### Harmful Algal B l ooms and Their Effect s on Marine and Estuarine Animals

Jan H. Landsberg (1) and Sandra S. Shum way (2)

1 Florida Departm e nt of Environm ental Protecti on, Florida Marine Research Institute, 100 Eighth Avenue Southeast, St. Petersburg, Flor ida 33712 USA, landsberg_j @epic7.dep.state.fl.us

2 Natural Science Division, Southam p t on Colle ge, Long Island Universi ty Southam p ton, New York 11968 USA, sshumway@sunburn.liunet.edu

Abstract Increasing docum e ntation of har m ful algal blooms (HABs) in m a rine and estuarine system s has begun to demonstrate th eir far reach ing im pacts on ecosystem in teg r ity, sp ecies interactions, aquatic anim al health and population growt h, hum an health, econom y, industry, and ecology.

While som e 5000 species of m i croalgae are known world wide and less than 2% are known to be harmful or toxic, the number of toxic species appears to be increasing (Hallegraeff 1993, Sournia 1995). Much of the increase can be attributed to the study of benthic m i croalgae and the detection of toxic species or to species previous ly described that were not known to be toxic. While this increase partially re flects technological im prove m e nt in accurate identification of HAB species and their toxins, and enhanced m o n itoring and surveillan ce, it is also ass o ciated

with continu e d anthropo genic influences and in teracting natural pro cess e s. Because som e HABs tend to be planktonic, visibly obvi ous, acute in nature, and lead to fast-acting shellfish poisoning

events or m a ss m o rtalities of aquatic organism s, these are the HABs about which m o st is known.

Marine and estuarine H A Bs cause anim al m o rtalit ies, shellfish and tropi cal fish poisonings, and respiratory irritation and neur ocognitive disease in hum a ns (Steidinger 1993, Burkholder and Glasgow 1997). At least 85 species of toxic or harmful m a rine m i croalgae are know n worldwide; all potentially have varying im pacts on natura l resources and public (Sournia 1995, Steidinger

pers. comm .). Aquatic anim als are typically expose d to toxic or harm ful algae when planktonic or benthic species bloom and dom i nate the food web, but there are al so m o re subtle and insidious

exposure m echanism s that are not so obvious. E xposure to toxins occurs through ingestion of cells (filter f eeders e.g. sponges, m o l l uscs, crus tacea), b i oaccum ulation b y consum ption of toxic prey (e.g. crustacea, gastropods, fish, birds, tu rtles, m a mmals), aerosolized transport (e.g. respiratory irritation in hum a ns and potentially in m a mmals, turtles, birds), water-borne toxin

af

ter ce ll ly s i s (f ish, she l lf ish), sed i ment si nks (benthic organism s) , and possibly through

consum ption of toxic benthic stages.

Fish or invertebrate kills have been attributed to low dissolved oxygen associated with non toxic, high biom ass, plankton bloom s such as Cera tium or Noctiluca (Mahoney and Steim l e 1979, Adnan 1989). Most bloom s of toxic photosynthetic m i croalgae (Heterocapsa, Gym n odinium

, Gyrodinium, Alexandrium, Cochlodinium

, Prorocentrum , Chattonella, Heterosigm a, Prym nesium, Chrysochrom u lina, and Nodularia) cau se m o rtalities of m a rine, estuarine, or

associated terrestrial anim als, both in the wild and in aquaculture (Gunter et al. 1948, Steidinger et al. 1973, Cross and Southgate 1978, Morten sen 1985, Okaichi 1985,Yuki and Yoshim atsu 1989, Chang et al. 1990; Guz m an et al. 1990, S humway 1990, Kaartvedt et al. 1991, R obertson1991, Shumway and Cembella 1993, Su et al. 1993, Heidal and Mohus 1995, Horiguchi 1995, Negri et al. 1995, Yongjia et al. 1995, Burkholder 1998, Steidinger et al. 1998). Recently, a series of shellfish and fish kills, ul cerated fish disease events, and public health threats have also highlighted th e presence of small, heterotrophic, lightly-armored dinoflagellates with different life cycle strate gies to those of the more t ypical planktonic photosynthetic blooming forms. Although massive fish kills (mostly menhaden) were prevalent in North Carolina's estuaries for many years, it was not until 1991 that Pfiesteria pi scicida was implicated. P. piscicida continues to threaten natural re sources and public health along the eastern USA (Burkholder et al. 1992; Burkhol der and Glasgow 1997). Other Pf iesteria species are also suspected as being ichthyot oxic (Landsberg et al. 1995, Bu rkholder and Glasgow 1997) and several other new heterotrophic dinoflagellate species that have recently been described (Steidinger et al. 1996, Stei dinger et al. in review) are being i nvestigated for thei r potential role

in fish kill and disease events. Filter-feeding shellfish accumulate microalgal toxins which in turn become available to consumers, both animal and human, through th e food chain. Several toxic dinoflagellates (Alexandrium, Gymnodinium, Pyrodinium , Dinophysis, Prorocentrum), diatoms (Pseudonitzschia) and cyanobacteria (Anabaena) are associated w ith human shellfish poisonings such as Amnesic Shellfish Poisoning, Diarrh eic Shellfish Poisoning, Paralytic Shellfish Poisoning, and Neurotoxic Shellfish Poisoning (Shumway 1989, Steidinger 1993), yet these same toxins can also impact animals through the food chain e.g. Pseudoni tzschia (domoic acid) for birds (Work et al. 1996), Alexandrium for fish, birds, and mammal s (Armstrong et al. 1978, White 1980, Geraci et al. 1989, Montoya et al . 1996), and Anabaena for mammals (Nehring 1993). Benthic Gambierdiscus, Prorocentr um, Ostreopsis, and Coolia are t oxic dinoflagellates that often inhabit reefs and hard grounds in subtropical and tropical regions (Anderson and Lobel 1987). They are associated with the human tropical fish poisoning, ciguatera (Ste idinger, 1993), but are not typically considered to aff ect other organisms involved in the food chain. It was recently postulated that tropical reef fish disease and mortalities in the USA were triggered by fish immunosuppression associated with the consumption of ciguatera-associated toxins (Landsberg 1995). The species of fish implicated in the ci guatera food chain in Fl orida (de Sylva 1994) are similar to those species that were affected during the 1980 and 1993/94 reef mortalities and disease outbreaks in Florida (Landsberg 1995). The majority of HAB events are associated with i nvertebrate, fish, and bird mortalities, yet there have also been numerous accounts of other unexpla ined marine animal mo rtalities, such as dolphins and sea turtles, where biotoxins have be en implicated (Geraci et al. 1989, Hokama et al. 1990, Hernández et al. 1998, FDEP unpublished data). The definitive role of biotoxins in marine

mammal mortalities has been c ontroversial. For example, although Gymnodinium breve was implicated in mortalities of th e endangered Florida manatee, Tric hechus manatus latirostris, in 1963 and 1982 (O'Shea et al. 1991), it was only prove n in 1996 when 149 animals died from G. breve exposure in southwest Florida (Bossart et al. 1998, Landsberg and Steidinger 1998). Terrestrial organisms (e.g. bears, raccoons, otters, birds) associated with marine or estuarine food webs may also be at risk from toxin exposure. It is already known th at terrestrial domestic

animals such as cattle are at risk from toxi c cyanobacterial blooms in freshwater systems (Falconer 1993). For obvious reasons, algal species kn own to be associated with human health risks have received the most attention. Many of th e potential longer-term chronic e ffects associated with these biotoxins are typically not well kno wn, nor is it clear what is the fate of these toxins in the ecosystem. There are, however, many algal spec ies which have had severe impacts on lower vertebrates and invertebrate spec ies (many commercially important) that are also deserving of our attention. Further, even when the imp acts on non-human species are considered, it is frequently only the acute or lethal influences which receive recognition. Sublethal or chronic effects of algal species have long been overlooked in both human and non-human species. Onlyrecently has attention been drawn to the fact that microalgal toxins and their chronic effects need to be considered at all biological levels and as major threats to animal health, sustained fisheries, endangered species, and ecosystems (Landsbe rg 1995, 1996, Burkholder 1998) . Chronic dietary exposure of animals to biotoxins can exert lethal or sub-lethal eff ects at all trophic levels, leading to impaired feeding, avoidance behavior, physio logical dysfunction, impa ired immune function, reduced growth and reproduction, pathological effects, or mortality (Lesser and Shumway 1993, Luckenbach et al. 1993, Wickfors and Smolow itz 1993, Burkholder 1998). Potential long-term effects of biotoxins on the health of aquatic anim als may be expressed in terms of susceptibility to disease, immunosuppression, pathologies, and in the development of neoplasia. Cyanobacteria produce several toxins that are known to be tumor promoters (Falconer and Humpage 1996) and have been implicated in dise ase in freshwater/brackish animals (Phillips et al. 1985, Andersen et al. 1993). Rarely are the potentia l effects of marine bi otoxins considered as etiological agents of tumor i nduction. This is surprising gi ven their defined widespread geographical distribution and the resultant probability that many marine and estuarine animals are chronically exposed to tumor-promoting biotoxi ns. Recently, the potentia l role of microalgal toxins in tumor development in marine an imals has been explored (Landsberg 1995, 1996, Landsberg et al. in review). Landsberg ( 1995) recently suggested that there is strong

circumstantial evidence for a correlation between the worldwide distribution of biotoxins in molluscs associated with shellfish poisonings in humans and the distribution of tumors in bivalves. In some cases, disseminated neoplasia and germinomas were highly associated with biotoxin components on both a temporal and spatia l basis. No experiment al assays or field monitoring studies to investigat e or corroborate these relationships have yet been done. In another example, fibropapillomatos is (FP) in green turtles is a debilitating, ne oplastic disease that has reached worldwide epizootic levels. Th e etiology of FP is unknown but has been linked to oncogenic viruses (Herbst 1994). Toxic benthi c dinoflagellates (Prorocentrum spp.) are not typically considered tumorigeni c agents, yet they have a worl dwide distribution and produce a tumor promoter, okadaic acid (OA) (Fujiki and Suganuma 1993). Prorocentrum spp. are epiphytic on macroalgae and seagrasses that are normal components of green turtle diets. Landsberg et al. (this conference) recently considered that in the Hawaiian Islands, green turtles consume Prorocentrum, and that high-risk FP areas are linked to areas where P. lima and P. concavum are both highly prevalent and abunda nt. The presence of OA in the tissues of Hawaiian green turtles indicates ex posure and a potential role fo r this tumor promoter in the etiology of FP (Landsberg, in press, Landsberg et al. this conference).

The overall effects of HABs on food webs are probably the leas t understood of all impacts. Not only are pathways of transmission of algal toxi ns complex and not completely known, long-term impacts of sublethal, chronic effects (e.g. recruitment failure and subsequent loss of species within an ecosystem, reduced filtration of wa ter masses and subsequent impacts on benthicpelagic coupling) are virtually unknown. Long-term impacts (e.g. toxin accumulation) on higherlevel consumers also need to be investigated. Wh ile there are many examples of these sublethal, chronic effects, perhaps one of the most revealing in terms of the breadth of impact is the community response to the apparently nontoxic br own tide algae, Aureococcus anophagefferens and Aureoumbra lagunensis (Cosper et al. 1987, Bu skey and Stockwell 1993). These algae cause reduced feeding activity in filter-feeding shel lfish through ciliary inhibition, depressed egg hatching success in red and black drum, and decl ines in zooplankton abundance, shellfish and other benthic filter feeders (Tracey 1988, Draper et al. 1990). Thes e species are also responsible for decimation of sea grass beds (critical habitat for a multitude of species) as a result of severe shading (Dennison et al. 1989). Fi nally, A. anophagefferens is responsible for the demise of the bay scallop fishery on Long Island, New York, USA, due to induced starvation and subsequent recruitment failure (Tettlebach and Wenczel 1993) . Similar impacts have been associated with persistent cyanobacterial blooms in Florida Bay, Florida, USA and their association with sponge

mortalities and reduction in recr uitment of spiny lobsters (Butle r et al. 1995). These sublethal, chronic impacts taken in concert have alrea dy had far-reaching impacts on the communities, andthe continued presence of these algal species is bound to have even more profound effects over the ensuing years. Although most attention has been focused on the di rect effects of toxic algae, there are other indirect effects caused by species that may be harmful to marine animals. For example, blooms of nontoxic diatoms such as Chaetoceros, Skelet onema, Rhizosolenia, or dictyophytes (Parry et al. 1989, Erard-Le Denn and Ryckaert 1990, Albright et al. 1993, Kent et al. 1995, Tester and Mahoney 1995), that have setae, proc esses, or spines can become trapped in the gills of fish or shellfish, cause mechanical damage, impair respiration, and may lead to mortality. Cyanobacterial blooms of Trichodesmium erythraeu m that are not usually considered harmful have been implicated for their effects on zoopl ankton (Guo and Tester 19 94), association with ciguatera-like outbreaks in Australia (Hahn and Capra 1992), mortalities of coral polyps (Endean 1977), and a potential role in coral bleaching (Coles 1994). In the last 5 years several important devel opments have occurred in the field of HABs: 1) recognition that genera of sm all, previously undescribed micr oalgae are involved in animal mortalities, disease a nd public health events, 2) technological breakthroughs in verifying and id entifying the presence of toxins in animals,

and 3) public awareness and political recogn ition that HABs are a universal problem. In the next few years we anticipate that there will be: 1) technologies that will improve the diagnosis of toxins in anim al tissues, e.g., probes, and that will track blooms and provide better predictive capabilities for the management of wildlife, fisheries, and aquaculture, 2) better integration and inte rdisciplinary activity between sc ientists and resource managers across fields to investigate animal mortalities and disease, 3) better integrated management strategi es that will look toward "managing HABs", 4) the recognition that chronic e ffects of biotoxins are likely to be very significant in animal health and may help to explain many curren tly "unidentified dis eases" or "unexplained mortalities", and 5) recognition that the interaction of biotoxins and pathogens needs to be evaluated. For example, mortalities may be attributed to the presence of a virus without necessarily determining if viral expression was enhanced by chr onic biotoxin exposure. These as pects may be particularly revealing e.g. in the cases of morbillivirus and potential biot oxin exposure in marine mammals and with oncogenic viruses and tumor promoter s in the expression of fibropapillomas in sea turtles. In addition, the potential role of HABs as vectors for aqua tic animal pathogens is also an emerging issue.

References Adnan, Q. 1989. Red tides due to Noctiluca scintillans (MacCartney) Ehrenb. and mass mortality of fish in Jakarta Bay. pp. 53-55. In: Red Tides, Biology, Environmental Sc ience and Toxicology, eds. T. Okaichi, D.M. Anderson and T. Nemoto, Elsevier Press, New York.

Albright, L.J., Yang, C.Z. and Johnson, S. 1993. S ub-lethal concentrations of the harmful diatoms, Chaetocerus concavicornis and C. convolutus , increase mortality rates of penned Pacific salmon. Aquaculture. 117:215-225.

Andersen, R.J., Luu, H.A., Chen, D.Z., Holmes, C.F. B., Kent, M.L., Le Blanc, M., Taylor, F.J.R. and Williams, D.E. 1993. Chemical and biological ev idence links microcystins to salmon 'netpen

liver disease'. Toxicon 31:1315-1323.

Anderson, D. M. and Lobel, P. S. 1987. The conti nuing enigma of ciguatera. Biol. Bull. 172: 89-

107Armstrong, I.H., Coulson, J.C., Hawkey, P. and Hudson, M.J. 1978. Further mass seabird deaths from paralytic shellfish poisoning. British Birds 71:58-68.

Burkholder, J. M. 1998. Implications of harmfu l microalgae and heterotr ophic dinoflagellates in management of sustainable marine fi sheries. Ecol. Applic. 8:S37-S62

Burkholder, J.M. and Glasgow, H.B. Jr. 1997. Pfiesteria piscicida and other Pfiesteria -like dinoflagellates: Behavior, impacts and environmental controls. Limnol. Oceanogr. 42:1052-1075.

Burkholder, J.M., Noga, E.J., Hobbs, C.H., Glasgow, H.B. Jr. and Smith, S.A. 1992. New "phantom" dinoflagellate is the causative agent of major estuarine fish kills. Nature 358:407-410.

Buskey, E.J. and Stockwell, D.A. 1993. Effects of a persistent 'brown tide' on zooplankton populations in the Lagune Madre of South Te xas. pp. 659-666. In: Toxic Phytoplankton Blooms in the Sea, eds. T. J. Smayda and Y. Shimuzu, Elsevier Press, Amsterdam.

Butler, M. J. IV., Hunt, J. H., Herrnkind, W. F ., Childress, M. J., Bertelsen, R., Sharp, W., Matthews, T., Field, J. M. and Marshall, H. G. 1995. Cascading disturbances in Florida Bay, USA: cyanobacteria blooms, sponge mortality, and implications for juvenile spiny lobsters Panulirus argus . Mar. Ecol. Prog. Ser. 129:119-125.

Chang, F.H., Anderson, C. and Bous tead, N.C. 1990. First record of Heterosigma (Raphidophyceae) bloom with associated morta lity of cage-reared salmon in Big Glory Bay,

New Zealand. N.Z.J.Mar. Fresh. Res. 24: 461-469.

Coles, S. L. 1994. Extensive coral disease outbrea k at Fahl Island, Gulf of Oman, Indian Ocean.

Coral Reefs 13:242.

Connell, C.H. and Cross, J.B. 1950. Mass mortality of fish associated with the protozoan Gonyaulax in the Gulf of Mexico. Science 112:359-363.

Cosper, E.M., Dennison, W.C., Carpenter, E.J., Br icelj, V.M., Mitchell, J.G., Kuenstner, S.H., Colflesh, D. and Dewey, M. 1987. Recurrent and pe rsistent brown tide bl ooms perturb coastal marine ecosystem. Estuaries. 10: 284-290.

Cross, T.F. and Southgate, T. 1980. Mortalities of fa una of rocky substrates in south-west Ireland

associated with the occurrence of Gyrodinium aureolum blooms during autumn 1979. J. Mar.

biol. Ass. UK. 60:1071-1073.

Dennison, W.C., Marshall, G.J. and Wigand, C. 1989. Effect of "brown tide" shading on eelgrass ( Zostera marina L.) distributions. pp. 675-692. In: Nove l Phytoplankton Blooms eds. E. M. Cosper, V.M. Bricelj and E. J. Carpenter, Springer Verlag, Berlin.

Draper, C., Gainey, L., Shumway, S. and Shapiro, L. 1990. Effects of Aureococcus anophagefferens ("brown tide") on the lateral cilia of 5 species of bivalve molluscs. pp. 128-131. In: Toxic Marine Phytoplankton, eds. E. Graneli, B. Sundstrom, L. Edler and D. M. Anderson, Elsevier Publishers, New York.

Endean, R. 1977. Destruction and recovery of coral reef communities. pp. 215-254. In:Biology and Geology of Coral Reefs, eds. O. A. Jones and R. Endean, Academic Press, New York.

Erard-Le Denn, E. and Ryckaert, M. 1990. Trout mortality associated with Distephanusspeculum . p. 137. In: Toxic Marine Phytoplankton, eds. E. Graneli, B. Sundstrom, L. Edler and D.M. Anderson, Elsevier Press, New York.

Falconer, I.R. 1993. Mechanism of t oxicity of cyclic peptide toxi ns from blue-green algae. pp. 177-186. In: Algal Toxins in Seafood and Drinking Wa ter. ed. I. R. Falconer, Academic Press,

London.

Falconer, I.R. and Humpage, A.R. 1996. Tumor pr omotion by cyanobacterial toxins. Phycologia.

35:74-79

Fujiki, H. and Suganuma, M. 1993. Tumor promo tion by inhibitors of protein phosphatases 1

and 2A:the okadaic acid class of compounds. Adv.Cancer Res. 61:143-194.

Forrester, D.J., Gaskin, J.M., White, F.H., Thompson, N.P., Quick, J.A. Jr, Henderson, G. and Woodard, J.C. 1977. An epizootic of waterfowl asso ciated with a red tide episode in Florida.

J.Wildl. Disin. 13:160-167.

Geraci, J.R., Anderson, D.M., Timperi, R.J., Sta ubin, D.J. Early, G.A., Prescott, J.H. and Mayo, C.A. 1989. Humpback whales ( Megaptera novaeangliae ) fatally poisoned by di noflagellate toxin. Can. J. Fish. Aquat. Sci.46:1895-1898.

Gunter, G., Williams, R.H., Davis, C.C. and Sm ith, F.G.W. 1948. Catastr ophic mass mortality of

marine animals and coincident phytoplankton bloom on the west coast of Florida, November 1946 to August 1947. Ecol. Monogr. 18:309-324.

Guo, C. and Tester, P. A. 1994. T oxic effect of the bloom-forming Trichodesmium sp. (Cyanophyta) to the copepod Acartia tonsa . Nat. Toxins 2: 222-227

Guzman, H.M., Cortes, J., Glynn, P.W. and Ri chmond, R.H. 1990. Coral mortality associated with dinoflagellate blooms in the eastern Pacific (Costa Rica and Panama). Mar. Ecol. rog. Ser.

60:299-303.

Hallegraeff, G. M. 1993. A review of harmful al gal blooms and their apparent global increase. Phycologia 32:79-99.

Hahn, S.T. and Capra, M. F. 1992. The cyanobacterium Oscillatoria erythraea - a potential source of toxin in the ciguatera food chain. Food Addit. Contam. 9:351-355.

Heidal, K. and Mohus, A. 1995. The toxic Chrysochromulina - salmon disaster of 1991 in northern Norway with some follow-up mon itoring records of 1992 and -93. pp. 163-168. In: Harmful Marine Algal Blooms, eds. P. Lassus, G. Arzul, E. Erard-Le-Denn, P. Gentien and C. Marcaillou-Le-Baut, Technique et Documentation, Lavoisier, Paris.

Herbst, L. H. 1994. Fibropapillomatosis of marine turtles. Ann. Rev. Fish Dis. 4:389-425.

Hernández, M., Robinson, I., Aguilar, A., Gon zález, L.M., López-Jurado, L.F., Reyero, M.I., Cacho, E., Franco, J., Lopez-Rodas, V. and Co stas, E. 1998. Did algal toxins cause monk seal mortality? Nature 393:28-29.

Hokama, Y., Asahina, A.Y., Hong, T.W.P., Katsura, K., Shang, E., Miyahara, J.T., Sweeney, J.C., Stone, R. 1990. Causative toxin(s) in the deat h of two Atlantic dolphins. J. Clin. Lab. Anal.

4:474-478.Horiguchi, T. 1995. Heterocapsa circularisquama sp. nov. (Peridiniales, Dinophyceae): a new marine dinoflagellate causing mass mortality of bivalves in Japan. Phycol. Res. 43:129-136.

Kaartvedt, S., Johnsen, T.M., Aksnes, D.L., Lie, U. & Svendesen, H. 1991. Occurrence of the toxic phytoflagellate Prymnesium parvum and associated fish mort ality in a Norwegian fjord system. Can. J. Fish. Aquat. Sci. 48:2316-2323.

Kent, M.L., Whyte, J.N.C. and LaTrace, C. 1995. Gill lesions and mortality in seawater penreared Atlantic salmon Salmo salar associated with a dense bloom of Skeletonema costatum and

Thalassosira species. Dis. Aquat. Org.22:77-81.

Landsberg, J. H. and Steidinger, K. A. 1998. A historical review of Gymnodium breve red tides implicated in mass mortalities of the manatee ( Trichechus manatus latirostris ) in Florida, USA, pp. 97-100, Harmful Algae, eds. Reguera, B. et al. Xunta de galicia and Intergovernmental Oceanographic Commission of UNESCO.

Landsberg, J. H. 1995. Tropical reef-fish diseas e outbreaks and mass mortalities in Florida, USA: what is the role of dietary biol ogical toxins? Dis. aquat. org. 22:83-100.

Landsberg, J. H. 1996. Neoplasia an d biotoxins in bivalves: is th ere a connection? J. Shellfish

Res. 15:205-233.

Landsberg, J. H. (in review). The potential role of biotoxins in sea turtle fibropapillomas. Proceedings of the Second Sea Turtle Fi bropapilloma Workshop, Hawaii, December 1997.

NOAA Technical Memorandum.

Landsberg, J. H., Balazs, G. H., Steidinger, K. A ., Baden, D.G., Work, T. M ., Russell, D. G. (this conference). Preliminary evidence links sea tu rtle fibropapillomatos is to tumor-promoting microalgae.

Landsberg, J.H., Steidinger, K.A. and Blakesle y, B.A. 1995. Fish-killing dinoflagellates in a tropical marine aquarium. pp. 65-70. In: Harmful Marine Algal Blooms, eds. P. Lassus, G. Arzul, E. Erard-Le-Denn, P. Gentie and C. Marcaillou- Le-Baut, Technique et Documentation, Lavoisier,

Paris.

Lesser, M. P. and Shumway, S.E. 1993. Effects of toxic dinoflagellates on clearance rates and survival in juvenile bivalve molluscs. J.Shellfish Res. 12: 377-381.

Luckenbach, M. W., K. G. Sellner, S. E. Sh umway and K. Greene. 1993. Effects of two bloomforming dinoflagellates, Prorocentrum minimum and Gyrodinium uncatenatum , on the growth and survival of the eastern oyster (Gmelin, 1791). J. Shellfish Res. 12:411-415.

Mahoney, J.B. and Steimle, F.W. Jr. 1979. A mass mort ality of marine animals associated with a

bloom of Ceratium tripos in the New York Bight. pp. 225-230 In: Toxic Dinoflagellate Blooms, eds. D.L.Taylor and H.H. Seliger, Elsevier, New York.

Mortensen, A.M. 1985. Massive fish mortalities in the Faroe Islands caused by a Gonyaulax excavate red tide. pp. 165-170. In: Toxic dinoflagella tes, eds. D. M. Anderson, A. White and D. G. Baden, Elsevier, New York.

Montoya, N.G., Akselman, R., Franco, J. and Carr eto, J.I. 1996. Paralytic shellfish toxins andmackerel ( Scomber japonicus ) mortality in the Argentine Sea. pp. 417-420. In: Harmful and Toxic Algal Blooms, eds. T. Yasumoto, Y. Oshima and Y. Fukuyo, IOC/UNESCO, Paris.

Negri, A.P., Jones, G.J. and Hindmarsh, M. 1995. Sheep mortality associated with paralytic shellfish poisoning toxins from the cyanobacterium Anabaena circinalis . Toxicon 33:1321-1329.

Nehring, S. 1993. Mortality of dogs associated with mass development of Nodularia spumigena (Cyanophyceae) in a brackish lake at the German North Sea coast. J.Plankton Res. 15: 867-872.

Okaichi, T. 1985. Fish kills due to the red tides of Chattonella . Bull. Mar. Sci. 37: 772

Parry, G.D., Langdon, J.S. and Huisman, J.M. 1989. Toxic effects of a bloom of the diatom
Rhizosolenia chunii on shellfish in Port Phillip Bay, Sout heastern Australia. Mar.Biol. 102:25-41.

Phillips, M.J., Roberts, R.J., Stewart, J.A. and Codd, G.A. 1985. The toxicity of the cyanobacterium Microcystis aeruginosa to rainbow trout, Salmo gairdneri Richardson. J. Fish

Dis. 8: 339-344

Robertson, A. 1991. Effects of a toxic bloom of Chrysochromulina polylepis on the common dog-whelk, Nucella lapillus , on the Swedish west coast. J. Mar. biol. Ass. UK. 71:569-578.

Shumway, S. E. 1990. A review of the effects of algal blooms on shellfish and aquaculture. J. World Aquacult. Soc. 21:65-104.

Shumway, S. E. and A. D. Cembella. 1993. The im pact of toxic algae on scallop culture and

fisheries. Rev. Fish. Sci. 1:121-150.

Sournia, A. 1995. Red tide and toxic marine phytopl ankton of the world ocean: an inquiry into biodiversity. pp. 103- 112. In: Harmful Marine Algal Bl ooms, eds. P. Lassus, G. Arzul, E. ErardLe-Denn, P. Gentien and C. Marcaillou-Le-Baut, Technique et Documentation, Lavoisier, Paris.

Steidinger, K. A. 1993. Some taxono mic and biological aspects of toxic dinoflagellates. pp. 1-28. In:Algal Toxins in Seafood and Drinking Water, ed. I.R. Falconer, Academic Press, London.

Steidinger, K.A., Burklew, M. and Ingle, R.M. 1973. The effects of Gymnodinium breve toxin on estuarine animals. pp. 179-202. In: Marine Phar macognosy:Action of Marine Toxins at the cellular level. Academic Press, New York.

Steidinger, K.A., Landsberg, J. H., Truby, E.W. and Blakesley, B.A. 1996. The use of scanning electron microscopy in identifying small "gymn odinioid" dinoflagellates. Nova Hedwigia.

112:415-422.

Steidinger, K.A., Landsberg, J.H., Truby, E.W. and Roberts, B.S. 1998. First report of Gymnodinium pulchellum Larsen 1994 (Dinophyceae) in North Amer ica and associated fish kills in the Indian River, Florida. J. Phycol. 34:431-437.

Su, H.M., Liao, I.C. and Chiang, Y.M. 1993. Mass mortality of prawn caused by Alexandrium

tamarense blooming in a culture pond in southern Taiwan. pp. 329-334. In: Toxic Phytoplankton Blooms in the Sea, eds. T. J. Smayda a nd Y. Shimuzu, Elsevier Press, Amsterdam.

Tester, P.A. and Mahoney, B. 1995. Implication of the diatom, Chaetocerus convolutus , in the death of red king crab, Paralithodes camtschatica , Captains Bay, Unalaska Island, Alaska. pp.95-100. In: Harmful Marine Algal Blooms, eds. P. Lassus, G. Arzul, E. Erard-Le-Denn, P. Gentien and C. Marcaillou-Le-Baut, Techni que et Documentation, Lavoisier, Paris.

Tettelbach, S.T. and Wenczel, P. 1993. Reseedi ng efforts and the status of bay scallop Argopecten irradians (Lamarck, 1819) populations in New York following the occurrence of "brown tide" algal blooms. J. Shellfish Res. 12:423-431.

Tracey, G.A. 1988. Feeding reduction, repr oductive failure, and mortality in Mytilus edulis during the 1985 'brown tide' in Naragansett Bay, Rhode Island. Mar. Ecol. Prog. Ser. 50:73-81.

White, A.W. 1980. Recurrence of kills of Atlantic herring ( Clupea harengus harengus ) caused by dinoflagellate toxins transfe rred through herbivorous zooplankton. Can. J. Fish. Aquat. Sci.

37: 2262-2265.

Wickfors, G.H. and Smolowitz, R.M. 1993. Detrimental effects of a Prorocentrum isolate upon hard clams and bay scallops in laboratory feeding studies. pp. 447-452. In: Toxic Phytoplankton Blooms in the Sea, eds. T. J. Smayda and Y. Shimuzu, Elsevier Publishers, Amsterdam.

Work, T. M., Beale, A. M., Fritz, L., Quilliam, M. A., Silver, M., Buck, K., Wright, J. L. C. 1993.

Domoic acid intoxication of br own pelicans and cormorants in Santa Cruz, California. pp. 643- 649. In: Toxic Phytoplankton in the Sea, eds. T. J. Smayda and Y. Shimuzu, Elsevier Publishers,

Amsterdam.

Yongjia, Z., Munday, B.L. and Handlinger, J. 1995. Mass mortality of flat oysters ( Ostrea

rivularis ) associated with a bloom of Prorocentrum sp. in the port of Zhanjiang, South China.

Bull. Eur. Ass. Fish Pathol. 15:61-63.

Yuki, K. and Yoshimatsu, S. 1989. Two fish-killing species of Cochlodinium from Harima Nada, Seto Inland Sea, Japan. pp. 451-454. In: Red Tides, Biology, Environmental Science and Toxicology, eds. T.Okaichi, D.M. Anderson a nd T. Nemoto, Elsevier Press, New York.