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Pfiesteria piscicida Steidinger et al., 1996

Species Overview:

Pfiesteria piscicida is a putatively toxic dinoflagellate species with flagellated and cyst stages. This species, dubbed the 'ambush predator', was first observed in the Pamlico Sound, North Carolina, USA, in 1991 after a massive fish kill. Pfiesteria piscicida has been associated with fish kills, and then feeds on the dead prey (Burkholder et al., 1992, Burkholder et al., 1995, Steidinger et al., 1996).

Taxonomic Description:

Pfiesteria piscicida is a polymorphic and multiphasic dinoflagellate species with a number of unicellular stages throughout its life cycle: bi- and triflagellated zoospores, and nonmotile cyst stages. Within the different life stage forms there is a wide range in size and morphology (Steidinger et al., 1996).

The flagellated stages are small and oblong thecate cells that resemble gymnodinioid cells, although they are actually small cryptic peridinioid cells (Figs. 1-3). The biflagellated stages, zoospores, have two size groups: 5-8 µm (gametes) and 10-18 µm (vegetative)(Fig. 3). The larger triflagellated stage, 25-60 µm, is a planozygote with the features of a vegetative cell along with one transverse and two longitudinal flagella (Fig. 4). Cyst stages, with highly resistant cell walls, range in size from 25-33 µm (Fig. 5). The flagellated forms are typically planktonic and ephemeral, whereas the cyst stages are benthic (Steidinger et al., 1996).

Thecal Plate Description:

The biflagellated stages of P. piscicida have thin thecal plates with a plate formula unique to the Dinophyceae: Po, cp, X, 4', 1a, 5'', 6c, 4s, 5''', 2'''' (Figs. 7-10). Raised sutures designate plate tabulation (Fig. 6). Thecal nodules border plate sutures (Figs. 7,9). Theca is smooth with scattered pores; trichocysts are present. The epitheca is equal to or exceeds the hypotheca in height (Figs. 1,6). The apical pore complex (APC) houses a broadly ovate apical pore plate (Po) and closing plate (cp) (Figs. 7,8). The elongate canal plate (X plate) is at a slight angle to the APC (Figs. 7,8). The first apical plate (1') is rhomboid in shape (Fig. 8). The broad and shallow cingulum is without lists, and descends almost 1 time its width. The sulcus is excavated, without lists, descends to the right, and slightly invades the epitheca via the anterior sulcal plate (s.a.)(Figs. 1,9) (Steidinger et al., 1996).

Morphology and Structure:

P. piscicida exhibits a number of different life cycle stages. This species uses both heterotrophic and mixotrophic nutritional modes depending on the life stage. Flagellated stages are mixotrophic: they use a peduncle (Figs. 1,2) to capture and ingest prey (myzocytosis), and kleptochloroplasts (chloroplasts retained from ingested algal prey) to photosynthesize when prey supply is low. Large food vacuoles are often found in the epitheca, the mesokaryotic nucleus is located in the hypotheca (Schnepf et al., 1989, Elbrächter, 1991, Fields and Rhodes, 1991, Stoecker, 1991, Steidinger et al., 1996, Lewitus et al., 1999).

Reproduction:

Biflagellated zoospores reproduce asexually via temporary cysts. Sexual reproduction has also been documented for this species: biflagellated zoospores produce anisogamous gametes (Fig. 3), which fuse to produce triflagellated planozygotes (two longitudinal flagella and one transverse) (Fig. 4). Sexual and asexual reproduction can occur on either a fish or algal diet (P.A. Tester, pers. com.).

Species Comparisons:

P. piscicida is a distinct free-living estuarine dinoflagellate (Fensome et al., 1993, Burkholder and Glasgow, 1995, Burkholder and Glasgow, 1997).

Ecology and Toxicity:

P. piscicida is an estuarine species with a wide temperature and salinity tolerance. A cryptic heterotrophic species, it is a prey generalist that feeds on bacteria, algae, microfauna, finfish and shellfish, and may well represent a significant estuarine microbial predator. Feeding mode is governed by the presence or absence of fish and fish material. Life cycle stage is governed by the presence of live or dead fish (Burkholder et al., 1995, Burkholder and Glasgow, 1997).

In the absence of fish, biflagellated stages feed myzocytotically on bacteria, algae and microfauna; i.e. prey is suctioned into a food vacuole via a feeding tube or peduncle (Fig. 2), and then digested (Burkholder and Glasgow, 1995, Glasgow et al., 1998). Similar to other heterotrophic dinoflagellate species, a large food vacuole allows P. piscicida to phagocytize large prey items (Gaines and Elbrachter, 1987, Schnepf and Elbrachter, 1992, Burkholder et al., 1998).

Pfiesteria piscicida is a strong ichthyotoxic dinoflagellate species: in the presence of live fish, P. piscicida's behavior is stimulated by a chemosensory cue, an unknown substance in fish secreta/excreta. Benthic stages (Fig. 6) then rapidly emerge as flagellated forms that swarm, immobilize, and kill the prey. Some prey experience ulcerative fish disease (open skin lesions) before dying (Fig. 11). P. piscicida is lethal to fish at relatively low concentrations (> 250-300 cells/ml). At lower levels (~100-250 cells/ml) ulcerative fish disease results. Similar ulcers have been reported from shellfish as well. After a kill benthic stages form which inconspicuously descend back to the sediments (Burkholder and Glasgow, 1995, Burkholder et al., 1995, Noga et al., 1996, Steidinger et al., 1996, Burkholder and Glasgow, 1997, Burkholder et al., 1998).

P. piscicida and possibly other Pfiesteria-like species are suspected to be responsible for a number of major fish and shellfish kills in the North Carolina Albemarle-Pamlico estuary, and in the Maryland Chesapeake Bay (Burkholder et al., 1995, Burkholder and Glasgow, 1997). The ever changing morphology of this species may give answers to a number of mysterious fish kills along the southeast coast of the United States (Steidinger et al., 1996).

This species was initially linked to serious health problems in humans who had come in direct contact with it (narcosis, respiratory distress, epidermal lesions, and short-term memory loss); however, a study sponsored by the Centers for Disease Control (CDC) has revealed no such relationship (Swinker et al., 2001). Other CDC-funded studies are currently addressing possible associated human health problems with Pfiesteria and Pfiesteria-like species in several states, including Maryland and North Carolina (P.A. Tester, pers. com.).

Habitat and Locality:

Pfiesteria piscicida was first identified from the Pamlico Sound in North Carolina. Since its emergence; however, and Pfiesteria-like species have been reported from other eutrophic, temperate to subtropical estuarine systems in the eastern United States: from Delaware inland bays to Mobile Bay, Alabama (Burkholder et al., 1993, Burkholder et al., 1995, Lewitus et al., 1995). This natural range is expected to expand, considering the warming trend in global climate, and the increased human impact on coastal areas resulting in decreased water quality (Smayda, 1992, Adler et al., 1993, Epstein et al., 1994, Hallegraeff, 1993, Burkholder and Glasgow, 1997).

Pfiesteria piscicida