Figure 1. Living cell of Protoceratium reticulatum, dorsal side. Indian River Lagoon at Vero Beach.
Figure 2. Schematic drawing, P. reticulatum, ventral side, ‘Po’ = apical pore; red arrow indicates ventral pore on first apical plate. Modified from Dodge 1982.
Figure 3. Hypnocyst, P. reticulatum, from Tampa Bay, FL.
Figure 4. P. reticulatum, dissociated epitheca, red arrow indicates ventral pore on first apical plate. Light micrograph modified from von Stosch 1969.
Figure 5. Clustered cells of P. reticulatum from a culture isolated from the IRL at Fort Pierce, ‘a’ = apical view; ‘at’ = oblique antapical view; ‘d’ = dorsal view; ‘v’ = ventral view.
Figure 6. Apical view of P. reticulatum epitheca. Arrow indicates ventral pore on first apical plate.
Protoceratium reticulatum (Claparède et Lachmann) Bütschli
Gonyaulax grindleyi Reinecke
Operculodinium centrocarpum (Deflandre et Cookson) Wall
Protoceratium aceros Bergh
This organism was originally described as a species of Peridinium. Because of the obscure plate pattern, the same organism was described as a species of Gonyaulax by Reinecke in 1967, and it often appears in the literature under that name. The hypnospore, originally described from Miocene deposits (Matsuoka et al. 1997) was identified as O. centrocarpum, but its exact relationship to extant P. reticulatum is not certain.
This dinoflagellate exists as unicells with an oval shape (Figures 1, 2 & 5), occasionally becoming somewhat polygonal. The cingulum is displaced about one cingular width circumferentially (Figures 2 & 5), and is located anterior to the cell midpoint, making the hypotheca larger than the epitheca (Figures 1 & 2). The sulcus does not reach the antapex (Figures 2 & 5). The cell surface is highly reticulate, which makes the plate pattern difficult to evaluate (Figures 1, 4 & 5). The first apical plate (1’) has a ventral pore on its left side (Figures 2, 4 & 6). Both Steidinger & Tangen (1997) and Throndsen et al. (2007) give a plate formula for the genus as Po,3’, 0a, 6’’, 6c, 6s, 6’’’, 0p,2’’’’. The hypnocyst (Figure 3) is spherical or subspherical and hyaline, with a smooth cyst wall and ornamented with 20-40 slender spines. Spines have capitate ends (Figure 3) and are about ¼ the length of the cyst diameter, though with some variation in length depending on salinity and temperature (Mertens et al. 2010).
There are numerous brown chloroplasts, which often obscure the plates. The longitudinal (trailing) flagellum does not extend very far beyond the antapex. Additional characterizations of morphological variability are found in Hansen et al. (1997) and Hernandez-Becerril et al. (2010). The relationship of P. reticulatum to other toxin producing species, based on molecular genetics, is found in Howard et al. (2009) and Riccardi et al. (2006).
HABITAT & REGIONAL OCCURENCE:
Nearly all records of occurrence are coastal or estuarine. Because of its shape and cryptic plates (due to the reticulation), P. reticulatum is fairly easy to recognize, particularly if cysts are also seen. It is very widely distributed in temperate and tropical areas, and has been recorded from sub-boreal locations in summer (Throndsen et al. 2007). It has also been recorded in the North and South Atlantic, as well as North and South Pacific, and seas associated with the Indian Ocean (e.g. Red Sea). Some older records of its occurrence use Reinecke’s name, Gonyaulax grindleyi.
INDIAN RIVER LAGOON DISTRIBUTION:
In the IRL, this species occurs most often in summer and fall, though apparently not in significant numbers. It is more common in the central IRL than in the northern parts.
Vegetative cells are 28-53 µm in apical length and 25-45 µm in width (literature records). The cysts are about 30-40 µm in diameter.
REPRODUCTION & ABUNDANCE:
Details of the life history have not been adequately investigated. This species is widespread and fairly common throughout the IRL, but rarely in bloom proportions (e.g. more than 106 cells per liter). The hypnocysts have not been verified from the IRL, though they are present on Florida’s west coast. Blooms have been reported from South Africa (as G. grindleyi, Reinicke 1967) and New Zealand.
P. reticulatum is a cause of extensive fish kills due to a group of lipophilic sulphated polyether toxins called yessotoxins (YTX), named after Patinopecten yessoensis, the mollusk in which they were first identified. Yessotoxins were first assumed to be a cause of diarrhetic shellfish poisoning (Paz et al. 2008), but their chemical structure and biological mode of action is different. Although human toxicity of YTZ and its 40+ analogs are unknown, the occurrence of P. reticulatum has been of concern in shellfish aquaculture (Paz et al. 2008). Some shellfish aquaculture facilities have reportedly closed for long periods due to yessotoxins in the shellfish (Guerini et al. 2007). Experiments with zooplankton and field observations have demonstrated the inhibitory properties of yessotoxins on growth, reproduction, and mortality of marine animals (Horstman 1981; Huntley et al. 1986; Makino et al. 2008).
Toxin production appears to be dependent on geographic location and growth conditions (Gallardo Rodríguez et al. 2010). Guerrini et al. (2007) demonstrated toxin increases under P-limitation, but N-limitation produced toxin levels similar to controls. Moreover, their strains of P. reticulatum grew at salinities of 22-42 PSU and temperatures of 16-26 °C. At present no toxin production has been confirmed from IRL strains. Bioluminescence is apparently strain specific and uncommon, but has been reported in some strains (Poupin et al. 1999).
Gallardo Rodríguez, JJ, Sanchez Mirón, A, García Camacho, F, Cerón Garcia, MC, Belarbi, EH & E Molina Grima. 2010. Culture of dinoflagellates in a fed-batch and continuous stirred-tank photobioreactors: Growth, oxidative stress and toxin production. Process Biochem. 45: 660-666.
Guerrini, F, Ciminello, P, Dell’Aversano, C, Tartagione, L, Fattorusso, E, Boni, L & R Pistocchi. 2007. Influence of temperature, salinity and nutrient limitation on yessotoxin production and release by the dinoflagellate Protoceratium reticulatum in batch cultures. Harmful Algae 6: 707-717.