An examination of the epiphytic nature of Gambierdiscus toxicus, a dinoflagellate involved in ciguatera fish poisoning

Abstract

Twenty-four specimen of macroalgae were collected in nearshore waters of the island of Hawaii, identified, and maintained to examine how the epiphytic relationship between Gambierdiscus toxicus (isolate BIG12) varied among the macroalgal species. Gambierdiscus cells were introduced to petri dishes containing 100 g samples of each macroalgal host, which were examined at two, 16, 24, and every 24 to 72 hours thereafter, over a 29-day period. Gambierdiscus proliferated in the presence of some host species (e.g., Galaxaura marginata and Jania sp.), but grew little in the presence of other species (e.g., Portieria hornemannii). Gambierdiscus exhibited high survival rates (>99%) in the presence of Chaetomorpha sp., but died before the end of the experiment (after 21 days) with other host species (e.g., Dictyota and Microdictyon spp.). Gambierdiscus avoided contact with Portieria hornemannii, but averaged up to 30% attachment with other host species. The numbers of Gambierdiscus cells belonging to one of three classes (alive and attached; alive and unattached; and dead) were determined for each time point. The 24 algal hosts were grouped according to their commonalities relative to these three classes using a Bray-Curtis similarity index, similarity profile (SIMPROF) permutation tests, and multi-dimensional scaling (MDS) analysis (PRIMER 6). The resultant six groupings were used to construct different Gambierdiscus growth profiles for the different algal hosts. Group A is characterized by a preponderance of unattached cells and high mortality rates. Groups B, C, E, and F also displayed high proportions of unattached cells, but mortality either occurred later (Groups B and C) or rates were lower (Groups E and F). Group D had the highest proportion of attached cells. Group E contained three out of the four chlorophyte species, while Group F contained the majority of the rhodophytes. Over 50% of the species in Group F are considered to be palatable, whereas Groups A, B, and C are composed of species that exhibit chemical defenses against herbivory. The results of this study coupled with previous findings indicate that Gambierdiscus is not an obligate epiphyte; it can be free-swimming and found in the plankton. The conditions that lead to changes between epiphytic and planktonic stages need to be better studied in order to determine how they affect Gambierdiscus growth and physiology, connectivity and dispersion mechanisms, and toxin movement up into the foodweb.

Figure 1

Map of the island of Hawaii showing the location (Leleiwi) of the site where macroalgae were collected for this study.

Figure 2

A cluster analysis of the different algal host species according to their similarity in the three Gambierdiscus-based parameters (%attached; %unattached; and %dead). The clusters were based on a Bray-Curtis similarity index and were determined using group averaging calculations. Similarity profile (SIMPROF) permutation tests were used to test for significant differences in the hierarchical cluster structure (i.e., the red dotted lines) at a Bonferroni-corrected α value of 0.002. The algal host abbreviations are provided in Table 4.

Figure 3

A two-dimensional (2D) plot of the non-metric Multi-Dimensional Scaling (MDS) analysis of the different algal host species according to their similarity in the Gambierdiscus-based parameters (%attached; %unattached; and %dead). The cluster results (dotted ovals) were overlaid on the MDS plot with similarity boundary values of 82% as determined by the average significant similarity based on the SIMPROF results. The algal host abbreviations are provided in Table 4.

Figure 4

The group-averaged Gambierdiscus responses for each of the six algal groups determined in Figure 3 and presented in Table 4. The percentage of attached (filled circles), unattached (open circles), and dead (filled triangles) Gambierdiscus cells is plotted for each group (A – F) over the course of the experiment (29 days).