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Growth and Grazing Responses of Two Chloroplast-Retaining Dinoflagellates: Effect of Irradiance and Prey Species

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Growth and Grazing Responses of Two Chloroplast-Retaining Dinoflagellates: Effect of Irradiance and Prey Species MARINE ECOLOGY PROGRESS SERIES Vol. 201: 121–128, 2000 Published August 9 Mar Ecol Prog Ser Growth and grazing responses of two chloroplast-retaining dinoflagellates: effect of irradiance and prey species Hans Henrik Jakobsen1, 2,*, Per Juel Hansen2, Jacob Larsen3 1Danish Institute for Fisheries Research, Department of Marine and Coastal Ecology, Kavalergården 6, 2920 Charlottenlund, Denmark 2Marine Biological Laboratory, Strandpromenaden 5, 3000 Helsingør, Denmark 3IOC Science and Communication Centre on Harmful Algae, Botanical Institute, Department of Phycology and Mycology, Øster Farimagsgade 2D, 1353 Copenhagen K, Denmark ABSTRACT: The effect of irradiance on growth and grazing responses of 2 phagotrophic dinoflagel- lates, Gymnodinium gracilentum Campbell 1973 and Amphidinium poecilochroum Larsen 1985, was studied. While G. gracilentum belongs to the plankton, A. poecilochroum is a benthic species that pri- marily feeds on prey associated with surfaces. Both organisms are able to retain functional chloro- plasts from their prey. They are both able to grow heterotrophically in the dark, but growth rates increase in the light. The maximum growth and ingestion rates of G. gracilentum are much higher than those of A. poecilochroum. However, the growth rate of A. poecilochroum is saturated at a lower irradiance (~6 µmol photons m–2 s–1) than to G. gracilentum (~60 to 80 µmol photons m–2 s–1). Also, the irradiance required for saturation of growth for both dinoflagellates matched that found for the prey algae. The effect of light on ingestion and growth was also studied during the light and dark periods of the day. Ingestion rates of G. gracilentum were higher during the light period, while division rates were higher during the dark period. Offered a variety of prey items belonging to different algal classes, G. gracilentum selectively feeds on species belonging to the class Cryptophyceae. KEY WORDS: Gymnodinium gracilentum · Amphidinium poecilochroum · Dinoflagellates · Mixotro- phy · Feeding rates · Growth rates · Chloroplast Resale or republication not permitted without written consent of the publisher INTRODUCTION effectiveness in light-harvesting, and are often quite constant in number (Laval-Peuto 1992). The plastids Many planktonic heliozoans, foraminifers, ciliates have only a limited lifespan within the ciliate cell, and dinoflagellates are pure heterotrophs. However, before they are either diluted out, digested or egested some species within these groups have the ability to (Stoecker et al. 1988, Stoecker & Silver 1990). In many retain functional chloroplasts from ingested algal prey cases, it is not known whether the relationship is facul- and thereby become mixotrophs. The most restricted tative or obligatory. Obligate mixotrophy has been form of this mixotrophy has been described in some demonstrated in only 1 chloroplast-retaining ciliate, heliozoans (Patterson & Dürrenschmidt 1987). In these Laboea strobila (Stoecker et al. 1988). heliozoa, the mixotrophy is transitory and the retention The importance and role of retained chloroplasts of plastids non-obligatory. More developed relation- for the metabolism of mixotrophic dinoflagellates is ships can be found among the ciliates. Here the plas- largely unknown. A notable exception is a recent study tids are placed at the periphery of the cell, probably for by Skovgaard (1998) that suggested sequestered chlo- roplasts help Gymnodinium gracilentum resist starva- tion at low prey densities by providing an alternative *E-mail: [email protected] source of carbon. © Inter-Research 2000 122 Mar Ecol Prog Ser 201: 121–128, 2000 The aim of the present study was to examine (1) the ing from 0 to 270 µmol photons m–2 s–1 for Gymnodinium effects of irradiance on the growth and ingestion rates gracilentum fed Rhodomonas salina and from 0 to of 2 chloroplast-retaining dinoflagellates, Gymnodin- 80 µmol photons m–2 s–1 for Amphidinium poecilochroum ium gracilentum and Amphidinium poecilochroum; fed Chroomonas sp. Control experiments on growth (2) cell division and feeding rates of G. gracilentum rates for R. salina and Chroomonas sp. in monoculture in light and dark periods of the day, and (3) the range were carried out parallel to experiments with the di- of prey organisms qualitatively and quantitatively noflagellates. Growth rates of prey algae in monoculture accepted by G. gracilentum. were iteratively fitted to a 2nd-order equation using Sigmaplot® (Jandel Scientific, California, USA): PII( ± ) MATERIALS AND METHODS µ = max min (1) IIImax/2 + ( ± min ) Isolation and maintenance of cultures. Gymnodin- where Pmax = maximum theoretically obtainable ium gracilentum Campbell 1973 was isolated in July growth rate, I = actual irradiance, I max/2 = irradiance from surface water samples from the northern part of that sustains 0.5 Pmax, and I min = point of light compen- Øresund, Denmark. Rhodomonas salina was added as sation where growth is zero (µ = 0) prey, and the cultures were maintained on a plankton Growth and ingestion rates were measured for Gym- wheel (1 rpm) at an irradiance of 50 µmol photons m–2 odinium gracilentum and for Amphidinium poecilo- s–1 in a light:dark cycle of 16:8 h at 15°C. chroum at saturating prey concentrations of >170 µg–1 Larsen (1985) originally described the benthic spe- C l–1, estimated from cell concentration and cell vol- cies Amphidinium poecilochroum as phototrophic. ume using the carbon to volume relationship given in Later he found that A. poecilochroum was able to Strathmann (1967). Prior to the experiments, all organ- retain functional chloroplasts from ingested crypto- isms were pre-incubated at experimental conditions phytes (Larsen 1988). The present culture of A. for at least 48 h. poecilochroum is the same strain as that originally Experiments with Gymnodinium gracilentum were isolated by Larsen (1985, 1988). Stock cultures were carried out in triplicate batch cultures using 50 ml tis- maintained by adding a few cells of A. poecilochroum sue bottles and paralleled by triplicate controls for prey to a culture of a small green cryptophyte Chroomonas growth. Sampling was done between 09:00 and 12:00 h sp., at intervals of 1 to 2 mo. The cultures were main- at intervals of 24 h in order to eliminate interference tained in tissue bottles (Nunclon‚) placed on a trans- from diurnal rhythms. Cells were fixed in Lugol’s solu- parent glass plate lit from below. The prey organism, tion (1% final concentration) and counted in a Sedg- Chroomonas sp., showed the same ability of adhering wick-Rafter chambers using an inverted microscope. to surfaces as A. poecilochroum, suggesting that this Because of the adhesive properties of Amphidinium species also lives in association with the sediment. poecilochroum and Chroomonas sp., it was not possible Experimental conditions. All experiments were con- to obtain homogeneous samples from tissue-culture ducted in autoclaved seawater based on B1 media bottles. Instead, experiments with A. poecilochroum and (Hansen 1989), with a salinity of 30 psu and a temper- Chroomonas sp. together and Chroomonas sp. alone ature of 15 ± 0.5°C. All cells used in experiments were were carried out in 0.4 ml microwells (Nunclon®). The from cultures grown under a light:dark cycle of 16:8 h wells were illuminated from below using unidirectional supplied from cool-light fluorescent tubes. Irradiance light; all cells settled to the bottom of the micro-wells was measured using a radiometer (LI-COR LI-1000, without adhering to the walls, and could thus be counted Li-Cor®, USA), equipped with a flat sensor (L-192SA) with an inverted microscope. At each irradiance, 8 wells inside a polystyrene tissue bottle (Nucleon®) for containing a suspension of A. poecilochroum and Gymnodinium gracilentum and through a multidish Chroomonas sp. and 8 wells with only Chroomonas sp. (Nucleon®) for Amphidinium poecilochroum in order cells as controls were set up. After pre-incubation, to compensate for the absorption of light by the exper- 4 wells with A. poecilochroum and 4 control wells were imental containers. Irradiance was regulated by vary- fixed in Lugols’ solution and counted. Depending on ing the distance between the plankton wheel and the the number of A. poecilochroum at the beginning of light source in the experiments with G. gracilentum. In the experiment, the remaining 4 experimental and 4 the case of A. poecilochroum, irradiance was varied by controls wells were fixed and counted after 3 to 5 d. attenuation with Letratone® screening film or by vary- Growth rates of Amphidinium poecilochroum and ing the distance from the light source. Gymnodinium gracilentum were assumed to be expo- Growth and ingestion rates as a function of irradi- nential and were estimated by linear regression of ance. Growth and ingestion rates for the 2 dinoflagel- log-transformed data. Experiments with a correlation lates were measured at different light intensities, rang- coefficient (r2) below 0.90 were not used. Jakobsen et al.: Growth and grazing responses of phagotrophic dinoflagellates 123 Ingestion rates (U) of both Gymnodinium gracilen- at one single irradiance (25 µmol photons m–2 s–1). tum and Amphidinium poecilochroum were estimated Unpublished TEM photographs of G. gracilentum from changes in prey cell numbers in treatments com- grown in excess of food and satiated levels of irradi- pared to prey densities in controls. These calculations ance reveal that food vacuoles are spherical and larger were based on a model developed by T. Fenchel and than retained
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