Coral Reefs

, Volume 38, Issue 2, pp 297–309 | Cite as

Temporal effects of ocean warming and acidification on coral–algal competition

  • Kristen T. BrownEmail author
  • Dorothea Bender-Champ
  • Tania M. Kenyon
  • Camille Rémond
  • Ove Hoegh-Guldberg
  • Sophie Dove


While there is an ever-expanding list of impacts on coral reefs as a result of ocean warming and acidification, there is little information on how these global changes influence coral–algal competition. The present study assessed the impact of business-as-usual ocean warming and acidification conditions on the survivorship, calcification, photosynthesis and respiration of the coral–algal interaction between the macroalga Halimeda heteromorpha and the coral Acropora intermedia over 8 weeks in two seasons. The physiological responses of A. intermedia and H. heteromorpha were highly dependent on season, with both organisms demonstrating optimal rates of calcification and photosynthesis under present-day conditions in summer. Contact with H. heteromorpha did not influence A. intermedia survivorship, however did reduce long-term calcification rates. Photosynthetic rates of A. intermedia were influenced by algal contact temporally in opposing directions, with rates reduced in winter and increased in summer. Enhanced photosynthetic rates as a result of algal contact were not enough to offset the combined effects of ocean warming and acidification, which regardless of coral–algal contact, reduced survivorship, calcification and photosynthesis of A. intermedia and the calcification rates of H. heteromorpha. These findings provide experimental support for the idea that the effects of coral–algal competition are temporally variable, and help improve our understanding of how future ocean warming and acidification may alter the dynamics of coral–algal interactions.


Competition Coral–algal interactions Climate change Macroalgae Ocean acidification Species interactions 


The rate and scale of anthropogenic climate change is unprecedented, and is exposing coral reefs to conditions not experienced in millions of years (Hoegh-Guldberg et al. 2007; Hönisch et al. 2012; Hughes et al. 2017b). As a result, the relative abundance of reef-building corals is declining in favour of other organisms, often macroalgae (Hughes et al. 2010; Roff and Mumby 2012). Altered competitive dynamics between coral and macroalgae are expected to exacerbate ecosystem shifts as ocean warming and acidification intensify (Diaz-Pulido et al. 2011; Kroeker et al. 2013a; Del Monaco et al. 2017). Despite having a fundamental role in the recovery of coral reefs (McCook 1999), a complete understanding of how mechanisms of coral–algal competition vary with natural (i.e. seasonal) and anthropogenic fluctuations remain relatively poorly understood (Longo and Hay 2015; Brown et al. 2017; Campbell et al. 2017).

Coral and macroalgae principally compete through direct physical or chemical mechanisms, such as abrasion, shading or allelopathy (McCook et al. 2001), which can be disrupted by anthropogenic ocean warming and acidification. Macroalgal contact in combination with elevated temperature has been shown to reduce photosynthetic efficiency and increase tissue loss in coral (Kersting et al. 2015). Ocean acidification can enhance the competitive mechanisms associated with the secondary metabolites of macroalgae, increasing coral mortality (Diaz-Pulido et al. 2011; Del Monaco et al. 2017) and reducing the survival and settlement of coral larvae (Campbell et al. 2017). How coral–algal interactions will be affected by the combined stressors of end-of-the-century ocean warming and acidification, however, has not been explored.

Here, we investigate how organismal physiology and competitive mechanisms are influenced by temporal changes in present-day and end-of-the-century conditions. The interaction between the staghorn coral Acropora intermedia and calcifying macroalga Halimeda heteromorpha was chosen as it is one of the most common interactions on the southern Great Barrier Reef (Castro-Sanguino et al. 2016; Brown et al. 2018). To determine the potential mechanisms by which A. intermedia and H. heteromorpha compete, we cultivated A. intermedia in winter and summer: (1) in contact with H. heteromorpha or (2) algal mimics and (3) in separation. The two temporally separated eight-week experiments simulated average present-day conditions, as well as future conditions by offsetting projected temperature and pCO2 anomalies from present-day baselines. We monitored the effects of competition and simulated climate change on respective survivorship, calcification and photosynthetic capacity. As rapid changes in ocean temperature and carbonate chemistry continue to occur, understanding ecological interactions in the context of global change will enable us to better understand how future coral reef ecosystems are likely to function.

Materials and methods

Specimen collection and experimental design

Experiments were performed over two austral seasons: winter (July–August 2015) and summer (late January–early March 2016), at Heron Island Research Station on the southern Great Barrier Reef (23°26′S 151°52′E). Corals and macroalgae were collected by hand from the reef slope (5–8 m) and acclimatized in tanks with running seawater pumped directly from the Heron Island reef flat for 7 d after collection. Respective treatment conditions were gradually introduced as quarter increments (¼, ½, ¾), representing 25% of full exposure over 14 d in winter and 12 d in summer. The representative concentration pathway (RCP) that projects 8.5 W m−2 of radiative forcing above pre-industrial levels by 2100 was selected because it represents our current ‘business-as-usual’ rate of fossil fuel emissions, despite global consensus for the adoption of policies that significantly reduce greenhouse gas emissions (Riahi et al. 2011; Pörtner et al. 2014; Jackson et al. 2017). While temporary stabilization in CO2 emissions was observed between 2014 and 2016, in 2017, global greenhouse gas emissions increased ~ 2% on 2016 levels, returning to the RCP8.5 pathway (Jackson et al. 2017; Le Quéré et al. 2017). Coral–algal pairs were exposed to four treatments simulating levels of climate change projected for 2100: (1) present-day (PD) temperature and PD pCO2; (2) RCP8.5 pCO2 only (set as 572 ± 11 µatm above PD); (3) RCP8.5 temperature only (set as 3.5 °C above PD); and (4) the combination of RCP8.5 temperature and RCP8.5 pCO2 (Table 1, Fig. S1).
Table 1

Summary of values for water chemistry parameters for all treatment levels in experiments based at Heron Island



T (°C)

TA (µmol kg SW−1)

Sump pCO2 (µatm)

In tank pCO2 (µatm)


HCO3 (µmol kg SW−1)

CO32− (µmol kg SW−1)

Ω aragonite


PD temperature and PD pCO2

21.1 (± 0.64)

2268 (± 5.34)

353 (± 2.04)

396 (± 0.97)

8.11 (± 0.02)

1801 (± 4.42)

187 (± 0.46)

2.9 (± 0.007)

PD temperature and RCP8.5 pCO2

21.1 (± 0.63)

2268 (± 4.06)

856 (± 1.14)

631 (± 1.16)

7.82 (± 0.01)

1933 (± 3.56)

135 (± 0.25)

2.1 (± 0.004)

RCP8.5 temperature and PD pCO2

24.6 (± 0.58)

2287 (± 5.06)

355 (± 1.74)

415 (± 0.96)

8.18 (± 0.005)

1785 (± 4.12)

202 (± 0.47)

3.2 (± 0.007)

RCP8.5 temperature and RCP8.5 pCO2

24.6 (± 0.51)

2283 (± 4.34)

903 (± 2.40)

781 (± 1.53)

7.89 (± 0.01)

1961 (± 3.84)

130 (± 0.25)

2.1 (± 0.004)


PD temperature and PD pCO2

27.1 (± 0.57)

2262 (± 1.46)

482 (± 2.11)

388 (± 0.26)

8.08 (± 0.01)

1712 (± 1.16)

221 (± 0.15)

3.6 (± 0.002)

PD temperature and RCP8.5 pCO2

27 (± 0.50)

2050 (± 2.19)

903 (± 1.15)

631 (± 0.67)

7.80 (± 0.01)

1871 (± 2.00)

162 (± 0.17)

2.6 (± 0.003)

RCP8.5 temperature and PD pCO2

30.7 (± 0.54)

2263 (± 2.74)

484 (± 2.25)

400 (± 0.51)

8.07 (± 0.01)

1674 (± 2.14)

237 (± 0.30)

3.9 (± 0.005)

RCP8.5 temperature and RCP8.5 pCO2

30.6 (± 0.66)

2264 (± 2.70)

956 (± 5.13)

770 (± 0.95)

7.76 (± 0.01)

1881 (± 2.32)

155 (± 0.19)

2.5 (± 0.003)

The four treatments simulated levels projected for 2100 under the business-as-usual RCP8.5 model (Riahi et al. 2011): (1) present-day (PD) temperature and PD pCO2; (2) PD temperature and RCP8.5 pCO2; (3) RCP8.5 temperature and PD pCO2; and (4) RCP8.5 temperature and RCP8.5 pCO2. Temperature (T), sump pCO2 and pH (summer) are given as means (± SD) of hourly measurements. pH (winter) and total alkalinity (TA) are means (± SD) of 24 replicates. In-tank pCO2, bicarbonate (HCO 3 −) , carbonate (CO32−) and aragonite saturation state (Ωaragonite) were estimated using the program CO2SYS. kg SW, kilogram of seawater

Treatment conditions were achieved by use of methods previously described in detail (Dove et al. 2013; Fang et al. 2013; Achlatis et al. 2017). Briefly, the ocean warming and acidification simulation system used computer-controlled procedures to replicate natural diurnal and seasonal fluctuations in temperature and pCO2 in an experimental setting (Dove et al. 2013; Fang et al. 2013; Achlatis et al. 2017). Seawater was continually pumped from the Heron Island reef flat to fill four 8000-L treatment sumps. Temperature and pCO2 concentrations in the PD treatment were determined from two to three hourly measurements recorded at the reference site, Harry’s Bommie reef slope ( Heron + Island), over the same period but in the previous years (2013–2014). All other treatments were then achieved by applying fixed offsets to PD levels. Using a computer-controlled feedback system that responded to conditions measured in experimental aquaria (SCIWARE Software Solutions, Springwood, NSW, Australia), conditions in each sump were manipulated by: (1) injection of air enriched to 30% CO2 or CO2-free air (Spherasorb soda lime, Intersurgical, Berkshire, UK) and/or (2) the use of industrial-scale heater chillers (Rheem HWPO17-IBB; Accent Air, Liverpool, Australia equipped with Eurotherm 3216 temperature regulators, Invensys Process Systems, Clayton, Australia and CO2-Pro CO2 regulators, Pro-Oceanus, Nova Scotia, Canada with accuracy of ± 0.5% CO2 concentration) (Dove et al. 2013; Fang et al. 2013; Achlatis et al. 2017). Seawater was pumped from the sumps into the flow-through experimental aquaria (33 L) at a rate of 0.8 L min−1, with circulation within each tank increased by a wave-maker (Nano 900, Hydor, Italy). The orthogonal design implemented six distinct treatment combinations using three factors, each with two levels: (1) contact (contact and no contact), (2) pCO2 (PD and RCP8.5) and (3) temperature (PD and RCP8.5). In this way, there were three replicate glass aquaria per treatment combination, totalling 24 tanks in each season (winter and summer). Each tank contained 10 coral–algal pairs and four coral fragments paired with algal mimics, totalling 240 coral–algal and 96 coral–algal mimic pairs per season. This multiple factorial approach meant that it was logically impractical to increase sump numbers (Cornwall and Hurd 2015; Hoadley et al. 2015). Very large sumps maintained in the dark with high flow rates were used instead to effectively eliminate any interaction between the sump walls and the bulk of the water that passes through them (i.e. differential confinement effects) (Schoepf et al. 2013; Cornwall and Hurd 2015).

Coral fragments 5–7 cm in length were randomly assigned to outdoor glass aquaria and suspended using fishing line. By covering tanks and lids with filters (marine blue #131, LEE Filters, Hampshire, UK), aquaria experienced natural irradiance corresponding with the representative light environment at the 5 m depth of the collection site [Fig S2; average 24 h irradiance winter 2015 = 70.11 µmol quanta m−2 s−1 (± 3.84 SE); summer 2016 = 89.09 µmol quanta m−2 s−1 (± 2.78 SE)]. Light values are determined over 24 h rather than 12 h because of the seasonal variation in day length at this relatively high latitude reef. Macroalgal thalli of approximately the same length and mass (6–8 cm and ~ 1.5 g), totalling 15 g per tank, were suspended using fishing line at two distinct lengths: (1) in direct and continuous contact with the coral nubbin (‘contact’) (Fig. 1b); and (2) approximately 7 cm away from the nearest point of contact to investigate the effects of macroalgae without contact (‘no contact’) (Fig. 1d). Plastic aquarium algae (‘algal mimics’) were cut to 6–8 cm and attached to A. intermedia fragments using fishing line to examine the physical effects of shading and abrasion alone (Fig. 1c).
Fig. 1

Images of the interaction between the coral Acropora intermedia and macroalga Halimeda heteromorpha from Heron Island, on the southern Great Barrier Reef. a A characteristic A. intermediaH. heteromorpha interaction found at a depth of 5 m. b Manipulated interaction between A. intermedia and H. heteromorpha, where H. heteromorpha remained in direct and continuous contact with the coral nubbin. c Manipulated interaction between A. intermedia and the algal mimic. d Manipulated effect of no contact between A. intermedia and H. heteromorpha, with H. heteromorpha suspended ~ 7 cm away from the A. intermedia nubbin

Tanks were cleaned every 3 days to remove algae growth on aquaria and to gently remove epilithic algal communities from macroalgal thalli using soft toothbrushes. Photosynthetically active radiation (Odyssey PAR sensor, Dataflow Systems Ltd, Christchurch, New Zealand) and temperature (HOBO Pendant UA-001-64, Onset, Bourne, USA) were measured continuously in each treatment and probes were rotated randomly between tanks (Figs. S1, S2). In winter, pH was determined via analysis of seawater samples taken from tanks (DGi101-SC, Mettler Toledo, Port Melbourne, Australia). In summer, pH was continuously recorded in each treatment by randomly rotating probes between tanks (InPro4501VP, Mettler Toledo X connected to a Aquatronica Aquarium Controller ACQ110, Reggio Emilia, Italy), with pH electrodes calibrated every other day (pHSW buffers 7.00 and 10.00, Radiometer Analytical, Hatch Pacific, Victoria, Australia) (Fig. S3). Total alkalinity (AT) was determined via titration using 0.1 M HCl and replicated 20 g seawater samples with a precision of ± 3 µmol kg−1 or better using the Gran titration method (Kline et al. 2012). Acid concentration was calibrated at the beginning of each titration session using the certified reference materials (CRM) from A.G. Dickson (Batch 142 and 146). pH electrodes (DGi101-SC, Mettler Toledo, Port Melbourne, Australia) were also calibrated at the beginning of each titration session using pHSW standard buffers of 7.00 and 10.00, with an average precision from triplicate measurements of less than 0.010 units. Parameters of the carbonate system in seawater were calculated from temperature, salinity, AT and pHSW using CO2SYS (using K1 and K2 from Millero 2010 and average salinity of 35) (Lewis et al. 1998).

Physiological analyses

Experiments lasted 55 d in winter and 39 d in summer. Coral and macroalgae survivorship was assessed visually daily. Coral mortality in RCP8.5 temperature treatments in summer meant that the collection of data ended before the 8-week period achieved in winter (Fig. 2). Calcification of coral fragments was measured using buoyant weight to evaluate net calcification over the entire experimental incubation (‘long-term calcification’) (Davies 1989). Buoyant weight was measured on all corals before exposure to full treatment conditions and at the end of the incubation period. Because of segment shedding in Halimeda (Campbell et al. 2016), calcification of macroalgal thalli was measured using the alkalinity anomaly technique to differentiate short-term (~ 1 h) net calcification at the end of the experimental period (‘short-term calcification’) (Chisholm and Gattuso 1991).
Fig. 2

Survivorship of Acropora intermedia with average experimental temperature as a function of time and treatment. a Survivorship in the austral winter (July–August 2015), with the inset showing weekly in-tank temperature (mean ± SE). b Survivorship in the austral summer (January–March 2016), with the inset showing weekly in-tank temperature (mean ± SE). Achievement of full treatment is indicated with a vertical dotted line. The initial population size for each treatment group was 84 corals. Survivorship was not significantly affected by contact with H. heteromorpha or the algal mimic. RCP pCO2 = + 500 ppm; RCP temp = + 4 °C; RCP temp and pCO2 = + 4 °C and 500 ppm; MMM = maximum monthly mean

Oxygen flux measurements were taken using oxygen optodes connected to an optical analyser (OXY-10, PreSens, Regensburg, Germany), as previously described in detail (Achlatis et al. 2017). Incubations of coral and macroalgae maintained in direct contact (Fig. 1b, c) were done separately, such that any effects of contact between organisms or mimics were a function of long-term carry-over effects and not instantaneous effects. Seawater conditions were replicated to those experienced in the tanks by: (1) using seawater collected from treatment tanks to provide initial pCO2 concentrations and (2) using a water bath to maintain respective treatment temperatures within the incubation chambers. Tank water was filtered using a 0.22-µm filter and O2 content of the water was lowered to 70% using N2 to avoid hyperoxia. Organisms were placed on a grate in 140 cm3 clear acrylic chambers with a magnetic stir-bar unobstructed at the bottom of the chambers. The chambers were placed on top of a magnetic stirrer, which successfully allowed for continuous mixing. A total of 12 coral and macroalgal fragments per treatment (i.e. four specimens per tank) were analysed at the end of the experimental period between 08:00 and 18:00, thus not considering any potential circadian rhythms. Chambers were completely drained and cleaned with a soft sponge in between trials. The maximum light exposure in the tanks at midday (12:00) was 1029 µmol quanta m−2 s−1 in winter and 1070 µmol quanta m−2 s−1 in summer. Therefore, each respirometry assay followed a light program of 20 min of darkness (0 µmol quanta m−2 s−1) to measure dark respiration (Rdark) and 25 min of max midday light levels (1050 µmol quanta m−2 s−1) to determine maximum net photosynthesis (Pnetmax). Trial lengths were optimized to enable the accurate calculation of Rdark and Pnetmax (Crawley et al. 2010). Seawater samples were collected for AT and total ammonia nitrogen (TAN = NH3 + NH4+) from the incubation chambers before and after incubations using a syringe fitted with a 0.45-µm filter to determine net short-term calcification rates.

Specimens were frozen in liquid nitrogen directly after oxygen flux measurements and stored at − 80 °C. Coral fragments were water-piked using 0.22-µm-filtered seawater to determine host protein concentration as a measure of nutritional condition (Ferrier-Pagès et al. 2003) and to quantify the density of dinoflagellate cells as an indicator of coral bleaching (Fitt et al. 2000). Protein content was determined spectrophotometrically using the empirical equations of Whitaker and Granum (1980). The dinoflagellate pellet was resuspended in 10 mL of seawater, and the number of cells (cell density) was measured by counting three aliquots. Total host protein and dinoflagellate densities were standardized to surface area (cm2), which was determined by dipping the nubbin in paraffin wax twice (Veal et al. 2010).

Statistical analyses

Coral survival was analysed using a Kaplan–Meier survival function and pairwise comparison of Mantel–Cox tests with Bonferroni adjustment using GraphPad Prism v7 (Pruitt 2012). All other statistical analyses were conducted using R version 3.3.2 software (2014), and graphical representations were produced using the package ggplot2 (Wickham 2016). The effects of season, temperature, pCO2 and contact on physiological parameters were analysed using factorial generalized linear mixed models (GLMM). The four categorical factors were: season (winter and summer), pCO2 (PD and RCP8.5), temperature (PD and RCP8.5) and contact (contact and no contact). The factor ‘tank’ was included as a random effect. Significant interactive effects were followed by pairwise comparison with Tukey post hoc tests. Data were visually assessed and met the assumptions for homogeneity of variance and normality of distribution (normal Q–Q plots).

To quantify the responses of coral and macroalgae Pnetmax/Rdark rates to temperature, a generalized additive model (GAM) was fit using temperature as an explanatory variable with the package mgcv (Wood 2006). A similar model was also fit including the effect of contact to test for the ‘carry-over’ effect of contact on respective Pnetmax/Rdark rates. The model structure was developed using a stepwise procedure, where models were compared and selected using Akaike information criterion for small sample sizes (AICc) and AICc weight (ωi). The number of knots was restricted (k = 4) to produce conservative models and avoid overfitting.


Effects of season, contact, temperature and pCO2 on the physiology of A. intermedia

Coral survivorship was not affected by contact with H. heteromorpha or the algal mimic (Mantel–Cox test, p > 0.5). In summer, coral survivorship declined significantly under RCP8.5 temperature conditions (Fig. 2, Mantel–Cox test, p < 0.0001 for all comparisons). Long-term coral calcification was independently influenced by contact and interactively influenced by season and temperature. Long-term coral calcification was significantly reduced when in contact with H. heteromorpha and the plastic algal mimic [F(1,636) = 10.26, p = 0.005, post hoc: no contact > mimic = H. heteromorpha] (Fig. 3a). Long-term calcification rates in summer were higher than winter only under PD temperature (PDT) conditions, as RCP8.5 temperature (RCP8.5T) led to significant reductions in long-term calcification [F(1,636) = 17.90, p < 0.00001 post hoc: PDTsummer > PDTwinter = RCP8.5Twinter > RCP8.5Tsummer] (Fig. 3b). Long-term calcification of surviving coral fragments was not affected independently or interactively by pCO2 [F(1,636) = 0.04, p > 0.83].
Fig. 3

Effect of contact and treatment on net long-term calcification rates of Acropora intermedia. a Effect of contact on the per cent change in net long-term calcification (mean ± SE; n = 96–328) measured via the buoyant weight technique and b temporal effect of temperature on the per cent change in net long-term calcification (mean ± SE; n = 161–168)

Coral photosynthesis (Pnetmax) and respiration (Rdark) showed complex responses among treatments and were governed by interactions among the factors. Pnetmax was highest under PD temperature in summer [F(1,157) = 226.7, p < 0.00001, post hoc: PDTsummer > PDTwinter = RCPTwinter > RCPTsummer]. Rdark showed a significant three-way interaction between season, temperature and pCO2 [F(1,157) = 11.1, p = 0.0008], with post hoc analyses revealing in summer, Rdark decreased with RCP8.5 temperature. Photosynthesis-to-respiration ratios (Pnetmax/Rdark) were affected by a three-way interaction between season, temperature and contact [F(1,157) = 8.82, p = 0.003]. This interaction led to increased coral Pnetmax/Rdark as a result of long-term contact with H. heteromorpha, but only under PD temperature in summer.

Host soluble protein content showed a significant three-way interaction between season, temperature and pCO2 [F(1,154) = 11.1, p = 0.0008]. This interaction involved a stepwise reduction in areal protein content across treatments in summer (PDT/PDPCO2 = PDT/RCPPCO2 > RCPT/PD PCO2 > RCPT/RCPPCO2), whereas in winter, areal protein content did not significantly change across treatments (PDT/PDPCO2 = PDT/RCPPCO2 = RCPT/PDPCO2 = RCPT/RCPPCO2) (Fig. 4a). Areal dinoflagellate densities were significantly reduced in surviving coral under RCP8.5 temperature conditions in the summer [F(1,157) = 61.6, p < 0.00001, post hoc: PDTsummer > PDTwinter = RCPTwinter > RCPTsummer] as well as under RCP8.5 pCO2 in the same season [F(1,157) = 11.7, p = 0.0006, post hoc: PDPCO2summer > PD PCO2winter = RCP PCO2winter = RCPPCO2summer] (Fig. 4b).
Fig. 4

Temporal effect of individual treatments on endosymbiotic dinoflagellate populations and host protein content of Acropora intermedia. a Endosymbiotic dinoflagellate densities (mean ± SE; n = 24) in each treatment. b Host protein content (mean ± SE; n = 24) in each treatment. Endosymbiotic dinoflagellate populations and host protein concentrations were unaffected by contact with H. heteromorpha or the algal mimic

Effects of season, contact, temperature and pCO2 on the physiology of H. heteromorpha

All macroalgae survived across the treatments. There was no evidence of A. intermedia contact having a residual effect on macroalgal short-term calcification [F(1,32) = 0.06, p > 0.8]. Winter short-term calcification rates of H. heteromorpha were significantly lower than summer under PD temperature, while under RCP8.5 temperature, winter rates improved, but summer rates were not enhanced (ANOVA, F(1,32) = 19.5, p < 0.00001, post hoc PDTsummer > PDTwinter = RCPTwinter = RCPTsummer) (Fig. 5a). The combination of RCP8.5 temperature and RCP8.5 pCO2 significantly reduced short-term H. heteromorpha calcification rates (ANOVA, F(1,32) = 4.71, p = 0.029, post hoc: PDT/PDPCO2 = PDT/RCPPCO2 = RCPT/PD PCO2 > RCPT/RCPPCO2) (Fig. 5b).
Fig. 5

Temporal effect of individual treatments on net short-term calcification rates of Halimeda heteromorpha. a Temporal effect of temperature on calcification rates (mean ± SE; n = 12) measured via the alkalinity anomaly technique and b the effect of temperature and pCO2 on calcification rates (mean ± SE; n = 12). Calcification rates were unaffected by contact with A. intermedia

Macroalgal Pnetmax and Rdark showed a significant three-way interaction between season, temperature and pCO2. Pnetmax significantly increased in summer when exposed to the combination of RCP8.5 temperature and RCP8.5 pCO2 [F(1,174) = 9.53, p = 0.002], whereas Rdark significantly decreased under the same treatment combination [F(1,174) = 7.45, p = 0.006]. Macroalgal Pnetmax/Rdark was governed by the significant interaction between season, temperature and pCO2 [F(1,174) = 51.61, p < 0.00001], with post hoc analyses supporting the observation that the combination of RCP8.5 temperature and RCP8.5 pCO2 in summer significantly increased Pnetmax/Rdark. Additionally, the significant interaction between season, temperature and contact revealed that contact with A. intermedia significantly increased macroalgal Pnetmax/Rdark under RCP8.5 temperature in winter [F(1,174) = 6.53, p = 0.0106].

Modelling the residual effect of contact on P netmax/R dark as a function of temperature

AICc and ωi indicated that the best-fit generalized additive model (GAM) incorporated contact to best explain both coral and macroalgal Pnetmax/Rdark rates to temperature (Table 2). Relationships between Pnetmax/Rdark and temperature in both coral (H. heteromorpha contact: edf = 2.956, F = 42.69, p < 0.00001; no contact: edf = 2.931, F = 29.42, p < 0.00001) and macroalgae (A. intermedia contact: edf = 2.656, F = 11.0, p < 0.00001; no contact: edf = 1.187, F = 7.449, p = 0.002) were nonlinear (Fig. 6). Temperature explained 57.6% of the deviance in coral Pnetmax/Rdark and 18.6% of the deviance in macroalgal Pnetmax/Rdark. At temperatures of ~ 22.5 °C, the ‘carry-over’ effect of contact with H. heteromorpha had a slightly negative effect on coral Pnetmax/Rdark, while at ~ 27.5 °C, the effect of contact boosted Pnetmax/Rdark (Fig. 6a). For macroalgae, at temperatures of ~ 25 °C, the effect of contact with A. intermedia enhanced Pnetmax/Rdark (Fig. 6b).
Table 2

Generalized additive model (GAM) fits for best models quantifying the responses of Acropora intermedia and Halimeda heteromorpha Pnetmax/Rdark rates to temperature and contact



Model structure



R2 (adj.)

Deviance explained (%)

Photosynthesis-to-respiration ratio (Pnetmax/Rdark)

Acropora intermedia






Temperature + contact (best model)





Halimeda heteromorpha






Temperature + contact (best model)





Shown are Akaike information criterion corrected (AICc), AICc weight (ωi) values, R2 (adjusted) and deviance explained (%)

Fig. 6

The effect of contact on Pnetmax/Rdark relative to temperature based on fitted parameter estimates ± 95% confidence intervals (shaded). a The effect of Halimeda heteromorpha contact on Acropora intermedia Pnetmax/Rdark across temperature. b The effect of A. intermedia contact on H. heteromorpha Pnetmax/Rdark across temperature. Monthly maximum mean (MMM) for the region is indicated with a vertical dotted line


Few studies have examined the effects of ocean warming and acidification on coral–algal interactions, with temporal variability, species interactions and the combined impacts of multiple stressors often ignored in assessments of climate change impacts (Wernberg et al. 2012; Kroeker et al. 2013b; Ban et al. 2014). Here, we reveal organismal physiology fluctuated with temporal variability, coral–algal competition, and projected end-of-the-century conditions. Both A. intermedia and H. heteromorpha exhibited peak calcification and photosynthetic rates under present-day conditions in summer, which coincided with the highest values of host protein content and dinoflagellate densities in A. intermedia. Contact with H. heteromorpha did not affect A. intermedia survivorship or the extent of coral bleaching, yet reduced overall calcification rates and enhanced photosynthetic rates in summer. Ocean warming and acidification did not result in harmful effects on physiological parameters measured for either study organism in winter. In summer, the independent effect of temperatures associated with RCP8.5 was more harmful to A. intermedia physiology than the individual effect of RCP8.5 pCO2. The combined effects, however, generated the most detrimental impacts to both A. intermedia and H. heteromorpha. As rapid changes in ocean temperature and carbonate chemistry continue to occur, these findings help improve our understanding of species interactions in the context of global change.

Under PD conditions in a thermally non-stressful summer, A. intermedia displayed the greatest rates of calcification and photosynthesis, which is consistent with other tropical corals (Crossland 1984; Castillo et al. 2014). Peak calcification and photosynthetic rates coincided with the highest values of protein and dinoflagellate densities per surface area. The individual effect of RCP8.5 warming resulted in no adverse consequences to the physiology of A. intermedia in winter, as temperatures remained below the region’s maximum monthly mean (MMM). In contrast, when temperatures exceeded the MMM in summer, survivorship, calcification and photosynthesis were significantly reduced. RCP8.5 temperature effects were amplified by RCP8.5 pCO2 in summer, leading to further declines in photosynthesis, dinoflagellate densities and protein content. These results are consistent with previous findings that demonstrate multiple stressors will act synergistically in the future and are of great concern to reef-building corals (Anthony et al. 2008; Dove et al. 2013; Horvath et al. 2016). Considering that this experiment simulates an average summer response that excludes El Niño events which currently devastate reefs (Hughes et al. 2017a, 2018), these results are even more significant as they relate to years considered to offer recovery potential from such events (Gilmour et al. 2013).

Similar to A. intermedia, calcification rates of H. heteromorpha were highest under PD conditions in summer, which is consistent with previously reported growth rates (Castro-Sanguino et al. 2016). Increases in temperature have been shown to boost calcification rates of Halimeda (Campbell et al. 2016), and here, the individual effect of RCP8.5 temperature increased short-term calcification rates of H. heteromorpha only in winter. The individual effect of RCP8.5 pCO2 did not influence short-term calcification rates of H. heteromorpha, which is consistent with previous work on H. macroloba and H. taenicola and in contrast to work on H. opuntia and H. minima, with effects believed to be species-specific (Comeau et al. 2013; Johnson et al. 2014; Campbell et al. 2016). Short-term calcification rates of H. heteromorpha, however, were impaired under the combined effects of RCP8.5 temperature and RCP8.5 pCO2, demonstrating that a concurrent increase warming and pCO2 will have the greatest impacts on calcification rates of H. heteromorpha, which is consistent with a previous study examining H. macroloba and H. cylindracea (Sinutok et al. 2012). Interestingly, calcification rates of H. heteromorpha did not coincide with highest rates of production-measured either as Pnetmax or Pnetmax/Rdark. Instead, H. heteromorpha Pnetmax was greatest under conditions that lead to high coral mortality, that is, under RCP8.5 temperature and RCP8.5 pCO2 conditions in summer. Calcification in Halimeda occurs within the inter-utricle space, isolated from direct contact with seawater (Borowitzka and Larkum 1976; Wizemann et al. 2014). Photosynthesis is usually linked to an increase in the rate of calcification (Jensen et al. 1985; Campbell et al. 2016) due to the removal of CO2 that increases tissue pH and facilitates a shift to dissolved inorganic carbon (DIC) dominated by carbonate ions (CO32−) (Borowitzka and Larkum 1976; Wizemann et al. 2014). In the present case, however, rates of photosynthesis and rates of calcification were decoupled under projected future conditions. If energy being gained from increased photosynthesis under RCP8.5 conditions is not being directed towards calcification, then potentially, it is directed towards the accumulation of biomass or the synthesis of chemical compounds (Castro-Sanguino et al. 2016, 2017). In the latter case, corals that are already weakening under future conditions may demonstrate further reductions in growth and increases in mortality when in contact with Halimeda (Rasher and Hay 2014; Longo and Hay 2015).

Under PD conditions, there was no evidence that contact with H. heteromorpha or the algal mimic increased coral mortality or bleaching, which is consistent with a previous study (Atapattu 2009). Furthermore, there was no evidence of the combined effects H. heteromorpha contact and RCP8.5 pCO2 or RCP8.5 temperature on any aspect of A. intermedia physiology. Our results are in contrast with recent work on other types of macroalgae that show chemical competitive mechanisms can become enhanced with ocean warming or acidification, leading to decreased photosynthetic efficiency and increased tissue loss in corals (Diaz-Pulido et al. 2011; Kersting et al. 2015; Del Monaco et al. 2017). Chemical mechanisms employed by macroalgae are generally more damaging to corals than physical effects (Jompa and McCook 2003; Rasher and Hay 2010; Bonaldo and Hay 2014); however, Halimeda are erect, rigid and strongly calcified macroalgae, thus have the potential to abrade or damage corals through physical contact. The lack of chemical competitive mechanisms was supported by the present study’s observation of: (1) equal reductions in A. intermedia calcification rates when exposed to either H. heteromorpha or the algal mimic and (2) the observation that physical contact did not lead to increased bleaching or mortality. When considered together, these results suggest that a physical, rather than chemical driver, was the principle competitive mechanism utilized by H. heteromorpha.

The effects of coral–algal competition were dependent on environmental conditions, shifting in direction from winter to summer. Contact with A. intermedia increased H. heteromorpha Pnetmax/Rdark under RCP8.5 temperature in winter. Although the mechanism by which contact enhanced H. heteromorpha Pnetmax/Rdark could not be deduced in our study, Halimeda have been shown to increase canopy height, volume and biomass when growing within staghorn Acropora habitats (Castro-Sanguino et al. 2016,2017). The effect of contact with H. heteromorpha on A. intermedia resulted in relative decreases in Pnetmax/Rdark rates in winter when exposed to the potentially higher light associated with O2 flux incubations. This result suggests a lack of investment in enzymes associated with photochemical quenching (i.e. cytochrome b6f) that limits the ability of the photoautotrophs to increase electron transport in response to an increase in photon flux (Dustan 1979; Falkowski and Dubinsky 1981; Stitt and Schulze 1994). The opposite, however, was observed for PD summer, where the effect of contact led to a significant increase in Pnetmax/Rdark relative to corals not in contact with H. heteromorpha. The increase in temperature relative to winter under PD summers increases the catalytic activity of enzymes, potentially enabling a shade-adapted photoautotroph with an enriched light harvesting capacity to significantly elevate rates of photosynthesis (Niyogi 1999). These results demonstrate that by providing intermittent shade, and/or limiting access through competition to resources such as DIC or dissolved inorganic nitrogen (DIN), long-term contact with this calcareous macroalga can alter the ability of corals to upregulate photosynthesis in response to periods of elevated light. Efforts to artificially shade sections of a reef during periods of thermal stress have been suggested (Rau et al. 2012; Coelho et al. 2017); however, the photosynthetic benefits provided to A. intermedia through reductions in light collapsed under RCP8.5 temperature and RCP8.5 pCO2 conditions in summer.

Given the rapidly shifting coral reef ecosystem dynamics due to rising anthropogenic CO2, coral–algal interactions are more relevant than ever. While the results of this research provide a greater understanding of the complicated dynamics regulating the mechanisms of coral–algal competition, ultimately more research is needed if we are to comprehensively understand coral–algal interactions in changing settings. The forthcoming research should focus on investigating the interactions of multiple coral–algal species to explore competitive mechanisms under human driven global change. The complexity and severity of climate change on coral reef ecosystems highlights the urgent need for action to reduce CO2 emissions in line with the goals of the Paris Climate Agreement to maintain some semblance of structure and function of today’s coral reef ecosystems.



This work was supported by the Australian Research Council (ARC) LP110200874 (SD and OHG), the ARC Centre of Excellence for Coral Reef Studies CE140100020 (SD and OHG) and an ARC Laureate Fellowship FL120100066 (OHG). It was also supported by the Holsworth Wildlife Research Endowment-Equity Trustees Charitable Foundation & the Ecological Society of Australia (KTB), the PADI Foundation (KTB) and a XL Catlin Seaview Survey scholarship (KTB). We would like to thank Aaron Chai for support in the field, colleagues of the Coral Reef Ecosystem Laboratory, and the staff of Heron Island Research Station. Research was conducted under GBR Marine Park Authority Permit #G15/37620.1.

Supplementary material

338_2019_1775_MOESM1_ESM.docx (409 kb)
Supplementary material 1 (DOCX 409 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Coral Reef Ecosystems Lab, School of Biological SciencesUniversity of QueenslandSt. LuciaAustralia
  2. 2.Global Change InstituteUniversity of QueenslandSt. LuciaAustralia
  3. 3.ARC Centre for Excellence for Coral Reef StudiesUniversity of QueenslandSt. LuciaAustralia
  4. 4.Marine Spatial Ecology Lab, School of Biological SciencesUniversity of QueenslandSt. LuciaAustralia

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