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The role of CCA as reef consolidators
We found a significant correlation between the proportion of reefs that contain CCA as secondary reef builders and the proportion of true reefs over the last 150 million years. Coral reefs can benefit from CCA in various ways. Relating to the reef ridge, the stony pavement made up by the algae protects the ridge from onrushing waves and also consolidates the reef flats behind the ridges11. With reference to the whole reef, CCA reinforce the structure created by corals, fill cracks, bind together much of the sand, dead corals and debris, and thereby create a stable substrate and reduce reef erosion22. Larval settlement, metamorphosis, and recruitment of several coral species is strictly determined by chemosensory recognition of specific signal molecules uniquely available in specific CCA23.
However, it has to be considered that there are modern reefs that cope with wavy, high-energy environments without the aid of CCA, as for example the Alacran reef in Mexico12. CCA are not the only possibility to add rigidity to a reef. Submarine lithification can be more important than CCA in creating calcite precipitates, especially when environmental and ecological conditions are unfavourable for the growth of CCA, e.g. because of the lack of light. Submarine lithification in the form of Mg-calcite precipitates exists in many forms, including cemented micritic crusts and infillings of cracks. Additionally, their respective carbonate sources may be abiotic24 or originate from a great variety of organisms, including reef fish25. Therefore, they do also play an important role for the structural integrity of coral reefs24. CCA abundance may benefit from reef growth in terms of ecological niches provided, additionally increasing the positive correlation. We thus suggest that the significant correlation between the proportion of reefs reinforced by CCA as secondary reef builders and the proportion of true reefs can be interpreted as a mutual benefit. On the one hand, the presence of CCA can add stability to coral reefs, especially when the reef ridge is exposed to heavy wave action. On the other hand, sufficient reef growth can be a prerequisite for a larger abundance of CCA. A shift towards one side in this mutual dependence is subject to the particular features of each reef, as for example if CCA rather benefit from the shelter of crevices in reefs with high grazing pressure or if corals rather benefit from the presence of CCA at sites of intense wave exposure.
The physicochemical parameters ocean temperature, sea level, and RCO2
CCA occur worldwide from the tropics10 to polar latitudes26 and temperature is one of the primary determinants in their geographical distribution, and the boundaries of their biogeographical regions are associated with isotherms27. Therefore, the identification of ocean temperature as an important driver of CCA reefs is reasonable. Aguirre, et al.28 reported that throughout the history of CCA, species richness broadly correlates with global mean palaeotemperature. However, only the diversity of the order Sporolithales varies positively with temperature, whereas the diversity of the order Corallinales varies negatively with temperature. Accordingly, the warm-water Sporolithales were most species-rich during the warm Cretaceous, but they declined and were rapidly replaced by the Corallinales as Cenozoic temperatures declined. In recent environments, members of the Sporolithales are confined to greater water depths while in euphotic reefs, they do not play a role as reef stabilizers28 and occupy only cryptic habitats sensu Kobluk29, i.e. cavities that serve as well-protected habitats and are not subject to the full spectrum of environmental and biotic controls that exist on the reef surface28. The wave-pounded intertidal algal ridges are built predominantly by Porolithon onkodes (Heydrich) Foslie 1909, P. gardineri (Foslie) Foslie 1909, P. craspedium (Foslie) Foslie 1909, and Lithophyllum kotschyanum Unger 1858 in the Indo-Pacific. In the Atlantic, the main reef reinforcers are Porolithon onkodes (Heydrich) Foslie 1909 and Lithophyllum congestum (Foslie) Foslie 1900. All these species belong to the ‘cool’-water adapted Corallinales. Thus, the increasing capacity of CCA to stabilize coral reefs is in line with the general trend of decreasing ocean temperatures.
A change in sea level does not impact the capacity of CCA to reinforce coral reefs, likely because sea level changes measured on the level of geological stages have no effect on reef formation5. On shorter time scales, sea level is expected to influence the formation of coral reefs, but probably not the CCA’s reef enforcing capacity. We conclude this because the environmental tolerances of CCA in terms of sea level fluctuation are much wider than those of reef corals. Most CCA species appear uniquely tolerant of aerial exposure10. Additionally, many CCA are very well adapted to changes in salinity and especially to low photon irradiances30. The environmental tolerances of reef corals are narrower31,32.
Considering our assumption that there is a mutual relationship between the presence of CCA and the growth of true reefs, another reason might be that one of the most important genera in modern coral reefs, Acropora Oken, 1815, is well adapted to cope with rapid sea-level changes. First observed as an important reef builder in the Oligocene33, Acropora has become a dominant reef builder from the Pleistocene until today, when sea-level fluctuations increased in rate and magnitude34. Indeed, there is a temporal overlap between the first decline in the fraction of CCA reefs—between the Turonian and the Campanian—and a maximum in sea level. Despite this, sea level is not selected as a relevant explanatory variable for the fraction of CCA reefs by the GLM because the relationship between the fraction of CCA reefs and sea level varies inconsistently throughout entire time series of the analysed 150 million years. While the decline in the fraction of CCA reefs may additionally be linked to an increase in temperature before and a significant drop in CCA diversity during the period with a low fraction of CCA reefs, data of the analysis are not suitable to conclusively identify the driver for this particular CCA crisis.
For the entire time series, RCO2, was identified by the model as a minor driver, which may be explained by the fact that an increase of atmospheric pCO2 has only little to no impact on mean ocean surface pH on timescales exceeding 10,000 years35. A plausible reason is that slow rates of CO2 release lead to a different balance of carbonate chemistry changes and a smaller seawater CaCO3 saturation response. This is because the alkalinity released by rock weathering on land must ultimately be balanced by the preservation and burial of CaCO3 in marine sediments. The burial is controlled by the CaCO3 saturation state of the ocean and therefore, the saturation is ultimately regulated by weathering on long time scales, and not by atmospheric pCO2. The effect of weathering on atmospheric pCO2 is much weaker than the effect of weathering on ocean pH. The much stronger effect of weathering on ocean pH allows pH and CaCO3 saturation to be almost decoupled for slowly increasing atmospheric pCO235.
The influence of CCA species diversity
The quantification of CCA species diversity in the geological past is associated to a number of challenges. While for recent CCA the extensive use of molecular phylogenetic methods resolved the four orders (Corallinales, Hapalidiales, Sporolithales, and Rhodogorgonales) currently recognized in the subclass Corallinophycidae as monophyletic lineages36,37, we have to rely on morphological characters since molecular methods are not available for the identification of fossil CCA. Because CCA show a pronounced phenotypic plasticity depending on environmental factors, their taxonomic identification depends on morphological characters like conceptacles (i.e. spore chambers) and the arrangement of cells in different areas of the thallus, features often not adequately preserved in fossil CCA. This has led to a great number of fossil CCA taxa that have been described on the basis of only a few anatomical characters of doubtful taxonomic value38. The inclusion of such taxa precludes fully reliable diversity estimations. To circumvent such problems, we used rarefied species data reviewed by experts on fossil CCA taxonomy28.
Our results show that high CCA diversity is linked to a higher abundance of CCA in true coral reefs. This might seem to contrast with the fact that in modern reefs, the wave-pounded intertidal algal ridges are built predominantly by only a few species while the ones making up the majority of diversity have a cryptic, hidden mode of life protected from full or direct exposure to major physical environmental factors and therefore do not contribute significantly to reef stabilization. However, if several CCA species were contributing to the same ecosystem function, a higher species diversity may have buffered reef systems from losing all species associated with the key function of supporting reef development39. As discussed in detail in the next section, the abundance of CCA in true reefs was transiently reduced four times since the Early Cretaceous. Except for the earliest crisis, this was likely caused by the origin and diversification of echinoids and parrot fish, prominent groups of bioeroding organisms that denude CCA. However, the CCA-coral reef system successfully recovered all times. We argue that this was supported by functional redundancy of CCA, because a diverse group of abundant species with a wider range of responses can help absorb disturbances39. This redundancy of responses to events among species within a functional group—the reef cementers—is an important component of resilience and the maintenance of ecosystem services. The amount of CCA biomass is critical in terms of the cementing capacity. Multi-species community models40 have shown that with consecutive native species’ extinctions at high diversity levels, species extinction usually only leads to a slight decrease in the total biomass of the native community. However, when starting from a lower initial diversity, a few consecutive species extinctions cause a relatively large biomass loss that ultimately leads to collapse. It should also be stressed that sometimes single species are responsible for the functioning of an ecosystem (i.e., keystone species), even if the ecosystem features a generally high biodiversity. Therefore, such ecosystems will decline if this key species is removed41.
Experiments with plants in rangelands42 showed that functional diversity maintains ecosystem functioning. At heavily grazed sites, some species dominant in the ungrazed communities were lost or substantially reduced. In four out of five cases, the minor species that replaced these lost ones were their functional analogues. Accordingly, we suggest that formerly less dominant but functionally analogous grazing-tolerant species increased in abundance and contributed to the maintenance of ecosystem functions. CCA species removed or reduced in biomass by grazing pressure can be replaced in terms of their ecosystem service, i.e. reef cementation, by other CCA that are better adapted to grazing.
This implies that in recent coral reef environments, areas with high CCA diversity—potentially including species occupying cryptic habitats—are more resilient against disturbance. Because the skeletal mineralogies of CCA vary considerably among species43, this resilience possibly applies also to future ocean acidification.
The evolution of herbivory and transient reef crises
The data reveal four crises in the abundance of CCA within true reefs, during the Cretaceous (Turonian–Campanian), the Paleocene (Selandian–Thanetian), the Miocene (Serravallian), and the Pliocene (Zanclean–Piacenzian). The reason that the timing of the Paleocene crisis differs from the known Paleocene–Eocene crisis20 might be that our study focuses on the number of true reefs, while the Paleocene-Eocene crisis is expressed by a change in cumulative metazoan reef volume. Except for the first one, all crises observed here occurred synchronous with pronounced evolutionary events in clades of grazing organisms. Cementing and binding is the main function of CCA in the facilitation of true coral reefs. The decline in CCA abundance during the Selandian–Thanetian corresponds with a marked increase in the rate of morphological evolution in echinoids (Fig. 2). This includes major shifts in lifestyle and the evolution of new subclades in this group44, with a net trend towards improved mobility and feeding ability also on CCA16. Regarding the Serravallian and Zanclean–Piacenzian crises, echinoids appear to play a very minor role as their evolutionary rates constantly decreased over time44. However, another important clade of coralline grazers, the parrot fishes (Scarinae Rafinesque, 1810) may have become major players45. Although reef-grazing fish have existed for nearly 400 Ma, specialized detritivores feeding on macroalgae have only been known since the Miocene46. This is also in line with the radiation of acroporid corals since the mid Miocene47, whose branched morphologies create interstitial niches for parrot fish but also for cryptic CCA species. The parrot fishes (Scarinae) first appeared in the Serravallian45, which may have caused the third crisis in CCA reef cementing capacity. The lineage diversification of Scarinae was most pronounced during the Zanclean-Piacenzian, which we deem responsible for the third crisis.
The abundance of CCA in true coral reefs recovered relatively fast after all crises probably due to morphological adaptations developed within the CCA. Experiments have shown that echinoids are able to graze tissues to depths averaging 88 µm16, which is critical for CCA with thin crust morphologies. The resulting decline of thin crust morphologies led to the occupation of niches by branching CCA16. The twig-like morphologies of branching CCA prevent echinoids from denuding CCA thallus and confine this process to the tips of the branches. CCA are able to transfer nutrients within their thallus16. Therefore, these superficial grazing wounds can be rapidly healed if sufficient nutrient reservoirs are present in other, ungrazed parts of the algae. Meristems and conceptacles engulfed in the thallus may be another adaptation pertinent to the relatively low impact of echinoid grazing, as this is a plausible strategy to protect the reproductive and growth structures of the CCA. The more intense grazing pressure exerted by the parrot fishes, which bite CCA to an average depth of 288 µm16 and are able to eat the tips of branched CCA48 may have resulted in a greater abundance of CCA with very thick crusts. Thick-crust CCA possess larger nutrient reservoirs making them capable to recover also from grazing exerted by parrot fishes. All these adaptations and their development are congruent with the origination and diversification of the grazer clades as already outlined in other studies16,49,50. Today and potentially already during the geological history, CCA did not only successfully adapt to various grazer clades but even required the grazing pressure to stay free of epiphytes49. Here we show for the first time that the process of grazer evolution may also have affected the potential capacity of the CCA to reinforce coral reefs for three times during the geological past.
Future implications for the capacity of CCA to reinforce coral reefs
As it concerns some of the most important biodiversity hot spots on our planet2, the potential future impact of the ongoing global change on the capacity of CCA to reinforce coral reefs should become a focal point of reef research. Despite the implementation of numerous mesocosm and aquaria experiments51,52,53, long-term data in the magnitude of months on CCA responses to modified environmental parameters are still sparse. Also, the change from ambient to modified parameters (e.g. pCO2, temperature) happens much faster than at natural rates.
The impact of elevated pCO2 on CCA depends on the rate of change. While fast rates are critical, slow pCO2 increase may even result in increased net calcification at moderately elevated pCO2 levels54. However, this comes at the cost of structural integrity of the CCA skeleton which, in turn, makes the CCA likely more susceptible to bioerosion. Bioerosion by echinoids and parrot fishes is beneficial to CCA at the present state, as it removes fast growing fleshy algae and other epiphytes49, but nothing is known about the future of this interaction when the integrity of the CCA skeletons is altered. Additionally, it has been shown that elevated pCO2 levels accelerate sponge reef bioerosion55,56,57. Therefore, a combination of increased bioerosion rates affecting corals and CCA might lead to strongly deteriorated conditions for coral reef formation. As outlined above, a greater CCA diversity might also increase their resilience against ocean acidification because of the great variety in skeletal mineralogies.
Regarding elevated temperatures, the outcome for CCA is unpredictable. Depending on the examined species, elevated temperatures affect CCA primary production in different ways: some species show no or negligible response30, some change their skeletal chemistry in terms of dolomite concentration58, and others respond with strongly impaired germination success59 or declining skeletal densities60. Due to the positive influence of cooler temperatures on CCA’s abundance in true reefs detected in our study, elevated temperatures will likely have a negative outcome but also here, the rate of change might be similarly important as the magnitude.
To estimate the future of CCA’s potential to facilitate coral reef growth in the face of global change, we encourage long term experiments—preferably in near-natural mesocosm studies—including the main reef stabilizing CCA species. More

Plants
Wheat (variety Galaxie) was sown on John Innes No. 2 compost in 24-cell trays with 2–5 plants per cell, and maintained on a 16:8 h light:dark cycle at 18 °C (day) and 15 °C(night), with 80% RH in a MLR-352H-PE climate chamber (Sanyo). All plants were used for experiments at 2 weeks old.
Bacteria and fungi
Pseudomonas syringae pv. syringae strains reported to exhibit ice nucleation activity (281, 3010) or not reported to exhibit ice nucleation activity (1902, 3012) were purchased from the National Collection of Plant Pathogenic Bacteria (FERA, UK). Strains selected were not originally isolated from wheat (281, 1902—isolated from Syringa vulgaris; 3010, 3012—isolated from Malus sylvestris) and are not known wheat pathogens. Ice-nucleation activity was confirmed by floating smooth foil squares on the surface of a water/methanol ice bath, cooled to − 10, − 8, − 6, − 4 or − 2 °C. 100 μL droplets of sterile, distilled water were pipetted onto the foil squares and ice crystals formed spontaneously, within 1 min, only at − 10 °C. Two microliters of overnight bacterial culture were added to water droplets and time taken for ice formation recorded. Strain 281 showed the strongest ice nucleation activity and 1902 showed no detectable effect on ice formation; 3010 and 3012 were intermediate (Supplementary Table S1). Bacteria were maintained in 50% glycerol at − 80 °C and were grown on LB agar at 28 °C for all applications. For all experiments involving Z. tritici, the model isolate IPO3237 was used.
Bacterial pathogenicity tests
Bacteria were streaked onto LB agar and grown for 3 days before resuspension in 10 mM MgCl2 at 107 cfu/mL. Bacterial suspensions were sprayed onto wheat plants using a hand held atomiser at a rate of approximately 0.5 mL per cell of 2–5 two week old plants, giving visible misting of both leaf surfaces, on all leaves, without runoff of inoculum. Six cells of plants were inoculated with each strain. Plants were then returned to growth chambers and monitored for symptom development for 28 days. Only strain 3010 induced clear symptoms within this timeframe, although some plants inoculated with strain 3012 also showed mild chlorosis of leaf tips after day 14 (Supplementary Table S2). In further experiments, only strains 281 (INA+) and 1902 (INA−) were used.
Ion leakage measurements
10 cm lengths of 6–9 treated leaves were excised and placed in 10 mL ddH2O for 12 h. Conductivity of the ddH2O was measured using a conductivity meter and then leaves were boiled for 1 h and measurement repeated. ddH2O controls, without leaves, were treated in the same fashion. Ion leakage was reported as a percentage of total conductivity after boiling; control values were subtracted.
Propidium iodide staining for cell death
1 cm leaf sections were immersed for 1 h, in the dark, in 0.05% (w/v) propidium iodide (PI), mounted in 0.1% (v/v) phosphate buffered saline (PBS, pH 7) and viewed using a Leica SP8 confocal microscope using argon laser emission at 500 nm with detection at 600–630 nm. Five leaf sections were viewed for each treatment and 3 fields of view visualised in each leaf section. Cell death was scored as number of cells showing internal (cytoplasmic or nuclear) red fluorescence / total number of cells in field of view. No cell death was recorded.
Wheat inoculation
14 day-old wheat plants were inoculated with either INA+ or INA− bacteria suspended in 10 mM MgCl2 at 107 cfu/mL by spraying with a handheld atomiser until leaves were visibly beaded with moisture on both surfaces, avoiding runoff. Controls were sprayed with 10 mM MgCl2 only.
For assays involving co-inoculation of plants with bacteria and Z. tritici, plants were allowed to dry for an hour before inoculation with Z. tritici blastospores. Blastospores were suspended in sterile distilled water at 105 cfu/mL, a low inoculum density preventing saturation of infection28. Inoculated plants were returned to growth chambers and kept under plastic cloches for 72 h, then maintained as usual.
Analysis of STB speed and severity
Plants were observed at 7, 10, 12, 14, 16, 18, 21, 24 and 28 days post inoculation (dpi) and the most severe symptom on each leaf recorded. At 28 dpi, all inoculated leaves were harvested, rehydrated for 1 h, then scanned at high resolution. Pycnidia were enumerated and leaf area measured in scanned images using ImageJ28.
Antibiotic and competitor application
INA+ bacterial inoculation was carried out as before. Plants were allowed to dry for 1 h at room temperature, then spray inoculated with INA− bacteria suspended in 10 mM MgCl2 at 107 cfu/mL, or sprayed with ampicillin solution (50 μg/mL). Following this second treatment, plants were returned to growth chambers for 24 h. Freezing treatment and subsequent Z. tritici inoculation was then carried out as above.
Estimation of bacterial populations
Two methods were used to estimate bacterial populations on leaves. Firstly, 1 cm leaf samples were harvested from 3 randomly selected leaves in each treatment. These samples were mounted on glass slides in phosphate buffered saline, to which BacLight Green bacterial stain and propidium iodide counterstain were added at 0.05% (w/v) each. After 10 min, leaf samples were imaged at 20× magnification using a Leica SP8 confocal microscope. 5 μM z-stacks were collected at three randomly selected fields of view for each leaf sample and maximum projections created from these. Laser power, gain, and other parameters were held constant between fields of view and samples. The number of green pixels in each projection was then counted using ImageJ software and summed across the three fields of view. The percentage of pixels in the three fields of view which were green was then calculated and used as a proxy for percentage leaf area covered by bacteria. Secondly, 1 cm leaf samples were harvested from 3 more randomly selected leaves in each treatment and homogenised in 10 mM MgCl2. Homogenate was diluted 1/10, 1/100 and 1/1000 in MgCl2 and five 10 μL samples of each dilution spotted onto King’s B29 agar with Pseudomonas selective supplement CFC (Oxoid). Colonies were counted after 24 h incubation at 28 °C. Both procedures were carried out at 1, 4, 7, 10 and 14 dpi.
Experimental design and statistical methods
Specific details of experimental design and analyses are presented in the figure legends alongside the relevant results. Some general principles were applied. Randomisation: where a set of pots of plants was divided between treatments, pots were numbered and randomly generated numbers used to select those assigned to each treatment. For selection of microscope fields of view within a leaf, the slide was placed so that the ‘bottom left’ part of the leaf was in view and a random distance (in mm, bounded by length and width of the leaf) moved in the x and y dimensions to select each field of view, returning to the 0,0 position before each selection.
Replication: technical replication was used in all experiments, with the number of such replicates given in each figure legend. Three complete repeat experiments were carried out in most cases, with figure legends stating where replication was different (min. 2 repeats) and all data presented represent the mean of such replicates, with error bars showing standard errors. Statistical analyses: data were analysed using ANOVA unless otherwise stated, with appropriate checks for homoscedasticity and other assumptions. More

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