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Vertical Migration, Nutrition and Toxicity in the Dinoflagellate Alexandriumtamarense

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Vertical Migration, Nutrition and Toxicity in the Dinoflagellate Alexandriumtamarense MARINE ECOLOGY PROGRESS SERIES l Vol. 148: 201-216.1997 Published March 20 / 1 Mar Ecol Prog Ser Vertical migration, nutrition and toxicity in the dinoflagellate Alexandrium tamarense J. Geoff Mac1ntyre1r*, John J. Cullenl, Allan D. cembella2 'Center for Environmental Observation Technology and Research, Department of Oceanography, Dalhousie University, Halifax, Nova Scotia, Canada B3H 451 'Institute For Marine Biosciences, National Research Council, Haliiax, Nova Scotia, Canada B3H 321 ABSTRACT: The effect of nitrate-N availabil~tyon paralytic shellfish toxin production by the dinofla- gellate Alexandrium tamarense was studied in a vertically stratified laboratory water column (tank) where swimming behavior could influence photosynthes~sand nutrition. Results were compared with those from batch and seml-cont~nuouscultures In wh~chmigratory behavior was not a factor The batch and semi-continuous cultures demonstrated a dlrect posltlve relat~onsh~pbetween N avallablllty and toxln content. Steady-state cultures, maintained at 2 contrasting rates of semi-continuous N supply, also demonstrated significantly diffel-ent cellular toxin profiles (relative proportion of toxlns) The tank experiment was carried out In a 2.1 m PVC cylinder (0.29 m internal d~ameter)and lasted for 24 d. lni- tially, nitrate was replete throughout the water column (50 PM) and the h~ghlytoxic cells fol-med a thin surface layer which persisted throughout the 14 h light:lO h dark cycle. When nltrate was depleted in the surface layer as a result of uptake by the phytoplankton, the cells began a nocturnal migration to the nitracline. During this phase the toxln content of the cells decreased gradually as the C:N of the cells increased. In the third phase, the deep nitrate pool bvas exhausted and the cells penetrated deeper durlng the dark period. The toxln content of the crlls reached the lowest level during this phase. When nitrate was added to the deep layer, a fourth phase began, dur~ngwhich nocturnal descent of the rnigratlng cells was again restricted to the nitracline; toxicity of the cells increased and C:N declined. Finally, N was added to the surface layer. During this flfth and final phase, cellular tox~citycontinued to rlse, C:N declined further, and the cells continued to mlgrate to the thermocline dur~ngthe dark period. The toxicity of the cells during the N-stratified phases of the water column exper~mentwas ~ntermediatebetween the N-replete and N-depleted phases, indicating that A. tamarense is capable of producing PSP toxins from N acquired during a nocturnal descent. It is concluded that toxic dinofla- gellates inhabiting N-depleted coastal waters are likely capable of sustaining growth and a moderate level of toxicity through nocturnal migrations to deep N pools. KEY WORDS: Alexandr~i~mtamarense PSP Vertlcal migration . Nitrogen . D~noflagellate. Toxin profile . N-stratified . Red-t~de INTRODUCTION (White et al. 1992, Busto et al. 1993). A better under- standing of the ecophysiology of toxin producers, as Paralytic Shellfish Poisoning (PSP) is a severe afflic- well as the factors and relationships involved in the tion of the vertebrate nervous system caused by the production of PSP toxins, is required to more effec- ingestion of shellfish or finfish which have consumed tively manage coastal waters where PSP is a factor dinoflagellates that produce PSP toxlns. A single inci- Dinoflagellates of the genus Alexandrium have been dence of PSP can cause closure of shellfish ha.rvesting implicated as causative organisms in PSP around the over widespread areas, eliminating both an important world and they pose a widespread threat to shellfish source of income and a valuable source of protein and finfish resources. The toxin content of such PSP producing phytoplankton is known to vary with envi- ronmental conditions such as salinity (White 1978), 0 Inter-Research 1997 Resale of ill11 artlrle not permitted Mar Ecol Prog Ser 148: 201-216, 1997 temperature (Anderson et al. 1990b),photon flux den- in working out relationships between nutrition and sity (Ogata et al. 1987) and nutrient levels (Boyer et al. toxicity (Boyer et al. 1987, Anderson et al. 1990b),cul- 1987, Anderson et al. 1990b, Flynn et al. 1994) and also tures in small containers clearly cannot be used to with growth stage (Boczar et al. 1988), growth rate study the consequences of vertical migration through (Ogata et al. 1987) and cell cycle (Anderson 1990). gradients of light, temperature and nutrients. Here, we Although studies have shown a strong relationship describe an experiment in a laboratory water column between phosphorus limitation and toxicity (Boyer et that was designed to elucidate both the pattern of al. 1987, Anderson et al. 1990b), we focus here on the DVM as influenced by the distribution of nitrate and its positive relationship between inorganic N availability effects on toxicity in Alexandrium tamarense. In addi- and PSP toxin content in toxic dinoflagellates of the tion to presenting such results for the first time, the genus Alexandrium (Boyer et al. 1987, Anderson et al. effects of N starvation in batch cultures and N limita- 1990b, Flynn et al. 1994). Because toxic dinoflagellates tion in semi-continuous cultures are re-examined with typically inhabit coastal nearshore areas (Cembella & a new focus. Therriault 1989, Iwasaki 1989) which are frequently limited by nitrogen (Ryther & Dunstan 1971, Boekel et al. 1992; but see Sakshaug & Jensen 1971 concerning MATERIALS AND METHODS phosphorus-limited fjords), and periodically N strati- fied, the relationship between toxin content and N lim- Nitrate-stratified laboratory water column. To ex- itation is relevant in nature and needs to be further amine the relationships between behavior, nutrition understood. and toxicity, a thermally stratified water column Several species of dinoflagellates are known to per- (Fig. 1) was established in a single opaque polyvinyl form diel vertical migrations (DVM) through gradients chloride (PVC) cylinder 2.10 m in height with an inter- of nutrients and temperature in both natural (Eppley & nal diameter of 0.29 m (Heaney & Eppley 1981). The Harrison 1975, Kiefer & Lasker 1975, Blasco 1978) and tank was in an environmentally controlled room at a laboratory conditions (Eppley et al. 1968, Cullen & temperature of -17°C. A thermocline was established Horrigan 1981, Heaney & Eppley 1981, Kamykowski and maintained using a temperature-controlled, circu- 1981, Cullen et al. 1985, Rasmussen & Richardson lating water bath (5°C)to cool the bottom 100 cm of the 1989, Santos & Carretto 1992). Migrational behavior tank. Temperature ranged from approximately 17.0°C consequently enables dinoflagellates to utilize deep N at the surface to 7.4"C at the bottom with the major pools (Fraga et al. 1992) and confers some competitive thermocline occurring between 100 and 140 cm depth advantage for phytoplankton in N-depleted surface with a 6 to ?'C decrease in temperature. Irradiance waters (Holmes et al. 1967).Thus, N-stratified coastal was provided by a 250 W metal halide lamp on a 14 h waters with a steep thermocline provide an environ- ment which is suitable for bloom formation by verti- cally migrating dinoflagellates. Although the toxic L~ghrsource L dinoflagellate Alexandrium tamarense does not reach Hear [rap high standing stocks generally, it is known to form dense near-surface populations in coastal waters (Sak- Acrylic cover - shaug & Jensen 1971, Anderson & Stolzenbach 1985, Iwasaki 1989, Carretto et al. 1990, Esteves et al. 1992, Rensel 1993) and has demonstrated directed swim- lnsulat~ng ming ability in laboratory conditions (Rasmussen & blanker Richardson 1989, Santos & Carreto 1992); conse- quently, we hypothesize that this species has the abil- i PVC column f ity to migrate vertically to deep pools of nitrogen. Given the effects of nutrition on the toxicity of A. tamarense, a diel migration between high and low lev- els of N availability by this toxic dinoflagellate might influence cellular toxicity in a manner that could not be simulated in conventional lab experiments. D~tcrcreanalyses Although behavior seems likely to have a large influ- ence on the ecophysiology of dinoflagellate popula- tions in nature, such effects on the toxicity of dinofla- gellates have yet to be addressed. While conventional laboratory experiments have proved extremely useful Fig. 1. Laboratory water column used for tank experiment MacIntyre et al.: Migration, nutrition and toxic~tyin Alexandrium tamarense 203 1ight:lO h dark cycle with the light period from 08:OO to Day 21, 1.5 l of the N-rich replacement medium was 22:OO h. Irradiance, measured in situ (prior to inocula- added to the surface layer. tion) with a Li-Cor (Li 185B) 417 PAR photometer, The experiment ran for 24 d with samples taken ranged from 390 pm01 quanta m-2 S-' at the surface to twice daily at 03:OO h (middle of the dark period) and 17.5 pm01 quanta m-2 S-' at the bottom. Enriched sea- 14:OO h (middle of the light period) for the first week. water (K medium; Keller et al. 1987), with NO3- and Once vertical migration of the cells began, sampling concentrations modified to 50 pM and 20 pM was increased to 4 times daily to include samples at the respectively, was sterile-filtered (0.2 pm Gelman Cul- end of the light and dark periods, giving samples at ture Capsule filter) directly into the tank. An inoculum 02:00, 07:00, 14:00,and 21:OO h for the remainder of the consisting of seven 1 1 cultures of exponentially grow- experiment. Due to a suspicion that N was recycling ing Alexandrium tamarense (Prl8b), a highly toxic near the bottom of the tank (Heaney & Eppley 1981), strain isolated from the lower St. Lawrence estuary in samples for NH,' analysis were collected, filtered eastern Canada, was grown at 140 pm01 quanta m-2 S-' (Whatman GFC) and frozen at 21:OO h on Day 17 of the on a 14 h 1ight:lO h dark cycle in K medium.
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