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

Reference: Biol. Bull. 226: 169 –186. (June 2014) © 2014 Marine Biological Laboratory

Fate of Calcifying Tropical Symbiont-Bearing Large Benthic Foraminifera: Living Sands in a Changing Ocean STEVE S. DOO1*, KAZUHIKO FUJITA2, MARIA BYRNE1,3, AND SVEN UTHICKE4 School of Biological Sciences, University of Sydney, NSW, Australia; 2Department of Physics and Earth Sciences, University of the Ryukyus, Okinawa, Japan; 3School of Medical Sciences, University of Sydney, NSW, Australia; and 4Australian Institute of Marine Science, Townsville, QLD, Australia

1

acidifying oceans may be due to (1) differences in the carbonate species’ use in formation of the CaCO3 skeleton (CO2 vs. CO32-), (2) varied responses of the symbiont types (diatom, dinoflagellate, rhodophyte) to stressors, or (3) the degree of nutritional dependence of the host to its symbiont. We also summarize current estimates of carbonate production by LBFs to provide a context of their contribution to reefs. Finally, we outline major gaps in knowledge in addressing the potential for LBF species persistence in a changing ocean.

Abstract. Concerns regarding the response of calcifiers in future warmer and more acidic oceans have been raised in many studies. Tropical large benthic foraminifera (LBF) are important carbonate producers that reside in coral reefs worldwide. Similar to corals, these organisms live in symbioses with microalgae, which promote high calcification rates. The contribution of LBFs to reef sediments is under threat due to climate change. In this review, we synthesize research conducted on the effects of increased temperature and acidification on these organisms, and assess the potential impacts on reef carbonate production. A meta-analysis of all available experimental data (18 publications, 84 individual experiments) on the effects of ocean warming and acidification on LBF holobiont health was performed using log-transformed response ratios (LnRR) comparing presentday ambient and projected future scenarios. For the latter, we used Representative Concentration Pathway 8.5 from the Intergovernmental Panel on Climate Change, which projects changes of ⫹4 °C and ⫺0.3 pH units by the year 2100. Overall, a general negative trend on holobiont growth was observed across most species of LBFs in response to both stressors. The only exception was the hyaline species (porous CaCO3 test composed of interlocking microcrystals) that have diatom symbionts. Species in this group appear resilient to future ocean acidification scenarios. Differences in the response of LBF species to warming and

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 CO2 alters seawater carbonate chemistry, leading to more acidic conditions (lower pH) and lower saturation states (⍀) 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; Ho¨nisch et al., 2012). Surface ocean pH has decreased 0.1 pH units since preindustrial times (equivalent to a 30% increase in H⫹ 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

Received 9 December 2013; accepted 15 May 2014. * To whom correspondence should be addressed. E-mail: steve.doo@ sydney.edu.au Abbreviations: GBR, Great Barrier Reef; LBF, large benthic foraminifera; LnRR, log-transformed response ratio; RCP, Representative Concentration Pathway. 169

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2.6 – 4.8 °C under the same projection by the end of the century, with a likely mean increase of 3.7 °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 CaCO3 test composed of interlocking microcrystals) and porcelaneous (non-porous CaCO3 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 lowlying 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 et 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 pCO2 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


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LBFS IN A CHANGING OCEAN Table 1 Effects of acidification, thermal, and interactive (acidification and thermal) stress on tropical symbiont-bearing large benthic foraminifera Acidification Stress

Family Family Alveolinidae Alveolinella quoyi Family Amphisteginidae Amphistegina lobifera

Control pH

Significant Effects

Thermal Stress Control °C

Acidification and Thermal Stressors Control pH/°C

Significant Effects

Significant Effects

ND

ND

26

32°C, Decreased Fv/Fm

ND

ND

ND

No change in elevated pCO2 No change in elevated pCO2 No change in elevated pCO2

ND

ND

ND

ND

20

32°C, Bleaching

ND

ND

23–26

31°C, Reduced Growth & Fv/Fm

ND

ND

8.16

pH 7.92–7.75, Increased calcification

25–26

ND

ND

Calcarina gaudichaudii

8.16

25

ND

ND

Calcarina hispida

ND

pH 7.92–7.75, Increased calcification ND

ND

ND

Calcarina mayori

ND

ND

26

34°C, Decreased RuBiSCO expression; 30°C, maximum photosynthesis/ respiration 30°C, maximum photosynthesis/respiration 33°C, Decreased Fv/Fm & chl-a No change in elevated temperature

ND

ND

Family Nummulitidae Heterostegina depressa

8.13

pH 7.48–7.83, no change in elevated pCO2

23–26

31°C, Decreased Fv/Fm & chl-a

8.1/28

7.9/31°C, Decreased Fv/Fm, chl-a, survivorship

Subfamily Soritinae Amphisorus hemprichii

8.16

pH 7.92–7.75, Decreased calcification, slight decrease in photosynthesis pH 7.91, Decreased calcification

ND

ND

ND

ND

25

30°C, maximum photosynthesis; 33°C maximum respiration 32°C, Dissolution; 34°C, Decreased Fv/Fm & increased bleaching

ND

ND

8.1/28

7.9/32°C, Decreased calcification, Fv/ Fm, Increased dissolution

22

ND

Amphistegina gibbosa

8.09

Amphistegina radiata

8.10–8.13

Family Calcarinidae Baculogypsina sphaerulata

Amphisorus kudakajimensis

8.22

Marginopora vertebralis

8.10–8.18

Marginopora rossi

7.98

Sorties dominicensis Family Peneroplidae Peneroplis sp.

ND

Peneroplis planatus

8.1

pH 7.95, Decreased calcification/dissolution in elevated pCO2, conflicting results observed on photosynthesis

23

26

pH 7.68, Decreased calcification with elevated pCO2, decreased photosyntheis with elevated pCO2 ND

ND

ND

28°C, Decreased growth ND

28

31°C, Increased bleaching

ND

ND

No change in elevated pCO2 ND

ND

ND

ND

ND

26

No change in elevated temperature

ND

ND

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


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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 °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 CO2-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 pCO2 directly in an incubator (McIntyre-Wressnig et al., 2013). Of these approaches, bubbling CO2-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 CO2 seeps, where pCO2 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 CO2 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 pHNBS 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 pCO2 seawater (1169 and 1662 ppm/pHTotal 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; McIntyreWressnig et al., 2013). In pCO2 levels ranging from 300 to 1000 ␮atm (pHTotal 8.17–7.76), calcification of Baculogypsina sphaerulata and Calcarina gaudichaudii, measured as growth of asexually reproduced juveniles, increased with elevated pCO2 (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 pCO2 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, pCO2 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 pCO2 of 2000 ppmv (pHTotal ⬃7.5), seen by scanning electron microscopy (McIntyre-Wressnig et al., 2013). Shell


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LBFS IN A CHANGING OCEAN

Calcification/Growth Responses

Mean Effect Size (LnRR) Acidification Scenarios

1

*

*

-0.5

All Forams (n=25)

Dinoflagellate/ Porcelaneous forams (n=13)

Diatom/ Hyaline forams (n=12)

-1

1

C

0.5

All Forams (n=15)



D

0.5

*

0

-0.5

-1

*

0

-0.5

0

B

0.5

0

1

Mean Effect Size (LnRR) Warming Scenarios

1

A

0.5

-1

Photosymbiont Responses

*

*

-0.5

All Forams (n=6)



-1 All Forams (n=38)

Dinoflagellate/ Diatom/ Porcelaneous Porcelaneous forams (n=8) forams (n=1)

Diatom/ Rhodophyte Hyaline forams (n=1) forams (n=29)

Figure 1. Mean effect of near-future ocean acidification effects on (A) calcification/growth response and (B) photosymbiont responses (e.g., Fv/Fm, chl-a) in tropical symbiont-bearing large benthic foraminifera (LBFs). The mean effect of warming on (C) LBF calcification/growth and (D) photosymbiont physiology. Data were compiled from 84 studies from 18 manuscripts and used estimates of acidification and warming for year 2100 based on Representative Concentration Pathway 8.5 (IPCC, 2013) (see Appendix 1). Significance is determined with 95% confidence intervals that do not cross zero and is denoted with an asterisk (*). Individual studies are denoted in parenthesis. Studies to the right of vertical dashed line are separated into photosymbiont and shell microstructure and are combined left of the vertical dashed line.

surfaces of Amphistegina sp. also dissolved in seawater with less extreme conditions (pCO2 444 ␮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 CaCO3 test from changes in seawater chemistry (Erez, 2003). On the other hand, porcela-

neous 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 pCO2 (higher pH) seawater than are hyaline foraminifers.


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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 pCO2 (lowering pH) in volcanic CO2 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 (Enrı´quez 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 (pHTotal 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 O2 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 LBFs 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. For instance, Hikami et al. (2011), using these techniques, concluded that carbonate ion affected growth of Amphisorus hemprichii (porcelaneous foraminifer), while the CO2 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 (CO32⫺ vs. CO2) and the type of symbiotic algae (diatom vs. dinoflagellate). Calcification of porcelaneous taxa may decrease in acidification conditions because more CO2 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 pCO2 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 CO2 (Fujita 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 CaCO3 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


LBFS IN A CHANGING OCEAN

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 al., 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 °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 ratelimiting enzyme) at ⫹8 °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 °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 °C (Fujita et al., 2014). In that study, optimal photosynthesis and respiration was observed at about 5 °C greater than mean seawater temperature for all species, reflecting acclimation to life in thermally variable environ-

175

ments (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 mayori, 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 shortterm 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 °C (⫹6 °C above ambient) for 3 weeks (Doo et al., 2012a). Decreased oxygen production was observed with elevated temperatures (⫹4 °C above ambient) for M. vertebralis after longerterm exposure (Uthicke and Fabricius, 2012). Amphistegina gibbosa cultured in elevated temperatures (⫹12 °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 °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 °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


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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). Amphistegina 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 °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 °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 (CaCO3) in the Majuro Atoll is up to 10,000 g m⫺2 y⫺1 (Fujita et al., 2009), with a world-wide average of 230 g m⫺2 y⫺1 (Langer et al., 1997). At Green Island, GBR, up to 30% of CaCO3 formed is composed of LBF tests (Yamano et al., 2000; Table 2). Other emergent


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LBFS IN A CHANGING OCEAN 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

Sea

Reef Type/ Lagoon

Worldwide

Reef Flat Lagoon North Pacific Lagoon Reef

Site

Latitude*

Water depth (m)

CaCO3 (g m2 y–1)

Worldwide Worldwide Palau Palau

NA NA 7°N 7°N

1–2 m 1–2 m

Majuro Atoll, Marshall Islands Kailua Bay, Hawaii

7°N

Intertidal-4 m

0–10,000

21°N

Surface-25 m

10–140

O’ahu, Hawaii Irabu/Shimoji Islands, Japan Sesoko Island, Japan

21°N 25°N

2–10 m Intertidal-1 m

100–2800 70–1000

27°N

Intertidal-1 m

560

Sesoko Island, Japan

27°N

Intertidal-1 m

1020

10°S

1–35 m

Reef

Warraber Island, Torres Strait Raine Reef, GBR

11°S

Intertidal-1 m

1800

Reef

Green Island, GBR

16°S

Intertidal-1 m

480

Reef

One Tree Island, GBR Elat

23°S

Intertidal

29°N

4m

Reef Reef Reef Lagoon Reef Lagoon

South Pacific Reef

Reef

230 (30–1000) 30.4 (1.2–120) 110–660 60–3000

30–230

3000 400

Estimation Method†

Major Species Reef foraminiferal assemblage Reef foraminiferal assemblage Amphistegina sp., Calcarina sp. Calcarina sp., Baculogypsina sphaerulata Calcarina sp., Amphistegina sp.

Reference

SC SC

Langer et al. (1997) Langer et al. (1997) Hallock (1981) Hallock (1981)

SC

Fujita et al. (2009)

Amphistegina lessonii, A. lobifera, Heterostegina depressa‡ Amphistegina sp., Peneroplis sp. Marginopora (Amphisorus) kudakajimensis Calcarina gaudichaudii, Baculogypsina sphaerulata, Neorotalia calcar Marginopora (Amphisorus) kudakajimensis Inferred from Hallock et al. (1981)

GC SC SC

Harney and Fletcher (2003) Harney et al. (1999) Fujita et al. (2000)

SC

Hohenegger (2006)

SC

Hohenegger (2006)

Unknown

GC

Hart and Kench (2007)

Baculogypsina sphaerulata, Marginopora vertebralis, Amphistegina lobifera Calcarina hispida, Baculogypsina sphaerulata, Amphistegina lessonii Marginopora vertebralis, Baculogypsina sphaerulata Amphisorus hemprichii

SC

Dawson et al. (in press)

SC

Yamano et al. (2000)

DC

Doo et al. (2012a)

SC

Zohary et al. (1980)

* NA, not applicable. † DC, density counts with remote sensing; GC, gross carbonate production; SC, season standing crop sampling. ‡ Inferred from Hallock et al. (1981).

reef platforms have smaller contributions of LBFs ranging from 2% to 8% in studies of reef systems across the IndoPacific (Ve´nec-Peyre´, 1991; Harney and Fletcher, 2003; Hart and Kench, 2007). Reefs in Palau have been documented to produce an excess of 3000 g m⫺2 y⫺1 CaCO3 (Hallock, 1981), while at a high-latitude reef at Sesoko Island, Japan, production is 560 g m⫺2 y⫺1 (Hohenegger, 2006). Foraminifera that live as epiphytes on algal-dominated reef platforms along the GBR produce a large amount of CaCO3, with LBF production at One Tree Reef estimated to be 3000 g m⫺2 y⫺1 (Doo et al., 2012a), and at Raine Island Reef to be 1800 g m⫺2 y⫺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⫺2 y⫺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⫺2 y⫺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


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the need for further work on LBFs and, in particular, multistressor 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 be 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. 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.

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181

LBFS IN A CHANGING OCEAN 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 °C), and acidification (⫺0.3 pH unit or 960 ppm). Shell Wall Type*

Hyaline

Porcelaneous

Foraminifera

Porcelaneous

Hyaline Porcelaneous

Hyaline

Control Mean

Treatment Mean

Effect Size

Marginopora vertebralis Marginopora rossi

A. OCEAN ACIDIFICATION EFFECTS ON CALCIFICATION Growth rate (% surface area) 0.350 0.390 0.108 Growth rate (% surface area d⫺1) 0.175 0.216 0.211 Final shell weight (alpha population) 16.260 15.270 ⫺0.063 Final shell weight (beta population) 14.580 14.310 ⫺0.019 Final diameter (alpha population) 298.000 297.000 ⫺0.003 Final diameter (beta population) 283.500 285.000 0.005 Final shell weight (alpha population) 40.855 32.190 ⫺0.238 Final shell weight (beta population) 39.660 37.380 ⫺0.059 Final diameter (alpha population) 358.250 355.000 ⫺0.009 Final diameter (beta population) 368.000 372.250 0.011 Final shell weight 20.954 26.295 0.227 Growth rate (% surface area d⫺1) 0.186 0.168 ⫺0.102 Growth rate (% surface area d⫺1) 0.394 0.331 ⫺0.173 Final shell weight (alpha population) 40.460 36.360 ⫺0.107 Final shell weight (beta population) 65.150 57.630 ⫺0.123 Final diameter (alpha population) 626.750 631.750 0.008 Final diameter (beta population) 759.750 704.250 ⫺0.076 Final shell diameter 0.580 0.510 ⫺0.129 Final shell weight 27.600 14.000 ⫺0.679 Final shell weight 41.276 35.415 ⫺0.153 Growth rate (% surface area d⫺1) 0.052 0.047 ⫺0.109 Alkalinity anomaly (% dry wt. d⫺1) 0.438 0.269 ⫺0.489 in Fig. 3a Alkalinity anomaly (% dry wt. d⫺1) 0.472 0.395 ⫺0.178 in Fig. 3b Growth rate (% surface area d⫺1) 0.075 0.111 0.398 Growth rate (% surface area d⫺1) 0.740 0.320 ⫺0.838

Amphistegina radiata Amphistegina radiata Heterostegina depressa Heterostegina depressa Heterostegina depressa Heterostegina depressa Heterostegina depressa Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Marginopora rossi

B. OCEAN ACIDIFICATION EFFECTS ON PHOTOBIOLOGY chl-a 142.625 160.085 0.115 Fv/Fm 0.671 0.625 ⫺0.071 chl-a 215.525 220.511 0.023 Fv/Fm 0.702 0.669 ⫺0.048 Oxygen production 0.079 0.066 ⫺0.184 chl-a 0.161 0.156 ⫺0.031 Oxygen production 0.021 0.006 ⫺1.223 chl-a 198.244 228.769 0.143 Fv/Fm 0.637 0.635 ⫺0.003 Oxygen production 0.071 0.090 0.239 Oxygen production in Fig 1C ⫺0.566 0.288 Oxygen production in Fig 1D 0.259 0.554 0.761 Oxygen production in Fig 1F 0.644 1.099 0.535 chl-a 0.165 0.153 ⫺0.077 Oxygen production 0.012 0.013 0.107 Oxygen production 3.640 1.780 ⫺0.715

Amphistegina radiata Heterostegina depressa Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis

Growth Growth Growth Growth Growth Growth

Amphistegina gibbosa Amphistegina radiata Baculogypsina sphaerulata Baculogypsina sphaerulata Baculogypsina sphaerulata Baculogypsina sphaerulata Calcarina gaudichaudii Calcarina gaudichaudii Calcarina gaudichaudii Calcarina gaudichaudii Calcarina gaudichaudii Heterostegina depressa Heterostegina depressa Amphisorus hemprichii Amphisorus hemprichii Amphisorus hemprichii Amphisorus hemprichii Amphisorus kudakajmensis Amphisorus kudakajmensis Amphisorus kudakajmensis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis

Hyaline

Measurements Made

Amphistegina Amphistegina Amphistegina Amphistegina Amphistegina

gibbosa radiata radiata radiata radiata

C. OCEAN WARMING EFFECTS ON CALCIFICATION rate (% surface area) 0.072 0.042 ⫺0.538 rate (% surface area) 0.394 0.303 ⫺0.262 rate (% surface area) 1.601 0.765 ⫺0.739 rate (% surface area) 2.540 2.290 ⫺0.104 rate (% surface area) 0.010 0.008 ⫺0.243 rate (% surface area) 0.075 0.080 0.076 D. OCEAN WARMING EFFECTS ON PHOTOBIOLOGY % Healthy (1-bleached) 0.880 0.780 ⫺0.121 Fv/Fm 0.742 0.741 0.000 Fv/Fm 0.735 0.727 ⫺0.010 Fv/Fm 0.699 0.707 0.011 chl-a 126.000 143.937 0.133

Treatment Group

Reference

1000 ppm 1169 ppm 970 ppm 970 ppm 970 ppm 970 ppm 970 ppm 970 ppm 970 ppm 970 ppm 907 ppm 1169 ppm pH 7.9 970 ppm 970 ppm 970 ppm 970 ppm pH 7.7 pH 7.7 907 ppm 1169 ppm pH 7.57

McIntyre-Wressnig et al. (2013) Vogel and Uthicke (2012) Fujita et al. (2011) Fujita et al. (2011) Fujita et al. (2011) Fujita et al. (2011) Fujita et al. (2011) Fujita et al. (2011) Fujita et al. (2011) Fujita et al. (2011) Hikami et al. (2011) Vogel and Uthicke (2012) Schmidt et al. (in press) Fujita et al. (2011) Fujita et al. (2011) Fujita et al. (2011) Fujita et al. (2011) Kuroyanagi et al. (2009) Kuroyanagi et al. (2009) Hikami et al. (2011) Vogel and Uthicke (2012) Uthicke and Fabricius (2012)

pH 7.65

Uthicke and Fabricius (2012)

pH 7.9 pH 7.6– 7.7

Schmidt et al. (in press) Reymond et al. (2013)

1169 ppm 1169 ppm 1169 ppm 1169 ppm 1307 ppm pH 7.9 pH 7.9 1169 ppm 1169 ppm 1307 ppm pH 7.55 pH 7.74 pH 7.75 pH 7.9 pH 7.9 pH 7.6– 7.7

Vogel and Uthicke (2012) Vogel and Uthicke (2012) Vogel and Uthicke (2012) Vogel and Uthicke (2012) Vogel and Uthicke (2012) Schmidt et al. (in press) Schmidt et al. (in press) Vogel and Uthicke (2012) Vogel and Uthicke (2012) Vogel and Uthicke (2012) Uthicke and Fabricius (2012) Uthicke and Fabricius (2012) Uthicke and Fabricius (2012) Schmidt et al. (in press) Schmidt et al. (in press) Reymond et al. (2013)

⫹5°C ⫹3°C ⫹4°C ⫹6°C ⫹3°C ⫹3°C

Schmidt et al. (2011) Schmidt et al. (in press) Doo et al. (2012a) Reymond et al. (2011) Uthicke et al. (2012) Schmidt et al. (in press)

⫹5°C ⫹5°C ⫹5°C ⫹5°C ⫹5°C

Talge and Hallock (2003) Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011)


182

S. S. DOO ET AL. Appendix 1 (Continued)

Shell Wall Type*

Porcelaneous

Foraminifera Amphistegina radiata Amphistegina radiata Amphistegina radiata Amphistegina radiata Baculogypsina sphaerulata Baculogypsina sphaerulata Calcarina gaudichaudii Calcarina hispida Calcarina hispida Calcarina mayori Calcarina mayori Calcarina mayori Heterostegina depressa Heterostegina depressa Heterostegina depressa Heterostegina depressa Heterostegina depressa Heterostegina depressa Heterostegina depressa Heterostegina depressa Heterostegina depressa Heterostegina depressa Heterostegina depressa Heterostegina depressa Alveolinella quoyi Marginopora kudakajimensis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Marginopora vertebralis Peneroplis planatus

Control Mean

Treatment Mean

Effect Size

Treatment Group

chl-a chl-a Fv/Fm chl-a RuBisCO expression Oxygen production Oxygen production Fv/Fm chl-a Fv/Fm chl-a Fv/Fm in Figure 3B Fv/Fm Fv/Fm Fv/Fm chl-a chl-a chl-a Fv/Fm chl-a Fv/Fm in Figure 3A chl-a chl-a Oxygen production Fv/Fm in Figure 3C Oxygen production

146.302 106.068 0.658 126.984 1.480 1.820 1.590 0.801 137.058 0.708 174.850 0.697 0.717 0.749 0.731 113.000 101.880 95.512 0.696 109.724 0.732 159.093 0.161 0.021 0.761 2.710

163.281 94.682 0.646 82.374 1.430 2.570 2.210 0.792 159.176 0.707 146.534 0.704 0.709 0.754 0.731 105.200 104.957 91.691 0.633 33.905 0.722 123.268 0.076 0.004 0.753 3.190

0.110 ⫺0.114 ⫺0.019 ⫺0.433 ⫺0.034 0.345 0.329 ⫺0.012 0.150 ⫺0.001 ⫺0.177 0.010 ⫺0.011 0.006 0.001 ⫺0.072 0.030 ⫺0.041 ⫺0.094 ⫺1.174 ⫺0.014 ⫺0.255 ⫺0.758 ⫺1.618 ⫺0.011 0.163

⫹5°C ⫹5°C ⫹5°C ⫹5°C ⫹4°C ⫹5°C ⫹5°C ⫹5°C ⫹5°C ⫹5°C ⫹5°C ⫹4°C ⫹5°C ⫹5°C ⫹5°C ⫹5°C ⫹5°C ⫹5°C ⫹5°C ⫹5°C ⫹4°C ⫹4°C ⫹3°C ⫹3°C ⫹4°C ⫹5°C

Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011) Doo et al. (2012) Fujita et al. (2014) Fujita et al. (2014) Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011) van Dam et al. (2012) Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011) Schmidt et al. (2011) van Dam et al. (2012) van Dam et al. (2012) Schmidt et al. (in press) Schmidt et al. (in press) van Dam et al. (2012) Fujita et al. (2014)

Fv/Fm in Figure 3D Fv/Fm in Figure 3E chl-a chl-a Oxygen production chl-a Oxygen production Fv/Fm in Figure 3F

0.688 0.732 214.637 0.165 0.518 0.165 0.012 0.588

0.681 0.698 135.322 0.142 0.514 0.042 0.007 0.566

⫺0.010 ⫺0.048 ⫺0.461 ⫺0.152 ⫺0.008 ⫺1.365 ⫺0.557 ⫺0.038

⫹4°C ⫹4°C ⫹4°C ⫹3°C ⫹3°C ⫹3°C ⫹3°C ⫹4°C

van Dam et al. (2012) van Dam et al. (2012) van Dam et al. (2012) Uthicke et al. (2012) Uthicke et al. (2012) Schmidt et al. (in press) Schmidt et al. (in press) van Dam et al. (2012)

Measurements Made

Reference

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


183

LBFS IN A CHANGING OCEAN 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

Shell Wall Type* Hyaline

Foraminifera Amphistegina lobifera Amphistegina gibbosa Amphistegina radiata

Experimental Design†

Laboratory/closed system/ bottle Laboratory/closed system/ incubator Laboratory/flow-through system Laboratory/semi-closed circulation system Baculogypsina Laboratory/flow-through sphaerulata system/AICAL Calcarina Laboratory/flow-through gaudichaudii system/AICAL Laboratory/flow-through system/AICAL Heterostegina Laboratory/flow-through depressa system Laboratory/semi-closed circulation system Laboratory/flow-through system Porcelaneous Amphisorus Laboratory/closed system/ hemprichii bottle Laboratory/flow-through system/AICAL Amphisorus Laboratory/closed system/ kudakajmensis bottle Laboratory/flow-through system/AICAL Marginopora Laboratory/recirculated vertebralis system/two-factors (temp) Laboratory/flow-through system Field & on board/at CO2 vent, Papua New Guinea Laboratory/closed system/ vials Laboratory/semi-closed circulation system Laboratory/flow-through system Marginopora Laboratory/closed system/ rossi two-factors (nutrient) Peneroplis sp. Laboratory/semi-closed circulation system

Duration

Light Condition (␮mol m⫺2 s⫺1; L:D cycle)

Temperature and Salinity (°C; psu)

2 days

750; 13:11h

26–28: ND

6 weeks

11; 12:12h

25; 38–40

6 weeks

8–12: ND

Carbonate Chemistry Manipulation Acid/base

pCO2 Range (␮atm) ND

pH Range (scale) 6.0–9.6 (NBS)

Omega Calcite ND

TA‡ (␮mol kg⫺1) ND

DIC¶ (␮mol kg⫺1) ND

Atmospheric CO2 aerated 27.2–27.5: ND CO2 bubbling

385–2000 ppmv 7.56–8.10 (total)

1.84–6.36 2480–2624 2100–2517

467–1662

7.66–8.14 (total)

1.8–4.8

7.60–8.22 (NBS) 1.90–6.52 2617–2709 2343–2603

2280–2282 1999–2192

25.9–26.0: ND CO2 bubbling

432–2151

12 weeks 60; 12:12h

27.5; 34.4

CO2 bubbling

261–972

7.76–8.17 (total)

2.7–6.4

2188

1796–2043

12 weeks 60; 12:12h

27.5; 34.4

CO2 bubbling

261–972

7.76–8.17 (total)

2.7–6.4

2188

1796–2043

4 weeks

100; 12:12h

27.1; 34.1

CO2 bubbling

245–907

7.76–8.23 (total)

2.9–6.8

2224

1821–2075

6 weeks

8–12: ND


467–1662

7.66–8.14 (total)

1.8–4.8

2280–2282 1999–2192

4 days

30: ND

4 days

30: ND


432–2151

7.60–8.22 (NBS) 1.90–6.52 2617–2709 2343–2603

35 days

10–17; 12:12h


479–738

8.15–7.98 (NBS) 3.8–5.1

2232–2235 2031–2134

2 days

750; 13:11h

26–28: ND

Acid/base

ND

6.0–9.6 (NBS?)

ND

ND

ND

7.76–8.17 (total)

2.7–6.4

2188

1796–2043

12 weeks 60; 12:12h

27.5; 34.4

CO2 bubbling

261–972

10 weeks 190; 12:12h

25: ND

Acid/base

ND

7.7–8.3 (NBS)

ND

ND

ND

4 weeks

100; 12:12h

27.1; 34.1

CO2 bubbling

245–907

7.76–8.23 (total)

2.9–6.8

2224

1821–2075

5 weeks

300; 12:12h

28–34; 33

CO2 bubbling

33.2–262 Pa

7.4–8.1 (NBS)

1.84–8.02 2314–2827 1923–2749

6 weeks

29–34: ND


467–1662

7.66–8.14 (total)

1.8–4.8

1 day

2–12: ND

27.4–29.9; 33.2–35.7

7.07–8.19 (total)

0.40–5.92 2239–2619 1926–2919

1 day

2–12: ND

333–2314

7.43–8.17 (total)

1.35–6.41 2103–2335 1841–2296

4 days

30: ND

25.7–29.3; CO2 bubbling 31.5–35.2 25.9–26.0: ND CO2 bubbling

432–2151

7.60–8.22 (NBS) 1.90–6.52 2617–2709 2343–2603 8.15–7.98 (NBS) 3.8–5.1

Natural CO2 seeps 373–12105

2280–2282 1999–2192

53 days

38–45; 12:12h


479–738

2232–2235 2031–2134

35 days

45–50; 12:12h

25; 35

CO2 bubbling

252–1048

7.6–8.1 (NBS)

4 days

30: ND

25.9–26.0

CO2 bubbling

432–2151

7.60–8.22 (NBS) 1.90–6.52 2617–2709 2343–2603

1.91–5.38 2036–2075 1960–2140

* The symbionts of all hyaline species listed here are pennate diatoms; those of all porcelaneous species are dinoflagellates. † AICAL, a Japanese system; Acidification Impacts on Calcifiers. ‡ TA, total alkalinity. ¶ DIC, dissolved organic carbon. Appendix 2, Continued


184

S. S. DOO ET AL. Appendix 2 (Continued) B. CALCIFICATION AND PHOTOSYNTHESIS PARAMETERS AND FINDINGS Measurement Methods of Calcification

Foraminifera Amphistegina lobifera Amphistegina gibbosa

Amphistegina radiata

Baculogypsina sphaerulata Calcarina gaudichaudii

Heterostegina depressa

Amphisorus hemprichii



14

C tracer technique (␮g C mg foram⫺1 2d⫺1) Growth rate (% surface area)

Growth rate (% surface area d⫺1) Ca2⫹ microsensor Final shell weight and diameter Final shell weight and diameter Final shell weight Growth rate (% surface area d⫺1) Ca2⫹ microsensor Growth rate (% surface area d⫺1) 14 C tracer technique (␮g C mg foram⫺1 2d⫺1) Final shell weight and diameter Final shell weight and diameter, number of chambers Final shell weight Buoyant weight technique (mg CaCO3 d⫺1)

Growth rate (% surface area d⫺1) Not measured Alkalinity anomaly techinique (% dry wt. d⫺1) Ca2⫹ microsensor

Marginopora rossi

Growth rate (% surface area d⫺1) Growth rate (% surface area d⫺1)

Peneroplis sp.

Ca2⫹ microsensor

Calcification

Measurement Methods of Photosynthesis C tracer technique (␮g C mg foram⫺1 2d⫺1)

Decrease with elevated pCO2

14

No change but partial dissolution of shell surfaces at 2000 ppmv No change with elevated pCO2 No change with elevated pCO2 Increase with elevated pCO2 Increase with elevated pCO2 Increase with elevated pCO2 No change with elevated pCO2 No change with elevated pCO2 Decrease with elevated pCO2 Decrease with elevated pCO2

Not measured

Decrease with elevated pCO2 Decrease with elevated pCO2 Decrease with elevated pCO2 Decrease (dissolution) with elevated pCO2 and / or high temperature Increased rates with elevated pCO2

Fv/Fm, chl-a

No change but partial Slight decrease with elevated pCO2

Reference ter Kuile et al. (1989)

McIntyre-Wressnig et al. (2013)

Vogel and Uthicke (2012) Glas et al. (2012)

Not measured

No change with elevated pCO2 No change with elevated pCO2 –

Not measured

–


Not measured

–

Hikami et al. (2011)

O2 microsensor

Fv/Fm, O2 production (␮g O2 h⫺1 mg (ww)⫺1) O2 microsensor


No change with elevated pCO2 No change with elevated pCO2 No change with elevated pCO2 Slight decrease with elevated pCO2

Vogel and Uthicke (2012) Glas et al. (2012)

Not measured

–


Not measured

–

Kuroyanagi et al. (2009)

Not measured

–

Hikami et al. (2011)

Fv/Fm, O2 production (␮g O2 h⫺1 mg (ww)⫺1) 14 C tracer technique (␮g C mg foram⫺1 2d⫺1)

Schmidt et al., in press ter Kuile et al. (1989)

Fv/Fm, O2 production (␮mol O2 L⫺1)

Decrease with elevated pCO2 and/or high temp.

Sinutok et al. (2011)

Fv/Fm, O2 production (␮g O2 h⫺1 mg (ww)⫺1) O2 production (␮g O2 mm⫺2 d⫺1) O2 production (␮g O2 mm⫺2 d⫺1)

No change with elevated pCO2 Increase with elevated pCO2 Increase with elevated pCO2

Vogel et al. (2012)

No change with elevated pCO2 No change with elevated pCO2 Decrease with elevated pCO2

O2 microsensor

Glas et al. (2012)

No change with elevated pCO2

O2 microsensor

No change with elevated pCO2 No change with elevated pCO2 Decrease with elevated pCO2; no effects of nutrients No change with elevated pCO2

Decrease with elevated pCO2

Fv/Fm, O2 production (␮g O2 h⫺1 mg (ww)⫺1) O2 production (␮mol O2 g⫺2 h⫺1)

Uthicke and Fabricius (2012) Uthicke and Fabricius (2012)

Schmidt et al. (2014) Reymond et al.,(2013)

Glas et al. (2012)

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


185

LBFS IN A CHANGING OCEAN 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 Type* Hyaline

Foraminifera Amphistegina gibbosa Amphistegina radiata

Baculogypsina sphaerulata

Calcarina gaudichaudii Calcarina hispida Calcarina mayori


Porcelaneous

Alveolinella quoyi Amphisorus kudakajimensis Sorties dominicensis Marginopora vertebralis

Peneroplis planatus

Experimental Design

Duration

Light Condition (␮mol m⫺2 s⫺1)

Temperature Range (°C)

Laboratory/closed system/ incubator Laboratory/closed system/ bottle Laboratory/flow-through Laboratory/closed system/ bottle Laboratory/closed system/ bottle Laboratory/closed system/ bottle Laboratory/closed system/ bottle Laboratory/flow-through Laboratory/closed system/ incubator Laboratory/closed system/ bottle Laboratory/flow-through Laboratory/closed system/ incubator Laboratory/flow-through Laboratory/closed system/ incubator Laboratory/closed system/ bottle Field-based study Laboratory/closed system/ bottle Laboratory/closed system/ bottle Laboratory/closed system/ incubator Laboratory/flow-through Laboratory/closed system/ incubator

5 weeks

6⫺15

20–32

6 days

11–15

23–33

30 days 5 hours

200 250

26–31 26–34

1 day

100

5–45

1 day

100

5–45

6 days

11–15

23–33

30 days 96 hours

200 10

26–31 26–34

6 days

11–15

23–33

30 days 96 hours

200 10

26–31 26–34

35 days 96 hours

8–12 10

28–31 26–34

1 day

100

5–45

2 days 3 weeks

ND 150

28–31 26–32

6 weeks

6–9

22–28

96 hours

10

26–34

53 days 96 hours

45–50 10

28–31 26–34

* 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. Appendix 3, Continued


186

S. S. DOO ET AL. Appendix 3 (Continued) B. CALCIFICATION AND PHOTOSYNTHESIS PARAMETERS AND FINDINGS

Foraminifera Amphistegina gibbosa Amphistegina radiata

Measurement Methods of Calcification

Calcification

Measurement Methods of Photosynthesis

Not measured

–

Growth rate (% surface area d⫺1) Not measured

Decreased growth at elevated temperature –

Not measured

–

Calcarina gaudichaudii

Not measured

–

O2 production (␮g O2 h⫺1 mg (ww)⫺1)

Calcarina hispida

Not measured

–

Fv/Fm, chl-a

Calcarina mayori

Not measured

–

Fv/Fm, chl-a

Not measured

–

Fv/Fm

Not measured

–

Fv/Fm, chl-a

Not measured

–

Fv/Fm, chl-a

Not measured

–

Fv/Fm, visual observation of bleaching


Decreased growth with elevated temperature –

Fv/Fm, chl-a, O2 production (␮g O2 h⫺1 mg (ww)⫺1) Fv/Fm


Not measured

–

O2 production (␮g O2 h⫺1 mg (ww)⫺1)

Sorties dominicensis

Not measured

–


Growth rate (% surface area d⫺1)

Decrease growth (dissolution) with elevated temperature Decreased growth with elevated temperature –

Visual observation of bleaching Not measured

Baculogypsina sphaerulata


Alveolinella quoyi


Peneroplis planatus


Decreased growth with elevated temperature

Histological observation of bleaching Fv/Fm, chl-a

Western blotting, RuBisCO enzyme O2 production (␮g O2 h⫺1 mg (ww)⫺1)

Not measured

Fv/Fm, visual observation of bleaching

Fv/Fm, chl-a, O2 production (␮g O2 h⫺1 mg (ww)⫺1) Fv/Fm

Photosynthesis Bleaching with elevated temperature Decreased Fv/Fm and chl-a at increased temperature Decreased with elevated temperature Increased with mild (⫹5°C) elevated temperature Increased with mild (⫹5°C) elevated temperature Decreased Fv/Fm and chl-a at increased temperature No signifcant effect with temperature Decreased Fv/Fm at elevated temperature Decreased Fv/Fm and chl-a at increased temperature Decreased Fv/Fm and chl-a at increased temperature Decreased Fv/Fm and increased bleaching with elevated temperature Decreased Fv/Fm and chl-a, O2 production at increased temperature Decreased Fv/Fm at elevated temperature Increased with mild (⫹5°C) elevated temperature Bleaching with elevated temperature –

–

Decreased Fv/Fm and increased bleaching with elevated temperature Decreased Fv/Fm and chl-a, O2 production at increased temperature No change by elevated pCO2

Reference Talge and Hallock (2003) Schmidt et al. (2011)

Doo et al. (2012b) Fujita et al. (2014)


Schmidt et al. (2011)

Schmidt et al. (2011) van Dam et al. (2012) Schmidt et al. (2011)

Schmidt et al. (2011)

van Dam et al. (2012)

Schmidt et al. (in press)

van Dam et al. (2012) Fujita et al. (2014)

Richardson (2009) Doo et al. (2012a)

Reymond et al. (2011)

van Dam et al. (2012)

Schmidt et al. (in press)

Glas et al. (2012)


Variation in sensitivity of large benthic Foraminifera to the combined effects of ocean warming and local impacts.

A survey of benthic assemblages of foraminifera in tropical coastal waters of pulau pinang, malaysia.

Recruitment and Succession in a Tropical Benthic Community in Response to In-Situ Ocean Acidification.

Phylogeography of the tropical planktonic foraminifera lineage globigerinella reveals isolation inconsistent with passive dispersal by ocean currents.

Calcifying species sensitivity distributions for ocean acidification.

A decline in benthic foraminifera following the deepwater horizon event in the northeastern Gulf of Mexico.

Evolutionary potential in a changing ocean.

Extremely heat tolerant photo-symbiosis in a shallow marine benthic foraminifera.

Large retroperitoneal calcifying fibrous tumor.

PALEOBIOLOGICAL APPLICATIONS OF THREE-DIMENSIONAL BIOMETRY ON LARGER BENTHIC FORAMINIFERA: A NEW ROUTE OF DISCOVERIES.

Coral calcifying fluid pH dictates response to ocean acidification.

Responses of benthic foraminifera to the 2011 oil spill in the Bohai Sea, PR China.

Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera.

Distributions and biomass of benthic ciliates, foraminifera and amoeboid protists in marine, brackish, and freshwater sediments.

Reprogramming cell fate: a changing story.

Growth and calcification of marine bryozoans in a changing ocean.

Surviving anoxia in marine sediments: The metabolic response of ubiquitous benthic foraminifera (Ammonia tepida).

Perspectives on massive coral growth rates in a changing ocean.

Seaweed fails to prevent ocean acidification impact on foraminifera along a shallow-water CO2 gradient.

Rewiring Host Lipid Metabolism by Large Viruses Determines the Fate of Emiliania huxleyi, a Bloom-Forming Alga in the Ocean.

Molecular evidence for Lessepsian invasion of soritids (larger symbiont bearing benthic foraminifera).

Correction: A Decline in Benthic Foraminifera following the Deepwater Horizon Event in the Northeastern Gulf of Mexico.

A New Integrated Approach to Taxonomy: The Fusion of Molecular and Morphological Systematics with Type Material in Benthic Foraminifera.

A hierarchical classification of benthic biodiversity and assessment of protected areas in the Southern Ocean.