Bull Mar Sci. 91(2):271–290. 2015 coral reef paper http://dx.doi.org/10.5343/bms.2014.1045
Ocean acidification enhances the bioerosion of a common coral reef sponge: implications for the persistence of the Florida Reef Tract
1 Cooperative Institute for Ian C Enochs 1, 2 * Marine and Atmospheric Derek P Manzello 2 Studies, Rosenstiel School of 1, 2 Marine & Atmospheric Science, Renee D Carlton University of Miami, 4600 Danielle M Graham 3 Rickenbacker Causeway, Miami, 4 Florida 33149. Rob Ruzicka Michael A Colella 4 2 Atlantic Oceanographic and Meteorological Laboratories (AOML), NOAA, 4301 Rickenbacker Causeway, Miami, ABSTRACT.—The increase in anthropogenic carbon Florida 33149. dioxide in seawater, termed ocean acidification (OA), 3 University of Miami, Coral depresses calcification rates of coral and algae, and may Gables, Florida 33124. contribute toward reef ecosystem degradation. To test how 4 Fish and Wildlife Research future OA conditions will influence biologically-mediated Institute, 100 8th Ave SE, St. dissolution (bioerosion) of coral by the common Caribbean Petersburg, Florida 33701. boring sponge Pione lampa (de Laubenfels, 1950), we * Corresponding author email: conducted a series of carefully controlled incubations and
model showed that all FRT reefs had a positive CaCO3 budget [mean = 8.257 (SE 0.8077) kg m−2 yr−1] in preindustrial times, whereas approximately 89% of reefs presently exhibit net erosion. Present-day reef-specific calcification would need to increase by 29.4% to compensate for projected end of the century OA-enhancement of total bioerosion. These findings Date Submitted: 17 June, 2014. show that OA may accelerate Caribbean and Atlantic coral Date Accepted: 5 January, 2015. reef degradation more rapidly than previously predicted. Available Online: 23 January, 2015.
Increasing atmospheric CO2 as a result of burning fossil fuels is well known to have far reaching ramifications for the world’s climate, ultimately influencing economies and ecosystems alike (IPCC 2007a). Recently scientists have focused attention on the uptake of this CO2 by the world’s oceans, a process that leads to a decrease in seawater pH and a reduction in the saturation state of calcium carbonate (Kleypas et al. 1999). This phenomenon, termed ocean acidification (OA), is currently occurring at a rate faster than in the past 300 million years (Hönisch et al. 2012). At its current pace, OA will detrimentally affect numerous marine ecosystems, among them coral reefs (Hoegh-Guldberg et al. 2007). Bulletin of Marine Science 271 OA © 2015 Rosenstiel School of Marine & Atmospheric Science of the University of Miami Open access content 272 Bulletin of Marine Science. Vol 91, No 2. 2015
Coral reefs are ecologically and economically important. They are hotspots of biodiversity and productivity, providing valuable services through tourism, fishing, and breakwater protection (Moberg and Folke 1999). Many functions of a coral reef are ultimately related to its three-dimensional structure that is the net result of the additive process of calcification and the subtractive process of erosion. While the primary reef builders are scleractinian corals, bioeroding taxa are highly diverse, including fishes, urchins, sponges, cyanobacteria, algae, fungi, bivalves, crustaceans, and worms (Glynn 1997). OA is projected to depress the calcification rates of scleractinian corals (Langdon and Atkinson 2005) and crustose coralline algae (CCA; Johnson and Carpenter 2012). This could potentially shift the calcification/erosion balance away from growth, lead- ing to habitat loss and a decline in ecosystem function (Alvarez-Filip et al. 2009). Emerging evidence suggests that OA will also increase bioerosion rates, causing a more rapid decline in reef structure than previously anticipated. OA has been shown to accelerate the erosive capabilities of a Pacific species of zooxanthellate sponge (Wisshak et al. 2012, Fang et al. 2013) and Pacific endolithic algae (Tribollet et al. 2009, Reyes-Nivia et al. 2013), as well as a temperate shell-boring Atlantic sponge species (Duckworth and Peterson 2013, Wisshak et al. 2014). Moreover, Stubler et al. (2014) have shown that OA can alter the net calcification of living coral/sponge pairs. These studies have used a variety of techniques including image analysis (surface area), mass loss, and chemical incubations (alkalinity anomaly) to evaluate changes in erosion rate with high CO2, sometimes in concert with temperature stress. Sponge bioerosion occurs as a result of the combined processes of chemical dis- solution and mechanical erosion. Dissolution is thought to take place at the cellular level, carving small (15–85 µm) convex chips that are subsequently ejected through the exhalent canals of the sponge (Pomponi 1980, Zundelevich et al. 2007). Carbonic anhydrase (CA) plays an important role in sponge-mediated dissolution and works by catalyzing the hydration of CO2, producing hydrogen ions and bicarbonate (Hatch 1980, Ehrlich et al. 2009). Several mechanisms have been proposed for how CA activity facilitates erosion, including the transport of hydrogen ions to the site of dissolution, exchange of bicarbonate for hydrogen ions, and/or pH optimization of additional enzymes and chelating agents (Hatch 1980, Ehrlich et al. 2009). The increase in dissolved seawater CO2 results in a greater concentration of hydrogen and bicarbonate ions and could thereby enhance chemical dissolution (Chétail and Fournié 1969). The degree to which chemical dissolution contributes to total sponge erosion is not well understood. Early work, including studies performed on Pione lampa (de Laubenfels, 1950), used microscopy to investigate the mechanics of sponge erosion and estimated that chemical dissolution accounts for only 2%–10% of total bioero- sion (Warburton 1958, Cobb 1969, Rützler and Rieger 1973). Recent work has inde- pendently quantified both erosional components in the congeneric Pione cf. vastifica (Hancock, 1849) and estimated that chemical dissolution was responsible for approx- imately 76% of total erosion (Zundelevich et al. 2007). Additionally, measurements by Fang et al. (2013) on Cliona orientalis Thiele, 1900 are consistent with the hypothesis that a high proportion of total erosion is chemical (40%) and that proportion in- creased to 66% under experimentally elevated CO2 and temperature. Regardless of the relative contribution, the positive relationship between OA and chemical erosion is likely to lead to enhanced total erosion of reef substrate. Enochs et al.: Acidification enhances bioerosion and impacts Florida Reef ractT 273
Basic research on the bioerosion rates of various taxa and the potential influ- ence of changing climate and ocean chemistry is increasingly important given the large-scale degradation of coral reefs (e.g., Gardner et al. 2003). A comprehensive approach to modeling reef frameworks has been successfully applied to Caribbean reefs whereby taxon-specific rates of calcification and erosion are combined into a single vector of reef persistence (Perry et al. 2012, 2013). This modeling suggests that recent degradation has resulted in a large number of Caribbean reefs currently exist- ing near or in a net erosional state. Model predictions are based on present-day con- ditions and do not account for the dynamic nature of calcification and bioerosion, which will be strongly affected by global change. To this end, Kennedy et al. (2013) modeled the impact of multiple stressors (warming, OA, eutrophication, disease, fishing) on the carbonate budget of a hypothetical Caribbean reef system and found that climate change scenarios will likely have strong impacts on Caribbean reef per- sistence. Their models showed that reefs with lower coral cover are more susceptible to those stressors influencing erosion. Understanding how OA will influence erosion is therefore of paramount importance in the Caribbean region, where live coral cover has declined by approximately 80% since the 1970s and the present CaCO3 produc- tion is roughly 50% below historical averages (Gardner et al. 2003, Perry et al. 2013). Furthermore, the magnitude of change in calcium carbonate saturation state due to OA in the Caribbean region will be among the highest globally (Friedrich et al. 2012), which could make OA-related bioerosion enhancement more pronounced than in other regions. Despite these concerns, we are unaware of any research on the response of
Caribbean bioeroding taxa to high CO2 independent of living host corals or sym- bionts. Additionally, there have not been any studies that have explored how the expected changes in both calcification and bioerosion from acidification will alter real-world Caribbean reef systems. Therefore, we first completed an experiment on the response of the common boring sponge P. lampa to elevated CO2, comprising multiple short-term incubations (<24 hrs) to understand how biologically-mediated chemical dissolution responded to elevated CO2. Second, to explore the implications of this OA-accelerated bioerosion for the Florida Reef Tract (FRT), we applied these data to a carbonate budget model of 37 reefs from four reef regions. Across these reefs, we compared present-day and preindustrial conditions to five different future scenarios: (1) enhanced bioerosion; (2) depressed calcification; (3) enhanced bioero- sion and depressed calcification; (4) reduction in coral cover; (5) enhanced bioerosion and depressed calcification, as well as a reduction in coral cover. We hypothesize that elevated seawater CO2 will enhance the chemical dissolution of P. lampa and that OA-accelerated bioerosion will negatively impact the carbonate budget of the FRT. Our study represents the first time an OA-bioerosion experiment has been per- formed on a tropical coral reef species without the added influence of symbionts or co-occurring stressors, as well as the first time that OA-altered bioerosion rates have been applied to carbonate budget models parameterized with real-world benthic data to examine the implications for habitat persistence.
Methods
Chemical Dissolution Incubations.—Fragments of coral rock infested with P. lampa (Fig. 1) were collected using a hammer and chisel at Cheeca Rocks, an inshore 274 Bulletin of Marine Science. Vol 91, No 2. 2015
Figure 1. Bioerosion of the boring sponge Pione lampa. (A) Pione lampa (orange) eroding coral rock at a patch reef in the Florida Reef Tract. (B) Three-dimensional micro-computed tomogra- phy scan of an eroded coral skeleton showing transverse slices of the eroded surface and undis- turbed skeleton underneath. (C) Vertical cross-section of Pione lampa tissues penetrating into a coral skeleton. patch reef in the upper Florida Keys (24.90°N, 80.62°W). Fragments were collected from three to six colonies to enhance genetic diversity. The mean volume of sponge/ rock fragments was 96 (SE 14) cm3 and sponge tissue was observed to penetrate roughly 1 cm into the accompanying coral rock substrate. Sponges were collected in autumn of 2012 and were allowed to acclimate to laboratory conditions for approxi- mately 3 wks before experimental procedures were conducted. While not subjected to incubations, specimens were maintained in semi-recirculating 150 L tanks, which were maintained at 25 °C and received 4.5 L hr−1 fresh seawater. Sponges were fed weekly with Roti-Rich liquid invertebrate food. Biologically-mediated chemical dissolution was investigated using a modified al- kalinity anomaly methodology, wherein controlled system alkalinity is exclusively affected by CaCO3 precipitation and dissolution (Zundelevich et al. 2007). The pres- ent study consisted of 12 individual P. lampa fragments that were each subjected to four CO2 treatments ranging from present-day conditions to those expected by the end of the century (+0, +200, +400, and +600 ppm), comprising a grand total of 48 separate experimental incubations (Fig. 2). Bioerosion rates of boring sponges are highly variable among colonies, as is the skeletal density of the coral skeleton pen- etrated (Neumann 1966, Rützler 1975, Highsmith 1981, Schönberg 2002). Because each fragment was exposed to each of the CO2 treatments, a repeated measures anal- ysis of variance (ANOVA) was employed to test significance while accounting for the potentially high inter-colony variability among individual P. lampa fragments. Additionally, 16 control block incubations were conducted on clean/unbored car- bonate skeleton to account for potential abiotic dissolution or changes in alkalinity due to evaporation. Dead coral blocks were of similar volume [mean = 61 (SE 8) cm3] to the sponge fragments and were baked and thoroughly rinsed with fresh water Enochs et al.: Acidification enhances bioerosion and impacts Florida Reef ractT 275
Figure 2. (A) Experimental design showing the samples sizes, individual sponge replicates and dead coral block controls, the order of treatments, as well as the duration between treatments and experimental rounds. (B) The incubation setup showing the method of treatment gas mixing and delivery, as well as the equipment used for the alkalinity incubations. a, air compressor, b, mass flow controller, c, flow meter and valved controller, d, compressed CO2 gas, e, incubation cham- ber, f, temperature controlled water bath, g, sample for incubation (sponge or control block), h, elevated stand and stir bar, i, stir plate. to ensure they were free of foreign material. Blocks were thoroughly soaked before the initial incubations and were maintained in the same semi-recirculating seawater tanks as the P. lampa while not subject to incubations. Each control block was visu- ally inspected before incubation and cleaned of biota, though little to none was ob- served. Two rounds of incubations were conducted (separated by 15 d), each with the four randomly-ordered and sequential CO2 treatments (+0, +200, +400, +600 ppm). Within each experimental treatment, eight incubation chambers containing one fragment each—six sponge/coral fragments and two dead coral control blocks—were subjected to one CO2 level for approximately 22 hrs. Following 24 hrs of acclima- tion between treatments, the same fragments were subjected to a different, randomly chosen CO2 treatment; this occurred until all CO2 treatments were applied, each over an approximate 22-hr period (Fig. 2A). Incubations were conducted in covered acrylic chambers, maintained at 25 °C with a water bath (Fig. 2B). Treatment gases were mixed using mass flow controllers and bubbled into chambers at 0.2 L min−1 using mechanical flow controllers. Gas entered/ exited the closed chambers through bulkhead fittings to control air-water exchange and minimize evaporation. Pione lampa is azooxanthellate and incubations were run under dark conditions to minimize the possible influence of photosynthetic or- ganisms (e.g., endolithic algae) on water chemistry. Holding tanks were also kept in darkened conditions to reduce fouling and minimize the growth of endolithic algae within experimental replicates and controls. All plugs were visually examined before, during, and after the experiment and neither endo- or epilithic algae were observed. Prior to each experimental run, an 8-L reservoir of seawater was vigorously bubbled −1 (4.0 L min ) with the CO2 treatment gas to reach equilibrium. A sample of the source water was preserved using mercuric chloride, stored in CO2-impermeable borosili- cate bottles, and subsequently analyzed for total alkalinity (TA) and dissolved in- organic carbon (DIC) using Apollo SciTech instruments (DIC analyzer, model no. 276 Bulletin of Marine Science. Vol 91, No 2. 2015
AS-C3; TA analyzer, model no. AS-ALK2). Incubations began after each of the eight chambers were filled with 0.5 L of treatment water and one each of six P. lampa frag- ments and two clean coral rock controls. Incubations were halted after roughly 22 hrs, at which point temperature and salinity were measured and a water sample was fixed with mercuric chloride and reserved for analysis of TA. Chemical dissolution rates due exclusively to sponge erosion were calculated as the difference in TA between water in each experimental sponge chamber and the mean TA of water in control chambers after each incubation. This can be expressed mathematically as follows:
TA(Control Incubation) = TA(Initial) + ΔTA(Abiotic Dissolution) + ΔTA(Evaporation)
TA(Sponge Incubation) = TA(Initial) + ΔTA(Sponge Dissolution) + ΔTA(Abiotic Dissolution) + ΔTA(Evaporation)
Therefore,
ΔTA(Sponge Dissolution) = TA(Sponge Incubation) − TA(Control Incubation)
It is noted that this equation assumes that abiotic/bacterial dissolution occurring on the dead calcium carbonate in our controls is equivalent to that in our experimen- tal replicates. We feel that this is a reasonable assumption given that both skeletons were maintained in the same seawater tanks, that the aragonite saturation state was never recorded to fall below 1, and that bacterial dissolution is likely negligible com- pared to sponge-permeated rock (Bissett et al. 2011). In fact, TA changes in control incubations after salinity standardization were <5% of the average sponge-induced TA flux, showing that abiotic and bacterial dissolution of the control fragments was very low. Previous incubation studies (e.g., Zundelevich et al. 2007) have measured TA flux- es as TAFinal − TAInitial in a single volume of water. While this may be suitable for completely closed systems, given that gas exchange due to bubbling throughout the duration of the experiment could theoretically alter TA via evaporation, we calculat- ed the biologically-mediated dissolution (ΔTA) as the difference between the TA of water incubated with the sponge and that incubated in the bubbled clean coral rock controls. This procedure therefore eliminated complications that would arise from changes in TA associated with evaporation as the TA flux due to non-sponge sources is subtracted from the total TA with the sponge. Changes in salinity, however, were small over the duration of the incubations. The mass of calcium carbonate dissolved was calculated as follows and was adapt- ed from Zundelevich et al. (2007):
−1 M(CaCO3) = 0.5 (mol eq ) × ΔTA × 100 × VSW × ρSW
M is the mass of CaCO3, ΔTA is the difference in TA between sponges and controls −1 after the experiment in eq kg , 100 is the molecular mass of CaCO3, VSW is the vol- ume of water in the incubation (0.5 L), and ρSW is the approximate density of seawater (1.028 kg L−1). Dissolution was standardized to time and to the outer surface area of the P. lampa on each of the fragments, measured after the experiment with a 3D scanner (HDI Advance, 3D3 Solutions, Online Supplementary Fig. 1A). Rates were Enochs et al.: Acidification enhances bioerosion and impacts Florida Reef ractT 277 square-root transformed and tested using a repeated-measures ANOVA. Posthoc rate comparisons were performed using the Holm-Sidak method (Holm 1979). Nutrient concentrations were not assessed during these incubations. While par- ticular nutrients are known to influence alkalinity, they have been previously shown to be of low concentration in our source water (e.g., Caccia and Boyer 2005) and of minimal importance in boring sponge incubations of longer duration (Wisshak et al. 2012, 2014). For example, even if the maximum phosphate concentrations reported in Wisshak et al. (2014) are assumed to have been produced entirely by the sponges in our incubations, the influence on total alkalinity would still be <2 μmol kg−1 during the entire 22 hrs of incubation.
Florida Reef Tract Model.—To estimate how the CaCO3 budget of the FRT will change with OA, we used the rates of erosion and calcification presented by Perry et al. (2012) as a present-day baseline and combined our data on the response of P. lam- pa to increasing CO2 with projected OA-related changes reported in the literature for other taxa (corals, Langdon and Atkinson 2005; CCA, Johnson and Carpenter 2012; endolithic algae, Tribollet et al. 2009). Data sources are summarized in Table 1. Benthic data and boring sponge cover for 37 reefs along the FRT were obtained from the Coral Reef Evaluation and Monitoring Project (CREMP 2014). Individual reefs were divided into four distinct reef regions: Dry Tortugas; Upper Keys; Middle Keys; and Lower Keys. This division follows the long-standing characterization of this re- gion based on differing reef development as discussed in Manzello et al. (2012). Preindustrial, present-day, and five different future scenarios were evaluated: Scenario 1, no change in coral cover, no change in calcification, increase in bioero- sion; Scenario 2, no change in coral cover, reduction in calcification, no change in bioerosion; Scenario 3, no change in coral cover, reduction in calcification, increase in bioerosion; Scenario 4, 50% decrease in coral cover, no change in calcification, no change in bioerosion; Scenario 5, 50% reduction in coral cover, reduction in calcifica- tion, increase in bioerosion.
Preindustrial scenarios were parameterized with an atmospheric CO2 concentra- tion of 280 ppm (IPCC 2007b) and future scenarios were parameterized with 750 ppm, similar to IPCC predictions for the end of the century (e.g., IPCC model A1B). As historical records of coral cover are difficult to come by, we conservatively use the estimate of Gardner et al. (2003) for the Caribbean region in the 1970s and pa- rameterized each reef as having 50% coral cover. We assume a direct and inverse relationship between coral cover and bare substrate. When coral cover was increased from present levels in our model (preindustrial), bare substrate was lowered accord- ingly, and when coral cover was lowered (Scenarios 4,5), bare substrate was increased accordingly. In the preindustrial model, where the calculated increase in coral cov- er was greater than the site-specific amount of bare substrate, bare substrate was constrained to zero rather than an artificial negative value. The Perry et al. (2012) model calculates the bioerosion of endolithic algae as a function of bare substrate; therefore, changes in live coral cover altered algal erosion as well. Boring sponge percent cover data were collected in 2009 and all other benthic data were collected in 2010, both by CREMP. Present-day species-specific coral calcification rates as well as multi-species averages for CCA calcification, sponge bioerosion, and endolithic algae bioerosion were obtained from Perry et al. (2012). These rates were multiplied by present-day benthic cover to calculate present mean calcification and bioerosion 278 Bulletin of Marine Science. Vol 91, No 2. 2015
Table 1. Model parameters utilized in Florida Reef Tract model including the geographic region from which the data were collected, as well as the source of the data. CREMP, Coral Reef Evaluation and Monitoring Project; AGRRA, Atlantic and Gulf Rapid Reef Assessment.
Model parameter Geographic region Reference Corals Cover Florida Keys CREMP Calcification (present day) Atlantic/Caribbean Perry et al. 2012 Calcification (OA-alteration) Pacific, generalized Langdon and Atkinson 2005 CCA Cover Florida Keys CREMP Calcification (present day) Generalized Perry et al. 2012 Calcification (OA-alteration) Pacific Johnson and Carpenter 2012 Boring sponges Cover Florida Keys CREMP Dissolution (present day) Generalized Perry et al. 2012 Dissolution (OA-alteration) Florida Keys Present study Endolithic algae Cover Florida Keys CREMP Dissolution (present day) Atlantic/Caribbean Perry et al. 2012 Dissolution (OA-alteration) Pacific Tribollet et al. 2009 Parrotfishes Abundance and size distribution Florida Keys AGRRA Size-specific grazing rates Atlantic/Caribbean Perry et al. 2012 rates from sponges and endolithic algae. Predicted changes in bioerosion and calcifi- cation rate were calculated at 280 ppm for the preindustrial scenario, at 390 ppm for present-day, and at 750 ppm for use in future scenarios. Rates of bioerosion measured in the field are often different to those measured in controlled laboratory environments (Neumann 1966) and heterogeneous substrates in the reef environment can influence boring rates (Highsmith 1981, Schönberg 2002). For these reasons, in our model we use generalized present-day erosion rates compiled by Perry et al. (2012) and applied percent changes calculated from our study and from previous literature (Table 1). Proportional increases in endolithic algae erosion rates were calculated for the aforementioned CO2 scenarios using a regression of previously published rates (Tribollet et al. 2009). Percent change in sponge chemical erosion was determined from a linear regression of the +0 to +400 ppm chemical sponge dissolution treatments in our study (approximately 500 to 900 2 µatm seawater pCO2, respectively, R = 0.9426) and calculation of the erosion rate at modeled carbonate chemistry parameters (i.e., 280, 390, 750 ppm). To convert per- cent increase in chemical erosion reported here to change in total erosion needed to parameterize our model, we conservatively assumed no increase in mechanical ero- sion (Wisshak et al. 2012). Recent direct enumeration of both chemical and mechani- cal erosion rates have resulted in various estimates for the percent contribution of chemical dissolution to total erosion rate. Zundelevich et al. (2007) measured a 76% chemical contribution for the congeneric P. cf. vastifica. We prefered to use the more conservative rate of 40% published by Fang et al. (2013). Therefore, for our model, we applied only our measured changes in OA-accelerated chemical dissolution to this proportion of total erosion and kept the rest constant. Enochs et al.: Acidification enhances bioerosion and impacts Florida Reef ractT 279
Table 2. Summary of water chemistry information from incubation experiment. Initial conditions for Pione lampa incubations and chemical erosion rates expressed as alkalinity shifts and grams of CaCO3 chemically eroded. Round 2 was conducted several weeks after round 1, contributing to the reduced rate in erosion in round two vs one. ΔTA -1 -2 −1 −2 −1 in µmol kg cm hr . ΔCaCO3 in μg cm d . DIC = dissolved inorganic carbon, TA = total alkalinity, Temp = Temperature, Sal = Salinity. SE in parentheses.
Initial conditions Chemical erosion
+CO2 DIC TA Temp pCO2 pH −1 −1 (ppm) (µmol kg ) (µmol kg ) (°C) Salinity (µatm) (total) Ωarag ΔTA ΔCaCO3 +0 2,202.3 2,484.1 25 35.83 517.0 7.977 3.27 4.93 (1.33) 126.8 (34.1) +200 2,232.5 2,458.2 25 36.35 676.5 7.873 2.68 5.69 (2.06) 146.3 (53.0) +400 2,292.7 2,470.3 25 35.82 873.1 7.781 2.24 6.83 (2.48) 175.5 (63.7) Round 1 +600 2,331.4 2,492.5 25 35.79 972.5 7.743 2.09 6.08 (2.01) 156.2 (51.6)
+0 2,131.4 2,412.0 25 37.08 506.3 7.970 3.17 1.03 (0.17) 26.4 (4.3) +200 2,224.0 2,471.8 25 36.24 609.8 7.914 2.91 1.76 (0.35) 45.3 (9.0) +400 2,259.0 2,452.2 25 36.78 808.7 7.805 2.35 2.11 (0.35) 54.2 (9.0) Round 2 +600 2,318.0 2,477.8 25 37.32 1,004.8 7.725 2.04 1.59 (0.13) 40.9 (3.4)
To estimate how coral calcification rate would change on the FRT from present- day to preindustrial 280 ppm and future 750 ppm scenarios, we calculated propor- tional changes in coral calcification using the first-order rate reaction and expected changes in Ωarag (Langdon and Atkinson 2005). We used temperature, salinity, TA, and pCO2 data collected from FRT offshore reef sites (2009–2011, n = 45 bottle sam- ples, Manzello et al. 2012) to calculate Ωarag. We assumed the addition of 1 ppm at- mospheric CO2 equals roughly 1 µatm seawater pCO2, and calculated the carbonate system by holding everything constant, subtracting 110 µatm for the preindustrial scenario, and adding 360 µatm to present-day 390 µatm for future scenarios. Percent changes in CCA calcification under all scenarios were calculated from a linear re- gression of data from Johnson and Carpenter (2012). Mean parrotfish erosion rates per reef region were calculated from Atlantic and Gulf Rapid Reef Assessment (AGRRA) abundance data applied to species and size- specific bioerosion rate equations presented by Perry et al. (2012). The minimum and maximum sizes used for binning fish size-classes were different for the AGRRA and Perry et al. (2012) approaches. Therefore, to apply the AGRRA data to the Perry et al. (2012) calculations, the mean size of each AGRRA size-class was used to identify the corresponding Perry et al. (2012) size-class. Net calcium carbonate flux was calcu- lated by subtracting bioerosion rates from calcification rates.
Results
Water chemistry and TA fluxes during incubations are given in Table 2. High
CO2 exposures caused increased bioerosion (Fig. 3, repeated measures ANOVA: P < 0.001). The highest incremental increase [mean = 66.0 (SE 20.6) to 95.8 (SE 29.8) −2 −1 μg CaCO3 cm d ) in chemical dissolution was observed at the 643 µatm treatment, after the addition of +200 ppm CO2. The highest overall rates [114.8 (SE 35.7) μg −2 −1 CaCO3 cm d ] were observed in 841 µatm water during the +400 ppm treatment
(Fig. 3, Table 2). At this CO2 treatment, roughly analogous to a conservative predic- tion for the end of the century (IPCC 2007b), chemical dissolution rates were 99% higher than those calculated for present-day levels. This percent increase in erosion is more than twice the predicted decline in calcification over the same CO2 increase 280 Bulletin of Marine Science. Vol 91, No 2. 2015
Figure 3. Mean chemical dissolution rates (SE) of P. lampa fragments under four CO2 scenarios from short-term incubation experiments. Values that do not share a letter are significantly differ- ent. Curve represents second order polynomial fit to the mean bioerosion rates for each treatment (y = 0005x2 + 0.8271x – 226, R2 = 0.9947).
(approximately 48%, Langdon and Atkinson 2005). Chemical erosion at the highest −2 −1 treatment levels (988.7 µatm, +600 ppm) were less [98.6 (SE 30.2) μg CaCO3 cm d ] than at the previous treatment level. According to the predictions of our model, these data equated to an increase in total erosion rate of 40% at 750 ppm and a decrease of 12% from present to pre- industrial times (280 ppm). Data from Langdon and Atkinson (2005) were used to calculate a 27% increase in calcification from present-day to the preindustrial era and a 48% reduction in calcification from present-day to future scenarios (750 ppm). The decline in CCA calcification (−11%) in future scenarios was taken from Johnson and Carpenter (2012) and calculation of a preindustrial rate via linear regression revealed an increase in calcification of 3%. Our regression of data from Tribollet et al. (2009) predicted a 15% decrease in endolithic algae erosion from present-day to preindus- trial and a 49% increase from present-day to future model scenarios. When we applied our data on changes in the chemical erosion rate of P. lampa along with previously reported responses of endolithic bioeroders and calcifiers (Table 1) to benthic cover from the FRT (Table 3), we found that OA levels associ- ated with an atmospheric CO2 concentration of 750 ppm would alter the balance of calcification and erosion (Fig. 4A). The projected enhancement of sponge and -en dolithic algae bioerosion increased the number of net erosional reefs. The mean net −2 −1 accretion changed by −0.067 kg CaCO3 m yr , 5.0% lower than the present-day −2 −1 mean of −1.341 kg CaCO3 m yr (Present vs Scenario 1; Fig. 4B, Table 4). The mean reef-specific calcification would have to increase by 29.4% (SE 6.7) just to offset the increase in total erosion, but only 0.7% (SE 0.5) to offset the increase in sponge ero- sion projected for 750 ppm. A 50% reduction in coral cover had the greatest influence of any single parameter, reducing net calcification by 27.8% to −1.714 (SE 0.0836) kg −2 −1 CaCO3 m yr (Present vs Scenario 4; Fig. 4B, Table 4). A reduction in calcification projected to occur at 750 ppm resulted in a reduction in net ecosystem calcification −2 −1 of 26.0% to −1.690 (SE 0.1358) kg CaCO3 m yr , even if present-day levels of coral cover are maintained (Present vs Scenario 2; Fig. 4B, Table 4). When expected calcifi- cation declines and erosion increases are combined, mean net reef accretion declines Enochs et al.: Acidification enhances bioerosion and impacts Florida Reef ractT 281
Figure 4. Responses of coral reefs to OA. (A) Mean change in bioerosion and calcification rate (SE) due to OA for 37 reefs in the Florida Keys. (B) Calcification (light gray), sponge and endo- lithic algae bioerosion (black) and mean net reef accretion including parrotfish erosion (gray) for the same 37 reefs (SE). Bold values are numbers of positively accreting reefs. Preindustrial, Present, Sc. 1, no change (nc) in coral cover, no change in calcification, increase in bioerosion; Sc. 2, no change in coral cover, reduction in calcification, no change in bioerosion; Sc. 3, no change in coral cover, reduction in calcification, increase in bioerosion; Sc. 4, 50% reduction in coral cover, no change in calcification, no change in bioerosion; Sc. 5, 50% reduction in coral cover, reduction in calcification, increase in bioerosion. by 31.0% throughout the Florida Keys to a net erosional state of −1.757 (SE 0.0875) −2 −1 kg CaCO3 m yr (Present vs Scenario 3; Fig. 4B, Table 4). When a 50% reduction in coral cover is incorporated into the model, net reef accretion declines 46% relative to present, resulting in a net erosional state of −1.959 (SE 0.0679) kg m−2 yr−1 (Present vs Scenario 5; Fig. 4B, Table 4). With the exception of Scenario 1, with three positively accreting reefs, none of the future scenarios had a single coral reef that was actively accreting, whereas presently we calculated four to have positive growth. According to our calculations for preindustrial reefs, mean net accretion across the FRT was 8.257 (SE 0.8076) kg m−2 yr−1 (Fig. 4B, Table 4) with all of the 37 considered reefs positively accreting. Of the four regions within the FRT that we examined, all were presently net ero- sional, when averaged across all considered reefs (Table 4). The Dry Tortugas had the highest coral cover, relatively lower percent cover of both bare substrate and bor- ing sponges, as well as the lowest parrotfish erosion rates (Table 3), resulting in the lowest mean net erosion and the greatest resistance to future alteration of its car- bonate budget (Table 4). The Lower Keys, despite having the second highest coral cover among regions, had the highest present-day erosion rates owing to abundant parrotfish populations, high boring-sponge cover and a large amount of bare sub- strate (Tables 3, 4). The Middle Keys, which have the lowest coral cover and highest percentage of bare substrate, had low parrotfish erosion rates and, according to our model, were the second most stable of the four considered reef regions (Tables 3, 4). The Upper Keys had the second lowest coral cover, lowest percent cover of boring sponges, and parrotfish erosion rates were comparable to that in the Lower Keys (Table 3). This resulted in the second most negative net carbonate budget calculated for present-day reef regions in our study (Table 4). 282 Bulletin of Marine Science. Vol 91, No 2. 2015 Scenario 5 −2.211 (0.0569) −2.211 −1.224 (0.1419) −2.140 (0.0801) −1.507 (0.0334) −1.959 (0.0679) Scenario 4 −0.935 (0.2403) −1.952 (0.1061) −1.882 (0.1422) −1.321 (0.0585) −1.714 (0.0836) Scenario 3 −0.949 (0.266) −1.380 (0.064) −1.995 (0.1147) −1.921 (0.1533) −1.757 (0.0875) Scenario 2 −1.626 (0.1132) −0.476 (0.2554) −1.160 (0.0622) −1.537 (0.1499) −1.408 (0.0863) Scenario 1 −1.306 (0.1175) −1.925 (0.2155) −0.902 (0.4793) −1.858 (0.2838) −1.690 (0.1358) , standard error in parentheses) as calculated by subtracting boring sponge, endolithic algae, and parrotfish erosion Present −1 yr −1.087 (0.1158) −1.556 (0.2144) −0.428 (0.4686) −1.474 (0.2806) −1.341 (0.1346) −2 Preindustrial 6.848 (1.3168) 9.094 (2.3068) 8.705 (1.4016) 8.257 (0.8077) 10.203 (1.7825) Middle Keys Lower Keys Dry Tortugas Upper Keys from coral and crustose coralline algae (CCA) calcification. Net accretion calculated at preindustrial levels, present-day conditions, as well as five potential future potential five as well as conditions, present-day levels, preindustrial at calculated accretion Net calcification. (CCA) algae coralline crustose and coral from scenarios: Scenario 1, no change in coral no cover, change in calcification, increase in endolithic bioerosion (both sponge and algae); Scenario 2, no change bioerosion; in increase in calcification, in reduction cover, coral in change no 3, Scenario bioerosion; endolithic in change no calcification, in reduction cover, coral calcification, in reduction cover, coral in reduction 50% 5, Scenario bioerosion; in change no calcification, in change no cover, coral in reduction 50% 4, Scenario increase in bioerosion. Keys wide Table 4. Mean net accretion rates (kg m Table Enochs et al.: Acidification enhances bioerosion and impacts Florida Reef ractT 283
Discussion
Previous studies have shown OA-accelerated erosion of Pacific (Wisshak et al. 2012, Fang et al. 2013) and temperate Atlantic sponges (Duckworth and Peterson 2013, Wisshak et al. 2014), as well as Pacific endolithic algae communities (Tribollet et al. 2009, Reyes-Nivia et al. 2013). Working with a tropical Caribbean species, Stubler et al. (2014) found that living Porites furcata Lamarck, 1816 infested with zooxanthellate Cliona varians (Douchassaing and Michelotti, 1864) had reduced net calcification (coral calcification − erosion) in elevated seawater 2CO . Duckworth and Peterson (2013) observed a doubling in the weight of carbonate removed by boring sponges from temperate scallop shells as pH was experimentally manipulated by HCl addition from present values to those projected by the end of the century (8.1 to 7.8). Wisshak et al. (2012) also used mass loss techniques and calculated a much more conservative increase of 20.4% in total sponge bioerosion from 390 to 750 µatm. Our alkalinity anomaly incubations showed that a brief reduction in aragonite saturation state was sufficient to immediately enhance biologically-mediated chemi- cal dissolution. While our experiments were relatively short-term incubations, we do not expect this to be a brief short-term “shock” response as long-term studies from other regions and species have observed similar responses (e.g., Wisshak et al. 2012, Duckworth and Peterson 2013). Wisshak et al. (2013) conducted alkalinity incuba- tions of C. orientalis, a Pacific species of boring sponge, and developed a relation- ship between CO2 and chemical erosion rate that predicted an approximate doubling (119% increase) in dissolution from today (390 µatm) to 750 µatm. Similarly, working with the temperate Cliona celata Grant, 1826, Wisshak et al. (2014) developed a re- lationship that predicted a 132% increase in chemical dissolution over the same car- bonate chemistry scenarios. The linear regression ofP. lampa erosion applied to our FRT model, developed from an entirely different species of boring sponge, predicted a similar increase (99%) over the same CO2 scenarios. Furthermore, the chemical erosion rates predicted by linear regression of our P. lampa data (0.18 kg m−2 yr−1, 390 µatm) are comparable to those calculated by Wisshak et al. (2013) for C. orientalis at 25 °C (0.21 kg m−2 yr−1, 390 µatm). The similarity of these rates and their proportional increases are disconnected at higher CO2 levels due to the relatively depressed ero- sion rate measured for P. lampa in the 986 µatm treatment (+600 ppm). It is possible that P. lampa was stressed by high CO2 levels at the most extreme of our treatments and may therefore have been physiologically inhibited, resulting in lower chemical dissolution. Alternatively, it is possible that the parabolic response we observed for the chemi- cal dissolution of P. lampa may be different than that of C. orientalis because the latter species possesses symbiotic photosynthetic dinoflagellates. Similar to the photosynthetic enhancement of calcification in corals, boring sponge erosion is en- hanced by the activity of their zooxanthellae symbionts (Hill 1996). These species may therefore be stimulated by elevated CO2 if light is sufficiently high to cause 2CO - limitation of photosynthesis (Suggett et al. 2013). Indeed, Fang et al. (2014) observed an increase in the carbon produced by zooxanthellae and available to C. orientalis at elevated pCO2. Conversely, OA-stimulation of symbiont photosynthesis may buffer accelerated erosion by absorbing CO2 and decreasing the acidity at dissolution sites. 284 Bulletin of Marine Science. Vol 91, No 2. 2015
In this situation, asymbiotic bioeroding sponges could demonstrate greater accelera- tion of erosion due to OA. The only other alkalinity incubation of a non-photosynthetic boring sponge was conducted on a temperate species by Wisshak et al. (2014), who presented a strong linear relationship between elevated CO2 and chemical dissolution. This differs from our findings and suggests different responses of these two asymbiotic species. We, however, measured a peak in chemical dissolution at a mean of 841 µatm seawater pCO2, a treatment range absent from their study, which increased from a treatment level of 644 µatm to 1135 µatm. Therefore, it is still possible that a similar relation- ship exists for these two species. It is interesting that the second of the two rounds of our incubations displayed markedly lower chemical erosion rates while still exhibiting the same pattern of OA- enhanced chemical dissolution (Table 2). This difference could be due to the 2-wk period between incubation rounds. As a sponge permeates coral rock, its erosion rate changes due to the availability of new substrate, food, and shelter (Rützler 1975). Over the time that samples were held in captivity, erosion rates would have gradually declined as more of the rock sample was permeated and less new substrate was avail- able for dissolution. Additionally, P. lampa maintained in laboratory settings have previously been shown to have lower erosion rates than in the wild (Neumann 1966). Consequently, the reduced erosion recorded in the second round of experimental incubations could have been due to the greater time in captivity. Because of the brief period between incubations within rounds (approximately 24 hrs) and the random order of CO2 treatments, neither of these scenarios are likely to have influenced the relative rate of chemical erosion under different OA treatments, which displayed the same patterns across both rounds of incubations. We note that it is possible that other bioeroding taxa within the sponge/coral rock replicates contributed to the chemical bioerosion in our study. We visually inspected fragments to insure no other conspicuous taxa were present, minimized light to re- duce photosynthetic bioeroders, and used controls that had been resting in the same holding tanks as the experimental sponges. Fang et al. (2014) have demonstrated that the biomass of endolithic algae within sponge-permeated specimens is low. Additionally, the erosion rate of endolithic algae per unit area is an order of magni- tude less than conservative sponge erosion rates (Perry et al. 2012). Combined, these factors would likely render the algal component negligible.
It is also noted that unenhanced “control” water had a higher pCO2 than present- day oceanic levels of 390 µatm. While it is difficult to target the causative agent, this is likely due to the specific chemistry of the source water and the unique biogeochemical characteristics of Biscayne Bay, which is a shallow, semi-enclosed lagoon. While these pCO2 values are high compared to the open ocean, they are still within the range of values presently measured on coral reefs, especially those in the Florida Keys (up to 600–700 µatm during autumn, Cheeca Rocks MAPCO2 2014). The similarity of OA-accelerated erosion responses despite the phyletic diversity of previously investigated taxa (algae vs sponges) and their geographic separation suggests that these patterns may occur in presently unconsidered groups, such as lithophagine bivalves, endolithic cirripedes, polychaete worms, and sipunculans. However, differences in boring methodologies/morphologies could result in differ- ential responses to OA and further work is needed to confirm the response of these animals. Increased endolithic bioerosion can lead to less stable carbonate structures Enochs et al.: Acidification enhances bioerosion and impacts Florida Reef ractT 285 and ultimately may facilitate more rapid erosion by epilithic grazers, invertivores breaking apart substrate to feed on endoliths (Guzmán 1988), and abiotic physical disturbance such as storms (Tunnicliffe 1979). Additionally, OA is known to impact the crystalline structure of coral skeletons (Cohen et al. 2009), which may enhance the initial colonization and penetration by endolithic algae (Kobluk and Risk 1977). The influence of accelerated bioerosion on carbonate budgets and framework persis- tence is therefore not limited to enhanced biochemical dissolution. The balance between sponge erosion and coral calcification is of particular impor- tance, especially with respect to the perturbation by acidification. The Perry et al. (2012) compilation of coral growth rates lists a generalized massive coral calcifica- tion rate of 8.74 kg m−2 yr−1. Therefore, their generalized sponge erosion rate of 2.31 kg m−2 yr−1 can directly counteract 26% of this calcification per unit area. According to the relationships calculated here, at 750 µatm, calcification can be expected to de- crease to 4.57 kg m−2 yr−1, while total sponge erosion will increase to 3.23 kg m−2 yr−1. This equates to sponge bioerosion accounting for 71% of calcification per unit area or a net gain of 1.34 kg m−2 yr−1. While the percent cover of coral and boring sponges are not equal in the Florida Keys, this alteration in erosion/calcification balance makes the net carbonate budget especially sensitive to changes in the percent cover of these taxa. Our application of OA-modified bioerosion rates to present-day reef cover high- lights the contribution of endolithic bioeroders, especially algae, to the persistence of coral reef frameworks in an era of major global change. The ubiquity of bare sub- strate on Florida Keys coral reefs contributed to the dominance of endolithic algae erosion (relative to sponge erosion) at the ecosystem level, despite the fact that rates of endolithic algae bioerosion (per m2) are nearly an order of magnitude less than boring sponges. It should be noted that our model incorporated only the more con- spicuous sponge taxa. It is likely that, had it been possible to more accurately quan- tify the large proportion of cryptic sponge area (Schönberg 2001), the proportion of total erosion caused by sponges would be greater. Furthermore, we parameterized our model with the conservative sponge erosion rate of 2.31 kg m−2 yr−1 presented by Perry et al. (2012), whereas an extensive body of literature suggests much higher rates are possible in the Caribbean region (Pione lampa, mean = 13.1 kg m−2 yr−1 (Neumann 1966, Rützler 1975); Cliona (Anthosigmella) varians, mean = 13.1 kg m−2 yr−1 (Hill 1996); Cliona aprica, mean = 13.2 kg m−2 yr−1 (Rützler 1975); Cliona carib- baea, mean = 8 kg m−2 yr−1 (Acker and Risk 1985). Finally, several species of Atlantic boring sponges possess symbiotic zooxanthellae (e.g., Granados et al. 2008) and may therefore demonstrate different responses to OA-induced acceleration of bioerosion (Wisshak et al. 2013). The greater degree to which sponge erosion rates, irrespective of benthic cover, respond to OA relative to endolithic algae and corals suggests they will play an in- creasingly important role in reef framework dynamics. Presently, however, given the scarcity of conspicuous boring sponges relative to other benthic calcifiers and erod- ers in our data set, sponge erosion is most important on localized scales, where ero- sion rates can be as high as 24 kg m−2 yr−1 (Neumann 1966). At these scales, they are known to weaken coral skeletons (Tunnicliffe 1979) and frameworks (Carballo et al. 2008), as well as contribute greatly to sediment production (Neumann 1966). High parrotfish abundances throughout the FRT, especially in the Upper Keys, contribute greatly to erosion in our model (Fig. 4, Table 3). This was an expected, but 286 Bulletin of Marine Science. Vol 91, No 2. 2015 complicated finding. While these fishes remove large amounts of framework per year and contribute strongly to a net erosive system, they also play an important role in grazing and removing competitively harmful algae (Mumby 2009). Higher parrotfish abundances may therefore correspond to greater coral cover and more calcification. Overfishing may therefore result in less bioerosion by parrotfish, but may correspond to less coral cover, less calcification, and ultimately more substrate for other bioerod- ers to colonize. This would lead to a proportionally greater contribution from endo- lithic vs epilithic eroders. The highly positive accretion of the FRT in the preindustrial scenario is drasti- cally different from the negative carbonate budget in the present-day scenario (Fig. 4, Table 4). This difference incorporates changes in erosion, calcification, and coral mortality, ultimately highlighting the degree to which global change has influenced Caribbean reefs in the last century (Gardner et al. 2003, Alvarez-Filip et al. 2009). Furthermore, the large numbers of net erosional reefs presently (33) and in future scenarios (34, 37, 37, 37 for Scenarios 1, 2, 3, 4, 5, respectively) are alarming consider- ing that our models are conservative and do not include the dissolution of a diverse suite of bioeroding endolithic phyla (Glynn 1997). The difficulty of compiling species-specific erosion rates necessitated our general- ization of sponge boring rates across species and the parameterization of endolithic algae dissolution with those from the Pacific Ocean (e.g., Perry et al. 2012). This same approach was used by Kennedy et al. (2013), but our model had the added benefit that we were utilizing the response of a Caribbean sponge species to high CO2 rather than the response of C. orientalis from the Pacific Ocean to OA. Additionally, no models to date have incorporated the various densities of the coral rock substrate, which may significantly influence erosion (Highsmith 1981) and is hypothesized to be influ- enced by OA (Enochs et al. 2014). This simplification of processes and the continued need to rely on parameters obtained from Pacific species underscore the need for a better understanding of both the present-day rates of Caribbean bioerosion and the degree to which they will be influenced by OA. Additionally, we note that our model represented large-scale carbonate budget −2 −1 scenarios (kg CaCO3 m yr ) parameterized from numerous shorter-term studies of corals, CCA, endolithic algae, and sponges. While we do project rates many years in the future, it is important to understand that they still represent instantaneous fluxes, rather than actual year-averaged changes in reef framework habitat. The pos- sibility exists that organisms may suffer unforeseen stress not captured in our exper- iments or, by contrast, may exhibit long-term adaptation to CO2 stress. Furthermore, numerous other stressors, each with temporal and spatial variability, may influence bioerosion and reef framework permanence. For example, coastal eutrophication is known to stimulate sponge bioerosion (Ward-Paige et al. 2005), thus the added pressures from human populations in- habiting the Florida Keys may act in concert with OA to stimulate reef framework degradation. In addition to nutrient gradients, overfishing may indirectly affect the dissolution of coral reefs. Angelfishes are known to control the distribution of bio- eroding sponges (Hill and Hill 2002) and removing these species may lead to rap- id proliferation of sponge populations with implications for the persistence of reef framework structures. Clearly further experimentation is necessary to quantify the potential synergistic impacts of these factors and further replication is necessary to determine the differential responses of various sponge genotypes and species. Enochs et al.: Acidification enhances bioerosion and impacts Florida Reef ractT 287
Regardless, management of coral reefs with climate change and ocean acidification will require a holistic approach, whereby neighboring ecosystems like seagrasses, which have the potential to buffer OA (Manzello et al. 2012), must be protected in tandem with the careful management of healthy reef fish populations and minimiza- tion of coastal pollution. Our data suggest that the bioerosion of Caribbean coral reefs will accelerate as a result of OA. Declining coral cover (Gardner et al. 2003) due to cold (Lirman et al. 2011) and warm water bleaching events (Baker et al. 2008), as well as disease (Aronson and Precht 2001), will exacerbate the effects of OA-enhanced bioerosion (Scenario 4; Fig. 4B, Table 4). Coral mortality not only reduces ecosystem calcifica- tion, but creates new space for endolithic eroders to colonize and for external eroders to graze. Additionally, bioeroding taxa have less restrictive environmental tolerances than corals and may gain a competitive advantage in more extreme conditions pre- dicted to occur as a result of climate change (Schönberg et al. 2008). The confluence of coral mortality and OA-altered bioerosion/calcification ratios will contribute to an accelerated leveling of Caribbean coral reefs (Alvarez-Filip et al. 2009), leading to reduced ecosystem function and the loss of important ecosystem services (Hoegh- Guldberg et al. 2007, Kennedy et al. 2013). To more accurately predict and monitor the decline of Caribbean coral reefs, it is important that we continue to examine the dynamics of bioeroding organisms and the subtractive components of coral reef carbonate budgets, especially as they pertain to OA.
Acknowledgments
Funding was provided through NOAA’s Coral Reef Conservation Program and Ocean Acidification Program. Incubation chambers were designed and built by Hoffman Design Works. T Burton provided assistance monitoring tank chemistry. A Chaves-Fonnegra pro- vided information on the best practices for boring sponge collection. M Brandt helped ac- quire parrotfish data. We are grateful to CM Eakin for discussions that led us to this avenue of investigation.
Literature Cited
Acker K, Risk M. 1985. Substrate destruction and sediment production by the boring sponge Cliona caribbaea on Grand Cayman Island. J Sediment Res. 55(5):705–711. http://dx.doi. org/10.1306/212f87c4-2b24-11d7-8648000102c1865d Alvarez-Filip L, Dulvy NK, Gill JA, Côté IM, Watkinson AR. 2009. Flattening of Caribbean cor- al reefs: region-wide declines in architectural complexity. Proc R Soc Lond: B: 276(1669). http://dx.doi.org/10.1098/rspb.2009.0339 Aronson RB, Precht WF. 2001. White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia. 460:25–38. http://dx.doi.org/10.1023/A:1013103928980 Baker AC, Glynn PW, Riegl B. 2008. An ecological assessment of long-term impacts, re- covery trends and future outlook. Estuar Coast Shelf Sci. 80(4):435–471. http://dx.doi. org/10.1016/j.ecss.2008.09.003 Bissett A, Neu TR, de Beer D. 2011. Dissolution of calcite in the twilight zone: bacterial control of dissolution of sinking planktonic carbonates is unlikely. PLoS ONE. 6:e26404. http:// dx.doi.org/10.1371/journal.pone.0026404 Caccia VG, Boyer JN. 2005. Spatial patterning of water quality in Biscayne Bay, Florida as a function of land use and water management. Mar Pollut Bull. 50(11):1416–1429. http:// dx.doi.org/10.1016/j.marpolbul.2005.08.002 288 Bulletin of Marine Science. Vol 91, No 2. 2015
Carballo J, Bautista-Guerrero E, Leyte-Morales G. 2008. Boring sponges and the modeling of coral reefs in the east Pacific Ocean. Mar Ecol Prog Ser. 356:113–122. http://dx.doi. org/10.3354/meps07276 Cheeca Rocks MAPCO2 [internet] NOAA PMEL. 2014. Available from: http://www.pmel. noaa.gov/co2/story/Cheeca+Rocks Chétail M, Fournié J. 1969. Shell-boring mechanism of the gastropod, Purpura (Thais) lapil- lus: A physiological demonstration of the role of carbonic anhydrase in the dissolution of
CaCO3. Am Zool. 9(3):983–990. http://dx.doi.org/10.1093/icb/9.3.983 Cobb W. 1969. Penetration of calcium carbonate substrates by the boring sponge, Cliona. Am Zool. 9(3):783–790. http://dx.doi.org/10.1093/icb/9.3.783 Cohen AL, McCorkle DC, de Putron S, Gaetani GA, Rose KA. 2009. Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawa- ter: Insights into the biomineralization response to ocean acidification. Geochem Geophys Geosyst. 10(7):1–12. http://dx.doi.org/10.1029/2009GC002411 CREMP (Coral Reef Evaluation and Monitoring Project) Fish and Wildlife Research Institute; 2014. Available from: http://ocean.floridamarine.org/FKNMS_WQPP/pages/cremp.html Duckworth AR, Peterson BJ. 2013. Effects of seawater temperature and pH on the boring rates of the sponge Cliona celata in scallop shells. Mar Biol. 160(1):27–35. http://dx.doi. org/10.1007/s00227-012-2053-z Ehrlich H, Koutsoukos PG, Demadis KD, Pokrovsky OS. 2009. Principles of demineralization: modern strategies for the isolation of organic frameworks. Part II. Decalcification. Micron. 40(2):169–193. http://dx.doi.org/10.1016/j.micron.2008.06.004 Enochs IC, Manzello DP, Carlton R, Schopmeyer S, van Hooidonk R, Lirman D. 2014. Effects of
light and elevated pCO2 on the growth and photochemical efficiency of Acropora cervicor- nis. Coral Reefs. 33(2):477–485. http://dx.doi.org/10.1007/s00338-014-1132-7 Fang JKH, Mello-Athayde MA, Schönberg CHL, Kline DI, Hoegh-Guldberg O, Dove S. 2013. Sponge biomass and bioerosion rates increase under ocean warming and acidification. Glob Change Biol. 19(12):3581–3591. http://dx.doi.org/10.1111/gcb.12334 Fang JKH, Schönberg CHL, Mello-Athayde MA, Hoegh-Guldberg O, Dove S. 2014. Effects of ocean warming and acidification on the energy budget of an excavating sponge. Glob Change Biol. 20(4):1043–1054. http://dx.doi.org/10.1111/gcb.12369 Friedrich T, Timmermann A, Abe-Ouchi, Bates NR, Chikamoto MO, Church MJ, Dore JE, Gledhill DK, González-Dávila M, Heinemann M, Ilyina T, Jungclaus JH, McLeod E, Mouchet A, Santana-Casiano JM. 2012. Detecting regional anthropogenic trends in ocean acidification against natural variability. Nat Clim Chang. 2:167–171. http://dx.doi. org/10.1038/nclimate1372 Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR. 2003. Long-term region-wide declines in Caribbean corals. Science. 301(5635):958–960. http://dx.doi.org/10.1126/science.1086050. Glynn PW. 2007. Bioerosion and coral-reef growth: a dynamic balance. In: Birkeland C, edi- tor. Life and Death of Coral Reefs. New York: Chapman & Hall. p. 68-95. http://dx.doi. org/10.1007/978-1-4615-5995-5_4 Granados C, Camargo C, Zea S, Sánchez JA. 2008. Phylogenetic relationships among zooxan- thellae (Symbiodinium) associated to excavating sponges (Cliona spp.) reveal an unexpect- ed lineage in the Caribbean. Mol Phylo Evol. 49(2):554–560. http://dx.doi.org/10.1016/j. ympev.2008.07.023 Guzmán HM. 1988. Distribución y abundancia de organismos coralívoros en los arrecifes cor- alinos de la Isla del Caño, Costa Rica. Rev Biol Trop. 36 2A:191–207. Hatch W. 1980. The implication of carbonic anhydrase in the physiological mechanism of pen- etration of carbonate substrata by the marine burrowing sponge Cliona celata. Biol Bull. 159(1):135–147. http://dx.doi.org/10.2307/1541014 Highsmith RC. 1981. Coral bioerosion: damage relative to skeletal density. Am Nat. 117(2):193– 198. http://dx.doi.org/10.1086/283698 Hill MS. 1996. Symbiotic zooxanthellae enhance boring and growth rates of the tropical sponge Anthosigmella varians forma varians. Mar Biol. 125(4):649–654. http://dx.doi.org/10.1007/ BF00349246 Enochs et al.: Acidification enhances bioerosion and impacts Florida Reef ractT 289
Hill MS, Hill AL. 2002. Morphological plasticity in the tropical sponge Anthosigmella vari- ans: responses to predators and wave energy. Biol Bull. 202(1):86–95. http://dx.doi. org/10.2307/1543225 Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science. 318(5857):1737–1742. http://dx.doi.org/10.1126/science.1152509 Holm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Stat. 6(2):65–70. Hönisch B, Ridgwell A, Schmidt DN, Thomas E, Gibbs SJ, Sluijs A, Zeebe R, Kump L, Martindale RC, Greene SE, et al. 2012. The geological record of ocean acidification. Science. 335(6072):1058–1063. http://dx.doi.org/10.1126/science.1208277 IPCC. 2007a. Climate Change 2007: impacts, adaptation and vulnerability. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE, editors. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press. p. 80-131. http://dx.doi.org/10.2134/ jeq2008.0015br IPCC. 2007b. Climate Change 2007: The physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, editors. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change “The Physical Science Basis.” Cambridge: Cambridge University Press. p. 748–845. http://dx.doi.org/10.1260/095830507781076194 Johnson MD, Carpenter RC. 2012. Ocean acidification and warming decrease calcification in the crustose coralline alga Hydrolithon onkodes and increase susceptibility to grazing. J Exp Mar Biol Ecol. 434-435:94–101. http://dx.doi.org/10.1016/j.jembe.2012.08.005 Kennedy EV, Perry CT, Halloran PR, Iglesias-Prieto R, Schönberg CHL, Wisshak M, Form AU, Carricart-Ganivet JP, Fine M, Eakin CM, et al. 2013. Avoiding coral reef functional collapse requires local and global action. Curr Biol. 23(10):912–918. http://dx.doi.org/10.1016/j. cub.2013.04.020 Kleypas JA, Buddemeier RW, Archer D, Gattuso J-P, Langdon C, Opdyke BN. 1999. Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science. 284(5411):118–120. http://dx.doi.org/10.1126/science.284.5411.118 Kobluk DR, Risk MJ. 1977. Rate and nature of infestation of a carbonate substratum by a boring alga. J Exp Mar Biol Ecol. 27(2):107–115. http://dx.doi.org/10.1016/0022-0981(77)90131-9
Langdon C, Atkinson MJ. 2005. Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient en- richment. J Geophys Res. 110:C09S07. http://dx.doi.org/10.1029/2004JC002576 Lirman D, Schopmeyer S, Manzello DP, Gramer LJ, Precht WF, Muller-Karger F, Banks K, Barnes B, Bartels E, Bourque A, et al. 2011. Severe 2010 cold-water event caused unprec- edented mortality to corals of the Florida Reef Tract and reversed previous survivorship patterns. PLoS ONE. 6:e23047. http://dx.doi.org/10.1371/journal.pone.0023047 Manzello DP, Enochs IC, Melo N, Gledhill DK, Johns EM. 2012. Ocean acidification refu- gia of the Florida Reef Tract. PLoS ONE. 7:e41715. http://dx.doi.org/10.1371/journal. pone.0041715 Moberg F, Folke C. 1999. Ecological goods and services of coral reef ecosystems. Ecol Econ. 29(2):215–233. http://dx.doi.org/10.1016/S0921-8009(99)00009-9 Mumby PJ. 2009. Herbivory versus corallivory: are parrotfish good or bad for Caribbean coral reefs? Coral Reefs. 28:683–690. http://dx.doi.org/10.1007/s00338-009-0501-0 Neumann A. 1966. Observations on coastal erosion in Bermuda and measurements of the boring rate of the sponge, Cliona lampa. Limnol Oceanogr. 11:92–108. http://dx.doi. org/10.4319/lo.1966.11.1.0092 Perry CT, Edinger EN, Kench PS, Murphy GN, Smithers SG, Steneck RS, Mumby PJ. 2012. Estimating rates of biologically driven coral reef framework production and erosion: a new census-based carbonate budget methodology and applications to the reefs of Bonaire. Coral Reefs. 31(3):853–868. http://dx.doi.org/10.1007/s00338-012-0901-4 290 Bulletin of Marine Science. Vol 91, No 2. 2015
Perry CT, Murphy GN, Kench PS, Smithers SG, Edinger EN, Steneck RS, Mumby PJ. 2013. Caribbean-wide decline in carbonate production threatens coral reef growth. Nat Commun. 4(1402):1–7. http://dx.doi.org/10.1038/ncomms2409 Pomponi SA. 1980. Cytological mechanisms of calcium carbonate excavation by boring spong- es. Int Rev Cytol. 65:301–319. http://dx.doi.org/10.1016/S0074-7696(08)61963-4 Reyes-Nivia C, Diaz-Pulido G, Kline D, Hoegh-Guldberg O, Dove S. 2013. Ocean acidifica- tion and warming scenarios increase microbioerosion of coral skeletons. Glob Change Biol. 19(6):1919–1929. http://dx.doi.org/10.1111/gcb.12158 Rützler K. 1975. The role of burrowing sponges in bioerosion. Oecologia. 19(3):203–216. http://dx.doi.org/10.1007/BF00345306 Rützler K, Rieger G. 1973. Sponge burrowing: fine structure ofCliona lampa penetrating cal- careous substrata. Mar Biol. 21(2):144–162. http://dx.doi.org/10.1007/BF00354611 Schönberg CHL. 2001. Estimating the extent of endolithic tissue of a Great Barrier Reef clionid sponge. Ophelia. 31(1):29–39. http://dx.doi.org/10.1007/bf03042834 Schönberg CHL. 2002. Substrate effects on the bioeroding demosponge Cliona orientalis. 1. Bioerosion rates. Mar Ecol (Berl). 23:313–326. http://dx.doi. org/10.1046/j.1439-0485.2002.02811.x Schönberg CHL, Suwa R, Hidaka M, Loh WKW. 2008. Sponge and coral zooxanthel- lae in heat and light: preliminary results of photochemical efficiency monitored with pulse amplitude modulated fluorometry. Mar Ecol (Berl). 29(2):247–258. http://dx.doi. org/10.1111/j.1439-0485.2007.00216.x
Stubler AD, Furman BT, Peterson BJ. 2014. Effects of pCO2 on the interaction between an exca- vating sponge, Cliona varians, and a hermatypic coral, Porites furcata. Mar Biol. 161:1851– 1859. http://dx.doi.org/10.1007/s00227-014-2466-y Suggett DJ, Dong LF, Lawson T, Lawrenz E, Torres L, Smith DJ. 2013. Light availability deter- mines susceptibility of reef building corals to ocean acidification. Coral Reefs. 32(2):327– 337. http://dx.doi.org/10.1007/s00338-012-0996-7
Tribollet A, Godinot C, Atkinson M, Langdon C. 2009. Effects of elevated pCO2 on dissolution of coral carbonates by microbial euendoliths. Global Biogeochem Cycles. 23(3):1–7. http:// dx.doi.org/10.1029/2008GB003286 Tunnicliffe V. 1979. The role of boring sponges in coral fracture. Colloq Int CNRS. 291:309–315. Warburton EF. 1958. The manner in which the sponge Cliona bores in calcareous objects. Can J Zool. 36(4):555–562. http://dx.doi.org/10.1139/z58-051 Ward-Paige CA, Risk MJ, Sherwood OA, Jaap WC. 2005. Clionid sponge surveys on the Florida Reef Tract suggest land-based nutrient inputs. Mar Pollut Bull. 51(5–7):570–579. http:// dx.doi.org/10.1016/j.marpolbul.2005.04.006 Wisshak M, Schönberg CHL, Form A, Freiwald A. 2014. Sponge bioerosion accelerated by ocean acidification across species and latitudes? Helgol Mar Res. 68(2):253–262. http:// dx.doi.org/10.1007/s10152-014-0385-4 Wisshak M, Schönberg CHL, Form A, Freiwald A. 2013. Effects of ocean acidification and global warming on reef bioerosion – lessons from a clionaid sponge. Aquat Biol. 19(2):111– 127. http://dx.doi.org/10.3354/ab00527 Wisshak M, Schönberg CHL, Form A, Freiwald A. 2012. Ocean acidification accelerates reef bioerosion. PLoS ONE. 7:e45124. http://dx.doi.org/10.1371/journal.pone.0045124 Zundelevich A, Lazar B, Ilan M. 2007. Chemical versus mechanical bioerosion of coral reefs by boring sponges-lessons from Pione cf. vastifica. J Exp Biol. 210(1):91–96. http://dx.doi. org/10.1242/jeb.02627
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