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Pfiesteria Piscicida and P Journal of Experimental Marine Biology and Ecology 264Ž. 2001 29–45 www.elsevier.comrlocaterjembe Chemosensory attraction of zoospores of the estuarine dinoflagellates, Pfiesteria piscicida and P. shumwayae, to finfish mucus and excreta Paul J. Cancellieri, JoAnn M. Burkholder ), Nora J. Deamer-Melia, Howard B. Glasgow Center for Applied Aquatic Ecology, North Carolina State UniÕersity, 620 Hutton St., Suite 104, Raleigh, NC 27606, USA Received 26 October 2000; received in revised form 13 November 2000; accepted 21 May 2001 Abstract Toxic strains of the estuarine dinoflagellates, Pfiesteria piscicida and P. shumwayae, can cause fish death and disease, whereas other estuarine ‘lookalike’ species such as cryptoperidiniop- soids have not been ichthyotoxic under ecologically relevant conditions. Chemosensory attraction of three functional types of these Pfiesteria spp. were separately evaluated for their attraction to fresh fish mucus and excreta. Clonal cultures of actively toxicŽ. TOX-A, engaged in killing fish and temporarily nontoxicŽ tested as toxic but without access to live fish for )1 week to 5 months Ž.in most experiments, F3 months as ‘short-duration’ TOX-B; and without access to live fish for G1.5 years as ‘long-duration’ TOX-B. functional types of P. piscicida and P. shumwayae were derived from the same clones whereas the non-inducible culturesŽ NON-IND, tested as incapable of toxic activity in the presence of fish. , of necessity, were from different clonal isolates. NON-IND cultures previously had been grown on algal prey for 3–8 months, and had repeatedly been tested as incapable of causing fish distress, disease or death via toxic activity. Attraction to fish materials was based on the number of zoospores that entered microcapillary tubes containing sterile-filtered 15-ppt waterŽ. controls , vs. entry into tubes with sterile-filtered mucus and excreta Ž.collected in 15-ppt water that had been collected from live tilapia, bluegill, hybrid striped bass, and Atlantic menhadenŽ. tested separately within 3 h of removal from live fish . TOX-A zoospores of both Pfiesteria species exhibited the strongest attraction to the fish mucus and excreta, with comparable response to the materials from all four test fish species. Short-duration TOX-B zoospores showed an intermediate response that apparently depended on the duration of mucus separation from the live fish: the shorter the separation period, the stronger the zoospore attraction ) Corresponding author. Tel.: q1-919-515-2726; fax: q1-919-513-3194. E-mail address: joann– [email protected]Ž. J.M. Burkholder . 0022-0981r01r$ - see front matter q2001 Elsevier Science B.V. All rights reserved. PII: S0022-0981Ž. 01 00299-4 30 P.J. Cancellieri et al.rJ. Exp. Mar. Biol. Ecol. 264() 2001 29–45 to the fish materials. In contrast to TOX-A and short-duration TOX-B zoospores, NON-IND and long-duration TOX-B zoospores generally showed little or no response to the fish materials. Zoospores of the cryptoperidiniopsoid demonstrated a moderate attraction that did not appear to depend on the time of isolation from fish. TOX-A zoospores were also tested for attraction to sterile-filtered vs. non-filtered fish mucusŽ. time separated from the live animal, 3–96 h . These zoospores, which initially had been actively attracted, were no longer attracted to the unfiltered fish materials after 48 h, whereas attraction to the sterile-filtered fish mucus and excreta persisted throughout the duration of the experiment. Thus, the attractant signal in the materials was degraded or effectively blocked by the bacterial community within hours of isolation from live fish. This study indicates the importance of functional type or toxicity status, and the importance of the history of exposure to live fish, in the behavioral ecology of Pfiesteria spp. Initial attraction to fish materials strongly depended on the functional type, and on the history of toxic activity. Non-inducible and long-duration TOX-B cultures of Pfiesteria spp., unlike actively toxic and short-duration TOX-BŽ. potentially toxic strains, initially were virtually unresponsive to fish mucus. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Chemosensory; Functional type; Estuary; Fish; Mucus; Non-inducible; Toxic dinoflagellate; Toxic Pfiesteria complex; Cryptoperidiniopsoid 1. Introduction Dinoflagellates within the genus Pfiesteria Žtwo species known thus far, P. piscicida Steidinger & Burkholder and P. shumwayae Glasgow and Burkholder. form the toxic Pfiesteria complexŽ. TPC; Glasgow et al., 2001; Burkholder et al., 2001 . Their ichthyotoxic strains have been implicated as primary and secondary causative agents of certain major fish kills and fish epizootic in the largest and second largest estuaries on the US mainlandŽ Chesapeake Bay and the Albemarle-Pamlico Estuarine System, respectively; Burkholder et al., 1992; Burkholder and Glasgow, 1997. They are stimulated to produce toxin by live fish or their fresh secretarexcreta and tissues Ž.Burkholder and Glasgow, 1997 , to which they are strongly attracted Ž Pfiesteria Interagency Coordination Working Groupwx PICWG , 2001; Burkholder et al., 2001. Toxic strains of Pfiesteria spp. have a complex life cycle including an array of flagellated, amoeboid, and cyst stagesŽ Burkholder and Glasgow, 1995; Steidinger et al., 1996. The presence of live fish stimulates amoebae and cysts to produce toxic zoospores, and nontoxic zoospores to become toxicŽ Burkholder and Glasgow, 1995, 1997; Burkholder et al., 2001. On the basis of repeated observations of Pfiesteria toxicity in the presence vs. absence of fishŽ. Burkholder et al., 1992, 1995; Burkholder and Glasgow, 1997 , three functional types of Pfiesteria zoospores have been definedŽ. Burkholder et al., 2001 . TOX-A zoospores are actively toxic, and are found in the presence of live fish Ž.Burkholder and Glasgow, 1997; PICWG, 2001 . Within hours of separation from fish prey, zoospore toxicity diminishes, then is re-induced after additional exposure to fish Ž.Burkholder and Glasgow, 1997 . TOX-B zoospores are capable of toxicity, but cease toxin production in the absence of live fish and prey on other organisms such as bacteria and algae. This functional type has been described as temporarily nontoxicŽ Burkholder and Glasgow, 1997.Ž , although it may retain negligible or residual toxicity Springer, P.J. Cancellieri et al.rJ. Exp. Mar. Biol. Ecol. 264() 2001 29–45 31 2000.Ž . As in many other toxic algal species here, including heterotrophic dinoflagel- lates; e.g., Anderson, 1990; Gentien and Arzul, 1990; Bates et al., 1998; Edvardsen and Paasche, 1998.Ž , non-inducible strains NON-IND functional type . of both Pfiesteria spp. have been isolated. These strains are apparently incapable of toxin production based on present knowledge about toxicity, although molecular controls that can re-initiate toxin production in this functional type may eventually be foundŽ Burkholder et al., 2001. As a separate phenomenon and an artifact of culture conditions, toxic strains become non-inducible, or lose toxin-producing ability, after extended culture with fish Ž.typically, G6 months , accelerated when Pfiesteria is given other prey in the absence of fishŽ. toxicity loss in most clonal cultures within G6 weeks . Other researchers have described Pfiesteria lookalike speciesŽ term, APfiesteria-likeB as used by Steidinger et al., 1996; Litaker et al., 1999; Seaborn et al., 1999; Marshall et al., 2000. that have been informally named as ‘shepherd’s crook,’ ‘Lucie’, and Cryptoperidiniopsis gen. ined. Že.g., C. brodyii gen. et sp. ined.; Dr. K. Steidinger, Department of Environmental Protection, Florida Marine Research Institute, St. Petersburg, FL, USA, personal com- munication. These organisms have been present in estuaries where Pfiesteria spp. have been documented. Unlike toxic strains of Pfiesteria spp., thus far none of the lookalike species have been ichthyotoxic under ecologically relevant conditionsŽ live or sonicated cells and fish in the standardized fish bioassay process, at similar densities as found under field conditions; Marshall et al., 2000; Burkholder et al., 2001. Our research team has sought to compare the two known toxic Pfiesteria spp. and lookalike species by investigating their cellular and behavioral differences in response to various environmen- tal stimuli. Toxic Pfiesteria outbreaks require that benthic and suspended stages of TPC species Ž.amoebae and cysts, and TOX-B zoospores, respectively producertransform to actively toxic zoosporesŽ. TOX-A functional type when sufficient live fish are detectedŽ Burk- holder and Glasgow, 1997; Burkholder et al., 1999. TPC zoospores have shown positive chemotaxis toward fresh fish tissues in laboratory trials; therefore, it is expected that toxic strains of TPC zoospores exhibit positive chemotaxis toward fish and their fresh secreta in estuarine watersŽ. Burkholder and Glasgow, 1997 . The stimulatory substance in fish materials is believed to be a water-soluble chemical released by live fish, including potential candidates within methylamines, methylaminoxides, mucus proteins, or mucopolysaccharidesŽ Burkholder et al., 1995; Burkholder and Glasgow, 1997; Boriss et al., 1999. Fresh fish secreta has been documented to affect aquatic microfauna other than dinoflagellates. For example, zooplankton species respond to glycosaminoglycans in fish mucus, which induce life cycle changes and migratory activity as defenses against the fish predatorsŽ. Forward and Rittschof, 1999, 2000 . In Pfiesteria,
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