Ever since the 18th century, humanity has caused raised and still increasing emission of greenhouse gases (GHGs), mainly carbon dioxide (CO₂) with annual averages of 410 ppm in 2019 (IPCC, 2021) and predicted CO₂ levels four times higher compared to pre-industrial (Wigley, 1983) levels (IPCC, 2021). Global warming, including the rise of ocean temperature, is the most direct consequence of increasing CO₂ levels in the atmosphere. The ocean plays a relevant role mitigating the CO₂ rise in the atmosphere through the absorption of around a third of the anthropogenic emissions (Gruber et al., 2019). This CO₂ uptake impacts the chemical balance of seawater by increasing bicarbonate ion concentration (HCO₃^–) and reducing the availability of carbonate ions (CO₂^3–) by 60% (Feely et al., 2004). This shift in water chemistry results in a decrease of seawater pH, a process referred to as Ocean Acidification (OA; Doney et al., 2009). In fact, sea surface pH is expected to decrease from 0.3 to 0.5 units by the end of this century (Caldeira and Wickett, 2003). Ocean acidification is a global phenomenon, impacting calcification and metabolism of organisms, which has been documented in many marine regions (Kroeker et al., 2013).

The Mediterranean Sea is strongly affected by climate change and is among the marine regions with the highest rates of warming, from two to four times higher than in other ocean regions (Vargas-Yáñez et al., 2010; Burrows et al., 2011). Despite its high productivity, the semi-enclosed Mediterranean Sea is most likely to be more impacted by climate change than other seas (Richon et al., 2019), due to its physical properties with a short mixing and water exchange period of around 70 years (Durrieu de Madron et al., 2011). The Mediterranean Sea is therefore defined as a “hotspot for climate change” (Giorgi, 2006), with additional disturbances interacting in this region, both natural and anthropogenic (Lejeusne et al., 2010). Natural disturbances such as more extreme and frequent meteorological events (Parry, 2000; IPCC, 2013) and anthropogenic disturbances due to progressing urbanization, habitat destruction, pollution, overfishing, and species introduction induce additional pressure on the marine ecosystems (Lejeusne et al., 2010). The intrusion of invasive species into the Mediterranean has dramatically increased due to growing aquatic trade, aquaculture, maritime traffic (Raitsos et al., 2010) and most severe, the opening of the Suez Canal in 1869 and its latest widening in 2015 (Galil et al., 2015). More than 600 alien species have already established in the Mediterranean (Zenetos et al., 2017) and this number is expected to increase by 2050 (Sardain et al., 2019).

Although seagrasses occupy only a 0.1% of the ocean surface and their extension is limited to the coastal regions of temperate, sub- and tropical waters (Kennedy et al., 2010), their communities are among the most productive marine ecosystems (Duarte and Chiscano, 1999), modulate biogeochemical processes (Duarte, 1999), and provide valuable ecosystem functions (Costanza et al., 1997). Seagrass meadows form dense meadows providing food, habitat, and nursery grounds for various species (Duarte, 2002) and contribute to the physical protection of the coastal zone by providing wave attenuation and forming dense rhizomes below-ground stabilizing the sediment, thus preventing coastal erosion (Costanza et al., 1997; Fourqurean et al., 2012). Furthermore, they eliminate nutrients from the water column (Barry et al., 2013; Grall and Chauvaud, 2017), P. oceanica meadows are known to be net sinks for Nitrate and Phosphate (Barrón and Duarte, 2009) and contribute greatly to ecosystem resistance to eutrophication (Duarte, 1995; Lloret et al., 2008). Seagrasses have also demonstrated a high capacity of capturing CO₂ (Duarte et al., 2010, 2013), accounting for 20% of the global marine carbon sequestration (Duarte et al., 2013; Duarte and Krause-Jensen, 2017) and are referred to as blue carbon habitats (Macreadie et al., 2019). Seagrass meadows are mainly autotrophic, their productivity exceeds their carbon needs and they can export 24.3% of their production to adjacent ecosystems (Duarte, 2002), or even up to 50–70% (Kennedy et al., 2010). By removing carbon, seagrass canopies also locally mitigate the effects of OA during the daytime, acting as a buffer increasing pH in their canopies (Hendriks et al., 2014).

However, seagrass meadows are susceptible to various threats to their habitat, and face most of the serious threats to marine ecosystems: physical modifications by human activity, decreasing water quality, pressure from invasive species and climate change (Waycott et al., 2009). The Western Mediterranean basin accounts for a total of 510,715 ha of Posidonia oceanica meadows (Telesca et al., 2015), the endemic seagrass species in the Mediterranean Sea, which represents the major coastal ecosystem of the Balearic Islands. Posidonia oceanica is distributed throughout the temperate Mediterranean Sea and is impacted by warming since elevated temperatures cause physiological stress and shoot mortality increases (Diaz-Almela et al., 2007; Marbà and Duarte, 2010). The slow-growing P. oceanica is prone to show a stronger negative response to higher temperatures, due to a low thermal tolerance with optimal temperatures for growth of 15.5–18°C (Olsen et al., 2012), although average optimum temperatures for photosynthesis are typically higher (30–32°C; Lee et al., 2007). More temperature tolerant species such as Cymodocea nodosa, a seagrass of tropical origin has a higher optimal temperature for growth (24.5°C) than the temperate P. oceanica (Olsen et al., 2012) and appears to be better adapted to increasing water temperature (Lee et al., 2007; Olsen et al., 2012; Savva et al., 2018). The tropical green alga Halimeda incrassata was reported for the first time in 2011 in Palma Bay (Balearic Islands), introduced most likely by recreational boats (Alós et al., 2016). The alga found favoring conditions to expand rapidly, forming dense meadows over 41% of the monitored area in Palma Bay between 2011 and 2015 (Alós et al., 2016). Still, to the best of our knowledge, a specific growth rate has not been estimated. Benefitting from increasing water temperatures, H. incrassata is more likely physiologically affected by water with a lower pH and less calcium carbonate available for calcification, than increasing temperatures, although through the link between photosynthesis and energy compensation calcification might not be impacted directly (Hofmann and Bischof, 2014). Gradually increasing temperatures with more frequent heatwaves are expected to severely impact the persistence of temperate species with low thermal tolerance (Short and Neckles, 1999; Jordà et al., 2012). Changes in the composition of marine vegetation and structure of seagrass meadows and hence changes in the metabolic activity of these habitats directly affect biogeochemical processes of the coastal zone, impacting the carbon sequestration capacity and the oxygen dynamics, thereby impairing the functioning of these coastal ecosystems (Sand-Jensen and Borum, 1991; Duarte, 1995). These ecosystems are heavily impacted by global warming and increased presence of exotic species (Han and Liu, 2014) and loss of seagrass meadows increases the risk of erosion of historically deposited carbon, releasing it from the sediment and emitting it to the atmosphere (Marbà et al., 2015).

Here we evaluate how three Mediterranean macrophyte species contribute to biogeochemical processes in the coastal zone by evaluating their metabolic activity during the most productive period of the year. We conduct field incubations to estimate oxygen production, directly linked to carbon consumption, and nutrient use comparing seagrass species P. oceanica and C. nodosa and the non-indigenous calcifying alga H. incrassata. We chose to evaluate two distinct time points during growth season, one in spring and one in summer, with expected differences in productivity peaks between the three species and within their preferred temperature optima. The western Mediterranean Sea shows a strong seasonality in temperature and we chose April, when temperatures start to rise and H. incrassata was observed entering an active state while spring is known as the most productive time for P. oceanica, and July, when temperatures start to reach the annual maxima. Additionally, to estimate a growth rate for the tropical H. incrassata, that can serve as an indicator of the mechanism for its rapid expansion in the Mediterranean Sea it is crucial to include the actual growth period. Possible shifts in community composition favoring species more tolerant to warmer temperatures will change the impact of coastal marine vegetation in the Mediterranean Sea on the carbon cycle and nutrient uptake. Our comparison between three macrophyte species with contrasting future trajectories highlights the importance of these vital coastal ecosystems in climate change mitigation and can help to predict changes we might expect in the future.

Marine macrophytes play a foundational role in coastal ecosystem productivity, though not all seagrass and macroalgae taxa have the same potential for eliminating CO₂ from the water column. The habitat of P. oceanica is a highly productive coastal ecosystem with a high potential for eliminating CO₂ from the water column. Posidonia oceanica’s large biomass and the formation of vast and dense meadows make it an invaluable carbon sink with a high capacity of carbon storage beneath its meadows. Although C. nodosa appears to have a more efficient metabolism when normalized by biomass, the superior biomass and physiology of P. oceanica provides a larger photosynthetic active surface than canopies of C. nodosa. However, the in-situ biomass of the macrophytes was rather low and values for metabolic response rates [>160 mmol O₂/d/m² for GPP and >125 mmol O₂/d/m² CR in P. oceanica meadows (Duarte et al., 2010; Champenois and Borges, 2012; Eggert, 2012); >160 mmol C/d/m² for GPP and >80 mmol C/d/m² for CR in C. nodosa after conversion from O₂ metabolic rates (Egea et al., 2020)] in previous studies exceeded the values measured in this study. The Mediterranean Sea has experienced a decline in seagrass coverage (Delgado et al., 1999), estimated to be between 13 and 38% of initial coverage of P. oceanica since 1960 (Marbà et al., 2014). Physiological stress due to progressing coastal eutrophication, enhanced organic loading of the water column and respective increased light attenuation are contributing to this decline (Brocke et al., 2015), and in fact, the available underwater light at our study site in Punta Negra was generally lower than in other locations in the Western Mediterranean (González-Correa et al., 2008). Additionally, the intrusion of non-indigenous species like H. incrassata have resulted in higher competition for nutrients and light (Davis and Fourqurean, 2001). Although the temperature measured in summer (25.68–27.12°C) is favorable to the settlement and colonization of H. incrassata, the growth rate of 0.93 new segments per day for the time period investigated is lower than for the congenerous H. tuna in a tropical reef system in Florida, probably related to environmental differences between these studies (Vroom et al., 2003). However, environmental differences to these studies on sites where Halimeda spp. are endemic are apparent and the growth rate for this study might be an underestimation due to its exponential growth pattern. H. incrassata maintains its basic functioning in an inactive state in low temperatures (15.09–17.38°C measured in spring) (Thorhaug, 1976) and benefits from a higher temperature in summer, increasing photosynthesis, and promoting calcification (Campbell et al., 2016). Evidently, we see the expected better metabolic performance of H. incrassata in summer, whereas the water temperature exceeded the preferred growing temperature range for P. oceanica (Olsen et al., 2012), which could reduce its growth to cope with thermal stress (Marín-Guirao et al., 2018). The observed decline in autotrophy in summer is in line with the observations of thermal stress in summer (García et al., 2013), specifically when seawater exceeds 28°C associated with the occurrence of heat waves (Marbà and Duarte, 2010), whereas the more tolerant C. nodosa seems to be less affected. The elevated NCP and decline in CR in summer suggests a resource reallocation toward growth rather than energy storage. Whole ecosystem metabolic rates calculated with oxygen data from the multiparametric sensors showed trends of increased productivity in summer in all habitats. Since the hydrolabs were installed 0.2 m above the seafloor, and the measurement of the oxygen profile in the water column is the net result of mixing of water bodies passing through various benthonic as well as pelagic compartments with lateral water movement the multiparametric sensors represent ecosystem values. The distinction between the three macrophyte species and each habitat can only be made with a system preventing this lateral movement like the benthic chambers. However, P. oceanica is known to export a substantial amount of its productivity toward adjacent ecosystems (Duarte, 2002; Kennedy et al., 2010) and the increase in NCP measured by the multiparametric sensors is possibly due to the export of oxygenated water out of P. oceanica meadows.

Apart from warming, the Mediterranean Sea shows a trend of decreasing pH of −0.0044 ± 0.00006 pH units per year (Flecha et al., 2015). Seagrass species might have the ability to increase productivity with decreasing pH, using CO₂ as an alternative carbon source; the photosynthetic activity and function of seagrass meadows causes fluctuations of 0.2–0.7 pH units (0.05–0.19 pH units in this study) on a daily scale, making them a valuable buffer system against OA (Hendriks et al., 2010, 2014). The major source of carbon for H. incrassata is the precipitation of bicarbonate to build up structural components, hence a higher calcification rate that can be observed in summer (Invers et al., 1997, 2001). However, for the vegetated sites with lower shoot density of C. nodosa and H. incrassata, we cannot rule out a substantial contribution of bacterial activity in the sediment to calcification rates, a correction for bare sediment did not lead to reliable results due to the large deviation within incubation settings. Although H. incrassata finds favorable conditions in the study site, its physiology is most likely to be negatively affected by progressing OA due to changes in the water chemistry and further limitation of carbonate (Nelson, 2009; Price et al., 2011; Hofmann and Bischof, 2014). Low water temperatures and elevated levels of CO₂ in spring present the additional risk of dissolution, although non-living segments of Halimeda spp. might be resistant to dissolution under elevated CO₂ (Peach et al., 2017). However, epiphytic coverage, although not investigated here, and potential nutrient limitations on plant growth cannot be excluded.

Nutrient availability is setting an overall limit for the development of seagrasses (Lucea et al., 2003) and the oligotrophic waters around the Balearic Islands are characterized by enriched nutrient concentrations during spring and low concentrations in summer (Alcoverro et al., 1997, 2001), corresponding with our findings. C:N:P ratios in the water column in our study exceeded the Seagrass Redfield Ratio of 500–550:25–30:1 (Duarte, 1990; Fourqurean et al., 2007). Low ratios in spring are likely to result from increased demand for nutrients due to favorable conditions for growth (Fourqurean et al., 2007), whereas increasing demand for N in summer is likely to lead to P limitation. In addition, our results suggest that the methodology used in this study might have led to P limitation within the incubation bags, most likely due to the limited volume of the incubation chamber (2.27 L for P. oceanica, 1.27 L for C. nodosa, and 1.11 L for H. incrassata). N:P ratios for P. oceanica were considerably higher (5.178 in spring and 3.741 in summer) than reported in previous work (Barrón and Duarte, 2009). Posidonia oceanica represents an important nutrient filter and acts as a net sink of inorganic nutrients, although associated micro- and macroalgae within the meadows contribute to nutrient depletion (Touchette and Burkholder, 2000). Posidonia oceanica depends on bioavailable NOX and ammonium as nitrogen sources and shows net uptake rates in both seasons, whereas it is assumed to be a net source of ammonium and DON on an annual scale (Barrón and Duarte, 2009). Yet, DON and its bioconversion into bioavailable forms by seagrass associated microbiota (Tarquinio et al., 2018) can function as an important alternative nitrogen source for seagrasses (Vonk et al., 2008; Van Engeland et al., 2011). In fact, P. oceanica seems to depend on DON as co-substrate during its optimal growth period in spring, the substantial uptake of DON during the day to meet the demand for biomass production decreases the overall net release of the habitat (Hemminga et al., 1991; Day et al., 2012). A net release of DON of 2.182 μM/m² per day in spring is far lower than in summer (14.575 μM/m² per day) and average daily rates based on annual rates (12.055 μM/m² per day; Barrón and Duarte, 2009). The utilization of DON as co-substrate is hindered in summer due to progressing P-limitation, overall decreased nutrient availability and intensified the competitive pressure by beneficial growth conditions for C. nodosa and H. incrassata. Whereas both tropical species are acting as net nutrient sources in spring, C. nodosa undertakes a shift to a net sink of NOX and ammonium, suggesting the utilization as a source of nitrogen under enhanced growth. H. incrassata presents a net source of inorganic nutrients even under favorable growth conditions in summer and together with a further decline of P. oceanica increases the risk of further eutrophication.

Concluding, temperature and its implications on metabolism is the key driver for the development of biomass of all three macrophytes and therefore for the vegetative structure and carbon sink activity in coastal settings. Yet, the data presented here also confirms the influence of changing environmental parameters between season on the metabolic activity of the macrophytes. A shift toward higher average temperatures as predicted in climate change scenarios (van Vuuren et al., 2011; IPCC, 2013) will lead to unfavorable conditions for P. oceanica, exceeding its temperature optimum and therefore contribute to further regression of P. oceanica (Telesca et al., 2015). Moreover, a rise in SST might facilitate the colonization by sub- and tropical species and ongoing warming facilitates the settlement and expansion of non-indigenous species such as H. incrassata. Furthermore, progressing nutrient limitation in coastal settings and advantages in competition for nutrients, light and space favoring macroalgae contributes to the decline of seagrasses (Van Tussenbroek and Van Dijk, 2007; Thomsen et al., 2009; Han and Liu, 2014). The loss of vital P. oceanica meadows threatens the autochthonous biodiversity, potentially causing a shift in coastal marine vegetation (Cheung et al., 2009; Lejeusne et al., 2010; Burrows et al., 2011). Further regression of P. oceanica and the inherent loss of ecosystem services will severely impact the productivity and biogeochemical cycling of the coastal ecosystem in the Mediterranean Sea.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

IH: conception. IH and SF: design of the study. LM: draft the first version of the manuscript. All authors conducted the relevant field work jointly, contributed to data acquisition and sample analysis, revised the manuscript critically, contributed, and had substantial impact on the final draft of the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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