296 CHLOROPLAST E.R.: EVOLUTION OF ONE MEMBRANE

dinoflagellate to release photosynthate outside the cell for absorption by the animal cells (Wang and Douglas, 1997).

Corals with symbiotic dinoflagellates do not incorporate calcium into their skeletons as fast as corals without symbiotic dinoflagellates. During the daytime, corals with and without symbiotic dinoflagellates calcify at the same rate. Calcification occurs three times faster during the day than at night (Gattuso et al., 2001).

In the symbiosis between the marine anemones and marine dinoflagellates, the dry weight ratio of host to alga is about 300 : 1 (Taylor, 1969). When the anemone is subjected to poor growing conditions, it responds by excreting some of the dinoflagellate cells, which the anemone obviously has difficulty in maintaining. Even under normal growing conditions the algal population divides too rapidly, and the anemone reacts by pruning the population down to a level it can support. In this situation the older dinoflagellate cells in the outer regions of the host (crown and tentacles) respond by thickening the outer secreted layer around the cell wall and subsequently forming cysts. As the thickness of the cyst’s outer layer increases, the cells begin to show signs of degeneration. The host then seems to become sensitive to the degenerate condition of the cysts and reacts by removing them from these outer regions and transporting them to the mesenteries as intracellular inclusions of its undifferentiated amoeboid cells. They are stored in the mesenteries in varying states of decomposition until they are finally excreted by the host.

In the flatworm Amphiscolops langerhansi, D. L. Taylor (1971) has found that the cells of the dinoflagellate Amphidinium klebsii occur exclusively between the cells of the peripheral parenchyma of the host and appear as a conspicuous layer below the composite muscle (Fig. 7.53). Each cell of Amphidinium has a specific and uniform orientation within the host. The anterior of the cell is directed toward the central parenchyma, and the posterior with the large nucleus is directed toward the epithelium. By rearing the flatworm from eggs, it is possible to obtain individuals without the dinoflagellate symbiont. When these flatworms are grown in culture with a number of different types of dinoflagellates, only species of

Amphidinium are able to infect the host. When contact is made, the animal seizes and ingests the alga. Once inside the flatworm, the alga is not retained in the central digestive paranchyma but passes freely between the animal cells to the peripheral parenchyma, where it comes to lie intercellularly below the composite muscle. The alga remains unchanged within the host and still has its typical two flagella. In nature the association between the flatworm and the dinoflagellate is probably essential for the survival of the animal. It is not known whether the dinoflagellate receives any benefit.

In addition to Dinophyceae living symbiotically inside other organisms, there are other organisms that live inside dinoflagellate cells. Noctiluca scintillans is a heterotrophic omnivorous feeder that ingests zooplankton, mesozooplankton, and their eggs (Fig. 7.47) (Hansen et al., 2004). However, in the tropical to subtropical areas of Southeast Asia, a green form of N. scintillans is found. The cells have 6 000 to 12 000 green flagellates actively swimming in the fluid within the large vacuoles (Fig. 7.54), especially around the periphery of the vacuole. The green flagellate resembles the green alga Pedinomonas in being bright green, 2 5 m in size, with no eyespot, and having a single posterior flagellum. Whether the dinoflagellate gains any advantage from the association is not known.

Classification

There is a single class in the Dinophyta, the Dinophyceae. Four orders are considered here. Molecular studies have shown that the Prorocentrales, Peridiniales, and Gymnodiniales represent three clear lines of evolution (Zardoya et al., 1995). The Dinophysiales are probably related to the Prorocentrales since they are both divided vertically into two halves.

Order 1 Prorocentrales: cell wall divided vertically into two halves; no girdle; two flagella borne at cell apex.

Order 2 Dinophysiales: cell wall divided vertically into two halves, cells with elaborate extensions of the theca.

DINOPHYTA 297

Fig. 7.53 (a) Cross section of the flatworm Amphiscolops langerhansii showing the dinoflagellate Amphidinium klebsii

(a) in the peripheral parenchyma (pp). (cp) Central parenchyma; (d) dorsal surface; (e) epithelium; (v) ventral surface. 90. (b) Diagrammatic reconstruction of the above association. (a) Accumulation body; (c) chloroplast; (ci) cilia; (cm) circular muscle; (cr) ciliary root; (f) flagellum; (l) lipid; (lm) longitudinal muscle; (n) nucleus; (p) pyrenoid;

(pu) pusule; (s) starch; (v) vacuole. (After D. Taylor, 1971.)

(b)

(a)

Fig. 7.54 Noctiluca containing green algae in its vacuoles. (a) Whole cell. (g) Green algae; (t) tentacle. (b) Green symbiont. (After Sweeney, 1971.)

Order 3 Peridiniales: motile cells with

an epicone and hypocone separated by a girdle, relatively thick theca.

Order 4 Gymnodiniales: motile cells with an epicone and hypocone separated by a girdle; theca thin or reduced to empty vesicles.

Prorocentrales

These cells have the cell wall divided vertically into two halves, no girdle, and two apically inserted flagella, Prorocentrum (Figs. 7.55, 7.56(b), (c)) can be used as an example of the order. The cell is divided vertically into two halves, each half containing a relatively thick thecal plate, the suture joining them running from the anterior to the posterior end. The cell is flattened parallel to the suture so the two halves are like two watch glasses. The two flagella emerge apically through a pore, and there is a single tooth containing cytoplasm. Usually there are two brownish-yellow chloroplasts, apposed to the two valves. Asexual reproduction takes place by longitudinal division, the daughter cells retaining one valve of the parent and forming a new second valve.

298 CHLOROPLAST E.R.: EVOLUTION OF ONE MEMBRANE

Fig. 7.55 Scanning electron micrographs of Prorocentrum

hoffmanianum. (From Faust, 1990.)

Dinophysiales

This order consists of morphologically complex organisms that are mainly in tropical seas, with the cells having adaptations to the floating habit such as elaborate wings (lists). One of the more complex organisms in this order is Ornithocercus (Fig. 7.56(d), (e)). The cell is divided vertically into two halves by an anterior posterior suture. The cells have a girdle and sulcus, with the side having the sulcus being the ventral side and the opposite side being the dorsal side. The respective flagella lie in the girdle and transverse sulcus. The epicone is usually much smaller than the hypocone, and the edges of the thecal plates next to the girdle and sulcus are expanded into the lists. In asexual reproduction the cell is cleaved vertically, with the two halves separating and the missing half being formed by the protoplasm. The oldest fossil of this group is Nannoceratopsis from the Lower Jurassic (Loeblich, 1974, 1976).

Peridiniales

The dinoflagellates in this order have relatively thick thecal plates, in contrast to the next order,

the Gymnodiniales, which has no, or thin, thecal plates. The algae in this order have the classic dinoflagellate structure (Figs. 7.1, 7.2) with an epicone and hypocone and two furrows, the transverse girdle and the longitudinal sulcus.

The widely distributed genus Ceratium (Figs. 7.12, 7.57, 7.58) is markedly asymmetric, with one apical horn and two to three long antapical horns filled with cytoplasm. The girdle is nearly horizontal and divides the body into two approximately equal, but dissimilar halves. In the middle of the ventral surface is a large rhombic hyaline area, which is probably similar to a sulcus. Like other Dinophyceae and Prymnesiophyceae, Ceratium is more common in warmer water than in colder polar waters. There are fewer than ten species common in the colder waters of the North Atlantic, whereas more than 20 species are common in the warmer more southerly waters (Graham and Bronikovsky, 1944). Ceratium is one of the members of the phytoplankton that has shade forms which show an increase in frequency from the surface to 100 m depth. These shade forms are found only in the relatively sterile warm oceanic waters where the upper layers are usually depleted of nitrogen and phosphorus. The shade forms of Ceratium have a survival value in that

DINOPHYTA 299

Fig. 7.56 (a) Oxyrrhis marina. (f) Fat globule; (g) girdle; (l) longitudinal flagellum; (n) nucleus; (o) tentacle. (b),(c)

Prorocentrum micans, side (b) and front (c) views. (n) Nucleus;

(s) suture; (v) vacuole. (d),(e) Ornithoceros magnificus, a righthand view (d) and an “exploded” view (e) of the theca. (DA) Dorsal accessory moiety of the left sulcal list; (LLG) left lower girdle list; (LS(am)) anterior moiety of the left sulcal list; (LS(pm)) posterior moiety of the left sulcal list; (LUG) left upper girdle list; (RS) right sulcal list; (RLG and RUG) right lower and upper girdle list; (g) girdle; (p) pore; (w) wing. ((d),(e) after F. Taylor, 1971.)

they are able to take advantage of the higher levels of nitrogen and phosphorus deeper in the water and still are able to receive enough light to keep their photosynthetic rate above their respiratory rate. These shade forms adapt themselves to absorb the maximum amount of light by increasing the surface area of the cell by expansion of the cell body and/or horns and packing these extensions with chloroplasts. Long-horned forms are found among surface forms also, but the shade