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Home , Amphidinium, Blastodinium, Ceratium, Ceratium furca, Ciliate, Gambierdiscus

J Eukaryn Microbiol.. 46(4). 1999 pp. 397-401 0 1999 by the Society of Protozoologists Mixotrophy among ’

DIANE K. STOECKER University of Maryland Center for Environmentul Science, Horn Point Laboratory, P.O. Box 775, Cambridge, Marylund 21613, USA

ABSTRACT. Mixotrophy, used herein for the combination of phototrophy and phagotrophy, is widespread among dinoflagellates. It occurs among most, perhaps all, of the extant orders, including the , Dinophysiales, , , Gon- yaulacales, , , Phytodiniales, and Dinamoebales. Many cases of mixotrophy among dinoflagellates are probably undocumented. Primarily photosynthetic dinoflagellates with their “own” plastids can often supplement their nutrition by preying on other cells. Some primarily phagotrophic species are photosynthetic due to the presence of kleptochloroplasts or algal . Some parasitic dinoflagellates have plastids and are probably mixotrophic. For most mixotrophic dinoflagellates, the relative importance of , uptake of dissolved inorganic nutrients, and feeding are unknown. However, it is apparent that mixotrophy has different functions in different physiological types of dinoflagellates. Data on the simultaneous regulation of photosynthesis, assimilation of dissolved inorganic and organic nutrients, and phagotophy by environmental parameters (irradiance, availablity of dissolved nutrients, availability of prey) and by history events are needed in order to understand the diverse roles of mixotrophy in dinoflagellates. Key Words. Endosymbioses, harmful algal blooms, kleptoplastidy, .

INOFLAGELLATES have traditionally been categorized Smalley, G. W., unpubl. data) or are specialized predators on D as autotrophic or heterotrophic, based on the presence or particular types of live prey (Bockstahler and Coats 1993a, b; absence of chlorophyll and plastids. It has long been recognized Jacobson and Anderson 1996; Skovgaard 1996a; Smalley, that some photosynthetic dinoflagellates have food and Coats and Adam 1999). Conversely, reports of ingestion of bac- feed on other (Biecheler 1936, 1952); however, only terial-size prey by dinoflagellates, including photosynthetic spe- recently has the prevalence of feeding among common photo- cies, are questionable because dinoflagellates prey on relatively synthetic dinoflagellates been documented (Bockstahler and large-size particles and absorption of prey on surfaces or uptake Coats 1993b; Jacobson and Anderson 1996; Li et al. 1996; of dissolved label may have confounded the results (Hansen Stoecker et al. 1997). Likewise, it has long been known that 1998; Hansen and Calado 1999). However, many new cases of some dinoflagellates have plastids with pigment and membrane mixotrophy among dinoflagellates remain to be discovered. characteristics not typical of dinoflagellates, but recent inves- Among the Prorocentrales, food vacuoles or the ingestion of tigations have shown that some of these atypical species harbor prey have been observed in one common bloom-forming pho- kleptochloroplasts or algal endosymbionts obtained from non- tosynthetic species, Prorocentrum minimum (Stoecker et al. prey (Fields and Rhodes 1991; Larsen 1988; Stei- 1997) and in several tropical, benthic Prorocentrum spp. (Table dinger et al. 1996; Steidinger and Tangen 1997; Sweeney 1976). 1). In natural assemblages, ingested cryptophyte material has In some cases, it has been demonstrated that dinoflagellates been observed in up to 50% of the P. minimum cells. In this with kleptochloroplasts are photosynthetically functional (Skov- primarily phototrophic species, feeding may be a response to gaard 1998) or that the dinoflagellates can grow for several days inorganic nutrient limitation during summer stratification of the in the light but not in the dark in the absence of prey, indicating water column (Stoecker et al. 1997). that the plastids/endosymbionts are functional and benefit the Among the Dinophysiales, food vacuoles have been observed host (Fields and Rhodes 1991; Skovgaard 1998; Sweeney in two photosynthetic species, acuminata and D. 1971). However, most cases of feeding by photosynthetic di- nowegica (Jacobson and Andersen 1994). It has been argued noflagellates and of plastid-retention and endosymbiosis in di- that the Dinophysiales are a basically heterotrophic lineage in noflagellates have not been experimentally investigated, and the which some taxa have secondarily acquired photosynthetic or- relative contributions of phototrophy (photosynthesis and up- ganelles or photosynthetic endosymbionts (Schnepf and El- take of inorganic nutrients) and phagotrophy to survival and brachter 1988). Thus, feeding is expected to be common among growth are largely unknown. Mixotrophy (used herein in the the photosynthetic members of this order. restricted sense for the combination of phototropy and phago- Among the Gymnodiniales, there is evidence for mixotrophy trophy) is a common, but physiologically and ecologically di- in many genera (Table I). latum, Amphidinium verse phenomenon among many taxa of marine and freshwater poecilochroum, acidotum, Gymnodinium ‘graci- protists (Jones 1997; Jones 1994; Raven 1997; Reimann et al. lentum, ’ and possibly Gymnodinium aeruginosum lack their 1995; Sanders 1991; Stoecker 1998). “own” plastids and are phagotrophic, but retain kleptochloro- are reported among all the major extant orders plasts or reduced algal endosymbionts, which are usually de- of dinoflagellates, although evidence for mixotrophy is stronger rived from their cryptophyte prey (Fields and Rhodes 1991; in some taxa than in others (Table 1). Mixotrophy is often dif- Horiguchi and Pienaar 1992; Larsen 1988; Schnepf, Winter and ficult to detect in dinoflagellates for several reasons. Chloro- Mollenhauer 1989; Skovgaard 1998). Photosynthetic rates plasts may mask food vacuoles and it can be difficult to distin- equivalent to 187% of body C fixed per d have been measured guish food vacuoles from other types of inclusions (reviewed in Gymno. ‘gracilentum’ fed the cryptophyte Rhodornonas. In in Li et al. 1996; Gaines and Elbrachter 1987; Hansen 1998; the absence of prey, both growth and photosynthetic rates de- Hansen and Calado 1999). Experimentally, it is often difficult crease to near zero within two days in this dinoflagellate (Skov- to induce feeding in mixotrophic dinoflagellates because some gaard 1998). In this case of mixotrophy, the dinoflagellate is species only feed under certain conditions or have low feeding dependent on feeding for growth and for replenishment of func- rates (Li et al. 1996; Stoecker et al. 1997; Li, A., unpubl. data; tional plastids. Photosynthesis by kleptochloroplasts is thought to increase growth and survival during starvation in Gymno. ‘gracilentum’. Corresponding Author: D. Stoecker-Telephone number: 4 10-22 1- 8407; FAX number: 410-221 -8490; e-mail: [email protected] Among the Gymnodiniales, some photosynthetic species with I Symposium presentation for a joint meeting of the Society of Pro- their own plastids are capable of phagotrophy. Amphidinium tozoologists, American Phycological Society, and the International So- cryophilum ingests other dinoflagellates (Wilcox and Wede- ciety of Evolutionary , August 7, 1998, Flagstaff, AR. mayer 199 1). Gymnodinium sanguineum, Gyrodinium instria- 397 398 J. EUKARYOT. MICROBIOL., VOL. 46, NO. 4, JULY-AUGUST 1999

Table 1. Confirmed or suspected cases of mixotrophy in dinoflagellates.”

Taxa Habitat Evidence Reference PROROCENTRALES Prorocentrum micam Mar’ Photosynthetic, observation of microtubular basket Schnepf and Winter 1990 P. minimum Mar Photosynthetic, ingestion of cryptophytes and fluo- Li et al. 1996; Stoecker et al. 1997 rescently labelled prey P. belizeunum Mar Photosynthetic, observation of food vacuoles Faust 1998 P. hoffmannianum Mar Photosynthetic, observation of food vacuoles Faust 1998 DINOPHY SIALES Dinophysis acuminata Mar Photosynthetic, observation of food vacuoles Jacobson and Andersen 1994 D. norvegica Mar Photosynthetic, observation of food vacuoles Jacobson and Andersen 1994 GYMNODINI ALES Amphidinium cryophilum FW‘ Photosynthetic, ingestion of other dinoflagellates Wilcox and Wedemayer 1991 Amphi. latum Mar Phagotrophic, observation of kleptochloroplasts Horiguchi and Pienaar 1992 Amphi. poecilochroum Mar Phagotrophic, observation of kleptochloroplasts Larsen 1988 Gymnodinium acidotum FW Phagotrophic, observation of algal endosymbionts/ Fields and Rhodes 1991 kleptochloroplasts Gymno. aeruginosum FW Phagotrophic, observation of algal endosymbiontsl Schnepf, Winter, and Mollenhauer 1989 kleptochloroplasts Gymno. ‘gracilentum’ Mar Phagotrophic, photosynthetic due to kleptochloro- Skovgaard 1998 plasts Gymno. sanguineum Mar Photosynthetic, observation of food vacuoles, inges- Bockstahler and Coats 19931, b tion of small Gyrodinium galatheanum Mar Photosynthetic, observation of food vacuoles and Li et al. 1996 (as Gymno. Estuariale) ingestion of cryptophytes and other small protists Gyro. instriaturn Mar Photosynthetic, ingestion of Uchida, Kamiyama, and Matsuyama 1997 Gyro. pavillardi Mar Photosynthetic, ingestion of ciliates & dinoflagel- Biecheler 1936; Biecheler 1952 lates Gyro. uncatenum Mar Photosynthetic, observation of food vacuoles with Bockstahler and Coats 1993b choreotrich ciliates Torodinium teredo Mar Observation of plastids and defecation Elbrachter 1991 Nemarodinium sp. Mar Observation of plastids, food items and defecation Elbrachter 1991 NOCTILUC ALES Noctiluca miliaris Mar Phagotrophic, green strains with algal endosymbi- Sweeney 1971 ont, limited growth in light in absence of prey GONYAULAC ALES declinatutn j: Mar Photosynthetic, observation of inclusion bodies that Cbang and Carpenter 1994 normnle may be food vacuoles C. furca Mar Photosynthetic, observation of food vacuoles with Bockstahler and Coats 1993b choreotrich ciliates c. fuscus Mar Photosynthetic, observation of inclusion bodies that Chang and Carpenter 1994 may be food vacuoles C. longipes Mar Photosynthetic, observation of food vacuoles Jacobson and Anderson 1996 C. lunula Mar Photosynthetic, possible observation of ingested Norris 1969 Prey C. teres Mar Photosynthetic, observation of inclusion bodies that Chang and Carpenter 1994 may be food vacuoles Alexandrium ostenfeldii Mar Photosynthetic, observation of food vacuoles Jacobson and Anderson 1996 toxicus Mar Photosynthetic, observation of food vacuoles Faust 1998 Ostreopsis spp. Mar Photosynthetic, observation of food vacuoles Faust 1998 diegensis Mar Photosynthetic, observation of food vacuoles Jacobson and Anderson 1996 G. grindleyi Mar Photosynthetic, observation of food vacuoles Jacobson and Anderson 1996 G. spinifera Mar Photosynthetic, observation of food vacuoles and Hansen, Moestrup, and Roberts 1996; Ja- microtubular strand cobson and Anderson 1996 Fragilidium heterolobum Mar Photosynthetic, predator on Gonyaulax Jeong et al. 1997 F. rnexicanum Mar Photosynthetic, predator on other dinoflagellates Jeong et al. 1997 F. subglobosum Mar Photosynthetic, selective predator on Ceratium spp. Hansen and Nielsen 1997; Skovgaard 1996a, b PERIDINIALES Scrippsiella sp. Mar Observation of food Jacobson and Anderson 1996 Heterocapsa triquerra Mar Photosyn., ingestion of fluorescently labeled Legrand, GranCli, and Carlsson 1998 BLASTODINIALES Blastodinium spp. Mar Parasitic on , usually have Cachon and Cachon 1987 Protoodinium spp. Mar Parasitic on , usually have chloroplasts Cachon and Cachon 1971; 1987 Piscinoodinium sp. Mar Parasitic on fish, have chloroplasts Cachon and Cachon 1987 Creoidoodinium Mar Parasitic on fish, have chloroplasts Cachon and Cachon 1987 Dissodinium pseudolunula Mar Parasitic and photosynthetic life stages Drebes 1984 STOECKER-MIXOTROPHY AMONG DINOFLAGELLATES 399

Table 1. Cont.

Taxa Habitat Evidence Reference PHYTODINIALES Stylodinium spp. Fw Photosynthetic. but can feed holozoically on algae Cachon and Cachon 1987 Cystodinedria spp. Fw Photosynthetic, but can feed holozoically on algae Cachon and Cachon 1987 Cysiodinium spp. FW Photosynthetic, but can feed holozoically on algae Cachon and Cachon 1987 DINAMOEBALES piscicidu Mar , can have kleptochloroplasts Steidinger et al. 1996

a Cases in which the results have been retracted or the methods questionable are not included (refer to text). Mar = marine. FW = freshwater.

tum, and Gyrodinium uncateum are predators on planktonic cil- these reports are either questionable or have been retracted (re- iates, with Gyro. instriatum preying on tintinnids and the others viewed in Hansen 1998; Hansen and Calado 1999). preying primarily on non-loricate oligotrichous ciliates (Bock- Fragilidium spp. are specialized predators on other dinofla- stahler and Coats 1993a, b; Uchida, Kamiyama, and Matsuyama gellates (Table 1). Fragilidium subglobosurn is unusual among 1997). In natural assemblages, up to 27% of the Gymno. san- dinoflagellate mixotrophs in that it is a specialized predator on guineum and 12% of the Gyro. uncatenum cells have been ob- certain Ceratium spp. and can grow as a in mono- served to contain food vacuoles with > 98% of the food vac- culture or as a phagotroph in the dark, although its mixotrophic uoles with recognizable prey containing ciliates growth rate is higher than either its strictly phototrophic or pha- (Bockstahler and Coats 1993b). Gyrodinium pavillardi preys on gotrophic growth rates (Hansen and Nielsen 1997; Skovgaard small ciliates and small dinoflagellates and, after making con- 1996a, b). In contrast to F. subglobosum, F. cf. mexicanum does tact with a prey items, it has been observed to immobilize them not appear to be able to grow in the dark when provided with prior to ingestion (Biecheler 1936, 1952). This behavior may prey (Jeong et al. 1997). explain how some dinoflagellates are able to capture and ingest The Blastodiniales are parasites of fish and invertebrates, but relatively fast moving prey such as ciliates. The small photo- many of them have plastids and thus may be mixotrophic (Table synthetic dinoflagellate Gyrodinium galatheanum ( = Gymno- 1). Dissodinium pseudolunula is unusual in that it has a para- dinium galatheanum) preys on small protists including crypto- sitic phase that feeds on eggs, plastidic free-living pri- phytes (as Gymnodinium estuariale in Li et al. 1996). Field mary and secondary cyst stages, and plastidic dinospores, orig- observations and experiments suggest that inorganic nutrient, inally described as Gymnodinium lunula (Drebes 1984; Schnepf particularly phosphate limitation stimulates feeding in this spe- and Winter 1990). During its life cycle, it depends on both cies (Li, A,, unpubl. data). In culture, Gyro. galatheanum grows phagotrophy and phototrophy and thus can be considered a as a phototroph in the absence of prey, but its maximum mix- . In the Blastodiniales, phototrophy might be partic- otrophic growth rate is about twice its maximum phototrophic ularly important in providing nutrition during dispersal between growth rate. However, it can not grow in the dark, even in the hosts. presence of ample prey (Li, A., unpubl. data). It is not known Mixotrophy also appears to occur among the Phytodiniales whether the feeding and growth responses of Gyro. galathean- and Dinamoebales (= Dinococcales). Many of the freshwater um to environmental variables are typical of phagotrophic pho- members of the Phytodiniales have plastids, but also feed on tosynthetic gymnodinioids. algae (Table 1). In some cases, the plastids may be derived from The Noctilucales is a basically heterotrophic order, but green the algal prey (Cachon and Cachon 1987). An unusual mixo- strains of Noctiluca miliaris occur in southeast Asia (Sweeney troph in the Dinamoebales is Pjesteria piscicida, which is pha- 197 1). Green N. miliaris harbor a prasinophyte gotrophic and lacks chloroplasts in most of its life stages, but (Sweeney 1976) and can grow and survive for as long as a the flagellated zoospores often have kleptochloroplasts derived month in the light in the absence of prey. However, prey are from ingested cryptophytes (Steidinger et al. 1996; Lewitus, A., required for long-term survival and growth. as the endosym- unpubl. data). The kleptochloroplasts are photosynthetically bionts are gradually lost during starvation (Sweeney 1971). functional (Lewitus, A., unpubl. data) and thus P. piscicida is, Among the photosynthetic members of the at times, a mixotroph. and Peridiniales, mixotrophy appears to be common in plank- Even from the limited number of examples of mixotrophy tonic and benthic species. Food vacuoles or feeding have been that have been investigated in dinoflagellates, it is clear that reported in the planktonic taxa Ceratium spp., Gonyaulax spp., there is a diversity of mixotrophic strategies in this taxon. How- Fragilidium spp., Alexandrium ostenfeldii, Scrippsiella sp., and ever, it may be possible to group most cases of mixotrophy into Heterocapsa triquetra and in the benthic taxa Gambierdiscus major categories based on functional types (Stoecker 1998). toxicus and Ostreopsis spp. (Table 1). is a well Among the mixotrophic dinoflagellates, many species are pri- known photosynthetic dinoflagellate that can prey on choreo- marily phototrophic and can assimilate dissolved inorganic nu- trich ciliates and on the photosynthetic rub- trients, but use phagotrophy to supplement limiting inorganic rum (Bockstahler and Coats 1993b; Smalley, G. W., unpubl. nutrients and/or to increase their growth rate. In general, these data; DKS., unpubl. data). Feeding in C. furca is variable and species are obligate and can not grow in the dark. may be stimulated by nitrogen limitation (Smalley, G. W., un- Most of the common, mixotrophic bloom-forming dinoflagel- publ. data). It is not known whether the other marine Ceratium lates such as Prorocentrum minimum, Gymnodinium sangui- spp. in which food vacuoles have been reported (Table 1) have neum, Gyrodinium galatheanum, Ceratium furca, and Hetero- similar feeding habitats to C. furca. Feeding has also been re- capsa triquetra (Table 1) appear to fit in this category. Pha- ported in the freshwater species, Ceratium hirundinella, but gotrophy may contribute to their ability to form dense, often 400 J. EUKARYOT. MICROBIOL., VOL. 46, NO. 1, JULY-AUGUST 1999 almost mono-specific blooms, and to persist at high densities Algae, Proceedings of the Vlll International Conference on Hurrnful under stratified, nutrient-limited conditions. It is noteworthy Algae, Vigo, Spain, 1997. Xunta de Galicia & Intergovernmental. p that many of these mixotrophic, but primarily photosynthetic 390-393. dinoflagellates are sometimes responsible for harmful algal Fields, S. D. & Rhodes, R. G. 1991. Ingestion and retention of Chroo- blooms (Grezbyk et al. 1997; Nielsen and Stromgren 1996; mona.v spp. () by Gymnodinium acidoruni (Dinophy- Smayda 1997; Steidinger et al. 1996). ceae). J. Phycol., 27525-529. Gaines, G. & Elblchter, M. 1987. Chapter 6, Heterotrophic nutrition, Other mixotrophic dinoflagellates, such as those with klep- In: Taylor, E J. R. (ed.), The Biology of Dinoflagellates. Blackwell tochloroplasts or unstable algal endosymbionts, appear to be Scientific Publications, Oxford. p. 224-268. primarily phagotrophic. Phototrophy involves both photosyn- Grezbyk, D., Denardou, A., Berland, B. & Pouchus, Y. E 1997. Evi- thetic ability and the ability to assimilate inorganic nutrients dence for a new toxin in the red-tide dinoflagellate Prorocentrum (Raven 1997). Dinoflagellates with kleptochloroplasts or algal minimum. J. Pkznkfon Res., 19: 1 1 1 1-1 124. endosymbionts may only be able to assimilate inorganic nutri- Hansen, G., Moestrup, 8. & Roberts, K. R. 1996. Fine structural ob- ents to a limited degree or perhaps not at all. However, data are servation on Gonyaulax spinifira (), with special em- generally lacking on this aspect of their physiology. In these phasis on the flagellar apparatus. Phycologica, 35:354-366. types, phototrophy may be primarily a mechanism to increase Hansen, P J. 1998. Phagotrophic mechanisms and prey selection in mixotrophic phytoflagellates. In: Anderson, D. M., Cembella, A. D. survival under food-limiting conditions. Gymnodinium ‘graci- & Hallegraff, G. M. (ed.), Physiological Ecology of Harmful Algal lentum, ’ green Noctiluca miliaris, and Pjiesteria piscicida may Blooms. Springer-Verlag, Berlin. p. 525-537. fit this category. In parasitic dinoflagellates, such as Dissodi- Hansen, I? J. & Calado, A. J. 1999. Phagotrophic mechanisms and prey nium pseudolunula, phototrophy may be primarily a mechanism selection in free-living dinoflagellates. J. Euk. Microbiol., 46:382- to increase survival during dispersal. 389. The extent of mixotrophy among dinoflagellate taxa is still Hansen F? J. & Nielsen T. G. 1997. Mixotrophic feeding of Frugilidium largely unknown. For some dinoflagellates, it is not clear subglobosum (Dinophyceae) on three species of Cerurium: effects of whether their photosynthetic machinery is their own or derived prey concentration, prey species and light intensity. Mar. Ecol. Prog. from prey, nor is it clear whether the plastids or endosymbionts Ser., 147:187-196. need to be periodically replenished through ingestion. For most Horiguchi, T., & Pienaar, R. N. 1992. Amphidinium larum Lebour (Di- mixotrophic dinoflagellates, information on functional respons- nophyceae), a sand-dwelling dinoflagellate feeding on cryptonionads. Jpn. J. Phycol., 40:353-363. es to light, dissolved inorganic and organic nutrients, and prey Jacobson, D. M. & Andersen, R. A. 1994. The discovery of mixotrophy quality and quantity are unavailable. This information is nec- in photosynthetic species of Dinoph?;.sis (Dinophyceae): light and essary to understand the evolutionary, physiological, and eco- electron microscopical observations of food vacuoles in Dinophysis logical roles of mixotrophy in dinoflagellates. ucuniinafu, D. norviegica and two heterotrophic dinophysiod dinofla- gellates. Phycologia, 33:97-1 10. ACKNOWLEDGMENTS Jacobson, D. M. & Anderson, D. M. 1996. Widespread of I thank the Society of Protozoologists for support to present ciliates and other protists by marine mixotrophic and heterotrophic this paper. Preparation of the manuscript was supported by NSF thecate dinoflagellates. J. Phycol., 32:279-285. Jeong, H. J.. Lee, C. W., Yih, W. H. & Kim, J. S. 1997. Fragilidium grant OCE-931772. I thank D. W. Coats, D. E. Gustafson, A. cf. mexicanum, a thecate mixotrophic dinoflagellate which is prey for Li, r! J. Hansen, A. Skovgaard, and G. W. 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