ANTECEDENTS 2 • Anteriors al 2001:

Occurrence and distribution

Benthic microalgae dominate in estuaries with large intertidal areas and contribute to primary production in these estuaries (Adams and Bate, 1999b). It has been shown that in most South African estuaries the microphytobenthic biomass could even contribute much more than phytoplankton to primary production and its importance is now being recognized (Rodriguez, 1993; Walker, 2003). In Rodriguez‟s study, it was only in the Sundays Estuary that the total phytoplankton biomass exceeded the microphytobenthos (Table 2.1), and this could be due to this estuary being channel-like and lacking adequate exposed intertidal areas for the benthic microalgae to colonise. A variety of physical, chemical, and biological factors may regulate the standing stock of benthic microalgae in shallow aquatic ecosystems. Assessment of the

35 effects of these factors is thus important to understand and manage these ecosystems (McIntyre et a1., 1996). Since many benthic diatom species are cosmopolitan, there have been considerations that estuarine species tolerate a broad range of environmental conditions

Table 2.1: The comparison of phytoplankton and microphytobenthos biomass (as kg chlorphyll- a/estuary) for selected South African systems (adapted from Rodriguez, 1993)

Estuary Whole estuary phytoplankton chlorophyll-a (kg)

Whole estuary benthic chlorophyll-a (kg) Goukou 0.07 23 Gourits 0.04 16 Keubooms 0.06 20 Gamtoos 17 14 Sundays 86 14

Although a number of algal divisions are found in the microphytobenthic community, the most dominant group is usually diatoms (Rodriguez, 1993; Barranguet et al., 1998; Brotas and Plante-Cuny, 1998). Rodriguez (1993) found 75% of the microphytobenthic community to be consisting of diatoms in the Swartkops Estuary. The composition of the diatom community may however change along the length of the estuary and with the level of nutrient loading in a system (Walker, 2003). Some studies have shown that an increase in riverine nutrient input leads to an increase in benthic microalgal biomass. The phytoplankton community quickly absorbs these nutrients, however, and eventually the benthic microalgae become shaded out by phytoplankton blooms (Adams and Bate, 1999b). Nevertheless, it has been noted that even under conditions of low nutrient availability in the water column, benthic microalgae can survive by benefiting from the relatively high nutrient concentrations in the pore water of sediment (Meyer and Meyer-Reil, 1999). Thus, water column nutrients usually have no direct relation to benthic microalgal biomass.

Alternatively, Underwood et al. (1998) found relations between the distribution patterns of some epipelic diatom taxa and salinity and nutrient gradients, particularly ammonium. Underwood et al. (1998) found that some diatom species were located and abundant according to the estuarine salinity and nutrient gradients along the Colne Estuary. Navicula phyllepta and Navicula gregaria were abundant at the meso- and oligohaline sites respectively and Pleurosigma angulatum and Plagiotropis vitrea were found at the polyhaline sites. Species that were found at the seaward end were Nitzschia frustulum, Cylindrotheca signata and Navicula pargemina. Findings from a study by Minne (2003), where a number of eastern and western Cape estuaries in South Africa were investigated (including the Bushmans Estuary), also showed a division of the diatom species into four groups according to water column salinity and nutrients. The data was presented with a Canonical Correspondence Analysis (CCA). The groups were divided into species associated with high salinity (Amphora arcus, Amphora coffeaeformis, Amphora sublaevis, Cylindrotheca closterium, Entemoneis paludosa, Gyrosigma prolongatum, Halsea crucigera,

36 Haslea ostrearia, Navicula salinicola, Navicula tenelloides, Nitzschia angularis, Opephora minuta, Plagiotrphis tayrecta, Planothidium delicatum and Seminavis species 2), low salinity (Nitzschia littoralis), high ammonium (Amphora suacutiuscula), high nitrate and soluble reactive phosphorus (Achnanthes delicatula, Amphora helenensis and Navicula perminuta). However, statistically, only salinity and ammonium had significant effects on the distribution of the diatom taxa; the nitrate and soluble reactive phosphorus had little effect. Most of the Bushmans Estuary diatom taxa were indicative of high salinity and high ammonium.

Other factors that control benthic biomass are water currents, light flux, depth, physical disturbance, grazing, sedimentary composition and disturbances and water speeds (McIntyre et al., 1996; Adams and Bate, 1999b). In a survey of a number of South African estuaries, Rodriguez (1993) found no clear pattern when comparing subtidal with intertidal sites. Nel (1998), however, found that in the Gamtoos Estuary intertidal biomass was two to three times higher than subtidal.

Sediment type influences microphytobenthic biomass (Walker, 2003) because it influences nutrient availability for microphytobenthic organisms. Fine cohesive estuarine sediments usually have high organic matter content, with high rates of bacterial mineralization and high porewater concentrations of dissolved nutrients, while sandflats are more oligotrophic (Admiraal, 1984). Longitudinally, the distribution of the microphytobenthic biomass was found to be strongly influenced by position in the Kwelera Estuary by Walker (2003). It was concluded that the more turbulent hydrological conditions and loose sediment in the mouth area did not allow biomass to develop. The distribution of biomass showed a consistent pattern of low level in sandy sediments near the mouth and higher concentrations at the muddier stations (Walker, 2003). However, when these findings were compared to results from a Swartkops study (Rodriguez, 1993), it was found that in the Swartkops Estuary the benthic microalgal biomass was high in the sandy sediments. Walker (2003) thus concluded that the level of exposure also influenced benthic microalgae. The microalage in the Swartkops Estuary were found in the sandy sediment because it occurred in areas where there was low tidal action and thus the sediment was stable. Due to the coarser nature of sand, high absorption of light could have also played a role. The microphytobenthos tend to be dominant in the upper 1 cm euphotic zone, according to Rodriguez (1993), and benthic microalgae have the potential to remain dormant in the dark until favourable conditions prevail (Sundbäck and Granéli, 1988). When sediment containing microalgae was exposed to the dark, the chlorophyll-a content only decreased slightly and then remained constant for several weeks. The chlorophyll-a content increased rapidly when this sediment was re-exposed to light (Sundbäck and Granéli, 1988).

There are processes that may disturb the benthic community and temporarily lead to the benthic flora taking up a planktonic habitat (Baillie and Welsh, 1980; Adams and Bate, 1999b). These disturbances could be wind mixing and tidal currents. It appears that biomass is higher in sheltered, muddy habitats than in exposed, sandy regions (Miller et al., 1996).

37 Sandy sediment is more „loose‟ and can easily be moved by tidal currents and thus forms an unstable environment for microalgae to attach and settle in. Therefore, shelter may be an important factor in their distribution. Light limitations associated with increased wave height as well as the physical disturbance caused by waves are the main cause of reduced biomass, (Fielding et al. 1988, Rodriguez 1993). Desiccation, as a result of a drop in water level, has a serious effect on the succession of benthic algal communities. Some diatom taxa have, however, been reported to be able to resist long periods of desiccation (van der Molen, 2000). Water speed determines sediment texture, which controls the accumulation of nutrient-rich organics. Higher flow rates lead to coarser, nutrient-poor sediments, while mud can sustain twice as much benthic microalgal production because it retains more nutrients (Adams and Bate, 1999b). Diatoms can attach themselves more easily to mud than sand and the solid environment provided by mud mitigates against mechanical damage (De Jonge, 1985). Davies and McIntire (1983) also found that biomass increased in sites with siltier sediment opposed to sandy sediments. A recent study on the Keurbooms, Mngazana, Gamtoos, Swartkops, Sundays and Mngazi estuaries by Snow (2007) showed that the microphytobenthic biomass had the strongest associations with sediment related variables. These were high organic content (> 3%) and fine sediment content (< 125 µm sediment contributes more than 20% of the sediment). These findings were similar to that reported for other systems. Benthic microalgal biomass was sampled in sediments collected from two sets of North Carolina estuaries, Massachusetts and Cape Cod bays, and Manukau Harbour in New Zealand. Comparisons of benthic microalgal biomass and sediment grain-size distributions in these coastal and estuarine ecosystems frequently showed a negative relationship between the proportion of fine-grained sediments and benthic microalgal biomass measured as chlorophyll-a. The highest sedimentary chlorophyll-a levels generally occurred in sediments with lower percentages of fine particles (diameter < 125 mm) (Cahoon et al., 1999).

Ecological importance

Benthic microalgae are now recognized as significant primary producers in shallow aquatic ecosystems (McIntyre et al. 1996). Their production and biomass can equal or surpass that of phytoplankton in the overlying water column. Rajesh et al. (2001) found the total annual production contributed by benthic microalgae to be more than that of the overlying water column (33.59 and 10.51 g C.m-2 respectively). Case studies on selected Cape estuaries show that the highest intertidal microalgal biomass was found in the Sundays Estuary (197 mg.m-2) and the highest subtidal in the Goukou Estuary (205 mg.m-2). In most of the estuaries the benthic microalgal biomass was higher than that of the phytoplankton, except for the Sundays and Gamtoos estuaries. Both these estuaries are surrounded by agricultural-dominated catchments and therefore had more phytoplankton biomass because of the fertiliser-enriched freshwater input (Adams and Bate, 1994b).

38 Benthic microalgae are likely to be important in nutrient cycling, and may act to control nutrient availability to other primary producers (Cahoon et al., 1999). They cycle nitrogen within the sediments by evolving oxygen during photosynthesis that inhibits denitrification (Dong and Underwood, 1998). Oxygen production by benthic microalgae also prevents the release of phosphate and ammonia from the sediment (Sundbäck and Granéli, 1988). Their photosynthetic activity has also been found to stimulate nitrification (conversion of ammonia to nitrate) in the sediment (Thornton et al., 1999). They support deposit feeders directly (Connor et al. 1982; McIntyre et al., 1996) and suspension feeders through resuspension by physical processes (Baillie and Welsh, 1980).

As producers of new organic matter, microphytobenthos can enter the benthic and pelagic food web; thus they form the key component of the carbon cycle in benthic environments. Furthermore, in shallow aquatic ecosystems, benthic microalgae provide a major food source for meio- and macro-invertebrate grazers such as annelids, nematodes, flat worms, crustaceans, mollusks and some demersal fishes and larvae (Rajesh et al., 2001). Finally, they play an ecological role in the stabilization of sediments through the production of extracellular polymeric substances during locomotion (Miller et al., 1996).

Disturbances and threats

Anthropogenic disturbances are increasingly placing the goods and services of the aquatic benthos under threat. The primary determinants of benthic microalgal composition and abundance (i.e. water depth, flow, sediment chemistry and grain-size) are being altered by the dredging of channels, the disposal of spoil, the discharge of pollutants and increased sedimentation from the land(Bishop, 2007).

Sediment disturbance

Benthic organisms are adapted to the natural processes of sediment movement, erosion and deposition (Turner and Miller, 1991; Miller et al., 1992). However, when sedimentation exceeds natural thresholds, then impacts may involve total loss of the community and subsequent colonization by pioneer species (Alongi, 1997; Miller et al., 2002). Extreme sediment disturbance events can result from man‟s modifications of the aquatic environment, and the scale and magnitude of these alterations can often greatly exceed that of natural occurrences. Probert (1984) listed the following human activities as being of great concern when it comes to disturbances on the benthic environment: dredging; spoil and mining waste disposal; marine mining; organic pollution; oil pollution; and bait digging.

Dredging activities for the purpose of opening estuarine mouths have become customary in temporarily open/closed estuaries for various reasons. Such disturbances result in flushing and sediment scouring, reducing the microalgal biomass stock. Anandraj et al. (2008)‟s study investigated the recovery of microalgal biomass and production following a breaching event

39 and the key environmental parameters influencing primary production during the open and recovery phases. This study established that the disturbance of the breaching event in the Mdloti Estuary drastically altered the dynamics of both benthic and pelagic microalgae. Following the breaching of the mouth, almost the entire stock (94–99%) of estuarine microalgal biomass was washed out to sea. However, after some time, the open mouth phase significantly stimulated the benthic microalgal production by almost an order of magnitude compared to the closed phase. This recovery of estuarine primary production and biomass appeared to be primarily influenced by optimal environmental conditions that prevailed during the open phase compared to the closed period, with the shallow waters (< 1 m) contributing to favourable light, temperature and nutrient levels for the benthic habitat (Anandraj et al., 2008). It should most importantly be noted that continuous flushing and sediment scouring prevent the buildup of microalgal biomass. Thus dredging, which is a proposed activity for the Bushmans Estuary, should be strongly regulated.

Licursi and Gómez (2009) assessed the effects of dredging on the structure and composition of diatom assemblages in a lowland stream (Rodrıguez Stream in Argentina). The results of the study showed that the effects of dredging in the stream involved two types of disturbances: the removal and destabilization of the substrate in the stream bed; and chemical changes and an alteration of the light environment in the water column. The physical and chemical modifications, after dredging, in the benthic habitat resulted in an immediate increase in the diversity and species numbers of the benthic diatoms, which decreased at the end of the study period. Also, in the post-dredging period, the sensitive benthic diatom species were replaced by species that seemed to be tolerant to organic pollution and eutrophication, resulting from the resuspension of sediment-trapped nutrients and organic matter due to the dredging (Licursi and Go‟mez, 2009).

Excessive sediment deposition can lead to burial, smothering or crushing of benthic organisms. Conversely, erosion removes sediment and organisms (Hall, 1994; Thistle et al., 1995). Both deposition and erosion can result in a change of bottom sediment level and possibly sediment grain size. Materials placement, for example dredge material disposal, should allow community responses to follow natural seasonal and successional trends and to exhibit minimal anthropogenic impacts (Miller et al., 2002). Unfortunately, there is little of the quantitative information necessary for predicting how materials placement, sediment deposition and erosion will affect the ecology of these environments.

Studies were conducted on the impacts of the introduction of the bivalve Tapes philippinarum in the Venice lagoon and its harvesting by hydraulic and mechanical dredges, which strongly increased the amount of sediment resuspension and settlement (Facca et al., 2002). This activity caused a marked increase in water turbidity and the disruption of the benthic microlayer of the lagoon bottoms. In the areas affected by the highest sedimentation fluxes, resuspension of many benthic taxa, such as Amphora, Cocconeis, Navicula, Nitzschia, Pleurosigma and Thalassiosira, occurred and so they were found in all the water column

40 samples and they were more abundant than exclusively planktonic diatoms (Facca et al., 2002).

Boating, like many other human activities, represents a major disturbance to the benthic habitat. There is a high susceptibility of sediment erosion due to boat activities, which cause waves that disturb intertidal sediments. Boating impact, through the suspension of sediment, can result in major alteration of bottom morphology and sediment grain-size (Osborne and Boak, 1999), resulting in sizeable effects on assemblages of the macrobenthos (Bishop, 2004). The disturbance and resuspension of the sediment are the major impacts, of which, in return decrease the biomass of the standing stocks of the benthic microalgae, due to physical removal and increases in turbidity.

Sediment contamination

Land-based nutrient pollution represents a significant human threat to aquatic environments. The findings of lab experiments on the reaction of benthic diatoms to artificial eutrophication showed a decrease of diversity and evenness with colonization time while species numbers initially increased but subsequently reached a plateau (Hillebrand and Sommer, 2000). This outcome was attributed to an increase in dominance of few species outgrowing their competitors (i.e. lowered evenness). The enhanced nutrient supply decreased microalgal diversity by increasing the dominance of single species in eutrophicated habitats. And thus, only few microalgal species respond significantly to nutrient enrichment.

Compared with macroorganisms, microorganisms are more sensitive to toxin contamination because their surface/volume ratio is higher and thus exposure to toxicants is more direct. Moreno-Garrido et al. (2007) conducted an investigation of the response of diatoms to sediments with different levels of pollutants, collected from the Aveiro Lagoon (Portugal). Benthic diatoms seem to be sensitive organisms in sediment toxicity tests. Among the microalgal species used, Cylindrotheca closterium seems to be a little more sensitive, although populations of all assayed species show comparable pattern responses when exposed to the different sampled sediments. The other species were Phaeodactylum tricornutum and Navicula sp. Concentrations of Sn, Zn, Hg, Cu and Cr (among all physico- chemical analyzed parameters) in the sediment had the most significant impacts on the benthic diatoms.

The results of an analysis done on the benthic diatoms of a metal-polluted stream in the Riou Mort watershed in France also showed that the diatom communities were negatively affected by the metal accumulation (consisting of cadmium and zinc) in the sediment (Morin et al., 2008). Morphological abnormalities were particularly evident in the genera Ulnaria and Fragilaria while the rest of the diatom community displayed induced tolerance, seen through structural impact and dominance of small, adnate species. This led to the reduction in species diversity as the species assemblages were characterized by taxa known to occur in metal-

41 polluted environments (i.e. high numbers of Eolimna minima, Nitzschia palea, Pinnularia parvulissima, Surirella brebissonii, Achnanthidium minutissimum, Navicula lanceolata and Surirella angusta were recorded).