Influence of Environmental Variables on Gambierdiscus spp. (Dinophyceae) Growth and Distribution

Abstract

Benthic dinoflagellates in the genus Gambierdiscus produce the ciguatoxin precursors responsible for the occurrence of ciguatera toxicity. The prevalence of ciguatera toxins in fish has been linked to the presence and distribution of toxin-producing species in coral reef ecosystems, which is largely determined by the presence of suitable benthic habitat and environmental conditions favorable for growth. Here using single factor experiments, we examined the effects of salinity, irradiance, and temperature on growth of 17 strains of Gambierdiscus representing eight species/phylotypes (G. belizeanus, G. caribaeus, G. carolinianus, G. carpenteri, G. pacificus, G. silvae, Gambierdiscus sp. type 4-5), most of which were established from either Marakei Island, Republic of Kiribati, or St. Thomas, United States Virgin Island (USVI). Comparable to prior studies, growth rates fell within the range of 0-0.48 divisions day(-1). In the salinity and temperature studies, Gambierdiscus responded in a near Gaussian, non-linear manner typical for such studies, with optimal and suboptimal growth occurring in the range of salinities of 25 and 45 and 21.0 and 32.5°C. In the irradiance experiment, no mortality was observed; however, growth rates at 55 μmol photons · m(-2) · s(-1) were lower than those at 110-400 μmol photons · m(-2) · s(-1). At the extremes of the environmental conditions tested, growth rates were highly variable, evidenced by large coefficients of variability. However, significant differences in intraspecific growth rates were typically found only at optimal or near-optimal growth conditions. Polynomial regression analyses showed that maximum growth occurred at salinity and temperature levels of 30.1-38.5 and 23.8-29.2°C, respectively. Gambierdiscus growth patterns varied among species, and within individual species: G. belizeanus, G. caribaeus, G. carpenteri, and G. pacificus generally exhibited a wider range of tolerance to environmental conditions, which may explain their broad geographic distribution. In contrast, G. silvae and Gambierdiscus sp. types 4-5 all displayed a comparatively narrow range of tolerance to temperature, salinity, and irradiance.

Fig 1. Growth rates of Gambierdiscus strains versus culture salinity of 10–60.

Each point is the mean of triplicate measurements, and the bars represent standard deviation (SD). Black arrows represent the maximum growth rate for a species.

Fig 2. Average growth response of Gambierdiscus species to salinity of 10–60.

For ease of viewing, error bars shown in Fig 1 are omitted here.

Fig 3. Gambierdiscus growth rate responses (black squares) to salinities of 10–60 and simulated growth curves (red line) by polynomial regressive analysis.

(A) G. belizeanus (BP Mar10_6, BP Mar10_7, BP Mar10_22, FC Dec10_13), (B) G. caribaeus (BP Aug08, FC Nov09_4, SH Nov09_3), (C) G. carolinianus (SH Mar10_12, BB Apr10_3, BP May10_1), (D) G. carpenteri (KML1), (E) G. pacificus (3S0509-27, 3S0510-19), (F) G. silvae (FC May10_9), (G) Gambierdiscus sp. type 4 (1D0509-16, 1D0510-22), and (H) Gambierdiscus sp. type 5 (DS0511-03).

Fig 4. Growth rates of Gambierdiscus strains versus culture irradiance of 55–400μmol photons · m^-2 · s^-1.

Each point is the mean of triplicate measurements, and the bars represent standard deviation (SD). Black arrows represent the maximum growth rate for a species.

Fig 5. Average growth response of Gambierdiscus species to irradiance of 55–400μmol photons · m^-2 · s^-1.

For ease of viewing, error bars shown in Fig 4 are omitted here.

Fig 6. Growth rates of Gambierdiscus strains versus culture temperature of 16–36°C.

Each point is the mean of triplicate measurements, and the bars represent standard deviation (SD). Black arrows represent the maximum growth rate for a species.

Fig 7. Average growth response of Gambierdiscus species to temperatures of 16–36°C.

For ease of viewing, error bars shown in Fig 6 are omitted here.

Fig 8. Gambierdiscus growth rate responses (black squares) at 16–36°C and simulated growth curves (red lines) by polynomial regressive analysis.

(A) G. belizeanus (BP Mar10_6, BP Mar10_7, BP Mar10_22, FC Dec10_13), (B) G. caribaeus (BP Aug08, FC Nov09_4, SH Nov09_3), (C) G. carolinianus (SH Mar10_12, BB Apr10_3, BP May10_1), (D) G. carpenteri (KML1), (E) G. pacificus (3S0509-27, 3S0510-19), (F) G. silvae (FC May10_9), (G) Gambierdiscus sp. type 4 (1D0509-16, 1D0510-22), and (H) Gambierdiscus sp. type 5 (DS0511-03).