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Adult copepods Centropages harnatus were induced to feed on 10 to 40 pm Sephadex beads by adding Thalassiosira weissflogii or ScrippsieUa trochoidea wholecell extract, or filtrate from a T. weissflogii culture, to a bead suspension. Beads were neither ingested in the absence of a chemical stimulus, nor in the presence of filtrates from cultures of S. trochoidea and Olisthodiscus luteus, or 0. luteus extracts. Extracts from both S. trochoidea and 0. luteus, and filtrate from an 0. luteus culture, appear to exert an inhibitory effect when applied in combination with T. weissflogii extract. Copepods acclimated to T. weissflogii for 24 h did not significantly increase their feeding rate on T. weissflogiiflavored beads and did not ingest S. trochojdea-flavored beads. Food choice by herbivorous copepods can be influenced by the size, shape and chemical composition of potential prey. Earlier stu&es of food choice by copepods focused on the effects of phytoplankton size because copepods were thought to be passive filter feeders and limited in their ability to actively select food items (e.g. Boyd 1976, Nival & Nival 1976, Frost 1977). However, since Alcarez et al. (1980) and Koehl & Stnckler (1981) have shown that copepods actively select their prey, more studies have focused on the role of chemical stimuli produced by the prey in determining food choice by copepods (e.g. Donaghay & Small 1979, Huntley et al. 1983). Huntley et al. (1986) have shown that Calanus pacificus and Paracalanus p m s reject particular dinoflagellate species and that in one case the rejection is based upon the presence of exudates released by the alga. Here, I show that feeding behavior in the herbivorous copepod Centropages hamatus can be stimulated by Thalassiosira weissflogii whole cell homogenates or Research supported by Summer Student Fellowship from Woods Hole Oceanographic Institution and by National Science Foundation grant OCE 82-15188 to Timothy J. Cowles " Present address: Department of Zoology NJ-15, University of Washington, Seattle, Washmgton 98195, USA O Inter-Research/Printed in F. R. Germany by filtrates taken from cultures of these cells. I further document that the presence of homogenates or filtrates of 2 other phytoplankton species, Scrippsiella trochoidea and OListhodiscus luteus, can inhibit feeding in these copepods. Material and Methods. Thalassiosira weissflogii (Bacillariophyceae), Scrippsiella trochoidea (Dinophyceae) and Olisthodiscus luteus (Xanthophyceae) were grown in unialgal cultures in f/2 culture medium (based on Guillard's F, medium from Guillard & Ryther 1962). Whole-cell extracts were made by centrifuging 13 mm3 of cells taken from cultures exhibiting exponential growth. They were put into 10 m1 of filtered seawater (henceforth meaning seawater that was filtered through a 0.8 pm filter) and sonicated for three 30 s intervals, cooling the cells for intervals of 3 to 5 rnin after sonicating. The extract was then centrifuged at 5000 rpm for 15 min. The supernatant was poured off, filtered through a 0.8 pm filter and brought up to a volume of 25 rnl with filtered seawater. Exudates from phytoplankton cultures were collected by vacuum filtering cells from the medium in which they were growing using a 0.8 pm filter at pressure differentials of no more than 5 mm Hg. Adult Centropages harnatus were collected from the Woods Hole Oceanographic Institution dock in Woods Hole, Massachusetts (USA) in July and August of 1983. Unless otherwise specified, the collected copepods were starved in filtered seawater for 6 to 8 h prior to the start of each experiment. The term 'acclimated copepods' refers to copepods fed Thalassiosira weissflogii for at least 24 h prior to the experiment. Each experiment consisted of 3 replicate bottles. Each bottle contained 400 rnl of filtered seawater, 20 copepods, and an initial bead concentration of about 500 Sephadex G-50 Superfine (10 to 40 pm) beads ml-l. The beads had been rehydrated in filtered seaMar. Ecol. Prog. Ser 34: 187-190, 1986 water for l h prior to the start of the experiment. To each set of bottles a total of 2 m1 of phytoplankton extract or filtrate from a phytoplankton culture was added singly or in combinations of l m1 of each to determine the effects of these substances on copepod feeding behavior. Additions of 2 m1 of filtered seawater or f/2 culture medium were used as controls. Initial bead concentrations were determined by averaging Coulter counter measurements from 12 to 15 replicate samples from each bottle. Copepods were allowed to feed for 1 h whlle the bottles were rotated at 1 to 2 rev min-' to keep the beads suspended. Limiting the feeding experiments to 1 h ensured that there was insufficient time for the beads to pass through the guts of the copepods and then become resuspended in the seawater. Copepods were subsequently removed from the bottles and final bead concentrations were measured in 15 replicate bead samples from each bottle. Differences in initial and final concentrations of beads were compared using a 2-way ANOVA without replication in which differences in initial bead concentrations were considered random effects and changes over time were examined. Single-classification ANOVA's were used to compare differences in ingestion rates. Multiple comparisons of mean ingestion rates were made using the T-method for unplanned comparisons (Sokal & Rohlf 1981). Results. There was no significant change over time in initial and final bead concentrations (based on the time component of a 2-way ANOVA; p<0.05) when filtered seawater alone was added to the bottles (Fig. l ) , indicating that Centropages hamatus would not ingest Sephadex beads in the absence of a chernical feeding stimulus. Likewise, addition of f/2 culture medium did not stimulate feeding. When Thalassiosira weissflogii and Scrippsiella trochoidea extracts or T. weissflogii medium were added there was a significant decrease in bead concentration (p < 0.025). Ingestion of beads flavored with T. weissflogii extract was significantly higher (p < 0.05; T-method) than with S. trochoidea-flavored beads. There was no difference (p > 0.75) between ingestion rates when T. weissflogii extract and T, weissflogii medium were added. Ingestion rates were also not significantly dfferent in the presence of 1 rather than 2 m1 of T. weissflogii extract. And, there was no significant (p > 0.05) change in bead concentrations when either S. trochoidea medium or Olisthodiscus luteus extract were added. Copepods acclimated to live T. weissflogii for l d prior to the experiments did not significantly increase (p > 0.05) their consumption of beads flavored with T. weissflogii extract relative to copepods that had not been acclimated to T. weissflogii (Fig. 2). However, acclimated copepods did not ingest beads flavored with S. trochoidea extract. Fig. 1. Centropages hamatus. Mean ingestion rates of Sephadex beads (beads copepod-' h-') when phytoplankton extracts and exudates are added to the bead suspension. Vertical lines: + 1 SE; asterisks: additives causing significant (p t 0.05) changes in bead concentration. SWC: seawater control; CMC: f/2 culture medium control; TE: Thalassiosira weissflogii extract; TM: T weissflogii medium; SE: Scrippsiella trochoidea extract; SM: S. trochoidea medium; OE: Olisthodiscus luteus extract In order to determine whether any of these phytoplankton extracts and exudates might have an inhibitory effect on feeding behavior, Scrippsiella trochoidea and Olisthodiscus luteus extracts and media were added in combination with Thalassiosira weissflogii extract. Addition of S. trochoidea extract with T. weissflogii extract resulted in significantly lower ingestion rates (p < 0.05 using the T-method) than when either substance was added separately (Table 1). Addition of 0. luteus extract in combination with T. weissflogii extract -resulted in ingestion rates intermediate beFig. 2. Centropages hamatus Mean ingestion rates (beads copepod-' h' ) of Sephadex beads flavored by ThdlaS~l~~Jra weissflogu and Scrippsiella trocho~dea. Solid bars: acclimated copepods; open bars. non-accl~mated copepods; vertical lines: f l SE Van Alstyne. Effects of phytoplankton taste and smell on feed~ng behav~or of a copepod tween the ingestion rates obtained when either was added separately. Mean ingestion rates in the presence of 0 . luteus medium and T. weissflogii extract were 43 '10 lower than those obtained when only T. weissflogii extract was added; however, due to high variance in ingestion rates these numbers were not significantly different. Discussion. The responses by Centropages hamatus to the exudates and extracts of the 3 phytoplankton species correspond well with preferences shown by other copepod species. Digestive enzyme activity in Calanus pacificus drops when fed ScrippsieUa trochoidea over a 24 d period (Hassett 1986). When fed Thalassiosira weissflogii, cellobiose activity drops but laminarase and maltase activity remain relatively constant. Hassett (1986) also showed that C. pacificus had a much lower survival rate when fed S. trochoidea than when fed T. weissflogii. And, Olisthodiscus luteus is known to be a less preferred food item for Acartia spp. (Tomas & Deason 1981). Thus, S. trochoidea and 0. luteus tend to be less preferred food items because of their chemical composition rather than because of their size or morphological features. The negative responses of Centropages hamatus to Scrippsiella trochoidea and Olisthodiscus luteus are similar to the responses obtained by Huntley et al. (1986). They found that exudates but not homogenates of Protoceratium reticulatum inhibit feeding by Calanus pacificus on Gyrodnium resplendens. Many phytoplankters are known to produce toxins (Carmichael & Gorham 1977, Schmidt & Loeblich 1979, White 1980) or structures such as trichocysts (Ukeles & Sweeney 1969) which could deter feeding by herbivorous zooplankton. Many other substances, which might serve as

Effects of phytoplankton taste and smell on feeding behavior of the copepod Centropages hamatus