Effects of Competitors, Predators, and Prey on the Grazing Behavior of Herbivorous Calanoid Copepods

BULLETIN OF MARINE SCIENCE, 43(3): 573-582, \988

EFFECTS OF COMPETITORS, PREDATORS, AND PREY ON THE GRAZING BEHAVIOR OF HERBIVOROUS CALANOID COPEPODS

C Kim Wong

ABSTRACT Gut fluorescence was measured to test the effects of potential competitors, predators, and alternate animal prey on the short term (1,5-2 h) herbivorous feeding rates of the marine calanoid copepods Calanus pac!ficus Brodsky, Pseudocalanus minutus (Kroyer), and Metridia pacl}ica Brodsky. The diatoms Thalassiossira weissjlogii and Coscinodiscus perforatus were used as food. The presence of the predatory copepod Euchaeta elongata Esterly affected the swimming behavior and caused a significant reduction in the gut fullness of Pseudocalanus. Neither the presence of conspecifics nor other herbivorous grazers affected the gut fullness of any of the copepods, Feeding on algae by the omnivore Metridia was not significantly affected by the presence of Artemia nauplii as alternate prey, despite the fact that Artemia were ingested along with algae.

Grazing by zooplankton may influence the growth and abundance of phytoplankton (Riley, 1946; Steele, 1974). Because calanoid copepods are important grazers in the ocean, many factors that affect their feeding performance have been studied to estimate the grazing impact on the phytoplankton community. The most intensively studied are food concentration, size and quality of food particles, size and previous feeding history of the copepods, temperature, and light (reviewed by Conover and Huntley, 1980; Frost, 1980). While many of these studies were carried out in single-species experiments where the grazers were excluded from other animals, zooplankton typically occur in patches that are multi-species ag- gregates (Haury and Wiebe, 1982). Both the density and species composition of zooplankton patches can vary over a wide range of temporal scales. Thus, a herbivorous zooplankter must often survive and feed in an environment where encounter rates with potential competitors and predators are high. The feeding efficiency of a herbivorous zooplankter can be affected by the presence of other animals in several ways. First, food concentration may be reduced as a result of exploitation by other grazers. Second, feeding activity may be reduced as a result of direct behavioral interference. For example, the grazing rate of the freshwater copepod Diaptomus tyrrelli was decreased by chemicals produced by its potential competitor and predator Epischura lacustris (Folt and Goldman, 1981). Copepods also avoid physical contacts with other zooplankters by jumping away (Strickler, 1975). The jumping frequency of Diaptomus minutus is altered by the presence of other zooplankters (Wong et al., 1986). In areas of high animal density, avoidance reactions may exact a cost by reducing time available for feeding. Herbivorous copepods generate feeding currents to capture algae (Koehl and Strickler, 1981). Because the hydromechanical signals from these feeding currents may be sensed by tactile predators, potential prey may stop all feeding movements to reduce the risk of predation. Finally, omnivorous copepods may switch from herbivory to carnivory during periods of high prey density and low algal abundance (Landry, 1981). Even for copepods that are predominantly herbivorous, feeding on animals may reduce the need and time for grazing on phytoplankton. Omnivorous calanoid copepods may change their swimming pattern when exposed to zooplankton prey (Wong

573 574 BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988 and Sprules, 1986). Some swimming behaviors that facilitate the capture of zooplankton prey (e.g. ambush behavior) may decrease the efficiency of grazing on phytoplankton. Thus, it is somewhat surprising that the impact of other zooplankters on the feeding performance of herbivorous calanoid copepods has rarely been examined. The purpose of this research is to study the effects of other zooplankters on the grazing behavior of the marine calanoid copepods Pseudocalanus minutus (Kroy- er), Calanus pacificus Brodsky, and Metridia pacifica Brodsky. The specific ques- tions addressed in this study are: (1) Is the grazing behavior of Pseudocalanus, Calanus, and Metridia affected by the density of conspecifics? (2) Is the grazing behavior of Pseudocalanus, Cala nus, and Metridia affected by the presence of other grazers? (3) Is the grazing behavior of the omnivore Metridia (Haq, 1967) affected by the presence of alternate animal prey? (4) Is the grazing and swimming behavior of Pseudocalanus affected by the presence of its predator Euchaeta elongata Esterly (Yen, 1985).

MATERIALS AND METHODS

Calanoid copepods were collected between April and August 1986 from Saanich Inlet, Vancouver Island, B.c. (48°39'N, I 23°30'W). Pseudocalanus minutus, Calanus pacijicus, and Metridia pacifica were collected from 120-m daytime vertical hauls (0.2- or 0.3-mm mesh, 0.5-m mouth diameter). The zooplankton samples were immediately diluted with surface seawater in 15 liter carboys. Euchaeta elongata was caught in 150-m daytime oblique hauls (0.5-mm mesh, I-m mouth diameter) and sorted into 2 liter glass jars (1 to 5 copepods per jar) containing seawater from 20 to 30 m (temperature below 15°C). All animals were kept at 12°C under a reversed 14L: 10D light cycle in the laboratory. Concentrated surface phytoplankton from Saanich Inlet was added to the carboys to feed the herbivorous copepods every 1 or 2 days. Euchaeta were fed small zooplankters. The copepods were allowed at least 3 days to acclimatize to the conditions in the laboratory. Only copepods kept in the laboratory for more than 3 days but less than 10 days were used for experiments. Grazing experiments were carried out in 450-ml glass fleakers (Corning) containing 250 ml of filtered (1.5 I'm Whatman 934AH fiber glass filters) surface seawater. Experimental animals were sorted and transferred to the fleakers with wide-bore glass pipets. Pseudocalanus (prosome length 0.7-1.0 mm) was sorted under a stereomicroscope. Calanus (prosome length 2.0-2.6 mm), Metridia (prosome length 1.7-2.0 mm), Euchaeta (prosome length 4.6-5.4 mm), and Artemia nauplii (2-3 days post-hatch) were usually sorted without optical aids. With the exception of a few C5 and adult male Calanus, only adult female copepods were used. The animals were allowed a 0.5 to 1 h acclimation period. Because estimates of gut passage time were 0.4 h for Pseudocalanus (Wong, unpubl.), 0.4 h for Calanus and 0.6 h for Metridia (Mackas and Burns, 1986), animals were assumed to have empty guts when algal monocultures of Thalassiossira weissjlogii (8-12 I'm) or Coscinodiscus perforatus (70-80 I'm) were added to the fleakers to initiate grazing experiments. Both acclimation and grazing were carried out in darkness at 12°C. All experiments were performed between 1000 and 1500 h, and lasted from 1.5 to 2 h. For experiments with Coscinodiscus, the contents of the fleakers were stirred every 30 min to keep cells in suspension. Food concentration never changed more than 10% over the short duration of the experiment. At the end of each experiment, the contents of each fleaker were poured through a 102-l'm mesh. Copepods on the mesh were washed with filtered seawater and kept frozen in closed petri dishes until analysis. The amount of chlorophyll and its derived pigments in the guts was used as an index of the amount of phytoplankton ingested in the short interval prior to the termination of the grazing period. Copepods were removed from the filter and soaked overnight in 90% aqueous acetone. The fluorescence of the acetone extract before and after acidification with 5% BCL was measured with a Turner Designs fluorometer. Gut fullness (chlorophyll + phaeopigment) was calculated using the equations from Dagg (1983). The method assumes that chlorophyll-a was converted to phaeophorbide-a with 100% molar efficiency, and that no fluorescing compounds were lost due to digestion. Some authors (Dagg and Grill, 1980; Kiorboe et aI., 1982; 1985) have found close agreement between ingestion rates determined by gut fluorescence method and other direct measurements of filtration rates. Others argue that more than 90% of chlorophyll-derived pigment may at times be lost due to digestive processes (Conover et aI., 1986a; Wang and Conover, 1986). If pigment was indeed lost, the gut fluorescence method underestimated the amount of chlorophyll ingested. I assumed that the chemical process of pigment destruction during gut passage was not related to treatment effects such as density of copepods and WONG: EFFECTS OF COMPETITORS AND PREDATORS ON GRAZING 575

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Figure 1. Relationship between gut pigment content and copepod density. A) Calanus fed Thalas- siossira at 7.5 /lg Chla'liter-I; regression: Y = -0.18X + 10.56, t = -0.42, df = 30, P > 0.5. B) it1etridia fed Thalassiossira at 9.7 /lg Chla'liter-I; regression: Y = -0.70X + 15.25, t = -1.36, df = I 24, P > 0.1. C) Pseudocalanus fed Thalassiossira at 1.9 /lg Chla'liter- ; regression: Y = 0.02X + 0.26, t = 1.17, df= 32, P > 0.2. At I Pseudocalanus per fleaker, each point represents the average of two animals. All other points in this figure represent the mean for a given fleaker. presence of predators, and the fraction of pigment lost did not vary between treatment and control animals. One or two water samples (2-5 ml) from each fleaker were filtered with 0.45-/lm Millipore filters. Thc filters were extracted overnight in 90% aqueous acetone. Food concentration was measured fluorometrically as chlorophyll-a concentration. Although most of the experiments were done over several days to include more replicates, copepods used in each experiment were captured from the same net haul. Because treatment and control trials for each food density were always carried out at the same time, true biological effects could be evaluated by comparison between treatment and control animals at each food density. On the other hand, potential temporal variability in the physiological state of the copepods and the chlorophyll content of algal cells suggests that conclusions about the effect of food density should be interpreted with caution. The behavioral response of Pseudocalanus to the presence of Euchaeta was studied by videotaping prey swimming behavior with a Panasonic video camera (WV-1850) with a 12.5-mm lens. Five Pseudocalanus were transferred into each of two 30-ml tissue culture flasks (Corning) containing filtered (0.45 /lm Millipore) seawater and Thalassiossira (5.4 /lg Chla·liter-I). A single female Euchaeta was added to one of the flasks; the other one was used as control. The flasks were placed side by side in a temperature controlled room (12°C) and were illuminated by fiber optic lights produced by a tungsten lamp filtered to 780 nm (Schott Glass Filter RG-780). The animals were allowed to acclimate for I h before their swimming patterns were recorded. Videotaping was alternated between flasks at 10- min intervals and terminated after each flask had been recorded for 20 min. The arrangement of videotaping equipment and the procedures for analyzing swimming behavior were described in Wong and Sprules (1986).

RESULTS Effect of Conspecifics. - Calanus, Metridia, and Pseudocalanus were fed Thalas- siossira in fleakers containing various densities of conspecifics in an attempt to determine if their grazing behavior was influenced by intraspecific interference (Fig. 1). Linear regression was used to test for a relationship between gut fullness and number of copepods per container. Gut fullness did not vary with conspecific density for any of the copepods. In addition, gut fullness of animals feeding alone was never significantly different from gut fullness of animals feeding in the presence of conspecifics (> 1 animal per fleaker) (Wilcoxon two-sample tests, P > 0.5 for all three species). Effect of other Grazers. - The effect of other grazers on the gut fluorescence of Pseudocalanus was tested in a series of two species experiments. Four to six 576 BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, ]988

A 2.5 •. A 20 6.6. 2.0

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f \ , 0 , 0 ~-","---'------''---''''''''-Ij-'-- 4 5 6 11 12 0 2 4 6 B 12 119 Chi a . L-1 jAg Chla·L-1 Figure 2. (Left) Gut pigment content at different chlorophyll-a concentrations for Pseudocalanus fed Thalassiossira in the presence (open triangles) and absence (closed triangles) of Calanus (A) and ]\letridia (B). Each point represents the mean for a given fleaker. Figure 3. (Right) Gut pigment content at different chlorophyll-a concentrations for (A) Calanus fed Thalassiossira in the presence (open triangles) and absence (closed triangles) of Metridia, and (B) Metridia fed Thalassiossira in the presence (open triangles) and absence (closed triangles) of Calanus. Each point represents the mean of all Calanus or i\.1etridia in a given fleaker.

Pseudocalanus and two Calanus or Metridia were added to each treatment fleaker. Control f1eakers contained four to six Pseudocalanus alone. Thalassiossira was used as food. Because Pseudocalanus was never eaten or injured by the two larger copepods, any effect on its grazing activity was assumed to be the result of com- petitive interference, but not the result of predator avoidance. A nonparametric two-way ANOY A with treatment and food density as main effects was the most suitable test for the results of this and other experiments where the assumption of homogeneity of variance was not met. Unfortunately, the experiments were not carried out with equal numbers of replicates among food densities, and a parametric two-way ANOY A test was used instead. Neither Calanus nor Metridia (Fig. 2) influenced the gut fullness of Pseudocalanus (both P > 0.5). Pseudocalanus gut fullness increased with chlorophyll-a in both experiments (both P < 0.001). There was no evidence of interaction between the main effects in either experiments (both P > 0.05). The effect of Calanus and Metridia on the gut fullness of each other was tested in a series of two species experiments using Thalassiossira as food (Fig. 3). Four individuals of each species were added to each treatment fleaker. The gut fullness of the animals was measured and compared to that of single species controls containing eight individuals of each species alone. Two-way ANOYA with chlorophyll-a concentration and presence or absence of other grazer as main effects showed that gut fullness of Calanus and Metridia was not affected by either the WONG: EFFECTS OF COMPETITORS AND PREDATORS ON GRAZING 577

A 20 • •." /', i :a • ;, 15 .,. . • • . 00 • . r't> CD AI. 't> 12 • 0 /', t • • 10 • • ""!. ~ AI. 4 10 ---.------~--- I A , /', 8 --iii a 5 t •. "0 • • •. •. Q. ~ k- 'j .. • III a. 't> •. •. •. Q. 0 4 • 0 0 •. •.--"b U •. /', "" 2 •. 0 20 • /', B "" •. .•. • /', 0 . c /', " III <: 2. E AI. /', Ql 15 .~ AI. E • Q. • ,~ 20 AI. /', /', Q lJl c 10 • • "'" " i AI. • • 10 /', • . .._~. 5 _'0 •• - 000 .'.'.'-'!'-'-'-'-C a • • • • 0 .• 0 2 4 6 8 10 0 10 20 2. 30 3' 40 4' L _1 " nauplii . L-1 JJg Chla'

Figure 4. (Left) Gut pigment content at different chlorophyll-a concentrations for Metridia fed Thal- assiossira (A) and Coscinodiscus (B) in the presence (open triangles) and absence (closed triangles) of Artemia nauplii. Each point represents the mean for a given fleaker. Figure 5. (Right) Gut pigment content of Metridia (Y) in the presence of different concentrations of I Artemia nauplii (X). a) Thalassiossira at 5.3 ",g Chla·liter- ; regression: Y = -0.06X + 10.93, t = - 1.36, df = II, P = 0.2. b) Thalassiossira at 1.7 ",gChla'liter-I; regression: Y = -0.04X + 5.96, t I ~ - 1.33, df = 12, P > 0.2. c) Coscinodiscus at 4.2 ",gChla·liter- ; regression: Y = -0.04X + 8.54, t = -0.55, df = 17, P > 0.5. Each square, triangle, and diamond represents the mean for a given fleaker. Top panel (closed circles) shows predation rates by Metridia on Artemia at different prey densities during feeding experiments. presence ofthe other copepod (both P > 0.5) or chlorophyll-a concentration (both P > 0.5). Interactions between main effects were not significant in either experiment (both P > 0.1). Omnivory. - The effect of alternate animal prey on the grazing behavior of Me- tridia was tested in two series of experiments using Artemia nauplii as prey. These young Artemia nauplii did not feed on algae (Wong, unpub1.). Thus, the plant pigments in the guts of the copepods could not be derived from ingested prey. In the first series of experiments the gut fluorescence of Metridia grazing on various concentrations of Thalassiossira and Coscinodiscus was compared in the presence (10 per fleaker) and absence of Artemia nauplii (Fig. 4). Three to four copepods were used in each treatment and control fleaker. Because Metridia from two replicates where no predation occurred also contained no gut pigments, those replicates were not included in the analysis. The results were tested with two-way ANOVA with chlorophyll-a concentration and presence or absence of Artemia as main effects. The presence of Artemia had no effect on the gut fluorescence of lvfetridia in experiments with either algae. Chlorophyll-a concentration had a significant effect on gut fullness for Metridia fed with Thalassiossira (P < 0.001), but not with Coscinodiscus (P > 0.05). There was no significant interaction between the main effects (both P > 0.1). In a second series of experiments the concentration of algae was held constant 578 BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988

no predator 20 n = 71

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Figure 6. (Left) Gut pigment content at different chlorophyll-a concentrations for Pseudocalanus fed Thalassiossira in the presence (open triangles) and absence (closed triangles) of Euchaeta. Each point represents the mean for a given fleaker. Figure 7_ (Right) Frequency histograms of swimming speeds for Pseudocalanus in the presence and absence of Euchaeta. Probability of no difference in distribution between predator and no predator condition is <0.01 when tested as Chi-square contingency table with lumped classes (df = 8), and 0.05 when tested with Kolmogorov-Smirnov 2 sample test. while the density of Artemia nauplii was varied (Fig. 5). Again, three or four Metridia were used in each fleaker, and Metridia in fleakers containing animal prey were included in the analysis only if at least one prey had been eaten. Linear regression was used to test for a relationship between gut fluorescence and the number of alternate prey available. The results show that gut fluorescence of .i\1etridia was not influenced by the density of alternate animal prey. However, because the slopes of all three regressions were negative, this conclusion must be accepted with caution. Effect of Predator. - The effect of the presence of a predator (Euchaeta elongata) on the grazing rate of Pseudocalanus is shown in Figure 6. Each treatment fleaker contained four to six Pseudocalanus and one predator. Controls contained four to six Pseudocalanus alone. Thalassiossira was used as food for Pseudocalanus. Because predators that did not feed appeared to spend most of their time at the bottom of the container and rarely swam around to disturb the prey, replicates where no predation occurred (N = 9) were not included in the analysis. The presence of a predator caused a significant decrease in the gut fullness of Pseu- docalanus (Friedman's test, P < 0.005) (Zar, 1984). There was no significant effect due to food concentration (P > 0.05). Swimming Behavior. -Pseudocalanus spent most ofthe time alternating between swimming, when it glided smoothly using the mouthparts, and pausing, when it sank with its caudal-end first. Both swimming and sinking were occasionally interrupted by short jumps of about one or two body lengths. However, jumps were extremely rare and occupied a very small portion of the animal's time. Pseudocalanus exposed to a predator took shorter pauses (Table 1).The duration of swimming also appeared to be shorter, although not significantly so. The net result of these changes was that Pseudocalanus switched from swimming to pause more frequently. The circuitousness of the swimming path, as indicated by the WONG: EFFECTS OF COMPETITORS AND PREDATORS ON GRAZING 579

Table 1. Swimming pattern of Pseudocalanus minutus in the presence and absence of the predator Euchaeta elongata. Null hypothesis of no difference between predator and no predator condition tested by Student's {-test: ns = P > 0.1, * = P < 0.05

Swimming Swimming Pause Average speed duration duration speed (mm·s-') (s) (s) NGDR (mm's') No predator x 2.74 5.33 4.07 0.69 1.76 SE 0.30 0.87 0.67 0.06 0.23 ns ns * ns ns Predator x 2.23 3.84 2.23 0.57 2.24 SE 0.19 0.46 0.42 0.07 0.26 ratio of the linear distance between starting and ending points of a path to the actual distance traveled (NGDR) (Buskey, 1984) was not affected by the presence of Euchaeta. There was no change in the average overall speed and swimming speed either. The shift in behavior can be better illustrated by the frequency distribution of swimming speeds (Fig. 7). While the swimming speeds of Pseudacalanus in the control flask indicated slow cruising «2.5 mm's-l) and fast bursts (> 3 mm· S-I), Pseudacalanus exposed to Euchaeta swam more often at intermediate speeds and fast bursts were very rare.

DISCUSSION Variability in gut pigment among replicate samples was high. Some of the variabilities in Calanus were probably the result of including males and C5 individuals which ate less than adult females (Marshall and Orr, 1955). However, large variability of gut fullness was also observed among individual adult female copepods by Mackas and Burns (1986). In general, my results of gut fullness for all three species were within the range of those reported by other authors (Ni- colajsen et aI., 1983; Conover et aI., 1986b; Mackas and Burns, 1986). Gut fluorescence of Calanus, Metridia, and Pseudacalanus was not affected by the presence of conspecifics and other grazers. Phytoplankton are restricted to a narrow surface layer. Diurnal grazing rhythms observed in many herbivorous copepods suggested that feeding is confined to a short period each day (Mackas and Bohrer, 1976; Simard et aI., 1985). In addition, some copepods may aggregate for the purpose of mating or predator avoidance (Byron et aI., 1983; Hamner and Carleton, 1979; Hebert et aI., 1980). Thus, it is not surprising that they are able to feed efficiently in areas where zooplankton density is high. For example, arctic Pseudacalanus fed at rates comparable to the highest known for the genus in the 10 cm immediately under the ice where animal density was up to 103.liter- I (Conover et aI., 1986b). The presence of alternate Artemia nauplii prey did not significantly affect the herbivorous feeding of Metridia. Similarly, Lonsdale et ai. (1979) found that ingestion of algae by the omnivorous copepod Acartia tansa was independent of the presence of alternate animal prey. Feeding on animal food may be energetically beneficial for some omnivorous copepods (Corner et aI., 1976). In addition, predation may not interfere with grazing for two reasons. First, Metridia is not an ambush predator. It swims continuously (Anderson and Mackas, 1986), and probably could feed on algae while searching for prey. Second, handling time after prey capture could be very short because Artemia was not protected by thick armor. 580 BULLETINOFMARINESCIENCE,VOL.43,NO.3, 1988

The gut pigment content of Pseudocalanus was lower when the predator Eu- chaeta was present. Pseudocalanus must swim in order to encounter and capture algal particles. Mackas and Burns (1986) found that actively swimming Calanus had higher gut fluorescence than inactive but otherwise healthy animals. Encounter rates with predators increase with prey swimming speed (Gerritsen and Strickler, 1977). If gut fullness and swimming activity in Pseudocalanus were positively correlated, then animals with higher gut fluorescence would also have a higher probability of being eaten by predators than non-feeding animals. Selective re- moval of actively feeding individuals by predators would result in lower average gut fluorescence among the surviving prey. Alternatively, grazing rate could be reduced as the result of predator avoidance behavior. Herbivorous copepods may reduce the range of detection by vibration-sensitive predators by slowing down or stopping their appendage movements. Either behavior would also reduce feeding rates. Pseudocalanus modified their swimming behavior in the presence of Euchaeta. The distribution of swimming speeds, characterized by slightly faster cruising and much fewer high speed bursts, was quite different from that observed in control animals. The duration of pauses was also shortened. A decrease in the number of high speed bursts should reduce the frequency of detection by predators, but it is not clear how the probability of predation could be lowered by taking shorter pauses. Whether these behavioral changes directly affect food collection is un- known. The impact of reduced grazing on the phytoplankton community is interesting. Predators may influence the phytoplankton indirectly by reducing the number of grazers. They may also reduce the impact of herbivores on the phytoplankton by causing reductions in grazing rates, without reducing grazer abundance. Grazing pressure will be further reduced if interference by predators leads to starvation, mortality, and decreased fecundity among grazers. Some of the most important invertebrate planktivores in the sea are ambush- entangling predators (e.g., ctenophores and cnidarians) which rely on prey movements to initiate attacks and have high postcapture success (Greene, 1985). For small zooplankters such as copepods, the most effective defense against these predators is by sensing them from longer distances and to change swimming behavior to minimize encounter rates. If reduced feeding is a common defense in marine plankton communities, it should be most often used against predators which have high postencounter success. Becausethe gut fullness of Pseudocalanus was affectedby the predator Euchaeta, but not by Calanus and Metridia, two large but harmless copepods, it appears that Pseudocalanus can distinguish between potential predators and other non- predaceous grazers. Diaptomus tyrrelli fed at reduced rates when exposed to chemicals released into the water by its predator (Folt and Goldman, 1981). However, there is some evidence that the odor of the predator alone could not change the swimming pattern of Diaptomus minutus (Wong et al., 1986). Physical presence of the predator was required. At present, little is known about the relative importance of chemo- and mechanoreception in predator recognition. Future work should attempt to determine the mechanisms which trigger reduced feeding in herbivorous copepods.

ACKNOWLEDGMENTS

I am grateful to J. L. Littlepage and the Department of Biology, University of Victoria, for the use of the MSSV JOHN STRICKLAND.The ship crew and D. Moore provided valuable field assistance. I thank Y. Simard and D. L. Mackas for suggestions and discussions. D. L. Mackas and C. Ramcharan WONG: EFFECTS OF COMPETITORS AND PREDATORS ON GRAZING 581 provided valuable criticisms of the manuscript. The research was conducted while I was a postdoctoral fellowat the lOS and the U. of Victoria. Financial support was from a Natural Sciences and Engineering Research Council of Canada Postdoctoral Fellowship. The Zooplankton Behavior Symposium where this paper was presented was funded by Skidaway Institute of Oceanography.

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DATEACCEPTED: April 12, 1988,

ADDRESS: Institute of Ocean Sciences, P,O, Box 6000, Sidney, B,C V8L 4B2, Canada and Department of Biology, University of Victoria, Victoria, B.C. V8W 2Y2, Canada. PRESENTADDRESS: Department of Biology, The Chinese University of Hong Kong, Shatin, N. T., Hong Kong.

ApPENDIX: DISCUSSION AFTER WONG P. /Wayzaud: Do you know whether the gut clearance rate of the prey was affected by the predators? K. Wong: I did not measure that. But it seems unlikely that a physiological process such as gut passage could be affected so quickly. The experiments only lasted 2 h. W. Lampert: What can you conclude from these results in view of the high variability produced by the gut fluorescence method? K. Wong: Despite the variability, the effect of the predator was statistically significant, so the variability has actually strengthened the evidence for predator interference. II. Price: Since the Euchaeta densities in your experiments were quite high, do you think the observed decline in the prey's feeding rate is likely to occur in the field? K. Wong: I agree that the Euchaeta density was high. The importance of the prey's response at sea will depend on how long it takes an animal to "recover" after an encounter with a predator and to return to normal feeding. C Greene: You observed that the prey didn't slow down in the presence of the predator. This may be because, according to the model of Gerritsen and Strickler, encounter rates are not sensitive to prey speeds if the predator swims much more rapidly. K. Wong: Yes, I agree. P. Kremer: It might be interesting to look at another kind of predator, one like a ctenophore that does not lunge at its prey. K. Wong: With an ambush predator, I would anticipate that the prey copepods would swim more slowly to minimize their encounters.