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Full Text in Pdf Format AQUATIC MICROBIAL ECOLOGY Published May 28 Vol. 17: 167-179,1999 Aquat Microb Ecol A new method using fluorescent microspheres to determine grazing on ciliates by the mixotrophic dinoflagellate Cera tium furca Gabriela W. ~rnalle~'.~~:D. Wayne coats1,E. Jeremy dam' 'Smithsonian Environmental Research Center. PO Box 28. Edgewater. Maryland 21037, USA 'university of Maryland System, Center for Environmental Studies. Horn Point Laboratory, Cambridge, Maryland 21613. USA ABSTRACT: Feeding in the mixotrophc dinoflagellate Ceratium furca was investigated using 1 pm fluorescent microspheres to label prey. Microspheres added to natural plankton assemblages at a con- centration of 5 X 106 to 107 rnl-' were rapidly ingested by a variety of planktonic organisms including small flagellates, ciliates, dinoflagellates, ebriids and amoebae. Prey thus labeled were in turn phagocy- tized by C. furca and were easily detected within the predator using fluorescent microscopy. Ingestion rates were calculated by following the appearance of labeled food vacuoles in C. furca over time. C. furca did not ingest microspheres directly, and thus the calculated rates represented feeding on labeled prey only. Food vacuole contents and labeled prey were identified using a modified Protargol staining procedure that retained the integrity and fluorescent properties of the latex microspheres. Data on food vacuole content and potential prey availability indicated that C. furca preyed mainly on choreotrich cil- iates (i.e. Strobilidtum spp, and tintinnids) 10 to 40 pm in diameter. In addition, feeding rates were strongly correlated with choreotrich densities and suggested that C. furca preferred ciliates of the genus Strobilidium. Ingestion rates of C. furca ranged from 0 to 0.1 1 prey h-', and varied greatly from one year to the next. Clearance rates ranged from 0 to 12.49 pl (C. furca)-' h-', with an average of 2.1 2 0.41 rnl (C. furca)-' h-' Both ingestion and clearance rates were comparable to rates previously reported for mixotrophic and heterotrophic dinoflagellates. The method presented here has several advantages for the study of mixotrophy in large, slow-feeding dinoflagellates. Live prey found in natural water samples are used, and surface characteristics of prey remain unaltered. No addition of prey is necessary, and only a minimum amount of handling of the sample is required. Incubation experiments can last for 6 h, allowing sufficient time for the appearance of labeled food vacuoles in predators with low feeding rates. KEY WORDS: Ceratium furca . Mixotrophy . Dinoflagellates . Ciliates . Fluorescent microspheres . Chesapeake Bay INTRODUCTION gies may give mixotrophs a competitive advantage over strict phototrophs, since phagotrophy could Mixotrophic protozoa gain their nutrition through a enable them to acquire carbon and nutrients when combination of photosynthesis and uptake of dissolved photosynthesis is limited (Sanders et al. 1990, Sanders or particulate organic material. They vary widely in 1991, Bockstahler & Coats 1993a, Nygaard & Tobiesen their photosynthetic and phagotrophic capabilities, 1993). Conversely, mixotrophs may outcompete strict and may be regarded as occupying different points heterotrophs by fixing carbon to survive periods of along a spectrum of nutritional strategies that range reduced particulate food availability (Andersson et al. between pure autotrophy and pure heterotrophy 1989, Sanders et al. 1990, Rothhaupt 1996). Despite (Sanders 1991, Jones 1994). These nutritional strate- increasing reports of mixotrophy in a variety of pro- tists, the benefits and ecological advantages of this nutritional strategy remain largely speculative. Q Inter-Research 1999 Aquat Microb Ecol l?: 167-179, 1999 Mixotrophy is common among photosynthetic dino- prey, thus altering the original composition of the flagellates and appears particularly well developed in natural plankton assemblage. species of Ceratium (Schnepf & Elbrachter 1992). For Ingestion rates for various protists have also been example, Dodge & Crawford (1970) reported food vac- estimated using a 'gut clearance/gut fullness' approach uoles in C. hirundinella that contained bacteria, blue- (Kopylov & Tumantseva 1987, Dolan & Coats 1991a, green algae, and diatoms. Similarly, Hofender (1930) Bockstahler & Coats 1993b). In this approach, diges- observed C. hjrundinella feeding on a variety of prey tion rates determined by following the disappearance including cyanobacteria, diatoms, and ciliates, and of phagocytized prey over time are used in conjunction noted phagotrophy by C. Eurca, C, tripos, and C. cornu- with data on 'gut content' of specimens collected from tum. Predation on ciliates has also been demonstrated the field or from laboratory cultures to estimate in- for C. Eurca (Bockstahler & Coats 1993a, Li et al. 1996) gestion rate. Bockstahler & Coats (199313) used this and C. longipes (Jacobson & Anderson 1996), and food method to quantify feeding by Gymnodinium sangui- vacuoles containing unidentified prey have been found neum and estimate its impact on ciliate prey popula- in C. lunula, C. teres, C. declinatum f. normale, C. tions in Chesapeake Bay. This approach is attractive as furca, and C. fusus (Norris 1969, Cachon et al. 1991, no handling or incubation of the dinoflagellate is Chang & Carpenter 1994). While some of these studies needed to estimate ingestion rates; however, it is very have quantified the prevalence of food vacuoles in field labor-intensive, and several assumptions are required. populations (Bockstahler & Coats 1993a, Chang & Car- For example, digestion rate must be independent of penter 1994, Li et al. 1996),none have determined feed- 'gut content', and ingestion and digestion must be in ing rates for Ceratium species in culture or in the field. equilibrium (i.e.steady-state conditions). This lack of data on feeding rates might be partly Dolan & Coats (1991b) developed a technique using due to difficulties in selecting an appropriate method bacteria-sized fluorescent microspheres to demon- to investigate feeding in large mixotrophic dinoflagel- strate feeding in a variety of predacious ciliates in the lates like those of the genus Ceratium. Methods fre- laboratory. Microspheres added to ciliate cultures at a quently used to study feeding behavior and ingestion concentration of 107 ml-' were readily ingested by a rates of planktonic protists employ a variety of tracers number of bactivorous species, which yielded motile, such as fluorescently labeled, heat-killed bacteria and labeled prey with presumably unaltered surface char- algae, fluorescent rnicrospheres, and paint, dye, or acteristics. Prey ciliates so labeled were ingested by starch particles (McManus & Fuhrman 1985, Bird & larger ciliates and could be detected using fluores- Kalff 1987, Sherr et al. 1987, Rublee & Gallegos 1989, cence microscopy. In the present study, we modified Sherr et al. 1991). However, not all protists will ingest this method for use in the field to determine food inert surrogate prey (Stoecker 1988, Jones et al. 1993, vacuole contents and feeding rates of Ceratium Eurca, Cleven 1996), and phagotrophy may consequently go a large mixotrophic dinoflagellate which periodically undetected or be underestimated in certain taxa. A forms summer blooms in surface waters of Chesapeake variety of radioisotope labeling techniques that use Bay (Mulford 1963, Marshal1 1980, Bockstahler & Coats live prey labeled with 14C have also been developed 1993a). When we added fluorescent microspheres to (Nygaard & Hessen 1990). However, these approaches natural plankton assemblages that contained C. furca, are restricted to short-term incubations and require a microspheres were ingested by a variety of planktonic large amount of handling when prefiltering, incubat- organisms, some of which were in turn ingested by C. ing, washing and fractionating prey, procedures that Eurca. Food vacuoles containing labeled prey were may disturb or alter the natural prey assemblages easily located within C. furca using fluorescent micro- (Landry 1994).Recently, Li et al. (1996) used live prey, scopy, and could be distinguished from previously including phycoerythrin-containing cryptophytes that ingested, unlabeled prey. With this method, we were exhibit distinct yellow-orange autofluorescence and able to demonstrate mixotrophy in C, Eurca, determine protists stained with CMFDA (5-chloromethylfluores- food va.cuole contents and prey preferences, and quan- cein diacetate),a low-toxic, vital sta1.n.with green fluo- tify ingestion rates on labeled prey. rescence, to qualitatively demonstrate feeding in sev- eral rnixotrophic dinoflagellates. Unfortunately, none of these tracer techniques are ideal for measuring MATERIALS AND METHODS ingestion in large mixotrophic dinoflagellates that typ- ically feed at very low rates. To quantify ingestion rates All experiments were conducted aboard the RV in species like C. furca, Gyrodinium uncatenum, and 'Cape Henlopen' on Chesapeake Bay, USA, during the Gymnodinium sanguineum, within time constraints summer of 1995 and 1996. Natural water samples were imposed by digestive processes, would require addi- collected along the main axis of Chesapeake Bay, and tion of higher than 'tracer' concentrations of labeled treatments were incubated in polycarbonate sample Smalley et al.: Grazing on ciliates by Ceratium furca 169 bottles in a flowing seawater bath on deck. The water until >l00 individuals were counted. For all other bath was covered with a screen that reduced the
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