Occurrence and predominance of the fish killer Cochlodinium polykrikoides by Jose Carrasquero-Diaz

AFRICAN JOURNAL OF MARINE SCIENCE ISSN 1874–232X

Occurrence and predominance of the fish killer Cochlodinium polykrikoides on the Pacific coast of Costa Rica M Vargas-Montero1*, E Freer1, R Jiménez-Montealegre2 and JC Guzmán2 1

Centro de Investigación en Estructuras Microscópicas, Universidad de Costa Rica, Ciudad de la Investigación, Finca 2, San Pedro de Montes de Oca, CP 2060, Costa Rica 2 Parque Marino del Pacífico, Puntarenas, Costa Rica * Corresponding author, e-mail: vmontero@cariari.ucr.ac.cr

Water samples were collected at several points along the Pacific coast of Costa Rica (10°00’N, 84°15’E) fortnightly from January 2003 to June 2004. During this period, dense red-ochre discolourations dominated by Cochlodinium polykrikoides were observed, particularly over the dry season. In 2003, the highest cell density of 1.75 X 108 cells l–1 was observed in October. During April and June 2004, extensive blooms were present, with the highest cell density (3.8 X 108 cells l–1) occurring in April. These blooms were accompanied by a strong fetid odour and large quantities of yellow foam. Fish mortalities also occurred near some coastal areas. The observed discolourations tended to be

associated with the strongest north-west winds on the North Pacific coast of Costa Rica. To date, blooms caused by C. polykrikoides have been increasing in frequency and in extent. The previously unreported high cell densities and the increase in the duration and extent of these harmful algal blooms suggest that the environmental conditions have changed to the benefit of C. polykrikoides over other phytoplankton species that usually bloom at that time of year. The fish mortalities associated with C. polykrikoides blooms are cause for concern, as are the possible environmental changes contributing to the production of these extensive blooms.

Keywords: Cochlodinium polykrikoides, fish kill, Pacific coast

Introduction Cochlodinium polykrikoides is known to be associated with extensive fish kills, which result in severe economic losses in Japan and Korea (Yuki and Yoshimatsu 1989, Kim 1998, Okaichi 2003). Similar harmful effects have only recently been noted in Costa Rica. In 2002, on the Pacific coast of Costa Rica, fish mortalities and airborne human intoxication were noted for the first time during a bloom of C. polykrikoides (Vargas and Freer 2004a). Although the subject is of much interest, the mechanism behind its toxicity remains unclear (Taylor 1987). Laboratory cultures of C. polykrikoides have been shown to produce 40% mortality in juveniles of the fish Leiognathus nuchalis (pargo mancha) during the first eight hours of contact (Yuki and Yoshimatsu 1989). C. polykrikoides has known haemolytic properties that can adversely affect aquatic organisms. In fish bioassays at densities of above 1 000 cells l –1, fish showed signs of respiratory distress, loss of equilibrium, and an inability to maintain position in the water column (Landsberg 2002). Earlier reports of outbreaks of C. polykrikoides on the Pacific coast of Mexico were in 1999 in Manzanillo Bay (Morales-Blake et al. 2001) and in 2000 in the Gulf of California (Gárate-Lizárraga et al. 2000), possibly related to the La Niña phenomenon. On the Pacific coast of Costa Rica, the persistent trade winds produce turbulence in the water column, particularly in the upwelling area in the north

(Jiménez 2001). It has been suggested that the environmental conditions arising from trade winds are conducive to the development of blooms of C. polykrikoides (Vargas and Freer 2004a). This study presents the temporal distribution of C. polykrikoides along the Pacific coast of Costa Rica and the possible environmental effects that contribute to the establishment of these extensive blooms. Material and Methods Surface water samples for taxonomic analysis were collected every 15 days from January 2003 to June 2004, at 14 stations located over the main fishing grounds along the Pacific coast of Costa Rica (Figure 1). The samples were collected using a 1-litre acrylic Niskin bottle and a 20µm plankton net, fixed with acid Lugol’s solution and subsequently analysed using a Sedgewick-Rafter chamber under a Nikon light microscope. Wind data from various meteorological stations on the Pacific coast of Costa Rica were also collected. Results During the period of sampling, water discolourations owing to C. polykrikoides started in September 2003, and reached

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Figure 1: Map of the Pacific coast of Costa Rica showing the locality of the sample stations (Stations 1–3 are in the Gulf of Papagayo and Stations 6–9 in the Gulf of Nicoya)

the highest average cell density of 1.75 X 108 cells l–1 in October (Figure 2). The cells were generally present as chains of 4, 6 or 8 cells, each containing a red stigma. Large numbers of resistant cysts were also present in the water samples. At the beginning of January 2004, the bloom had reached its broadest spatial extent of approximately 50km2. The maximum concentration of 3.8 X 108 cells l–1 was attained in April 2004, by which time the bloom had decreased in size and was concentrated within a few kilometres from the coast. The major discolourations were observed during the dry season (December–May), generally after the strongest northeasterly winds (Figure 2). These discolourations were redochre in colour, and associated with a strong fetid odour and large amounts of yellow foam. Hundreds of dead fish, comprising members of the families Carangidae, Lutjanidae, Muraenidae, Engraulidae and Soleidae, were observed near the central Pacific coast. Discussion Although small blooms of C. polykrikoides have been observed since 1981, this is the first report of a large-scale bloom on the Pacific coast of Costa Rica. Extensive discolourations were observed over a period of less than one year and were associated with foam production, a fetid smell, and large fish mortalities. Fish kills associated with HABs are unusual in Costa Rican waters. However, in 2002 a large number of dead fish washed up on the beaches (Vargas and Freer 2004a). In 2004, fish and coral reef mortalities were observed in diverse sectors of the coast in close proximity to blooms of C. polykrikoides. It is possible that, owing to the high cell densities of C. polykrikoides, anoxic conditions following bloom decay could have contributed to some of these mortalities. The potential toxicity of C. polykrikoides has not been established in laboratory tests.

Cell density Wind speed

NICARAGUA

AVERAGE WIND SPEED (m s )

Vargas-Montero, Freer, Jiménes-Montealegre and Guzman

AVERAGE CELL DENSITY IN 1 WATER SURFACE (thousand cells l )

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50 J FMAM J J A S OND J FMAM J 2003 2004

Figure 2: Monthly average wind speed and average cell density in surface waters along the Pacific coast of Costa Rica between January 2003 and June 2004. Seawater temperature ranged between 25°C and 28°C during the sampling period

The first report of a HAB by C. polykrikoides (then named C. catenatum) on the Pacific coast of Costa Rica was in 1981 (Hargraves and Víquez 1981). Two decades later, in 2002, a bloom of this species was reported in the central Pacific region of Costa Rica, together with the cyanobacterium Trichodesmium erytraeum (Vargas and Freer 2004a). HAB events in general have become increasingly frequent and more persistent in Costa Rica since 2000. More specifically, C. polykrikoides blooms have increased in frequency and persistence since 2002 (Vargas and Freer 2003, Vargas et al. 2004), extending over the whole Pacific coast but concentrated in the main fishing area of the Gulf of Nicoya (Vargas and Freer 2004a). This recent increase suggests that environmental conditions along the coastal areas of Costa Rica may have changed to the benefit of previously unrecorded non-desirable micro-organisms. The high cell concentrations reported in this study have not been observed previously along the Pacific coast of Costa Rica. This is indicative of a shift in species dominance from toxic phytoplankton species that usually produce blooms, such as Pyrodinium bahamense and Gymnodinium cf. catenatum, to C. polykrikoides (Hargraves and Víquez 1981, Víquez and Hargraves 1995, Vargas and Freer 2003, 2004b). Blooms of C. polykrikoides are generally quasi-monospecific, with only very low concentrations of other species present. Other species encountered were the dinoflagellates Ceratium dens, Gonyaulax spinifera, Heterocapsa sp. and Heterolobatum sp., as well as the cyanobacterium Trichodesmiun erytraeum. The average wind speed for the upwelling area in the north along the Pacific coast of Costa Rica indicates that the strongest north-westerly winds occur during April, the period when an extensive bloom was observed. Along the central Pacific coast (Gulf of Nicoya) some of the blooms were also observed during the dry season. The period December–March is characterised by strong winds, which, by promoting turbulence, disrupt water column stratification and increase the availability of nutrients. Such conditions favour the emergence of cysts near the coast (Mcgillicuddy

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et al. 2003). Winds are very important in the formation and maintenance of HABs along some Central American coasts (Alonso and Ochoa 2004). Strong trade winds from the north-east could be, among others, a significant factor in the increase of HABs in Costa Rica — more so than the availability of nutrients, particularly for mixotrophic species like C. polykrikoides. Acknowledgements — We appreciate the contribution of the Vicerrectoría de Investigación of the University of Costa Rica to this research, which forms part of project no. 810-A4043. We also thank the Ministry of Science and Technology and the Netropica Foundation for their contribution. Dr Steve Hanson and two anonymous reviewers are thanked for their comments on an earlier version of the manuscript.

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