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Favella Panamensis</Emphasis> Marine Biology (1994) 119:105-113 Springer-Verlag 1994 D. W. Coats K. R. Bockstahler G. M. Berg J. H. Sniezek Dinoflagellate infections of Favella panamensis from two North American estuaries Received: 3 September 1993 / Accepted: 3 November 1993 Abstract Favella panamensis Kofoid and Campbell, producers to higher trophic levels and act as a major source 1929 is seasonally abundant in meso- to polyhaline waters of nutrient regeneration. In contemporary models of the of Chesapeake Bay and Indian River, Florida, USA, where marine planktonic food web, ciliates represent a two-way it reaches densities of 103 cells 1-1 . During the summers link of primary production to the larger zooplankton (Sherr of 1986-1992, F. panamensis populations of the two estu- et al. 1988). They form a direct connection by repackag- aries were commonly infected by the parasitic dinoflagel- ing the nanophytoplankton into a size fraction that is more late Duboscquella aspida Cachon, 1964. The intracellular readily grazed by the macrozooplankton and represent an phase of the parasite reached maturity in -21 h (30 ~ and indirect connection by forming the terminal link in a mul- consumed -35% of the host's biomass. Infections were not tiple step pathway between secondary bacterial production typically lethal to F. panamensis, but sometimes forced the and zooplankton, the "microbial loop" (Azam et al. 1983). host from its lorica. Several D. aspida were found in the Metazoan consumers are not, however, the only preda- cytoplasm of many hosts, and the number of parasites in- tors of planktonic ciliates. A variety of heterotrophic pro- fection-1 was directly related to infection level. Parasite tists including fungi (Ball 1969), sarcodines (Caron and prevalence averaged 24.0 and 11.5% with mean number of Swanberg 1990; Swanberg and Caron 1991), dinoflagel- parasites infection-1 being 1.5 and 1.3 for Chesapeake Bay lates (Hansen 1991; Schnepf and Elbr~ichter 1992), and and Indian River samples, respectively. D. aspida was es- other ciliates (Dolan and Coats 1991 a, b) utilize ciliated timated to remove up to 68% of host standing stock d -1 protozoa as a food source. Even some typical phytoplank- with a mean of ~ 10% for all samples. The average impact ton species that were conventionally viewed as strict pho- of parasitism on F. panamensis populations was somewhat totrophs are now known to feed on small choreotrich cili- less than would be expected from copepod grazing. ates (Bockstahler and Coats 1993 a, b). Grazing pressure exerted on ciliates by protozoan predators may at times ri- val that generated by larger zooplankton. For example, epi- demic infections of Eutintinnus pectinis by the parasitic Introduction dinoflagellate Duboscquella cachoni may remove in ex- cess of 50% of the host standing stock d -1 in Chesapeake Ciliated protozoa are widely recognized as playing a crit- Bay (Coats and Heisler 1989). The annual impact of this ical role in the trophodynamics of planktonic food webs parasite on host populations was estimated to equal that of (Stoecker and Capuzzo 1990; Gifford 1991; Reid et al. the dominant metazoan grazer, Acartia tonsa. 1991; Pierce and Turner 1992). These small heterotrophs Several other heterotrophic dinoflagellates act as intra- mediate the transfer of energy and matter from primary cellular parasites of loricate and aloricate ciliates (Cachon and Cachon 1987). Among these, Duboscquella aspida has been most thoroughly studied with infections reported for a number of tintinnids including Coxliella lacinosa, Codo- Communicated by J. R Grassle, New Brunswick nella campanula, Favella ehrenbergii, and Eutintinnus D. W. Coats ([]) K. R. Bockstahler J. H. Sniezek frakndii (Cachon 1964). The life cycle ofD. aspida, as de- Smithsonian Environmental Research Center, scribed for infections in E ehrenbergii (Cachon 1964), con- Box 28, Edgewater, Maryland 21037, USA sists of an intracellular vegetative phase followed by an extracellular reproductive/dispersal phase. During the tro- G. M. Berg Marine-Estuarine and Environmental Sciences, phont (i.e., vegetative) stage, the parasite increases in size University of Maryland, College Park, and forms a large yellowish mass within the cytoplasm of Maryland 20742, USA the host. This intracellular phase of the parasite's life cy- 106 cle is terminated when the trophont ruptures through the and photographed. These direct observations provided data on de- cortex of the host, and in the process phagocytizes a large velopmental events and the duration of sporogenesis. Information on the population dynamics of DuboscqueIla aspi- portion of the ciliate's cytoplasm. Cachon noted that emer- da was obtained through the study of a natural host-parasite assem- gence of the trophont through the host's cortex was often, blage. A 120-liter cylindrical plastic tub was filled with Indian Riv- but not always, fatal to F. ehrenbergii. Once outside the er water containing parasitized Favella panamensis and maintained host, the parasite undergoes a rapid series of divisions to at ambient temperature (~ 30 ~ in a flowing estuarine water bath. The isolated population was exposed to the natural light regime and produce numerous biflagellate dinospores that initiate new sampled at 2- to 4-h intervals over 34 h. For each sample, 4 liters of infections if ingested by another susceptible host. water were concentrated on 20-gm mesh Nitex, back-flushed to While Duboscquella aspida is not host specific, it ap- 25 ml using multiple rinses, and preserved in Bouin's fluid. F. pana- pears to parasitize Favella spp. more frequently than oth- mensis abundance, number of host Ioricae without ciliates, and num- er tintinnids, with infection levels in F. ehrenbergii some- ber of loricae containing parasite sporogenic stages were determined by examining 2-ml aliquots of preserved sample (=320 ml whole- times approaching 100% (Cachon 1964). Cachon also sug- water) using inverted microscopy (x200). Parasite prevalence, num- gested that epidemic outbreaks of D. aspida in the plank- ber of parasites infection-1 , and the relative occurrence of four se- ton of Algiers harbor caused abrupt decreases in the abun- quential stages (I-IV, respectively) in the intracellular, trophic phase dance of F. ehrenbergii, even though some host organisms of D. aspida were determined from hematoxylin preparations with 100 hosts examined sample-1. The abundance of parasite trophonts were capable of surviving infection. at each sampling time was calculated by multiplying mean number Here we document the occurrence of Duboscquella as- of intracellular parasites host-I by host density. pida in populations of Favella panamensis from two North An estimate for the duration of the parasite's trophic phase was American estuaries, Chesapeake Bay and Indian River, derived from data on the temporal occurrence of different intracel- lular stages of during this experiment. Data Florida. Data on parasite and host morphology, parasite Duboscquella aspida analysis was similar to that used by Heinbokel (1988) for determin- generation time, and in situ infection levels are used to es- ing duration of ciliate reproductive stages. The percentages of para- timate the potential impact of this parasite on host popu- sites represented by stage I-II and III-IV infections were plotted sep- lations. arately, and the time interval during which those percentages exceed- ed their respective mean values was determined by linear extrapola- tion. The mid-point of each interval provides an objective estimate for the time of maximum occurrence of each stage, and the differ- Materials and methods ence between the two mid-points equals half the intracellular devel- opment time. Parasitism of Favella panamensis Kofoid and Campbell, 1929 by The impact of parasitism on FavelIapanamensis populations, ex- the dinoflagellate Duboscquella aspida Cachon, 1964 was studied pressed as the percent of host standing stock removed d -1, was cal- by examining specimens collected from Chesapeake Bay and Indian culated as: River, Florida, USA. Samples from Chesapeake Bay were taken VvzrXNXD -1, at routine stations located along the major axis of the Bay during cruises in 1986 to 1991. Station protocol followed established where Vp/r is the mean value for the volume of the mature parasite procedures (Coats and Heisler 1989) and included conductivity-tem- divided by total parasite-host volume (=0.35); N is the number of perature-depth profiles, Niskin bottle samples at eight to ten depths, parasites (=infection level multiplied by parasites infection-I); and and vertical net tows (30-gm mesh). Plankton collections containing D is the development time for the intracellular phase of the parasite sufficient numbers of E panamensis for the present study were in days adjusted for sample temperature using a Q10 of 2. only obtained from the meso- to polyhaline portion of the Bay Living and stained specimens were viewed and photographed us- south of the Choptank River (i.e., between 38034 ' and 37o07 ' N lat- ing Zeiss microscopes equipped with brightfield, phase contrast, and itudes). differential interference contrast optics. Intracellular parasite stages Samples from the Indian River, a shallow polyhaline estuary on were measured on hematoxylin stained cells using a filar microme- the southeastern coast of Florida, were obtained in June and Septem- ter; means are reported with standard errors (+ SE) and sample siz- ber 1991, and in August 1992. On each occasion, 18 stations even- es (n). Cell volumes for hosts and the post-phagotrophic stage of Du- ly spaced along a 40-mile transect from Sebastian Inlet (27o52 ' N boscquella aspida were calculated using appropriate geometric for- lat.) to St. Lucie Inlet (27o10 ' N lat.) were sampled over a 1- to 2- mulae and cell dimensions obtained from photographic images of wk period. Whole-water and net tow (35-gin mesh) samples were living specimens. collected near the surface of each station, and measurements were made for temperature and salinity. Host abundance was determined by inverted microscopy (x200) using replicate 50-ml aliquots of whole-water samples preserved Results with a modified Bouin's solution (Coats and Heinbokel 1982).
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