Ruido en las señales

Submerged macrophytes are plants rooted in both soft subtidal and low intertidal substrata, whose leaves and stems are completely submersed for most states of the tide (Adams et al., 1999). There are about sixty such species worldwide. Touchette (2007) describes seagrasses as forming part of a critical, and fragile, ecosystem inhabiting shallow coastal embayments and estuaries throughout the world.

Occurrence and distribution

In South Africa the seagrass, Zostera capensis occupies the mudbanks of most permanently open Cape estuaries (Adams et al., 1999) and survives and grows best in the 15 to 35 PSU salinity range (Adams and Bate, 1994b). The leaf turnover of Z. capensis is in the order of days and shoot turnover is in the order of one to three months (Light and Woelkerling, 1992). During its life time, Z. capensis continually forms new leaves, and old leaves become senescent and detach, especially in late summer (Verhagen and Nienhuis, 1983). Halophila ovalis is an opportunistic species that seldom occurs on its own; it is usually associated with

21 Z. capensis (Day, 1981). It usually occupies estuaries immediately after flood events because it has the ability to rapidly colonize sandy substrata (Talbot et al., 1990). In temporarily open estuaries that are characterized by fluctuating salinities Ruppia cirrhosa occurs, however, it can also occur in the calm, brackish upper reaches of permanently open estuaries (Adams et al., 1992; Adams and Bate, 1994b).

Since these plants must photosynthesize, they are limited to growing submerged in the photic zone, and most occur in shallow water, but may grow in deeper areas where the water is particularly clear (Ohrel and Register, 2006). They are primarily limited to areas where they remain submerged, but some species can withstand exposure during low-water periods (e.g., low tide). However, prolonged exposure during low tide and inundation by deep water during high tide, especially when the water is cloudy, can make for undesirable habitat conditions. Desiccation or exposure periods can drastically affect the usually submerged aquatic vegetation. The ability of a submerged macrophyte to survive desiccation largely depends on its ability to recover from exposure, and its rapid ability to not only recuperate the desiccated leaves but also produce new leaves. Zostera capensis can recover within a day after short- term desiccation, while Ruppia cirrhosa took four days to recover (Adams and Bate, 1994b). The ability of Z. capensis to recover quickly is because of its possession of a leaf sheath that protects the basal meristem during exposure. However, with long periods of desiccation, Z. capensis cannot recover, as well as R. cirrhosa (Adams and Bate, 1994b). The rate of desiccation depends on light, temperature, humidity, wind, and nature and topography of the substrate. Waterlogged conditions of creek sediments and water being trapped in small pools or trapped within the seagrass beds allow seagrasses to meet the evaporative demand of their large leaves during tidal emergence (Talbot and Bate, 1987). Z. capensis is dominant in tidal marine South African estuaries because of its stronger morphological structure and ability to survive daily periods of exposure compared with that of R. cirrhosa (Adams and Bate, 1994b).

Salinity, temperature, and sediments also determine, to a large extent, which species can survive (Ohrel and Register, 2006). Heavy turbidity, siltation and decreased light penetration have been responsible for population losses in Kwa-Zulu Natal and Eastern Cape estuaries (Day, 1981). Below ground biomass often dominates the total plant biomass of seagrass communities (Stevenson, 1988; Kuo and McComb, 1989) because the plant allocates a big portion of their production to the roots (Duarte et al., 1998).

Seagrasses are sensitive to the deposition of sediment directly on top of them when the sediment deposition is greater than their ability to grow through it (McKenzie, 2007). Furthermore, sediment stability influences macrophyte colonization. Submerged macrophytes do not occur in systems where the sediment is constantly modified by dynamic processes (Adams et al., 1999). This was the case in the Palmiet River Estuary, found in a study by Adams and Talbot (1992), which is influenced by strong water currents and frequent

22 flooding. On the other hand the Kromme Estuary experienced increased biomass and area distribution of Zostera capensis. This was because freshwater inflow had been reduced and consequently sediment stability increased (Adams and Talbot, 1992).

Sediment characteristics affect seagrass growth, germination, survival and distribution. Sediment texture, in particular, affects diffusion of oxygen, rhizome elongation and levels of nutrients and phytotoxins, such as sulfides. Sandy-textured sediments tend to diffuse oxygen more readily, obstruct rhizome elongation, and have lower fertility. On the contrary, finer textured sediments will tend to have higher fertility, allow rhizome elongation, and will tend to have greater levels of anoxia as pore water will have less interaction with the overlying water column. These anaerobic conditions may stimulate germination in some species, but also result in elevated sulfide levels, which inhibit leaf biomass production in mature plants and are toxic to seedlings of some species (McKenzie, 2007).

In the Tweed River Estuary in New South Wales, Australia, Hossain (2005) found increases in area covered by seagrasses in the period 1999 to 2001. The increase was attributed to water clarity and salinity, which may be associated with drought conditions. Geomorphic stability was also considered as a contributor to seagrass increase. The study also showed variation in seagrass biomass between sites and periods of time (seasons). At the two different sites where seagrass biomass was monitored, the highest biomass of Zostera capicorni was recorded in spring. The mean biomass was 78 g.m-2 in the marine dominated open embayment site at Towra Point while at a site in the Tweed River Estuary the average mean biomass was 208 g.m-2. Both these sites were sandy marine deltas but differed in wave action and degree of pollution. The differing biomass was particularly attributed to high rates of sediment delivery in the Towra Point in Wooloova Bay (Hossain, 2005).

According to Adams et al. (1999), “in estuaries subject to episodic flooding the related sedimentary disturbances appear to be the most important factor determining the state of seagrasses”. However, complete removal is also a factor. For example, in the Kwelera and Nahoon estuaries, a 15 year flood completely removed Zostera capensis beds (Talbot et al., 1990). Adams et al. (1999) have noted that it is the moderate (2-3 years) and light floods (1 year) that lead to fluvial deposits and smothering of macrophyte beds, resulting in impaired growth and shortened leaf lengths. Also, currents that are greater than 1 m.s-1 have been said to result in the removal of submerged macrophytes (Adams et al., 1999), while 0.5 m.s-1 results in mechanical damage and those less than 0.1 m.s-1 favour the growth and establishment of the macrophytes (Adams, 2008). Studies on South African estuaries have shown that changes in Z. capensis biomass are linked to flooding activities rather than seasonal influences (Edgecumbe, 1980; Talbot et al., 1990). Sediment loading and removal caused by flooding can disturb the submerged macrophyte community. This would lead to reductions in light, and increased concentrations of silt, organic matter and nutrients (Campbell and McKenzie, 2001, 2004). In the Sandy Strait, Queensland the loss and recovery of intertidal seagrass meadows were assessed following the flood related catastrophic loss of

23 seagrass meadows in February 1999. Mapping surveys showed that approximately 90% of intertidal seagrasses in the northern Great Sandy Strait disappeared after the February 1999 flooding of the Mary River. Full recovery of all seagrass meadows took 3 years. Reduced water quality that was characterised by 2-3 fold increases in turbidity and nutrient concentrations during the 6 months following the flood, was followed by a 95% loss of seagrass meadows in the region. Reduction in available light due to increased flood associated turbidity in February 1999 was the likely cause of seagrass loss (Campbell and McKenzie, 2004).

On the other hand, due to the construction of water storage dams, the frequency of flooding events has been reduced. This leads to an increase in the growth and expansion of submerged macrophytes (Adams et al., 1999). This has been the case in the freshwater deprived Kromme Estuary, where upriver dams reduce the effect of all floods smaller than 1-in-30 years (Bickerton and Pierce, 1988). The submerged macrophytes in this estuary have expanded due to increased sediment stability and improved water clarity that was related to a lack of freshwater input (Adams and Talbot, 1992). Adams (2005) noticed that, since the construction of the Mpofu Dam, Zostera capensis biomass in the Kromme Estuary increased from 217 to 273 g.m-2 (Adams and Talbot, 1992). The reduced flooding and stable salinity and sediment conditions, due to the dam, had promoted the growth of the macrophyte (Adams, 2005).

Ecological importance

Seagrass meadows are a major source of primary production, providing habitat and food for associated organisms (Austoni et al., 2007). Under optimal conditions, seagrasses are highly productive with biomass accumulation rates comparable to many agriculturally important plant species. Aboveground tissues also provide substrate for epiphytic organisms, which further enhances total productivity of the system by as much as 35% (Touchette, 2007). Submerged macrophyte beds are highly diverse and productive ecosystems, and can harbour hundreds of associated species from all phyla, for example juvenile and adult fish, epiphytic and free-living macroalgae and microalgae, mollusks, bristle worms, and nematodes (Ohrel and Register, 2006). In addition, juvenile and larval fish and crustaceans use the macrophyte beds as protective nurseries and to hide from predators (Whitfield, 1984; Ohrel and Register, 2006). Shedding crabs conceal themselves in the vegetation until their new shells have hardened (Ohrel and Register, 2006). Thus, as stated by Touchette (2007), apart from their ecological significance, seagrasses provide considerable economic value by contributing to recreational and commercial fisheries, and outdoor sporting activities (e.g. waterfowl hunting and tourism).

The macrophytes feed epifaunal and benthic invertebrates because detritus, diatoms and filamentous algae are trapped in them (Whitfield, 1989; Ohrel and Register, 2006). Indirectly they provide food for carnivorous fish species which feed on the diverse and abundant

24 invertebrates they harbour (Whitfield, 1984). Although only a few truly aquatic species consume the living plants (e.g., manatees, sea turtles, and some species of fish), several types of waterfowl and small mammals rely on them as a major portion of their diet (Ohrel and Register, 2006). Bait organisms are mainly found in the Zostera zone (Adams et al., 1999), for example, mudprawn (Upogebia africana), cracker shrimp (Alpheus crassimanus), bloodworm (Arenicola loveni) and pencil bait (Solen cylindraceus).

During the growing seasons of spring and summer, submerged macrophytes supply oxygen to the water through the process of photosynthesis, thereby helping to support the survival of aquatic organisms. They also play an important role in nutrient trapping and recycling (Adams et al., 1999). The plants take up large quantities of nutrients, which remain locked in the plant biomass throughout the warm weather seasons. As the plants die and decay in autumn, they slowly release the nutrients back into the ecosystem at a time when phytoplankton blooms pose less of a problem (Ohrel and Register, 2006). In Swartvlei, Potamogeton pectinatus acted as a nutrient pump by utilizing the sediment as a phosphorus source and releasing it into the water after decay (Howard-Williams and Allanson, 1987). Since roots bind the sediments on the estuary bottom and retard water currents, plants minimize water movement and allow suspended sediments to settle, thus improving water clarity (Fonseca et al., 1982; Ohrel and Register, 2006; McKenzie, 2007). The submerged macrophyte community acts as a protection layer (buffer) between the coast and the catchment environment. The macrophyte beds buffer the shoreline and minimize erosion by dampening the energy of incoming waves (Ohrel and Register, 2006). They also affect coastal water quality by absorbing nutrients and trapping sediments acting as a buffer between catchment inputs and reef communities (McKenzie, 2007).

In the early to mid-1930s, the importance of seagrass became apparent after 90 % of Zostera marima was destroyed along the European and North American coasts. This catastrophic seagrass declines was called the “wasting disease” and while the primary cause of this episode has not been resolved, the geomorphological and biological consequences to seagrass loss became apparent. Often in the absence of seagrasses, it was noticeable that substrates became increasingly coarser, sandy beaches eroded to rocky slopes, and macroinvertebrate assemblages shifted from burrowing and deposit-feeding species to encrusted filter feeding organisms (Touchette, 2007). In North America, other organisms that rely on seagrasses as food or habitat also declined with eelgrass disappearance, including waterfowl (e.g. Branta bernicla) and shellfish (e.g. Argopecten irradians).

Disturbances and threats

According to the above important ecological facts, submerged macrophytes are an important component of marine ecosystems; however, their distribution is in decline due to anthropogenic disturbances and declining water quality (Austoni et al., 2007; Touchette,

25 2007). Such activities include cultural eutrophication, herbicide runoff, and increased turbidity related to coastal development, boat traffic, and dredging activities. Seagrasses are particularly vulnerable to environmental perturbations that result in diminished light availability, that is, eutrophication and suspended sediments (Touchette, 2007).

Recreational activities

Due to their diverse and protected nature, estuaries are popular recreational outlets with an ever-growing demand for leisure and recreational opportunities. Pressure on estuarine environments is thus an inevitable phenomenon, which then ends up affecting the biological inhabitants. Recreational boating can result in an increase in turbidity which then reduces light penetration into the water column (Forbes, 1999; Adams, 2005). This reduces photosynthetic activity, and has been thought to be one of the major factors responsible for reduced biomass of submerged macrophytes (Mason and Bryant, 1975).

It has been noted that boats, with two-stroke outboard motors, release about 40 % fuel into the water (Muratori, 1968). Substantial amounts of fuel enter water courses and rapidly become dispersed through the mixing action of the propellers, which detrimentally affects water quality (Forbes, 1998). A retardation of plant growth due to boat emissions was observed in the Bushmans Estuary by Hooker (1996) but the concentration of these emissions was not sufficiently toxic to kill the plants over the four week study period. The fuel compounds, which mostly consist of raw fuel, non-volatile oil, volatile oil, lead and phenols (Jackivics and Kuzminski, 1973), can also retard faunal growth by inhibiting respiratory appendages from functioning adequately (Forbes, 1998).

Hooker (1996) also highlighted the physical removal of the plants by boat propellers. The finding was that up to 58 % of the total biomass of Z. capensis beds can be lost at one time when a boat is driven over the beds.

Bait digging was another activity that was found to have a big impact on the Zostera capensis beds of the Bushmans Estuary (Hooker, 1996). In the areas where bait digging was occurring the submerged macrophytes were growing sparsely. Marginal vegetation may also be damaged by people walking parallel to the waters edge or seeking access to the water for swimming and fishing. Forbes (1999) found that low levels of human trampling decrease both the total plant cover and species diversity in a variety of habitats.

Increased nutrient input

While nitrogen and phosphorus may play an important role in the growth of aquatic macrophytes, an excess of these can have deleterious effects. With high nutrient concentrations, the macroscopic and microscopic algae grow in large amounts and become abundant as attached epiphytes or free floating forms, reducing light penetration in the water

26 column (McKenzie, 2007; Austoni et al., 2007; Touchette, 2007). Increased epiphytic growth can result in up to 65% shading of the macrophyte leaves, reducing photosynthetic rate and leaf densities of the seagrasses (McKenzie, 2007). As the problem progresses, internal equilibria undergo a short circuit and the imbalance of phosphorus to nitrogen ratio can favour cyanobacteria and/or picoplankton species (Austoni et al., 2007) as well as nutrient toxicity (e.g. NH4+ and NO

−2

; Touchette, 2007). Macroalgal blooms have been recognized as one of the most catastrophic symptoms of community degeneration. In a study by Campbell and McKenzie (2001), investigations on seagrass meadows have been undertaken in Queensland in order to provide an early warning mechanism for detecting potential threats and damage to seagrass resources. A persistant and frequent abundance of filamentous epiphytic algae on seagrass in Whitsundays was detected and was cause for concern as these algae place at risk important productive seagrass meadows used for feeding by dugong and turtle populations. The excessive abundance of filamentous algae in Pioneer Bay appears to be detrimentally impacting the density of seagrasses in the region. Sewage derived nitrogen has been implicated in the growth of filamentous algae. There are, however, many factors that can lead to filamentous algal blooms and these include nutrient enrichment, organic enrichment and favourable light and temperature conditions (Campbell and McKenzie, 2001).

Other anthropogenic disturbances

A case of complete destruction of Zostera marina in the Thau lagoon (French Mediterranean Sea) has occurred and recolonisation of this macrophyte was studied (Plus et al., 2003). For many years, the Thau lagoon (south Mediterranean coast of France) suffered from anoxic events. The triggering factor was the degradation of green algae and probably organic matter coming from aquaculture, accelerated by high temperatures. Proportional oxygen saturation decreased to 0% in bottom waters during the episode, and toxic sulphuric compounds were released by the sediment (Plus et al., 2003). Subsequently, benthic vegetation which had been previously described as dense within the shellfish cultivation structures, comprising of Zostera marina meadows mixed with Gracilaria spp., Alsidium corallinum and Codium fragile populations, totally disappeared. Then, Plus et al. (2003) studied the recolonization of the eelgrass and found that the recolonisation took place surprisingly rapidly as biomass similar to those from untouched areas were reached only nine months after seed germination. The recolonisation success was partly due to a high seedling survival rate as well as a rapid vegetative recruitment (ranging from 0.012 to 0.042 per day). Two phases of recovery could be observed: a rapid multiplication of shoots during the first 3 months was followed by an increase in biomass due to elongation of leaves.

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