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HARMFUL ALGAL BLOOMS IN THE BENGUELA UPWELLING SYSTEM

The Benguela system is characterised by upwelling circulation along the entire west coast of southern Africa. Here Harmful Algal Blooms [HABs] are common and although attributed to a number of marine planktonic algae, harmful impacts are most often ascribed to one or another dinoflagellate species and are associated with either their high biomass or the toxigenicity of some species. These blooms are able to impact both commercial and recreational interests in the coastal region causing fish kills, contaminating seafood with toxins resulting in serious public health problems, or altering ecosystems in ways that are perceived by humans as harmful.

Discolouration of an inner basin of Cape Town Harbour in November 2003 was caused by a bloom of the toxic dinoflagellate Alexandrium minutum. This species is known to produce paralytic shellfish poisoning toxins and the bloom persisted in the harbour for several weeks. This was the first record of this species on the South African coast [Photographs – © D .Calder].

Harmful impacts attributed to high biomass dinoflagellate blooms which ultimately lead to low oxygen events and in some cases the production of hydrogen sulphide, have for many years lead to spectacular mortalities of marine life in the Benguela. Referred to as red tides, Gilchrist [1914] listed these blooms as one of the factors causing fluctuations in fish stocks in the Benguela. Monitoring has indicated that the distribution of these blooms is typically associated with the upwelling system, with few red tides reported east of Cape Agulhas [Pitcher and Calder, 2000]. 

Bright green discolouration of the waters of Saldanha Bay in January 2003 was of concern to port authorities. Investigations determined that the bloom was dominated by an unknown species of Tetraselmis. Although these blooms show no signs of toxicity and pose no serious threat they are often considered aesthetically unpleasant and are in many cases perceived to be associated with eutrophied or polluted waters. For this reason blooms such as these have significant negative effects on the recreational uses of coastal areas.

Anoxia in continental shelf waters may be ascribed to the advection of oxygen-deficient water from a remote source and from in situ formation. In the southern Benguela, in situ formation resulting from the degradation of organic-rich material derived from phytoplankton blooms is generally thought to be the controlling factor. The inshore decay of red tides after the exhaustion of nutrients has in many instances been responsible for marine mortalities as a consequence of oxygen depletion.

In March 1994 large marine mortalities were experienced in St Helena Bay on the South African west coast as a consequence of hydrogen sulphide poisoning. This followed the decay of a red tide dominated by the dinoflagellates Ceratium furca and Prorocentrum micans. Oxygen concentrations were maintained at less than 0.5 ml.l-1 in the bottom waters of the Bay and hydrogen sulphide, generated by anaerobic bacteria in the absence of dissolved oxygen, was recorded in excess of 50 μmol.l-1. Although common in the northern Benguela, this was the first recorded case of hydrogen sulphide poisoning in the southern Benguela.

Apart from those species responsible for high biomass blooms, the Benguela is characterized by a variety of toxic microalgae which may impact directly on marine life. The northern Benguela is for example characterised by the fish-killing dinoflagellate Karlodinium micrum, originally described as Gymnodinium galatheanum by Braarud [1957] from samples collected off Namibia by Steeman Neilson in 1950 during a fish kill. The distribution of this species does not however appear to extend into the southern Benguela. Another fish-killing dinoflagellate is the newly described species Karenia cristata [Botes et al., 2003]. Initially responsible for large abalone mortalities in the 1980s, this species appears to be restricted to the Western Agulhas Bank. This species shares several characteristics with Karenia brevis, common off the coast of Florida, and the recently described species from New Zealand waters, Karenia brevisulcata, in that it also produces an aerosol toxin responsible for respiratory and skin disorders. 

Approximately 30 tons of abalone were washed ashore in the Betty’s Bay region in 1989 following a bloom of the toxic dinoflagellate Karenia cristata. In addition to marine mortalities this species also produces an aerosol toxin causing skin and respiratory irritations to humans.

Although most marine mortalities in the Benguela have been associated with dinoflagellate blooms, phytoplankton belonging to other groups known to produce toxins are common in the Benguela. The raphidopyte Heterosigma akashiwo renowned for its ichthyotoxic properties has, for example, been observed to bloom in the northern and southern Benguela. Only recently have fish mortalities in the Benguela been associated with this species. 

The first fish mortality in the Benguela attributed to Heterosigma akashiwo was observed in Saldanha Bay in March 2004. High concentrations of this raphidophyte caused a yellow brown discolouration of the water, and although the mortalities were not particularly extensive large shoals of disorientated fish were observed in shallow water [Photographs – © J. de Goede].

One major category of public health impact from HABs occurs when toxic phytoplankton are filtered from the water by shellfish such as clams, mussels, oysters and scallops, which then accumulate the algal toxins to levels that are potentially lethal to humans and other consumers. Of particular concern in the Benguela are the shellfish poisoning syndromes known as Paralytic (PSP) and Diarrhetic (DSP) Shellfish Poisoning.

In the southern Benguela, blooms of Alexandrium catenella, responsible for PSP are common and have historically been the primary concern of public health officials. Although some of the earlier possible accounts of PSP in the Benguela date back to the 1880s, confirmed cases of PSP were only described in 1948 [Sapeika, 1948]. The full northern extent of Alexandrium catenella is not clearly defined, but it is known to extend into southern Namibia. A. catenella has not been recorded east of Cape Point, but another toxic Alexandrium species has recently been isolated from the Western Agulhas Bank [Ruiz Sebastian et al., in press]. This species does, however, not appear to form substantial blooms and the cell toxin quota is low; thus, it is unlikely to render shellfish toxic. The distribution of these species is confirmed by the incidence of PSP-contaminated shellfish, with no recordings of PSP east of Cape Point, while the highest incidence of contaminated shellfish is found on the southern Namaqua coast. Monitoring on the Namaqua coast has indicated that A. catenella appears almost every year, typically during the latter part of the upwelling season. A. catenella in the Benguela can be found at exceedingly high cell concentrations of many million cells l-1 and these blooms not only render shellfish toxic to consumers, but are also seemingly responsible for fish and shellfish mortalities [Pitcher and Calder, 2000].

Vegetative and cyst stages of Alexandrium catenella responsible for PSP in the Benguela region. Dormant cysts of A. catenella are able to settle to the seafloor and can survive there for several years. When favourable conditions return, cysts are able to germinate and reinoculate the water with vegetative cells that can again bloom. Recognising the role of cysts in bloom initiation, growth and termination is critical to our understanding of HAB phenomena [Joyce and Pitcher in press].

The other very common form of shellfish poisoning in the Benguela is DSP, usually attributable to Dinophysis acuminata or Dinophysis fortii. Dinophysis species often form relatively minor components of blooms dominated by other dinoflagellates, but can nevertheless attain high cell concentrations of the order of one million cells l-1 [Pitcher et al., in prep]. Despite considerable interannual variation in cell densities, time-series data have revealed the intermittent presence of Dinophysis spp. throughout the upwelling season, with concentrations peaking in the late summer and autumn [Pitcher and Calder, 2000], at which time their distribution is often widespread. For both D. acuminata and D. fortii, cell toxin quota data indicate that these species are only moderately toxic in the Benguela, with okadaic acid identified as the primary toxin. Time-series data from the Namaqua coast of okadaic acid concentrations in mussels reveals that toxin concentrations during summer and autumn frequently exceed the harvestable limit, indicating the severity of the problem posed by DSP in the Benguela [Pitcher et al., in prep].

Dinophysis acuminata and Dinophysis fortii are the dinoflagellate species most often responsible for DSP in the southern Benguela. DSP on the South African coast was identified for the first time in 1991 and attributed to D. acuminata. Monitoring has revealed that DSP is commonplace on both the West and South coasts and several other Dinophysis species known to cause DSP have been recognised as a component of the phytoplankton on the South African coast.

Other algal species reported to form red tides or to be toxic are listed by Pitcher and Calder [2000]. Common in the Benguela, but only of potential harm are various species of Pseudo-nitzschia, known to cause Amnesic Shellfish Poisoning [ASP] in other parts of the world. Pseudo-nitzschia australis, for example, has been identified as a very common bloom-forming species in the Benguela, but to date no trace of the toxin domoic acid has been found in cultures of this species and no form of shellfish poisoning has been associated with these blooms [Marangoni et al., 2001]. Similarly, Protoceratium reticulatum [formerly Gonyaulax grindleyi] is known to bloom in the southern Benguela [Horstman 1980], but no attempts have been made to establish the presence of the yessotoxins. Lingulodinium polyedrum [formerly Gonyaulax polyedra] has also been recorded within the region [Kruger, 1980] but no harmful effects have been attributed to this dinoflagellate.

REFERENCES

Botes, L., S.D. Sym and G.C. Pitcher. 2003. Karenia cristata sp. Nov. and Karenia bicuneiformis sp. Nov. (Gymnodiniales, Dinophyceae): two new Karenia species from the South African coast. Phycologia. 42: 563-571.

Braarud, T. 1957. A red tide organism from Walvis Bay (Gymnodinium galatheanum n. sp.). Galathea Deep Sea Exped. 1: 137-138.

Gilchrist, J.D.F. 1914. An enquiry into fluctuations in fish supply on the South African coast. Mar. Biol. Rep., Cape Town 2: 8-35.

Joyce, L.B. and G.C. Pitcher. In prep. The role of cyst germination in the initiation of Alexandrium catenella blooms on the west coast of South Africa: characteristics of cyst germination.

Kruger, I. 1980. A checklist of South West African marine phytoplankton, with some phytogeographical relations. Fish. Bull. S. Afr. 13: 31-53.

Horstman, D.A. 1980. Reported red-water outbreaks and their effects on fauna of the west and south coasts of South Africa, 1959-1980. Fish. Bull. S. Afr. 15: 71-88.

Marangoni, C., R.N. Pienaar, S.D. Sym and G.C. Pitcher. 2001. Pseudo-nitzschia australis Frenguelli from Lambert’s Bay South Africa. Microscopy Society of Southern Africa – Proceedings 31: 53.

Pitcher, G.C. and D. Calder. 2000. Harmful algal blooms of the southern Benguela current: a review and appraisal of monitoring from 1989 to 1997. S. Afr. J. mar. Sci. 22: 255-271. 

Pitcher, G.C., M.L. Fernandez and D. Calder. In prep. Observations of the bloom dynamics of okadaic acid producing Dinophysis species and the consequent contamination and depuration of shellfish in the southern Benguela upwelling system.

Sapeika, N. 1948. Mussel poisoning. S. Afr. med J. 22: 337-338.

Ruiz Sebastian, C., S.M. Etheridge, P.A. Cook, C. O’Ryan and G.C. Pitcher. In Press. Phylogenetic analysis of toxic Alexandrium (Dinophyceae) isolates from South Africa: Implications for the global phylogeography of Alexandrium tamarense species complex. Phycologia.