Regime shifts in seagrass beds are characterised by a collapse of seagrass beds and a transition into either an algae dominated regime or a barren sediment regime. The key drivers are nutrient loading/eutrophication from e.g. agricultural run-off, and overfishing, which both cause slow changes in the system that eventually lead to a sudden collapse of the seagrass regime; or more abrupt shocks like physical disturbance, both anthropogenic and natural, and disease outbreaks that cause direct seagrass decline. Seagrass ecosystems provide valuable ecosystem services such as fishing grounds and coastal protection, which are lost when a shift occurs. Once the system has shifted into a new regime it is difficult or even impossible to restore it to its previous seagrass dominated state. Therefore ecosystem management should be focused on enhancing resilience in order to avoid a regime shift, e.g. limit nutrient input, reduce physical disturbance and prevent overfishing.
Key direct drivers
- Vegetation conversion and habitat fragmentation
- Harvest and resource consumption
- External inputs (eg fertilizers)
- Infrastructure development
- Species introduction or removal
- Environmental shocks (eg floods)
- Land use impacts are primarily off-site (e.g. dead zones)
- Marine & coastal
Key Ecosystem Processes
- Primary production
- Nutrient cycling
- Wild animal and plant products
- Climate regulation
- Water purification
- Regulation of soil erosion
- Aesthetic values
- Food and nutrition
- Livelihoods and economic activity
- Cultural, aesthetic and recreational values
Typical spatial scale
Typical time scale
- Irreversible (on 100 year time scale)
- Contemporary observations
Confidence: Existence of RS
- Well established – Wide agreement in the literature that the RS exists
Confidence: Mechanism underlying RS
- Well established – Wide agreement on the underlying mechanism
Links to other regime shifts
Seagrass beds are marine ecosystems that can be found in the subtidal and intertidal zones in the majority of oceans worldwide (Orth et al. 2006). Regime shifts in these systems have been identified as a transition to either an algae dominated regime (Valentine and Duffy 2006; Burkholder et al. 2007; Nyström et al. 2012) or a barren sediment regime (van der Heide et al. 2007, 2011; Nyström et al. 2012), although most literature interchangeably describes these phenomena as seagrass decline and not regime shifts. Although this review uses a social-ecological systems lens, the focus lies on the shift in the ecosystem, and humans are considered as beneficiaries of ecosystem services and as drivers of system change.
Seagrass dominated regime
Healthy seagrasses form large beds, usually dominated by one seagrass species. They are considered ecosystem engineers as they significantly modify the abiotic conditions of their ecosystem to benefit their own success, by reducing current speed, stabilising sediments and creating oligotrophic conditions by trapping inorganic and organic material (Duarte 2002; Orth et al. 2006; Burkholder et al. 2007). Together with epiphytic algae seagrasses form the basis of complex food webs, making these systems highly productive (Valentine and Duffy 2006). Seagrass beds also support high biodiversity and provide important habitats, refuges and nursery grounds for a variety of species, many of which are commercially and ecologically important (Orth et al. 2006).
Algae dominated regime
This regime is characterised by dominance of macroalgae (algae attached to the bottom sediments that can form extensive beds), phytoplankton (free-living, planktonic algae) or epiphytic algae (algae growing on the surface of seagrass leaves), or a combination thereof (Cardoso et al. 2004; Burkholder et al. 2007). They are inherently superior competitors to seagrass, particularly in high nutrient conditions such as eutrophication (Valentine and Duffy 2006), which is a characteristic of this regime. Under such conditions seagrasses are prone to smothering by epiphytes and encroachment by opportunistic macroalgae that can form beds that are resistant to seagrass recolonisation (Valentine and Duffy 2006). Shallow waters tend to be dominated by macroalgae and epiphytes, while deeper areas are dominated by phytoplankton (Burkholder et al. 2007). In general this regime supports lower biodiversity as the variety of habitats associated with seagrass beds are not provided (Duarte et al. 2006).
Bare sediment regime
A third alternate regime is that of a barren sediment landscape (van der Heide et al. 2007, 2011; Nyström et al. 2012). The shift can occur due to extensive removal of seagrasses or sudden disease outbreaks causing large seagrass die-off (van der Heide et al. 2007, 2011). In this regime sediments can easily be re-suspended, causing high turbidity and light attenuation due to a reduction in, or depletion of, the seagrass engineering function (van der Heide et al. 2011). The benthic sediments are coarse in comparison to the seagrass regime and can seasonally host macroalgal beds. Biodiversity is low and the community structure different compared to seagrass beds, as the seagrass habitats are removed (Cardoso et al. 2004).
Drivers and causes of the regime shift
Shift from Seagrass Beds to Algae Dominated Regime
The shift from seagrass beds to algal dominated state is driven by multiple stressors, but nutrient loading and overfishing stand out as key drivers (Burkholder et al. 2007). Seagrasses are dependent on high influx of light, oligotrophic conditions and sediment bottoms (Eklöf 2008). In coastal waters eutrophication causes an increase of epiphytic or macroalgal biomass, while in shallow parts it will cause phytoplankton blooms, reducing light penetration to a level that will no longer sustain seagrasses but promote algal dominance (Orth et al. 2006; Burkholder et al. 2007). The drivers of eutrophication are anthropogenic, such as nutrient input from agriculture, aquaculture and sewage (Duarte 2002; Burkholder et al. 2011).
There is evidence that altering food webs through overfishing has similar effects, or can further augment the effects of eutrophication, by reducing herbivory, thus releasing algae from the pressure of grazing which can lead to a shift in regimes (Heck Jr and Valentine 2007). Changes in food webs are in turn linked to increased coastal migration, tourism, increased unemployment rates and increased population in coastal areas (Eklöf 2008).
Another important driver is the sediment load in the water column since it contributes to turbidity, i.e. decreases light penetration. Erosion, coastal development and deforestation are the main drivers of increased sediment loading in the water column (Duarte 2002; de Boer 2007). Activities such as boating, anchoring, dredging and trawling can also affect seagrass beds negatively throughout a long period of time. They all cause water turbidity and resuspension of sediments as well as physical damage to the seagrasses. Resuspension of sediments can also lead to a release of nutrients, promoting algal growth (de Boer 2007).
Shift from Seagrass Beds to Barren Sediment Regime
Another shift that can occur is from seagrass beds to a barren sediment regime with increased turbidity and where seasonal macroalgae take over (Cardoso 2003). Drivers of this shift are mainly physical disturbances such as actual removal of beds from e.g. beach replenishment or dredging, and a wasting disease that can cause extensive seagrass die-off (Duarte 2002; Cardoso et al. 2004). These drivers are shocks to the system, thus it appears that the shift is more abrupt than the shift to the algae dominated state. Physical disturbance could either be anthropogenic, such as dredging, boating activities, trawling and various coastal developments; or natural, such as storms (Duarte 2002). Eutrophication can also be a driver for this shift, as in the Mondego estuary in Portugal, where the loss of seagrasses and their ability to bind sediments also resulted in a bare, coarse sediment regime (Cardoso et al. 2004).
How the regime shift works
The seagrass regime and associated feedback loops
Seagrass beds occur under low nutrient, clear water conditions created by seagrasses modifying the abiotic environment to favour their own growth (Burkholder et al. 2007; de Boer 2007). Herbivory keeps algal abundance low and facilitates healthy seagrass beds. Feedbacks maintaining the seagrass bed regime are primarily seagrasses reducing turbidity through absorption of nutrients and sediment stabilisation. Thus, light conditions are improved which otherwise work as a limiting factor for seagrass growth (Burkholder et al. 2007). Additionally, the sediment stabilisation reduces the resuspension of nutrients in the water column, which further controls algal blooms and prevents eutrophication (Duarte 2002). These feedback loops maintain the seagrass dominated regime.
External drivers can slowly undermine seagrass resilience by reducing the engineering function which hampers conditions for seagrass growth. This can eventually lead to a sudden shift to algal dominance due to a reversal of the aforementioned feedback loops once the thresholds have been crossed (Cardoso et al. 2004; Nyström et al. 2012). Such shifts show hysteretic behaviour. That is, a return to previous seagrass regime is difficult due to the alteration of feedback loops (Nyström et al. 2012) and the state can usually not be recovered by re-establishing previous environmental conditions (Scheffer et al. 2005).
Shift from Seagrass Beds to Algae Dominated Regime
The key drivers causing seagrasses to shift to an algal dominated regime are nutrient loading and overfishing (Valentine and Duffy 2006; Burkholder et al. 2007). Nutrient loading from agricultural run-off and sewage, will increase the available nutrients in the water column and possibly lead to a eutrophied state. Algae are superior competitors to seagrass under high nutrient levels and nutrient enrichment will therefore promote algal blooms (Duarte 2002; Valentine and Duffy 2006). This in turn decreases light conditions through an increase in turbidity by phytoplankton, shading by macroalgae and overgrowth (fouling) by epiphytic algae (Burkholder et al. 2007). Moreover, the phytoplankton blooms are further fuelled by decomposing algae and seagrasses as this releases nutrients into the water column (Eklöf 2008). It is difficult to determine a threshold of critical nutrient concentration since it is case specific and depends on factors such as current velocity and herbivory (Valentine and Duffy 2006; Burkholder et al. 2007). A more specific threshold is light availability and if the conditions drop below seagrass tolerance it can cause the regime to shift (de Boer 2007); however, light tolerance is species-specific (Orth et al. 2006).
Overfishing modifies community structure causing trophic cascades due to removal of top predators. This causes an increase in meso-predators which in turn will reduce herbivores through higher levels of predation. A reduction in herbivores releases epiphytic algae from grazing pressure, which leads to algal overgrowth on seagrasses. This eventually suffocates them by obstructing light, and since seagrasses engineer their own habitat the loss will make the environment less suitable for a recolonisation, due to resuspension of sediments (Heck Jr and Valentine 2006; Duarte 2002). Seagrass beds are dependent on grazers to feed on algae before they get too thick to be eaten (Heck Jr and Valentine 2006). The threshold in amount of herbivory is hard to identify but it can be reduced to the same threshold associated with light conditions (de Boer 2007). Herbivory is important as it enhances the resilience of seagrass beds to nutrient enrichment by keeping algal population in low abundance (Valentine and Duffy 2006).
Once established, the algae dominated regime is maintained by the loss of seagrass engineering capacity which keeps the system in a high turbidity and nutrient state. Once macroalgal beds are established they are highly resistant to seagrass encroachment since they are better competitors under high nutrients levels (Valentine and Duffy 2006). In this regime oxygen depletion (anoxia) in the sediments is common due to higher levels of decomposing organic material and algal respiration as these processes consume oxygen, which eventually can result in hypoxia. This further prevents seagrass recolonisation as it causes an increase in hydrogen sulphide concentration in the sediments which is directly toxic to seagrasses. Such toxicity can also result in a decline in herbivores, thus reduce herbivore pressure (Burkholder et al. 2007) and further reinforce the algal dominance.
Shift from Seagrass Beds to Barren Sediment Regime
Both physical disturbance and diseases can remove extensive seagrass cover in one single event, which could eventually lead to a sudden collapse of the whole population and cause the regime shift (van der Heide et al. 2007). Although not specified, van der Heide et al. (2007) argue for the existence of a threshold in seagrass density below which the seagrass engineering function is severely reduced, thus causing high turbidity and poor light penetration. Hence, as which the shift to the algae regime, this can also be reduced to a threshold regarding the light availability. Such collapse has been observed in the seagrass Zostera marina in areas around the north Atlantic in the 1930's where extensive die-off of seagrass due to an outbreak of the wasting disease caused a shift to a barren sediment regime (Duarte et al. 2006). In the Dutch Wadden Sea the meadows have not yet recovered, which is believed to be due to a synergistic effect between the disease outbreak and subsequent eutrophication (van der Heide et al. 2007).
The barren regime is reinforced by the reversed feedback loop that is created by the seagrass engineering function and otherwise maintains the seagrass regime. Without seagrass cover currents are not attenuated and sediments and nutrients are resuspended, which cause increased turbidity and light conditions below seagrass tolerance. It is therefore extremely difficult for seagrasses to recolonize once this regime is established (Cardoso et al. 2004; van der Heide et al. 2007). Furthermore, the increased current velocity renders a mobile and coarse bottom substrate that undermines seagrass root attachment, which can result in any new seedlings or remaining plants becoming uprooted (Cardoso et al. 2004). Surviving seedlings are also prone to fouling by epiphytic algae, as grazing pressure is low in young seagrass patches since they provide poor refuges from predators, and this further inhibits seagrass re-establishment (Valentine and Duffy 2006).
Uncertainties regarding climate change and regime shifts
The aspects of climate change that have been shown to affect regime shifts in seagrasses are sea level rise, increased CO2 and temperature rise (Short and Neckles 1999, Duarte 2002). But the connection to a regime shift remains speculative due to a lack of research (Short and Neckles 1999) and the fact that the outcome of climate change is co-dependent on other human activities in marine areas (Borum et al. 2004); most effects will vary spatially and depend on species in question. Temperature rise will affect photosynthesis in both algae and seagrasses and will depend on species thermal preference, but it has been shown that epiphytic algae growing on eelgrass will be favoured by higher sea temperatures (Short and Neckles 1999). Sea level rise will result in seagrasses losing their habitat and being forced to move in order to regain the light conditions needed and in addition the sea level rise will cause erosion that further will decrease light conditions for seagrasses (Short and Neckles 1999; Borum et al. 2004). An increase in CO2 levels might lead to an advantage for seagrass over algae since they require more CO2, but this is contested since evidence is weak (Borum et al. 2004). Most significantly, climate change will increase the risk for more extreme weather with more frequent and bigger storms which will cause sediment resuspension decreasing light conditions together with physical disturbance (Short and Neckles 1999; Duarte 2002).
Impacts on ecosystem services and human well-being
Seagrass beds play a significant role in providing habitats and nursery grounds for marine organisms targeted for human consumption e.g. scallops, shrimps, crabs and juvenile fish (Duarte 2002; Terrados et al. 2004; Eklöf 2008; Barbier et al. 2011). Thus, they are important habitats which enhance the welfare of people who directly are dependent on its resources (De la Torre-Castro et al. 2004). If seagrass beds are lost due to a regime shift, its provisioning ecosystem services may diminish, which can be detrimental for the well-being of dependent people, especially affecting provision of food and livelihood. Fishermen, whose main source of income comes from seagrass-associated species, may be the user group most affected by the regime shift (De la Torre-Castro et al. 2004). Seagrass beds play an important regulating role by capturing carbon dioxide and transforming it into organic carbon (Duarte, 2002; Orth et al. 2006; Barbier et al. 2011). It has been suggested that the carbon stored in living seagrasses globally is on average 2.52±0.48 Mg C ha-1 (Fourqurean et al. 2012). Seagrass bed decline could lead to a significant loss in the CO2 sequestration capacity and reduction in carbon storage, with potential negative effects at the global scale associated with climate change.
Seagrass beds attenuate waves and stabilize sediments and in doing so reduce coastal erosion and erosion of bottom substrates (Duarte 2002; Orth et al. 2006; Eklöf 2008; Barbier et al. 2011). They also can reduce the effects of storms and extreme weather events like hurricanes, providing a coastal protection service. It can be assumed that the lack of this service may affect the sense of security as material security of coastal populations and socio-economic activities in place such as fisheries, tourism, marine transport and aquaculture. In turn, fishing activity associated with seagrass beds benefit consumers by meeting food demand at local but also distant locations. In terms of access to enough nutritious food as a constituents of well-being (Reid et al. 2005), a regime shift may impact the adequacy of material for a good life of especially coastal communities. In addition, although in a limited way, some communities benefit from seagrass in that it is used as raw material and as food, as well as a fertilizer in some other regions (De la Torre-Castro et al. 2004; Barbier et al. 2011).Non-material services related to the aesthetic and cultural values of seagrass beds that benefits some traditional groups (Kenworthy et al. 2006; Barbier et al. 2011) could be lost if a regime shift takes place. Although tourism may threaten seagrass beds (Ochieng et al. as cited in Eklöf 2008) they could have an overall positive effect on the tourist industry (Duarte 2002) by providing an aesthetic setting with high water clarity and habitats for diverse species (Barbier et al. 2011). Therefore, as regime shift resulting in a reduction of these services could have a potential negative effect on the tourism industry.
One of the most crucial management actions is to limit nutrient input. Important measures for doing this are limiting the use of fertilizers in agriculture; protecting marsh areas, as they can act as a buffer against nutrient loading; treating wastewater (Duarte 2002) and regulating its disposal so that it is discharged in areas with efficient water exchange. These measures are also effective for reducing organic matter loading. Human-provoked physical disturbance should also be controlled. For example, management should limit dredging and marine constructions to areas outside seagrass beds when possible, and should limit dredging and sand reclamation to short periods that seagrasses can overcome (Borum et al. 2004). Management should also regulate fishing activity in order to avoid overfishing on top-predators and prevent cascading effects in the food-web, which otherwise can lead to algal dominance (Eklöf 2008). Efforts should also be made at an international scale to mitigate climate change (Borum et al. 2004). For an effective implementation of these measures, it would be necessary to increase public awareness about the ecological functions seagrass beds carry out and the services they provide to society (Duarte 2002; Orth et al. 2006; Eklöf 2008).
Once seagrass ecosystems have shifted into a new state, recovery can be difficult or even irreversible in human time scale (Duarte 2002; van der Heide et al. 2007). Therefore, it is preferable to maintain or to build the resilience of these systems to prevent a regime shift, as restoring them once a shift has occurred can prove difficult if not impossible (Orth et al. 2006). In the event of a regime shift it is possible to return to a seagrass-dominated regime by resorting to seagrass transplantations. However these techniques have high costs and the success rates are low (Duarte 2002; van der Heide et al. 2007) therefore regime shifts are best prevented (Orth et al. 2006).
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