Climate change: impacts on the Mediterranean seagrass Posidonia oceanica
Seagrasses are aquatic angiosperms that form coastal underwater meadows responsible for a variety of ecosystem services. There are 50 extant species of seagrass in temperate, subtropical, or tropical waters with a global coverage of between 300,000km2 and 600,000km2 (Fourqurean et al., 2012; Den Hartog, 1970; Hemminga and Duarte, 2000). Anthropogenic disturbances are reducing seagrass coverage by 5-7% per year, recently climate change (CC) resulting primarily from the combustion of fossil fuels has also been found to contribute to seagrass decline (Lejeusne et al., 2010; Marba and Duarte, 2010; Short and Neckles, 1999). CC affects oceans through ocean acidification, sea level rises, ocean warming and extreme weather events (Collins et al., 2013). The Mediterranean Sea is particularly susceptible to future CC due to its small size and is one of the fastest warming regions on Earth (Marba and Duarte, 2010; Burrows et al., 2011; Giorgi and Lionello, 2008; Boero, 2015). In addition, the Mediterranean Sea has been identified by the International Union for Conservation of Nature and Natural Resources (IUCN) as a biodiversity hotspot and plays host to an endemic species of seagrass, Posidonia oceanica (P.oceanica) (Cuttelod et al., 2009). P.oceanica are large, long-lived, slow-growing species present between 0.3-0.48 metres deep, in meadows covering up to 50,000km2 of the Mediterranean Sea (Bethoux and Copinmontegut, 1986; Diaz-Almela et al., 2007). The life history traits, as well as the light and temperature sensitivity of P.oceanica puts the future of the species at high risk to CC (Lejeusne et al., 2010). Ruiz et al., (2017) described the effects of CC on organisms as “a global experiment in adaptive capacity, as species tolerate, adapt, or die with changing conditions”. This essay will explore the potential effects by the end of the 21st century that CC will have on P.oceanica and the services that it provides.
- Ocean warming
P.oceanica has an upper thermal tolerance limit of 28°C. Increases in sea surface temperature (SST) above this limit induce thermal stress, which impairs the plants metabolism (Lee et al., 2007; Procaccini et al., 2012; Tuya et al., 2016). Increases in the mortality of P.oceanica accompany any significant increases in SST because thermal stress causes disruption of the photosynthetic balance between the amount of carbon fixed and respired, skewing the balance in favour of respiration and relieving the plant of valuable energy (Lee et al., 2007; Collier and Waycott, 2014; Jorda et al., 2012). Annual maximum SST’s have exceeded the upper thermal limit of P.oceanica in most years since the turn of the 21st century (Jorda et al., 2012; Temperatures, 2018). By 2100 the mean SST in the Mediterranean will be 5.8°C higher than at present, and the upper thermal tolerance limit of P.oceanica is likely to be exceeded on a frequent basis by annual SST maxima (Sakalli, 2017). Jorda et al., (2012) predicted a functional extinction, or a reduction to less than 10% of the current population size of P.oceanica by 2049(±10 years). The functional extinction is predicted for the year 2093(±7 years) when only increases in SST are considered (Jorda et al., 2012).
Jorda et al., (2012)’s study incorporated only the effects of ocean warming on photosynthesis and respiration, however ocean warming also affects the reproductive mechanisms used by P.oceanica (Ruiz et al., 2017). In a similar fashion to terrestrial plants, P.oceanica switches from clonal growth to sexual reproduction when exposed to high temperatures (Carey et al., 2002; Diaz-Almela et al., 2007). Ruiz et al., (2017) showed that this change to sexual reproduction, or flowering was a response to thermal stress by taking samples of P.oceanica and placing them in either elevated or control temperature groups; samples exposed to elevated temperatures displayed inflorescence whereas the controls showed no signs of flowering. This response to elevated temperature was also observed in situ during 2003, when a heatwave swept across the Mediterranean Sea and widespread inflorescence of P.oceanica occurred (Ruiz et al., 2017). Changing from clonal to sexual reproduction is beneficial to P.oceanica to overcome changing conditions, as sexual reproduction favours genetic variation. Epigenetic changes that provide resistance to warmer waters may become fixed within the next generation, and beneficial mutations may arise that confer additional environmental resistance (Ruiz et al., 2017). Furthermore, sexual reproduction involves seed dispersal, which can provide a route of escape from regions that induce thermal stress and seeds may survive severe impacts that living plants may not (Ruiz et al., 2017; Diaz-Almela et al., 2007). Through genetic plasticity, P.oceanica may be more resistant to a changing environment than previously thought.
Ocean warming also has indirect implications for P.oceanica. Excess nutrients under elevated temperatures may result in the creation of a toxic sediment in which P.oceanica cannot grow (Duarte, 2002). Another indirect impact involves competition for resources, which already occurs within P.oceanica meadows with algae. Algal growth will increase with rising SST’s and lead to reduced light availability as algal blooms discolour the water, increasing the turbidity by releasing pigments and toxins, thus hindering photosynthesis by P.oceanica (Neckles et al., 1993; Williams, 2007).
- Sea level rise
Light is a requirement for the growth of angiosperms and many species of temperate seagrass, including P.oceanica, base their distribution on light availability (Dennison and Alberte, 1985). Sea levels worldwide are predicted to increase by between 0.45 and 0.98 metres by the year 2100, resulting in meadows of P.oceanica becoming situated in deeper waters with reduced light penetration (Church et al., 2013). Sea level rises have occurred previously in history and P.oceanica populations have persisted, however the current rate of sea level rise is unprecedented and as one of the slowest growing plants with a low natural rate of sexual reproduction, P.oceanica may struggle to adapt to changes in light availability with rapid changes in depth (Collins et al., 2013; Short and Neckles, 1999). Furthermore, light availability is reduced by algal growth (P4.) and by self-shading (Hemminga and Duarte, 2000). Self-shading occurs when individuals grow above the leaves of adjacent plants to obtain light, consequently this reduces the light available for the plants beneath; as sea levels rise and light becomes more scarce, self-shading will increase due to increases in competition for light (Hemminga and Duarte, 2000). Experimental evidence where P.oceanica samples were exposed to high and low light environments, has shown that with reductions in light availability, concurrent reductions in shoot density, leaf width, number of shoots, and overall growth rate occur and these resulted in a higher chance of mortality (Short and Neckles, 1999). Assuming moderate greenhouse gas emissions throughout the 21st century, and thus moderate sea level rises of approximately 0.70 metres, the light available for P.oceanica meadows may be reduced by as much as 50%, which will reduce their growth by between 30% and 40% (Beer and Koch, 1996). In contrast to the effects of ocean warming, reductions in light availability reduce the prevalence of sexual reproduction within P.oceanica meadows due to a lack of available energy (Diaz-Almela et al., 2006).
- Extreme weather events
Climate models indicate increases in the frequency and the intensity of extreme events in the Mediterranean throughout the 21st century (Collins et al., 2013). Storm surges and heat waves pose major threats to P.oceanica meadows. Heatwaves are detrimental as they induce thermal stress, whereas storms can have a variety of impacts. Increased siltation due to disruption of sediment by storm surges, results in reduced availability of light for photosynthesis by P.oceanica and sand-waves may bury the plants (Duarte et al., 2004; Hemminga and Duarte, 2000). Cyclonic impact has been shown to increase the mortality of P.oceanica by uprooting individual plants, and cyclogenesis across the Mediterranean is high in future climate projections and therefore poses a threat to the future of P.oceanica populations (Giorgi and Lionello, 2008; Cote-Laurin et al., 2017).
- Ocean acidification
By 2100 the global ocean pH is predicted to drop by 0.4pH units, from 8.1 to 7.7 (Schnoor, 2014). The effects of ocean acidification on P.oceanica are highly dependent on local nutrient concentrations but in contrast to other impacts from CC they appear relatively beneficial (Ravaglioli et al., 2017). Productivity of P.oceanica meadows is likely to increase due to frequent carbon limitation throughout the Mediterranean, it is also one of the few species able to utilise hydrogen carbonate (HCO3–, a product of ocean acidification) in photosynthetic reactions (Short and Neckles, 1999; Hendriks et al., 2010). Carbon enrichment through ocean acidification may therefore provide P.oceanica with a competitive advantage over its algal competitors that are favoured by warming (Duarte et al., 2004). P.oceanica has displayed a greater tolerance to thermal stress in laboratory experiments where researchers prevented carbon from acting as a limiting factor (Vizzini et al., 2010). However as has been shown in coral reef ecosystems, it is also likely that ocean acidification may impair the sensory systems of inhabitants of seagrass meadows, thus leading to reductions in their species richness and biodiversity (Munday et al., 2009).
- Users of seagrass ecosystems
Few animals are solely dependent on seagrass ecosystems, however the endemic mussel Pinna nobilis (P.nobilis) is an exception and only exists within meadows of P.oceanica (Richardson et al., 1999). If functional extinction of P.oceanica meadows occurs, populations of P.nobilis will also be at risk of extinction. Other species utilise seagrass meadows in certain situations, such as the endangered green turtle Chelonia mydas (C.mydas), which grazes on P.oceanica during migration (Cuttelod et al., 2009). C.mydas would not suffer such dramatic impacts if a functional extinction occurred as they would be able to graze on other species of seagrass within the Mediterranean and elsewhere along their migratory paths.
Species abundance within meadows of P.oceanica is greater than in unvegetated areas as the ecosystem provides services such as protection from predation, enhanced food sources, and acts as a suitable habitat for nurseries (Vizzini et al., 2002; Hemminga and Duarte, 2000)
The capacity for a habitat to provide protection from predation is based on a threshold level of habitat complexity, below which the habitat is too simple to protect organisms (Vizzini et al., 2002). By 2100, meadows of P.oceanica are likely to have deteriorated substantially, due to CC and other detrimental activities, and may exhibit reduced canopy cover and fewer individual plants. Mediterranean seagrass ecosystems may therefore become too simple in terms of habitat complexity to provide protection from predation.
Food sources rich in carbon and nitrogen, such as the detritus of P.oceanica as well as its leaves, rhizomes, and shoots, are essential dietary components for many small invertebrates living within meadows such as crustaceans (Vizzini et al., 2002; Hemminga, 1998). Consumers higher in the food web rely on animals such as crustacea and so nutrients from seagrass is transferred up through trophic levels (Hemminga and Duarte, 2000). Declines in P.oceanica populations, and reductions in the nutritional value of P.oceanica due to increased metabolic costs, could detrimentally affect the food webs within the Mediterranean Sea and result in decreased biodiversity.
Nursery habitats require shallow waters, and as sea levels rise meadows of P.oceanica may become unsuitable for use as nursery habitats due to their positioning in greater depths of the Mediterranean (Francour, 1997). This may result in increased mortality of juveniles within the seagrass ecosystems of the Mediterranean by 2100.
- Carbon storage
Seagrass ecosystems act as carbon sinks and store 15% of the carbon stored within marine ecosystems (Duarte and Chiscano, 1999). P.oceanica meadows store the most carbon of all seagrass species through the formation of layered mattes of carbon rich sediment (Fourqurean et al., 2012). The amount of carbon stored within the sediment beneath P.oceanica is approximately 362.4MgCha-1, and with a coverage estimated at 50,000km2 this equates to a total amount of carbon stored within P.oceanica sediment of 1.812Pg (Fourqurean et al., 2012). This figure does not include the carbon stored within living biomass, which has been estimated at 165.6MgCha-1 (Fourqurean et al., 2012). Seagrass meadows store roughly twice the amount of carbon per hectare than do terrestrial soils, and the globally averaged stored carbon within seagrass meadows is equal to that stored within tidal marshes and mangroves combined (Fourqurean et al., 2012).
Remineralisation of carbon within living biomass will occur rapidly upon destruction of seagrasses and the oxidisation of sediment carbon will follow (Fourqurean et al., 2012). One study has estimated the yearly return of carbon to the ocean-atmosphere system from remineralisation of P.oceanica biomass to be between 11.3-22.7TgCyr-1, and from oxidising of its sediment to be between 63-297TgCyr-1, and if these processes occur, a positive feedback mechanism for CC would take place upon degradation of P.oceanica (Fourqurean et al., 2012). If the upper estimates are true, the amount of carbon released back into the ocean-atmosphere system by 2100 would be 1.997PgC from living biomass, and potentially 26.136PgC from sediment carbon.
Atmosphere-Ocean-General-Circulation-Model’s from the Fourth Assessment Report by the Intergovernmental Panel on Climate Change (IPCC) were used for the projections of future SST by Jorda et al., (2012). Sea-level rises, and changes in ocean acidification were taken from the IPCC’s Fifth Assessment Report (Collins et al., 2013). These model projections constitute a source of uncertainty due to natural variability, uncertainty within the model, and the emissions scenario used (scenarios in this paper assumed moderate greenhouse gas emissions throughout the 21st century)(Stainforth et al., 2005; Deser et al., 2012). Extreme weather events are particularly difficult to predict due to exhibiting large natural variations, and constitute a greater source of uncertainty than other projections (Collins et al., 2013).
In conclusion, CC is likely to have significantly reduced the coverage of P.oceanica by the year 2100 and in result, carbon emissions to the ocean-atmosphere system will increase. The greatest threat from CC is ocean warming inducing thermal stress and promoting algal growth. The rise in sea level poses the second greatest threat to P.oceanica by reducing light availability, however through sexual reproduction induced by ocean warming, the migration of meadows to shallower waters may occur, and the previous habitat may be colonized by seagrass species with lower light requirements. Ocean acidification is relatively understudied and therefore it is more difficult to determine its significance in the future. Extreme weather events will likely damage the P.oceanica meadows in the Mediterranean and have been shown to reduce the overall species richness within the ecosystem, but how these events will progress through the 21st century is uncertain. Common responses by organisms to warming include northwards migration, however in P.oceanica the European continent will prevent direct northward shifts. It is essential for the longevity of this species that sexual reproduction provides resistance to these changing environments, or enables range shifts to allow expansion of the species’ distribution into the cooler North Atlantic Ocean. To protect this species, reductions in the emissions of greenhouse gases need to occur, and legislation should be updated with respect to the great importance of these ecosystems.
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