Asynchrony of Gambierdiscus spp. Abundance and Toxicity in the U.S. Virgin Islands: Implications for Monitoring and Management of Ciguatera

Abstract

Ciguatera poisoning (CP) poses a significant threat to ecosystem services and fishery resources in coastal communities. The CP-causative ciguatoxins (CTXs) are produced by benthic dinoflagellates including Gambierdiscus and Fukuyoa spp., and enter reef food webs via grazing on macroalgal substrates. In this study, we report on a 3-year monthly time series in St. Thomas, US Virgin Islands where Gambierdiscus spp. abundance and Caribbean-CTX toxicity in benthic samples were compared to key environmental factors, including temperature, salinity, nutrients, benthic cover, and physical data. We found that peak Gambierdiscus abundance occurred in summer while CTX-specific toxicity peaked in cooler months (February-May) when the mean water temperatures were approximately 26-28 °C. These trends were most evident at deeper offshore sites where macroalgal cover was highest year-round. Other environmental parameters were not correlated with the CTX variability observed over time. The asynchrony between Gambierdiscus spp. abundance and toxicity reflects potential differences in toxin cell quotas among Gambierdiscus species with concomitant variability in their abundances throughout the year. These results have significant implications for monitoring and management of benthic harmful algal blooms and highlights potential seasonal and highly-localized pulses in reef toxin loads that may be transferred to higher trophic levels.

Keywords: Caribbean; Dictyota; Gambierdiscus; algal toxin; benthic algae; ciguatera poisoning; ciguatoxin; dinoflagellate; harmful algal bloom.

Figure 1

Map of long-term field sampling sites in St. Thomas, US Virgin Islands. Map created in ArcGIS Professional with overlaid shapefiles of benthic cover with coral, hardbottom, and seagrass from [35] and macroalgae from the St. Thomas and St. John benthic habitat dataset [36], both from the National Oceanic and Atmospheric Administration, U.S. Dept. Commerce.

Figure 2

Time-series of benthic cover over the study period as determined by benthic habitat video surveys. Data highlights the temporal change in the percent (%) cover of combined macroalgae (black) and % Dictyota spp. cover (green) at each sampling site. Missing data points are time periods when benthic surveys were not conducted. Feb* denotes that FC was surveyed on 23 February 2010.

Figure 3

Asynchrony between cell toxin load (C-CTX eq cell⁻¹ * cells g Dictyota⁻¹) and mean (+s.d.) Gambierdiscus spp. abundance (cells g Dictyota⁻¹), with 7-day averaged bottom temperatures from each site. Open circles represent “No Data” for either toxin load or Gambierdiscus abundance count.

Figure 4

Time series of toxin cell quota (pg C-CTX-1 eq. cell⁻¹) determined from benthic microalgal (20–200 µM fraction) field samples collected monthly from nearshore (Black Point; Coculus Rock) and offshore sites (Flat Cay; Seahorse Shoal) of St. Thomas, Virgin Islands. Black Point and Flat Cay (black bars) are western sites, whereas Coculus Rock and Seahorse Shoal (blue bars) are eastern sites. Colored circles represent “No Data” collected from the corresponding sites, with all other zeros indicating true non-detections of toxicity.

Figure 5

Truncated violin plot of log-transformed toxin load. Medians (dashed) and quartiles (dotted) shown. Trace detections were designated at toxin load 0.25 pg C-CTX-1 eq. g Dictyota⁻¹ (log-transformed to −0.6). Letters on plot indicate significant differences in toxin load between sites.