Biology and Ecology of the Benthic Algae

Abstract

This chapter describes the diversity of the microscopic and macroscopic benthic algal assemblages of the Bahía Blanca Estuary, including ecological aspects like their habitats, their role as primary producers, and the main interactions with other biota of the estuary. The microphytobenthic community is well developed in the soft sediments of the estuary. It is dominated by cyanobacteria and diatoms, which are key elements in the stabilization of sediments and nutrient cycling. They also interact with the macrobenthic fauna. On the other hand, the assemblages of macroscopic algae are poor in number of taxa. The majority of macroalgae are annual and opportunistic species, making use of the artificial substrate that is eventually available for their attachment. A few macroalgae are perennial mat-forming species, and there are also species considered exotic or introduced. Despite the fact that the little availability of hard substrate and the turbid waters limit the development of macroscopic algae, there are local species that flourish when conditions become favorable and produce blooms. These blooming species constitute promising candidates for their utilization in biomitigation. Although the benthic algae have been less studied than other biological groups, there is no doubt that these primary producers are vital components of this estuarial system.

6.1 What Are Algae?

Algae form a heterogeneous group of organisms that range from single microscopic cells to giant seaweeds belonging to diverse evolutionary lineages. The term algae has no formal taxonomic standing; it is routinely used to designate a polyphyletic, non-cohesive, and artificial group of eukaryotes and prokaryotic photosynthetic organisms. Algae include two main groups, according to their body size, macroscopic algae (macroalgae) and a highly diversified group of microorganisms known as microalgae (Barsanti and Gualtieri 2006). The profound diversity of forms, sizes, ecological niches, levels of organization, photosynthetic pigments, storage products, structural polysaccharides, and life histories reflects the separate evolutionary origins of this diverse group.

By definition, algae are considered photoautotrophs; they use sunlight and CO₂ to produce carbohydrates and ATP, depending entirely upon their photosynthetic apparatus for metabolic processes. However, most algal lineages include colorless heterotrophic species that obtain organic carbon from the environment, either by taking up dissolved substances or by engulfing bacteria and other cells. Some species of algae are called mixotrophs, as they combine both photoautotrophy and heterotrophy as nutritional strategies. There is a gradient among these three strategies; thus, the algae can be classified as obligate heterotrophic, facultative mixotrophic (e.g., some dinoflagellates), obligate phototrophic (e.g., Dinobryon Ehrenberg species), and obligate mixotrophic (e.g., Euglena Ehrenberg species) (Graham et al. 2016).

6.1.1 Habitats Colonized by Algae

Algae are mainly aquatic organisms , except for subaerial species that live exposed to the atmosphere and rely on liquid or vapor to carry out their metabolic functions. Aquatic algae display a broad range of tolerance to pH, temperature, turbidity, and concentrations of O₂ and CO₂, being able to colonize almost every aquatic environment; however, obligate photoautotrophic species are limited to shallow areas because of the rapid attenuation of light with depth. Aquatic algae can be found suspended in water bodies (planktonic algae), even under ice in polar areas, or attached to substrates or within sediments (benthic algae).

Benthic algae, either macroscopic or microscopic, can grow on stones (epilithic), on mud or sand (epipelic), on the thallus of other algae or plants (epiphytic), or on animals (epizoic). The term microphytobenthos is used to designate the community composed of eukaryotic microalgae, mainly diatoms, and cyanobacteria, that live on illuminated surfaces of a wide variety of aquatic habitats, ranging from tidal flats and marshes to submerged aquatic vegetation beds and subtidal sediments (Macintyre et al. 1996; Miller et al. 1996). The term periphyton is also used to designate this group of algae; however, it is more frequently used to refer to freshwater benthic microalgae. Even though microphytobenthos is less conspicuous than macroalgae or vascular plants, it contributes significantly to total primary productivity in coastal areas, and in many shallow aquatic systems, the biomass of the microphytobenthic community far exceeds that of phytoplankton (Pinckney and Zingmark 1993; Daehnick et al. 1992). The distribution of benthic microscopic algae varies extensively from place to place depending on the presence of suitable substrata, water depth, light availability, and physical perturbation (Sand-Jensen and Borum 1991). If strongly attenuated irradiances reach the sea bottom because of deep and/or turbid water, then benthic primary producers will be absent. In contrast, if high irradiances reach the bottom, as in shallow transparent waters, then the primary production of benthic microalgae can be dominant (Stevenson 1996).

Microphytobenthic algae occur in marine and freshwater habitats, while benthic macroalgae mainly habit marine environments. Large marine macroalgae are usually called seaweeds. Macroalgae that live in estuaries and marine coasts are usually classified according to the levels of the coast at which they occur. Supralittoral macroalgae are those that grow above the high-tide level, within the reach of waves and spray; intertidal macroalgae are those that grow on shores exposed to tidal cycles; and sublittoral macroalgae are those that grow in the benthic environment from the extreme low-water level to around 200 m deep (Graham et al. 2016). Their distribution along the coastal gradient is related with their photosynthetic capacities (red and brown macroalgae have accessory pigments that allow them to photosynthesize in regions where the light is attenuated) and their tolerance to salinity and desiccation. The influence of these factors on macroalgal assemblages will be described in Sect. 6.3.1.

6.1.2 Forms and Body Types of Algae

Many microalgal species occur solitary as unicellular individuals with or without flagella, hence motile or non-motile, in a variety of shapes. Other algae exist as aggregates of several single cells held together loosely or in a highly organized fashion, the colony. In these types of aggregates, the cell number is indefinite, growth occurs by cell division of its components, and each cell can survive on its own. When the number and arrangement of cells are determined at the time of origin and remain constant during the lifespan of the individual colony, this is termed coenobium (e.g., Volvox Linnaeus). Solitary and colonial species propelled by flagella are referred to as flagellates; however, not all flagellates include algal species.

Another common type of algal body is the filament, formed by a series of cells arranged end to end, with adjacent cells sharing a common cross wall, and forming chains where the daughter cells are connected to each other by their end wall. Filaments may be formed by one, two, or several rows of cells, and they may be unbranched as in Oscillatoria Vaucher ex Gomont (Cyanophyceae) or Ulothrix Kützing (Ulvophyceae), have false branching as in Tolypothrix Kützing ex É. Bornet and C. Flahault (Cyanophyceae), or have true branching as in Cladophora Kützing (Ulvophyceae) (Barsanti and Gualtieri 2006).

Macroalgal body is called thallus; it may be constructed by branched or unbranched filaments, coenocytic siphons (siphonous thallus), parenchyma, or pseudoparenchyma. Coenocytic thalli are composed of one giant multinucleate cell, lacking internal cell walls, except for septa that occur in reproductive states. Examples of this morphology can be found in the family Bryopsidales such as Bryopsis J.V. Lamouroux and Codium Stackhouse. Parenchymatous thallus is composed of tissues with a three-dimensional array of cells often connected by intercellular connections; this tissue organization is found in Ulva Linnaeus (Ulvophyceae) and many of the brown algae such as kelps. Pseudoparenchymatous algae are made up of a loose or close aggregation of numerous, intertwined, branched filaments that collectively form the thallus, held together by mucilages, especially in red algae such as Gelidium J.V. Lamouroux (Florideophyceae). Thallus construction is entirely based on a filamentous construction with little or no internal cell differentiation (Graham et al. 2016).

6.2 Classification of Algae

6.2.1 Taxonomic Classification

Among algal systematists, a wide range of classification schemes have been proposed (Bold and Wynne 1978; South and Whittick 1987; Margulis et al. 1990; Van den Hoek et al. 1995; Graham and Wilcox 2000). Considering the polyphyletic nature of algae as a group of organisms, algal classification is somewhat difficult to cope with the traditional taxonomic systems. However, it is still useful to represent the general characters and levels of organization, despite the fact that taxonomic opinion may change as new information accumulates.

The algae are traditionally classified into lineages or phyla, according to numerous characteristics: the photosynthetic pigments; the chemical nature of the energy storage product; the organization of the thylakoid membranes and other features of the chloroplasts; the composition and structure of the cell wall; the number, arrangement, and ultrastructure of the flagella; and the life cycle. Cyanobacteria make up a particular phylum of the domain Eubacteria, whereas eukaryotic algae are classified into more than 10 phyla of the domain Eukarya; these are Chlorophyta (green algae), Rhodophyta (red algae), Glaucophyta (glaucophytes), Cryptophyta (cryptomonads), Dinophyta (dinoflagellates), Bacillariophyta (diatoms), Phaeophyta (brown algae), Haptophyta (haptophytes), Chlorarachniophyta (chlorarachniophytes), and Euglenophyta (euglenoids). Molecular studies aiming to assess the internal genetic coherence of nuclear genes and ribosomal RNA are increasingly unraveling the relationships among these major lineages (Graham et al. 2016).

Cyanophyta (also known as blue-green algae, cyanobacteria, or cyanophytes) are unique algae, as they are prokaryotes. This is the most ancient algal lineage, with fossils dating back almost 3000 million years. The blue-green algae exhibit a variety of forms and are the most widely distributed of algal groups. Their cellular organization can be unicellular, branched or unbranched filamentous, or unspecialized colonial. The cyanophytes are distributed in marine and freshwater environments, occasionally forming blooms in eutrophic waters. They are an important component of benthic systems forming mats on soil, mudflats, and hot springs but are less conspicuous in soils along reef margins. Cyanobacteria can be found as symbiotic organisms in diatoms, ferns, lichens, cycads, sponges, algae, and other systems (Stewart et al. 1983; Costa and Lindblad 2002; Charpy et al. 2012; Rikkinen 2013).

Glaucophyta algae can be unicellular flagellates or form colonies in freshwater habitats, although some species can be found in soil samples. They are dorsoventrally constructed and have blue-green photosynthetic plastids. Glaucophytes are of particular importance in evolutionary studies because their plastids differ from those of other eukaryotic algae and resemble cyanobacteria in some way (Barsanti and Gualtieri 2006).

Red algae, or formally, Rhodophyta, occur as single cells, individual filaments, aggregations of filaments, or sheets of cells. Photosynthetic pigments are present in the red plastids of most species, except in certain parasitic genera. They are unusual among eukaryotes because of the lack of flagella in any stages of their life cycle and the presence of accessory phycobiliproteins organized in phycobilisomes. Although a few studies have noticed subtle motility of red algal propagules (Rosenvinge 1927; Geitler 1944; Lin et al. 1975; Hill et al. 1980; Pickett-Heaps et al. 2001), it is generally accepted that they are non-motile, especially compared with brown and green algae. The dispersal and settlement of red algal propagules are strongly dependent on the abiotic factors of the benthic environment (Ogata 1953; Luther 1976; Harlin and Lindbergh 1977). In most species, cytokinesis is incomplete; thus, the daughter cells are separated by a proteinaceous plug that fills the junction between cells (pit connection), which successively becomes a plug. Most red algae have sexual life cycles which usually involve alternation of three generations. Red algae are especially diverse and abundant in tropical and subtropical marine waters, but they are also present in freshwater and terrestrial environments. Red algae can be classified under two main classes, the Bangiophyceae that retain morphological characters that are found in the ancestral pool of red algae, ranging from single cells to multicellular filaments or sheetlike thalli, and the Florideophyceae that include morphologically complex red algae and are widely considered to be a derived, monophyletic group. One of the most striking features of the Florideophyceae is that they are the most diverse algal group regarding the thallus construction.

The phylum Phaeophyta is defined by one particular feature, that is, the presence of two different flagella in the cells. Flagellate cells are thus termed heterokont, possessing a long mastigonemate flagellum, and a short smooth one that points backward along the cell. This division includes several classes, Phaeophyceae, Bacillariophyceae, Cryptophyceae, Dictyochophyceae, Haptophyceae, and Xanthophyceae, of which the first two are the most relevant in coastal environments. The class Phaeophyceae (brown algae) is almost exclusively marine and is dominant in temperate waters. They include more than 250 genera, ranging from microscopic filaments to giant kelps that can reach 80 m long. Some species of Phaeophyceae display the greatest complex organization of tissues and cells among algae. Many have photosynthetic blades, as well as specialized blade-bearing stipes, holdfasts, and specialized conductive cells. The class Bacillariophyceae, integrated by organisms informally called diatoms, represents the most common algal group. They are very abundant and thus significant primary producers responsible for an estimated 20% of global carbon fixation. Diatoms dominate the phytoplankton of cold, nutrient-rich waters, such as upwelling areas of the oceans and recently circulated lake waters. Diatoms are the most significant producers of biogenic silica, dominating the marine silicon cycle. It is estimated that over 30 million km² of ocean floor is covered with sedimentary deposits of diatom frustules (Harris et al. 2006). These organisms are also important components of the benthic estuarine environment forming the microphytobenthic community.

The members of the phylum Dinophyta (dinoflagellates) are typically unicellular flagellates. Dinoflagellates have two flagella with independent beating patterns, conferring a characteristic rotatory swimming motion. Flagella are apically inserted in a region close to the midpoint of the ventral side of the cell. They are common components of the freshwater and marine habitats (Barsanti and Gualtieri 2006).

The phylum Euglenophyta includes mostly unicellular widely distributed flagellates; predominantly occupants of interfaces, such as the air-water and sediment-water boundaries. They are especially abundant in highly eutrophic environments and are known to be tolerant to extreme conditions of desiccation, low pH, and heat (Walne and Kivic 1990).

Chlorarachniophyta are amoeboid, coccoid or flagellate cells with secondary green plastids (Hibberd and Norris 1984). They are phototrophic and phagotrophic, engulfing bacteria, flagellates, and eukaryotic algae. The name chlorarachniophytes refers to the green color of their plastids and the spider shape of the cells. Chlorarachniophytes occur in temperate and tropical marine waters, growing among sand grains, on mud, in tide pools, on seaweeds, or in plankton.

The phylum Chlorophyta (green algae) displays a large range of somatic differentiation varying from flagellates to complex multicellular thalli differentiated into macroscopic structures that resemble organs. The different levels of thallus organization (unicellular, colonial, filamentous, siphonous, and parenchymatous) have served as the basis of their classification. Chlorophytes include at least nine lineages of early-diverging, unicellular prasinophytes (Lemieux et al. 2014) and a more-derived, monophyletic assemblage known as the “core Chlorophyta” (Fučikova et al. 2014). Traditionally, the chlorophytes were divided into the classes Ulvophyceae (ulvophyceans), Trebouxiophyceae (trebouxiophyceans), and Chlorophyceae (chlorophyceans).

The taxonomic treatment that will be used throughout this chapter for the algae occurring in the Bahía Blanca Estuary originates from morphological identifications of recently collected specimens or from local coastal reports. For this reason, some algae will be mentioned to the genus level, while others to the species level.

6.2.2 Morpho-functional Classification

In every biological community, each species occupies a unique ecological niche and commonly there are groups of species that utilize the resources in similar ways. That is, there are species that may be geographically distant and evolutionarily distinct, but have similar ecological functions in the ecosystem and thus occupy similar adaptive zones. As mentioned before, benthic algae can be single cells or large seaweeds with internal structural complexity. This variability and diversity can be simplified by classifying algae into functional-morphological categories. In oceanic systems, this classification is used to describe macroalgal assemblages (Vanderklift and Lavery 2000; Konar and Iken 2009), to address physiological questions (Littler and Arnold 1982; Johansson and Snoeijs 2002), and to examine the impact of several types of disturbance on benthic communities (Dethier 1981). The recognition of such aggregates by ecologists enables them to understand and predict the outcome of interspecific interactions and to interpret patterns in community structure without studying individual species (Steneck and Watling 1982). Littler and Littler (1980) and Steneck and Watling (1982) proposed models for algae, where the overall form of the thallus was hypothesized to predict aspects of its physiology and ecology, and resistance to consumers. The general models hypothesize that the type of growth and mineralization of algae dictates relative rates of primary productivity, growth rate, competitive ability, resistance to consumption by grazers, resistance to physical disturbance, tolerance to physiological stress, and successional stage, and that all of these functions are correlated with each other.

The model proposed by Littler and Littler (1984) considers algal form groups: sheet, filamentous, coarsely branched, thick leathery, jointed calcareous, and crustose. Steneck and Watling (1982) later created a slightly different ranking that included filamentous, foliose, corticated, leathery, articulated calcareous, and crustose forms. A more recent model of classification, proposed by Steneck and Dethier (1994), is based on the productivity and susceptibility to grazing, incorporating algal groups such as microalgae, filamentous, crustose, foliose, corticated foliose, corticated macrophyte, leathery macrophyte, and articulated calcareous (Table 6.1). Balata et al. (2011) proposed a new expanded classification of morphological functional groups based on several characteristics of the thallus like structure, growth form, branching pattern, and also on the taxonomic affinities of the alga (Table 6.2).

Table 6.1 Classification of algae into morpho-functional groups

Table 6.2 Classification of macroalgae from the Bahía Blanca Estuary into morpho-functional groups

6.3 Factors Affecting Algal Assemblages in Estuarine Environments

6.3.1 Abiotic Factors

Estuarial environments are fluctuating habitats , characterized by a mixture of freshwater and seawater which originates unstable conditions; hence, the communities that develop in estuaries are well adapted to this habitat. Physical and chemical factors of the estuarine environment clearly influence the functional morphology and behavior of the benthic communities. For example, in intertidal flats community structure is regulated by sediment particle size, oxygen concentration, salinity, and temperature, to which the species may respond differently (Coull 1999; Schweiger et al. 2008). Periodic inundation and exposure to air is harsh in these environments. Light intensity, salinity, pH, nutrient levels, grazing, and sediment stability limit the productivity of algae (Kennish 2017). In estuaries, high biogeochemical rates account for a relatively low number of species (Costanza et al. 1993); this is because only a limited number of species are adapted to salinity variation (Webb et al. 1997).

Microphytobenthic and macroalgal communities are regulated by light, temperature, and nutrient availability, which are the major parameters controlling their reproduction (Denis et al. 2012). Seaweeds disperse either as free-floating macroscopic forms or as microscopic propagules (e.g., spores, gametes, and zygotes). The spatial patterns of seaweed in estuaries are contingent upon the dispersal capabilities of the populations; hence, tidal currents play a crucial role in these habitats as they influence the dispersal, settlement, and attachment of macroalgae (Kennish 2017).

6.3.2 Biotic Interactions

Community structure of estuarine environments is influenced by various biotic interactions, involving grazing and competition (Buffan-Dubau and Carman 2000). The trophic dynamics of estuaries are complex because this environment is occupied by different types of primary producers such as phytoplankton, salt marsh plants, submersed seagrass, and benthic algae. Unlike the open sea, where practically all phytoplankton is consumed alive, in estuaries, primary producers are not heavily grazed, but die and begin to decompose before being consumed, contributing to the detritus food web (Omstedt et al. 2014). Algae generate abundant organic detritus constituting an important food source available all year round; they also can provide new habitats where some species can find a refuge from predators (Valiela et al. 1997; Raffaelli et al. 1998). Thus, organic matter from benthic macroalgae together with phytoplankton may support both benthic and pelagic food webs in the intertidal and adjacent subtidal areas of shallow bay systems (Kang et al. 2003). Macroalgal thallus tends to have higher nitrogen and phosphorus contents than seagrass tissues (Atkinson and Smith 1983; Duarte 1995). When macroalgal decomposition occurs, the derived nutrients accumulate and increase the nutritional value of the sediment, stimulating the growth of other primary producers, microalgae and bacteria (Rossi 2006), therefore promoting the increase in abundance and biomass of grazers and deposit feeders (Hull 1987; Ford et al. 1999; Rossi and Underwood 2002). In the case of organic matter transported through the water column, this is used by filter feeders such as oysters, clams, and mussels; while the organic matter that accumulates in the sediment is later used by deposit feeders such as worms, amphipods, and a many other small organisms (Day et al. 2013).

In estuarine soft sediments, macroalgae are often spatially distributed forming a mosaic of patches of different species interspersed with bare substratum (Berezina et al. 2007). Several studies have detected that benthic macroalgal communities support higher abundances of both epibenthos and infauna than do other comparable unvegetated bottoms (Summerson and Peterson 1984; Irlandi and Peterson 1991). The effects of macroalgae on benthic organisms are probably density dependent, because at moderate densities, macroalgae create a more heterogeneous environment (Thiel and Watling 1998). This favors the increase of subsurface deposit feeders and the abundance of epifaunal species, which find abundant shelter and food in the new algal substratum (Raffaelli et al. 1998). At high densities, macroalgal blooms alter the natural balance between production and decomposition of organic matter and can have dramatic effects on the local fauna (Valiela et al. 1997). The extent of these effects depends on the composition of the dominant faunal assemblages at the bloom onset, the magnitude and nature (drifting or steady) of the bloom, the season, and, to a lesser extent, the type of bloom-forming algae (Raffaelli et al. 1998).

Isaksson and Pihl (1992) observed that when algae cover approximately 30–50% of the surface in soft-bottom marine ecosystems, the abundance of epibenthic fauna associated with vegetation increases, whereas with algal coverages of 90%, the abundance of mobile epibenthic fauna declines. The decomposition of large deposits of macroalgae can affect the availability of oxygen in the sediment and cause episodes of anoxia and sulfide production, accentuated by reduced water flow under the algae and increased sedimentation rate (Nedergaard et al. 2002). In these situations, the abundance and diversity of the assemblages can decrease because animals can be displaced or killed or because of an alteration between predator and prey relationships (Renaud et al. 1999; Kelaher and Levinton 2003). In areas with fluctuating oxygen levels, mobile predators can temporarily leave hypoxic areas and then return when oxygen rises to capture the infaunal invertebrates that emerged during low oxygen (Nestlerode and Diaz 1998).

Infauna from shallow soft bottoms, for example burrowing adult bivalves, respond to high biomass of bloom-forming algae by migrating on the surface. Juvenile bivalves, on the other hand, can reach high abundance among algal strands and filaments, while highly mobile species, such as the gastropod Hydrobia W. Hartmann, 1821, often reach high densities in algal mats (Raffaelli et al. 1998). In contrast, Franz and Friedman (2002) observed that the blooms of Ulva lactuca Linnaeus drastically reduced the abundance of epibenthic copepods, attributing that reduction to the anoxic conditions registered within the algal mats. In drifting algae, Norkko et al. (2000) found high epifaunal abundance on the macroalgae Ectocarpus siliculosus (Dillwyn) Lyngbye and Pilayella littoralis (Linnaeus) Kjellman, with intermediate oxygen levels within the drifting seaweed, and only found hypoxic conditions at the algal-sediment interface. In the case of the mobile infauna, filamentous algae provide a refuge from physical stresses. However, for sedentary infauna, the cover by laminar algae forms a barrier between the animals and the oxygenated water column generating an adverse effect on survivorship (Perkins and Abbott 1972; Bach and Josselyn 1979; Dauer and Conner 1980). The physical structure provided by algae serves as a refuge and reduces the predation rate of mobile epibenthic species in soft-sediment communities (Lenanton et al. 1982; Robertson and Lenanton 1984; Marx and Herrnkind 1985; Wilson et al. 1990; Smith and Herrnkind 1992). For instance, the increased cover of Ulva and Cladophora reduces the predation rates of the crustaceans Crangon crangon (Linnaeus, 1758) and Carcinus maenas (Linnaeus, 1758) by the cod Gadus morhua (Linnaeus, 1758) (Isaksson et al. 1994; Pihl et al. 1995). The juveniles of many fish species also find shelter and abundant food between macroalgal communities, and, after reaching a certain size, they swim to deeper waters (Coles et al. 1993; Ross and Moser 1995; Rooker et al. 1998). Seagrass meadows thus play an important role as “nurseries” for numerous fish species (Heck et al. 2003).

In summary, anoxic conditions have an overall negative effect on the abundance of the faunal community in spite of all the other possible concomitant positive effects of the bloom (i.e., enhanced refuge, food, and structure for recruitment) (Sagasti et al. 2001). The relative tolerance of organisms to hypoxic conditions generated by algae may determine the increase or decrease of predation rates. For example, predation on larval fish by jellyfish can increase during hypoxic episodes, because jellyfish tolerate hypoxia, but larval fish are unable to evade predators in low oxygen. Concurrently, predation on larval fish by adult fish decreases, because the adult fish are intolerant to hypoxia (Breitburg et al. 1994).

On the other hand, it is important to mention the impact of herbivores on the biomass of benthic algae (i.e., top-down control). Microphytobenthic algae are affected by grazing (Hillebrand et al. 2000). Several studies report that the extent of herbivory on benthic algae is highly variable (Cebrian et al. 1998; Cebrian 1999, 2002). In some cases , herbivores may remove a large percentage of the production of microphytobenthic communities (Nicotri 1977; Baird and Ulanowicz 1993), but in other instances, herbivory only represents a minor loss for the community (Admiraal et al. 1983; Montagna 1984). In spite of the large variability found within each community type, microphytobenthos and macroalgae tend to lose higher percentages of primary production due to grazing than do seagrass communities (Bennett et al. 1999; Blanchard et al. 2001), influencing the dynamics of producers biomass and nutrient recycling.

6.4 Adaptations Mechanisms of the Benthic Algae

Estuaries are habitats with high variability; hence, the communities that live in them are frequently disturbed. Some species of algae rapidly recolonize the substrates after a disturbance; a new generation can appear within a few weeks, and several generations may develop in one year. Such a fast succession of generations allows the adaptation of algal species that are able to tolerate the abrupt changes that occur in estuarine conditions (Larsen and Sand-Jensen 2006). These changes favor the development of fast-growing, short-lived, and morphologically simple algae, like phytoplankton, epiphytic algae, and ephemeral macroalgae, whereas benthic macrophytes such as kelp do not occur (Pedersen and Borum 1996).

Macroalgal species tend to exhibit vertical patterns of distribution, from the upper to the lower tidal levels, originating different zonation patterns. This is because different species have different adaptive responses to the physical, chemical, and biotic conditions. The lack of hard substrates, the low light penetration, the variations of salinity, pollution, competition, and grazing are factors that explain the reduced seaweed richness of estuaries and the occurrence of some annual species (Druehl 1967; Larsen and Sand-Jensen 2006). Although estuaries are stressful environments to most marine algae, a few adapted species can flourish. For example, eutrophic estuaries promote the proliferation of opportunistic and tolerant macroalgae like Ulva, Chaetomorpha Kützing, Cladophora, Monostroma Thuret, Ceramium Roth, Gracilaria Greville, Porphyra C. Agardh, Pyropia J. Agardh, Ectocarpus Lyngbye, and Pilayella Bory, which can bloom into large proportions (Morand and Merceron 2005; Scanlan et al. 2007).

Wilkinson (1981) exposed three fundamental points to explain macroalgal distribution patterns in estuaries: (1) The colonization occurs almost wholly by marine species, with freshwater ones abundant only in the uppermost reaches of the estuary. (2) In the uppermost regions of estuaries, there is a reduction in species number and diversity due to the decrease of red algae (Rhodophyta) and then of brown algae (Phaeophyta). Green algae (Chlorophyta) and blue-green algae (Cyanophyta) do not necessarily become more numerous, in terms of species, but they constitute a much greater proportion of the algal community because they extend further inland. (3) Colonization of the mid-reaches is dominated by brackish water algae.

The algae that live in estuaries generally proliferate under a broad range of temperatures, irradiances, salinities, and nutrient conditions (Martins et al. 1999; Taylor et al. 2001; Sousa et al. 2007; Choi et al. 2010; Kim et al. 2011). For example, the growth rate of Ulva increases at low salinity and high nutrient levels in laboratory culture conditions (Taylor et al. 2001). Ulva has physiological adaptations to grow as free-floating mats. Some species of Ulva have partially hollow branched tubular thalli filled with air generated through photosynthesis, which under unfavorable conditions produce thalli that can float for 2 or 3 months favoring survival (Kim et al. 2011).

The filamentous algae are well adapted to overcome the low light intensities of estuarine waters. They have thin photosynthetic tissues, with high contents of pigments per cell volume that reduce the trajectory of light through the tissue. As they have high area/volume ratio, they use efficiently the light and nutrients per biomass unit (Kirk 1994; Niklas 1992; Nielsen and Sand-Jensen 1990; Duarte 1995; Duarte et al. 1995).

Estuarine filamentous green algae with heterotrichous growth such as Cladophora present densely pigmented assimilatory cells that penetrate upward through the mud and the covering mats that contrast greatly with the weakly pigmented cells of the prostrate system. This morphological characteristic constitutes an ecological adaptation to burial by soft sediment, as it helps retain moisture during low tides (Boedeker and Hansen 2010).

Cladophorales algae have other strategies for protection against desiccation and fluctuating salinities, for example, the formation of a thick gelatinous cover produced by swelling of the outer cell wall layers (Wille 1909), endophytic habit (Polderman 1976), and the presence of hematochrome/oil droplets (Wille 1909).

Chaetomorpha has been mainly studied for its ecological role as a possible regulator of nutrient availability in estuarine habitats (Krause-Jensen et al. 1996, 1999; Menendez 2005) and for its ability to tolerate a wide range of salinities. The identification of ascorbate oxidase activity in Chaetomorpha linum (O.F. Müller) Kützing suggests a novel mechanism of adaptation to increased salinity, because this enzyme could have a role in salt stress by catalyzing intracellular production of water, which could mitigate the stress (Caputo et al. 2010).

Algae that are unicellular, colonial, or have a thallus with 1–4 cell layers can change their pigment concentration, affecting light absorbance as a mechanism of adaptation to irradiance variations (Agusti et al. 1994).

In most estuaries, microphytobenthic communities are composed of a mixture of different taxa that can form conspicuous biogenic structures on intertidal and supratidal sediments commonly called biofilms and microbial mats, the latter being among the oldest ecological structures on Earth (van Gemerden 1993). The main difference between biofilms and mats is that the first one is formed by a single layer of microorganisms embedded in an organic matrix, while microbial mats are vertically stratified microbial communities dominated by cyanobacteria. Microbial mats are regarded as advanced stages of biofilms (Noffke 2010). Biofilms and microbial mats result from the growth and activity of microphytobenthic organisms that trap sediment particles and bind them in extracellular polymeric substances (EPS) produced by the organisms (Margulis et al. 1980; Krumbein 1994). Although many microorganisms are capable of secreting EPS, phototrophs are especially important since they produce them de novo through CO₂ fixation, while chemotrophic organisms form EPS by converting other organic compounds, which may be limited (Stal 2006).

Extracellular polymeric substances are a complex mixture of high-molecular-weight polymers consisting of 90% or more of polysaccharides (Hoagland et al. 1993). They allow the locomotion of microorganisms and also provide protection against changes in salinity, temperature, UV radiation, and desiccation (Decho 2000). At the same time, they generate high cohesion in the sediment since they form an adherent cover on the particles (de Winder et al. 1999; Decho 2000). Microphytobenthos develops mainly in marine sediments of the intertidal and supratidal region because the extreme and strongly fluctuating environmental conditions that prevail in this region exclude, or at least reduce the abundance of grazers (Stal 2006). In open coastal environments, coarse sand is deposited over high-energy areas, becoming unsuitable for the development of microbial mats or biofilms because of the damage caused by the abrasion of sand particles induced by the action of wind and waves (Eckman et al. 2008). On the other hand, silt and clay sediments are deposited in low-energy areas such as estuaries and deltas; these sediments are characterized by low light penetration and high sedimentation rate, which difficult the phototactic migration response of cyanobacteria. In addition, this type of sediment usually contains large amounts of nutrients, conditions under which the cyanobacteria are outcompeted by opportunistic organisms, mainly diatoms, which have high growth rates under high nutrient conditions. This is why cyanobacteria prefer sediments of fine to medium sand as a substrate for the formation of microbial mats, while in silt-clay sediments, biofilms of diatoms predominate (Watermann et al. 1999).

In extreme conditions, microphytobenthic organisms are able to regulate their photosynthesis to avoid photoinhibition (Cartaxana et al. 2011), thereby maintaining relatively high abundance in the sediment. For example, epipelic life forms are able to migrate vertically in the sediment to position themselves in favorable light conditions, and diatoms can adapt their photosynthetic apparatus efficiently to the light conditions in a few minutes (Glud et al. 2002). In these ways, physiological photoinhibition is avoided at high light levels of solar radiation. However, the microgradients of sediment grain sizes and organic particle sizes, percentages of organics, porosity, light attenuation, and oxygen govern vertical microalgal distribution patterns (Kennish 2017).

6.5 The Benthic Algae of the Bahía Blanca Estuary

Among the benthic algae that occur in the Bahía Blanca Estuary, microscopic epipelic algae are the most studied. The first studies of the microphytobenthos appeared in the 1980s (i.e. Cicerone 1987; Farías 1988) which initially depicted the diversity of the microscopic algae of this region. These preliminary studies were subsequently followed by qualitative studies conducted on specific coasts of the estuary (Parodi and Barria 2003). The most recent studies focus on ecological aspects (Da Rodda 2004) or were motivated by the anthropic impact caused by the expansion of the industrial area (Pizani 2009).

Thanks to these studies, there is a fair knowledge of the diversity of microalgal taxa that can be found in many of the coastal regions of the estuary. The relevance that diatoms and Cyanophyceae have in the process of sediment stabilization and their contribution to the formation of microbial mats has led the phycological studies in this region. These topics will be discussed later in the chapter and in Box 6.1.

A different scenario stands for the macroscopic algae (including their microscopic life stages), to which less attention has been paid. There are fair explanations for this situation. The Bahía Blanca Estuary is located in a coastal region considered to be poor in macroalgal flora (Liuzzi et al. 2011). From a biogeographic point of view, the Bahía Blanca Estuary is located in a transition zone between the Argentinean and the Magellanic biogeographic provinces that is characterized by a reduction of macroalgal biodiversity (Balech and Ehrlich 2008). This scarcity of macroscopic algae is a consequence of two factors that are related with the characteristics of the sediment and its dynamics: (1) in the majority of the coasts, the dominant fraction of the sediment is composed of small-sized particles, which may prevent the settlement of the macroalgal reproductive cells and/or compromise the successful attachment of the microscopic life stages of macroalgae (Parodi 2004); and (2) the turbid waters resulting from the suspended fine sediment reduce the penetration of light into the lower layers of the water column, limiting the depth at which the macroalgae are able to photosynthesize. These combined conditions restrict the occurrence of the microscopic and macroscopic thalli to the hard substrata submerged in shallow waters or exposed to air during low tide, where the reproductive cells, either motile or non-motile, can fix and access to light intensities that allow them to photosynthesize. Examples of appropriate substrates are the consolidated sediments and any artificial or natural solid object set on the coast. Despite that the turbid waters significantly reduce the penetration of light in the water, the shallow tidal flats that span in some sectors of the Bahía Blanca Estuary allow the development of small intertidal communities of macroalgae, where several species can thrive.

As a consequence of these unfavorable conditions, the macroalgal assemblages of the Bahía Blanca Estuary are less conspicuous and go unnoticed, unlike the assemblages of other coasts of Argentina. The estuarial coasts have high sedimentation rates; therefore, some macroalgae are usually buried under the sediment. This adds to the fact that the actual diversity of macroalgal species is usually obscured by the existence of cryptic species. As the worldwide trend suggests, it is expected that the number of macroalgal taxa in the Bahía Blanca Estuary increases as the coastal industrialization advances, providing available artificial substrate, increasing the nutrient loads in the water, and promoting the ingression of alien marine species through ballast water.

6.5.1 Diversity and Composition of Soft-Bottom Microalgal Assemblages

Many studies about different microphytobenthic communities have been carried out in the Bahía Blanca Estuary to examine the biodiversity, structure, and dynamics of this estuarine benthic ecosystem (Cicerone 1987; Parodi and Barría de Cao 2003; Da Rodda and Parodi 2005; Pizani 2009). A particular feature of the tidal flats of the Bahía Blanca Estuary is that they are colonized by extensive microbial mats (Cuadrado and Pizani 2007; Cuadrado et al. 2011, 2012). They have been widely studied to explore the relationship between microphytobenthos, sediment, and physical factors, such as irradiance, temperature, sedimentation rate, and wave height (Cuadrado et al. 2012, 2013; Pan et al. 2013a). Most of these studies have been conducted in Puerto Rosales and, to a lesser extent, in Puerto Cuatreros, Villarino Viejo, and Almirante Brown locations (Figs. 2.2, 2.3, and 2.4; Chap. 2).

Even though the surface of the mudflats of the Bahía Blanca Estuary is often apparently devoid of vegetation, the richness of microphytobenthic algae is high since a total of 144 taxa have been recorded by different authors (Parodi and Barría de Cao 2003; Da Rodda 2004; Da Rodda and Parodi 2005; Pizani 2009; Fernández et al. 2018). Diatoms are the dominant group with 109 taxa, whereas 34 taxa of Cyanobacteria and only 1 taxon of Euglenophyta have been registered. Regarding diatoms, Nitzschia Hassall and Navicula Bory are the best represented genera, with 27 and 13 taxa, respectively. Figure 6.1 shows some common benthic microalgae found in the Bahía Blanca Estuary.

Fig. 6.1

Common benthic microalgae of the Bahía Blanca Estuary, (a) Euglena sp. (scale bar: 6 μm), (b) trichomes of Coleofasciculus chthonoplastes (scale bar: 20 μm), (c) biofilm of diatoms and filamentous cyanobacteria developing on hard substrate (scale bar: 50 μm), (d) centric diatom Melosira and filamentous cyanobacteria (scale bar: 6 μm), (e) centric diatoms on Blidingia sp. (scale bar: 60 μm), (f) Nitzschia clausii (scale bar: 50 μm), (g) Gyrosigma spencerii (scale bar: 50 μm), (h) Cylindrotheca closterium (scale bar: 6 μm), (i) Navicula sp. (scale bar: 6 μm). (Photos by (a) Natalia Pizzani, (b, d, f, g, h, and i) Carolina Fernandez, (c and e) M. Emilia Croce)

The unique characteristics of estuarine environments allow the coexistence of freshwater, estuarine, and marine species; according to this, the diatom species found in the microphytobenthos of the Bahía Blanca Estuary are mostly holo-euryhaline forms, which can tolerate large changes in the salinity of water from hypotonic to hypertonic. On the other hand, freshwater species are also present, which arrive from the discharges of freshwater tributaries (Pizani 2009). In addition, some of the species found in surface sediments are typically planktonic forms, namely, species of Triceratium Ehrenberg, Podosira stelligera (Bailey) A. Mann, Planothidium delicatulum (Kützing) Round and Bukhtiyarova (reported as Achnanthes delicatula (Kützing) Grunow), Luticola mutica (Kützing) D.G. Mann, Craticula halophila (Grunow) D.G. Mann (cited as Navicula halophila (Grunow) Cleve), Navicula salinicola Hustedt (reported as Navicula incertata Lange-Bertalot), Gyrosigma attenuatum (Kützing) Rabenhorst, Paralia sulcata (Ehrenberg) Cleve, and Petrodictyon gemma (Ehrenberg) D.G. Mann (cited as Surirella gemma (Ehrenberg) Kützing), or are species that are usually found in both planktonic and benthic habitats, such as Entomoneis alata (Ehrenberg) Ehrenberg, Cylindrotheca closterium (Ehrenberg) Reimann and J.C. Lewin, Gyrosigma fasciola (Ehrenberg) J.W. Griffith and Henfrey, Nitzschia sigma (Kützing) W. Smith, and Petrodictyon gemma (Ehrenberg) D.G. Mann (Parodi and Barría de Cao 2003; Da Rodda and Parodi 2005; Pizani 2009). This is because the surface of the sediment in the tidal mudflat is constantly subjected to the action of waves and tidal currents, which results in the resuspension of benthic individuals, as well as in the incorporation of planktonic species by sedimentation.

The microphytobenthic community of Puerto Rosales consists mainly of filamentous cyanobacteria and small diatoms. Among filamentous cyanobacteria, Coleofasciculus chthonoplastes (Thuret ex Gomont) M. Siegesmund, J.R. Johansen, and T. Friedl (reported as Microcoleus chthonoplastes Thuret ex Gomont) is dominant, whereas species of Oscillatoria and Arthrospira Sitzenberger ex Gomont are less abundant. C. chthonoplastes typically has many trichomes within a common sheath threaded into a spiral arrangement; the resulting mesh of interweaving cyanobacterial filaments together with the microbially secreted EPS traps the sand grains and significantly increases the cohesiveness of sediments (Stal et al. 1985). In that sense, the dominance of C. chthonoplastes is indicative of well-developed microbial mat, presenting an elevated resistance to erosion, and a protective cover to the underlying sediments. The microbial mats in which this cyanobacterium is dominant were termed “epibenthic mats” by Noffke (2010) and are typically found in the supratidal zone.

The diatoms recorded in the Bahía Blanca Estuary are mainly small pennate diatoms; the genera Nitzschia, Navicula, Diploneis Ehrenberg ex Cleve, and Amphora Ehrenberg ex Kützing are quantitatively dominant. Other larger diatoms of the genera Pleurosigma W. Smith, Gyrosigma Hassall, and Cylindrotheca Rabenhorst are also present, but they are less frequent. Among central diatoms, the genera Thalassiosira Cleve and Coscinodiscus Ehrenberg and the species Cyclotella meneghiniana Kützing and Paralia sulcata have been mentioned by different authors (Pizani 2009; Pan et al. 2013a, b). The dominance of small diatoms is attributed to the fact that small cells have higher growth and nutrient uptake rates than bigger cells since they have higher surface/volume ratio, which allows small cells to outcompete bigger cells when they are subjected to frequent physical disturbances (Williams 1964; Snoeijs et al. 2002).

6.5.2 Hard Substrate Available for Algal Settlement

In the Bahía Blanca Estuary, the hard substrate available for the settlement of algae comprises natural and artificial structures (Fig. 6.2). The hard substrate of natural origin consists of rocks made of consolidated fine sedimentary particles (henceforth named outcrops) and the mollusk shells (oysters, mussels, snails, and barnacles). The outcrops are made up of compacted sand and clay material giving rise to a relatively hard substrate (Spalleti 1980; Aliotta and Lizasoain 2004). These outcrops are common in the southeastern coasts of the estuary like Villa del Mar (Fig. 2.4; Chap. 2). These substrates are called outcrops because they appear interrupting the large tidal flats or sand beaches. In the Bahía Blanca Estuary, macroalgal assemblages inhabit the depressions (tidal pools) that form on these outcrops, which remain filled with water during low tide (Fig. 6.2b).

Fig. 6.2

Artificial and natural substrata of the Bahía Blanca Estuary colonized by benthic algae, (a) general view of a bloom of green macroalgae on a salt marsh in Villa del Mar, (b) macroalgal assemblage in a tidal pool located in the outcrops of Villa del Mar, (c) macroalgae attached to mollusk shells, (d) macroalgae attached to a floating platform in CNBB, (e) green and red macroalgae growing on concrete rocks in the upper intertidal zone of Puerto Rosales, (f) detail of Blidingia sp. on a concrete rock in Puerto Rosales, (g) green macroalgae on a wheel in Villa del Mar, (h) green macroalgae covering the surface of a sewer pipe in Club Náutico Bahía Blanca (CNBB). (Photos by M. Emilia Croce)

The main artificial hard substrate consists of wooden docks, concrete barriers, metal ladders, floating platforms and bridges, mooring ropes, sewer pipes, buoys, and rubber wheels. All these surfaces appear in the different coasts of the Bahía Blanca Estuary and are colonized by micro- and macroalgae. Although the hard substrate is scarce in the Bahía Blanca Estuary, the industrial growth in the region has modified the environment in such a way that the surfaces available for algal attachment have increased in number by the artificial structures constructed by humans.

Although microbial mats develop conspicuous biogenic structures on soft sediments, the biofilms composed of diatoms and filamentous cyanobacteria can also be found covering hard natural or artificial substrates in the intertidal zone (Fig. 6.1c). In contrast to microalgae, macroscopic algae are always found attached to hard substrates (except for the drifting species). This is because the main condition for a macroalga to colonize a substrate is that the substrate is relatively stable, for the algae to remain attached and to avoid being flushed away by waves or currents. Consequently, macroscopic algae are virtually able to occupy any type of substrate as long as the surface is suitable to attach for the microscopic propagules (spores or gametes), or a fragment of the thallus, in the case of vegetative propagation (Amsler et al. 1992; Fletcher and Callow 1992). Because of the different tolerances of each species of macroalgae to desiccation stress (Dromgoole 1980; Davison and Pearson 1996), the success to colonize a stable substrate greatly depends on the location of the substrate with respect to the coastline (Lobban and Harrison 1994). The establishment and persistence of benthic algal populations depend on the reproductive performance of the species but also on the successful survival of their propagules. Any factor that influences the recruitment, the settlement, and/or the post-settlement of algal propagules becomes an important factor determining the establishment, dynamics, and structure of algal communities (Wahl and Hoppe 2002). For example, substratum microtopography has been recognized as one of the major factors structuring marine benthic communities (Emson and Faller-Fristch 1976; Woodin 1978; Menge et al. 1983; Brault and Bourget 1985; Bergeron and Bourget 1986). In the case of artificial substrate, the type of material that constitutes the substrate also influences the colonization and survival of the macroalgal species. For example, substrates that retain water like ropes are favorable for species that are less tolerant to desiccation (Nienhuis 1969).

In general, marine macroalgae have a wide capacity of dispersal through a variety of forms, from unicellular to multicellular propagules, either sexual or asexual (Santelices 1990; Norton 1992). Due to their potential for colonization of new habitats, any modification of the habitat can quickly lead to changes in the macroalgal diversity of the coast. The factors associated with the expansion of the industrial area, such as the increased availability of substrate, the introduction of exotic species through ballast water, and the increase of nutrient loads into the water, are promoting changes in the diversity and distribution of macroalgae in the Bahía Blanca Estuary.

6.5.3 Diversity and Composition of Macroalgal Assemblages

The richness of macroalgae in the Bahía Blanca Estuary is low compared with other coasts of Argentina (Miloslavich et al. 2011). According to the literature, a total of 19 macroalgal taxa have been recorded on the coasts of this estuary (Perillo et al. 2001; Parodi 2004; Bremec et al. 2004; Croce et al. 2015; Hoshino et al. 2020; Koller 2021). Eighteen of those taxa were found in the most recent surveys from 2015 to 2019, together with three new taxa, Blidingia marginata (J. Agardh) P.J.L. Dangeard ex Bliding, Blidingia minima (Nägeli ex Kützing) Kylin, and a species of Pyropia J. Agardh. The complete list of 22 taxa is shown in Table 6.2. Red and green macroalgae are the dominant groups with nine taxa each. According to the classification of functional groups proposed by Balata et al. (2011), six morpho-functional groups are recognized; the majority of the taxa belong to the categories bladelike and filamentous uniseriate and pluriseriate with erect thallus.

Although the turbid waters in this region limit the growth of macroalgae because of the low light penetration through the water column, some tolerant species such as opportunistic species with rapid growth rates and small turf-like forms flourish in these habitats. In terms of biomass, the most abundant red macroalgae are Polysiphonia abscissa J.D. Hooker and Harvey, Polysiphonia morrowii Harvey, and Ceramium diaphanum (Lightfoot) Roth. These three filamentous species grow in the tidal pools of the outcrops in Villa del Mar, where they are present almost all year round, although their bushy thalli are larger in winter (Fig. 6.3a, c). Species of Polysiphonia Greville also live attached to floating platforms near the surface in the recreational harbor of the Bahía Blanca Nautic Club (CNBB), where they are continuously submerged. The presence of Gracilaria verrucosa (Hudson) Papenfuss in the tidal flats of Villa del Mar is reported in the literature (Parodi 2004); however, this species has not been found in recent surveys. The macroscopic thalli of Pyropia are abundant during the winter on the hard substrates of the upper intertidal of Puerto Rosales. Pyropia grows in the mooring ropes that are frequently exposed to air during low tide, on the wooden pillars that support the docks, and on concrete rocks (Fig. 6.3d). In general, the distribution of benthic red macroalgae that inhabit the Bahía Blanca Estuary is limited to the intertidal flats and salt marshes of Villa del Mar; except for Pyropia, they have not been recorded in other coasts with hard substrate available. The lack of mobility of the propagules may restrict the spread of red macroalgae in this estuary. Two species of Gelidium J.V. Lamouroux grow exclusively in the tidal pools of the outcrops located in the tidal flats of Villa del Mar. They form dense mats on the consolidated sediment or grow as epiphytes on mollusk shells (Fig. 6.3b). Gelidium species are perennial in these coasts and reproduce sexually all year round. They also reproduce and spread vegetatively, due to their ability for regeneration and reattachment from fragments by the formation of rhizoids. This behavior has been observed during culture experiments (unpublished data) and is reported for other species of Gelidium as well (Santelices and Varela 1994; Titlyanov and Titlyanova 2006; Otaiza et al. 2018).

Fig. 6.3

Common benthic red macroalgae of the Bahía Blanca Estuary, (a) Polysiphonia morrowii , detail of the thallus and axes (scale bar: 500 μm), (b) Gelidium pusillum , general aspect of the thallus (scale bar: 1 cm), (c) Ceramium diaphanum , general aspect of the thallus (scale bar: 1 cm), (d) Pyropia sp. : thalli in nature (scale bar: 1 cm). (Photos by (a, b, and d) M. Emilia Croce, (c) Ailen Poza)

The green algae are the second dominant group, represented by nine taxa (Table 6.2). Ulva Linnaeus is the most conspicuous genus, represented by four species that reach high biomass in winter (Fig. 6.4c). They cover large surfaces of the intertidal flats and tidal pools in Villa del Mar. They also colonize submerged objects and cover the concrete walls and rocks located in the upper intertidal zone of the harbors. Green algae of the family Ulvophyceae are the most common group of macroalgae in estuarine habitats. This is because they withstand desiccation occasioned by the strong irradiance and wind during low tide and tolerate a wide range of salinities. The presence of the genus Enteromorpha Link was reported by Perillo et al. (2001), Parodi (2004), and Bremec et al. (2004), although this genus has been now merged into Ulva (Hayden et al. 2012). Isolated thalli of Cladophora surera E.R. Parodi and E.J. Cáceres are usually found in tidal pools or on the concrete structures, but are most frequently found as an epiphyte on other macroalgae. C. surera and Ulva flexuosa Wulfen (= Enteromorpha flexuosa (Wulfen) J. Agardh) are tolerant to salinity changes and more related to freshwater environments (Parodi 2004). The coenocytic algae Bryopsis plumosa (Hudson) C. Agardh forms dense bushes during winter in the upper tidal pools of the outcrops of Villa del Mar (Fig. 6.4b). Chaetomorpha linum grows as an epiphyte on other macroalgae, but it also occurs on the shaded regions of the concrete walls of the harbor of the CNBB. Green macroalgae such as Blidingia minima and B. marginata grow usually on concrete rock in the upper intertidal zone where they can reach high densities (Fig. 6.4a).

Fig. 6.4

Common benthic green and brown macroalgae of the Bahía Blanca Estuary, (a) Blidingia marginata , detail of the thallus (scale bar: 60 μm), (b) Bryopsis plumosa , general aspect of the thallus (scale bar: 2 cm), (c) Ulva lactuca , general aspect of the thallus (scale bar: 1 cm), (d) Punctaria latifolia (scale bar: 2 cm). (Photos by (a, c, and d) Ailen Poza, (b) M. Emilia Croce)

The brown algae are less frequent in this habitat; they are represented only by four taxa, the Ectocarpaceae Ectocarpus siliculosus and Hincksia hincksiae (Harvey) P.C. Silva, the Chordariaceae Punctaria latifolia Greville, and the Scytosiphonaceae Planosiphon nakamurae M. Hoshino, M.E. Croce, Hanyuda, and Kogame (Table 6.2). The Ectocarpaceae have been almost exclusively found as epiphytes on other macroalgae. Macroscopic thalli of P. nakamurae can be found in winter, growing on the walls and concrete blocks in the harbor of CNBB that are completely exposed during low tide. P. latifolia occurs in the salt marshes dominated by Spartina Schreb., located in Villa del Mar. The stems of this vascular plant offer a temporary substrate for the attachment during the winter where the macroscopic thalli of P. latifolia (Fig. 6.4d) attach sparsely (Parodi 2004, as Punctaria latifolia var. crouanii).

Among the macroalgae that live in the Bahía Blanca Estuary, three of them are considered exotic (or alien): Polysiphonia morrowii ; Neosiphonia harveyi (Bailey) M.-S. Kim, H.-G. Choi, Guiry, and G.W. Saunders; and Planosiphon nakamurae . These species have been registered in other coasts of the Patagonian region as well. P. morrowii is present in Puerto Madryn (Raffo et al. 2014), Bahía Anegada (Croce and Parodi 2014), and Las Grutas (personal observation). There are different hypotheses of the introduction of P. morrowii. The vectors may have been ballast water (Hewitt et al. 2007) or other exotic marine organisms such as the Pacific oyster in Bahía Anegada or the macroalgae Undaria pinnatifida (Harvey) Suringar, that have been introduced in the 1980s and the 1990s (Verlaque 2001; Kim et al. 2004; Geoffroy et al. 2012). There is no evidence about the initial site of their introduction, but it may have dispersed along the South Atlantic coast by shipping among different harbors. N. harveyi is also present in the southern coasts of Argentina (Raffo et al. 2014), and it is catalogued as introduced, given that it is worldwide known as an invasive species. Planosiphon nakamurae was recently found in the coasts of the South Atlantic Ocean. Its identity was confirmed by molecular tools, which also evidenced its relationship with a Japanese haplotype (Hoshino et al. 2020).

The exotic macroalgae are characterized by fast vegetative growth and dispersal, usually by fragmentation, by a rapid completion of the life cycle, and wide tolerances to environmental variables (Nyberg and Wallentinus 2005). For several reasons, exotic macroalgae are common in estuarine environments. First, because estuaries are areas of entrance to the new environment, usually through ballast water that is released by the international vessels. Second, the strong environmental variations, mainly salinity changes and desiccation, are more easily tolerated by exotic species. And third, because estuaries are regions occupied by human settlements, and consequently, they constitute eutrophic environments where the exotic species with fast-growing capabilities can exploit outcompeting with the native species.

6.6 Epiphytic Algae

Epibiosis is defined as a nonsymbiotic facultative association between an epibiont (an organism that lives attached to a living surface) and a basibiont (a substrate organism or host) (Wahl 1989). This phenomenon is common in aquatic environments and among macroalgae (epiphytes), which may live attached to animals, vascular plants, or other macroalgae.

In the Bahía Blanca Estuary, there are natural substrates such as the leaves and stems of halophyte plants, and the thalli of the macroalgae themselves, where epiphytic macroalgae and microalgae can attach. For example, P. latifolia grows attached to the stems of Spartina. Although the population is relatively ephemeral, this epiphytic association is persistent throughout the years, suggesting that it is well established. The most frequent taxa that live attached to other macroalgae are the filamentous red and green macroalgae Ceramium Roth, Acrochaetium Nägeli, Cladophora, and Ulva sp. (Koller 2021); however, the diatoms Melosira C. Agardh, Achnanthes Bory, and Cocconeis Ehrenberg frequently appear attached to the surfaces of the macroalgae thallus, solitary or in chains. Blidingia species are sometimes covered by epiphytic diatoms; the most frequent is Melosira that forms dense brown tufts of long chains (Fig. 6.1e).

Epiphytic associations among macroalgae and benthic fauna are also common in the Bahía Blanca Estuary. Polysiphonia and Gelidium species are epiphytes on two dominant bivalves, the native mussel Brachidontes rodriguezii (d’Orbigny, 1842) and the exotic Pacific oyster Magallana gigas (Thunberg, 1793) (= Crassostrea gigas Thunberg, 1793). Succession and ecological studies in other coasts of the northern Patagonian region have shown that M. gigas offers a suitable substrate for the settlement of native and exotic macroalgae (Borges 2006; Croce and Parodi 2012) in areas where no suitable hard substrate is available. Gelidium lives also attached to the gastropod Crepidula aculeata (Gmelin, 1791). This association is very frequent suggesting that the symbiosis may be beneficial to both species. The macroalgae may benefit from nutrient loadings produced by the gastropod beneath, and the gastropod may enhance the dispersal of the macroalgae by carrying them from one place to another. From the perspective of the mollusk, the benefit may be related to the avoidance of predators, since the macroalgae cover the shell completely.

6.7 Mat-Forming Macroalgae

The term “turf” is widely used in marine ecology to identify a layer of short and densely branched algae that is several millimeters to a few centimeters tall (Connell et al. 2014). Several macroalgal species fall under this definition, although the more common are small-sized species of red algae representatives of the orders Ceramiales, Gelidiales, and Corallinales. A more specific term, the word “mat”, identifies a small group of algae defined as short and densely branched and formed by prostrate and erect axes and which grow entangled into a thick mass (Hay 1981). These groups of algae, either turf-forming or mat-forming species, are relevant to the dynamics of benthic ecosystems (Airoldi et al. 1995; Bulleri and Benedetti-Cecchi 2006; Gorman and Connell 2009). One reason for that is that these cushions trap large amounts of sediment particles in relation with their small size, influencing the transportation of energy and organic matter in intertidal marine environments (Airoldi 2003). It is known from several studies that the macroalgae that form this type of mats have an important influence on the nutrient dynamics. Besides their role in the dynamics of the mentioned abiotic factors, they are also key components of biotic assemblages as they provide an excellent niche for little crustaceans, polychaetes, annelids, mollusks, and other small invertebrates (Prathep et al. 2003). Through many years of surveys in the intertidal regions of the Bahía Blanca Estuary, it has been noticed that the populations of the mat-forming Gelidiales may be key components of the benthic communities in this coast. The vegetative growth of these algae has been studied in culture conditions, and preliminary results showed that these algae have a high capacity of regeneration by producing numerous branches, rhizoids, and rhizoidal filaments, and they can also withstand a high load of epiphytes for long periods of time (unpublished data).

Box 6.1: Ecosystem Engineers in the Bahía Blanca Estuary: The Crab Neohelice granulata

Tidal currents are responsible for sediment transport, and waves produce either sediment deposition or erosion. These factors interact with the biological components of the coast determining whether deposition or erosion is the dominant process in a specific site. These complex processes ultimately determine the type and abundance of organisms in the sediment (Blanchard et al. 2000; Dyer et al. 2000).

Bioturbation is defined as the biological reworking of sediments and soils through animal activities like feeding and burrowing that generates changes in chemical gradients and relocates resources and microorganisms. Such sediment restructuring also promotes physical alterations, by changing the balance of material transported, and affects the structure and functioning of assemblages (Meysman et al. 2006; Kristensen et al. 2012). Organisms that directly or indirectly modify the physical environment and regulate the availability of resources for other species are called ecosystem engineers (Statzner et al. 2000; Gutiérrez et al. 2003; Berkenbusch and Rowden 2003; Cardinale et al. 2004).

Neohelice granulata (Dana, 1851) (= Chasmagnathus granulata) is an estuarine crab that excavates semipermanent burrows generating extensive burrowing beds which cover up to 80% of the intertidal areas of SW Atlantic estuaries and bays (Botto et al. 2006; Iribarne et al. 2005). N. granulata distributes from the northeastern coast of Patagonia, Argentina (42°25′S, 64°36′W), to Río de Janeiro, Brazil (22°57′S, 42°50′W) (Spivak 2010). In the muddy salt marshes of the Bahía Blanca Estuary, an association between the crab and the halophyte plant Sarcocornia perennis (Miller) A. J. Scott was described by Perillo and Iribarne (2003). This association has a particular configuration, where the plants form a ring surrounding a non-vegetated salt pan densely excavated by the crab. These ring-shaped configurations are 1.5–8 m in diameter and have high water retention at the inner part. Such ring-shaped configuration of the halophyte vegetation is the macroscopic evidence of the changes in salinity, humidity, and hardness that occur in the sediment and which are a consequence of the plant-crab interaction (Escapa et al. 2007).

The composition and structure of the microphytobenthic assemblage differ considerably among the different environments composing the rings. A thin diatom biofilm, characterized by high abundance of diatoms and reduced abundance of cyanobacteria, is observed in the inner part of the rings, associated with small grain sediment, while well-developed microbial mats, characterized by the presence of Coleofasciculus chthonoplastes , are present in the outer region of the rings. Both structures show differences in the EPS matrix, since the biofilms dominated by diatoms are less developed and more irregular than those formed in the presence of cyanobacteria (Fig. 6.5a). In cyanobacterial mats, EPS are found as an embedded continuous matrix, whereas in diatom biofilms, they develop as a web of spongelike fibrils with void spaces (Fernández et al. 2018) (Fig. 6.5b). Such differences in the microphytobenthic assemblages are the result of changes in the physical properties of sediments caused by the bioturbation of the burrowing crab.

Fig. 6.5

Structure of microphytobenthic assemblages, (a) scanning electron photomicrograph of biofilms dominated by pennate diatoms embedded in a compacted matrix of EPS (scale bar: 20 μm), (b) microbial mat dominated by filamentous cyanobacteria (arrows) (scale bar: 6 μm). (Photos by Constanza Da-Rodda)

A common consequence of the activity of burrowing deposit feeders is the increase in softness and water content of the sediment. Also, the burrows contribute to the accumulation of fine particles since the sediment with a high percentage of clay accumulates at the burrow tunnel during high tide (Davis 1993; Botto and Iribarne 2000). This physical mixture would restrain the formation of large and well-developed microbial mats on the superficial sediments of the salt marsh with abundant crabs. Then, the death of the plants in the inner part of the rings can also be associated with permanent modifications in the development of the microphytobenthos succession resulting from the biodisturbing action of crabs (Fernández et al. 2018).

Given the important role of microphytobenthos in recycling of nutrients, biofiltration, and sediment stabilization in coastal ecosystems , the study of the distribution patterns of micro- and macroorganisms provides valuable information for the formulation of integrated management plans, aiming to reduce the ecosystem erosion and contamination.

Box 6.2: Potential Use of Native Estuarine Macroalgae for Biomitigation

Marine macroalgae are used in a variety of domestic and industrial processes. The more ancestral use is as fresh food (Lee et al. 2017), but due to their varying intrinsic characteristics and chemical composition, they can also be used for the production of a variety of algal products, for example, fertilizers (Selvam and Sivakumar 2014), biogas by anaerobic digestion (Hinks et al. 2013), phycocolloids (Chan and Matanjun 2017), and polymers that can be incorporated into conventional plastic formulations to develop biodegradable plastics (Freile-Pelegrín et al. 2007). Macroalgae are also a source of bioactive compounds (polysaccharides, proteins, lipids, polyphenols, carotenoids, and vitamins). These phytochemicals have different functional groups including carboxyl, hydroxyl, phosphate, and amine that can bind pollutants (Areco and dos Santos 2010, Sanjeewa et al. 2016). The presence of sulfated polysaccharides in the cell wall of macroalgae, mainly in their fibrous matrix and intercellular spaces, is the main reason for their high capacity to bind contaminants. In fact, hydroxyl, sulfate, and carboxyl groups of the polysaccharide chains are strong ion exchangers; therefore, they are the important sites of complexation of metal cations (Vasconcelos and Leal 2001). Biosorption is one of the most promising remediation technologies for aquatic areas that are polluted with heavy metal ions (Gupta et al. 2015). The major advantages of biosorption using the macroalgal biomass for wastewater treatment are the low cost and investment needed, the simple design and easy operation, and the use of nontoxic substances. Hence, recently, the interest in using seaweed as biomitigators or for bioremediation of marine environments is increasing (Kim et al. 2017). For this reason, macroalgae can be exploited as a resource at the same time as it is used for ecological services.

Along the eastern coast of the Bahía Blanca Estuary, there are several human settlements. From the inner part of the estuary to the mouth, we find the towns of Villarino Viejo, General Daniel Cerri, Bahía Blanca, and Punta Alta. Of all these emplacements, the city of Bahía Blanca has the largest demographic growth due to the settlement of a fertilizer industry, a large petrochemical pole, and thermoelectric plants, as well as the expansion of the harbor. As a consequence of this economic development, the estuary is the receptor of waste discharges from industrial origin (oil derivatives, pesticides, heavy metals, etc.) as well as untreated domestic sewage, which have generated problems of contamination (Marcovecchio et al. 2010).

The macroalgal assemblages that inhabit the Bahía Blanca Estuary are potentially useful for implementing methodologies of pollutants remotion and eutrophication management. The most promising candidate for biomitigation is the green alga Ulva, which is particularly useful in the biosorption of heavy metals and other compounds due to its high surface area, relatively simple structure, and uniform distribution of binding sites (Sari and Tuzen 2008; Turner et al. 2007).

The multiple functions and uses of seaweeds discussed above would promote the cultivation of seaweeds to obtain high-quality raw materials for different applications. Biosorption by seaweeds is a promising method that utilizes efficiently the naturally existing raw material. It is noticeable that very few studies have used real wastewater for the treatment and most of the experiments have used simulated wastewater. Therefore, it is recommended that future studies consider the use of real wastewater, especially in impacted environments such as the Bahía Blanca Estuary.

Glossary

Amoeboid:

Type of cell organization that lacks a cell wall and the protoplasm undergoes frequent changes in shape.

Blade:

(= lamina) Flattened structure that is somewhat leaflike.

Bloom:

Massive or conspicuous growth of algae, usually a large percentage of the total cells belong to one or a few species.

Coccoid:

Simple cell type that is spherical, subspherical, or rod-shaped.

Cytokinesis:

The process by which one cell physically divides into two cells.

Epilithic:

Organisms living attached to the surfaces of rocks and stones.

Epipelic:

Organisms living attached to the surfaces of mud or sand.

Epiphytic:

Organisms living on the surfaces of plants or algae, using it for support but not for nutrition.

Epizoic:

Organisms living on the surfaces of animals.

Eukaryotic:

Organisms composed of cells with membrane-bounded nucleus. Most contain cells with a complex organization, with microtubules, membrane-bounded organelles, and chromatin organized into more than a single chromosome.

Eutrophic:

Waters that contain relatively high levels of dissolved nutrients (e.g., nitrate, phosphate); typically exhibit high levels of primary productivity.

Flagellum:

Long, threadlike organelle that projects out of the cell and functions in motility. In eukaryotic cells, they consist of a 9 doublet + 2 central singlet array of microtubules.

Frustule:

In diatoms, the silica cell wall or test, composed of two valves.

Holdfast:

A cell or multicellular structure that functions in attachment to a substrate.

Kelp:

Large phaeophytes that are members of the Laminariales.

Mastigonemate:

Stiff, lateral hairs borne by a flagellum, consisting of a base, a tubular shaft, and several terminal hairs.

Monophyletic:

Evolutionary term referring to a trait or group of organisms that evolved directly from a common ancestor.

Phagotrophic:

Mode of nutrition referring to heterotrophic protoctists or tissue cells that ingest solid food particles by phagocytosis.

Phycobiliproteins:

Complex of phycobilins with protein found in cyanobacteria, rhodophytes, glaucocystophytes, and some cryptophytes.

Phycobilisome:

Cellular structure containing phycobilin pigments and arranged as protrusions on the surface of the thylakoids of cyanobacteria, rhodophytes, and glaucocystophytes, but within the thylakoids (between membranous stacks) in the plastids of cryptophytes.

Photosynthetic pigments:

Pigments are chemical compounds present in algae by which the energy of sunlight is captured for photosynthesis.

Plastids:

Generic term for photosynthetic organelles present in algae. Plastids contain the enzymes and pigments for photosynthesis, ribosomes, and other structures.

Polyphyletic:

Evolutionary term referring to a trait or group of organisms that derived from more than one common evolutionary ancestor or ancestral group.

Prokaryotic:

Typically unicellular organism lacking a distinct nucleus and membrane-bound organelles.

Propagules:

Generative structure, any unicellular or multicellular, capable of survival, dissemination, and further growth.

Somatic:

General term referring to the body (soma) of an organism. The part not involved in reproduction or germination.

Spore:

Reproductive cell (motile or not) that originates by mitosis (mitospore) or meiosis (meiospore).

Stipe:

Stalk, stemlike portion of the algal thallus.

Symbiotic:

Physical association between organisms of different species.

Thallus:

The body of an alga that is not differentiated into roots, stalks, and leaves as in other plants.

Thylakoid:

Flat saclike structure formed by membranes that is present in the cytoplasm of cyanobacterial cells and in plastids of eukaryotic algae and plants.