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Tolerance of coralline algae to ocean warming and marine heatwaves [1]

['Erik C. Krieger', 'School Of Biological Sciences', 'Victoria University Of Wellington', 'Wellington', 'New Zealand', 'Aleluia Taise', 'Wendy A. Nelson', 'University Of Auckland', 'Auckland', 'National Institute Of Water']

Date: 2023-01 

Ocean warming (OW) and marine heatwaves (MHWs) rapidly transform marine ecosystems, especially when they impact keystone or foundation species. Foundation species such as kelps, fucoids and corals are highly sensitive to heat stress, which threatens the future of temperate seaweed forests and tropical reefs. However, functioning and resilience of these systems also relies on the less conspicuous coralline algae, whose thermal tolerances have gone largely untested. Here, we examined the sensitivity of four temperate coralline algal morphotypes from three different species to four realistic present day and future OW and MHW scenarios (ambient [16°C constant]; ambient+MHW [16°C baseline + a symmetric two-week heatwave with a peak intensity of 18.7°C]; future [18.7°C constant]; future+MHW [18.7°C baseline + a symmetric two-week heatwave with a peak intensity of 21.4°C]). Photo-physiology (e.g., Fv/Fm) and calcification physiology (e.g., proxies for calcifying fluid saturation state Ω CF ) were generally unaffected by the treatments, implying a high thermo-tolerance of our study species compared to other important marine foundation species. We ascribe this mainly to their photosynthetic apparatus that, unlike in other photoautotrophs, continued to function under heat stress. Experimental evidence presented here and elsewhere implies that coralline algae are likely to continue to play their crucial ecological roles in a warming ocean. Yet, such predictions are fraught with uncertainty due to the substantial gaps in our knowledge. We attempt to highlight some of these gaps and aim to present potential physiological underpinnings of their thermo-tolerance.

Tropical coral reefs and temperate kelp forests are extremely diverse and productive ecosystems that are threatened by OW and MHWs due to sensitivity of the dominant foundation species (coral and kelps/fucoids) to thermal stress. However, resilience and future functioning of these systems also depends on the much less conspicuous coralline algae. Yet, information regarding their thermal sensitivity is severely lacking. Thus, we investigated the impact of ocean warming and marine heatwaves and their interaction on photo-physiology and calcification of four temperate coralline algal morpho-types. We hypothesised that: (1) the chronic thermal stress associated with ocean warming will cause decreases in photosynthetic efficiency (Fv/Fm), pigment content (i.e., bleaching) and photosynthetic rates (approximated using electron transport rates), as well as decreased calcification rates and altered calcification physiology (mineralogy and crystal formation); (2) the expected negative impacts will be more pronounced under the acute heat stress of a marine heatwave; and (3) the interaction between acute and chronic heat stress will have the greatest negative impact on coralline algal calcification and photo-physiology.

Ocean warming and marine heatwaves negatively impact many marine biota, including sensitive foundation species such as coral and kelp [ 35 , 36 ] but whether coralline algae are equally susceptible is unclear. Many habitat-forming kelps and fucoids exposed to acute or chronic thermal stress exhibit heat-related decreases in chlorophyll content, and photosynthetic efficiency and output, indicating thermally-induced damage of the photosynthetic apparatus [ 37 – 40 ]. As a result, growth often declines and mortality tends to increase [ 37 , 41 ]. For coralline algae, such observations are, in comparison, sparse. However, there have been reports of reduced calcification and increased mortality in coralline algae due to heat-induced bleaching [ 21 , 42 ]. Yet, the occurrence of thermally-induced bleaching is inconsistent and in some cases elevated temperatures have had either no or positive impacts on coralline algal physiology [ 24 – 26 ]. Additionally, the link between temperature dependent bleaching and reduced calcification can be weak [ 22 , 42 , 43 ]. Further, many other causes such as light and handling stress have been linked with bleaching in coralline algae (e.g., [ 44 ]) which could have influenced earlier observations of bleaching in laboratory settings. Coralline algal bleaching is different to coral bleaching as it refers to the degradation of photosynthetic pigments [ 45 ], commonly followed by necrosis and death, and not the expulsion of endosymbionts that occurs in corals. Also, limited data suggests that coralline algal communities in the field do not seem to respond, like coral, with mass bleaching in response to MHWs [ 15 , 27 , 46 ]. For example, during the 2016 mass coral bleaching event in Western Australia, coral communities underwent between 29 and 80.6% mortality, whereas coralline algae in the same regions were seemingly unaffected [ 15 ]. Thus, there is the potential that coralline algae could buffer [ 8 , 9 , 18 ] some of the ecological impacts associated with the global decline in live coral cover [ 47 – 49 ] caused by more frequent and intense mass coral bleaching and mortality events [ 50 , 51 ].

Rising anthropogenic greenhouse gas forcing is progressively heating the world’s oceans [ 28 – 30 ]. Over the last 170 years, the average temperatures of the surface ocean (SST) have increased by 0.88°C and will continue to rise over the 21 st Century [ 31 ]. It is projected that by 2100, mean SST will have increased further by at least 0.86°C (SSP1-2.6) and up to 2.89°C (SSP5-8.5) [ 31 ]. Concurrent with ocean warming (OW), local extreme temperature events (marine heatwave, MHWs) have also increased in duration, frequency, and intensity [ 32 ]. This is a trend that will accelerate with further ocean warming [ 33 , 34 ].

Coralline algae are important engineers of biogenic reefs and other benthic ecosystems across all latitudes and throughout the photic zone [ 1 , 2 ]. In temperate and subpolar regions, coralline algae monopolise the understory below the canopy formed by larger brown algae [ 3 – 5 ]. The positive interactions between the two functional guilds promote their coexistence and are key for the functioning of these seaweed forests [ 5 , 6 ]. In the tropics, coralline algae are crucial for the construction of coral reefs, acting as consolidators and binders of the reef framework [ 7 – 11 ]. However, coralline algae not only support coral reefs but also construct extensive reef systems of their own [ 12 – 15 ]. In addition to being important foundation taxa, coralline algae act as settlement substrate for many invertebrates, including corals, abalone and sea urchins [ 16 – 19 ]. The ability of coralline algae to play these important ecological roles is threatened by global change, especially ocean acidification [ 20 ]. Yet, how coralline algae will respond to ocean warming is relatively uncertain given the comparably low number of studies and the contrasting results. For example, reported impacts of ocean warming on coralline algal photosynthesis and calcification range from negative [ 21 , 22 ] over neutral [ 23 , 24 ] to positive [ 25 , 26 ]. In addition, responses of coralline algae to marine heatwaves are virtually unknown [ 27 ]. Given their high ecological importance, it is crucial that we gain a better understanding regarding the effects of ocean warming, marine heatwaves, and their interactive effects on coralline algae. Increasing this understanding is the aim of this study.

The effect of temperature and the heatwave on all measured parameters was examined using linear mixed effect models (R package “lme4”) whenever possible. Temperature, MHW and their interaction was used as a fixed, water bath and header tank as random effects. The assumptions of normality and equality of variance were evaluated through graphical analyses of residuals using the R software package “sjPlot”. Treatment effects were determined using one‐way ANOVAs with p-values calculated using “lmerTest”. Proportions of the variation (R 2 ) explained by the full models were calculated using the package “MuMin”. The data underlying this study are available at Dryad [ 69 ].

Confocal Raman spectroscopy was used to determine sample minerology and proxies that follow calcifying fluid saturation state (Ω CF ) in coral and likely do so in coralline algae also [ 63 , 64 ]. Measurements were conducted with a Horiba Jobin-Yvon Labram HR Raman spectroscope (Horiba France SAS, Longjumeau, France) using a green 514 nm Ar-ion laser following DeCarlo et al. [ 65 ] (further details regarding the configuration see [ 52 ]). Therefore, a total of 20 individuals per species (five per treatment) were taken out of the experiment, bleached, and analysed at the timepoints t5 (peak of impact phase) and t8 (end of recovery period). An additional 10 individuals were removed at t6 (MHW treatments only), but these were not analysed (for more details regarding sample removal see S1 Table ). For each individual, three spectra (integration 4x3s) were obtained (one spectrum each from surface cells located on three different growth margins). Low quality or contaminated spectra were excluded from the analysis. The minerology of the sample was determined by the presence and shape of two peaks. The ν1 peak (1,085–1,090 cm -1 ) which is indicative for CaCO 3 and the shape of the ν4 peak (700–720 cm -1 ) which indicates presence of aragonite (double peak) or calcite (single peak) [ 66 ]. Full width at half maximum intensity (FWHM) and position of the ν1 peak were used to determine Mg content and to approximate calcifying fluid Ω [ 65 ]. Abiogenic calibrations of Perrin et al. [ 67 ] were used to estimate mol% Mg after correcting for the divergence of the Si wavenumber obtained in this study and that reported by Perrin et al. [ 67 ]. The calculated Mg content was also used to account for the effects of high Mg content on FWHM. Residual v1 FWHM was considered a proxy for calcifying fluid Ω of high-Mg calcite.

Mean-net calcification rates were quantified using the buoyant weight technique [ 62 ]. Organisms were weighed at the start of the experiment (t0), the end of the acclimation phase (t4), the end of the impact phase (t6) and the end of the recovery phase (t8). The difference in weight between individual timepoints was converted into dry weight of calcite and used to calculate net calcification for the different experimental periods (t0 and t4 = pre-impact/baseline period; t4 and t6 = impact period; t6 and t8 = recovery period). Net weight changes were transformed into calcification rates (mg CaCO 3 cm -2 d -1 ) by normalising for time (in days) and surface area (in cm 2 , for details see Section 2.6). To ensure the correct calculation of calcification rate for the geniculate coralline algae, the weight of the epoxy bases had to be subtracted. Therefore, bases were weighed after the experiment following the complete removal of the algae, and the obtained weight was subtracted from the individual sample weight from each timepoint.

Pigment content was determined from samples taken at t5 and t8 ( Fig 1 ). Therefore, five individuals of each species in each treatment were taken out of the experiment at each timepoint to obtain fresh tissue samples. An additional 10 individuals were removed at t6 (MHW treatments only), but these were not analysed (for more details regarding sample removal see S1 Table ). Red pigments (phycocyanin and phycoerythrin) were extracted using phosphate buffer (after [ 60 ]). Chlorophyll a (Chl a) content was extracted using ethanol (after [ 61 ]). Pigment absorbance was measured with a spectrophotometer (Evolution 300, Thermo-Fisher Scientific, Loughborough, UK) and pigment content was calculated after [ 60 ] for red pigments and [ 61 ] for chlorophyll pigments.

Effective photosynthetic capacity and light acclimation state were assessed at t4, t6 and t8 ( Fig 1 ) using the PAM’s rapid light curve (RLC) function. Relative electron transport rates (rETR) were obtained at noon from five individuals of each species in each treatment. Individuals were exposed for 20 s to nine increasing light steps ranging from 0 to 213 μmol photons m -2 s -1 PAR. Here too, distance between samples and the PAM fibre optic was set to 2 mm using pre-set PAM clips. Non-linear models were then fitted to the data based on least-square error calculations, to determine maximum relative electron transport rate (rETR max ), light use efficiency (α or initial curve slope) and minimum saturation intensity (E k ) [ 58 , 59 ].

The Fv/Fm of each individual was measured at all timepoints (t0–t8) ( Fig 1 ) using a Pulse Amplitude Modulated chlorophyll fluorometer (Diving PAM/R, Heinz Walz GmbH, Effeltrich, Germany) [ 58 , 59 ]. Settings were adjusted for each species to ensure reliable results (saturation light intensity = 8 for Corallina complex. 1, Corallina complex. 2 and Corallina/Arthrocardia “robust” and 7 for Phymtolithopsis complex; gain = 1; damping = 2; measuring light intensity = 1; saturation pulse width = 0.8). Individuals were dark-adapted prior to each measurement for at least 30 min. Thus, measurements were only taken after 9 pm and if Fo >120. The distance between the PAM fibre optic and the samples was standardised to 2 mm using pre-set PAM clips.

Light was provided by 72 W light emitting diode (LED) panels (Zeus 70, Shenzhen Ledzeal Green Lighting Co., Ltd, Shenzhen, China) mounted over each water bath. The LEDs were designed to mimic a natural coastal underwater light spectrum (for details see [ 52 ]) and followed a natural diel cycle. Irradiance increased gradually in two steps (6:30–9:30 and 9:30–12:30) to reach maximum levels in the afternoon (12:30–16:30 h) and decreased again in two steps (16:30–18:30 h and 18:30–20:30 h). Light levels were set to a peak irradiance of 80 μmol photons m -2 s -1 PAR (daily dose 2.3 mol photons m -2 d -1 PAR) in all tanks, as these organisms encounter this frequently in their natural environment (see [ 52 ]). Maintenance of the light level in the individual tanks was achieved by covering them with coated metal mesh and shade cloth. Light levels were checked regularly using an underwater PAR meter (Apogee MQ-510, Apogee Instruments, Inc., North Logan, USA).

Intermediate tanks that collected chilled seawater (see Section 2.4.1) also contained three submersible 300 W heaters that, together with the aquarium chiller, allowed a reduction of the natural temperature variability and the creation of a baseline temperature (14.5–15°C). Temperature in the individual water baths was controlled using two submersible 300 W titanium heaters. All chillers and heaters were connected to an aquarium control system (AquaController, Neptune systems, USA) that turned the individual units on or off at set points when required. Temperature was measured using temperature probes that were connected to the control systems and placed in each water bath. Pumps (Jeboa DC-650, 650 L h -1 ) placed in each water bath ensured good mixing of water within the water bath to enhance temperature control. Smaller jet pumps placed in each experimental tank were used to create sufficient horizontal water motion (Hailea BT100, 150 L h -1 ) and to aid pH and temperature control in the tanks. Temperature in the experimental tanks was checked at regular intervals (results see S2 Table ) and daily variability in the treatments did not exceed ±0.3°C (see S5 Fig ), keeping in mind that some level of daily and day-to-day variability occurs at our field sites (see S7 Fig ).

The seawater used for the experiment was pumped directly from the shore in front of the laboratory facilities, sand-filtered (mesh size 10 μm) and then fed into our flow-through setup. Seawater was first passed through aquarium chillers to decrease temperature variability. Chilled water was collected in two intermediate tanks (one per shelf level with ~60 L in each; 56 cm W x 76 cm L x 18.5 cm H) and pumped from there into the header tanks (~20 L in each; 30 cm W x 25 cm L x 38 cm H) using submersible pumps (Jeboa DC-650, 200 L h -1 ). There were a total of eight header tanks, and one header tank supplied each of six experimental tanks with 80 mL seawater per minute. These were equally distributed over two neighbouring water baths (three per water bath). Header tanks contained one pump (Jeboa DC-650, 650 L h -1 ) for strong water mixing.

The study was conducted at the Wellington University Coastal Ecology Laboratory located on Wellington’s Cook Strait coastline. The experiment consisted of four treatments each representing a different temperature regime (ambient; amb.+MHW; future; and fut.+MHW; see Fig 1 ). Ambient temperature was set to a constant 16°C to reflect average temperatures encountered by the organisms at the time of collection in late summer/early autumn ( S2 and S3 Figs). Future temperatures were set to a constant 18.7°C to account for the projected increase of 2.73°C in the global mean SST at the end of this century under the relative concentration pathway 8.5 [ 55 ]. The baseline temperatures in the two marine heatwave treatments were set to 16°C and 18.7°C respectively, but on top of this a symmetric two-week-long MHW was simulated after an exposure period of three weeks (t2–t4). The peak temperature (t5) of the MHW was set to 18.7°C (amb.+MHW) and 21.4°C (fut.+MHW), which reflects the strength of past MHWs in the region ( S3 Fig ). Each treatment was replicated at the tank level twelve times for a total of 48 experimental tanks ( S4 Fig ). Six experimental tanks from one treatment (~4 L each; 17.5 cm W x 23 cm L x 12 cm H) were organised together in one 60 L water bath (56 cm W x 76 cm L x 18.5 cm H). Thus, a total of eight water baths (two per treatment) were used to accommodate all the experimental tanks. The water baths themselves were distributed over two shelf levels due to logistical constraints. These were later treated in our analysis as random factors (see further below).

To verify the taxonomic consistency of the species groups recognised using morph-anatomical characters ( S1 Fig ), five to seven specimens of each species (~10% of total samples) were randomly selected for DNA-based identification (for further details regarding DNA extraction and sequencing please see [ 52 ]). The sequences obtained were compared to the findings of Twist et al. [ 53 ] and showed that none of the four groups was consistently identified to the species level using morpho-anatomic characteristics, reflecting the well-known difficulties of this approach [ 53 , 54 ]. (Species codes below follow Twist et al. [ 53 ] and are based on sequence data and herbarium voucher material. Representative material has been deposited in the herbarium of the Museum of New Zealand Te Papa Tongarewa, Wellington, New Zealand [WELT].) The crustose samples grouped under Phymatolithopsis complex contained two species of Hapalidiales (Phymatolithopsis repanda (= Hapalidiales ZT ~85% and Hapalidiales sp. D ~15%). The geniculate group Corallina/Arthrocardia “robust” was revealed to consist of Corallina spp. (~60%) and Arthrocardia sp. C (~40%). The samples grouped as Corallina complex 1 included at least three closely related Corallina species (~20% C. berteroi, ~20% C. chamberlainiae and ~60% C. sp.) while the samples grouped as Corallina complex 2 also consisted solely of species from the genus Corallina (~20% C. chamberlainiae and ~80% C. sp.).

Coralline algae were collected (Special Permit 711 issued to Victoria University of Wellington by the New Zealand Ministry of Primary Industries) by snorkellers around two months prior (4 th March 2020) to the experiment from one field site located in Te Moana-o-Raukawa Cook Strait, Te Whanganui a Tara Wellington, Aotearoa New Zealand (41° 20’ 55.7”S, 174° 47’ 25.8”E; also see Site A/Sharks Tooth in Fig 1 in [ 52 ]). Since morphological identification of coralline algae is notoriously difficult, snorkellers were instructed to collect four morphologically distinct groups that a priori we considered most likely to be species or species complexes (for details regarding taxonomy see Section 2.2). These included one species of non-geniculate (Phymatolithopsis complex, N = 63), as well as three groups of geniculate coralline algae including two Corallina morpho-types from different depths (Corallina complex 1 sampled in the subtidal between 1–2 m deep, N = 70; Corallina/Arthrocardia “robust”, N = 70; Corallina complex 2 sampled in the subtidal <1 m deep, N = 48). Mean dry weight of geniculate samples ranged between 0.36 and 0.46 g while crust covered rocks/cobbles were around 6 x 6 cm big with a mean dry weight of 38 g. For collection, geniculate coralline algae were chiselled from the rock with the attaching crust to avoid damaging them. Cobbles or rocks covered with crusts were collected directly from the seafloor. All samples were placed in separate resealable plastic bags filled with seawater while underwater, that were then placed in black plastic bags to reduce light stress and prevent physical damage before bringing them to the surface. After collection, organisms were transported to the laboratory facilities within 20 min in cooler bins filled with ice and cool packs, to further minimise thermal and light stress. At the laboratory, organisms were kept under low light (~8 μmol photons m -2 s -1 photosynthetically active radiation [PAR]) for two days to allow for slow acclimation to laboratory conditions. Light was then gradually increased to 80 μmol photons m -2 s -1 PAR over the course of fourteen days, during which organisms were also carefully cleaned of epibionts and labelled according to the morpho-anatomic classification. Epoxy (Z-Spar A-788 Splash Zone) was used to form a base for geniculate coralline algae. Specimens were then distributed into the experimental tanks. Each tank contained one or two specimens of at least three, but up to four, different species (for more details see S1 Table ). After this initial sixteen-day period, organisms were kept for six weeks at around 16°C which reflects the average temperatures in the field around the time of collection in late summer/early autumn temperatures. For most of this time, access to the laboratory facilities was not permitted due to COVID restrictions, with limited access only possible after week five. After this period, we started the experiment by beginning to increase the temperatures in the ‘future’ treatments over the course of one month (~0.1°C d -1 ). The experiment ran from the 11/05/2020 to the 28/07/2020 (79 days).

4 Discussion

4.1 Impact of heat-stress on coralline algal photo-physiology This study revealed the tolerance of temperate coralline algae to low and moderate heat stress that corresponds to realistic present day and future temperature scenarios. This is contrary to our initial expectations, but generally supported by the findings of three single-species studies from the Mediterranean and the Atlantic [70–72]. The displayed thermo-tolerance is likely linked to the photosynthetic apparatus, which continued to function under heat stress. Photosynthesis is a fundamental yet complex physiological process that is highly sensitive to environmental stress [73]. Upon exposure to adverse abiotic conditions, photosynthetic performance declines rapidly and often well before other physiological processes are impaired [74]. This is readily observable in more intensively studied taxa, including many species of kelp [38, 39], corals [75–77], and higher plants [78, 79], when temperatures approach and exceed (upper) thermal tolerance thresholds. Therefore, we initially expected to see similar patterns in coralline algae, since they were grown far above their maximum summer temperatures, a threshold that has been found to be significant and associated with adverse impacts in many taxa, such as corals [80]. However, photosynthetic efficiency (Fv/Fm) and all other fluorescence parameters (rETR max , α, E k ) were not significantly affected by acute or chronic heat stress in any of the four morpho-types, indicating tolerance to these changes in temperature. The changes we observed in these parameters and in pigment content appeared to be largely driven by biological and/or technical variability and (if at all) only weakly by temperature, since (statistically significant) variations appeared to be rather sporadic and contradictory at times. In Corallina complex 2 for example, chlorophyll a content during the impact phase decreased due to OW and the MHW but increased in the treatment where the interactive effects of both were assessed. Moreover, phycocyanin content, generally unaffected, increased during the same period in this species in the OW treatment. Furthermore, the magnitude of variation in the physiological parameters was extremely small compared to thermosensitive taxa [81] and thus of seemingly limited physiological significance. Collectively, these results suggest a high thermo-tolerance.

4.2 Impacts of elevated temperatures on calcification and minerology Calcification physiology was largely unaffected by heat stress. We hypothesised that calcification rates would decline due to heat stress, reflecting knock-on impacts from heat-induced photoinhibition. However, the hypothesized heat-induced photoinhibition did not occur here. A significant effect of temperature on standardised calcification rates was only detected once, in Corallina/Arthrocardia “robust” during the impact phase. This effect was positive, however. Our results are thus generally consistent with the findings of a recent meta-analysis [27] that assessed the effects of temperature on coralline algal calcification. The analysis concluded that a mean negative impact on coralline algal calcification only manifests itself at temperatures of about 5.2°C above ambient conditions. The relative robustness of this process could be attributed to the fact that calcium carbonate (CaCO 3 ) precipitation is thermodynamically favoured at higher temperatures [82–84]. Additionally, until upper thermal thresholds are reached, increasing temperatures tend to enhance metabolic processes [85]. Based on our results, we suggest that this is also linked to the thermostability of coralline algal photosynthesis that allows continued calcification and enhances overall tolerance. This is supported and complemented by the findings of three other studies that also report limited to no effect of OW or MHWs on coralline algal physiology [70–72, 86]. Together, this implies the resilience of most coralline algae to short- and long-term heat stress. Magnesium incorporation (Mg) and the internal calcium carbonate saturation state (Ω CF, approximated using FWHM) were also principally unaffected by elevated temperature. In hindsight, stability is logical for FWHM, given the lack of impacts on photo-physiology. This lack of an effect on photo-physiology likely allowed the maintenance of a stable internal carbonate chemistry which in turn underpinned steady calcification rates [87]. However, we note that, while stable FWHM could indicate the maintenance of a favourable internal carbonate chemistry (i.e., Ω CF ), further calibrations are required for the correct correlation of the two parameters [63]. The lack of a detectable temperature signal in the Mg content was somewhat surprising. The incorporation of Mg into the calcite lattice is favoured at higher temperatures [88]. In field samples, Mg content is thus generally highest in summer and lowest in winter with a relationship of ~1 mol% per °C [88–90]. In our study species, this relationship was much lower (0.1 to 0.4 mol% per °C) which reemphasises the need for species- and location-specific proxy calibrations [91]. Here, this is likely related to the rate of calcification. Faster calcification is known to increase Mg% irrespective of temperature [52, 92]. Exposure to more favourable light conditions, for example, triggers faster calcification and the increased incorporation of Mg, likely due to the depletion of the internal calcium pool [52]. Thus, it is known that Mg bands in field samples also represent periods of fast (summer) and slow (winter) calcification, with other complex drivers of Mg content usually playing lesser roles [93]. This means that Mg bands incorporate both biology (e.g., more favourable growth conditions in summer) and chemistry (e.g., endothermic substitution of Mg in calcite). In our experiment, calcification rates were stable and seemingly unaffected by temperature. Thus, we only observed a weak “chemical temperature” effect. However, there were exceptions, such as the pronounced increase of Mg in Phymatolithopsis complex in the OW and MHW treatments. Yet, in these treatments, calcification rates increased after the impact phase, supporting the hypothesis that Mg is controlled by calcification rate and temperature.

4.3 Ecology of coralline algae in a warming ocean and indirect effects The tolerance of coralline algae to OW and MHWs displayed here and elsewhere [27, 70–72] suggests that coralline algae are likely to play their ecological roles in a warming ocean (other outcomes of climate change notwithstanding, e.g. ocean acidification or altered biotic interactions). In the tropics, this could mean that coralline algae take up space formerly occupied by corals and thus play a larger role in supporting existing reef structures [11]. Conversely, tropical coralline algae tend to have narrow thermal tolerances which may increase their susceptibility to OW and MHWs [19, 70] and thus diminish their ability to support reef frameworks in the future. However, the thermal sensitivity of taxa with narrow thermal windows has not been examined experimentally. Additionally, such algal dominated reefs would suffer from a decline in structural complexity and the profound alteration of ecosystem functioning [94]. Coralline algae from temperate regions tend to have broader thermal windows and are therefore arguably more robust to heat stress than tropical ones. However, the impacts of OW and MHWs could be more strongly felt in temperate kelp forest communities. Kelps and fucoids are highly susceptible to OW and MHWs and the loss of canopy-forming brown algae has a strong impact on the understory coralline algal community. In particular, while coralline cover tends to increase, community diversity decreases [95]. Thus, taxa that rely on (heat-sensitive) canopy species are likely to be strongly impacted by OW and MHW irrespective of their own thermo-sensitivity. On the other hand, coralline taxa that do not depend on kelp species, or those that rely on canopy species expanding their range, might profit. Yet, there are many unknowns. Manifestation of heat stress ultimately depends on duration, intensity and rate of the temperature increase [96], but the individual and interactive impact of these factors is unknown. This also applies to impacts of OW and MHWs on early life-stages of coralline algae. In addition, the oceans are not only warming but also pH is decreasing, which is likely the greatest threat to coralline algae [20]. The interactions of ocean warming and acidification seem mostly additive [20], but interactions of OA with heatwaves have not been examined so far. Thus, large uncertainties remain about the fate of coralline algae in a future ocean.

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