Marine Species Identification Portal : Alexandrium tamarense

Alexandrium tamarense (Lebour) Balech, 1985b

Species Overview:

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

Taxonomical Description:

Cells of A. tamarense are small to medium in size, almost isodiametric, and slightly longer than wide (Fig. 1). No apical horn is present. The first apical plate bears the ventral pore (Figs. 2,3). Cells are commonly found single or in pairs (Fig. 1), and less commonly in fours. Paired cells may contain an anterior attachment pore (aap) and a posterior attachment pore (pap) (Figs. 4,5). Thecal plates are smooth and thin (Figs. 1-3). The size and shape of this species is highly variable: cells range in size between 22-51 µm in length and 17-44 µm in transdiameter width (Lebour, 1925, Fukuyo et al., 1985, Fukuyo et al., 1990, Hallegraeff, 1991, Hallegraeff et al., 1991, Larsen and Moestrup, 1989, Balech, 1995, Taylor et al., 1995, Steidinger and Tangen, 1996).

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. The apical pore plate (Po) houses a large fishhook shaped foramen and a small round aap (Figs. 2,4). The first apical plate (1') (Figs. 2,3) is variable in shape: from a broad triangle to a narrow rectangle, and bears a small ventral pore. The 1' plate comes in direct contact with the Po (Fig. 2) (Lebour, 1925, Fukuyo et al., 1985, Fukuyo et al., 1990, Larsen and Moestrup, 1989, Balech, 1995, Taylor et al., 1995, Steidinger and Tangen, 1996).

The epitheca and hypotheca are nearly equal in height (Figs. 1,6). The epitheca is broadly conical (Figs. 1,6), while the hypotheca is roughly trapezoidal (Figs. 1,6). The posterior end is slightly indented resulting in two hypothecal lobes; the left lobe is slightly larger than the right (Figs. 1,6). The deeply excavated cingulum is displaced in a descending fashion one time its width; it has a narrow list (Figs. 1,2,6). The deep sulcus, with lists, widens posteriorly (Fig. 1). The pap, if present, is small and located in the right half of the posterior sulcal plate (Fig. 5) (Lebour, 1925, Fukuyo et al., 1985, Fukuyo et al., 1990, Larsen and Moestrup, 1989, Balech, 1995, Taylor et al., 1995, Steidinger and 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 (Fukuyo, 1985, Larsen and 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 (Figs. 7,8) (Loeblich and Loeblich, 1975, Turpin et al., 1978, Silva, 1962).

Species Comparisons:

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 and Moestrup, 1989, Steidinger and 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 and Moestrup, 1989, Steidinger and Tangen, 1996).

Ecology:

A. tamarense is a planktonic dinoflagellate species associated with toxic 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 and Hansen, 1988), and are common along the NE coast of North America (New England and Canada) (Bicknell and Walsh, 1975, Hurst, 1975, Loeblich and Loeblich, 1975). During a red tide event reported in the Faroe Islands, Norway, in 1984, population levels of A. tamarense were estimated at 1 X 10^7 cells/L and completely dominated the plankton (Mortensen, 1985, Moestrup and Hansen, 1988).

This species produces a 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 (Figs. 7,8). Cysts often contain colorless granules and distinct reddish lipid bodies. Size ranges from 36-56 µm in length and 23-32 µm in width (Turpin et al., 1978, Fukuyo, 1985, Bolch and 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 and Moestrup, 1989): GTX I, II, III, IV and V, neosaxitoxin and saxitoxin (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 and Hansen, 1988) and the Gulf of Thailand (Fukuyo et al., 1988) are all non-toxic.

The usual route of PSP toxin transmission is via tainted 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.

Habitat and Locality:

A. tamarense is a widely distributed coastal and estuarine dinoflagellate species (Lebour, 1925, Steidinger and 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 and Tangen, 1996, Taylor et al., 1995).

Adachi, M., Y. Sako, A. Uchida and Y. Ishida 1995. Ribosomal DNA internal transcribed spacer regions (ITS) define species of the genus Alexandrium. In: P. Lassus, G. Arzul, E. Erard, P. Gentien and C. Marcaillou (eds), Harmful Marine Algal Blooms, Lavoisier, Intercept Ltd: 15-20.

Balech, E. and K. Tangen 1985. Morphology and taxonomy of toxic species in the tamarensis group (Dinophyceae): Alexandrium excavatum (Braarud) comb. nov. and Alexandrium ostenfeldii comb. nov. Sarsia 70: 333-343.

Balech, E. 1971b. Microplancton del Atlantico Ecuatorial Oeste (Equalant I). Servicio de Hidrografia Nava, Buenos Aries H 654: 1-103.

Balech, E. 1985b. The genus Alexandrium or Gonyaulax of the tamarensis group. In: D.M. Anderson, A.W. White and D.G. Baden (eds), Toxic Dinoflagellates, Elsevier, New York: 33-38.

Balech, E. 1995. The Genus Alexandrium Halim (Dinoflagellata), Sherkin Island Marine Station, Ireland. 151 pp.

Bicknell, W.J. and D.C. Walsh 1975. The first 'red tide' in recorded Massachusetts history: managing an acute and unexpectd public health emergency. In: V.R. LoCicero (ed), Proc. First Int. Conf. Toxic Dinoflagellate Blooms, Massachusetts Sci. Tech. Found., Wakefield: 447-458.

Bolch, C.J. and G.M. Hallegraeff 1990. Dinoflagellate cysts in Recent marine sediments from Tasmania, Australia. Bot. Mar. 33: 173-192.

Braarud, T. 1945. Morphological observations on marine dinoflagellate cultures (Porella perforata, Goniaulax tamarensis, Protoceratium reticulatum). Avh. Utgitt. Nor. Vidensk. Akad. Oslo Mat.-Naturvidensk. Kl. 11: 1-18.

Dale, B., C.M. Yentsch and J.W. Hurst 1978. Toxicity in resting cysts of the red-tide dinoflagellate Gonyaulax excavata from deeper water coastal sediments. Science 201: 1223-1223.

Fukuyo, Y., K. Yoshida and H. Inoue 1985. Protogonyaulax in Japanese coastal waters. In: D.M. Anderson, A.W. White and D.G. Baden (eds), Toxic Dinoflagellates, Elsevier, New York: 27-32.

Fukuyo, Y., P. Pholpunthin and K. Yoshida 1988. Protogonyaulax (Dinophyceae) in the Gulf of Thailand. Bull. Plank. Soc. Jpn. 35: 9-20.

Fukuyo, Y., H. Takano, M. Chihara and K. Matsuoka 1990. Red Tide Organisms in Japan. An Illustrated Taxonomic Guide. Uchida Rokakuho, Co., Ltd., Tokyo. 407 pp.

Fukuyo, Y. 1985. Morphology of Protogonyaulax tamarensis (Lebour) and Protogonyaulax catenella (Whedon and Kofoid) Taylor from Japanese coastal waters. Bull. Mar. Sci. 37: 533-534.

Hallegraeff, G.M., C.J. Bolch, S.I. Blackburn and Y. Oshima 1991. Species of the toxigenic dinoflagellate genus Alexandrium in southeastern Australian waters. Bot. Mar. 34: 575-587.

Hallegraeff, G.M. 1991. Aquaculturists Guide to Harmful Australian Microalgae. Fishing Industry Training Board of Tasmania/CSIRO Division of Fisheries, Hobart, 111 pp.

Hayashi, T., Y. Shimizu and A.W. White 1982. Toxin profile of herbivorous zooplankton during a Gonyaulax bloom in the Bay of Fundy. Bull. Japan. Soc. Sci. Fish. 48: 1673.

Hurst, J.W., Jr. 1975. History of paralytic shellfish poisoning on the Maine coast 1958-1974. In: V.R. LoCicero (ed), Proc. First Int. Conf. Toxic Dinoflagellate Blooms, Massachusetts Sci. Tech. Found., Wakefield: 525-528.

Larsen, J. and O. Moestrup 1989. Guide to Toxic and Potentially Toxic Marine Algae. The Fish Inspection Service, Ministry of Fisheries, Copenhagen. 61 pp.

Lebour, M.V. 1925. The Dinoflagellates of Northern Seas. Marine Biol. Assoc. U.K., Plymouth. 250 pp.

Loeblich, L.A. and A.R. Loeblich, III 1975. The organism causing New England red tides: Gonyaulax excavata. In: V.R. LoCicero (ed), Proc. First Int. Conf. Toxic Dinoflagellate Blooms, Massachusetts Sci. Tech. Found., Wakefield: 207-224.

Loeblich III, A.R. and L.A. Loeblich 1979. The systematics of Gonyaulax with special reference to the toxic species. In: Taylor, D.L. and H.H. Seliger (eds), Toxic Dinoflagellate Blooms, Elsevier / North Holland, New York: 41-46.

Moestrup, O. and P.J. Hansen 1988. On the occurrence of the potentially toxic dinoflagellates Alexandrium tamarense (= Gonyaulax excavata) and A. ostenfeldii in Danish and Faroese waters. Ophelia 28: 195-213.

Mortensen, A.M. 1985. Massive fish mortalities in the Faroe Islands caused by a Gonyaulax excavata red tide. In: Anderson, D.M., A.W. White and D.G. Baden (eds), Toxic Dinoflagellates, Elsevier, New York: 165-170.

Ogata, T. and M. Kodama 1986. Ichthyotoxicity found in cultured media of Protogonyaulax spp. Mar. Biol. 92: 31-34.

Ogata, T., M. Kodama, Y. Fukuyo, T. Inoue, H. Kamiya, F. Matsuura, K. Sekiguchi and S. Watanabe 1982. The occurrence of Protogonyaulax spp. in Ofunato Bay, in association with the toxification of the scallop Patinopecten yessoensis. Bull. Jap. Soc. Sci. Fish.48: 563-566.

Oshima, Y., L.J. Buckley, M. Alam and Y. Shimizu 1977. Heterogeneity of paralytic shellfish poisons. Three new toxins from cultured Gonyaulax tamarensis cells, Mya arenaria and Saxidomus giganteus. Comp. Biochem. Physiol. 57C: 31-34.

Oshima, Y., T. Yasumoto, M. Kodama, T. Ogata, Y. Fukuyo and F. Matsuura 1982. Features of paralytic shellfish poison occurring in Tohoku District. Bull. Jap. Soc. Sci. Fish. 48: 525-530.

Reyes-Vasquez, G., E. Ferraz-Reyes and E. Vasquez 1979. Toxic dinoflagellate blooms in northeastern Venezuela during 1977. In: D.L. Taylor and H.H. Seliger (eds), Toxic Dinoflagellate Blooms, Elsevier / North Holland, New York: 191-194.

Shimizu, Y., M. Alam, Y. Oshima and W.E. Fallon 1975. Presence of four toxins in red tide infested clams and cultured Gonyaulax tamarensis cells. Biochem. Biophys. Res. Commun. 66: 731-737.

Silva, E.S. 1962. Some observations on marine dinoflagellate cultures. Not. E. Estud. Instit. Biol. Marit. 26: 1-26.

Steidinger, K.A. and K. Tangen 1996. Dinoflagellates. In: C.R. Tomas (ed), Identifying Marine Diatoms and Dinoflagellates, Academic Press, New York: 387-598.

Tamiyavanich, S., M. Kodama and Y. Fukuyo 1985. The occurrence of paralytic shellfish poisoning in Thailand. In: D.M. Anderson, A.W. White and D.G. Baden (eds), Toxic Dinoflagellates, Elsevier, New York: 521-524.

Taylor, F.J.R., Y. Fukuyo and J. Larsen 1995. Taxonomy of harmful dinoflagellates. In: G.M. Hallegraeff, D.M. Anderson and A.D. Cembella (eds), Manual on Harmful Marine Microalgae, IOC Manuals and Guides No. 33. UNESCO, France: 283-317.

Taylor, F.J.R. 1979b. The toxigenic gonyaulacoid dinoflagellates. In: Taylor, D.L. and H.H. Seliger (eds), Toxic Dinoflagellate Blooms, Elsevier / North-Holland, New York: 47-56.

Turpin, D.H., P.E.R. Dobell and F.J.R. Taylor 1978. Sexuality and cyst formation in Pacific strains of the toxic dinoflagellate Gonyaulax tamarensis. J. Phycol. 14: 235-238.

White, A.W. 1980. Recurrence of kills of Atlantic hering caused by dinoflagellate toxins transferred through herbivorous zooplankton. Can. J. Fish. Aquat. Sci. 37: 2262-2265.

Yentsch, C.M., B. Dale and J.W. Hurst 1978. Coexistence of toxic and nontoxic dinoflagellates resembling Gonyaulax tamarensis in New England coastal waters (NW Atlantic). J. Phycol. 14: 330.

Images

Alex.tamarense2.TIF (Fig. 2. SEM. Apical view. Po and 1' plate come in direct contact. Po=apical pore plate.)
Alex.tamarense3.TIF (Fig. 3. LM. 1' plate: bears a round vp. Shape varies: from broad triangle to narrow rectangle. vp=ventral pore.)
Alex.tamarense4.TIF (Fig. 4. SEM. APC: Po rectangular and narrows ventrally housing large fishhook shaped foramen, and a small round aap. aap=anterior attachment pore.)
Alex.tamarense5.TIF (Fig. 5. LM. Paired cells may contain a small pap on sp plate. pap=posterior attachment pore; sp=posterior sulcal plate.)
Alex.tamarense6.TIF (Fig. 6. LM. Live single cell. Cingulum lipped. Epitheca and hypotheca nearly equal in height. Left hypothecal lobe slightly larger than right (arrow).)
Alex.tamarense7.TIF (Fig. 7. LM. Resting cysts of A. tamarense (indistinguishable from those of A. catenatum). Cysts with rounded ends, reddish lipid bodies, and covered in mucilage.)
Alex.tamarense8.TIF (Fig. 8. LM. Resting cysts.)
Alex.tamarense9.TIF (Fig. 9. Line drawing.)
Alex.tamarense10.TIF (Fig. 10. Line drawing.)

Alexandrium tamarense