Effects of Ocean Acidification on Population Dynamics and Community ...

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and Community Structure of Crustose Coralline Algae. ALEXANDRA ORDON˜ EZ1,* .... Post-settlement processes such as species competition (e.g., with fleshy ...

Reference: Biol. Bull. 226: 255–268. (June 2014) © 2014 Marine Biological Laboratory

Effects of Ocean Acidification on Population Dynamics and Community Structure of Crustose Coralline Algae ˜ EZ1,* CHRISTOPHER DOROPOULOS2,3, AND ALEXANDRA ORDON GUILLERMO DIAZ-PULIDO1,3 1

Griffith School of Environment and Australian Rivers Institute–Coast & Estuaries, Nathan Campus, Griffith University, 170 Kessels Road, Brisbane, Nathan, Queensland 4111, Australia; 2Marine Spatial Ecology Lab, School of Biological Sciences, The University of Queensland, Brisbane, St Lucia, Queensland 4072, Australia; and 3ARC Centre of Excellence for Coral Reef Studies, Queensland, Australia

impacts of OA on key coral reef builders go beyond declines in calcification and growth, and suggest important changes to aspects of population dynamics and community ecology.

Abstract. Calcification and growth of crustose coralline algae (CCA) are affected by elevated seawater pCO2 and associated changes in carbonate chemistry. However, the effects of ocean acidification (OA) on population and community-level responses of CCA have barely been investigated. We explored changes in community structure and population dynamics (size structure and reproduction) of CCA in response to OA. Recruited from an experimental flow-through system, CCA settled onto the walls of plastic aquaria and developed under exposure to one of three pCO2 treatments (control [present day, 389 ⫾ 6 ppm CO2], medium [753 ⫾ 11 ppm], and high [1267 ⫾ 19 ppm]). Elevated pCO2 reduced total CCA abundance and affected community structure, in particular the density of the dominant species Pneophyllum sp. and Porolithon onkodes. Meanwhile, the relative abundance of P. onkodes declined from 24% under control CO2 to 8.3% in high CO2 (65% change), while the relative abundance of Pneophyllum sp. remained constant. Population size structure of P. onkodes differed significantly across treatments, with fewer larger individuals under high CO2. In contrast, the population size structure and number of reproductive structures (conceptacles) per crust of Pneophyllum sp. was similar across treatments. The difference in the magnitude of the response of species abundance and population size structure between species may have the potential to induce species composition changes in the future. These results demonstrate that the

Introduction Crustose coralline algae (CCA) are important marine calcifiers that play critical roles in marine ecosystems, particularly coral reefs. Firstly, CCA are contributors to limestone formation and, importantly, consolidate reef framework by binding adjacent substrata together (Littler, 1972; Adey, 1998). Secondly, CCA induce settlement of invertebrate larvae (Day and Blake, 1979; Pearce and Scheibling, 1990), especially corals, making them critical in the recovery of reefs after disturbances (Sebens, 1983; Morse et al., 1988; Heyward and Negri, 1999; Harrington et al., 2004; Diaz-Pulido et al., 2012; Doropoulos et al., 2012a, 2014). CCA are also ecosystem engineers that create habitats for a variety of faunal and floral assemblages, particularly in temperate and subtropical regions, thereby promoting marine biodiversity (Foster, 2001). Finally, CCA play important roles in biogeochemical cycling, particularly contributing to carbon sequestration (Mackenzie et al., 2004). The increase of anthropogenic CO2 since industrialization has caused surface ocean pH to decrease by 0.1 units, and it will continue to decline by 0.3 to 0.4 units by 2100 according to oceanographic projections (Caldeira and Wickett, 2003; Orr et al., 2005; IPCC, 2014). The reduction of seawater pH and associated decline in calcium carbonate saturation state (⍀) has negative consequences for calcifying organisms (Doney et al., 2009; Kroeker et al., 2010).

Received 15 December 2013; accepted 10 June 2014. * To whom correspondence should be addressed. E-mail: a.ordonez [email protected] Abbreviations: CCA: crustose coralline algae; OA: ocean acidification. 255

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Studies have demonstrated that CCA are particularly sensitive to ocean acidification (OA) due to the presence of a skeleton of high-magnesium calcite, which is a highly soluble form of CaCO3 (Morse et al., 2006). As a consequence of their mineralogy, CCA skeletons exposed to moderate to high levels of OA have rates of skeletal dissolution that exceed rates of skeleton formation, resulting in reduced net calcification (e.g., Anthony et al., 2008; Ries et al., 2009; Diaz-Pulido et al., 2011). Several physiological processes of CCA are negatively affected by OA. For example, net calcification and growth (Anthony et al., 2008; Jokiel et al., 2008; Kuffner et al., 2008; Martin and Gattuso, 2009; Comeau et al., 2013; Noisette et al., 2013) as well as primary production have been found to decrease under elevated CO2 concentrations (Anthony et al., 2008; Martin and Gattuso, 2009; Hofmann et al., 2012), although other studies demonstrate moderate positive responses of net calcification to OA (Ries et al., 2009). Despite these advances in our understanding of the impacts of OA on CCA, very little is known about the responses of reproduction processes, early life stages, and populations of CCA to elevated CO2 concentrations. Successful recruitment of benthic macroalgal populations requires the success of a series of processes in the life history of the alga, including formation of healthy reproductive structures and spores; spore release, attachment, and germination; and subsequent settlement (Santelices, 1990). Post-settlement processes such as species competition (e.g., with fleshy macroalgae) may also be important in determining whether the CCA recruits or not (Kendrick, 1991; Kroeker et al., 2012). Declines in primary production, growth, and calcification may modify the allocation of energy and resources intended for reproduction and early-lifestage processes, with important consequences for population dynamics (e.g., Kroeker et al., 2010). There is limited evidence of negative effects of OA on algal reproduction, although Porzio et al. (2011) found that reduced pH levels in naturally acidified seawater in the Mediterranean strongly affected the reproduction of calcifying algae. Reproduction of other red and brown algal species (Porzio et al., 2011) and the rates of germination and size of propagules of the giant kelp Macrocytis pyrifera showed minor changes under OA conditions (Roleda et al., 2012). The limited information available on the effects of OA on CCA reproduction and early life states (e.g., Kuffner et al., 2008; Bradassi et al., 2013) suggests that OA may have implications for CCA populations. However, it is not clear to what extent OA affects reproductive output or other processes of the early life history of CCA. Ocean acidification not only affects physiological-level responses (e.g., growth, calcification), but may also have consequences at population and community levels. For example, declines in CCA abundance (percent cover) (HallSpencer et al., 2008; Kuffner et al., 2008), recruitment

(Kuffner et al., 2008; Russell et al., 2009), and increased mortality (Martin and Gattuso, 2009; Diaz-Pulido et al., 2011) have been previously documented. However, few studies have examined the effects of OA on CCA community structure and composition (but see Doropoulos et al., 2012a), and there are no studies addressing its direct effects on CCA population dynamics. Understanding how CCA population structure and dynamics respond to OA will provide insight into which life stages are most sensitive to OA and the potential ramifications of OA to coral reef resilience and ecology. CCA coral reef communities are composed of species populations with varied morphological characteristics that show different survival strategies. The presence and abundance of CCA with a particular morphology will be to a large extent determined by the suite of physical and biological disturbances taking place in a certain habitat (Steneck, 1985, 1986). Steneck (1986) divides crustose (encrusting) coralline algae on reefs into three main groups: thin crusts, thick crusts, and branching forms. Thin crusts are characterized by thalli with a thickness ⬍500 ␮m, rapid growth rates, high reproductive output, and high rates of substrate colonization. Thick crusts are characterized by individuals with thicker thalli (normally ⬎500 ␮m) and slower growth rates, and these crusts are usually late colonizers. Branching corallines are generally thick-crusted species. In our study area in the Great Barrier Reef, Australia, CCA are particularly abundant in shallow (⬍about 5 m depth) coral reef zones such as reef flats, reef crests, and shallow fore reefs. In these environments, thick-crusted species such as Porolithon onkodes are dominant, while species with thinner crusts such as Pneophyllum spp. are more abundant in deeper environments (e.g., below reef crest habitat; pers. obs., AO and GD-P). Given the differences in morphologies and survival strategies, we hypothesize that different CCA populations will show varied responses to the stress of human-induced OA. Understanding individual population responses will help us predict how entire CCA communities will respond to OA. The aim of this study was to test the effects of OA on the recruitment, population dynamics, and community structure of CCA in mesocosm experiments to gain insights into the effects of elevated CO2 on the ecology of key coral-reef-building organisms. To understand the potential role of reproductive output on population dynamics, we further tested the effects of high CO2 on CCA reproductive potential. To gain a better understanding of the mechanistic effects of OA on the ecology of CCA without the interference of space competition with filamentous algal turfs and fleshy seaweeds, we isolated the effect of OA on CCA by removing algal turfs (Kuffner et al., 2008; Russell et al., 2009) and fleshy seaweeds (Kroeker et al., 2012) from our experimental surfaces.

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CORALLINE ALGAE AND ACIDIFICATION Table 1 Summary of water chemistry parameters for the different CO2 levels; data are means of n ⫽ 16 ⫾ SEM (range)

CO2 level Control Medium High

Temp °C

pH

Total alkalinity ␮mol kg⫺1

pCO2 ␮atm

HCO3⫺ ␮mol kg⫺1

CO2⫺ 3 ␮mol kg⫺1

⍀High Mg-Calcite

27.1 ⫾ 0.28 (26.0–28.2) 27.1 ⫾ 0.28 (26.0–28.2) 27.1 ⫾ 0.28 (26.0–28.2)

8.04 ⫾ 0.03 (7.90–8.18) 7.81 ⫾ 0.02 (7.71–7.91) 7.60 ⫾ 0.02 (7.50–7.70)

2291 ⫾ 8.5 (2257–2325) 2291 ⫾ 8.25 (2258–2324) 2290 ⫾ 8.25 (2257–2323)

389 ⫾ 1.5 (383–395) 753 ⫾ 2.75 (742–764) 1267 ⫾ 4.75 (1248–1286)

1735 ⫾ 6.75 (1708–1762) 1935 ⫾ 7.25 (1906–1964) 2052 ⫾ 7.5 (2022–2082)

226 ⫾ 1 (222–230) 145 ⫾ 0.5 (143–147) 97 ⫾ 0.25 (96–98)

1.31 ⫾ 0.005 (1.265–1.350) 0.84 ⫾ 0.002 (0.815–0.863) 0.56 ⫾ 0.002 (0.547–0.575)

High Mg-Calcite, high-magnesium calcite saturation state.

Materials and Methods Experimental approach and CO2 manipulations We conducted an outdoor flow-through experiment at Heron Island Research Station (southern Great Barrier Reef, Australia, 23°26⬘32.3⬙ S, 151°54⬘45.9⬙ E), using 10-l plastic aquaria whose walls served as artificial substratum for CCA recruitment. The CCA community developed over the course of 2.5 mon (5 Dec 2010 to 15 Feb 2011) during austral summer. We exposed the CCA community to three levels of CO2 concentration and measured total CCA cover, species composition, size structure of the two most common CCA species, and reproductive potential of one CCA species (Pneophyllum sp.). The three CO2 treatments followed projections by the Intergovernmental Panel on Climate Change (IPCC) for CO2 stabilization scenarios (IPCC, 2014) using standard protocols for OA research (Gattuso et al., 2010). The levels included control (present day, pCO2 without dosing: 383– 395 ppm, pHNBS/NIST ranged from 7.90 to 8.18); medium (pCO2: 742–764 ppm, pH target value 7.85–7.95); and high (pCO2: 1248 –1286 ppm, pH target value 7.60 –7.70) (Table 1). The pH fluctuations in our control treatment are comparable to those observed in the Heron Island reef flat (e.g., 8.0 to 8.4 [Kline et al., 2012], although not as extreme as those reported in Santos et al., 2011: 7.69 to 8.44). CO2 concentrations were manipulated by bubbling pure CO2 into 200-l seawater mixing sumps. An aquarium control system (Aquatronica, AEB Technologies, Italy) monitored the seawater pH, using temperature-compensated electrodes (Mettler-Toledo, inPro4501VP), and temperature every 30 s within the mixing sumps. When seawater pH exceeded the desired threshold, the control system opened solenoid valves to inject CO2 into the mixing sumps (as described in Diaz-Pulido et al., 2011; Doropoulos et al., 2012b). pH probes were calibrated daily with Mettler-Toledo NBS/ NIST primary standard buffer solutions to 0.01 pH units when necessary. Ambient seawater temperature was used

among treatments throughout the experiment (27.1 ⫾ 1.1 °C, Table 1). Each CO2 treatment had five replicate tanks, with the exception of the high CO2 treatment which had only four replicates. CCA communities developed on the walls of the plastic aquaria during the experiment, and the experimental system was fed by unfiltered seawater drawn from the reef flat. Each replicate tank received a continuous flow of ambient, medium, or high CO2 seawater from the sumps at a rate of 1 l min⫺1. Individual tanks contained small power heads for extra seawater circulation, and all sides of the tanks were regularly cleaned with a soft sponge to remove any fleshy algae, with care being taken to avoid dislodgement of CCA crusts. The tank positions were randomly allocated on an outdoor table, which was covered with shade cloth and neutral density filter (Lee 298 ND 0.15; Lee Filters Limited, Andover, UK) to accommodate any heterogeneity in light. Light averaged 143.5 ⫾ 1.8 ␮mol m⫺2 s⫺1 between 0600 and 1800 (measured with the LI-COR LI1400 datalogger). Irradiance levels from the experiment approximate natural values in the field, which were recorded as 170 ␮mol m⫺2 s⫺1 (6 m) to 230 ␮mol m⫺2 s⫺1 (2 m) on Heron Island reefs during sunny summer days. Water chemistry analyses Total alkalinity was measured on seawater sampled every 6 h for 48 h from each treatment over a spring (2.8 m) and a neap (1.5 m) tidal cycle (Table 1). Total alkalinity replicates within a sample were measured using Gran titration until a maximum 1% error was met, using a T50 titrator (Mettler-Toledo). Saturation state of seawater with respect to high-Mg calcite was calculated for a 16.8 mol% MgCO3, following protocol described in Diaz-Pulido et al. (2012). CCA identification At the end of the experiment, the walls of the plastic aquaria were cut into several panels for ease of manipulation, taking care not to dislodge the algal crusts. Recruited

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CCA were identified to the finest taxonomic resolution using the following taxonomic resources: Wolkerling (1988); Irvine and Chamberlain (1994); Littler and Littler (2003); Harvey et al. (2005, 2006); Adey and Macintyre (1973), and AlgaBase (Guiry and Guiry, 2014). Three different taxonomic procedures were used for identification. (1) Simple microscopic slide preparation. (2) Histological procedures following methods described in Harvey et al. (2005) that included decalcifying crusts with 5% HCl, rinsing, staining with 5% potassium permanganate, then dehydrating using four concentrations of ethanol solution (30%, 60%, 90%, and 100%), embedding in LR White resin, and cross sectioning using a microtome. (3) Scanning electron microscope observations (SEM, JSM-6510 series): for this purpose, samples were taken from plastic aquaria walls that were previously dried out under the sun. Each sample was coated with carbon using a sputter coater (SC7620) and then placed in the SEM. Images were taken at different magnifications (70⫻ to 300⫻) at 5 kV of high voltage with a spot size of 50 and a working distance of 12 mm to 16 mm. Taxonomic features used for identification included type of cell connections (fusions and secondary pits), thallus organization, presence/absence and position of mega cells (trichocytes), and characteristics of the reproductive structures (conceptacles) (Appendix Table A1; Appendix Figs. S1–S6). Some species were unable to be identified and these we classified into two groups: unidentified mix of crusts smaller than 10 mm2 and unidentified mix of crusts larger than 10 mm2 (Appendix Figs. S7 and S8).

Variables and data analyses Community level. To explore the effects of OA on the community structure of CCA that recruited onto the plastic tanks, the number of individual crusts of each species per unit area (density) was recorded in each tank. A total of 7328 crusts were counted, of which 4658 were assigned to six taxonomic species (or morphs). The total area covered by the CCA community was measured in each tank by placing a grid (1⫻1-cm mesh size) over each aquarium panel and visually estimating the percentage of the area covered by the algae. The total area of each tank was 2404 cm2. Mean cover was compared among CO2 treatments using a one-way ANOVA. Data normality and homogeneity of variance were tested using the Kolmogorov-Smirnov and Levene’s tests, respectively. Data were Log10 transformed to meet requirements prior to analysis. Post hoc comparisons were then made using Tukey’s tests. To investigate patterns in community structure and composition, we used the software PRIMER E-v6 (Clarke and Gorley, 2006) for multivariate analyses on the (squared root transformed) density data, and community similarities were plotted using Principal Coordinate Analysis (PCO). To test whether CCA

community structure differed among CO2 treatments, we ran a PERMANOVA (Anderson et al., 2008) on a BrayCurtis similarity matrix of the root transformed data. Unidentified adults and juveniles were not included in the multivariate analyses. Population level. The most abundant CCA species were chosen for a detailed analysis of the potential effects of OA on population dynamics. We selected the thin-crust species Pneophyllum sp. and the thick-crust Porolithon onkodes (Heydrich) Foslie. Two aspects of the populations were studied in this experiment: (1) Population size-structure distribution: Determined by measuring the area of every individual crust. Photographs of a representative side of each of the five plastic tanks (per CO2 treatment) were taken at the end of the experiment, and the area of each individual of Pneophyllum sp. and Porolithon onkodes was measured using the software ImageJ 1.48v (Abra`moff et al., 2004). To compare the size distribution among CO2 treatments we used the nonparametric test Kolmogorov-Smirnov for two independent samples. This test was applied to all possible comparisons (control vs. medium CO2, control vs. high CO2, and medium vs. high CO2), and P-values were adjusted using Bonferroni multiple-comparison corrections with the statistic software R 3.1.0. (2) Reproductive potential of Pneophyllum sp.: Analyzed by counting the number of individuals with and without reproductive structures (conceptacles), and the number of conceptacles per reproductive individual. P. onkodes crusts were excluded from this analysis because the extremely small size of their conceptacles were difficult to see using a stereo microscope. The proportion of reproductive individuals of Pneophyllum sp. was determined from the same representative panel of the tank (as before), while the number of conceptacles per individual was counted on a subset of crusts. We found two types of reproductive structures in Pneophyllum sp.—intact and eroded—therefore we counted them separately. Intact conceptacles maintain the dome form and have a complete chamber and a clearly defined circular pore; these features may indicate healthy structures with the potential to produce spores. Eroded conceptacles may reflect a damaged conceptacle or conceptacles that have already released their spores and collapsed (Littler and Littler, 2003); they have lost their dome-shaped aspect, and the form of the pore is not clearly defined. The proportion of individuals with and without conceptacles and the number of reproductive structures per unit area were compared across CO2 treatments using a one-way ANOVA. Data were Log10 transformed to meet assumptions of normality and homogeneity. Statistical analyses were performed with Systat 11.0.

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CORALLINE ALGAE AND ACIDIFICATION Table 2

One-way ANOVA table for the effects of different CO2 levels on the density of six species of crustose coralline algae found in the community recruited on the plastic aquaria

Figure 1. Total cover (%) of crustose coralline algae crusts under different CO2 levels. Control: pCO2 389 ppm; medium: pCO2 753 ppm; high: pCO2 1267 ppm. Data are means ⫾ SEM; control and medium n ⫽ 5, high n ⫽ 4.

Results Percentage cover of CCA Crustose coralline algae (CCA) cover showed a negative linear response to increasing pCO2: under the highest CO2 treatment, cover decreased 79.58% compared to the control (Fig. 1) (ANOVA: F2 ⫽ 26.88, P ⬍ 0.001). Community-level response The structure of the CCA community varied significantly across CO2 treatments (PERMANOVA: pseudo-F2 ⫽ 16.09, P ⫽ 0.001), with pairwise analysis demonstrating that all CO2 treatments differed significantly from each other (C ⫽ M ⫽ H). Principal Coordinate Analysis showed clear segregation among different treatments, and samples from the high CO2 treatment were considerably more distant from the control than the medium was from the control (Fig. 2). The density of individuals (ind/cm2) for some CCA taxa decreased significantly with increased CO2 (i.e., Pneophyllum sp., P. onkodes, and Neogoniolithon sp., ANOVA P

Figure 2. Principal Coordinate Analysis (PCO) of communities exposed to different CO2 conditions. Control: pCO2 389 ppm; medium: pCO2 753 ppm; high: pCO2 1267 ppm.

Source of variation

Df

MS

F

P

Tukey’s test

Pneophyllum sp. Porolithon onkodes Sporolithon sp. Hydrolithon sp. Neogoniolithon sp. Hydrolithon boreale

2 2 2 2 2 2

0.47 1.64 0.04 0.01 2.01 0.17

35.82 18.11 0.81 0.12 15.46 0.54

⬍0.001 ⬍0.001 0.47 0.88 ⬍0.01 0.61

C⬎M⬎H C⫽M⬎H

C⫽M⬎H

C ⫽ Control pCO2; M ⫽ Medium pCO2; H ⫽ High pCO2.

⬍0.001, 0.001, and 0.01, respectively; Table 2), while other species (including Sporolithon sp., Hydrolithon sp., and Hydrolithon boreale (Foslie) Y. M. Chamberlain) barely changed at higher CO2 levels (ANOVA P ⫽ 0.47, 0.88, 0.61, respectively; Table 2). Pneophyllum sp. was the most abundant species in all treatments, followed by P. onkodes. Under the highest CO2 concentration, Pneophyllum sp. density decreased from 0.79 ind/cm2 in the controls to 0.17 ind/cm2 in the high CO2 treatment, a decline of 78.3%. The change in P. onkodes density was 91.3% with respect to the control treatment (Fig. 3). Further, when the changes in species density are examined in relative terms (i.e., standardized density), it is clear that the decline in the relative

Figure 3. Density of crustose coralline algae species in response to elevated CO2 treatments. Control: pCO2 389 ppm; medium: pCO2 753 ppm; high: pCO2 1267 ppm. Data are means ⫾ SEM; control and medium n ⫽ 5, high n ⫽ 4. Unknown 1: unidentified mix of crusts smaller than 10 mm2. Unknown 2: unidentified mix of crusts bigger than 10 mm2. Individuals growing on the aquarium walls under different acidifying conditions were identified and quantified. Data were standardized by the area of each individual.

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Figure 4. Size distribution of Pneophyllum sp. (A) and Porolithon onkodes (B) under three CO2 concentrations. Control: pCO2 389 ppm; medium: pCO2 753 ppm; high: pCO2 1267 ppm. Area of each individual was measured in square millimeters.

abundance of P. onkodes from the control to the high CO2 treatment was greater than that of Pneophyllum sp. (P. onkodes changed from a relative abundance of 24% under control to 8.3% under the high CO2 treatment—a change of 65%—while Pneophyllum sp. relative density did not experience significant change, varying from 38% in control CO2 to 37% in high CO2). The differences in community structure in response to varying CO2 concentrations were therefore mainly due to changes in species abundance (density), although the relative abundance of the two dominant species also varied according to the CO2 treatments, suggesting some variations in species composition. Due to their high abundance in the community, Pneophyllum sp. and P. onkodes were further analyzed for population-level responses.

varied among CO2 treatments (Fig. 4B). The KolmogorovSmirnov test for two samples indicated that all possible combinations were significantly different (control vs. medium CO2, P ⫽ 0.002; control vs. high CO2, P ⫽ 0.0001; and medium vs. high CO2, P ⫽ 0.0001), and Bonferroni corrections of P-values confirmed these results (control vs. medium CO2, P ⫽ 0.003; control vs. high CO2, P ⫽ 0.0001 and medium vs. high CO2, P ⫽ 0.005). In the control and medium CO2 treatments, the size distribution of P. onkodes population showed high frequencies of small individuals (⬍50 mm2) and also the presence of large individuals of different sizes (from 50 mm2 to 100 mm2). In contrast, under high CO2 conditions, few P. onkodes individuals reached sizes larger than 30 mm2, and the size distribution was more positively skewed (dominance of smaller crusts ⬍30 mm2).

Population-level responses The population dynamics of Pneophyllum sp. and P. onkodes responded differently to changes in carbonate chemistry. The size distribution of Pneophyllum sp. was not significantly different among CO2 treatments. The Kolmogorov-Smirnov test with the Bonferroni corrections for P-values showed no significant differences between combinations (control vs. medium CO2,, P ⫽ 1.00; control vs. high CO2, P ⫽ 0.12; and medium vs. high CO2, P ⫽ 0.14). The size distribution in all CO2 treatments was skewed toward smaller size classes (⬍50 mm2) and showed positive kurtosis (Fig. 4A). This indicates that OA did not have a significant effect on the size distribution of Pneophyllum sp. following 2.5 mon exposure to varying levels of pCO2. In contrast, the size structure of P. onkodes significantly

Reproduction of Pneophyllum sp. The number of reproductive individuals varied significantly across treatments (ANOVA F2 ⫽ 8.51, P ⬍0.001, Fig. 5, Table 3), with an observed decrease of 79.95% from control (0.17 ind.cm⫺2) to high (0.03 ind.cm⫺2) CO2 concentrations. Despite the decrease in the number of reproductive individuals with increased CO2 levels, the proportion of reproductive individuals within the population did not vary significantly across treatments (90.7%, 89.0%, and 83.9% for control, medium, and high CO2 treatments, respectively; ANOVA, P ⫽ 0.69, Table 3). The number of conceptacles per crust, either intact or eroded, was not significantly different among treatments (ANOVA, intact: F2 ⫽ 0.29, P ⫽ 0.74; eroded: F2 ⫽ 0.15, P ⫽ 0.86, Fig 6A,

CORALLINE ALGAE AND ACIDIFICATION

Total percentage cover of CCA

0.25

Density (ind/cm2)

Reproductive Nonreproductive

0.20 0.15 0.10 0.05 0.00 Control

Medium

High

CO2 level Figure 5. Density of reproductive and nonreproductive individuals of Pneophyllum sp. exposed to three CO2 concentrations. Control: pCO2 389 ppm; medium: pCO2 753 ppm; high: pCO2 1267 ppm.

Table 4). Similar results were obtained for the ratio of intact to eroded conceptacles per individual among treatment (Table 4). Overall, these results suggest that there is no effect of elevated CO2 to Pneophyllum sp. reproduction as such, but rather to the density and abundance of the crusts.

Studying the effect of ocean acidification (OA) at population and community levels is essential in understanding the ecological impacts of near-future OA (Fabry et al., 2008; Guinotte and Fabry, 2008). Here, our results demonstrate that elevated pCO2 severely altered crustose coralline algae (CCA) community structure by negatively affecting the abundance and development of several species of CCA. However, the effect of elevated pCO2 on the population dynamics of two key CCA species varied considerably, demonstrating the importance of understanding ecological variability of key reef calcifiers in response to chronic OA (Ries et al., 2009; Harley et al., 2012).

Table 3 One-way ANOVA table for the effects of different CO2 levels on the number and proportion of reproductive individuals of Pneophyllum sp. population

Density CO2 Proportion (%) CO2

Our results are consistent with other studies investigating the effect of OA on CCA cover (Kuffner et al., 2008; Fabricius et al., 2011; Doropoulos et al., 2012a) in that there was a significant decline of CCA exposed to both medium and high CO2 levels. In contrast to some hypotheses attributing the decline of CCA cover at elevated pCO2 to competition with fleshy algae (Kuffner et al., 2008; Russell et al., 2009), any potential effect of CCA-fleshy algae competition in our study was removed by equally cleaning the settlement substrata across CO2 treatments to avoid fleshy algal growth. Although, our study did not focus on understanding CCA-fleshy algae competition under acidifying conditions (as in Kroeker et al., 2012), the effect of elevated pCO2 still resulted in reduced CCA cover and abundance, suggesting that other unexplored reasons for the decrease in CCA cover and abundance are possible (other hypotheses discussed by Doropoulos et al., 2012a). It is most likely that post-settlement growth and survival of recruits are directly impacted by changes in ultrastructure (Ragazzola et al., 2012) and dissolution of the skeleton of CCA (Anthony et al., 2008; Martin and Gattuso, 2009; Semesi et al., 2009; Diaz-Pulido et al., 2011), which are effects caused by pH reduction. Population responses

Discussion

Source of variation

261

Df

MS

F

P

Tukey’s test

2

0.02

8.51

0.006

C⬎M⫽H

2

54.71

0.38

0.69

C ⫽ Control pCO2; M ⫽ Medium pCO2; H ⫽ High pCO2.

This study reveals that the effects of OA on some aspects of the population (e.g., size structure) are species-specific. The population of P. onkodes had few large individuals under high CO2 concentrations but high densities of small size classes under control conditions. This indicates successful settlement, recruitment, and early growth of recruits, but impairment of rapid growth or survival to larger crusts. On the other hand, the size structure of Pneophyllum sp. does not appear to be affected by OA at this early stage of development, with individuals in the high CO2 treatment reaching larger sizes of 100 mm2, similar to the control and medium CO2 treatments. The causes of the differential population responses are unclear, but may be related to the crust thickness and plant habits. P. onkodes has a thick tissue with several perithalial cell layers, whereas Pneophyllum sp. is only 1 to 2 cell layers thick (see Appendix Table A1 and Appendix figures). The thin thallus of Pneophyllum sp. may be a characteristic of early successional colonizers allowing the species to attain rapid horizontal growth rates and high reproductive output— characteristics that may allow the alga to cope with potential stressors and disturbances. Further, a thin photosynthetic thallus may give the crust better control of the internal carbonate chemistry (e.g., Noisette et al., 2013), enabling the alga to maintain calcium carbonate availability for the calcification process and internal supersaturation of high-magnesium calcite (⍀ ⬎ 1), potentially

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Figure 6. (A) Number of conceptacles per area of individuals of Pneophyllum sp. under different CO2 conditions. Control: pCO2 389 ppm; medium: pCO2 753 ppm; high: pCO2 1267 ppm. Data are means ⫾ SEM; control and medium n ⫽ 5, high n⫽ 4. (B) Scanning electron microscopic image of two types of conceptacles: (1) intact and (2) eroded.

reducing skeletal dissolution and mineralogical changes (e.g., Diaz-Pulido et al., 2014). Thick-crusted species such as P. onkodes have slower growth rates compared to thin-crusted taxa, and this may negatively affect competitive ability at least in the early stages of development (Steneck, 1985). In addition, P. onkodes has its photosynthetic tissue restricted to the upper 200 ␮m of the crust, while the white skeleton underneath is not protected by photosynthetic tissue. Thus, unpigmented tissue may be exposed to the direct effect of low pH bulk seawater, with implications for dissolution processes (Ragazzola et al., 2012; Diaz-Pulido et al., 2014). Thick crusts may then have less control of internal carbonate chemistry than thin-crusted species have. One possible explanation for the lack of larger individuals of P. onkodes under high CO2 conditions may be decreased CCA calcification and thalli lateral growth, and increased skeletal dissolution (Gao et al., 1993; Anthony et al., 2008; Jokiel et al., 2008; Semesi et al., 2009; Diaz-Pulido et al., 2011). To further examine the effects of OA on crust calcification/dissolution of P. onkodes, we examined individuals grown in control, medium, and high CO2 treatments using SEM. Images revealed damage on the growing edges of the crust grown under

Table 4 One-way ANOVA for effects of different CO2 levels on the number of conceptacles per area of Pneophyllum sp. crusts; two types of conceptacles were analyzed; intact and eroded Source of variation Density of Density of Proportion Proportion

intact conceptacles CO2 eroded conceptacles CO2 of intact to eroded CO2 of eroded to intact CO2

Df

MS

F

P

2 2 2 2

0.11 0.03 1434.73 365.48

0.29 0.15 1.56 0.37

0.74 0.86 0.21 0.69

medium compared to control CO2 treatment (Fig. 7). Because the CCA crusts under high CO2 were very small, we were not able to observe any damage to the crust margins using SEM. Damage to the marginal (edge) meristem under elevated CO2 conditions may suggest impairment of the calcification process and possible inhibition of crust lateral growth. Similar SEM images of the epithallium of dead Lithophyllum glaciale were observed by Ragazzola et al. (2012), who documented corroded surface layers of cells under high CO2. Reproduction of Pneophyllum sp. To explore possible mechanisms that may explain the dramatic reduction in the abundance of CCA in our experiment, we compared the reproductive output in Pneophyllum sp. (expressed as number of reproductive structures per crust) across CO2 treatments. Our results showed that there was no effect of elevated pCO2 on reproductive potential as such, but rather on the density and abundance of the crusts. We did not count the number of spores within the conceptacles; however, the presence of healthy, reproductive structures suggests that the alga is able to produce spores with potential to settle and recruit onto the experimental panels, as suggested for a number of macroalgal species (Santelices, 1990). Although our experiment was an open system and spores were constantly coming from the reef flat, we assumed that equal numbers of spores came into each of the tanks. Therefore, we investigated whether the similar reproductive output observed among CO2 treatments reflected comparable rates of recruitment. We compared the density of small individuals (⬍15 mm2) of the population among CO2 treatments and did not find significant differences. Consideration of the lack of effects of OA on both CCA reproductive potential and recruitment supports the hypothesis

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Figure 7. Stereoscopic and scanning electron microscopic (SEM) images of individuals of Porolithon onkodes observed in control treatment (A, C) and medium CO2 treatment (B, D). SEM images are close-ups of the respective margins of P. onkodes crusts shown in stereoscopic view.

that OA negatively affects post-recruitment processes, rather than those earlier in the life-cycle (i.e., reproduction and settlement). We have previously hypothesized that reproduction could be affected by the reduction of pH since there may be a change in energy allocation toward calcification and growth, which are known to be affected by acidifying conditions. However, as explained previously, because thin crusts have less non-photosynthetic tissue compared to thick algae, the cost of reproduction would be just slightly affected by the decrease of pH, explaining the result found in this study. Community-level response The variation in responses among CCA populations to OA resulted in changes to the CCA community structure. Half of the species found in the community declined in abundance and were highly sensitive to elevated CO2 concentrations, while the abundance of the remaining species did not change. This is consistent with previous results (Doropoulos et al., 2012a) demonstrating changes in community structure of CCA growing on the underside of ceramic tiles and exposed to low light under OA conditions. Porzio et al. (2011) and Kroeker et al. (2012) documented shifts in macroalgal communities of rocky shores near CO2 vents and found that the cover of calcifying species declined at high CO2 (pH 7.8), while the cover of most non-calcify-

ing algae increased. Interestingly, the thin-crusted coralline alga Hydrolithon cruciatum settled and grew at high CO2 (Porzio et al., 2011). In our study, the change in CCA community structure was not a consequence of competitive exclusion by filamentous algae or fleshy seaweeds (e.g., Kuffner et al., 2008; Russell et al., 2009; Kroeker et al., 2012), as they were removed regularly from our experimental tanks across all treatments. The subtle changes in species composition of the CCA community observed (i.e., the relative abundance of P. onkodes declined with increasing CO2, while that of Pneophyllum sp. remained unchanged) may be explained by different mechanisms, including (1) space competition among CCA species, (2) variability in rates of spore germination, (3) variations in settlement success, and (4) differential effects of direct CO2 enrichment on CCA physiology as discussed in the previous section. Regarding the first mechanism, it is possible that the thin morphology of Pneophyllum sp. crusts is a trait that contributes to the competitive superiority under the high CO2 treatment. It has been demonstrated (Steneck, 1985) that thin-crusted algae have higher reproductive and growth rates than thick-crusted species (such as P. onkodes), and these traits may confer some advantage to thinner crusts. Concerning the second and third mechanisms, there is no information on how OA may affect rates of spore germination and settlement. The available evidence on the effects of

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OA on post-settlement processes of CCA (Bradassi et al., 2013) indicates crust mortality, abnormal development, and calcification impairment with associated energetic tradeoffs. Perhaps a combination of mechanisms may be a plausible explanation. Regardless of the mechanisms involved, intensification of OA in the future could lead to species shifts from thick- to thin-crusted species (e.g., Porzio et al., 2011). Critically, thin-crusted CCA may not be able to play the same ecological role as thick CCA. For instance, P. onkodes is abundant and a significantly important reef builder in the tropical Pacific and Great Barrier Reef (Littler and Doty, 1973). In contrast, Pneophyllum sp. is less abundant than P. onkodes in shallow reef-crest habitats, and its contribution to reef accretion is more limited due to its thinner habit. Thin crusts may be able to hold the unconsolidated substrate together, as observed in areas where the calcium carbonate saturation state is low (e.g., Manzello et al., 2008), but may not be capable of cementing reefs in the way that may be needed to support continuous impacts of OA, cyclones, etc. Replacement of thick-crusted species such as P. onkodes by species with thinner crusts like Pneophyllum sp. may have important consequences for the stability and carbonate budgets of coral reefs. Research on responses of coralline algae to OA have demonstrated that they are sensitive to changes in seawater carbonate chemistry and that effects occur at a range of different organization levels, from alteration to individuals (e.g., impairment of calcification) to populations (e.g., decline in large size classes) and communities (e.g., shifts in structure). Given the importance of CCA for reef resilience and reef framework construction, these changes may have important implications for the ecology and stability of coral reef ecosystems in the future. Importantly, the variability in responses demonstrated here and in other studies (e.g., Ries et al., 2009; Comeau et al., 2013) implies that the direction and magnitude of effects will vary among CCA taxa, populations, and communities.

Acknowledgments We thank M. Herrero, A. Lloyd, B. McIntosh, and HIRS staff, who assisted in the field; M. Couraudon-Reale, who assisted in the laboratory; and E. Kennedy, who helped with preparation of the manuscript. Financial assistance was provided to C. Doropoulos from a Danielle Simmons Award, the Winifred Violet Scott Foundation, a QLD Smart Future Scholarship, and the HIRS Internship awarded by the University of Queensland. ARC-D DP0988039, ARC-D DP120101778, and ARC-L LP0989845 grants supported this study.

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Appendix Table A1 Description of morphs from the CCA community growing on the walls of plastic aquaria.

Taxa

Crust morphology

Type of cell connection

Trichocytes

Conceptacles

Other features

Figure

Orientation of cells in pore canal perpendicular to the pore NA

S1

Very raised, uniporate and with concentric bands around Few uniporate, slightly raised

NA

S3

NA

S4

Pneophyllum sp.

Thin crust, one or two cell Cell fusions layers thick, margin smooth and lobed

Numerous and in fields

Uniporate, raised

Porolithon onkodes

Thick crust with welldefined margin and rough surface Thin crust with increased thickness toward the middle

Numerous and in fields

Uniporate, flush

Sporolithon sp.

Hydrolithon sp.

Thick crust, similar to P. onkodes but with concentric band appearance Neogoniolithon sp. Thick crust, clearly lobed margin and granular texture Hydrolithon boreale Very thin crust (one cell layer thick), margin lobed and branched Very small (area⬍10 Unknown 1 (mix of mm2) and crust one cell crusts smaller than 10 2 thick mm ) Unknown 2 (mix of Crust one cell thick with crusts bigger than 10 area ⬎10 mm2 mm2) NA, not applicable.

Cell fusions

Cell fusions and occasional secondary pit connections

NA

S2

Cell fusions

Few trichocytes

Cell fusions

Numerous individual trichocytes

NA

Coaxial hypothallus

S5

Cell fusions

Individual trichocytes, mainly terminal

NA

NA

S6

Cell fusions

NA

NA

NA

S7

Cell fusions

NA

NA

NA

S8

CORALLINE ALGAE AND ACIDIFICATION

S1. S2. S3. S4.

Pneophyllum sp. (A) General morphology, (B) SEM of crust surface, (C) Cross section of crust. Porolithon onkodes. (A) General morphology, (B) SEM of crust surface, (C) Cross section of crust. Sporolithon sp. (A) General morphology, (B) SEM of crust surface. Hydrolithon sp. (A) General morphology, (B) SEM of crust surface.

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S5. Neogoniolithon sp. (A) General morphology, (B) SEM of crust surface. S6. Hydrolithon boreale. (A) General morphology, (B) SEM of crust surface. S7. Unknown 1. General morphology stereoscope view. S8. Unknown 1. General morphology stereoscope view.

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