RESEARCH ARTICLES

 

Evidence for an increasing incidence and severity of Harmful Algal Blooms in the southern Benguela region

 

 

Vanessa C. Stephen; Philip A.R. Hockey

DST/NRF Centre of Excellence at the Percy FltzPatrlck Institute, University of Cape Town, Rondebosch 7701, South Africa

 

 

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ABSTRACT

Harmful Algal Blooms (HABs) may lead to catastrophic mortality over a range of trophic levels and impact on fisheries, local species' populations, conservation management and the health of both livestock and humans. Consequently, any increase in frequency and/or toxicity of these events is of concern. Recently this concern has been realized, with reported increases in the frequency of HABs from all continents except Antarctica. This reported rise is supported by data from the Benguela coast of western South Africa, where, since 1930, there has been a significant increase in the frequency of HABs and a slight increase in their average severity. There has been a sixfold increase in the number of HABs per decade since the 1960s, with the period 1990-2005 experiencing the greatest number of blooms, as well as the most severe in terms of associated mortality. The recent occurrence of previously unrecorded HAB-causing species in this region may go some way to explaining this trend, and further implies that the increase is unlikely to diminish in the near future.

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References

1. Darwin C. (1845). Diary of the Voyage of H.M.S. Beagle, ed. J. Murray, pp. 15-17. Ward Locke, London.         [ Links ]

2. Hart T.J. (1934). Red 'water-bloom' in South African seas. Nature 130, 459-460.         [ Links ]

3. Horstman D.A. (1981). 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.         [ Links ]

4. McMinn A. (1989). Late Pleistocene dinoflagellate cysts from Botany Bay, New South Wales, Australia. Micropaleontology 35, 1-9.         [ Links ]

5. Hallegraeff G.M. (1993). A review of harmful algal blooms and their apparent increase. Phycologia 32, 79-99.         [ Links ]

6. Hallegraeff G.M. (1995). Harmful algal blooms: a global overview. In Manual on Harmful Marine Microalgae, eds G.M. Hallegraeff, D.M. Anderson and A. Cembella, pp. 1-22. UNESCO, Paris.         [ Links ]

7. Landsberg J.H. (2002). The effects of Harmful Algal Blooms on aquatic organisms. Rev. Fish. Sci. 10, 113-390.         [ Links ]

8. Anon. (1931). Mystery of dead fish. The Cape Argus (Cape Town), 24 February, 13.         [ Links ]

9. Anon. (1963). 'Red Peril' can cause a vast carpet of dead fish. The Cape Argus Special (Cape Town), 7 August, 8.         [ Links ]

10. Pitcher G. (1998). Harmful Algal Blooms of the Benguela Current. Sea Fisheries Research Institute, Cape Town.         [ Links ]

11. Kudela R., Pitcher G., Probyn T, Figueiras F., Moita T and Trainer V (2005). Harmful Algal Blooms in coastal upwelling systems. Oceanography 18, 184-197.         [ Links ]

12. Pitcher G.C. and Calder D. (2000). Harmful algal blooms of the southern Benguela Current: a review and appraisal of monitoring from 1989-1997. S. Afr. J. Mar. Sci. 22, 255-271.         [ Links ]

13. Hansen G., Daugbjerg N. and Henriksen P. (2000). Comparative study of Gymnodinium mikimotoi and Gymnodinium aureolum comb. nov. (= Gyrodinium aureolum) based on morphology, pigment composition, and molecular data. J. Phycol. 36, 394-410.         [ Links ]

14. Online at www.botany.uwc.ac.za/Envfacts/redtides        [ Links ]

15. Azanza R.V, Fukuyo Y., Yap L.G. and Takayama H. (2005). Prorocentrum minimum bloom and its possible link to a massive fish kill in Bolinao, Pangasinan, Northern Philippines. Harmful Algae 4, 519-524.         [ Links ]

16. Grindley J.R. and Nel E.A. (1970). Red water and mussel poisoning at Elands Bay, December 1966. Fish. Bull. S. Afr. 6, 36-55.         [ Links ]

17. Cockroft A.C. (2001). Jasus lalandii 'walkouts' or mass strandings in South Africa during the 1990s: an overview. Mar. Freshwater Resources 52, 1085-1093.         [ Links ]

18. Bell G.R. (1961). Penetration of spines from a marine diatom into the gill tissue of lingcod (Ophiodon elongatus). Nature 192, 279-280.         [ Links ]

19. Okaichi T. (1989). Red tide problems in the Seto Inland Sea, Japan. In Red Tides: Biology, Environmental Science and Toxicology, eds T Okaichi, D.M. Anderson and T Nemoto, pp. 137-142. Elsevier, New York.         [ Links ]

20. Anderson D.M. (1995). Toxic red tides and harmful algal blooms: a practical challenge in coastal oceanography. Rev. Geophysics 33, 1189-1200.         [ Links ]

21. Smayda T (1990). Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic. In Toxic Marine Phytoplankton, eds E. Granéli, B. Sundstrom, L. Edler and D.M. Anderson, pp 29-40. Elsevier, New York.         [ Links ]

22. Magaña H.A., Contreras C. and Villareal TA. (2003). A historical assessment of Karenia brevis in the western Gulf of Mexico. Harmful Algae 2, 163-171.         [ Links ]

23. Wasmund N. and Uhlig S. (2003). Phytoplankton trends in the Baltic Sea. ICES J. Mar. Sci. 60, 177-186.         [ Links ]

24. Wasmund N., Nausch G. and Matthäus W. (1998). Phytoplankton spring blooms in the southern Baltic Sea - spatio-temporal development and long-term trends. J. Plankton Res. 20, 1099-1117.         [ Links ]

25. Konovalova G.V. (1989). Phytoplankton blooms and red tides in the far east coastal waters of the USSR. In Red Tides, Biology, Environmental Science and Toxicology, eds T. Okaichi, D.M. Anderson and T. Nemoto, pp. 97-100. Elsevier, New York.         [ Links ]

26. Konovalova G.V. (1993). Harmful dinoflagellate blooms along the eastern coast of Kamchatka. Harmful Algae News 4, 2.         [ Links ]

27. Orlova T., Selina M.S. and Stonik I.V. (1998). Distribution of harmful microalgae in Peter the Great Bay, the Sea of Japan, Russia. In Harmful Algae, eds B. Reguera, J. Blanco, M.L. Fernández and T Wyatt, pp. 86-87. Xunta de Galicia, IOC, Paris.         [ Links ]

28. Zhou M.J., Li J., Luckas B., Yu R., Yan T, Hummert C. and Kastrup S. (1999). A recent shellfish toxin investigation in China. Mar. Pollut. Bull. 39, 331-334.         [ Links ]

29. Zhao D., Zhao L., Zhang F. and Zhang X. (2004). Temporal occurrence and spatial distribution of red tide events in China's coastal waters. Human Ecological Risk Assessment 10, 945-957.         [ Links ]

30. Lam C.W.Y. and Ho K.C. (1989). Red tides in Tolo Harbour, Hong Kong. In Red Tides: Biology, Environmental Science and Toxicology, eds T. Okaichi, D.M. Anderson and T. Nemoto, pp. 49-52. Elsevier, New York.         [ Links ]

31. Hong Kong Governmental Environmental Protection Act (1998). Chapter 6, Section G.         [ Links ]

32. White A.W. (1987). Relationship of environmental factors to toxic dinoflagellate blooms in the Bay of Fundy. Rapport Processes verbaux Réunion Conseil International pour Exploration du Mer 187, 38-46.         [ Links ]

33. The Argus (1936). City Late Edition. January 14, January 16.         [ Links ]

34. Botes L., Smit A.J. and Cook P.A. (2003). The potential threat of algal blooms to the abalone (Haliotis midae) mariculture industry situated around the South African coast. Harmful Algae 2, 247-259.         [ Links ]

35. Probyn T., Pitcher G., Pienaar R. and Nuzzi R. (2001). Brown tides and mariculture in Saldanha Bay, South Africa. Mar. Pollut. Bull. 42, 405-408.         [ Links ]

36. Grindley J.R. and Taylor F.J.R. (1962). Red water and marine fauna mortality near Cape Town. Trans. R. Soc. S. Afr. 37, 111-130.         [ Links ]

37. Bricelj V.M. and Lonsdale D.J. (1997). Aureococcus anophagefferens: causes and ecological consequences of brown tides in U.S. mid-Atlantic coastal waters. Limnol. Oceanogr. 42, 1023-1038.         [ Links ]

38. Maryland Department of Natural Resources Tidewater Ecosystem Assessment Division (2005). Online: www.dnr.state.md.us/coastalbays/bt_results.html.         [ Links ]

39. Cosper E.M., Dennison W.C., Carpenter E.J., Bricelji V.M., Michell J.G., Kuenster S.H., Colefish D. and Dewey W. (1987). Recurrent and persistent brown tide blooms perturb coastal marine ecosystem. Estuaries 10, 284-290.         [ Links ]

40. Shumway S.E., Barter J. and Sherman-Caswell S. (1990). Auditing the impact of toxic algal blooms on oysters. Environ. Audit. 2, 41-56.         [ Links ]

41. Popels L.C. and Hutchins D.A. (2002). Factors affecting dark survival of the brown tide alga Aureococcus anophagefferens (Pelagophyceae). J. Phycol. 38, 738-744.         [ Links ]

42. Doblin M.A., Popels L.C., Coyne K.J., Hutchins D.A., Cary S.C. and Dobbs F.C. (2004). Transport of the Harmful Bloom Alga Aureococcus anophagefferens by oceangoing ships and coastal boats. Appl. Environ. Microbiol. 70, 6495-6500.         [ Links ]

43. Herbert D.G. (1999). Siphonaria compressa, South Africa's most endangered marine mollusc. S. Afr. J. Sci. 95, 77-79.         [ Links ]

44. AngelA., Branch G.M., Wanless R.M. and Siebert P (2006). Causes of rarity and range restriction of an endangered, endemic limpet, Siphonaria compressa. J. Exp. Mar. Biol. Ecol. 330, 245-260.         [ Links ]

45. Coulson J.C., Potts G.R., Deans I.R. and Fraser S.M. (1968). Mortality of shags and other sea birds caused by paralytic shellfish poison. Nature 220, 23-24        [ Links ]

46. Ward V.L. and Williams A.J. (2004). Coastal killers: causes of seabird mortality. Bird Numbers 13, 14-17.         [ Links ]

47. Work TM., Beale A.M., Fritz L., Quilliam M.A., Silver M., BuckK. and Wright J.L.C. (1993). Domoic acid intoxication of Brown Pelicans and cormorants in Santa Cruz, California. In Toxic Phytoplankton Blooms in the Sea, eds T.J. Smayda and Y. Shimizu, pp. 763-768. Elsevier, Amsterdam.         [ Links ]

48. Shumway S.E., Allen S.M. and Boersma P.D. (2003). Marine birds and harmful algalblooms: sporadic victims or under-reported events? Harmful Algae 2, 1-17.         [ Links ]

49. Hockey P.A.R. and Cooper J. (1980). Paralytic shellfish poisoning - a controlling factor in black oystercatcher populations? Ostrich 51, 188-190.         [ Links ]

50. BirdLife International. (2004). Threatened Birds of the World - CD ROM. BirdLife International, Cambridge.         [ Links ]

51. Bossart G.D., Baden D.G., Ewing R.Y., Roberts B. and Wright S.D. (1998). Brevitoxicosis in manatees (Trichechus manatus latirostris) from the 1996 epizootic: gross, histologic and immunohistochemical features. Toxic. Path. 26, 276-282.         [ Links ]

52. Walsh C.J., Luer C.A. and Noyes D.R. (2005). Effects of environmental stressors on lymphocyte proliferation in Florida Manatees, Trichechus manatus latirostris. Vet. Immunol. Immunopath. 103, 247-256.         [ Links ]

53. Gilchrist J.D.F. (1914). An inquiry into fluctuations in fish supply on the South African coast. Mar. Biol. Rpt 2, 8-35.         [ Links ]

54. Lilly E.L., Kulis D.M., Gentien P and Anderson D.M. (2002). Paralytic shellfish poisoning toxins in France linked to a human-introduced strain of Alexandrium catenella from the western Pacific: evidence from DNA and toxin analysis. J. Plankton Res. 24, 443-452.         [ Links ]

55. South African Tourism - Strategic Research Unit (2005). 2004 Annual Tourism Report.         [ Links ]

56. Melville-Smith R. and van Sittert L. (2005). Historical commercial West Coast rock lobster Jasus lalandii landings in South African waters. Afr. J. Mar. Sci. 27, 33-44.         [ Links ]

57. Schwimmer D. and Schwimmer M. (1968). Medical aspects of phycology. In Algae, Man and the Environment, ed. D. Jackson, pp. 279-358. Syracuse University Press, Syracuse, NY.         [ Links ]

58. Anon. (1876). Local and general, column 2. Cape Times (Cape Town), 27 June,3.         [ Links ]

59. Anon. (1977). Local and general, column 1. Cape Times (Cape Town), 1 May, 3.         [ Links ]

60. Anon. (1963). Thousands of fish die in the 'red tide'. The Cape Argus City Late (Cape Town), 22 November, 2.         [ Links ]

61. Anon. (1931). Fish Hoek's gleaming sea. The Cape Argus (Cape Town), 19 Feb., 16.         [ Links ]

62. Anon. (1966). Red tide hits Elands Bay. The Cape Argus (Cape Town), 27 December, 5.         [ Links ]

63. Grindley J.R. and Nel E.A. (1968). Mussel poisoning and shellfish mortality on the west coast of South Africa. S. Afr. J. Sci. 64, 420-422.         [ Links ]

64. De Jager B. (1967). False Bay red tide is not a menace. The Cape Argus City Late (Cape Town), 21 August, 3.         [ Links ]

65. Anon. (1967). Millions of krill wash ashore. The Cape Argus (Cape Town), 10 November, 9.         [ Links ]

66. Brown P.C., Hutchings L. and Horstman D.A. (1979). A red-water outbreak and associated fish mortality at Gordon's Bay near Cape Town. Fish. Bull. S. Afr. 11, 46-52.         [ Links ]

67. Horstman D.A., McGibbon S., Pitcher G.C., Calder D. and Hutchings L. (1991). Red tides in False Bay, 1959-1989, with particular reference to blooms of Gymnodinium spp. Trans. R. Soc. S. Afr. 47, 611-628.         [ Links ]

68. Underhill G. (1994). Red Tide off city - shellfish warning. Cape Times (Cape Town), 22 March, 1.         [ Links ]

69. Pitcher G. and Matthews S. (1996). Noxious Gymnodinium species in South African waters. Harmful Algae News 15, 1-3.         [ Links ]

70. Anon. (1997). Kreef stap uit in Elandbaai. Die Burger (Cape Town), 8 April, 1.         [ Links ]

71. Steenkamp W. (1998). Smelly black tide unlikely to spread. Cape Times (Cape Town), 6 May, 3.         [ Links ]

72. Gosling M. (1999). Crayfish on the march. Cape Times (Cape Town), 16 April, 1.         [ Links ]

73. Cosgriff M. (2000). Red Tide kills 30m mussels. Independent Online, 2 June. http://www.whoi.edu/redtide/notedevents/foreign/SouthAfrica/SouthAfrica_6-2-00.html        [ Links ]

74. Oliver L. (2002) Toxic red tide moves in on Lamberts Bay. The Sunday Independent Online. October 25 at http://www.iol.co.za/index.php?click_id=14&art_id=ct20021025210634838R300518&set_id=1        [ Links ]

75. Wyatt T and Zingone A. (2004). Cape Agulhas. Harmful Algae News 27, 1-7.         [ Links ]

76. Environmental Writer. (2005). Now toxic tide hits the Peninsula. Cape Times (Cape Town), 27 April, 1.         [ Links ]

77. Ndenze B. (2005). Toxic red tide hits coast. Cape Times (Cape Town), 15 March, 1.         [ Links ]

78. Schantz E.J., Lynch J.M., Vayvada G., Matsumoto K. and Rapoport H. (1966). The purification and characterization of the poison produced by Gonyaulax catenella in axenic culture. Biochemistry 5, 1191-1195.         [ Links ]

79. Prakash A., Medcof J.C. and Tennant A.D. (1971). Paralytic shellfish poisoning in Eastern Canada. Bull. Fish. Res. Bd Canada 177, 87.         [ Links ]

80. Ogata T. and Kodama M. (1986). Ichthyotoxicity found in cultured media of Protogonyaulax spp. Mar. Biol. 92, 31-34.         [ Links ]

81. De Gange A.R. and Vacca M.M. (1989). Sea otter mortality at Kodiak Island, Alaska, during summer, 1987. J. Mammal. 70, 836-838.         [ Links ]

82. Oshima Y., Hirota M., Yasumoto T., Hallegraeff G.M., Blackburn S.I. and Steffensen D.A. (1989). Production of paralytic shellfish toxins by the dinoflagellate Alexandrium minutum Halim from Australia. Nippon Suisan Gakkaishi 55, 925.         [ Links ]

83. Hallegraeff G.M., Steffensen D.A., Wetherbee R. 1988. Three estuarine Australian dinoflagellates that can produce paralytic shellfish toxins. J. Plankton Res. 10, 533-541.         [ Links ]

84. Hallegraeff G.M. (1991). Aquaculturists' Guide to Harmful Australian Microalgae. Fishing Industry Training Board of Tasmania/CSIRO Division of Fisheries, Hobart.         [ Links ]

85. Mijares A.J., Sevcik C., Barboza C.A. and Saavedra J.A. (1985). Ichthyotoxism by a paralytic toxin produced by marine dinoflagellates of the genus Ceratium: relationship to fraction ß isolated from the sponge Tedania ignis. Toxicon 23, 221-233.         [ Links ]

86. Cembella A.D.(1989). Occurrence of okadaic acid, a major diarrheic shellfish toxin, in natural populations of Dinophysis spp. from the eastern coast of North America. J. Appl. Phycol. 1, 307-310.         [ Links ]

87. Lee J.S., Igarashi T. Fraga S., Dahl E., Hovgaard P. and Yasumoto T. (1989). Determination of diarrheic shellfish toxins in various dinoflagellate species. J. Appl. Phycol. 1, 147-152.         [ Links ]

88. Larsen J. and Moestrup O. (1989). Guide to Toxic and Potentially Toxic Marine Algae. The Fish Inspection Service, Ministry of Fisheries, Copenhagen.         [ Links ]

89. Yasumoto T (1990). Marine microorganisms toxins - an overview. In Toxic Marine Phytoplankton, eds E. Granéli, B. Sundstrom, L. Edler and D.M. Anderson, pp. 3-8. Elsevier, New York.         [ Links ]

90. Taylor F.J.R., Fukuyo Y. and Larsen J. (1995). Taxonomy of harmful dinoflagellates. In Manual on Harmful Marine Microalgae, eds G.M. Hallegraeff, D.M. Anderson and A. Cembella, pp. 283-317. UNESCO, Paris.         [ Links ]

91. Koizumi Y., Kohno J., Matsuyama N., Uchida T and Honjo T. (1996). Environmental features and the mass mortality of fish and shellfish during the Gonyaulax polygramma red tide occurred in and around Uwajima Bay, Japan, in 1994. Nippon Suisan Gakkaishi 62, 217-224.         [ Links ]

92. Forbes J.R. 1990. Massive bloom of Gonyaulax spinifera along the west coast of Vancouver Island. Red Tide Newsl. 3, 2-3.         [ Links ]

93. Seki T., Satake M., Mackenzie L., Kaspar H.F. and Yasumoto T. (1996). Gymnodimine, a novel toxicimine isolated from the Foveaux strait oysters and Gymnodinium sp. In Harmful and Toxic Algal Blooms, eds T. Yasumoto, Y. Oshima and Y. Fukuyo, pp. 495-498. Intergovernmental Oceanographic Commission of UNESCO, Paris.         [ Links ]

94. Oda M. (1935). The red tide of Gymnodinium mikimotoi Miyake et Kominami n. sp. (MS) and the influence of copper sulfate on the red tide. Zool. Mag. 47, 35-48.         [ Links ]

95. Kim H.G., ParkJ.S., Fukuyo Y., Takayama H., An K.H. and Shim J.M. (1995). Noxious dinoflagellate bloom of an undescribed species of Gyrodinium in Chungmu coastal waters, Korea. In Harmful Marine Algal Blooms, eds P. Lassus, G. Arzul, E. Erard-Le-Denn, P. Gentien and C. Marcaillou-Le-Baut, pp. 59-63. Lavoisier, Paris.         [ Links ]

96. Braarud T. (1957). A red water organism from Walvis Bay (Gymnodinium galatheanum n.sp.). Galathea Deep Sea Expedition, 1, 137-138.         [ Links ]

97. Pieterse F. and Van der Post D.C. (1967). The pilchard of Southwest Africa. Oceanographical conditions associated with red-tides and fish mortalities in the Walvis Bay region. Investl Rep. SWA. Mar. Res. Lab. 14, 1-125.         [ Links ]

98. Nielsen M.V. and Stromgren T. (1991). Shell growth response of mussels (Mytilus edulis) exposed to toxic microalgae. Mar. Biol. 108, 263-267.         [ Links ]

99. Okaichi T. and Nishio S. (1976). Identification of ammonia as the toxic principle of red tide of Noctiluca miliaris. Bull. Plankton Soc. Japan 23, 75-80.         [ Links ]

100. Aiyar R.G. (1936). Mortality of fish of the Madras coast in June 1935. Current Science 4, 488-489.         [ Links ]

101. Bhimachar B.S. and George P.C. (1950). Abrupt set-backs in the fisheries of the Malabar and Kanara coasts and 'red water' phenomenon as their probable cause. Proc. Indian Acad. Sci. 31, 339-350.         [ Links ]

102. Steidinger K.A. (1979). Collection, enumeration and identification of free-living marine dinoflagellates. In Toxic Dinoflagellate Blooms, eds D.L. Taylor and H.H. Seliger, pp. 435-442. Elsevier/North-Holland, New York.         [ Links ]

103.Granéli E., Wallström K., Larsson U., Graneli W and Elmgren R. (1990). Nutrient limitation of primary production in the Baltic Sea area. Ambio 19, 142-151.         [ Links ]

104.Uchida T. (1977). Excretion of a diatom inhibiting substance by Prorocentrum micans Ehrenberg. Jap. J. Ecol. 27, 1-4.         [ Links ]

105. Pinto J.S. and Silva E.S. (1956). The toxicity of Cardium edulum L. and its possible relation to the dinoflagellate Prorocentrum micans Ehr. Notas Estud. Instituto de Biologia Maritima 12, 1-20.         [ Links ]

106. Avaria S. (1979). Red tides off the coast of Chile. In Toxic Dinoflagellate Blooms, eds D.L. Taylor and H.H. Seliger, pp. 161-164. Elsevier, New York.         [ Links ]

107. Heil C.A., Gilbert P.M. and Fan C. (2005). Prorocentrum minimum (Pavillard) Schiller. A review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4, 449-470.         [ Links ]

108. Satake M., Ichimura T., Sekiguchi K., Yoshimatsu S. and Oshima Y. (1999). Confirmation of yessotoxin and 45, 46, 47-trinoryessotoxin production by Protoceratium reticulatum collected in Japan. Natural Toxins 7, 147-150.         [ Links ]

109. Work T.M., Bar B., Beale A.M., Fritz L., Quilliam M.A. and Wright J.L.C. (1992). Epidemiology of domoic acid poisoning in brown pelicans (Pelecanus occidentalis) and Brandt's cormorants (Phalacrocorax penicillatus) in California. J. Zoo Wildl. Med. 24, 54-62.         [ Links ]

110. Shimda M., Murakami T.H., Imahayashi T., Ozaki H.S., Toyoshima T. and OkaichiT. (1983). Effects of sea bloom Chatonella antique on gill primary lamellae of the young yellowtail, Seriola quinqueradiata. Acta Histochem. 16, 232-244.         [ Links ]

111. Chang F.H, Anderson C. and Boustead N.C. (1990). First record of Heterosigma (Raphidophyceae) bloom with associated mortality of cage-reared salmon in Big Glory Bay, New Zealand. N.Z.J. Mar. Freshwater Res. 24, 461-469        [ Links ]

112. Yang C.Z., Albright L.J. and Yousif AN. (1995). Oxygen-radical mediated effects of the toxic phytoplankter Heterosigma carterae on juvenile rainbow trout Oncorhynchus mykiss. Diseases of Aquatic Organisms 23, 101-108.         [ Links ]

113. Bricelj V.M. and Kuenstner S.H. (1989). Effects of the 'brown tide' on the feeding, physiology and growth of bay scallops and mussels. In Novel Phytoplankton Blooms, eds E.M. Cosper, V.M. Bricelj and E.J. Carpenter, pp. 491-509. Springer-Verlag, Berlin.         [ Links ]

114. Gainey L.F. and Shumway S.E. (1991). The physiological effect of Aureococcus anophagefferens ('brown tide') on the lateral cilia of bivalve molluscs. Biol. Bull. 181, 298-306.         [ Links ]

115. Hockey P.A.R., Dean W.R.J. and Ryan P.G. (eds) (2005). Roberts - Birds of Southern Africa, 7th edn. Trustees of the John Voelcker Bird Book Fund, Cape Town.         [ Links ]

 

 

Received 3 November 2006.
Accepted 29 June 2007.

 

 

‡Author for correspondence. E-mail: phil.hockey@uct.ac.za