WHOI-R-94-005 Anderson, D.M. Biogeograph

Marine Biology ( 1994) 120:467-478 © Springer-Ve rl ag 1994 D. M. Anderson · D. M. Kulis · G. J. Doucette J. C. Gall agher · E. Balech Biogeography of toxic dinoflagellates in the genus Alexandriu~ #l from the northeastern United States and Canada Received: II April 1994 I Accepted: 20 June 1994 Abstract Twenty-eight strains of toxic dinoflagell ates in widespread, homogeneous populati on, but rather is com the genus Alexandrium from the northeastern Uni ted States prised of several sub-populati ons, each with its own phys and Canada were characterized on the basis of morphol iological characteri tics and hi story. Two ce narios are ogy, biolu minesce nce capacity, mating compatibil ity, and considered with respect to this regiona l biogeography. The toxin composition. T he distributions of these characters first invokes recent and continuin g dispersal of isolates to were evaluated in the context of regional patterns of para the south from a center of origin in the north, fo ll owed by lytic hell fi sh poisoning (PSP) and coastal hydrography. recombination and strong selection. The second holds that Two morphospecies were identified - A. tamarense Lebour the northern and southern popul ati ons di verged from a and A. j imdyense Balech. The two are interspersed geo common ancestor (vicari ance), but now repre ent localized graphicall y though there are areas, such as the Gulf of population with little mixing of genotypes. Neither hy Maine, where apparently only A.f undyense occurs. South pothesis can be comp lete ly refuted by the data presented ern waters (Cape Cod, Connecticut, and Long Island) have here, though the weight of the evidence favors the latter. especiall y diverse populations. The two species are sexu The correct cenario may be a combination of both, with ally compatible. Virtua ll y all northern i olates are biolu recent and continuous spreading occuring within the G ulf minescent, whereas southern isolates inc lude biolumines of Mai ne and perphaps the Gulf of St. Lawrence, but with cent and non-bioluminescent strains. Cluster analyses, endemic localized populations persisting without geneti c based on high performance li quid chromatography (HPLC) exchange in most outhern locations. T hese data also in determinati ons of the sui te of toxins produced by each iso dicate that although morphological cri te ri a separate toxi c late, revealed two and perhaps three distinct groups. One Alexandrium isolates from the study region into two mor is comprised almost exc lu ively of northe rn strains, and phospecies, these as ignments do not coincide with c lu - the other of southern strains. A Cape Cod c lu ster may be terings based on toxin compo ition or a ll ozyme electro separable from the south ern group. These analy es explai n phoresis, and they are further violated by mating results. a previously reported north-to-south trend of decreasing A revision of taxon designations to the varietal level could Lox icity, a the northern isolates produce greater propor be justified. ti ons of the more potent toxins than do southern forms. The overall perspective is that the biogeography of toxic Alex andrium spp. in the study region is not that o f a single, Introduction Communicated by J. P. Grassle, New Brunswick Some species in the dinofl agell ate genus Alexandrium pro 1 D. M. Ande r so n ( ~)· D. M. Kulis· G. J. Doucette duce pote nt neurotoxins which are well known because Biology Department, Woods Hole Oceanographi c Institution, Woods Hole, Ma. sachusetts 02543. USA they cause paralyti c he ll fish poisoning (PSP), a syndrome of human illness and death foll owing the consumpti on of I 1. C. Gallagher Biology Department. City College of CUNY, contaminated shell fish. Alexandrium spp. toxins a lso move I 38th St. at Convent Ave .. New York, to other levels of the food chain. impacting zooplankton, New York I 003 I , USA fish, and e ven marine mammals. PSP is a global phe nom E. Balech enon that affects many coastal coun tries. Along the west Casilla de Correo 64. 7630 ecochea, Argentina ern Atlantic, it represents a real or potential threat from 1 New Je rsey in the United States north to the Sr. Lawrence Present address: National Marine Fisheries Service, Southeast Fisheries Science Center. C harleston Laboratory, P.O. Box 12607, estuary and Newfoundland in Canada (Fig. I A). She ll fish C harleston, South Carolina 29422, USA toxic ity ha been a problem for hundreds of years in east- 468 Lawrence (Cembella et al. 1988), as well as in scattered A Canada locations on ewfoundland (White and White 1985). Far to the south, toxic Alexandrium spp. blooms occur in iso so· lated embayments and estuari es in Cape Cod, Connecticut, Long Island, and New Jersey (Anderson et al. 1982; Schrey et al. 1984; Cohn et al. 1988) and PSP has recentl y been detected at hi gh levels in offshore shellfish on Georges ' Bank (White et a l. 1993). Between these southern and northern extremes, the Gulf of Maine (inc luding the mid dle and lower reaches of the Bay of Fundy) experiences United States PSP along virtually its entire coastline. Toxicity is local ized and infrequent along the eastern coast of Nova Scotia. There is considerable potential for genetic exchange among Alexandrium spp. popul ations fo r two reasons. First, the organi sms undergo a sexual phase resulting in the 70° so• production of re istant, overwintering cysts during the late stages of blooms (A nder on and Wa ll 1978). Furthermore , the areas affected by PSP are linked hydrographicall y B Canada (Smith and Schwing 199 1) and there is a general north-to south fl ow in the region (Fig. I B). orth of Cape Cod. 50' Alexandrium spp. blooms are geographically widespread phenomena, affecting hundreds of kil ometers of coastline (Cembe lla et al. 1988; Martin and W hite 1988; Franks and Anderson 1992), facilitating populati on dispersal over large distances. In contrast, southern blooms are locali zed within shallow e mbayments and estuaries (Anderson et al. United 1982; Schrey et al. 1984) . with little or no exchange with States local coastal waters. Little is known of the geneti c and ecological relati on shi ps that link different populations of Alexandrium spp. within this large region. Whether the 1972 outbreak was large enough to disper e these pecie as far south as Con 70° so· necticut or New Jersey in one spreading event is uncertain, nor is it known whether toxic Alexandrium specie were Fig. 1 T he study region. A Origins of the isolates examined in the present study. Strain names fol lowed by " F" or "T". designating Alex present in southern waters prior to that date , or whether andrium flmdyense and A. tamarense, respecti vely. B General pat there have been spreading events on a smaller scale since tern of non-tidal surface circulation in the study region (arrows). 1972. The first compari son of regional Alexandrium spp. Coastline areas affected by paralytic shellfish poisoning (PSP) are populations was a survey of the toxin content of isolates blac ke ned. Not shown: PSP toxicity also occurs in offshore shell fish within the central Gul f of Maine. on Georges Bank, and Nantucket originating between Nova Scotia and New York (Maranda Shoals (located j ust to the west of Georges Bank). Qualitati ve now et al. 1985). That study revealed a systematic decrease in patterns deri ved in part from Smith and Schwing ( 199 1) and re fer toxic ity from north to south, an o bservation that appears e nces therein inconsistent with the hypothesized recent dispersal of toxic cells from a common source during the 1972 bloom. Are search program was establ ished to compare isolates from ern Ca nada, but the western Gulf of Maine and areas fu r throughout the region using fi ve differe nt characters: mor the r so uth have only been affected during the last two phology. mating compatibility. bioluminescence capacity, decade. (P rakash et al. 197 1; A nderson e t al. 1982). A toxin composition. and all ozyme e lectrophoresis. Electro com mon belief is that the recent history of PSP in south phoretic results are given by Hayhome et al. ( 1989). Here ern waters reflects the di spersal of Alexandrium spp. from we present informati on on the other character and provide e ndemic populati ons in the north during a massive 1972 an overview o f the entire study. red tide, an event whi ch caused PS P toxicity for the fi rst time in southern New England (Hartwe ll 1975). She ll fi sh toxic ity is now a recurrent annual p roble m in the e previ Materials and methods ously una ffected area . PSP is not evenly distributed throughout the region (Fig. Isolation and culture I B). At the northern extreme, it is associated with she ll Twenty-eight clones of Alexandrium tamarense and A. frm dyense fish along the lower estuary of the St. Lawre nce Ri ver, in from waters between the Gulf of St. Lawrence. Canada and Long Is c luding the Gaspe peninsula a nd the western Gulf of Sl. land, NY were established in culwre (Table I). GT2 and GT7 were 469 Table I Alexam/rium ramarense and A. ftmdyense. List of i ~o l a t es and their characteristics. ordered from north-to-south. (a archived sam ple. Due to evaporatio n and chemical conversio ns during long-te rm ~ t orage . toxin contents not reported) Clo ne Species Locatio n Toxi n Biolum (fmol ce11 )1 (fgST X cell ) ATSLI2 A.

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