha population)

                 Calcarina              Final diameter (beta   368.000
                 gaudichaudii           population)

                 Calcarina              Final shell weight     20.954
                 gaudichaudii

                 Heterostegina          Growth rate (%          0.186
                 depressa               surface area
                                        [d.sup.-1])

                 Heterostegina          Growth rate (%          0.394
                 depressa               surface area
                                        [d.sup.-1])

Porcelaneous     Amphisorus             Final shell weight     40.460
                 hemprichii             (alpha population)

                 Amphisorus             Final shell weight     65.150
                 hemprichii             (beta population)

                 Amphisorus             Final diameter         626.750
                 hemprichii             (alpha population)

                 Amphisorus             Final diameter         759.750
                 hemprichii             (beta population)

                 Amphisorus             Final shell             0.580
                 kudakajmensis          diameter

                 Amphisorus             Final shell weight     27.600
                 kudakajmensis

                 Amphisorus             Final shell weight     41.276
                 kudakajmensis

                 Marginopora            Growth rate (%          0.052
                 vertebralis            surface area
                                        [d.sup.-1])

                 Marginopora            Alkalinity anomaly      0.438
                 vertebralis            (% dry wt.
                                        [d.sup.-1]) in Fig.
                                        3a

                 Marginopora            Alkalinity anomaly      0.472
                 vertebralis            (% dry wt.
                                        [d.sup.-1]) in Fig.
                                        3b

                 Marginopora            Growth rate (%          0.075
                 vertebralis            surface area
                                        [d.sup.-1])

                 Marginopora rossi      Growth rate (%          0.740
                                        surface area
                                        [d.sup.-1])

B. OCEAN ACIDIFICATION EFFECTS ON PHOTOBIOLOGY

Hyaline          Amphistegina radiata   chl-a                  142.625

                 Amphistegina radiata   Fv/Fm                   0.671

                 Heterostegina          chl-a                  215.525
                 depressa

                 Heterostegina          Fv/Fm                   0.702
                 depressa

                 Heterostegina          Oxygen production       0.079
                 depressa

                 Heterostegina          chl-a                   0.161
                 depressa

                 Heterostegina          Oxygen production       0.021
                 depressa

Porcelaneous     Marginopora            chl-a                  198.244
                 vertebralis

                 Marginopora            Fv/Fm                   0.637
                 vertebralis

                 Marginopora            Oxygen production       0.071
                 vertebralis

                 Marginopora            Oxygen production in   -0.566
                 vertebralis            Fig 1C

                 Marginopora            Oxygen production in    0.259
                 vertebralis            Fig 1D

                 Marginopora            Oxygen production in    0.644
                 vertebralis            Fig 1F

                 Marginopora            chl-a                   0.165
                 vertebralis

                 Marginopora            Oxygen production       0.012
                 vertebralis

                 Marginopora rossi      Oxygen production       3.640

C. OCEAN WARMING EFFECTS ON CALCIFICATION

Hyaline          Amphistegina radiata   Growth rate (%          0.072
                                        surface area)

                 Heterostegina          Growth rate (%          0.394
                 depressa               surface area)

Porcelaneous     Marginopora            Growth rate (%          1.601
                 vertebralis            surface area)

                 Marginopora            Growth rate (%          2.540
                 vertebralis            surface area)

                 Marginopora            Growth rate (%          0.010
                 vertebralis            surface area)

                 Marginopora            Growth rate (%          0.075
                 vertebralis            surface area)

D. OCEAN WARMING EFFECTS ON PHOTOBIOLOGY

Hyaline          Amphistegina gibbosa   % Healthy (1-           0.880
                                        bleached)

                 Amphistegina radiata   Fv/Fm                   0.742

                 Amphistegina radiata   Fv/Fm                   0.735

                 Amphistegina radiata   Fv/Fm                   0.699

                 Amphistegina radiata   chl-a                  126.000

                 Amphistegina radiata   chl-a                  146.302

                 Amphistegina radiata   chl-a                  106.068

                 Amphistegina radiata   Fv/Fm                   0.658

                 Amphistegina radiata   chl-a                  126.984

                 Baculogypsina          RuBisCO expression      1.480
                 sphaerulata

                 Baculogypsina          Oxygen production       1.820
                 sphaerulata

                 Calcarina              Oxygen production       1.590
                 gaudichaudii

                 Calcarina hispida      Fv/Fm                   0.801

                 Calcarina hispida      chl-a                  137.058

                 Calcarina mayori       Fv/Fm                   0.708

                 Calcarina mayori       chl-a                  174.850

                 Calcarina mayori       Fv/Fm in Figure 3B      0.697

                 Heterostegina          Fv/Fm                   0.717
                 depressa

                 Heterostegina          Fv/Fm                   0.749
                 depressa

                 Heterostegina          Fv/Fm                   0.731
                 depressa

                 Heterostegina          chl-a                  113.000
                 depressa

                 Heterostegina          chl-a                  101.880
                 depressa

                 Heterostegina          chl-a                  95.512
                 depressa

                 Heterostegina          Fv/Fm                   0.696
                 depressa

                 Heterostegina          chl-a                  109.724
                 depressa

                 Heterostegina          Fv/Fm in Figure 3A      0.732
                 depressa

                 Heterostegina          chl-a                  159.093
                 depressa

                 Heterostegina          chl-a                   0.161
                 depressa

                 Heterostegina          Oxygen production       0.021
                 depressa

Porcelaneous     Alveolinella quoyi     Fv/Fm in Figure 3C      0.761

                 Marginopora            Oxygen production       2.710
                 kudakajimensis

                 Marginopora            Fv/Fm in Figure 3D      0.688
                 vertebralis

                 Marginopora            Fv/Fm in Figure 3E      0.732
                 vertebralis

                 Marginopora            chl-a                  214.637
                 vertebralis

                 Marginopora            chl-a                   0.165
                 vertebralis

                 Marginopora            Oxygen production       0.518
                 vertebralis

                 Marginopora            chl-a                   0.165
                 vertebralis

                 Marginopora            Oxygen production       0.012
                 vertebralis

                 Peneroplis planatus    Fv/Fm in Figure 3F      0.588

  Shell Wall                            Treatment   Effect
    Type *           Foraminifera         Mean       Size

A. OCEAN ACIDIFICATION EFFECTS ON CALCIFICATION

Hyaline          Amphistegina gibbosa      0.390    0.108

                 Amphistegina radiata      0.216    0.211

                 Baculogypsina            15.270    -0.063
                 sphaerulatci

                 Baculogypsina            14.310    -0.019
                 sphaerulatci

                 Baculogypsina           297.000    -0.003
                 sphaerulata

                 Baculogypsina           285.000    0.005
                 sphaerulata

                 Calcarina                32.190    -0.238
                 gaudichaudii

                 Calcarina                37.380    -0.059
                 gaudichaudii

                 Calcarina               355.000    -0.009
                 gaudichaudii

                 Calcarina               372.250    0.011
                 gaudichaudii

                 Calcarina                26.295    0.227
                 gaudichaudii

                 Heterostegina             0.168    -0.102
                 depressa

                 Heterostegina             0.331    -0.173
                 depressa

Porcelaneous     Amphisorus               36.360    -0.107
                 hemprichii

                 Amphisorus               57.630    -0.123
                 hemprichii

                 Amphisorus              631.750    0.008
                 hemprichii

                 Amphisorus              704.250    -0.076
                 hemprichii

                 Amphisorus                0.510    -0.129
                 kudakajmensis

                 Amphisorus               14.000    -0.679
                 kudakajmensis

                 Amphisorus               35.415    -0.153
                 kudakajmensis

                 Marginopora               0.047    -0.109
                 vertebralis

                 Marginopora               0.269    -0.489
                 vertebralis

                 Marginopora               0.395    -0.178
                 vertebralis

                 Marginopora              0.1 II    0.398
                 vertebralis

                 Marginopora rossi         0.320    -0.838

B. OCEAN ACIDIFICATION EFFECTS ON PHOTOBIOLOGY

Hyaline          Amphistegina radiata    160.085    0.115

                 Amphistegina radiata      0.625    -0.071

                 Heterostegina           220.511    0.023
                 depressa

                 Heterostegina             0.669    -0.048
                 depressa

                 Heterostegina             0.066    -0.184
                 depressa

                 Heterostegina             0.156    -0.031
                 depressa

                 Heterostegina             0.006    -1.223
                 depressa

Porcelaneous     Marginopora             228.769    0.143
                 vertebralis

                 Marginopora               0.635    -0.003
                 vertebralis

                 Marginopora               0.090    0.239
                 vertebralis

                 Marginopora               0.288
                 vertebralis

                 Marginopora               0.554    0.761
                 vertebralis

                 Marginopora               1.099    0.535
                 vertebralis

                 Marginopora               0.153    -0.077
                 vertebralis

                 Marginopora               0.013    0.107
                 vertebralis

                 Marginopora rossi         1.780    -0.715

C. OCEAN WARMING EFFECTS ON CALCIFICATION

Hyaline          Amphistegina radiata      0.042    -0.538

                 Heterostegina             0.303    -0.262
                 depressa

Porcelaneous     Marginopora               0.765    -0.739
                 vertebralis

                 Marginopora               2.290    -0.104
                 vertebralis

                 Marginopora               0.008    -0.243
                 vertebralis

                 Marginopora               0.080    0.076
                 vertebralis

D. OCEAN WARMING EFFECTS ON PHOTOBIOLOGY

Hyaline          Amphistegina gibbosa      0.780    -0.121

                 Amphistegina radiata      0.741    0.000

                 Amphistegina radiata      0.727    -0.010

                 Amphistegina radiata      0.707    0.011

                 Amphistegina radiata    143.937    0.133

                 Amphistegina radiata    163.281    0.110

                 Amphistegina radiata     94.682    -0.114

                 Amphistegina radiata      0.646    -0.019

                 Amphistegina radiata     82.374    -0.433

                 Baculogypsina             1.430    -0.034
                 sphaerulata

                 Baculogypsina             2.570    0.345
                 sphaerulata

                 Calcarina                 2.210    0.329
                 gaudichaudii

                 Calcarina hispida         0.792    -0.012

                 Calcarina hispida       159.176    0.150

                 Calcarina mayori          0.707    -0.001

                 Calcarina mayori        146.534    -0.177

                 Calcarina mayori          0.704    0.010

                 Heterostegina             0.709    -0.011
                 depressa

                 Heterostegina             0.754    0.006
                 depressa

                 Heterostegina             0.731    0.001
                 depressa

                 Heterostegina           105.200    -0.072
                 depressa

                 Heterostegina           104.957    0.030
                 depressa

                 Heterostegina            91.691    -0.041
                 depressa

                 Heterostegina             0.633    -0.094
                 depressa

                 Heterostegina            33.905    -1.174
                 depressa

                 Heterostegina             0.722    -0.014
                 depressa

                 Heterostegina           123.268    -0.255
                 depressa

                 Heterostegina             0.076    -0.758
                 depressa

                 Heterostegina             0.004    -1.618
                 depressa

Porcelaneous     Alveolinella quoyi        0.753    -0.011

                 Marginopora               3.190    0.163
                 kudakajimensis

                 Marginopora               0.681    -0.010
                 vertebralis

                 Marginopora               0.698    -0.048
                 vertebralis

                 Marginopora             135.322    -0.461
                 vertebralis

                 Marginopora               0.142    -0.152
                 vertebralis

                 Marginopora               0.514    -0.008
                 vertebralis

                 Marginopora               0.042    -1.365
                 vertebralis

                 Marginopora               0.007    -0.557
                 vertebralis

                 Peneroplis planatus       0.566    -0.038

  Shell Wall                             Treatment
    Type *           Foraminifera          Group          Reference

A. OCEAN ACIDIFICATION EFFECTS ON CALCIFICATION

Hyaline          Amphistegina gibbosa   1000 ppm       McIntyre-
                                                       Wressnig et al.
                                                       (2013)

                 Amphistegina radiata   1169 ppm       Vogel and
                                                       Uthicke (2012)

                 Baculogypsina          970 ppm        Fujita et al.
                 sphaerulatci                          (2011)

                 Baculogypsina          970 ppm        Fujita et al.
                 sphaerulatci                          (2011)

                 Baculogypsina          970 ppm        Fujita et al.
                 sphaerulata                           (2011)

                 Baculogypsina          970 ppm        Fujita et al.
                 sphaerulata                           (2011)

                 Calcarina              970 ppm        Fujita et al.
                 gaudichaudii                          (2011)

                 Calcarina              970 ppm        Fujita et al.
                 gaudichaudii                          (2011)

                 Calcarina              970 ppm        Fujita et al.
                 gaudichaudii                          (2011)

                 Calcarina              970 ppm        Fujita et al.
                 gaudichaudii                          (2011)

                 Calcarina              907 ppm        Hikami et al.
                 gaudichaudii                          (2011)

                 Heterostegina          1169 ppm       Vogel and
                 depressa                              Uthicke (2012)

                 Heterostegina          pH 7.9         Schmidt et al.
                 depressa                              (in press)

Porcelaneous     Amphisorus             970 ppm        Fujita et al.
                 hemprichii                            (2011)

                 Amphisorus             970 ppm        Fujita et al.
                 hemprichii                            (2011)

                 Amphisorus             970 ppm        Fujita et al.
                 hemprichii                            (2011)

                 Amphisorus             970 ppm        Fujita et al.
                 hemprichii                            (2011)

                 Amphisorus             pH 7.7         Kuroyanagi et
                 kudakajmensis                         al. (2009)

                 Amphisorus             pH 7.7         Kuroyanagi et
                 kudakajmensis                         al. (2009)

                 Amphisorus             907 ppm        Hikami et al.
                 kudakajmensis                         (2011)

                 Marginopora            1169 ppm       Vogel and
                 vertebralis                           Uthicke (2012)

                 Marginopora            pH 7.57        Uthicke and
                 vertebralis                           Fabricius
                                                       (2012)

                 Marginopora            pH 7.65        Uthicke and
                 vertebralis                           Fabricius
                                                       (2012)

                 Marginopora            pH 7.9         Schmidt et al.
                 vertebralis                           (in press)

                 Marginopora rossi      pH 7.6-7.7     Reymond et al.
                                                       (2013)

B. OCEAN ACIDIFICATION EFFECTS ON PHOTOBIOLOGY

Hyaline          Amphistegina radiata   1169 ppm       Vogel and
                                                       Uthicke (2012)

                 Amphistegina radiata   1169 ppm       Vogel and
                                                       Uthicke (2012)

                 Heterostegina          1169 ppm       Vogel and
                 depressa                              Uthicke (2012)

                 Heterostegina          1169 ppm       Vogel and
                 depressa                              Uthicke (2012)

                 Heterostegina          1307 ppm       Vogel and
                 depressa                              Uthicke (2012)

                 Heterostegina          pH 7.9         Schmidt et al.
                 depressa                              (in press)

                 Heterostegina          pH 7.9         Schmidt et al.
                 depressa                              (in press)

Porcelaneous     Marginopora            1169 ppm       Vogel and
                 vertebralis                           Uthicke (2012)

                 Marginopora            1169 ppm       Vogel and
                 vertebralis                           Uthicke (2012)

                 Marginopora            1307 ppm       Vogel and
                 vertebralis                           Uthicke (2012)

                 Marginopora            pH 7.55        Uthicke and
                 vertebralis                           Fabricius
                                                       (2012)

                 Marginopora            pH 7.74        Uthicke and
                 vertebralis                           Fabricius
                                                       (2012)

                 Marginopora            pH 7.75        Uthicke and
                 vertebralis                           Fabricius
                                                       (2012)

                 Marginopora            pH 7.9         Schmidt et al.
                 vertebralis                           (in press)

                 Marginopora            pH 7.9         Schmidt et al.
                 vertebralis                           (in press)

                 Marginopora rossi      pH 7.6-7.7     Reymond et al.
                                                       (2013)

C. OCEAN WARMING EFFECTS ON CALCIFICATION

Hyaline          Amphistegina radiata   +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Heterostegina          +3[degrees]C   Schmidt et al.
                 depressa                              (in press)

Porcelaneous     Marginopora            +4[degrees]C   Doo et al.
                 vertebralis                           (2012a)

                 Marginopora            +6[degrees]C   Reymond et al.
                 vertebralis                           (2011)

                 Marginopora            +3[degrees]C   Uthicke et al.
                 vertebralis                           (2012)

                 Marginopora            +3[degrees]C   Schmidt et al.
                 vertebralis                           (in press)

D. OCEAN WARMING EFFECTS ON PHOTOBIOLOGY

Hyaline          Amphistegina gibbosa   +5[degrees]C   Talge and
                                                       Hallock (2003)

                 Amphistegina radiata   +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Amphistegina radiata   +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Amphistegina radiata   +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Amphistegina radiata   +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Amphistegina radiata   +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Amphistegina radiata   +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Amphistegina radiata   +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Amphistegina radiata   +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Baculogypsina          +4[degrees]C   Doo et al.
                 sphaerulata                           (2012)

                 Baculogypsina          +5[degrees]C   Fujita et al.
                 sphaerulata                           (2014)

                 Calcarina              +5[degrees]C   Fujita et al.
                 gaudichaudii                          (2014)

                 Calcarina hispida      +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Calcarina hispida      +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Calcarina mayori       +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Calcarina mayori       +5[degrees]C   Schmidt et al.
                                                       (2011)

                 Calcarina mayori       +4[degrees]C   van Dam et al.
                                                       (2012)

                 Heterostegina          +5[degrees]C   Schmidt et al.
                 depressa                              (2011)

                 Heterostegina          +5[degrees]C   Schmidt et al.
                 depressa                              (2011)

                 Heterostegina          +5[degrees]C   Schmidt et al.
                 depressa                              (2011)

                 Heterostegina          +5[degrees]C   Schmidt et al.
                 depressa                              (2011)

                 Heterostegina          +5[degrees]C   Schmidt et al.
                 depressa                              (2011)

                 Heterostegina          +5[degrees]C   Schmidt et al.
                 depressa                              (2011)

                 Heterostegina          +5[degrees]C   Schmidt et al.
                 depressa                              (2011)

                 Heterostegina          +5[degrees]C   Schmidt et al.
                 depressa                              (2011)

                 Heterostegina          +4[degrees]C   van Dam et al.
                 depressa                              (2012)

                 Heterostegina          +4[degrees]C   van Dam et al.
                 depressa                              (2012)

                 Heterostegina          +3[degrees]C   Schmidt et al.
                 depressa                              (in press)

                 Heterostegina          +3[degrees]C   Schmidt et al.
                 depressa                              (in press)

Porcelaneous     Alveolinella quoyi     +4[degrees]C   van Dam et al.
                                                       (2012)

                 Marginopora            +5[degrees]C   Fujita et al.
                 kudakajimensis                        (2014)

                 Marginopora            +4[degrees]C   van Dam et al.
                 vertebralis                           (2012)

                 Marginopora            +4[degrees]C   van Dam et al.
                 vertebralis                           (2012)

                 Marginopora            +4[degrees]C   van Dam et al.
                 vertebralis                           (2012)

                 Marginopora            +3[degrees]C   Uthicke et al.
                 vertebralis                           (2012)

                 Marginopora            +3[degrees]C   Uthicke et al.
                 vertebralis                           (2012)

                 Marginopora            +3[degrees]C   Schmidt et al.
                 vertebralis                           (in press)

                 Marginopora            +3[degrees]C   Schmidt et al.
                 vertebralis                           (in press)

                 Peneroplis planatus    +4[degrees]C   van Dam et al.
                                                       (2012)

* The symbionts of all hyaline species listed here are pennate
diatoms; those of all porcelaneous species are dinoflagellates, with
the exception of Alveolinella quoyi.

Appendix 2

All studies to date on ocean acidification effects on tropical
symbiont-bearing large benthic foraminifera physiology. Experiment
conditions are presented in the table A, and calcification and
photosynthesis parameters and findings for the corresponding studies
are found in the table B.

A. EXPERIMENT CONDITIONS

                                    Experimental
  Shell Wall                           Design
    Type *         Foraminifera      ([dagger])          Duration

Hyaline           Amphistegina     Laboratory/       2 days
                  lobifera         closed system/
                                   bottle

                  Amphistegina     Laboratory/       6 weeks
                  gibbosa          closed system/
                                   incubator

                  Amphistegina     Laboratory/       6 weeks
                  radiata          flow-through
                                   system

                                   Laboratory        4 days
                                   /semi-closed
                                   circulation
                                   system

                  Baculogypsina    Laboratory/       12 weeks
                  sphaerulata      flow-through
                                   system/AICAL

                  Calcarina        Laboratory/       12 weeks
                  gaudichaudii     flow-through
                                   system/AICAL

                                   Laboratory/       4 weeks
                                   flow- through
                                   system/AICAL

                  Heterostegina    Laboratory/       6 weeks
                  depressa         flow-through
                                   system

                                   Laboratory/       4 days
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       35 days
                                   flow-through
                                   system

Porcelaneous      Amphisorus       Laboratory/       2 days
                  hemprichii       closed system/
                                   bottle

                                   Laboratory/       12 weeks
                                   flow-through
                                   system/AICAL

                  Amphisorus       Laboratory/       10 weeks
                  kudakajmensis    closed system/
                                   botde

                                   Laboratory/       4 weeks
                                   flow-through
                                   system/AICAL

                  Marginopora      Laboratory/       5 weeks
                  vertebralis      recirculated
                                   system/
                                   two-factors
                                   (temp)

                                   Laboratory/       6 weeks
                                   flow-through
                                   system

                                   Field & on        1 day
                                   board/at
                                   C[O.sub.2]
                                   vent, Papua New
                                   Guinea

                                   Laboratory/       1 day
                                   closed system/
                                   vials

                                   Laboratory/       4 days
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       53 days
                                   flow-through
                                   system

                  Marginopora      Laboratory/       35 days
                  rossi            closed system/
                                   two-factors
                                   (nutrient)

                  Peneroplis sp.   Laboratory/       4 days
                                   semi-closed
                                   circulation
                                   system

                                                          Light
                                                        Condition
                                                       ([micro]mol
                                    Experimental        [m.sup.-2]
  Shell Wall                           Design          [s.sup.-1];
    Type *         Foraminifera      ([dagger])         L:D cycle)

Hyaline           Amphistegina     Laboratory/       750; 13:11h
                  lobifera         closed system/
                                   bottle

                  Amphistegina     Laboratory/       11; 12:12h
                  gibbosa          closed system/
                                   incubator

                  Amphistegina     Laboratory/       8-12: ND
                  radiata          flow-through
                                   system

                                   Laboratory        30: ND
                                   /semi-closed
                                   circulation
                                   system

                  Baculogypsina    Laboratory/       60; 12:12h
                  sphaerulata      flow-through
                                   system/AICAL

                  Calcarina        Laboratory/       60; 12:12h
                  gaudichaudii     flow-through
                                   system/AICAL

                                   Laboratory/       100; 12:12h
                                   flow- through
                                   system/AICAL

                  Heterostegina    Laboratory/       8-12: ND
                  depressa         flow-through
                                   system

                                   Laboratory/       30: ND
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       10-17; 12:12h
                                   flow-through
                                   system

Porcelaneous      Amphisorus       Laboratory/       750; 13:11h
                  hemprichii       closed system/
                                   bottle

                                   Laboratory/       60; 12:12h
                                   flow-through
                                   system/AICAL

                  Amphisorus       Laboratory/       190; 12:12h
                  kudakajmensis    closed system/
                                   botde

                                   Laboratory/       100; 12:12h
                                   flow-through
                                   system/AICAL

                  Marginopora      Laboratory/       300; 12:12h
                  vertebralis      recirculated
                                   system/
                                   two-factors
                                   (temp)

                                   Laboratory/       29-34: ND
                                   flow-through
                                   system

                                   Field & on        2-12: ND
                                   board/at
                                   C[O.sub.2]
                                   vent, Papua New
                                   Guinea

                                   Laboratory/       2-12: ND
                                   closed system/
                                   vials

                                   Laboratory/       30: ND
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       38-45; 12:12h
                                   flow-through
                                   system

                  Marginopora      Laboratory/       45-50; 12:12h
                  rossi            closed system/
                                   two-factors
                                   (nutrient)

                  Peneroplis sp.   Laboratory/       30: ND
                                   semi-closed
                                   circulation
                                   system

                                                       Temperature
                                    Experimental       and Salinity
  Shell Wall                           Design          ([degrees]C;
    Type *         Foraminifera      ([dagger])            psu)

Hyaline           Amphistegina     Laboratory/       26-28: ND
                  lobifera         closed system/
                                   bottle

                  Amphistegina     Laboratory/       25; 38-40
                  gibbosa          closed system/
                                   incubator

                  Amphistegina     Laboratory/       27.2-27.5: ND
                  radiata          flow-through
                                   system

                                   Laboratory        25.9-26.0: ND
                                   /semi-closed
                                   circulation
                                   system

                  Baculogypsina    Laboratory/       27.5; 34.4
                  sphaerulata      flow-through
                                   system/AICAL

                  Calcarina        Laboratory/       27.5; 34.4
                  gaudichaudii     flow-through
                                   system/AICAL

                                   Laboratory/       27.1; 34.1
                                   flow- through
                                   system/AICAL

                  Heterostegina    Laboratory/       27.2-27.5: ND
                  depressa         flow-through
                                   system

                                   Laboratory/       25.9-26.0: ND
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       27.9-28.1: ND
                                   flow-through
                                   system

Porcelaneous      Amphisorus       Laboratory/       26-28: ND
                  hemprichii       closed system/
                                   bottle

                                   Laboratory/       27.5; 34.4
                                   flow-through
                                   system/AICAL

                  Amphisorus       Laboratory/       25: ND
                  kudakajmensis    closed system/
                                   botde

                                   Laboratory/       27.1; 34.1
                                   flow-through
                                   system/AICAL

                  Marginopora      Laboratory/       28-34; 33
                  vertebralis      recirculated
                                   system/
                                   two-factors
                                   (temp)

                                   Laboratory/       27.2-27.5: ND
                                   flow-through
                                   system

                                   Field & on        27.4-29.9;
                                   board/at          33.2-35.7
                                   C[O.sub.2]
                                   vent, Papua New
                                   Guinea

                                   Laboratory/       25.7-29.3;
                                   closed system/    31.5-35.2
                                   vials

                                   Laboratory/       25.9-26.0: ND
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       27.9-28.1: ND
                                   flow-through
                                   system

                  Marginopora      Laboratory/       25; 35
                  rossi            closed system/
                                   two-factors
                                   (nutrient)

                  Peneroplis sp.   Laboratory/       25.9-26.0
                                   semi-closed
                                   circulation
                                   system

                                    Experimental        Carbonate
  Shell Wall                           Design           Chemistry
    Type *         Foraminifera      ([dagger])        Manipulation

Hyaline           Amphistegina     Laboratory/       Acid/base
                  lobifera         closed system/
                                   bottle

                  Amphistegina     Laboratory/       Atmospheric
                  gibbosa          closed system/    C[O.sub.2]
                                   incubator         aerated

                  Amphistegina     Laboratory/       C[O.sub.2]
                  radiata          flow-through      bubbling
                                   system

                                   Laboratory        C[O.sub.2]
                                   /semi-closed      bubbling
                                   circulation
                                   system

                  Baculogypsina    Laboratory/       C[O.sub.2]
                  sphaerulata      flow-through      bubbling
                                   system/AICAL

                  Calcarina        Laboratory/       C[O.sub.2]
                  gaudichaudii     flow-through      bubbling
                                   system/AICAL

                                   Laboratory/       C[O.sub.2]
                                   flow- through     bubbling
                                   system/AICAL

                  Heterostegina    Laboratory/       C[O.sub.2]
                  depressa         flow-through      bubbling
                                   system

                                   Laboratory/       C[O.sub.2]
                                   semi-closed       bubbling
                                   circulation
                                   system

                                   Laboratory/       C[O.sub.2]
                                   flow-through      bubbling
                                   system

Porcelaneous      Amphisorus       Laboratory/       Acid/base
                  hemprichii       closed system/
                                   bottle

                                   Laboratory/       C[O.sub.2]
                                   flow-through      bubbling
                                   system/AICAL

                  Amphisorus       Laboratory/       Acid/base
                  kudakajmensis    closed system/
                                   botde

                                   Laboratory/       C[O.sub.2]
                                   flow-through      bubbling
                                   system/AICAL

                  Marginopora      Laboratory/       C[O.sub.2]
                  vertebralis      recirculated      bubbling
                                   system/
                                   two-factors
                                   (temp)

                                   Laboratory/       C[O.sub.2]
                                   flow-through      bubbling
                                   system

                                   Field & on        Natural
                                   board/at          C[O.sub.2] seeps
                                   C[O.sub.2]
                                   vent, Papua New
                                   Guinea

                                   Laboratory/       C[O.sub.2]
                                   closed system/    bubbling
                                   vials

                                   Laboratory/       C[O.sub.2]
                                   semi-closed       bubbling
                                   circulation
                                   system

                                   Laboratory/       C[O.sub.2]
                                   flow-through      bubbling
                                   system

                  Marginopora      Laboratory/       C[O.sub.2]
                  rossi            closed system/    bubbling
                                   two-factors
                                   (nutrient)

                  Peneroplis sp.   Laboratory/       C[O.sub.2]
                                   semi-closed       bubbling
                                   circulation
                                   system

                                    Experimental       pC[O.sub.2]
  Shell Wall                           Design             Range
    Type *         Foraminifera      ([dagger])        ([micro]atm)

Hyaline           Amphistegina     Laboratory/       ND
                  lobifera         closed system/
                                   bottle

                  Amphistegina     Laboratory/       385-2000 ppmv
                  gibbosa          closed system/
                                   incubator

                  Amphistegina     Laboratory/       467-1662
                  radiata          flow-through
                                   system

                                   Laboratory        432-2151
                                   /semi-closed
                                   circulation
                                   system

                  Baculogypsina    Laboratory/       261-972
                  sphaerulata      flow-through
                                   system/AICAL

                  Calcarina        Laboratory/       261-972
                  gaudichaudii     flow-through
                                   system/AICAL

                                   Laboratory/       245-907
                                   flow- through
                                   system/AICAL

                  Heterostegina    Laboratory/       467-1662
                  depressa         flow-through
                                   system

                                   Laboratory/       432-2151
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       479-738
                                   flow-through
                                   system

Porcelaneous      Amphisorus       Laboratory/       ND
                  hemprichii       closed system/
                                   bottle

                                   Laboratory/       261-972
                                   flow-through
                                   system/AICAL

                  Amphisorus       Laboratory/       ND
                  kudakajmensis    closed system/
                                   botde

                                   Laboratory/       245-907
                                   flow-through
                                   system/AICAL

                  Marginopora      Laboratory/       33.2-262 Pa
                  vertebralis      recirculated
                                   system/
                                   two-factors
                                   (temp)

                                   Laboratory/       467-1662
                                   flow-through
                                   system

                                   Field & on        373-12105
                                   board/at
                                   C[O.sub.2]
                                   vent, Papua New
                                   Guinea

                                   Laboratory/       333-2314
                                   closed system/
                                   vials

                                   Laboratory/       432-2151
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       479-738
                                   flow-through
                                   system

                  Marginopora      Laboratory/       252-1048
                  rossi            closed system/
                                   two-factors
                                   (nutrient)

                  Peneroplis sp.   Laboratory/       432-2151
                                   semi-closed
                                   circulation
                                   system

                                    Experimental
  Shell Wall                           Design            pH Range
    Type *         Foraminifera      ([dagger])          (scale)

Hyaline           Amphistegina     Laboratory/       6.0-9.6 (NBS)
                  lobifera         closed system/
                                   bottle

                  Amphistegina     Laboratory/       7.56-8.10
                  gibbosa          closed system/    (total)
                                   incubator

                  Amphistegina     Laboratory/       7.66-8.14
                  radiata          flow-through      (total)
                                   system

                                   Laboratory        7.60-8.22 (NBS)
                                   /semi-closed
                                   circulation
                                   system

                  Baculogypsina    Laboratory/       7.76-8.17
                  sphaerulata      flow-through      (total)
                                   system/AICAL

                  Calcarina        Laboratory/       7.76-8.17
                  gaudichaudii     flow-through      (total)
                                   system/AICAL

                                   Laboratory/       7.76-8.23
                                   flow- through     (total)
                                   system/AICAL

                  Heterostegina    Laboratory/       7.66-8.14
                  depressa         flow-through      (total)
                                   system

                                   Laboratory/       7.60-8.22 (NBS)
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       8.15-7.98 (NBS)
                                   flow-through
                                   system

Porcelaneous      Amphisorus       Laboratory/       6.0-9.6 (NBS)
                  hemprichii       closed system/
                                   bottle

                                   Laboratory/       7.76-8.17
                                   flow-through      (total)
                                   system/AICAL

                  Amphisorus       Laboratory/       7.7-8.3 (NBS)
                  kudakajmensis    closed system/
                                   botde

                                   Laboratory/       7.76-8.23
                                   flow-through      (total)
                                   system/AICAL

                  Marginopora      Laboratory/       7.4-8.1 (NBS)
                  vertebralis      recirculated
                                   system/
                                   two-factors
                                   (temp)

                                   Laboratory/       7.66-8.14
                                   flow-through      (total)
                                   system

                                   Field & on        7.07-8.19
                                   board/at          (total)
                                   C[O.sub.2]
                                   vent, Papua New
                                   Guinea

                                   Laboratory/       7.43-8.17
                                   closed system/    (total)
                                   vials

                                   Laboratory/       7.60-8.22 (NBS)
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       8.15-7.98 (NBS)
                                   flow-through
                                   system

                  Marginopora      Laboratory/       7.6-8.1 (NBS)
                  rossi            closed system/
                                   two-factors
                                   (nutrient)

                  Peneroplis sp.   Laboratory/       7.60-8.22 (NBS)
                                   semi-closed
                                   circulation
                                   system

                                    Experimental
  Shell Wall                           Design             Omega
    Type *         Foraminifera      ([dagger])          Calcite

Hyaline           Amphistegina     Laboratory/       ND
                  lobifera         closed system/
                                   bottle

                  Amphistegina     Laboratory/       1.84-6.36
                  gibbosa          closed system/
                                   incubator

                  Amphistegina     Laboratory/       1.8-4.8
                  radiata          flow-through
                                   system

                                   Laboratory        1.90-6.52
                                   /semi-closed
                                   circulation
                                   system

                  Baculogypsina    Laboratory/       2.7-64
                  sphaerulata      flow-through
                                   system/AICAL

                  Calcarina        Laboratory/       2.7-64
                  gaudichaudii     flow-through
                                   system/AICAL

                                   Laboratory/       2.9-6.8
                                   flow-through
                                   system/AICAL

                  Heterostegina    Laboratory/       1.8-4.8
                  depressa         flow-through
                                   system

                                   Laboratory/       1.90-6.52
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       3.8-5.1
                                   flow-through
                                   system

Porcelaneous      Amphisorus       Laboratory/       ND
                  hemprichii       closed system/
                                   bottle

                                   Laboratory/       2.7-64
                                   flow-through
                                   system/AICAL

                  Amphisorus       Laboratory/       ND
                  kudakajmensis    closed system/
                                   botde

                                   Laboratory/       2.9-6.8
                                   flow-through
                                   system/AICAL

                  Marginopora      Laboratory/       1.84-8.02
                  vertebralis      recirculated
                                   system/
                                   two-factors
                                   (temp)

                                   Laboratory/       1.8-4.8
                                   flow-through
                                   system

                                   Field & on        0.40-5.92
                                   board/at
                                   C[O.sub.2]
                                   vent, Papua New
                                   Guinea

                                   Laboratory/       1.35-6.41
                                   closed system/
                                   vials

                                   Laboratory/       1.90-6.52
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       3.8-5.1
                                   flow-through
                                   system

                  Marginopora      Laboratory/       1.91-5.38
                  rossi            closed system/
                                   two-factors
                                   (nutrient)

                  Peneroplis sp.   Laboratory/       1.90-6.52
                                   semi-closed
                                   circulation       2280-2282
                                   system
                                   system

                                   Laboratory/       2617-2709
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       2232-2235
                                   flow-through
                                   system

Porcelaneous      Amphisorus       Laboratory/       ND
                  hemprichii       closed system/
                                   bottle

                                   Laboratory/       2188
                                   flow-through
                                   system/AICAL

                  Amphisorus       Laboratory/       ND
                  kudakajmensis    closed system/
                                   botde

                                   Laboratory/       2224
                                   flow-through
                                   system/AICAL

                  Marginopora      Laboratory/       2314-2827
                  vertebralis      recirculated
                                   system/
                                   two-factors
                                   (temp)

                                   Laboratory/       2280-2282
                                   flow-through
                                   system

                                   Field & on        2239-2619
                                   board/at
                                   C[O.sub.2]
                                   vent, Papua New
                                   Guinea

                                   Laboratory/       2103-2335
                                   closed system/
                                   vials

                                   Laboratory/       2617-2709
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       2232-2235
                                   flow-through
                                   system

                  Marginopora      Laboratory/       2036-2075
                  rossi            closed system/
                                   two-factors
                                   (nutrient)

                  Peneroplis sp.   Laboratory/       2617-2709
                                   semi-closed
                                   circulation
                                   system

                                                       TA ([double
                                    Experimental         dagger])
  Shell Wall                           Design          ([micro]mol
    Type *         Foraminifera      ([dagger])        [kg.sup.-1])

Hyaline           Amphistegina     Laboratory/       ND
                  lobifera         closed system/
                                   bottle

                  Amphistegina     Laboratory/       2480-2624
                  gibbosa          closed system/
                                   incubator

                  Amphistegina     Laboratory/       2280-2282
                  radiata          flow-through
                                   system

                                   Laboratory        2617-2709
                                   /semi-closed
                                   circulation
                                   system

                  Baculogypsina    Laboratory/       2188
                  sphaerulata      flow-through
                                   system/AICAL

                  Calcarina        Laboratory/       2188
                  gaudichaudii     flow-through
                                   system/AICAL

                                   Laboratory/       2224
                                   flow-through
                                   system/AICAL

                  Heterostegina    Laboratory/       2280-2282
                  depressa         flow-through
                                   system

                                   Laboratory/       2617-2709
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       2232-2235
                                   flow-through
                                   system

Porcelaneous      Amphisorus       Laboratory/       ND
                  hemprichii       closed system/
                                   bottle

                                   Laboratory/       2188
                                   flow-through
                                   system/AICAL

                  Amphisorus       Laboratory/       ND
                  kudakajmensis    closed system/
                                   botde

                                   Laboratory/       2224
                                   flow-through
                                   system/AICAL

                  Marginopora      Laboratory/       2314-2827
                  vertebralis      recirculated
                                   system/
                                   two-factors
                                   (temp)

                                   Laboratory/       2280-2282
                                   flow-through
                                   system

                                   Field & on        2239-2619
                                   board/at
                                   C[O.sub.2]
                                   vent, Papua New
                                   Guinea

                                   Laboratory/       2103-2335
                                   closed system/
                                   vials

                                   Laboratory/       2617-2709
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       2232-2235
                                   flow-through
                                   system

                  Marginopora      Laboratory/       2036-2075
                  rossi            closed system/
                                   two-factors
                                   (nutrient)

                  Peneroplis sp.   Laboratory/       2617-2709
                                   semi-closed
                                   circulation
                                   system

                                                           DIC
                                    Experimental      ([paragraph])
  Shell Wall                           Design          ([micro]mol
    Type *         Foraminifera      ([dagger])        [kg.sup.-1])

Hyaline           Amphistegina     Laboratory/       ND
                  lobifera         closed system/
                                   bottle

                  Amphistegina     Laboratory/       2100-2517
                  gibbosa          closed system/
                                   incubator

                  Amphistegina     Laboratory/       1999-2192
                  radiata          flow-through
                                   system

                                   Laboratory        2343-2603
                                   /semi-closed
                                   circulation
                                   system

                  Baculogypsina    Laboratory/       1796-2043
                  sphaerulata      flow-through
                                   system/AICAL

                  Calcarina        Laboratory/       1796-2043
                  gaudichaudii     flow-through
                                   system/AICAL

                                   Laboratory/       1821-2075
                                   flow-through
                                   system/AICAL

                  Heterostegina    Laboratory/       1999-2192
                  depressa         flow-through
                                   system

                                   Laboratory/       2343-2603
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       2031-2134
                                   flow-through
                                   system

Porcelaneous      Amphisorus       Laboratory/       ND
                  hemprichii       closed system/
                                   bottle

                                   Laboratory/       1796-2043
                                   flow-through
                                   system/AICAL

                  Amphisorus       Laboratory/       ND
                  kudakajmensis    closed system/
                                   botde

                                   Laboratory/       1821-2075
                                   flow-through
                                   system/AICAL

                  Marginopora      Laboratory/       1923-2749
                  vertebralis      recirculated
                                   system/
                                   two-factors
                                   (temp)

                                   Laboratory/       1999-2192
                                   flow-through
                                   system

                                   Field & on        1926-2919
                                   board/at
                                   C[O.sub.2]
                                   vent, Papua New
                                   Guinea

                                   Laboratory/       1841-2296
                                   closed system/
                                   vials

                                   Laboratory/       2343-2603
                                   semi-closed
                                   circulation
                                   system

                                   Laboratory/       2031-2134
                                   flow-through
                                   system

                  Marginopora      Laboratory/       1960-2140
                  rossi            closed system/
                                   two-factors
                                   (nutrient)

                  Peneroplis sp.   Laboratory/       2343-2603
                                   semi-closed
                                   circulation
                                   system

B. CALCIFICATION AND PHOTOSYNTHESIS PARAMETERS AND FINDINGS

                    Measurement                         Measurement
                    Methods of                          Methods of
 Foraminefera      Calcification     Calcification    Photosynthesis

Amphistegina      [sup.l4]C         Decrease with     [l4.sup.C]
lobifera          tracer            elevated          tracer
                  technique         pC[O.sub.2]       technique
                  ([micro]g C mg                      ([micro]g C mg
                  [foram.sup.-1]                      [foram.sup.-1]
                  2[d.sup.-1])                        2[d.sup.-1])

Amphistegina      Growth rate (%    No change but     Not measured
gibbosa           surface area)     partial
                                    dissolution of
                                    shell surfaces
                                    at 2000 ppmv

Amphistegina      Growth rate (%    No change with    Fv/Fm, chl-a
radicita          surface area      elevated
                  [d.sup.-1])       pC[O.sub.2]

                  [Ca.sup.2+]       No change with    [O.sub.2]
                  microsensor       elevated          microsensor
                                    pC[O.sub.2]

Baculogypsina     Final shell       Increase with     Not measured
sphaerulatci      weight and        elevated
                  diameter          pC[O.sub.2]

Calcarina         Final shell       Increase with     Not measured
gaudichaudii      weight and        elevated
                  diameter          pC[O.sub.2]

                  Final shell       Increase with     Not measured
                  weight            elevated
                                    pC[O.sub.2]

Heterostegina     Growth rate (%    No change with    Fv-Fm,
depressa          surface area      elevated          [O.sub.2]
                  [d.sup.-1])       pC[O.sub.2]       production
                                                      ([micro]g
                                                      [O.sub.2]
                                                      [h.sup.-1] mg
                                                      [(ww).sup.-1])

                  [Ca.sup.2+]       No change with    [O.sub.2]
                  microsensor       elevated          microsensor
                                    pC[O.sub.2]

                  Growth rate (%    Decrease with     Fv-Fm,
                  surface area      elevated          [O.sub.2]
                  [d.sup.-1])       pC[O.sub.2]       production
                                                      ([micro]g
                                                      [O.sub.2]
                                                      [h.sup.-1] mg
                                                      [(ww).sup.-1])

Amphisorus        [sup.l4]C         Decrease with     [sup.l4]C
hemprichii        tracer            elevated          tracer
                  technique         pC[O.sub.2]       technique
                  ([micro]g C mg                      ([micro]g C mg
                  [foram.sup.-1]                      [foram.sup.-1]
                  2[d.sup.-1])                        2[d.sup.-1])

                  Final shell       Decrease with     Not measured
                  weight and        elevated
                  diameter          pC[O.sub.2]

Amphisorus        Final shell       Decrease with     Not measured
kudakcijimensis   weight and        elevated
                  diameter,         pC[O.sub.2]
                  number of
                  chambers

                  Final shell       Decrease with     Not measured
                  weight            elevated
                                    pC[O.sub.2]

Marginopora       Buoyant weight    Decrease          Fv-Fm,
vertebralis       technique (mg     (dissolution)     [O.sub.2]
                  CaC[O.sub.3]      with elevated     production
                  [d.sup.-1])       pC[O.sub.2] and   ([micro]mol
                                    /or high          [O.sub.2]
                                    temperature       [L.sup.-1])

                  Growth rate (%    Increased rates   Fv-Fm,
                  surface area      with elevated     [O.sub.2]
                  [d.sup.-1])       pC[O.sub.2]       production
                                                      ([micro]g
                                                      [O.sub.2]
                                                      [h.sup.-1] mg
                                                      [(ww).sup.-1])

                  Not measured                        [O.sub.2]
                                                      production
                                                      ([micro]g
                                                      [O.sub.2]
                                                      [mm.sup.-2]
                                                      [d.sup.-1])

                  Alkalinity        Decrease with     [O.sub.2]
                  anomaly           elevated          production
                  techinique (%     pC[O.sub.2]       ([micro]g
                  dry wt.                             [O.sub.2]
                  [d.sup.-1])                         [mm.sup.-2]
                                                      [d.sup.-1])

                  [Ca.sup.2+]       No change with    [O.sub.2]
                  microsensor       elevated          microsensor
                                    pC[O.sub.2]

                  Growth rate (%    No change with    Fv-Fm,
                  surface area      elevated          [O.sub.2]
                  [d.sup.-1])       pC[O.sub.2]       production
                                                      ([micro]g
                                                      [O.sub.2]
                                                      [h.sup.-1] mg
                                                      [(ww).sup.-1])

Marginopora       Growth rate (%    Decrease with     [O.sub.2]
rossi             surface area      elevated          production
                  [d.sup.-1])       pC[O.sub.2]       ([micro]mol
                                                      [O.sub.2]
                                                      [g.sup.-2]
                                                      [h.sup.-1])

Peneroplis sp.    [Ca.sup.2+]       No change with    [O.sub.2]
                  microsensor       elevated          microsensor
                                    pC[O.sub.2]

                    Measurement
                    Methods of       No change but
 Foraminefera      Calcification        partial          Reference

Amphistegina      [sup.l4]C         Slight decrease   ter Kuile et
lobifera          tracer            with elevated     al. (1989)
                  technique         pC[O.sub.2]
                  ([micro]g C mg
                  [foram.sup.-1]
                  2[d.sup.-1])

Amphistegina      Growth rate (%                      McIntyre-
gibbosa           surface area)                       Wressnig et al.
                                                      (2013)

Amphistegina      Growth rate (%    No change with    Vogel and
radicita          surface area      elevated          Uthicke (2012)
                  [d.sup.-1])       pC[O.sub.2]

                  [Ca.sup.2+]       No change with    Glas et al.
                  microsensor       elevated          (2012)
                                    pC[O.sub.2]

Baculogypsina     Final shell             --          Fujita et al.
sphaerulatci      weight and                          (2011)
                  diameter

Calcarina         Final shell             --          Fujita et al.
gaudichaudii      weight and                          (2011)
                  diameter

                  Final shell             --          Hikami et al.
                  weight                              (2011)

Heterostegina     Growth rate (%    No change with    Vogel and
depressa          surface area      elevated          Uthicke (2012)
                  [d.sup.-1])       pC[O.sub.2]

                  [Ca.sup.2+]       No change with    Glas et al.
                  microsensor       elevated          (2012)
                                    pC[O.sub.2]

                  Growth rate (%    No change with    Schmidt et al.,
                  surface area      elevated          in press
                  [d.sup.-1])       pC[O.sub.2]

Amphisorus        [sup.l4]C         Slight decrease   ter Kuile et
hemprichii        tracer            with elevated     al. (1989)
                  technique         pC[O.sub.2]
                  ([micro]g C mg
                  [foram.sup.-1]
                  2[d.sup.-1])

                  Final shell             --          Fujita et al.
                  weight and                          (2011)
                  diameter

Amphisorus        Final shell             --          Kuroyanagi et
kudakcijimensis   weight and                          al. (2009)
                  diameter,
                  number of
                  chambers

                  Final shell             --          Hikami et al.
                  weight                              (2011)

Marginopora       Buoyant weight    Decrease with     Sinutok et al.
vertebralis       technique (mg     elevated          (2011)
                  CaC[O.sub.3]      pC[O.sub.2]
                  [d.sup.-1])       and/or high
                                    temp.

                  Growth rate (%    No change with    Vogel et al.
                  surface area      elevated peo,     (2012)
                  [d.sup.-1])

                  Not measured      Increase with     Uthicke and
                                    elevated          Fabricius
                                    pC[O.sub.2]       (2012)

                  Alkalinity        Increase with     Uthicke and
                  anomaly           elevated          Fabricius
                  techinique (%     pC[O.sub.2]       (2012)
                  dry wt.
                  [d.sup.-1])

                  [Ca.sup.2+]       No change with    Glas et al.
                  microsensor       elevated          (2012)
                                    pC[O.sub.2]

                  Growth rate (%    No change with    Schmidt et al.
                  surface area      elevated          (2014)
                  [d.sup.-1])       pC[O.sub.2]

Marginopora       Growth rate (%    Decrease with     Reymond et
rossi             surface area      elevated          al.,(2013)
                  [d.sup.-1])       pC[O.sub.2]; no
                                    effects of
                                    nutrients

Peneroplis sp.    [Ca.sup.2+]       No change with    Glas et al.
                  microsensor       elevated          (2012)
                                    pC[O.sub.2]
* The symbionts of all hyaline species listed here are pennate
diatoms; those of all porcelaneous species are dinoflagellates.

([dagger]]) AICAL, a Japanese system; Acidification Impacts on
Calcifiers.

([double dagger]) TA, total alkalinity.

([paragraph]) DIC, dissolved organic carbon.

DIC, dissolved inorganic carbon: ND, not determined; TA, total
alkalinity.

Appendix 3

All studies to date on ocean warming effects on tropical symbiont-
bearing large benthic foraminifera physiology. Experiment conditions
are presented in table A, while calcification and photosynthesis
parameters and finds for the corresponding studies are found in
table B.

A. EXPERIMENT CONDITIONS

  Shell Wall                         Experimental
    Type *         Foraminifera         Design           Duration

Hyaline           Amphistegina      Laboratory/       5 weeks
                  gibbosa           closed system/
                                    incubator

                  Amphistegina      Laboratory/       6 days
                  rcidicita         closed system/
                                    bottle

                                    Laboratory/       30 days
                                    flow-through

                  Baculogypsina     Laboratory/       5 hours
                  sphaerulata       closed system/
                                    bottle

                                    Laboratory/       1 day
                                    closed system/
                                    bottle

                  Calcarina         Laboratory/       1 day
                  gaudichaudii      closed system/
                                    bottle

                  Calcanna          Laboratory/       6 days
                  hispida           closed system/
                                    bottle

                  Calcarina         Laboratory/       30 days
                  mayori            flow-through

                                    Laboratory/       96 hours
                                    closed system/
                                    incubator

                  Heterostegina     Laboratory/       6 days
                  depressa          closed system/
                                    bottle

                                    Laboratory/       30 days
                                    flow-through

                                    Laboratory/       96 hours
                                    closed system/
                                    incubator

                                    Laboratory/       35 days
                                    flow-through

Porcelaneous      Alveolinella      Laboratory/       96 hours
                  quoyi             closed system/
                                    incubator

                  Amphisorus        Laboratory/       1 day
                  kudakajimensis    closed system/
                                    bottle

                  Sorties           Field-based       2 days
                  dominicensis      study

                  Marginopora       Laboratory/       3 weeks
                  vertebralis       closed system/
                                    bottle

                                    Laboratory/       6 weeks
                                    closed system/
                                    bottle

                                    Laboratory/       96 hours
                                    closed system/
                                    incubator

                                    Laboratory/       53 days
                                    flow-through

                  Peneroplis        Laboratory/       96 hours
                  planatus          closed system/
                                    incubator

                                                           Light
                                                         Condition
                                                        ([micro]mol
  Shell Wall                         Experimental       [m.sup.-2]
    Type *         Foraminifera         Design          [s.sup.-1])

Hyaline           Amphistegina      Laboratory/       6-15
                  gibbosa           closed system/
                                    incubator

                  Amphistegina      Laboratory/       11-15
                  rcidicita         closed system/
                                    bottle

                                    Laboratory/       200
                                    flow-through

                  Baculogypsina     Laboratory/       250
                  sphaerulata       closed system/
                                    bottle

                                    Laboratory/       100
                                    closed system/
                                    bottle

                  Calcarina         Laboratory/       100
                  gaudichaudii      closed system/
                                    bottle

                  Calcanna          Laboratory/       11-15
                  hispida           closed system/
                                    bottle

                  Calcarina         Laboratory/       200
                  mayori            flow-through

                                    Laboratory/       10
                                    closed system/
                                    incubator

                  Heterostegina     Laboratory/       11-15
                  depressa          closed system/
                                    bottle

                                    Laboratory/       200
                                    flow-through

                                    Laboratory/       10
                                    closed system/
                                    incubator

                                    Laboratory/       8-12
                                    flow-through

Porcelaneous      Alveolinella      Laboratory/       10
                  quoyi             closed system/
                                    incubator

                  Amphisorus        Laboratory/       100
                  kudakajimensis    closed system/
                                    bottle

                  Sorties           Field-based       ND
                  dominicensis      study

                  Marginopora       Laboratory/       150
                  vertebralis       closed system/
                                    bottle

                                    Laboratory/       6-9
                                    closed system/
                                    bottle

                                    Laboratory/       10
                                    closed system/
                                    incubator

                                    Laboratory/       45-50
                                    flow-through

                  Peneroplis        Laboratory/       10
                  planatus          closed system/
                                    incubator

                                                        Temperature
  Shell Wall                         Experimental          Range
    Type *         Foraminifera         Design         ([degrees]C)

Hyaline           Amphistegina      Laboratory/       20-32
                  gibbosa           closed system/

                                    incubator

                  Amphistegina      Laboratory/       23-33
                  rcidicita         closed system/
                                    bottle

                                    Laboratory/       26-31
                                    flow-through

                  Baculogypsina     Laboratory/       26-34
                  sphaerulata       closed system/
                                    bottle

                                    Laboratory/       5-45
                                    closed system/
                                    bottle

                  Calcarina         Laboratory/       5-45
                  gaudichaudii      closed system/
                                    bottle

                  Calcanna          Laboratory/       23-33
                  hispida           closed system/
                                    bottle

                  Calcarina         Laboratory/       26-31
                  mayori            flow-through

                                    Laboratory/       26-34
                                    closed system/
                                    incubator

                  Heterostegina     Laboratory/       23-33
                  depressa          closed system/
                                    bottle

                                    Laboratory/       26-31
                                    flow-through

                                    Laboratory/       26-34
                                    closed system/
                                    incubator

                                    Laboratory/       28-31
                                    flow-through

Porcelaneous      Alveolinella      Laboratory/       26-34
                  quoyi             closed system/
                                    incubator

                  Amphisorus        Laboratory/       5-45
                  kudakajimensis    closed system/
                                    bottle

                  Sorties           Field-based       28-31
                  dominicensis      study

                  Marginopora       Laboratory/       26-32
                  vertebralis       closed system/
                                    bottle

                                    Laboratory/       22-28
                                    closed system/
                                    bottle

                                    Laboratory/       26-34
                                    closed system/
                                    incubator

                                    Laboratory/       28-31
                                    flow-through

                  Peneroplis        Laboratory/       26-34
                  planatus          closed system/
                                    incubator

B. CALCIFICATION AND PHOTOSYNTHESIS PARAMETERS AND FINDINGS

                    Measurement                         Measurement
                    Methods of                          Methods of
 Foraminifera      Calcification     Calcification    Photosynthesis

Amphistegina      Not measured            --          Histological
gibbosa                                               observation of
                                                      bleaching

Amphistegina      Growth rate (%    Decreased         Fv/Fm, chl-a
radiata           surface area      growth at
                  [d.sup.-1])       elevated
                                    temperature

Baculogypsina     Not measured            --          Western
sphaerulata                                           blotting,
                                                      RuBisCO enzyme

                  Not measured            --          [O.sub.2]
                                                      production
                                                      ([micro]g
                                                      [O.sub.2]
                                                      [h.sup.-1] mg
                                                      [(ww).sup.-1])

Calcarina         Not measured            --          [O.sub.2]
gaudichaudii                                          production
                                                      ([micro]g
                                                      [O.sub.2]
                                                      [h.sup.-1] mg
                                                      [(ww).sup.-1])

Calcarina         Not measured            --          Fv/Fm, chl-a
hispida

Calcarina         Not measured            --          Fv/Fm, chl-a
mayori

                  Not measured            --          Fv/Fm

Heterostegina     Not measured            --          Fv/Fm, chl-a
depressa

                  Not measured            --          Fv/Fm, chl-a

                  Not measured            --          Fv/Fm, visual
                                                      observation of
                                                      bleaching

                  Growth rate (%    Decreased         Fv/Fm,
                  surface area      growth with       chl-a,
                  [d.sup.-1])       elevated          [O.sub.2]
                                    temperature       production
                                                      ([micro]g
                                                      [O.sub.2]
                                                      [h.sup.-1] mg
                                                      [(ww).sup.-1])

Alveolinella      Not measured            --          Fv/Fm
quoyi

Amphisorus        Not measured            --          [O.sub.2]
kudakajimensis                                        production
                                                      ([micro]g
                                                      [O.sub.2]
                                                      [h.sup.-1] mg
                                                      [(ww).sup.-1])

Sorties           Not measured            --          Visual
dominicensis                                          observation of
                                                      bleaching

Marginopora       Growth rate (%    Decrease growth   Not measured
vertebralis       surface area      (dissolution)
                  [d.sup.-1])       with elevated
                                    temperature

                  Growth rate (%    Decreased         Not measured
                  surface area      growth with
                  [d.sup.-1])       elevated
                                    temperature

                  Not measured                        Fv/Fm, visual
                                                      observation of
                                                      bleaching

                  Growth rate (%    Decreased         Fv-Fm, chl-a,
                  surface area      growth with       [O.sub.2]
                  [d.sup.-1])       elevated          production
                                    temperature       ([micro]g
                                                      [O.sub.2]
                                                      [h.sup.-1] mg
                                                      [(ww).sup.-1])

Peneroplis        Not measured                        Fv/Fm
planatus

                    Measurement
                    Methods of
 Foraminifera      Calcification    Photosynthesis       Reference

Amphistegina      Not measured      Bleaching with    Talge and
gibbosa                             elevated          Hallock (2003)
                                    temperature

Amphistegina      Growth rate (%    Decreased         Schmidt et al.
radiata           surface area      Fv/Fm and         (2011)
                  [d.sup.-1])       chl-a at
                                    increased
                                    temperature

Baculogypsina     Not measured      Decreased with    Doo et al.
sphaerulata                         elevated          (2012b)
                                    temperature

                  Not measured      Increased with    Fujita et al.
                                    mild              (2014)
                                    (+5[degrees]C)
                                    elevated
                                    temperature

Calcarina         Not measured      Increased with    Fujita et al.
gaudichaudii                        mild              (2014)
                                    (+5[degrees]C)
                                    elevated
                                    temperature

Calcarina         Not measured      Decreased         Schmidt et al.
hispida                             Fv/Fm and         (2011)
                                    chl-a at
                                    increased
                                    temperature

Calcarina         Not measured      No signifcant     Schmidt et al.
mayori                              effect with       (2011)
                                    temperature

                  Not measured      Decreased         van Dam et al.
                                    Fv/Fm at          (2012)
                                    elevated
                                    temperature

Heterostegina     Not measured      Decreased         Schmidt et al.
depressa                            Fv/Fm and         (2011)
                                    chl-a at
                                    increased
                                    temperature

                  Not measured      Decreased Fv/     Schmidt et al.
                                    Fm and chl-a at   (2011)
                                    increased
                                    temperature

                  Not measured      Decreased Fv/     van Dam et al.
                                    Fm and            (2012)
                                    increased
                                    bleaching with
                                    elevated
                                    temperature

                  Growth rate (%    Decreased         Schmidt et al.
                  surface area      Fv/Fm and         (in press)
                  [d.sup.-1])       chl-a,
                                    [O.sub.2]
                                    production at
                                    increased
                                    temperature

Alveolinella      Not measured      Decreased Fv/     van Dam et al.
quoyi                               Fm at elevated    (2012)
                                    temperature

Amphisorus        Not measured      Increased with    Fujita et al.
kudakajimensis                      mild              (2014)
                                    (+5[degrees]C)
                                    elevated
                                    temperature

Sorties           Not measured      Bleaching with    Richardson
dominicensis                        elevated          (2009)
                                    temperature

Marginopora       Growth rate (%                      Doo et al.
vertebralis       surface area                        (2012a)
                  [d.sup.-1])

                  Growth rate (%                      Reymond et al.
                  surface area                        (2011)
                  [d.sup.-1])

                  Not measured      Decreased Fv/     van Dam et al.
                                    Fm and            (2012)
                                    increased
                                    bleaching with
                                    elevated
                                    temperature

                  Growth rate (%    Decreased Fv/     Schmidt et al.
                  surface area      Fm and chl-a,     (in press)
                  [d.sup.-1])       [O.sub.2]
                                    production at
                                    increased
                                    temperature

Peneroplis        Not measured      No change by      Glas et al.
planatus                            elevated          (2012)
                                    PC[O.sub.2]

* The symbionts of all hyaline species listed here are pennate
diatoms; those of all porcelaneous species are dinoflagellates with
the exception of Alveolinella quoyi, which has a pennate diatom.


Acknowledgments

This research was supported by grants from the Sir Keith Murdoch Fellowship (American Australian Association), PADI Foundation, Australian Coral Reef Society, Cushman Foundation (SD), and Great Barrier Reef Foundation Grant (MB, SD). SD was also supported by a PhD scholarship from the University of Sydney International Scholarship (USydIS). SU's contribution was supported by funding from the Australian Government's National Environmental Research Program. KF is supported by the International Research Hub Project for Climate Change and Coral Reef/ Island Dynamics, University of the Ryukyus. Dr. R. Coleman (USyd) is thanked for his helpful advice on data analysis.

Literature Cited

Bozinovic, F., P. Calosi, and J. I. Spicer. 2011. Physiological correlates of geographic range in animals. Annu. Rev. Ecol. Evol. Syst. 42: 155-179.

Byrne, M. 2011. Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanogr. Mar. Biol. 49: 1-42.

Byrne, M. 2012. Global change ecotoxicology: identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Mar. Environ. Res. 76: 3-15.

Byrne, M., and R. Przeslawski. 2013. Multistressor impacts of warming and acidification of the ocean on marine invertebrates' life histories. Integr. Comp. Biol. 53: 582-596.

Byrne, M., S. Foo, N. A. Soars, K. D. L. Wolfe, H. D. Nguyen, N. Hardy, and S. A. Dworjanyn. 2013. Ocean warming will mitigate the effects of acidification on calcifying sea urchin larvae (Heliocidaris tuberculata) from the Australian global warming hot spot. J. Exp. Mar. Biol. Ecol. 448: 250-257.

Collen, J. 1996. Recolonization of reef flat by larger foraminifera, Funafuti, Tuvalu. J. Micropalaeontol. 15: 130.

Culver, S. J. 1991. Early Cambrian Foraminifera from West Africa. Science 254: 689-691.

Dawson, J. L., S. G. Smithers, and Q. Hua. In press. The importance of large benthic foraminifera to reef island sediment budget and dynamics at Raine Island, northern Great Barrier Reef. Geomorphology. doi: 10.1016/j.geomorph.2014.03.023.

Doney, S. C., M. Ruckelshaus, J. E. Duffy, J. P. Barry, F. Chan, C. A. English, H. M. Galindo, J. M. Grebmeier, A. B. Hollowed, N. Knowlton et al. 2012. Climate change impacts on marine ecosystems. Annu. Rev. Mar. Sci. 4: 11-37.

Doo, S. S., A. B. Mayfield, M. Byrne, H. K. Chen, H. D. Nguyen, and T. Y. Fan. 2012a. Reduced expression of the rate-limiting carbon fixation enzyme RuBisCO in the benthic foraminifer Baculogypsina sphaerulata holobiont in response to heat shock. J. Exp. Mar. Biol. Ecol. 430: 63-67.

Doo, S. S., S. Hamylton, and M. Byrne. 2012b. Reef-scale assessment of intertidal large benthic foraminifera populations on One Tree Island, Great Barrier Reef and their future carbonate production potential in a warming ocean. Zool. Stud. 51: 1298-1307.

Enriquez, S., and M. A. Borowitzka. 2009. The use of fluorescence signal in studies of seagrasses and macroalgae. Pp. 187-208 in Chlorophyll a Fluorescence in Aquatic Sciences: Methods And Applications. Development in Applied Phycology 4, D. J. Sugget, ed. Springer.

Erez, J. 2003. The source of ions for biomineralization in Foraminifera and their implications for paleoceanographic proxies. Rev. Mineral. Geochem. 54: 115-149.

Fujita, K., and H. Fujimura. 2008. Organic and inorganic carbon production by algal symbiont-bearing foraminifera on northwest Pacific coral-reef flats. J. Foraminifer. Res. 38: 117-126.

Fujita, K., H. Nishi, and R. Saito. 2000. Population dynamics of Marginopora kudakajimensis Gudmundsson (Foraminifera: Soritidae) in the Ryukyu Islands, the subtropical northwest Pacific. Mar. Micropaleontol. 38: 267-284.

Fujita, K., Y. Osawa, H. Kayanne, Y. Ide, and H. Yamano. 2009. Distribution and sediment production of large benthic foraminifers on reef flats of the Majuro Atoll, Marshall Islands. Coral Reefs 28:29-45.

Fujita, K., M. Hikami, A. Suzuki, A. Kuroyanagi, K. Sakai, H. Kawahata, and Y. Nojiri. 2011. Effects of ocean acidification on calcification of symbiont-bearing reef foraminifers. Biogeosciences 8: 2089-2098.

Fujita, K., T. Okai, and T. Hosono. 2014. Oxygen metabolic responses of three species of large benthic foraminifers with algal symbionts to temperature stress. PloS One 9(3):e90304.

Gates, R. D. 1990. Seawater temperature and sublethal coral bleaching in Jamaica. Coral Reefs 8: 193-197.

Glas, M. S., K. E. Fabricius, D. de Beer, and S. Uthicke. 2012. The [O.sub.2], pH and [Ca.sup.2+] microenvironment of benthic foraminifera in a high C[O.sub.2] world. PloS One 7: e50010.

Hallock, P. 1981. Production of carbonate sediments by selected large benthic foraminifera on 2 Pacific coral reefs. J. Sediment. Petrol. 51: 467-474.

Hallock, P., H. K. Talge, E. M. Cockey, and R. G. Muller. 1995. A new disease in reef-dwelling foraminifera--Implications for coastal sedimentation. J. Foramin. Res. 25: 280-286.

Hammond, L. 1995. The current magnitude of biodiversity. Pp. 113138 in Global Biodiversity Assessment, V. H. Heywood, ed. Cambridge University Press, Cambridge.

Hamylton, S., A. Pescud, J. X. Leon, and D. P. Callaghan. 2013. A geospatial assessment of the relationship between reef flat community calcium carbonate production and wave energy. Coral Reefs 32: 1025-1039.

Hardy, N. A., M. Lamare, S. Uthicke, K. Wolfe, S. Doo, S. Dworjanyn, and M. Byrne. 2014. Thermal tolerance of early development in tropical and temperate sea urchins: inferences for the tropicalization of eastern Australia. Mar. Biol. 161: 395-409.

Harney, J. N., and C. H. Fletcher. 2003. A budget of carbonate framework and sediment production, Kailua Bay, Oahu, Hawaii. J. Sediment. Res. 73: 856-868.

Harney, J. N., P. Hallock, C. H. Fletcher III, and B. M. Richmond. 1999. Sanding crop and sediment production of reef-dwelling foraminifera on O'ahu, Hawai'i. Pac. Sci. 53: 61-73.

Hart, D. E., and P. S. Kench. 2007. Carbonate production of an emergent reef platform, Warraber Island, Torres Strait, Australia. Coral Reefs 26: 53-68.

Harvey, B. P., D. Gwynn-Jones, and P. J. Moore. 2013. Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol. Evol. 3: 1016-1030.

Hikami, M., H. Ushie, T. Irie, K. Fujita, A. Kuroyanagi, K. Sakai, Y. Nojiri, A. Suzuki, and H. Kawahata. 2011. Contrasting calcification responses to ocean acidification between two reef foraminifers harboring different algal symbionts. Geophys. Res. Lett. 38: L19601.

Hoegh-Guldberg, O. 1999. Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshw. Res. 50: 839-866.

Hoegh-Guldberg, O. 2011. Coral reef ecosystems and anthropogenic climate change. Reg. Environ. Change 11: S215-S227.

Hoegh-Guldberg, O., P. J. Mumby, A. J. Hooten, R. S. Steneck, P. Greenfield, E. Gomez, C. D. Harvell, P. F. Sale, A. J. Edwards, K. Caldiera et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742.

Hohenegger, J. 2006. The importance of symbiont-bearing benthic foraminifera for West Pacific carbonate beach environments. Mar. Micropaleontol. 61: 4-39.

Honisch, B., A. Ridgwell, D. N. Schmidt, E. Thomas, S. J. Gibbs, A. Sluijs, R. Zeebe, L. Kump, R. C. Martindale, S. E. Greene et al. 2012. The geological record of ocean acidification. Science 335: 1058-1063.

Iglesias-Prieto, R., J. L. Matta, W. A. Robins, and R. K. Trench. 1992. Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc. Natl. Acad. Sci. USA 89: 10302-10305.

IPCC (Intergovernmental Panel on Climate Change). 2013. Summary for Policymakers. In Climate Change 2013: The Physical Science Basis. Working Group l Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, T. F. Stocker, D. Qin, G. K. Planner, M. Tignor, S. K. Allen, J. Boschung, A. Naueis, Y. Xia, V. Bex and P. M. Midgley, eds. Cambridge University Press, Cambridge.

Jones, R. J., O. Hoegh-Guldberg, A. W. D. Larkum, and U. Schreiber. 1998. Temperature-induced bleaching of corals begins with impair ment of the C[O.sub.2] fixation mechanism in zooxanthellae. Plant Cell Environ. 21: 1219-1230.

Kelly, M. W., and G. E. Hofmann. 2013. Adaptation and the physiology of ocean acidification. Fund. Ecol. 27: 980-990.

Kroeker, K. J., R. L. Kordas, R. Crim, I. E. Hendriks, L. Ramajo, G. S. Singh, C. M. Duarte, and J. P. Gattuso. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19: 1884-1896.

Kuroyanagi, A., H. Kawahata, A. Suzuki, K. Fujita, and T. Irie. 2009. Impacts of ocean acidification on large benthic foraminifers: results from laboratory experiments. Mar. Micropaleontol. 73: 190-195.

Lamare, M., D. Pecorino, N. Hardy, M. Liddy, M. Byrne, and S. Uthicke. 2014. The thermal tolerance of crown-of-thoms (Acanthaster planci) embryos and bipinnaria larvae: implications for spatial and temporal variation in adult populations. Coral Reefs 33: 207-219.

Langer, M. R. 2008. Assessing the contribution of foraminiferan protists to global ocean carbonate production. J. Eukaryot. Microbiol. 55: 163-169.

Langer, M. R., M. T. Silk, and J. H. Lipps. 1997. Global ocean carbonate and carbon dioxide production: the role of reef foraminifera. J. Foraminifer. Res 27: 271-277.

Langer, M. R., A. E. Weinmann, S. Lotters, J. M. Bernhard, and D. Rodder. 2013. Climate-driven range extension of Amphistegina (Protista, Foraminiferida): models of current and predicted future ranges. PloS One 8: e54443.

Lee, J. J. 2006. Algal symbiosis in larger foraminifera. Symbiosis 42: 63-75.

Lee, J. J., K. Sang, B. ter Kuile, E. Strauss, P. J. Lee, and W. W. Faber. 1991. Nutritional and related experiments on laboratory maintenance of three species of symbiont-bearing, large foraminifera. Mar. Biol. 109: 417-425.

Lesser, M. P. 1997. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16: 187-192.

Mclntyre-Wressnig, A., J. Bernhard, D. McCorkle, and P. Hallock. 2013. Non-lethal effects of ocean acidification on the symbiont-bearing benthic foraminifer Amphistegina gibbosa. Mar. Ecol. Prog. Ser. 472: 45-60.

Momigliano, P., and S. Uthicke. 2013. Symbiosis in a giant protist (Marginopora vertebralis, Soritinae): flexibility in symbiotic partnerships along a natural temperature gradient. Mar. Ecol. Prog. Ser. 491: 33-46.

Morse, J. W., A. J. Andersson, and F. T. Mackenzie. 2006. Initial responses of carbonate-rich shelf sediments to rising atmospheric pC[O.sub.2] and "ocean acidification": role of high Mg-calcites. Geochim. Cosmochim. Acta 70: 5814-5830.

Munday, P. L., M. E. Warner, K. Monro, J. M. Pandolfi, and D. J. Marshall. 2013. Predicting evolutionary responses to climate change in the sea. Ecol. Lett. 16: 1488-1500.

Orr, J. C., V. J. Fabry, O. Aumont, L. Bopp, S. C. Doney, R. A. Feely, A. Gnanadesikan, N. Gruber, A. Ishida, F. Joos et al. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686.

Pandolfi, J. M., S. R. Connolly, D. J. Marshall, and A. L. Cohen. 2011. Projecting coral reef futures under global warming and ocean acidification. Science 333: 418-422.

Pochon, X., L. Garcia-Cuetos, A. C. Baker, E. Castella, and J. Pawlowski. 2007. One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in sordid foraminifera. Coral Reefs 26: 867-882.

Poloczanska, E. S., C. J. Brown, W. J. Sydeman, W. Kiessling, S. S. Schoeman, P. J. Moore, K. Brander, J. F. Bruno, L. B. Buckley, M. T. Burrows et al. 2013. Global imprint of climate change on marine life. Nat. Clim. Change 3: 919-925.

Raja, R., P. K. Saraswati, K. Rogers, and K. Iwao. 2005. Magnesium and strontium compositions of recent symbiont-bearing benthic foraminifera. Mar. Micropaleontol. 58: 31-44.

Resig, J. M. 2004. Age and preservation of Amphistegina (foraminifera) in Hawaiian beach sand: implication for sand turnover rate and resource renewal. Mar. Micropaleontol. 50: 225-236.

Reymond, C. E., S. Uthicke, and J. M. Pandolfi. 2011. Inhibited growth in the photosymbiont-bearing foraminifer Marginopora vertebralis from the nearshore Great Barrier Reef, Australia. Mar. Ecol. Prog. Ser. 435: 97-117.

Reymond, C. E., S. Uthicke, and J. M. Pandolfi. 2012. Tropical Foraminifera as indicators of water quality and temperature. In Proceedings of the 12"' International Coral Reef Symposium, Cairns, Australia, 9-13 July 2012, D. Yellowlees and T. P. Hughes, eds. James Cook University, Townsville, Australia.

Reymond, C. E., A. Lloyd, D. I. Kline, S. G. Dove, and J. M. Pandolfi. 2013. Decline in growth of foraminifer Marginopora rossi under eutrophication and ocean acidification scenarios. Glob. Change Biol. 19: 291-302.

Richardson, S. L. 2009. An overview of symbiont bleaching in the epiphytic foraminiferan Sorites dominicensis. Smithson. Contrib. Mar. Sci. 38: 429-436.

Schmidt, C., P. Heinz, M. Kucera, and S. Uthicke. 2011. Temperature-induced stress leads to bleaching in larger benthic foraminifera hosting endosymbiotic diatoms. Limnol. Oceanogr. 56: 1587-1602.

Schmidt, C., M. Kucera, and S. Uthicke. 2014. Combined effects of warming and ocean acidification on coral reef Foraminifera Marginopora vertebralis and Heterostegina depressa. Coral Reefs doi: 10.1007/ S00338-014-1151-4.

Schulz, K. G., J. B. E. Ramos, R. E. Zeebe, and U. Riebesell. 2009. C[O.sub.2] perturbation experiments: similarities and differences between dissolved inorganic carbon and total alkalinity manipulations. Biogeosciences 6: 2145-2153.

Scoffin, T. P., and A. W. Tudhope. 1985. Sedimentary environments of the central region of the Great Barrier Reef of Australia. Coral Reefs 4: 81-93.

Sen Gupta, B. K. 1999. Systematics of modern foraminifera. Pp. 7-36 in Modern Foraminifera, B. K. Sen Gupta, ed. Kluwer Academic, Dordrecht, The Netherlands.

Sinutok, S., R. Hill, M. A. Doblin, R. Wuhrer, and P. J. Ralph. 2011. Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers. Limnol. Oceanogr. 56: 1200-1212.

Smith, D. F., and W. J. Wiebe. 1977. Rates of carbon fixation, organic carbon release and translocation in a reef-building foraminifer, Marginopora vertebralis. Aust. J. Mar. Freshw. Res. 28: 311-319.

Smith, D. J., D. J. Suggett, and N. R. Baker. 2005. Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Glob. Change Biol. 11: 1-11.

Stillman, J. H. 2003. Acclimation capacity underlies susceptibility to climate change. Science 301: 65.

Sunday, J. M., A. E. Bates, and N. K. Dulvy. 2012. Thermal tolerance and the global redistribution of animals. Nat. Clim. Change 2: 686690.

Talge, H. K., and P. Hallock. 2003. Ultrastructural responses in field-bleached and experimentally stressed Amphistegina gibbosa (Class Foraminifera). J. Eukaryot. Microbiol. 50: 324-333.

ter Kuile, B. 1991. Mechanisms for calcification and carbon cycling in algal symbiont-bearing foraminifera. Pp. 73-89 in Biology of Foraminifera, J. J. Lee and O. R. Anderson, eds. Academic Press, London.

ter Kuile, B., J. Erez, and E. Padan. 1989. Mechanisms for the uptake of inorganic carbon by two species of symbiont-bearing foraminifera. Mar. Biol. 103: 241-251.

Uthicke, S., and C. Altenrath. 2010. Water column nutrients control growth and C : N ratios of symbiont-bearing benthic foraminifera on the Great Barrier Reef, Australia. Limnol. Oceanogr. 55: 1681-1696.

Uthicke, S., and K. E. Fabricius. 2012. Productivity gains do not compensate for reduced calcification under near-future ocean acidification in the photosynthetic benthic foraminifer species Marginopora vertebralis. Glob. Change Biol. 18: 2781-2791.

Uthicke, S., N. Vogel, J. Doyle, C. Schmidt, and C. Humphrey. 2012. Interactive effects of climate change and eutrophication on the dinoflagellate-bearing benthic foraminifer Marginopora vertebralis. Coral Reefs 31: 401-414.

Uthicke, S., P. Momigliano, and K. E. Fabricius. 2013. High risk of extinction of benthic foraminifera in this century due to ocean acidification. Sci. Rep. 3: 1769.

van Dam, J. W., A. P. Negri, J. F. Mueller, R. Altenburger, and S. Uthicke. 2012. Additive pressures of elevated sea surface temperatures and herbicides on symbiont-bearing Foraminifera. PloS One 7: e33900.

Venec-Peyre, M. T. 1991. Distribution of living benthic foraminifera on the back-reef and outer slopes of a high island (Moorea, FrenchPolynesia). Coral Reefs 9: 193-203.

Vickerman, K. 1992. The diversity and ecological significance of protozoa. Biodivers. Conserv. 1: 334-341.

Vila-Concejo, A., D. L. Harris, A. M. Shannon, J. M. Webster, and H. E. Power. 2013. Coral reef sediment dynamics: evidence of sand-apron evolution on a daily and decadal scale. J. Coast. Res. 65: 606-611.

Vogel, N., and S. Uthicke. 2012. Calcification and photobiology in symbiont-bearing benthic foraminifera and responses to a high C[O.sub.2] environment. J. Exp. Mar. Biol. Ecol. 424/425: 15-24.

Warner, M. E., W. K. Fitt, and G. W. Schmidt. 1999. Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc. Natl. Acad. Sci. USA 96: 8007-8012.

Yamamoto, S., H. Kayanne, M. Terai, A. Watanabe, K. Kato, A. Negishi, and K. Nozaki. 2012. Threshold of carbonate saturation state determined by C[O.sub.2] control experiment. Biogeosciences 9: 1411-1450.

Yamano, H., T. Miyajima, and I. Koike. 2000. Importance of foraminifera for the formation and maintenance of a coral sand cay: Green Island, Australia. Coral Reefs 19: 51-58.

Zeebe, R. E., and A. Ridgwell. 2011. Past changes of ocean carbonate chemistry. Pp. 21-40 in Ocean Acidification, J.-P. Gattuso and L. Hansson, eds. Oxford University Press, New York.

Ziegler, M., and S. Uthicke. 2011. Photosynthetic plasticity of endosymbionts in larger benthic coral reef Foraminifera. J. Exp. Mar. Biol. Ecol. 407: 70-80.

Zmiri, A., D. Kahan, S. Hochstein, and Z. Reiss. 1974. Phototaxis and thermotaxis in some species of Amphistegina (Foraminifera). J. Protozool. 21: 133-138.

Zohary, T., Z. Reiss, and L. Hottinger. 1980. Population dynamics of Amphisorus hemprichii (Foraminifera) in the Gulf of Elat (Aqaba), Red Sea. Ecologae Geol. Helv. 73: 1071-1094.

STEVE S. DOO (1)*, KAZUHIKO FUJITA (2), MARIA BYRNE (1,3), AND SVEN UTHICKE (4)

(1) School of Biological Sciences, University of Sydney, NSW, Australia; (2) Department of Physics and Earth Sciences, University of the Ryukyus, Okinawa, Japan; (3) School of Medical Sciences, University of Sydney, NSW, Australia; and (4) Australian Institute of Marine Science, Townsville, QLD, Australia

Received 9 December 2013; accepted 15 May 2014.

* To whom correspondence should be addressed. E-mail: steve.doo@ sydney.edu.au

Table 1
Effects of acidification, thermal, and interactive (acidification
and thermal) stress on tropical symbiont-bearing large benthic
foraminifera

                                     Acidification Stress

                              Control
Family                        PH                Significant Effects

Family Alveolinidae
  Alveolinella quoyi          ND                ND

Family Amphisteginidae
  Amphistegina lobifera       ND                No change in elevated
                                                  PC[O.sub.2]
  Amphistegina gibbosa        8.09              No change in elevated
                                                  PC[O.sub.2]
  Amphistegina radiata        8.10-8.13         No change in elevated
                                                  PC[O.sub.2]

Family Calcarinidae
  Baculogypsina sphaerulata   8.16              pH 7.92-7.75,
                                                  Increased
                                                  calcification

  Calcarina gaudichaudii      8.16              pH 7.92-7.75,
                                                  Increased
                                                  calcification

  Calcarina hispida           ND                ND

  Calcarina mayori            ND                ND

Family Nummulitidae
  Heterostegina depressa      8.13              pH 7.48-7.83, no
                                                  change in elevated
                                                  PC[O.sub.2]

Subfamily Soritinae
  Amphisorus hemprichii       8.16              pH 7.92-7.75,
                                                  Decreased
                                                  calcification,
                                                  slight decrease in
                                                  photosynthesis
  Amphisorus kudakajimensis   8.22              pH 7.91, Decreased
                                                  calcification

  Marginopora vertebralis     8.10-8.18         pH 7.95, Decreased
                                                  calcification/
                                                  dissolution in
                                                  elevated
                                                  PC[O.sub.2],
                                                  conflicting
                                                  results observed
                                                  on photosynthesis
  Marginopora rossi           7.98              pH 7.68, Decreased
                                                  calcification with
                                                  elevated
                                                  PC[O.sub.2],
                                                  decreased
                                                  photosyntheis with
                                                  elevated
                                                  PC[O.sub.2]
  Sorties dominicensis        ND                ND

Family Peneroplidae
  Peneroplis sp.              8.1               No change in
                                                  elevated
                                                  PC[O.sub.2]
  Peneroplis planatus                           ND

                                         Thermal Stress

                              Control
Family                        [degrees]C        Significant Effects

Family Alveolinidae
  Alveolinella quoyi          26                32[degrees]C,
                                                  Decreased Fv/Fm

Family Amphisteginidae
  Amphistegina lobifera       ND                ND

  Amphistegina gibbosa        20                32[degrees]C,
                                                  Bleaching
  Amphistegina radiata        23-26             31[degrees]C,
                                                  Reduced Growth &
                                                  Fv/Fm

Family Calcarinidae
  Baculogypsina sphaerulata   25-26             34[degrees]C,
                                                  Decreased RuBiSCO
                                                  expression;
                                                  30[degrees]C,
                                                  maximum
                                                  photosynthesis/
                                                  respiration
  Calcarina gaudichaudii      25                30[degrees]C,
                                                  maximum
                                                  photosynthesis/
                                                  respiration
  Calcarina hispida           23                33[degrees]C,
                                                  Decreased Fv-Fm &
                                                  chi-a
  Calcarina mayori            26                No change in
                                                  elevated
                                                  temperature

Family Nummulitidae
  Heterostegina depressa      23-26             31[degrees]C,
                                                  Decreased Fv-Fm &
                                                  chl-a

Subfamily Soritinae
  Amphisorus hemprichii       ND                ND

  Amphisorus kudakajimensis   25                30[degrees]C,
                                                  maximum
                                                  photosynthesis;
                                                  33[degrees]C
                                                  maximum
                                                  respiration
  Marginopora vertebralis     26                32[degrees]C,
                                                  Dissolution;
                                                  34[degrees]C,
                                                  Decreased Fv/Fm &
                                                  increased
                                                  bleaching 22

  Marginopora rossi           ND                ND

  Sorties dominicensis        28                31[degrees]C,
                                                  Increased
                                                  bleaching

Family Peneroplidae
  Peneroplis sp.              ND                ND

  Peneroplis planatus         26                No change in
                                                  elevated
                                                  temperature

                                Acidification and Thermal Stressors

                              Control pH/
Family                        [degrees]C        Significant Effects

Family Alveolinidae
  Alveolinella quoyi          ND                ND

Family Amphisteginidae
  Amphistegina lobifera       ND                ND

  Amphistegina gibbosa        ND                ND

  Amphistegina radiata        ND                ND

Family Calcarinidae
  Baculogypsina sphaerulata   ND                ND

  Calcarina gaudichaudii      ND                ND

  Calcarina hispida           ND                ND

  Calcarina mayori            ND                ND

Family Nummulitidae
  Heterostegina depressa      8.1/28            7.9-31[degrees]C,
                                                  Decreased Fv-Fm,
                                                  chl-a,
                                                  survivorship

Subfamily Soritinae
  Amphisorus hemprichii       ND                ND

  Amphisorus kudakajimensis   ND                ND

  Marginopora vertebralis     8.1/28            7.9/32[degrees]C,
                                28[degrees]C,     Decreased
                                Decreased         calcification,
                                growth            Fv/Fm, Increased
                                                  dissolution

  Marginopora rossi           ND                ND

  Sorties dominicensis        ND                ND

Family Peneroplidae
  Peneroplis sp.              ND                ND

  Peneroplis planatus         ND                ND

Controls pH and significant effects, if any, are listed for each
species with experimental data available. All pH units were adjusted
to [pH.sub.SW] scale. See Appendixes 2 and 3 for further details of
individual studies. ND represents no data available.

Table 2
Carbonate production on lagoon and reef flats worldwide; only
studies in which entire populations of large benthic foraminifera
present in samples were assessed were included

                 Reef Type/
Sea              Lagoon       Site                 Latitude *

Worldwide        Reef Flat    Worldwide            NA

                 Lagoon       Worldwide            NA

North Pacific    Lagoon       Palau                7[degrees]N

                 Reef         Palau                7[degrees]N

                 Reef         Majuro Atoll,        7[degrees]N
                              Marshall Islands

                 Reef         Kailua Bay, Hawaii   21[degrees]N

                 Reef         O'ahu, Hawaii        21[degrees]N

                 Lagoon       Irabu/Shimoji        25[degrees]N
                              Islands, Japan

                 Reef         Sesoko Island,       27[degrees]N
                              Japan

                 Lagoon       Sesoko Island,       27[degrees]N
                              Japan

South Pacific    Reef         Warraber Island,     10[degrees]S
                              Torres Strait

                 Reef         Raine Reef, GBR      ITS

                 Reef         Green Island, GBR    I6[degrees]S

                 Reef         One Tree Island,     23[degrees]S
                              GBR

                 Reef         Elat                 29[degrees]N

                                               CaC[O.sub.3]
                 Reef Type/   Water depth      (g [m.sup.2]
Sea              Lagoon       (m)               [y.sup.-1])

Worldwide        Reef Flat                     230(30-1000)

                 Lagoon                        30.4(1.2-120)

North Pacific    Lagoon       1-2 m               110-660

                 Reef         1-2 m               60-3000

                 Reef         Intertidal-4 m     0-10,000

                 Reef         Surface-25 m        10-140

                 Reef         2-10 m             100-2800

                 Lagoon       Intertidal-1 m      70-1000

                 Reef         Intertidal-1 m        560

                 Lagoon       Intertidal-1 m       1020

South Pacific    Reef         1-35 m              30-230

                 Reef         Intertidal-1 m       1800

                 Reef         Intertidal-1 m        480

                 Reef         Intertidal           3000

                 Reef         4 m                   400

                                                        Estimation
                 Reef Type/                               Method
Sea              Lagoon       Major Species             ([dagger])

Worldwide        Reef Flat    Reef foraminiferal
                              assemblage

                 Lagoon       Reef foraminiferal
                              assemblage

North Pacific    Lagoon       Amphistegina sp.,             SC
                              Calcarina sp.

                 Reef         Calcarina sp.,                SC
                              Baculogypsina
                              sphaerulata

                 Reef         Calcarina sp.,                SC
                              Amphistegina sp.

                 Reef         Amphistegina lessonii,        GC
                              A. lobifera,
                              Heterostegina depressa
                              ([double dagger])

                 Reef         Amphistegina sp.,             SC
                              Peneroplis sp.

                 Lagoon       Marginopora                   SC
                              (Amphisorus)
                              kudakajimensis

                 Reef         Calcarina gaudichaudii,       SC
                              Baculogypsina
                              sphaerulata, Neorotalia
                              calcar

                 Lagoon       Marginopora                   SC
                              (Amphisorus)
                              kudakajimensis Inferred
                              from Hallock et al.
                              (1981)

South Pacific    Reef         Unknown                       GC

                 Reef         Baculogypsina                 SC
                              sphaerulata,
                              Marginopora
                              vertebralis,
                              Amphistegina lobifera

                 Reef         Calcarina hispida,            SC
                              Baculogypsina
                              sphaerulata,
                              Amphistegina lessonii

                 Reef         Marginopora                   DC
                              vertebralis,
                              Baculogypsina
                              sphaerulata

                 Reef         Amphisorus hemprichii         SC

                 Reef Type/
Sea              Lagoon       Reference

Worldwide        Reef Flat    Langer et al. (1997)

                 Lagoon       Langer et al. (1997)

North Pacific    Lagoon       Hallock (1981)

                 Reef         Hallock (1981)

                 Reef         Fujita et al. (2009)

                 Reef         Harney and Fletcher
                              (2003)

                 Reef         Hamey et al. (1999)

                 Lagoon       Fujita et al. (2000)

                 Reef         Hohenegger (2006)

                 Lagoon       Hohenegger (2006)

South Pacific    Reef         Hart and Kench (2007)

                 Reef         Dawson et al. (in press)

                 Reef         Yamano et al. (2000)

                 Reef         Doo et al. (2012a)

                 Reef         Zohary et al. (1980)

* NA, not applicable.

([dagger]) DC, density counts with remote sensing; GC, gross
carbonate production; SC, season standing crop sampling.

([double dagger]) Inferred from Hallock et al. (1981).
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