Harmful Algal Blooms and Their Effects on Marine and Estuarine Animals

Jan H. Landsberg (1) and Sandra S. Shumway (2) 

1 Florida Department of Environmental Protection, Florida Marine Research Institute, 100 

Eighth Avenue Southeast, St. Petersburg, Florida 33712 USA, landsberg_j@epic7.dep.state.fl.us 

2 Natural Science Division, Southampton College, Long Island University Southampton, New 

York 11968 USA, sshumway@sunburn.liunet.edu

Abstract 

Increasing documentation of harmful algal blooms (HABs) in marine and estuarine systems has 

begun to demonstrate their far reaching impacts on ecosystem integrity, species interactions, 

aquatic animal health and population growth, human health, economy, industry, and ecology. 

While some 5000 species of microalgae 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 microalgae and the 

detection of toxic species or to species previously described that were not known to be toxic. 

While this increase partially reflects technological improvement in accurate identification of 

HAB species and their toxins, and enhanced monitoring and surveillance, it is also associated 

with continued anthropogenic influences and interacting natural processes. Because some HABs 

tend to be planktonic, visibly obvious, acute in nature, and lead to fast-acting shellfish poisoning 

events or mass mortalities of aquatic organisms, these are the HABs about which most is known. 

Marine and estuarine HABs cause animal mortalities, shellfish and tropical fish poisonings, and 

respiratory irritation and neurocognitive disease in humans (Steidinger 1993, Burkholder and 

Glasgow 1997). At least 85 species of toxic or harmful marine microalgae are known worldwide; 

all potentially have varying impacts on natural resources and public (Sournia 1995, Steidinger 

pers. comm.). Aquatic animals are typically exposed to toxic or harmful algae when planktonic 

or benthic species bloom and dominate the food web, but there are also more subtle and insidious 

exposure mechanisms that are not so obvious. Exposure to toxins occurs through ingestion of 

cells (filter feeders e.g. sponges, molluscs, crustacea), bioaccumulation by consumption of toxic 

prey (e.g. crustacea, gastropods, fish, birds, turtles, mammals), aerosolized transport (e.g. 

respiratory irritation in humans and potentially in mammals, turtles, birds), water-borne toxin 

after cell lysis (fish, shellfish), sediment sinks (benthic organisms), and possibly through 

consumption of toxic benthic stages. 

Fish or invertebrate kills have been attributed to low dissolved oxygen associated with non toxic, 

high biomass, plankton blooms such as Ceratium or Noctiluca (Mahoney and Steimle 1979, 

Adnan 1989). Most blooms of toxic photosynthetic microalgae (Heterocapsa, Gymnodinium,

Gyrodinium, Alexandrium, Cochlodinium, Prorocentrum, Chattonella, Heterosigma, 

Prymnesium, Chrysochromulina, and Nodularia) cause mortalities of marine, estuarine, or 

associated terrestrial animals, both in the wild and in aquaculture (Gunter et al. 1948, Steidinger 

et al. 1973, Cross and Southgate 1978, Mortensen 1985, Okaichi 1985,Yuki and Yoshimatsu 

1989, Chang et al. 1990; Guzman et al. 1990, Shumway 1990, Kaartvedt et al. 1991, Robertson 
1991, 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, ulcerated fish disease events, and public health 

threats have also highlighted the presence of small, heterotrophic, lightly-armored dinoflagellates 

with different life cycle strategies to those of the more typical 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 piscicida was implicated. 

P. piscicida continues to threaten natural resources and public health along the eastern USA 

(Burkholder et al. 1992; Burkholder and Glasgow 1997). Other Pfiesteria species are also 

suspected as being ichthyotoxic (Landsberg et al. 1995, Burkholder and Glasgow 1997) and 

several other new heterotrophic dinoflagellate species that have recently been described 

(Steidinger et al. 1996, Steidinger et al. in review) are being investigated for their 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 the food chain. Several toxic dinoflagellates 

(Alexandrium, Gymnodinium, Pyrodinium, Dinophysis, Prorocentrum), diatoms 

(Pseudonitzschia) and cyanobacteria (Anabaena) are associated with human shellfish poisonings 

such as Amnesic Shellfish Poisoning, Diarrheic 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. Pseudonitzschia (domoic acid) 

for birds (Work et al. 1996), Alexandrium for fish, birds, and mammals (Armstrong et al. 1978, 

White 1980, Geraci et al. 1989, Montoya et al. 1996), and Anabaena for mammals (Nehring 

1993). 

Benthic Gambierdiscus, Prorocentrum, Ostreopsis, and Coolia are toxic 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 (Steidinger, 1993), but are 

not typically considered to affect 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 ciguatera food chain in Florida (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 invertebrate, fish, and bird mortalities, yet there 

have also been numerous accounts of other unexplained marine animal mortalities, such as 

dolphins and sea turtles, where biotoxins have been 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 controversial. For example, although Gymnodinium breve was 

implicated in mortalities of the endangered Florida manatee, Trichechus manatus latirostris, in 

1963 and 1982 (O'Shea et al. 1991), it was only proven 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 that terrestrial domestic 

animals such as cattle are at risk from toxic cyanobacterial blooms in freshwater systems 

(Falconer 1993). 

For obvious reasons, algal species known to be associated with human health risks have received 

the most attention. Many of the potential longer-term chronic effects associated with these 

biotoxins are typically not well known, nor is it clear what is the fate of these toxins in the 

ecosystem. There are, however, many algal species which have had severe impacts on lower 

vertebrates and invertebrate species (many commercially important) that are also deserving of 

our attention. Further, even when the impacts 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. Only 
recently 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 (Landsberg 1995, 1996, Burkholder 1998). Chronic dietary 

exposure of animals to biotoxins can exert lethal or sub-lethal effects at all trophic levels, leading 

to impaired feeding, avoidance behavior, physiological dysfunction, impaired immune function, 

reduced growth and reproduction, pathological effects, or mortality (Lesser and Shumway 1993, 

Luckenbach et al. 1993, Wickfors and Smolowitz 1993, Burkholder 1998). Potential long-term 

effects of biotoxins on the health of aquatic animals 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 disease in freshwater/brackish animals (Phillips et 

al. 1985, Andersen et al. 1993). Rarely are the potential effects of marine biotoxins considered as 

etiological agents of tumor induction. This is surprising given their defined widespread 

geographical distribution and the resultant probability that many marine and estuarine animals 

are chronically exposed to tumor-promoting biotoxins. Recently, the potential role of microalgal 

toxins in tumor development in marine animals 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 spatial basis. No experimental assays or field 

monitoring studies to investigate or corroborate these relationships have yet been done. In 

another example, fibropapillomatosis (FP) in green turtles is a debilitating, neoplastic disease 

that has reached worldwide epizootic levels. The etiology of FP is unknown but has been linked 

to oncogenic viruses (Herbst 1994). Toxic benthic dinoflagellates (Prorocentrum spp.) are not 

typically considered tumorigenic agents, yet they have a worldwide 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 abundant. The presence of OA in the tissues of 

Hawaiian green turtles indicates exposure and a potential role for 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 least understood of all impacts. Not 

only are pathways of transmission of algal toxins 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 water 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. While 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 brown tide algae, Aureococcus anophagefferens 

and Aureoumbra lagunensis (Cosper et al. 1987, Buskey and Stockwell 1993). These algae cause 

reduced feeding activity in filter-feeding shellfish through ciliary inhibition, depressed egg 

hatching success in red and black drum, and declines in zooplankton abundance, shellfish and 

other benthic filter feeders (Tracey 1988, Draper et al. 1990). These 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). Finally, 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 recruitment of spiny lobsters (Butler et al. 1995). These sublethal, 

chronic impacts taken in concert have already had far-reaching impacts on the communities, and 
the 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 direct 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, Skeletonema, 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, processes, 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 erythraeum that are not usually considered harmful 

have been implicated for their effects on zooplankton (Guo and Tester 1994), 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 developments have occurred in the field of HABs: 

1) recognition that genera of small, previously undescribed microalgae are involved in animal 

mortalities, disease and public health events, 

2) technological breakthroughs in verifying and identifying the presence of toxins in animals, 

and 

3) public awareness and political recognition 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 animal 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 interdisciplinary activity between scientists and resource managers 

across fields to investigate animal mortalities and disease, 

3) better integrated management strategies that will look toward "managing HABs", 

4) the recognition that chronic effects of biotoxins are likely to be very significant in animal 

health and may help to explain many currently "unidentified diseases" 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 chronic biotoxin exposure. These aspects may be particularly 

revealing e.g. in the cases of morbillivirus and potential biotoxin exposure in marine mammals 

and with oncogenic viruses and tumor promoters in the expression of fibropapillomas in sea 

turtles. In addition, the potential role of HABs as vectors for aquatic animal pathogens is also an 

emerging issue. 

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