Caribbean coral reefs, including the Florida Reef, are increasingly affected by local events and global climate change. One of these regional impacts is the growing prevalence of pelagic Sargassum algal species (S. natans and S. fluitans, simply referred to as Sargassum from here on) which are only found in the Atlantic Ocean basin and are carried by currents into the Caribbean Sea, Gulf of Mexico, and Florida Straits (Wang et al., 2019). Harmful benthic and pelagic algal blooms, such as these, are occurring with increasing frequency, duration and scale globally with other similar events recorded in the Southern Atlantic and Northwestern Pacific regions (Sissini et al., 2017; Xiao et al., 2021). For example, pelagic Sargassum was sighted in 46% of shipboard observations in 2011-2020 across the Western Atlantic with higher prevalence in the Gulf of Mexico/Florida Straits region (Goodwin et al., 2022). The interannual variation and increasing density of Sargassum in recent decades (Johnson et al., 2013; Goodwin et al., 2022) may be primarily due to higher nutrient concentrations (i.e., from agricultural runoff, changes in mixed layer depth, and/or Saharan dust) and warmer temperatures (Gower and King, 2011; Wang et al., 2019).

While studies on live pelagic Sargassum highlight potential ecosystem benefits of blooms, such as providing habitats and nurseries for marine species (Wells and Rooker, 2004) and feeding particulate organic matter (POM) into the biological carbon pump through detrital shedding (Baker et al., 2018; Zhao et al., 2023), many studies have investigated the negative impacts of decaying Sargassum algae on coastal communities and shallow-water marine ecosystems. In 2011, high densities of beached pelagic Sargassum led to decreased tourism which in turn harmed local economies (Louime et al., 2017). Inorganic heavy metals and organic pollutants have been known to contaminate Sargassum through bioaccumulation, and when stressed, Sargassum may leach micropollutants such as chlordecone and arsenic into surrounding environments (Devault et al., 2022). Decaying Sargassum also reduces water quality by lowering pH and dissolved oxygen to hypoxic conditions as well as increasing concentrations of hydrogen sulfide and organic matter (van Tussenbroek et al., 2017). This reduction of water quality can lead to mass mortality events of coastal marine fishes, crustaceans, echinoderms, molluscs, and polychaetes (Rodríguez-Martínez et al., 2019). Larval coral swimming behavior (Antonio-Martínez et al., 2020) and adult survivorship (van Tussenbroek et al., 2017) also are impacted by decaying Sargassum which may lead to reduced reef resilience in the future. However, prior to decay, Sargassum may provide benefits to coral reefs by acting as a buffer against global climate change impacts.

Climate change (ocean warming and acidification) will have widespread negative impacts on coral physiology which can scale up to influence reef ecosystem health. Caribbean reefs have experienced warming along with increased frequency and duration of marine heat waves over the past century (Orr et al., 2005; Muñiz-Castillo et al., 2019; Bove et al., 2022). Heat stress has caused widespread coral bleaching and mortality (Hughes et al., 2018; Sully et al., 2019; Virgen-Urcelay and Donner, 2023) and may be linked to the increased prevalence of coral diseases (Miller and Richardson 2015; van Woesik and Randall, 2017). Ocean acidification (OA) shifts seawater carbonate chemistry equilibrium to favor net calcium carbonate (CaCO₃) dissolution rather than precipitation. Given that reef-building corals deposit CaCO₃ in the form of aragonite to build their skeletons (Farfan et al., 2022), decreased carbonate availability and seawater pH under OA decreases coral biomineralization (Erez et al., 2011). The reduction in coral calcification rates and increased CaCO₃ dissolution rates can result in loss of reef accretion and flattening (Alvarez-Filip et al., 2011; Perry et al., 2013; Toth et al., 2015). The combined impacts of future ocean warming and OA on coral reefs are projected to cause declines in global reef carbonate production (i.e., reef accretion) by 2100 under every future CO₂ emission scenario (Cornwall et al., 2021).

Macroalgae, such as Sargassum, may buffer against these impacts by locally increasing seawater pH and shading, or accelerate reef health decline through altered competitive interactions. Pelagic Sargassum algae can provide localized shading which has been shown to reduce the prevalence of coral bleaching and disease (Muller and van Woesik, 2009; van Woesik and McCaffrey, 2017). Benthic macroalgae can buffer against acidification through daytime net community production (i.e., photosynthesis) (Jompa and McCook, 2003; Page et al., 2016; Doo et al., 2020). Fleshy macroalgae also tend to maintain or increase growth and photosynthesis under acidification depending on their carbon affinity and uptake mechanism (Cornwall et al., 2017). Pelagic and benthic Sargassum has been shown to adapt to and even benefit from future ocean scenarios (Xu et al., 2017; Kumar et al., 2017; Gao et al., 2019). Additionally, the outcome of coral-algal interactions may be modified under acidification to favor macroalgae (McManus and Polsenberg, 2004; Diaz-Pulido et al., 2011; del Monaco et al., 2017), though this phenomenon is not consistent or well understood (Brown et al., 2018; Rölfer et al., 2021; Page et al., 2021). More research is needed to fully understand how coral-algal interactions may be modified under changing environmental conditions across species and regions.

The Florida Reef was once dominated by Acroporid corals which supported a variety of socio-ecological services (Cramer et al., 2020). However, over 80% of the Acroporid population has disappeared due to human impacts, historical disease outbreaks, hurricane damage, and bleaching events (Aronson & Precht, 2016; Brandt, 2009; Walton et al., 2018; Cramer et al., 2020) with Acropora cervicornis in particular taking on great losses (Muller et al., 2021; Dilworth et al., 2024). Consequently, these species are now listed as threatened under the United States Endangered Species Act (Miller and Chiappone, 2013) and critically endangered under the International Union for Conservation of Nature Red List of Threatened Species (Crabbe et al, 2022). Many coral restoration programs throughout the Caribbean are focused on recovering these declining populations to restore historical ecosystem functions of these reefs (Young et al., 2012; Schopmeyer et al., 2017), including at the location of this study, in the lower Florida Keys. Therefore, it is of particular interest to investigate how future ocean conditions will influence local and global coral restoration programs. We investigated the interaction between pelagic Sargassum and OA (reduced seawater pH₎ on growth and physiology of A. cervicornis over two months to determine how this coral-algal relationship may interact with future ocean conditions.

Global increases in frequency and size of pelagic Sargassum blooms as well as predicted worsening of ocean acidification (OA) are expected to negatively impact coral reefs in future climate change scenarios. Phase shifts from coral towards algal dominance have already been observed on many coral reefs globally, including in Florida, since benthic macroalgae outcompete corals for space, light, CO₂, and other resources through a variety of mechanisms that are often amplified by a changing climate (McCook et al., 2001; Hughes et al., 2007; Enochs et al., 2014; Hillard, 2015; Brown et al., 2018; Enochs et al., 2018; Brown et al., 2019; Biscéré et al., 2019; Muller et al., 2021). Therefore, restoration programs have focused on the addition of historically dominant reef-building species like A. cervicornis to Caribbean reefs. Previous studies have shown negative synergistic impacts of OA and coral-algal competition on coral growth and survivorship, including for acroporids (Anthony et al., 2011; Brown et al., 2019; Vieira, 2020; Rölfer et al., 2021). These studies, however, focused on benthic macroalgae. This is the first study to quantify the combined effects of pelagic Sargassum and OA on an endangered coral species A. cervicornis. Furthermore, we demonstrate that the impacts of Sargassum and OA on coral growth and photo-physiology depend on length of exposure. After 1 month, growth was negatively impacted by the combination of low seawater pH and Sargassum presence. These differences in growth, however, disappeared by the end of the experiment ( Figure 1 ). Coral photo physiology was mostly affected by isolated stressors (low seawater pH or Sargassum presence) but there were no negative synergistic impacts of OA and Sargassum on Y(II), Y(NPQ), or ETR_max, rather, the algal presence improves photosynthetic performance instead ( Figure 2 , Table 2 ).

Corals initially showed lower growth rates in the OA + Sargassum treatment after 1 month of exposure, but this difference disappeared after two months, suggesting a degree of acclimation to their environment. This is demonstrated to occur through phenotypic or genotypic plasticity in previous studies (Sekizawa et al., 2017; Muller et al., 2021; Million et al., 2022; Dilworth et al., 2024). Earlier studies show A. cervicornis growth decreases after exposure to OA conditions for 1-2 months (Renegar and Riegl, 2005; Towle et al., 2015; Enochs et al., 2018), but more recent literature has revealed unaffected and even improved growth rates under OA (Bedwell-Ivers et al., 2017; Camp et al., 2017; Enochs et al., 2018; Langdon and Atkinson, 2005; Muller et al., 2021). Negative impacts of OA on A. cervicornis growth can also emerge or be amplified when combined with elevated nutrients (Renegar and Riegl, 2005), making it difficult to isolate the effects of the carbonate environment from other abiotic factors. However, when ideal light and temperature conditions are met, seawater carbonate chemistry does not necessarily limit growth. Enochs et al. (2014) and Comeau et al. (2014a, b) show that the growth rates of Acroporid corals including A. cervicornis are negatively impacted by OA pH levels, but that light plays a crucial modulating role in photosynthetically processing the excess CO₂ in acidified seawater (Suggett et al., 2012). Growth rates can increase with CO₂ concentration if met with saturating light, as seen in our initial OA controls, but can decrease together with photosynthetic efficiency if other conditions remain unchanged and there is no alternative energy source available. In this study, average peak daylight PAR and seawater temperature across all experimental aquaria throughout the study was 373 ± 26.5 µmol m^-2 s^-1 and 28.5 ± 0.15°C, respectively. These experimental conditions are within the optimum range for A. cervicornis physiology, resulting in a normal growth rate range of 0.09 to 1.2 mg cm^-2 d^-1, and expressing commonly cited Y(II) and ETR_max values across multiple studies ( Table 4 ). Given that our PAR exposure was not saturating, it is unlikely that increased growth under OA conditions (T1) as described in Enochs’ and Comeau’s research, can be maintained in the long-term.

After one month (T1) OA conditions negatively impacted photosynthetic performance as measured through Y(II) ( Figure 2A ), indicating a reduced percentage of available energy was being used for photosynthesis than in ambient treatments. However, Y(NPQ) and ETR_max were statistically similar. Therefore, energy may have instead been allocated towards maintaining stable calcification rates in the OA + Sargassum treatment. By the end of the experiment, significantly lower Y(II) as well as higher Y(NPQ) in OA controls show corals were still stressed by their environment, indicating that photo-physiology appears to be more sensitive to low seawater pH than growth rates given the differences emerge as early as T0. Research shows mixed results in terms of photosynthetic performance under predicted future OA conditions. Biscéré et al. (2019) suggests that some acroporids show increased gross photosynthesis in OA conditions without highlighting extraordinary changes to growth rate, while Brien et al. (2016) shows that corals including acroporids exposed to OA conditions can experience decreased photosynthetic yield in the short-term without sacrificing growth. Studies like Tanvet et al. (2023) and DeMerlis et al. (2022) further suggest that certain acroporid species express varying degrees of short- and long-term growth and photosynthetic adaptation to changing seawater pH based on whether they live in an environment with fluctuating or stable pH and temperature. In Tanvet et al., acroporids adapt their photosynthetic performance to pH shifts and reduce negative impacts on growth, although this adaptation takes place across longer timescales. Our coral samples came from a reef-based nursery with naturally dynamic diel and seasonal pH levels which may have stabilized their average growth rates in response to pH extremes. In contrast, previous studies show a range of results where A. cervicornis has maintained stable photosynthetic performance but showed improved growth under OA conditions (Bedwell-Ivers et al., 2017) or where carbonate concentrations rather than pH has a stronger effect on photosynthetic performance (Schneider and Erez, 2006). This wide range of results is attributed in part to genotype and multifactorial environmental differences where it is difficult to predict how a particular combination of stressors can amplify or negate each other. However, the pattern of improved photosynthetic performance when exposed to Sargassum in our results has prompted the question of whether the algae was providing a compensatory energy source.

Growth and photosynthesis have been demonstrated to be fueled by the same internal DIC pool in some models (Langdon and Atkinson, 2005) which can be supplemented by heterotrophically sourced carbon as well as photosynthesis, meaning that changes in growth do not have to come at the expense of photosynthesis, and vice versa. Additional feeding by stressed corals could buffer against potential negative growth impacts from acidification (Towle et al., 2015). Therefore, fluctuations in photosynthesis in the short-term do not immediately translate to changes in growth if there are adequate alternative nutrient sources. Sargassum algae can have beneficial or detrimental effects on coral growth and photo-physiology depending on the life stage of the algae. As initially hypothesized, other studies show that healthy benthic Sargassum and other macroalgae can buffer against OA by raising seawater pH through photosynthesis during the day (Jompa and McCook, 2003; Hillard, 2015; Page et al., 2016; Doo et al., 2020), whereas bacterial breakdown of dead or dying macroalgae could have the opposite impact on seawater carbonate chemistry by releasing CO₂ and other organic material into the water. Decaying Sargassum also produces hydrogen sulfide which can reduce coral growth (Resiere et al., 2021). We excluded decaying algae from the study by replacing the Sargassum bundles weekly to reduce bacterial breakdown. We cannot guarantee full elimination of bacterial communities; however, measurements of ETR_max, Y(II) and Y(NPQ) of Sargassum thalli at the beginning and end of several 1-week exposure cycles indicated no negative change in Sargassum health ( Supplementary Figures 7 - 9 ). Throughout the experiment, the Sargassum bundles shed detrital particles into the aquaria which is a typical characteristic of Sargassum blooms during reproduction or over-crowding (Ateweberhan et al., 2008). This shedding likely increased the abundance of particulate organic matter (POM) available in each experimental aquarium leading to unexpected impacts on coral photo-physiology.

Y(II) and ETR_max became higher after one and two months respectively when Sargassum was present relative to controls. Given that the presence of Sargassum did not increase pH in any treatments as we had hypothesized ( Supplementary Figure 6 ), improved photosynthetic performance in corals exposed to algae may have been due to a shift in reliance on heterotrophic behavior rather than pH stress relief (i.e., feeding on Sargassum-derived POM). The energy allocation balance between the zooxanthellae (i.e., primary productivity) and coral polyps (i.e., heterotrophy) can shift to favor heterotrophy in response to environmental stressors such as ocean acidification (Edmunds, 2011; Agostini et al., 2021) and warming (Krueger et al., 2018). Ferrier-Pagès et al. (2003, 2021) describes how heterotrophy provides a complementary pathway for obtaining nutrients that are essential for amino acid synthesis used to maintain zooxanthellae photosynthetic apparatus as well as growth. Given that the improved photosynthetic performance does not translate to improved growth in our samples, we note that heterotrophy does not always guarantee increased growth rates in all corals, but can disproportionately supplement photosynthetic maintenance and efficiency in zooxanthellae (Dubinsky et al., 1990; Titlyanov et al., 2001a, b; Davy and Cook, 2001; Houlbrèque et al., 2003). Some studies show that heterotrophy increases amino acid synthesis used in photosynthetic apparatus repair rather than increasing the production of glycerol and glucose for growth in algae-invertebrate symbiont relationships (Swanson and Hoegh-Guldberg, 1998; Wang and Douglas, 1998). Increased photosynthetic efficiency (ETR_max) despite stable growth in Sargassum exposed corals likely resulted from a higher number of available photosynthetic units, reflected in our Y(II) results ( Figure 2A ), without growth-directed energy transfer, supporting the notion by Davy and Cook (2001) that nutrients gained from heterotrophy can be retained by the zooxanthellae rather than being transferred to their symbiont hosts for growth. We therefore suspect that the Sargassum treatments show better photosynthetic performance due to the availability of POM that can supplement the maintenance of photosynthetic apparatus across pH treatments but particularly in OA stressed corals which show a steep trend of decreased growth rate when no POM is available.

This study highlights more multi-stressor research is needed across time and ecological scales. Coral reefs in the Florida Keys are exposed to long-term climate change (ocean acidification) combined with faster and more frequent episodic coastal acidification (Strong et al., 2014; Hicks et al., 2022) in response to short-term regional (Sargassum blooms and storms) impacts. Multi-stressor experiments, therefore, need to reflect the varying time scales to capture the full range of effects on coral health. In isolation, our results show that A. cervicornis growth rates were not significantly affected by ocean acidification conditions within the timeframe of this experiment. Likewise, the presence of Sargassum also had no significant effect on growth. However, coral photosynthetic efficiency improved when exposed to Sargassum under current ambient pH levels as well as future ocean acidification scenarios, likely due to providing additional particulate organic matter to a heterotrophic nutrition pathway, supplementing the maintenance and performance of their symbiont zooxanthellae photosynthetic apparatus. Further research is needed to understand coral responses to stressors at a cellular level, and to scale up responses to community and ecosystem scales (Edmunds et al., 2016).