J. Great Lakes Res. 23(3):369-381 Internat. Assoc. Great Lakes Res., 1997

The Feeding Ecology of the Cyclopoid Copepod Diacyclops thomasi

in Lake Ontario

LeBlanc J.S.1, W.D. Taylor1* & O.E. Johannsson2

1Department of Biology University of Waterloo Waterloo, Ontario N2L 3G1

2Department of Fisheries and Oceans Great Lakes Laboratory for Fisheries and Aquatic Sciences

Canada Centre for Inland Waters Burlington, Ontario L7R 4A6

Abstract. Diacyclops thomasi is the dominant crustacean zooplankton in Lake Onta-rio, making up much of the mesozooplankton biomass. However, the role of Diacyclops in the food-web dynamics of Lake Ontario is relatively unexplored. The feeding ecology of Diacyclops in Lake Ontario was examined by predator manipulation experiments, performed monthly from April 1991 until September 1991. Diacyclops consumed a variety of food items including: a mixotrophic dinoflagellate (Gymnodinium helveticum); ciliates (choreo-trichines); and other protozoans (heliozoans). Prey items were generally microplankton-sized (15-100 µm), motile, and without any hard external covering. Diacyclops had no effect on non-motile algae, small flagellates (<15 µm), or on organisms with tests or loricas. Keratella cochlearis, a loricate rotifer, was the most abundant rotifer through most of the stratification period but was not consumed by Diacyclops. However, we present evidence that Diacyclops preys on the eggs of this species without consuming the females to which the eggs are attached. Our results indicate that adult Diacyclops are selective omnivores in the pelagic food chain of Lake Ontario.

INDEX WORDS: Lake Ontario, Diacyclops thomasi, zooplankton, crustacean, copepod, fo-od webs.

Introduction The biomass of planktonic Crustacea in Lake Ontario is dominated by Diacyclops thomasi, a small cyclopoid copepod (Patalas 1969, Watson and Carpenter 1973, Johannsson 1987, Taylor et al. 1987). Diacyclops thomasi is present in most large lakes in the region (Carter et al. 1980, Keller and Pitblado 1989), but seldom comprises so much of the crustacean bio-mass. In a survey of 42 lakes north of Lake Ontario, cyclopoids comprised most of the sum-mer zooplankton biomass in only 6 lakes (Taylor and Carter, in press). Cyclopoid-dominated systems are common in tropical regions of Africa (Dumont 1980, Hecky 1984) and Asia (Fernando 1980). In temperate dimictic lakes, zooplankton communities are usually domi-nated by Cladocera and Calanoida. Generally, cyclopoids are more abundant in eutrophic lakes and in lakes with visual planktivores (Hessen et al. 1995, Almond et al. 1996). *Corresponding author E-mail: wdtay lor@sciborg .uwate r loo .ca

The cyclopoid-dominated system in Lake Ontario may be a result of predation pressure by alewives (Alosa pseudoharengus) and Mysis relicta, two effective planktivores with a limi-ted distribution in freshwater (Wells 1970, Taylor et al. 1987, Johannsson et al. 1991, Johan-nsson and O'Gorman 1991). The only lake we have sampled north of Lake Ontario to have comparably small zooplankton and such a high contribution from copepods, Charleston Lake, is also the only one with alewives (Taylor and Carter, in press). The microzooplank-ton-dominated grazer community of Lake Ontario (Mazumder et al. 1992) may provide ample prey for Diacyclops. Cyclopoids are thought to be omnivorous (Fryer 1957), but specific work on their feeding habits in natural systems is rarely done. They are generally classified as raptorial feeders, al-though some are classified as herbivores. There is evidence that some copepods are capable of highly selective feeding behaviour (Kerfoot 1978, Koehl and Strickler 1981), including prey-specific attack responses (Paffenhofer et al. 1982, Price et al. 1983) and "tasting" food at the mouth, resulting in rejection or acceptance of the food item (Vanderploeg et al. 1990, DeMott and Watson 1991). Raptorial cyclopoids, such as Diacyclops, are thought to depend primarily on mechanoreception, rather than chemoreception, to detect and capture prey (Ker-foot 1978, Kerfoot et al. 1980, Williamson 1983, DeMott and Watson 1991). Diacyclops has been described as "an extremely adept predator" due to its rapid attack responses (William-son and Gilbert 1980). Freshwater cyclopoids have been found to prey on a wide variety of other animals (Fryer 1957; Monakov 1972; Brandl and Fernando 1975a; 1975b, 1978; Lampitt 1978). Diacyclops will eat its own nauplii and copepodids, nauplii of other species, Cladocera, and some speci-es of rotifers (McQueen 1968, Lane 1979, Williamson 1983, Stemberger 1986, Vanderploeg et al. 1990). Dobberfuhl et al. (1997) report negative effects of D. thomasi on ciliates that result in positive effects among nano- and picoplankton. Fryer (1957) concluded from gut content analysis of several cyclopoid species that "indeterminate mush" often found in the stomachs must have been derived from soft-bodied organisms such as protozoans. Models of the Lake Ontario food web assumed that its zooplankton are non-selective her-bivores, e.g., Scavia (1979) and Halfon et al. (1996), despite that Diacyclops has the largest biomass and is likely at least partly carnivorous. Recent work has indicated that microzoo-plankton are the important grazers in Lake Ontario (Mazumder et al. 1992). Diacyclops is likely to be the major predator of those microzooplankton . The diet of Diacyclops, especially the extent of its carnivory, may have an important influ-ence on Lake Ontario's ecological efficiency, productive capacity, and tendency to biomagni-fy persistent, hydrophobic contaminants. The high contamination levels in Lake Ontario lake trout, relative to other lakes in the region (Bentzen et al. 1996) could be related to its unusual cyclopoid-dominated food web. The objective of this study was to describe the feeding of Diacyclops thomasi in the pelagic zone of Lake Ontario, especially the relative importance of algae versus microzooplankton in its diet and the breadth of its prey selection, through a series of predator-manipulation experiments.

Methods

WWaatteerr CCoolllleecctt iioonn

On six occasions from late April to late September, 1991, 20 L of water were collected from Station 41 (43°43'02"N, 78°01'36"W, station depth 130 m) near the center of Lake Ontario. Water was collected from a depth of 20 m, or, if collection was done at night, from 10 m. This collection pattern was adopted to adjust for the vertical migration of Diacyclops. A vertical net haul was also performed with a 64-um mesh net with a 0.5-m diameter opening. The net haul sampled from 20 m to the surface. The contents of the net haul were placed in a 10-L container with whole lake water. The zooplankton in this container were the source of experimental animals for treatments. After collection, water samples were stored in an air-

conditioned laboratory until the ship returned to the Canada Centre for Inland Waters in Burlington, approximately 8 h sailing time from Station 41. The water was transported to the University of Waterloo (~1 h from Burlington), where the predator-manipulation experi-ments were performed.

EExxppeerr iimmeennttaall MMaanniippuullaatt iioonn

The experimental manipulation began with the filtration of 5 L of whole lake water through a 202-µm mesh. Then the filtrate was passed through a glass-fiber filter (Whatman GF/F, nominal pore size: 0.7 µm) and used as filtered lake water for holding Diacyclops in petri dishes and for rinsing while setting up the experiments. The 202-µm filtrand, containing the copepods from 5 L of lake water, was reduced to a small volume (~30 mL) and placed into a zooplankton counting chamber with club soda (supersaturated CO2 solution) to facilitate enumeration. A stereoscopic microscope was used to count adult and immature Diacyclops, and this number was used as a rough estimate of abundance for setting abundances of adults in the experiments. On 25 July 1991 we estimated the natural density as only about 1 Dia-cyclops L-1. To avoid using very low predator densities, we set up the experiments as if the natural predator density was 2 L-1. Each experiment consisted of three replicates of four predator concentrations: zero Diacyc-lops (ON); natural density of adults (N); twice the natural density (2N); and three times the natural density (3N). Preparing the treatment bottles consisted of four steps: counting out the appropriate number of adult Diacyclops for each bottle; filtering the water for the treatment bottles; preserving 1 L of untreated lake water to assess initial prey densities; and adding the predators to the treatment bottles. Adult male and female Diacyclops were obtained for the experiments by decanting small vo-lumes (~25 mL) of the net haul water into a beaker. The copepods used in the treatments were not narcotized and were apparently healthy and active adults. They were removed from a hemispherical watch-glass with an eye dropper, the opening of which was large enough to allow the copepods to be picked up without damage. The Diacyclops to be used in each treatment were placed randomly into separate petri dishes containing filtered lake water until all treatments were ready. Beginning 27 June, equal numbers of each sex were added. When-ever possible, males with geniculate antennae and ovigerous females were used. The process of collecting experimental animals was done under laboratory conditions of light and tempe-rature. When all predators were ready, incubation bottles were prepared by filtering 1 L of whole lake water through a 202-µm nylon screen into clean, translucent 1-L polyethylene bottles. Beginning 27 June, the filtrand was returned to the incubation bottles after removing any copepods present, thereby ensuring that large prey items caught on the filter were returned to the incubation bottles. Including the filtering process, the longest that predators were isolated during preparation was ~3 h. When all treatment bottles were ready, the appropriate con-centration of Diacyclops was added and the four bottles were put into an incubator set to the temperature from which the water was collected. A single time-zero (t0) bottle, used to esti-mate initial prey densities, was preserved with Lugol's iodine. The entire procedure was repeated three times, resulting in three replicates of four treatment bottles and 3 t0 bottles, for a total of 15 bottles per experiment. Each treatment bottle was transferred to a 1-L glass bott-le and preserved with Lugol's iodine 24 h after being placed in the incubator. Nutrient additions are often used to reduce the likelihood of indirect effects on algal prey via nutrient regeneration in grazer manipulation experiments (e.g., Lehman and Sandgren 1985). We elected not to add nutrients for several reasons. First, we wanted to obtain information on prey growth rates under ambient nutrient conditions, and we did not want to affect prey quality given that the predator might be capable of selective feeding. Nutrient limitation is not strong in Lake Ontario relative to smaller temperate lakes (Lean et al. 1987) and we were manipulating only one member of the zooplankton community at near-natural densities. Lastly, many of the putative prey of interest were mixotrophic or heterotrophic, and unlikely

to be subject to indirect effects related to nutrient regeneration. Overall, we judged that it would be best to not add nutrients for these particular experiments. On 24 September 1991, the experiment was performed while on board the C.S.S. Limnos. Water was collected with a multiple-bottle Niskin sampler and zooplankton were collected with the same size net as in previous experiments. The experimental methods were identical except the treatment bottles were placed in black garbage bags to reduce light and incubated in a deck tank with flow-through lake water.

EEnnuummeerraatt iioonn ooff SSaammpplleess

For each sampling date, two replicates of each treatment were enumerated for phytoplankton and zooplankton using the Utermohl technique. Plankton were identified to genus, or to spe-cies when possible. Either a 50-mL or, more commonly, a 100-mL subsample was settled from each treatment bottle. In some instances (June, July, September), another 200-mL sample was counted to increase microzooplankton counts. Volumes were calculated for 20 individuals of each prey item on each date (10 from each of the 2 t0 replicates) using geomet-ric formulae.

AAnnaallyyss iiss ooff RReessuullttss

The effect of Diacyclops on any prey species or group was analyzed by calculating the instantaneous rate of population change using the following formula r = (ln(Nt) - ln(N0))/t, where Nt = number of prey at 24 h, No = number of prey at 0 h, t = 1 day. For each prey type, the slope of the relationship between instantaneous rate of population change and Diacyclops density was estimated using simple linear regression. The slope represents the mortality of that prey item per Diacyclops in a 1-L bottle, i.e., units are (day-1 Diacyclops -1). Standard errors of the slopes were calculated, and the probability that the slope was ≥ 0 was estimated with a one-tailed t-test. A linear model assumes clearance rates are constant across the predator density treatments (Frost 1972). This assumption is most likely to be true at low prey and predator densities, hence our modest predator manipulations (only 0N to 3N). While these modest manipulations make detection of weak effects difficult, they are advisable in view of the potentially complex predator-prey interactions involving cyclopoids and microplankton (e.g., Wickham 1995). We have chosen to report non-sig-nificant results, in addition to significant effects of Diacyclops on a particular prey, because the lack of an effect is equally important to our understanding of Diacyclops feeding. In the interest of brevity, we do not report here the results for all taxa that were enumerated, but instead provide results for selected genera and for higher taxa or morphological groups. A more complete summary of results can be found in LeBlanc (1992). To address concerns regarding violations of assumptions of linear regression, several cases, including both significant and non-significant regression results, were bootstrapped using the Resampling Stats program (Simon and Bruce 1991). In all cases, results of these tests confirmed results obtained by linear regression.

Results

2244 AApprr ii ll 11999911

Water was collected at a depth of 20 m and a temperature of 3.3°C. The density of adult Dia-cyclops thomasi was 2 Lr-1. Diatoms (mostly Melosira, Tabellaria, and Nitschzia) and small flagellates (mostly Rhodomonas and Chrysochromulina) were the most abundant phytoplan-kton. Microzooplankton, such as rotifers, protozoa, and nauplii, were few. None of the potential prey species enumerated showed the expected negative relationship between rate of increase and Diacyclops density (Table 1). Total protozoa in Table 1 were mostly choreo-trichine ciliates.

2299 MMaayy 11999911

Water was collected at a depth of 20 m and a temperature of 5.3°C. The density of adult Dia-cyclops was 3 L-1. The community was dominated by diatoms to a greater extent, and small flagellates to a lesser degree, than in April. The protozoan community had begun to diver-sify, but nauplii and rotifers were still relatively rare. The most negative slopes were for Os-cillatoria spp., "other algae" (mostly Ankistrodesmus), and Cryptomonas spp. (Table 2), but t-tests did not find any of the slopes significantly less than zero.

2277 JJuunnee 11999911

Water was collected at a depth of 15 m and a temperature of 9.0°C. In comparison to earlier experiments, there was a dramatic increase in the density of adult Diacyclops (13.4 L-1) and of late-stage (CIV-CV) copepodids. A density of 12 adult Diacyclops · L-1 was used as the natural density. The plankton community had also diversified with nonmotile green and blue -green algae and small flagellates dominating the phytoplankton (Table 3).

The highest mortality rate was for gravid rotifers (mostly Keratella cochlearis) and this slope was significantly less than zero. The slope for non-gravid rotifers was positive, but not signi-ficantly greater than zero. In contrast, Diacyclops had no significant effect on either K. coch-learis, the most abundant rotifer, or on the other rotifer species present (Kellicottia longispi-na, Keratella quadrata, or Polyarthra spp.) when gravid and non-gravid rotifers were analy-zed together. The impact on gravid rotifers was significant, but the slope was smaller than some non-signi-ficant impacts on previous dates. This is because the greater number of Diacyclops used produced a greater and more quantifiable effect, even though the effect per Diacyclops was not large. This rate can be multiplied by the Diacyclops density (12 L-1) to obtain a commu-nity mortality rate of 0.11· d-1. Comparable negative slopes were observed for some Cyanobacteria and Chlorophyta (about -0.01), but these were not significant even though the number of organisms counted was much greater.

2255 JJuullyy 11999911

In July, the water was collected from a depth of 10 m and at a temperature of 15.5°C. The natural density of adult Diacyclops was less than 1 L-1, but the experimental density was set at 2 L-1 to avoid excessively low densities in the incubation bottles. The community was dominated by non-motile green and blue-green algae, and the flagellate Cryptomonas spp. (Table 4). Nauplii were abundant. The three highest mortality rates for this date were filamentous diatoms, gravid rotifers, and Oscillatoria spp. (Table 4). Of these three, only gravid rotifers were significantly affected as judged by t-tests Once again, neither the most

abundant rotifer, K. cochlearis, nor the other rotifer species (mostly Polyarthra spp.) were affected by Diacyclops when gravid and non-gravid rotifers were analyzed together. The dinoflagellate Gymnodinium helveticum was also significantly affected by increasing densi-ties of Diacyclops.

2222 AAuugguusstt 11999911

Water was collected during the day, at a depth of 20 m and a temperature of 9°C. The natural density of adult Diacyclops was 6 L-1 and nauplii were still abundant. The plankton was aga-in dominated by non-motile green and blue-green algae and flagellates, while rotifer popula-tions had decreased (Table 5). The strongest effects of Diacyclops were on G. helveticum, "other algae" (mostly Pediastrum), and the ciliate Codonella. None of these slopes were significantly different from zero, although the probability value for G. helveticum was very close.

2244 SSeepptteemmbbeerr 11999911

In September, water was collected at a depth of 10 m with a temperature of 17.9°C. The natural density of Diacyclops was 2 L-1. Again, non-motile green and blue-green algae and flagellates were the most numerous plankton. Rotifers reached their highest abundance, and protozoa, while not numerically important, were more diverse than in any other month (Table 6). The three highest mortality rates were for other protozoa (mostly heliozoans), large choreotrichine ciliates, and small choreotrichine ciliates. All three of these rates were significantly less than zero, and corresponded to community mortality rates 0.36 d-1, 0.24 d-1, and 0.18 d-1.

Discussion

DDaatteess oonn wwhhiicchh NNoo EEffffeeccttss WWeerree DDeetteecctteedd

On 24 April, 29 May, and 22 August 1991, we could not detect an effect of Diacyclops on other members of the planktonic community. We believe that these negative results are beca-use the temperature and/or the Diacyclops density were low, making the impact of the Dia-cyclops less and more difficult to detect in our experiments. Predation can be demonstrated by manipulation experiments only when the conditions allow the density of predators present in the experimental vessels to consume a quantifiable proportion of the prey. Temperature was low (< 10°C) in all experiments where feeding was not demonstrated. Despite the fact that the observed effects were not significant, the taxa with the most negative slopes on these occasions, "other" dinoflagellates (which included G. helveticum) and "protozoa" (mostly choreotrichines), were significantly affected by Diacyclops on other dates. This would sug-gest that these organisms were probably being consumed, just not at rates high enough to be quantified with our protocol.

RRoott ii ffeerrss aanndd RRoott ii ffeerr EEggggss

The results from June and July indicate that either gravid rotifers or their eggs were preyed upon by Diacyclops. However, significant effects were not detected for individual rotifer species, non-gravid rotifers, for unattached eggs, or for total rotifers. Possible explanations for these observations include: gravid rotifers were eaten while non-gravid ones were not; eggs were removed from gravid rotifers and consumed; or, eggs were being jettisoned during predator-prey encounters. Results from both June and July do not support the third expla-nation, because there was no relationship between the number of unattached eggs in experi-mental vessels and density of Diacyclops. During the 25 June experiments, when the counts are highest and our power to detect effects is greatest, the number of non-gravid rotifers actually increased as one would expect if the eggs were being removed by Diacyclops. Keratella cochlearis was the most abundant rotifer in Lake Ontario on both dates when gra-vid rotifers were affected. Keratella spp. have been found to be highly resistant to predation by a number of cyclopoid species (Shcherbina 1970, Vardapetyan 1972, Brandl and Fernan-do 1978, Gilbert and Williamson 1978, Williamson 1983, Roche 1990) including Diacyclops (Williamson 1983, Stemberger 1986). The hard lorica of Keratella spp. appears to protect them from ingestion (Gilbert and Williamson 1978). Stemberger (1986) found D. thomasi ingested K. cochlearis at a rate ten times lower than it ingested Synchaeta spp., a preferred illoricate rotifer. However, the eggs of K. cochlearis are not protected by the lorica. Little research has been done on the interaction between gravid rotifers and copepods, but two studies have indicated that cyclopoids are able to remove eggs from these loricate rotifers and consume them (Shcherbina 1970, Roche 1990). We also assessed the probability that Diacyclops consumed gravid rotifers by estimating ingestion. We calculated the amount ingested relative to the body weight of Diacyclops assuming only eggs were eaten, and for comparison, assuming the entire gravid female was consumed. These biomass estimates were made for all dates on which Diacyclops had a significant effect on the population, although gravid rotifers were only present in June and July. If the consumption of eggs is assumed, mass-specific biomass consumption ranges up to 14% • day-1, which is well within published consumption ranges for carnivorous cyclo-poids (Brandl and Fernando 1975a, 1975b). If we assume that gravid females with their eggs are consumed, these rates would approximately double, but would still be tenable. However, if the mortality rate for gravid rotifers is applied to all rotifers, mass-specific biomass consumption ranges up to 225%. This value is much higher than previous observations for copepods; the highest is 109%, with most values around 50% (Monakov 1972, Brandl and Fernando 1975a, 1975b). We believe that these considerations of our data, and previous ob-

servations by others, strongly suggest that Diacyclops eats eggs of rotifers in Lake Ontario. This behavior would have a substantial impact on rotifer population dynamics during the mid-summer even if adults are not harmed. The clearance rates on rotifer eggs was 9 mL • Diacyclops'1 • d-1 in June and 160 mL • Diacyclops-1 • d-1 in July. This increase in clearance rates between the two dates could be caused by a number of factors: higher temperature in July (15.5°C versus 9°C); lower density of gravid rotifers in July (68 L-1 in July versus 265 L-1); and/or an increase in the relative proportion of illoricate rotifers in July, primarily Poly-arthra spp. as opposed to К. cochlearis in June. Polyarthra appear to be highly edible by Diacyclops because they are large and soft-bodied. However, this genus resists predation by virtue of its behavior (Williamson 1983). Polyarthra respond to impending attack by rapidly "skipping" a large distance (up to 280 body lengths) away from the predator using its paddle-like appendages (Vanderploeg 1990). Unlike the strategy employed by Keratella of possess-ing an ingestion-resistant lorica, the skipping behavior of Polyarthra would also protect its egg.

PPrroott iissttss aass PPrreeyy ffoorr DDiiaaccyyccllooppss

Gymnodinium helveticum, a large (~40 µm in length) mixotrophic dinoflagellate, was frequ-ently abundant and was negatively affected by Diacyclops during most experiments. Being both large and motile, it may have a high probability of detection by the mechanoreceptors of Diacyclops. It also lacks a theca, making it vulnerable to ingestion following capture. In Williamson's (1983) review of invertebrate predation, he indicated that many rotifers and crustaceans with soft bodies are vulnerable to predation by cyclopoids. This may hold true for athecate dinoflagellates. Several studies have noted that copepod clearance rates on ciliates are often higher than on other planktonic organisms (Wiadnyana and Rassoulzadegan 1989, Dolan 1991, Hartmann 1991, Turner and Graneli 1992). Protozoa may be an important food source since they con-tain amino acids and lipids not found in sufficient quantities in other food items such as phy-toplankton and detritus (Stoecker and Capuzzo 1990, Gifford 1991). Schulze and Folt (1990) found that although autotrophic nanoplankton was consumed by Epischura lacustris, animal prey was necessary for sustained growth and reproduction. D. thomasi has been successfully raised for many years on a diet of only Paramecium, a large ciliate (Brandl 1973). The three groups of protozoa significantly affected in this study were large choreotrichines (~40 µm, mostly Strombidium spp. and Strobilidium spp.), small choreotrichines (~15-20 µm, mostly Strobilidium spp. and Halteria spp.), and "other" protozoa (mostly heliozoans, ~25 µm). All three groups of protists significantly affected by Diacyclops are illoricate. Heliozoa are non-motile and large, especially if axopods are included in their radius. A preference for spined diatoms over non-spined forms has been noted in another copepod species and was attributed to an increased probability of detection by the mechanoreceptors (Gifford et al. 1981).

OOrrggaanniissmmss NNoott CCoonnssuummeedd bbyy DDiiaaccyyccllooppss

The advantage of the predator manipulation method is that predation rates on all potential prey can be examined with sufficient effort in enumeration. However, in practice, only reaso-nably abundant prey species can be assessed. Therefore, the effects on rare prey items cannot be adequately assessed with this method. That a slope is not significantly less than zero in these experiments does not prove that Diacyclops does not consume that taxon. Nonetheless, some generalities hold for the taxa on which we could not demonstrate an effect of Diacyc-lops. Nanoplankton (whether ciliates, flagellates, diatoms, or other algae < 20 µm) were not significantly affected by Diacyclops. Small choreotrichines were significantly affected on one date, but these are mostly 15 to 25 µm. Dobberfuhl et al. (1997) observed negative ef-fects of Diacyclops on ciliates as small as Mesodinium sp. (5,000 µm3 or about 25 µm). Raptorial copepods are thought to be inefficient consumers of nanoplankton (Stoecker and Capuzzo 1985, Gifford 1991).

Some microzooplankton were not affected by Diacyclops. For example, effects on the roti-fers Keratella cochlearis and Polyarthra spp. were detected only when gravid females were counted separately. While rotifers generally represent an available size class for copepods, it appears that Diacyclops has only a small impact on adults of the most abundant species. Synchaeta and other soft-bodied rotifers known to be vulnerable to Diacyclops were not en-countered in numbers sufficient to quantify their mortality. In addition to certain rotifer taxa, many ciliate microzooplankton were apparently unaffected by the presence of Diacyclops. These included the loricate ciliate, Codonella cratera, and the armored Coleps. Loricate forms are consumed by some copepods (Pierce and Turner 1992 and references therein) but apparently not by Diacyclops in Lake Ontario. The ciliate lorica, with agglutinated particles, works as an anti-predatory device by allowing the ciliate to sink quickly out of the path of a feeding zooplankter (Capriulo et al. 1982). The importance of algae, especially diatoms, as a food source for copepods has been stressed in some recent studies (Lair 1992, Adrian 1991). We must concede that, although we could not demonstrate consumption of phytoplankton, a low clearance rate on an abundant phyto-plankton species could yield a comparable amount of food relative to a higher and more de-monstrable clearance rate on microzooplankton. However, such a low clearance rate is probably of small significance to the phytoplankton. On several occasions, the slopes we estimated for certain phytoplankton (e.g., Cryptomonas on 29 May, Oscillatoria sp. and filamentous diatoms on 25 July, Rhodomonas on 24 September) approached statistical significance and were comparable to slopes we found to be significant for animal prey. This is despite the fact that phytoplankton are more numerous and our counts for them were generally much higher. It should have been easier to demonstrate feeding on phytoplankton if clearance rates were comparable. In view of the danger of type I error with so many reg-ression analyses, we do not wish to suggest that these organisms are consumed.

OObbsseerrvveedd CClleeaarraannccee aanndd FFeeeeddiinngg RRaatteess

Clearance rates for organisms significantly affected by Diacyclops ranged from 9-180 mL · Diacyclops-1 · d-1. In laboratory experiments with Diacyclops feeding on Synchaeta at 8°C, Stem-berger (1986) reported values of 38-123 mL · Diacyclops-1 · d-1. Given the temperature range, our clearance rates agree with these laboratory rates. The daily food consumption by Diacyclops was estimated as 6.9% of body weight in June, 16% in July, and 15% in September. These figures are within the range of published values (Brandl and Fernando 1975b, Lampitt 1978) which range from 10-109%. In a study of Cyclops spp. (Brandl and Fernando 1975a), the range was found to be narrower, between 4-51% day-1, which also agrees with this study.

PPootteenntt iiaall SSiiggnnii ff iiccaannccee ooff SSeexx aanndd SSttaaggee

Two shortcomings of this study are that we only examined the effect of adult Diacyclops and that we used equal numbers of males and females. Immature copepodids were usually more abundant than adults and, at certain times of the year, nauplii are also abundant. Given the different sizes of these stages (NI: ~0.15 mm; CVI: ~1.0 mm), it is likely that they have different diets. Although we used equal numbers of males and females in our experiments, several studies have documented significant differences in clearance rates between male and female copepods (Lampitt 1978, Adrian 1991, Lair 1992, Maier 1992). Females generally exhibit higher clearance rates and are more predatory. In some species, adult males may not feed at all (0resland 1991). Female to male ratios in excess of 2:1 have been recorded in the Great Lakes (Davis 1969). These differences of sex and stage need to be understood to fully assess the impact of Diacyclops.

IImmpplliiccaatt iioonnss

The results of this study suggest that adults of D. thomasi are primarily carnivorous. The only alga for which we were able to demonstrate an impact by Diacyclops was the mixo-trophic dinoflagellate Gymnodinium helveticum, which consumes other phytoplankton. Other recent work on copepod feeding has suggested a similar conclusion; the impacts of cyclopoid copepods are most intense on micro-zooplankton grazers, not phytoplankton, despite the lower abundance of these microzooplankton grazers relative to phytoplankton in most systems (Turner and Graneli 1992). Diacyclops may play a significant role in shaping the microzooplankton community of Lake Ontario. The two most common Lake Ontario rotifers, Keratella cochlearis and Polyarthra spp., are particularly resistant to predation by Diacyclops (Williamson 1983), although our results suggest that Diacyclops exacts a heavy toll on rotifer eggs. The relative impact on ciliates, with shorter generation times, may be less. Ciliate abundance is controlled more by food availability than by predation from upper trophic levels (Stenson 1984) and predation effects may be highly seasonal (Taylor and Johannsson 1991). Our study confirms that Diacyclops thomasi, the most abundant crustacean zooplankton in Lake Ontario, is highly selective and largely carnivorous, and is consistent with the view that this Great Lake has a particularly long and inefficient food chain.

Acknowledgments This study was supported by an NSERC Canada Research Grant to WDT, and by Depart-ment of Fisheries and Oceans who provided ship time and the technical assistance of Karen Ralph. We thank S.M. Smith, University of Waterloo, for his help with non-parametric sta-tistics.