Diversity and classification of marine macroalgae
Introduction
Marine macroalgae, commonly called seaweeds, are photosynthetic organisms that form an important component of shallow coastal ecosystems. They provide much of the primary production and habitat structure on rocky coasts and include three evolutionarily distinct groups: green algae, red algae and brown algae[1].
In the widest sense, algae share chlorophyll-based photosynthesis but differ widely in evolutionary origin (Fig. 1), cellular organization, and ecology (Cavalier-Smith, 2007[2]). In recent years our knowledge of these organisms has greatly advanced, thanks to new types of data (mainly electron microscopy observations and DNA sequence data). Based on these data, we now know that algae represent an artificial and unnatural agglomeration of very different organisms. This artificial grouping reflects a functional similarity rather than common ancestry, and modern classifications therefore treat the major algal lineages as separate evolutionary groups[3][4].
Although many algae are aquatic, numerous species occur in terrestrial, aerial, and symbiotic environments, including soils, rocks, snow, and lichens[5] (Fig. 2). Therefore, habitat alone cannot define the group.
Marine macroalgae are macroscopic photosynthetic organisms, traditionally described as plant-like, that are commonly designated by the term seaweeds[6]. Despite of the undeserved negative connotation associated with such a name, seaweeds play a fundamental role marine ecosystems, where they have a multitude of beneficial effects. Although unrecognized, they also have an important part in our everyday life. Substances extracted from seaweeds occur in toothpastes, shampoos, cosmetics, drugs, soups, ice creams, soft drinks, beer, jellies, marmelades, salad dressings, chewing gums and many other products of large use. In China, Korea and Japan some species of seaweeds are among the most popular foods, and for this reason they have been farmed for many centuries, see Seaweed (macro-algae) ecosystem services.
Most seaweeds grow attached to rock or other stable substrates, although some species also occur as unattached populations. Marine macroalgae are conventionally grouped as green, red and brown algae. These names refer to their characteristic pigmentation, but the three groups represent distantly related evolutionary lineages rather than subdivisions of a single taxonomic group. Besides the color, they differ in their photosynthetic pigments, storage compounds, composition of cell walls, presence/absence of flagella, ultrastructure of mitosis, fine structure of the chloroplasts and several other characters. Green and red algae belong to Archaeplastida, whereas brown algae belong to the Stramenopiles, a major lineage within the SAR supergroup (Stramenopiles, Alveolates and Rhizaria). This deep evolutionary separation reflects their different plastid histories [7]. This separation is due to the evolutionary origin of these groups (Fig. 1).
Instead than being killed and digested, the organism incorporated remained alive in its host and established a symbiotic relationship with it. The plastids of green and red algae originated from an ancient primary endosymbiosis, in which a cyanobacterium became incorporated into a non-photosynthetic eukaryotic host. Green and red algae subsequently diverged from this common photosynthetic ancestry. The plastids of green and red algae originated from an ancient primary endosymbiosis, in which a photosynthetic cyanobacterium was incorporated by a non-photosynthetic eukaryotic host. Instead of being digested, the cyanobacterium established a permanent metabolic relationship with its host and gradually evolved into the plastid. Green and red algae subsequently diverged from this common photosynthetic ancestry. Brown algae acquired photosynthesis later through secondary endosymbiosis, in which a red alga was incorporated by another eukaryotic host[8].
Green algae
The green algae represent a very diverse group, which includes members distributed not only in the sea, but also in freshwater and terrestrial habitats. Their classification has been revised in recent years, based on DNA sequence data. Green algae belong to the Viridiplantae (green plants), which also include land plants (Lewis and McCourt, 2004[9]). Many marine green algae belong to the class Ulvophyceae, although this group is phylogenetically diverse and includes multiple lineages with independent evolutionary histories[10]. It includes the familiar orders Ulvales, Cladophorales and Bryopsidales, which are distributed in all seas of the world.
In the green seaweeds, the body of the alga shows a great range of variation of forms, but usually its morphology is quite simple. Thin filaments, either branched or not, are a common growth form and are found in Cladophora (Fig. 3) and Chaetomorpha, two widespread genera. Sheets formed by two layers of cells are typical of Ulva (Fig. 4). Because of their appearance, species of this genus are popularly called sea lettuce. These algae are well known for their fast growth and high capacity to take up nutrients from seawater.
An abundant growth of Ulva is a common phenomenon in eutrophic waters; when such growth becomes uncontrolled, the accumulation of large masses of Ulva produces the so-called green tides, which may require mechanical removal of the algal biomass.
A type of body organization which is unique to the green seaweeds is the so-called siphonalean organization (or coenocytic organization). Siphonalean green algae are classified in two orders, Bryopsidales and Dasycladales, and are among the most ecologically successful seaweeds. The body of these algae is formed by one single giant cell, which contains numerous nuclei. The best-known example of siphonalean seaweeds is represented by the genus Caulerpa. Species of this genus consist of a creeping stolon (that grows attached to the rocky bottom), from which numerous erect frond of variable shape arise (Fig. 5). Species of Caulerpa are distributed in tropical and warm-temperate seas. Because of their beautiful habit, they are very popular among aquarium hobbyists and are widely used in tropical aquaria (Stam et al., 2006[11]). Unfortunately, algae of this genus have often the tendency to grow in aggressive and uncontrolled manner. The spread of Caulerpa taxifolia (Fig. 6) in the Mediterranean Sea, is thought to originate from an accidental release from the Monaco Oceanographic Museum, representing one of the most spectacular events of invasion by a marine organism. In subsequent years, a population of Caulerpa cylindracea introduced in an unknown way from Australia has also invaded aggressively the Mediterranean (Verlaque et al., 2003[12]; Piazzi et al., 2005[13]). Other common genera with siphonalean organization are Codium, Acetabularia, Halimeda, Udotea and Valonia. Halimeda has a peculiar appearance; it is a branched alga, whose body is formed by many connected segments with the shape of coins, wedges or sausages (Fig.7). This genus is widespread in tropical seas and is particularly important in the atolls. Its cell walls accumulate calcium carbonate, predominantly in the form of high-magnesium calcite. After death and fragmentation, the calcified thalli can make an important contribution to carbonate sediments in tropical coastal environments and to the white sand typical of atoll beaches.
Red algae
The red algae are one of the most ancient groups of eukaryotic algae (fossils of Bangiomorpha pubescens, believed to be the oldest red alga, are about one billion years old[14]). A distinctive characteristic of this group is that they are the only seaweeds lacking flagella (as well as centrioles and other structures typical of the flagellar apparatus) at any stage of their life histories (Maggs et al., 2007[15]). Their color, which ranges from pink to bright red, purple or sometimes dark brown, is due to the presence of pigments called phycobilins. At present, more than 7,000 red algal species are recognized. They have a complex life history, which usually involves the alternation of three generations (gametophyte, carposporophyte and tetrasporophyte).
Their sexual reproductive apparatus is a very sophisticated structure, whose arrangement has been used for a long time as the main criterion for taxonomy at ordinal level. Molecular data produced in the last two decades have revolutionised the classification of these organisms, which belong to a single phylum, the Rhodophyta. Rhodophyta constitute a well-supported evolutionary lineage, dominated in marine environments by the species-rich Bangiophyceae and especially Florideophyceae.
The red algae show a great range of morphological variation. The simplest forms consist of single cells like Porphyridium or thin filaments like Bangia. The habit of expanded blades is found in many genera, including some of the most spectacular, such as Delesseria (Fig. 8), Polyneura and Halymenia. A widespread and economically important genus with blade-like habit is Porphyra (Fig. 9). Neopyropia yezoensis and similar species are popularly known with the japanese name of nori and have been used as food for many centuries in eastern Asia; they are the seaweeds used as wrap for sushi. In other red algae, the body of the alga is formed by a crust which grows attached to the rocky bottom. A typical example is represented by species of the order Corallinales, in which the cell walls accumulate calcium carbonate in the form of calcite, conferring to their body a robust and coriaceous consistence. Algae of this order, such as Lithophyllum, Lithothamnion (Fig. 10) and Phymatolithon, look like pink or red calcified crusts, which are very resistent to grazing and mechanical dislodgement; they often thrive on very exposed rocky shores, where seaweeds with soft tissues would be easily dislodged by the violence of the waves. Many other species of red seaweeds have a branched plantlike shape and look like small bushes or trees. Species with this habit include many common genera, such as Chondrus, Gelidium (Fig. 11), Gigartina, Gracilaria, Hypnea and Laurencia. Species of Eucheuma and Kappahycus are the most important source of carrageenans (compounds widely used in the food industry), and for this purpose they are farmed on large scale in tropical regions, especially Philippines and Indonesia.
Brown algae
The brown algae are represented by about 2,000 species, currently classified in the class Fucophyceae of the phylum Ochrophyta (De Reviers et al., 2007[16]). Brown seaweeds are not close relatives of red and green seaweeds, although they are macroscopically similar and live mixed together on rocky shores. They belong to the Stramenopiles, a diverse group that also contains several major lineages of microscopic algae, including diatoms. Brown seaweeds are distributed in all seas of the world, but their largest and most spectacular representatives, particularly kelps (Laminariales), are characteristic of polar and temperate waters. Despite of this general trend, however, this group includes also some genera which are very common and diverse in tropical seas, such as Sargassum (Fig. 12) and Turbinaria.
The diversity of forms and shapes of the brown seaweeds is not inferior to that of the green and red seaweeds. Filamentous species consisting of thin branched threads, such as Ectocarpus and Pylaiella (Fig. 13), grow on rock or on larger seaweeds in the intertidal zone of many regions of the world. Most brown algae, however, have a bigger size and look like branched ribbons, bushes or small trees. Canopy-forming Fucales are important foundation species: their three-dimensional structure creates habitat, modifies local environmental conditions and supports diverse associated communities. The belts of Fucus (Fig. 14) in the northern Atlantic and canopy-forming species traditionally grouped in Cystoseira (now divided among Cystoseira, Ericaria and Gongolaria, Fig. 15) in the Mediterranean are well known-examples. This order also includes the exceptional holopelagic Sargassum species, which live permanently floating and are never attached to the sea bottom. The Sargasso Sea, located in the middle of the North Atlantic Ocean, is an area delimited by oceanic currents in which large masses of Sargassum float permanently.
The largest known algae are also species of brown seaweeds; they belong to the order Laminariales and are designated with the term kelps. The giant Pacific kelp Macrocystis pyrifera (Fig. 16) is the seaweed with the largest size. It can reach 60 meters in length and forms dense forests on the Pacific shores of Canada and U.S.A. Similar submerged forests are produced in other parts of the world by species of Ecklonia, Eisenia, Laminaria and Lessonia. Kelps exhibit a high degree of morphological differentiation, but they lack true vascular tissues such as xylem and phloem and are therefore not directly comparable to vascular plants[5]. See Kelp forests.
ACKNOWLEDGEMENTS. I am very grateful to the Marine Institute of Ireland for financial support received under the National Marine Biodiscovery Program. I am also thankful to Michael Guiry, Rob Anderson, John Bolton, Olivier De Clerck, Katrin Österlund, Erasmo Macaya, Eduardo Infantes Oanes, Colin Bates, Yukihiko Serisawa and Heroen Verbruggen for use of pictures, obtained from AlgaeBase (www.algaebase.org).
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References
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