Anthropogenic impacts on Thalassia testudinum Banks ex König
Many large-scales declines of seagrass meadows, affecting several different species in a wide geographical range, have been reported in recent decades (8); in more than 70% of the cases, human-induced disturbances have been held responsible for them (8, 21). Thalassia testudinum, in particular, is a species with a well-documented history of large die-offs and local declines (2, 12, 14, 17). Human-related changes in nutrient levels, salinity, composition of the biological community and climate have been identified as sources (or potential sources) of disturbance for this species.
Changes in nutrient levels: eutrophication.
Population growth and the massive use of fertilizers in agriculture have led to a generalized exponential increase in nutrient inputs to the coastal zones (8), which is most likely the main cause of seagrass decline worldwide (8). The most common mechanism for seagrass decline under eutrophic conditions is light reduction through stimulation of epiphytes, macroalgae and phytoplankton overgrowth (1, 7), although direct physiological responses such as ammonium toxicity may also contribute (1).
Specifically, seagrass leaves are often densely covered by epiphytic algae which can suppress seagrass productivity through the development of a thick coat as a result of nutrient enrichment (6, 7, 8); it has been proposed as a major mechanism for declines of seagrass meadows, and the importance of this factor has been experimentally proved for Th. testudinum (6, 7). However, it seems that the net effect of epiphytes on seagrass growth depends on a complex variety of ecological factors (7, 8). In a mesocosm experiment designed to test the effects of nutrient addition on the interactions among grazers, epiphytes, and Th. testudinum, it was shown that those effects depended critically on the intensity of grazing: in the presence of grazers, the turtle grass tended to produce a greater biomass in the tanks with higher nutrient load, but when grazers were absent, the direction of the effect was reversed, and plants with nutrients added grew less than the control plants (7).
Obviously, the control exerted by nutrient loads on this species’ productivity can led to shifts on the community composition and even to drastic alterations in seagrass beds dominance (1). The occurrence of those shifts has been experimentally demonstrated in Florida bay, where some areas previously dominated by Th. testudinum were intentionally fertilized with bird guano for eight years. For the first two years, T. testudinum production was positively affected by the nutrient enrichment, but gradually Halodule wrightii, normally an early-successional species in subtropical habitats, colonized the beds, and by the end of the study accounted for 97% of the aboveground seagrass biomass (1, 5). This shift in species dominance persisted at least eight years after nutrients were no longer added, suggesting that once an area has been fertilized, the system can be resistant to change (1).
The importance of considering watershed nutrient loads rather than water-column nutrient concentrations in assessing enriched conditions for Th. testudinum meadows (1) was shown in Sarasota Bay, Florida (24). There, the biomass and productivity of this species were negatively correlated with watershed N loads but not with water-column nutrient concentrations as assessed by routine monitoring programs (24). It demonstrates that the search for reliable early indicators of nutrient overenriched seagrass meadows is an urgent necessity in order to provide an effective management of these ecosystems (1); direct measures of water-column nutrients are generally ineffective, since in early phases of eutrophication the nutrients are rapidly taken up by plants, adsorbed to particulate sediments, or otherwise removed from the water (1).
Changes in salinity.
The role of human-induced changes in salinity as a possible cause of seagrass losses is not well understood (8). Some studies suggest that Th. testudinum meadows do not show an inmediate response to increased salinity; for example, a turtle grass meadow remained unaffected after more than six months exposure to the direct discharge of brine from a desalination plant (22). However, decreased freshwater inputs due to human activities have been proposed as a triggering factor for the most important die-off of Th. testudinum known to date, which occurred in Florida Bay in 1987 (17). About a third of the dense seagrass beds of western Florida were impacted over a period of just a year; 4,000 hectares were denuded and an additional 23,000 hectares were affected to a lesser degree (2, 17).
This die-off was probably the result of complex processes caused by an interaction of several factors (1), including eutrophication, enhanced pathogen virulence and elevated water temperatures (1, 12, 14, 16), but several authors indicate that increased salinity was a key factor in the initiation of this phenomenon (8, 12, 16, 27). Groundwater flow into the bay decreased as a result of extraction of water from the region’s aquifers (8, 27); canal construction, which diverted drainage water, further contributed to a diminished freshwater inflow (8, 27). This decrease in freshwater inflow supposedly caused a gradual transition in the original composition of the seagrass vegetation, resulting in dense monospecific meadows of Th. testudinum (27) that suffered a sudden decline, probably as a consequence of sulfide self-poisoning and other effects (1, 8, 12, 16).
Changes in composition of the biological community: invasive species.
A recent literature review has revealed that at least 56 non-native species, primarily invertebrates and seaweeds, have been introduced to seagrass meadows all around the world, largely through shipping/boating activities and aquaculture (26). There is, however, few specific data about the effects of these invasions, particularly for seagrass community structure and function (26).
Th. testudinum meadows have been locally colonized by the invasive green alga Caulerpa ollivieri Dostál, native from the Mediterranean Sea (26). To date, this alga has been reported from the Bahamas (11) and the Gulf of Mexico (9). A negative effect of C. ollivieri on Th. testudinum, by direct displacement, has been observed (11, 26). Eutrophication is considered a facilitating factor in the successful colonization of the meadows by C. ollivieri (11); in the locations were this invasive was recorded, Th. testudinum was covered by epiphytic algae, as typical under conditions of high nutrient loads, and C. ollivieri exhibited higher nutrient contents than native Caulerpa species, which was considered evidence for the role of sewage-derived nitrogen in its successful introduction (26). This proposition is consistent with the results of recent experiments in several different seagrass ecosystems, which confirmed that disturbance contributes to the invasibility of seagrass beds (26). Given the reduced knowledge about the role that introduced species, combined with nutrient pollution may play in global seagrass decline, more definitive studies and comprehensive surveys are required in this field (26).
The global change in Earth’s systems and functioning which is currently taking place, mainly due to anthropogenic release of greenhouse gases into the atmosphere, is likely to alter to some degree most of the terrestrial and marine ecosystems. Seagrass meadows in general, and Th. testudinum populations in particular, may potentially be impacted by many factors related to climate change, including higher atmospheric concentration of CO2, higher temperatures, rising sea level, increase in the frequency and intensity of storms and increase in UV-B radiation (20).
Rising levels of atmospheric CO2, and the consequent alterations in the CO2/HCO-3 equilibrium in marine water, is expected to have significant effects on seagrasses. Seagrass photosynthesis is frequently limited by the availability of dissolved inorganic carbon under natural conditions (20); it has been experimentally shown for Th. testudinum (3). This carbon limitation has been attributed to the thickness of the diffusion boundary layer surrounding leaf surfaces or to a relatively inefficient HCO-3 uptake system (20), factors which vary according to each species morphology and physiology (8). Differences among species in the ability to compete for carbon would be expected to lead to shifts in species abundances and distributions, but long-term experimental studies of seagrass community responses to carbon enrichment are lacking (20).
In a similar way, increasing water temperature will directly affect seagrass metabolism, which may result in changes in patterns of species abundance and distribution (20). These direct effects will depend on the individual species’ thermal tolerances and their optimum temperatures for photosynthesis, respiration, and growth. Rising temperatures may also alter seagrasses through direct effects on flowering and seed germination (20); in Th. testudinum, flowering is apparently controlled by the water temperature (15), which implies that a phenological impact could be expected.
As a consequence of global higher temperatures, which produce a thermal expansion of ocean water and an acceleration of polar ice cap melting (10, 20), sea level has been rising steadily along the 20th century (10). According to the IPCC 4th Assessment Report, the global average sea level rose about 3.1 mm/year over 1993 to 2003 (10); by the end of 21th century the projected level rise will go from 0.18 m to 0.59 m, depending on the emission scenarios (10), but the used model excludes future rapid dynamical changes in ice flow, which are likely to occur, resulting in even larger figures. The greatest direct impact of an increase in sea level will be an increase in the depth of water and the consequent reduction in available light to the bottom (20). A primary effect of increased water depth will be to alter the location of the maximum depth limit of plant growth, directly affecting seagrass distribution (20).
Increased global temperatures are expected to increase the intensity and frequency of extreme weather events (4). A regime of increased storm disturbance may lead to a decrease in distribution of climax species like Th. testudinum and an increase in abundance of early colonizing and mid-successional species within the seagrass community (20). It is due to the fact that recolonization in seagrasses occurs primarily by means of horizontal rhizome growth and branching; in Th. testudinum the rates for both processes are slow [around 70 cm/year for horizontal rhizome growth, and a branching rate of 1 branch/1600 internodes (8)] compared with the growing rates showed by other smaller seagrasses (8).
There is a general agreement that increases in the amount of UV-B radiation reaching the surface of the Earth will produce both mutagenic and physiological damage in plants, including seagrasses (20). For three seagrass species occurring in the Caribbean (Th. testudinum was not included in the study), it was shown that increased UV-B radiation negatively impacted their photosynthetic capacity (25). Under ozone depletion, increased UV-B radiation is most likely to affect tropical seagrass systems such as Th. testudinum meadows, where the greatest amount of direct UV light reaches the Earth’s surface (20).
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