Identifying Harmful Marine Dinoflagellates

Alexandrium tamarense
(Lebour) Balech, 1985
Plate 7, Figs. 1-6

Species Overview: Alexandrium tamarense is an armoured, marine, planktonic dinoflagellate. It is associated with toxic PSP blooms in cold water coastal regions.

Taxonomic Description: Cells of A. tamarense are small to medium in size, nearly spherical, and slightly longer than wide (Fig. 1). The first apical plate bears a ventral pore (Figs. 3, 5). Cells are commonly found single or in pairs (Figs. 1-3), and less commonly in fours. Paired cells may contain an anterior attachment pore (aap) and a posterior attachment pore (pap)(Fig. 4). Thecal plates are smooth and thin (Fig. 3). The size and shape of this species is highly variable: cells range in size between 22-51 Ám in length and 17-44 Ám in transdiameter width (Lebour 1925; Fukuyo et al. 1990; Hallegraeff 1991; Hallegraeff et al. 1991; Larsen & Moestrup 1989; Balech 1995; Taylor et al. 1995; Steidinger & Tangen 1996).

Nomenclatural Types:
Holotype: Gonyaulax tamarensis Lebour, 1925: 92, plate XIV, figs. 1a-1d
Type Locality: English Channel: River Tamar Estuary, near Plymouth, United Kingdom
Synonyms: Gonyaulax tamarensis Lebour, 1925
Gonyaulax tamarensis var. excavata Braarud, 1945
Gonyaulax excavata (Braarud) Balech, 1971
Gessnerium tamarensis (Lebour) Loeblich and Loeblich, 1979
Protogonyaulax tamarensis (Lebour) Taylor, 1979
Alexandrium excavatum (Braarud) Balech and Tangen, 1985

Thecal Plate Description: The plate formula for A. tamarense is: Po, 4', 6'', 6c, 8s, 5''', 2''''. The apical pore complex (APC) is rectangular and narrows ventrally (Fig. 3). The apical pore plate (Po) houses a large fishhook shaped foramen and a small round aap (Figs. 3, 4). The first apical plate (1') is variable in shape: from a broad triangle to a narrow rectangle, and bears a small ventral pore (Figs. 3, 5). The 1' plate comes in direct contact with the Po (Fig. 3) (Lebour 1925; Fukuyo et al. 1985; 1990; Larsen & Moestrup 1989; Balech 1995; Taylor et al. 1995; Steidinger & Tangen 1996).
The epitheca and hypotheca are nearly equal in height (Figs. 1, 2, 5). The epitheca is broadly conical, while the hypotheca is roughly trapezoidal (Figs. 1, 2, 5). The posterior end is slightly indented resulting in two hypothecal lobes; the left lobe is slightly larger than the right (Figs. 1, 2). The deeply excavated cingulum is displaced in a descending fashion one time its width with narrow lists (Figs. 2, 5). The deep sulcus, with lists, widens posteriorly (Figs. 2, 5). The posterior attachment pore (pap), if present, is small and located in the right half of the posterior sulcal plate (Lebour 1925; Fukuyo et al. 1985; 1990; Larsen & Moestrup 1989; Balech 1995; Taylor et al. 1995; Steidinger & Tangen 1996).

Morphology and Structure: A. tamarense is a photosynthetic species with a number of orange-brown chloroplasts. A lunar-shaped nucleus is situated ventrally just inside the cingulum (Fig. 1) (Fukuyo 1985; Larsen & Moestrup 1989).

Reproduction: A. tamarense reproduces asexually by binary fission; plane of fission is oblique. This species also has a sexual cycle with anisogamous mating types. The gametes join laterally for sexual fusion, produce a planozygote which then encysts into a characteristic resting cyst (Fig. 6) (Loeblich & Loeblich 1975; Turpin et al. 1978; Silva 1962).

Ecology: A. tamarense is a planktonic dinoflagellate species associated with toxic paralytic shellfish poisoning (PSP) events around the world. Toxic blooms are commonly reported in Japan (Fukuyo et al. 1985; Ogata et al. 1982; Oshima et al. 1982). Red tide blooms of A. tamarense have been reported in Europe (Mortensen 1985; Moestrup & Hansen 1988), and are common along the NE coast of North America (New England and Canada) (Bicknell & Walsh 1975; Hurst 1975; Loeblich & Loeblich 1975). During a red tide event reported in the Faroe Islands, Norway, in 1984, population levels of A. tamarense were estimated at 1X 107 cells/L and completely dominated the plankton (Mortensen 1985; Moestrup & Hansen 1988).
This species produces an ellipsoidal resting cyst that cannot be distinguished from the cyst produced by A. catenella. This cyst has rounded ends with a thick cell wall, and is covered in mucilage (Fig. 6). Cysts often contain colorless granules and distinct reddish lipid bodies. Size ranges from 36-56 Ám in length and 23-32 Ám in width (Turpin et al. 1978; Fukuyo 1985; Bolch & Hallegraeff 1990; Hallegraeff 1991; Hallegraeff et al. 1991).

Toxicity: Alexandrium tamarense is a known toxin-producing dinoflagellate species. This species produces very potent PSP neurotoxins which can affect humans, other mammals, fish and birds (Larsen & Moestrup 1989): gonyautoxins (GTX I, II, III, IV and V), neosaxitoxin (NSTX) and saxitoxin (SXT) (Shimizu et al. 1975; Oshima et al. 1977). This species is responsible for numerous human illnesses and several deaths after consumption of infected shellfish: ten deaths in Venezuela in 1977 (Reyes-Vasquez et al. 1979), and one death in Thailand in 1984 (Tamiyavanich et al. 1985). Resting cysts of A. tamarense can also harbor PSP toxins. Dale et al. (1978) demonstrated that cysts were more than ten times as toxic as their motile stage counterparts.
Not all strains of A. tamarense are toxic: both toxic and nontoxic strains have been reported in New England within the same red tide event (Yentsch et al. 1978). Strains in Australia (Hallegraeff 1991), River Tamar estuary, Britain (type locality) (Moestrup & Hansen 1988) and the Gulf of Thailand (Fukuyo et al. 1988) are all non-toxic.
The usual route of PSP toxin transmission is via contaminated shellfish; however, bloom events of A. tamarense have been linked to several massive fish kills: Atlantic herring in the Bay of Fundy, Canada (White 1980); and rainbow trout and salmon in the Faroe Islands, Norway (Mortensen 1985). Hayashi et al. (1982) attribute the fish kills to dinoflagellate toxins accumulated in the food chain; i.e. fish feed on zooplankton infected with PSP poisons and die. However, Ogata and Kodama (1986) report production of ichthyotoxins in cultured media of this species.

Species Comparison: A. tamarense can resemble a number of other species within the genus, but it can be distinguished by its cell shape and size, presence of a ventral pore (vp) on the 1' plate, and shape of the thecal plates (Balech 1995; Hallegraeff 1991; Larsen & Moestrup 1989; Steidinger & Tangen 1996).
A. tamarense is very similar morphologically (size, shape and thecal plate formula) to A. catenella; both also produce deadly PSP toxins. Morphological differences lie in the shape of the Po, and presence or absence of a vp: the Po in A. catenella is slightly smaller than that in A. tamarense, and the vp is absent (Fukuyo 1985). Molecular testing conducted on A. catenella from Japan and A. tamarense from Japan and the U.S.A. revealed a close genetic relationship between the two species, however they remain distinct (Adachi et al. 1995).
Morphologically, A. fundyense is nearly identical to A. tamarense except for the missing ventral pore on the 1' plate. A. minutum can also be misidentified as A. tamarense; however, A. tamarense is a smaller species, is always longer than wide, and is found in colder waters than A. minutum (Balech 1995; Hallegraeff 1991; Larsen & Moestrup 1989; Steidinger & Tangen 1996).

Habitat and Locality: A. tamarense is a widely distributed coastal and estuarine dinoflagellate species (Lebour 1925; Steidinger & Tangen 1996) mainly found in cold to cold-temperate waters in North America, Europe and Japan. However, this species has been reported from warmer waters around the world: Australia, Venezuela and the Gulf of Thailand (Balech 1995; Fukuyo et al. 1990; Hallegraeff 1991; Steidinger & Tangen 1996; Taylor et al. 1995).

Figure 1: Morphology of a Dinoflagellate