Feeding by Ciliates on Two Harmful Algal Bloom Species, Prymnesium Parvum and Prorocentrum Minimum Carol Holmes Rosetta∗, George B
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Harmful Algae 2 (2003) 109–126 Feeding by ciliates on two harmful algal bloom species, Prymnesium parvum and Prorocentrum minimum Carol Holmes Rosetta∗, George B. McManus Department of Marine Sciences, University of Connecticut, 1080 Shennecossett Road, Groton, CT 06340, USA Received 12 November 2002 ; received in revised form 11 December 2002 ; accepted 6 February 2003 Abstract We have focused on ciliates as potential grazers on toxic phytoplankton because they are major herbivores in aquatic food webs. Ciliates may exert top down control on toxic phytoplankton blooms, potentially suppressing or shortening the duration of harmful algal blooms (HABs). We measured the growth rates of several ciliate species on uni-algal and mixed diets of both HAB and non-HAB algae. The tintinnids Favella ehrenbergii, Eutintinnus pectinis and Metacylis angulata and the non-loricate ciliates Strombidinopsis sp. and Strombidium conicum were isolated from Long Island Sound (LIS), and fed HAB species including the prymnesiophyte Prymnesium parvum (strain 97-20-01) and the dinoflagellate Prorocentrum minimum (strains Exuv and JA 98-01). Ciliates were fed algal prey from cultures at various growth phases and at varying concentrations. We observed no harmful effects of P. minimum (Exuv) on any of the ciliates. However in a comparison of strains, P. minimum (Exuv) supported high growth rates, whereas P. minimum (JA 98-01) supported only nominal growth. P. parvum was acutely toxic to ciliates at high concentrations (2×104–3×104 cells ml−1). At low concentrations (5×103–1×104 cells ml−1), or in culture filtrate, ciliates survived for at least several hours. In mixed diet experiments, as long as a non-toxic alga was available, ciliates survived and at times grew well at concentrations of P. parvum (5 × 102–3 × 104 cells ml−1) that would otherwise have killed them. The present study suggests that prior to the onset of toxicity and bloom formation ciliates may exert grazing pressure on these HAB species, potentially contributing to the suppression or decline of P. minimum and P. parvum blooms. © 2003 Elsevier Science B.V. All rights reserved. Keywords: Ciliates; Grazing; Growth; Growth rates; Harmful algal blooms; Toxic 1. Introduction tory bacteria, or grazing zooplankton (Needler, 1949; Stoecker et al., 1981; Watras et al., 1985; Sellner and Phytoplankton blooms may be dispersed by phys Brownlee, 1990; Imai et al., 1993; Banse, 1994; Jeong ical factors or removed from the water column due and Latz, 1994; Nagasaki et al., 1994a,b; Brussaard to sinking, while mortality of individual cells within et al., 1995, 1996; Buskey et al., 1997; Turner and blooms may be effected by autolysis, viruses, preda Tester, 1997; Yih and Coats, 2000; Lawrence et al., 2001). Microzooplankton grazing of harmful algal bloom species (HABs) is important in two ways; first, ∗ Corresponding author. Tel.: +1-860-405-9089; fax: +1-860-405-9153. grazing may serve to prevent blooms or lessen their E-mail addresses: [email protected], magnitude; second, for toxin producing species, graz [email protected] (C.H. Rosetta). ers may accumulate and subsequently transfer toxins 1568-9883/03/$ – see front matter © 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S1568-9883(03)00019-2 110 C.H. Rosetta, G.B. McManus / Harmful Algae 2 (2003) 109–126 to higher trophic levels (Turner et al., 2000; Maneiro phytoplankton biomass (Stoecker et al., 1981; Watras et al., 2000). et al., 1985; Sellner and Brownlee, 1990; Jeong and It is well established that the microzooplankton (di Latz, 1994). For example, the ciliate microzooplank ameter 20–200 1m) are quantitatively the most impor ter Favella ehrenbergii has been credited with grazing tant grazers of phytoplankton biomass (e.g. Lee and down a Gonyaulax (Alexandrium) tamarense bloom Capriulo, 1990; Gifford, 1991; Cyr and Pace, 1992; in the Bay of Fundy (Needler, 1949). Additionally it is McManus and Ederington-Cantrell, 1992; Pierce and reported that ciliates attain optimal reproduction and Turner, 1992; Breteler et al., 1999; Montagnes and growth rates when fed some HAB species (Gifford, Lessard, 1999). This size class is primarily composed 1985; Stoecker et al., 1986; Kamiyama, 1997; Jeong of metazoan larvae and heterotrophic or mixotrophic et al., 1999). protists, and contains a biomass comparable to The production by phytoplankton of toxins (such as that of larger zooplankton size fractions. Protists okadaic acid, domoic acid and prymnesins) or grazing and other microzooplankters generally have higher deterrents (such as dimethylsulfide (DMS) or acrylic biomass-specific metabolic rates than larger zooplank acid) by phytoplankton, may have lethal or sublethal ton and thus would be expected to have higher commu effects on planktonic consumers and subsequently al nity ingestion and respiration rates. Moreover, many ter the role of grazers, possibly facilitating bloom for organisms in the microzooplankton size fraction have mation (Igarashi et al., 1996; Plumley, 1997; Smayda, growth rates commensurate with those of their phyto 1997; Turner and Tester, 1997; Arzul et al., 1999; plankton prey and hence can respond rapidly to higher Wolfe, 2000; Strom et al., 2003a,b). This is demon phytoplankton growth with higher growth rates of their strated by the acutely toxic effects of some Prym own (Strom and Morello, 1998). Thus, populations of nesium species on cladocerans, crustaceans, isopods microzooplankton and the phytoplankton they feed on and amphipods (Nejstgaard, 1997), compared to the should be more closely coupled than populations of sublethal effects on copepod fecundity and feeding larger phytoplankton and their correspondingly larger (Nejstgaard and Solberg, 1996; Koski et al., 1999). On metazoan grazers (Malone, 1971; Walsh, 1976). the other hand, some zooplankton, including ciliates The observation of closely matched growth rates and copepods, are able to graze on several species of between small grazers and small phytoplankton leads red tide or toxic dinoflagellates, such as Alexandrium to the prediction that blooms of smaller algal species spp., Gymnodinium spp., Prorocentrum minimum and would be more difficult to initiate and sustain unless Heterocapsa circularisquama, without any apparent they can avoid grazing by microzooplankton. This harmful effects (Hansen, 1989; Hansen et al., 1992; prediction is upheld in coastal and estuarine waters at Jeong et al., 1999; Montagnes and Lessard, 1999; mid-latitudes, where annual spring blooms of larger, Kamiyama, 1997; Colin and Dam, 2002; Frangópulos chain-forming diatoms mostly sink to the benthos et al., 2000). It has been suggested that the production ungrazed and smaller, relatively constant levels of of grazing deterrent compounds is widespread among microflagellate biomass dominate through late spring the phytoplankton and that these compounds may re and summer. These latter populations are usually more duce interspecfic competition and grazing pressure, productive per unit biomass and are grazed by micro- thereby facilitating bloom formation (Smayda, 1997; zooplankton at a similarly high rate (Capriulo, 1982; Turner and Tester, 1997; Arzul et al., 1999; Wolfe, Capriulo and Carpenter, 1983; Capriulo and Carpenter, 2000; Strom et al., 2003a,b). 1980; McManus and Ederington-Cantrell, 1992). We examined the effects of two HAB species, The specific role of microzooplankton in graz Prorocentrum minimum and Prymnesium parvum ing blooms of harmful or nuisance phytoplankton is on representative microzooplankton grazers. The poorly known, though it has been suggested that top mixotrophic dinoflagellate P. minimum is a common down control by zooplankton grazers may prevent component of the summer phytoplankton assem bloom formation or shorten the duration of blooms blage in North American coastal waters. Blooms of (Banse, 1994; Buskey et al., 1997; Turner and Tester, it contribute to poor survival, growth and develop 1997). Several studies have reported high grazer con ment of oysters and clams as well as mortality of centrations in blooms with concomitant losses of scallops (Wikfors and Smolowitz, 1993, 1995; Li C.H. Rosetta, G.B. McManus / Harmful Algae 2 (2003) 109–126 111 et al., 1996). Several Prorocentrum species, includ culture (Cembella and Therriault, 1998; Burkholder ing P. minimum, reportedly synthesize okadaic acid et al., 2001). Although this clone is still toxic to bi and are rich in dimethylsulfoniopropionate (DMSP) valves, we wanted to compare its effect on grazers both of which can function as grazing deterrents with that of the more recently isolated and reportedly (Zhou and Fritz, 1994; Wolfe, 2000). P. parvum,a more toxic strain JA 98-01 (Wikfors and Smolowitz, euryhaline species that has been implicated in recent 1993, 1995). Both strains of P. minimum were cultured and historic fish kills around the world exhibits both in 25 ml or 250 ml tissue culture flasks in F/2 growth ichthyotoxic and molluscotoxic properties (Parnas, medium (Guillard, 1975)at20◦ C and 100 1mol pho 1963; Johnsen and Lein, 1989; Hallegraeff, 1993). tons m−2 s−1 in a 12:12 light:dark cycle. The toxins of P. parvum (prymnesin 1 and prymnesin The P. parvum (strain 97-20-01) used in our ex 2) have cytolytic, hemolytic and neurotoxic effects periments was isolated in 1997 from a bloom in (Igarashi et al., 1996, 1999), and toxicity is reported Boothbay Harbor, ME, by R.R.L. Guillard (G. Wik to be variable within and among strains (Johnsen and fors pers com). P. parvum (97-20-01)