Density-dependent predation of early instar Chaoborus feeding on multispecies prey assemblages l

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1 Limnol. Omanogr., 33(2), 1988, , by the American Society of Limnology and Oceanography, Inc. Density-dependent predation of early instar Chaoborus feeding on multispecies prey assemblages l Marianne V. Moore2 Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire Abstract Prey selectivity and predation rates by second-instar Chaoborus punctipennis feeding on a threcspecies rotifer assemblage were dctermincd in a laboratory experiment. Chaoborus became less selective at the two highest of five total prey densities which ranged from 180-2,880 prey liter-. This change in selectivity seemingly contradicts optimal foraging theory, but may have occurred because Chaoborus used different search tactics at different prey densities. When feeding on rotifers, Chaoborus exhibited a type 2 functional response and achieved predation rates among the highest reported for an aquatic invertebrate predator. Chaoborus predation rates were high primarily because of rapid handling times (ingestion and digestion) which were quantified with Holling s disk equation and direct observations. Digestion was particularly rapid with crop evacuation times as brief as min for a food bolus of soft-bodied Synchaeta pectinata. The use of functional response experiments for determining Chaoborus predation rates is recommended over the application of digestion time to crop contents of field-collected Chaoborus, because crop passage time of Chaoborus is variable. Density-dependent changes in predator feeding rates and prey selectivity may influence the nutrition of predators, the behavior and life history characteristics of their prey, or both. Yet few functional response experiments have investigated the response of an aquatic invertebrate predator to a multispecies prey assemblage over a range of total prey densities (Peckarsky 1984). Rotifers often comprise much of the diet biomass of early instar (I and II) Chaoborus (Saunders 1980; Chimney et al. 1981; Hare and Carter 1987; Moore 1988), and field manipulations suggest that rotifer abundance influences survivorship of these instars (Neil1 and Peacock 1980; Neil1 1985). Although predation rates for several copepod predators that feed extensively on rotifers have been determined (Williamson 1983; Stemberger 1986; Williamson and Butler 1986), there is little or no information about predation rates of early instar Chaoborus. Fedorenko (1975b) quantified in situ predation rates of second-instar Chaoborus americanus and Chaoborus trivittatus feeding on copepod prey, and Moore -- * This work was supported by grants from the International Women s Fishing Association, the Theodore Roosevelt Memorial Fund, and the Dartmouth College Cramer Fund. 2 Present address: Zoology Department, Miami University, Oxford, Ohio and Gilbert (1987) determined predation rates of early instar Chaoborus punctipennis on five rotifer species, but only at one prey density. Clearly, feeding rate information for Chaoborus preying on rotifers is necessary to predict the effects of this predator on zooplankton communities and evaluate the potential for competition between Chaoborus and copepod predators. There are several ways of measuring predation rates for Chaoborus. The method that most closely duplicates the physical and biological environment of predator and prey is in situ predation experiments with enclosures (Fedorenko 197 5b) or submerged traps 256 (Kajak and Rybak 1979). To use this approach successfully, however, requires prior estimates of the ingestion rate of Chaoborus for a given food level and prey assemblage so that an appropriate experimental dura- tion is used. If the enclosure experiment is too long, Chaoborus depletes the prey population and the experimental measurement of predation rate is confounded by intrusion of a second variable-prey abundance. Another method for estimating predation rates recognizes that in situ feeding rates can be estimated from the predator s digestion rate and the average amount of food in the gut (or crop) of field-collected predators. This method, which I refer to as the gut-content method, was first developed by Bajkov (1935) to describe feeding in fish. Although

2 Juvenile Chaoborus predation 257 it has not been used to estimate predation rates for Chaoborus, it has been applied to a diverse array of aquatic predators: chaetognaths (Feigenbaum and Maris 1984), mysids (Rybock 1978), and larval predatory insects including stonefly (Allan 1982) and caddisfly (Hildrew and Townsend 1982) larvae. Still another method for estimating predation rates includes laboratory feeding experiments conducted at various prey densities (Pastorok 1980b; Vinyard and Menger 1980; Spitze 1985). Such functional response experiments yield not only estimates of predation rate but, when modeled (i.e. with Holling s disk equation), can reveal addi tional information about the predation sequence (e.g. search rate, handling time). Laboratory experiments can also elucidate changes in prey selectivity with increasing prey density when experiments are conducted with mixed-species assemblages. The purposes of my study were to determine predation rates of second-instar C. punctipennis feeding on mixed-species assemblages of rotifers at densities commonly found in both oligotrophic and eutrophic lakes, to examine prey selectivity of Chaoborus when feeding on multispecies prey assemblages that differ in total prey densities, and to compare estimates of Chaoborus predation rates determined with a functional response experiment to those calculated with the gut-content method. I thank R. Stemberger, C. Folt, and J. Gilbert for discussions of this study, and M. Bean for assistance with rotifer and algal culturing. C. Folt, J. Gilbert, J. Haney, R. Holmes, and N. Rodenhouse provided suggestions that improved the manuscript. Methods Rotifer species were isolated from local lakes and batch cultured (Stemberger 198 1) in filtered (Whatman GFK glass-fiber filters) lake water from Post Pond, Lyme, New Hampshire. EDTA (5.9 x 1 Oh6 M Na,) was added to the water to prevent toxicity from heavy metals. EDTA is also used in the laboratory culturing of marine ciliates (Gifford 1985). Rotifers were fed cryptomonad algae (Cryptomonas erosa or Cryptomonas sp.). Second-instar Chaoborus individuals used in the functional response experiments were cultured from eggs laid in the laboratory (Moore 1986). Thus, animals of known age were used in studies of feeding rates. Chaoborus larvae used for gut passage experiments were collected from Post Pond, New Hampshire. All Chaoborus larvae were maintained in filtered Post Pond water containing EDTA as described above and fed laboratory-cultured or field-collected (48- pm-mesh net) rotifers. Functional response -Three rotifer species, Synchaeta pectinata, Keratella testudo, and Keratella cochlearis f. typica (spined form), were offered in equal proportions but at different total densities to second-instar Chaoborus. (See figure 1 of Moore and Gilbert 1987 for illustrations of prey species.) Synchaeta pectinata, a softbodied rotifer, was the largest of the three prey species (Table 1). Both loricate Keratella species were similar in shape except that K. cochlearis typica had a single posterior spine and K. testudo lacked posterior spines. The lorica of K. testudo was significantly wider (t = 6.8, 23 df, P < 0.01) and longer (t = 20.6, 23 df, P < 0.01) than that of K. cochlearis typica. Several procedures were used to standardize predator hunger level. Because insects usually exhibit little or no feeding immediately before or after a moult (Bernays and Simpson 1982), I used Chaoborus individuals that were h into the second stadium. Before the experiments, individuals were offered cultured or field-collected prey ad libitum at 20 C for 16 h and then transferred to containers lacking prey for a 2-h interval. At the end of this starvation interval, all individuals had empty crops. The functional response experiment was conducted at five different total prey densities (180, 360, 720, 1,440, and 2,880 liter- ). These densities span the range reported for rotifers in oligotrophic and eutrophic lakes (Orcutt and Pace 1984). Experi mental containers were prepared by transferring rotifer prey and two individual Chaoborus into a 150-ml beaker containing 1.5 ml of Cryptomonas spp. algae and enough filtered Post Pond water with EDTA to achieve a total volume of 100 ml. Additions of 6, 12, 24, 48, and 96 individuals of each of the three rotifer species were made

3 258 Moore Table 1. Mean body length (pm) and width (pm) k 1 SD for the prey species used in the functional response experiment and to determine gut passage time. Body length includes anterior and posterior spines. N is the number of individuals measured FEZ-- 5-p ~- Kotikr species N Length (pm) Width (wm) Synchaeta pectinata Keratella test udo Keratella cochlearis f. typica Keratella cochlearis f. tccta - I tl k k k k7.4 57k t2.7 54k4.2 - to the appropriate containers to achieve total prey densities. Four experimental and three control (lacking Chaoborus) containers were prepared for each total prey density and placed in the dark at 20 C for I h. Containers were not rotated during the experiment because of the sensitivity of Chaoborus to water movements and vibrations. A visual inspection of the containers after 1 h revealed that prey species were swimming above the bottom and had not clumped or settled during the experiment. At the end of the feeding period, the remaining rotifers were counted under 50 x with a stereomicroscope. Recovery of rotifers in control containers ranged from 94 to 97%. Total prey depletion in experimental containers averaged only 16% (SD = 10.5%), thus ensuring that Chaoborus experienced a nearly uniform prey density throughout the feeding period. Diel periodicity of feeding by Chaoborus was not examined in this experiment. The number of rotifers ingested at each density was adjusted using the mean number recovered for the controls, and these data were fit to Holling s ( 1959) disk equa- tion. This equation describes the number of prey eaten (IV,) as a hyperbolic function of prey density (N) and can be written as a NTP N, = 1 + a T))N (1) where P is the number of predators, T the length of time the predator and prey arc exposed to one another, a the attack constant, and T/, the handling time per prey item. T/, in this model includes the time the predator spends capturing, ingesting, digesting, and egesting prey. This definition of handling time is used throughout this paper. The asymptote of the functional re- sponse curve is determined by T,*, because as the rate of prey capture increases, the predator spends an increasing proportion of its total time handling prey (N,,, = T/T,). The rate at which this asymptote is approached is a function of the attack constant (a ) which depends on the ability of the predator to search for, detect, and capture prey. Both T, and a are constants, meaning that the model assumes a fixed predatorprey encounter rate, a constant attack rate by the predator, and invariant handling times for all prey items. These assumptions are met when prey depletion is minimal and predator satiation does not occur. I used a nonlinear least-squares regression technique (NLIN program with Secant method: SAS Inst. 1982) to fit Holling s disk equation to the experimental data. This nonlinear procedure yields parameter estimates of a and Th that are considerably less biased than those obtained from procedures in which the data are transformed to linearize the functional response (Juliano and Williams 1985; Houck and Strauss 1985). Initial seed values used for the nonlinear regression were obtained from a linearization offlolling s disk equation with Livdahl and Stiven s ( 198 3) reciprocal transformation. Parameter estimates describing the functional response of Chaoborus feeding on K. cochlearis typica and S. pectinata (i.e. Table 2) were used to predict predation rates on K. cochlearis typica and Filinia longiseta in Post F ond. Chaoborus feeding rates on Synchaeta are assumed to be equal to those for Filinia because both rotifer species are softbodied and highly selected by Chaoborus (Moore and Gilbert 1987; Moore 1988). These predation rates were then compared to those estimated with the gut-content method (described below).

4 Juvenile Chaoborus predation 259 Table 2. Estimates (k 1 SE) for the parameters (a and T,,) of Helling s generalized model of the functional rcsponsc for Chaoborus feeding on an asscmblagc of three rotifer species. The cocffkient of determination (r*) measures the proportion of the total variance in prediction rates that is explained by Helling s model. Speciesspecific a and T,, values apply only to the situation where the three rotifer species arc equally abundant. Ilotlrcr prey I (0.1 liter h I) T, (W r Total rotifers Synchaeta pectinata Kcralella testudo Keratella cochlearis f. typica 0.17~ a kO to ~ kO tO kO Selectivity- Chaoborus selectivity for rotifer prey at different total prey densities was examined with the functional response data. Per capita clearance rates (ml Chaoborus - h-l), which represent the ability of Chaoborus to harvest different prey, were correctcd for controls and calculated after Gauld (195 1). Prey selectivity ( Wi) was determined for each prey density with standardized clearance rates (Vanderploeg and Scavia 1979). Possible values of W, range from 0 to 1.0, with neutral selectivity (random feeding) equal to l/n, where n is the number of prey types. Because of variance heterogeneity, a nonparametric test (Kruskal-Wallis test) was used to compare median Wi values for each prey type among prey densities and among prey species within each density. Mann-Whitney U-tests were used to make pairwise comparisons between 1+ 1 values (Sokal and Rohlf I98 1). Gut passage kinetics-two methods, a time-series predation experiment (Stember- ger 1986) and direct observations, were used to estimate gut passage kinetics of rotifer prey through Chaoborus at temperatures of C. The time-series experiment dc- tcrmined the time it takes a starved Chaoborus to reach a steady state ingestion rate when feeding on Synchaeta. Gut passage time can be estimated as the time when a steady state ingestion rate begins, because at this time the ingested volume of prey should approximately equal losses from defecation, absorption, and assimilation (Stcmberger 1986). Chaoborus individuals (four replicates containing one Chaoborus each in 50 ml) were exposed to a constant prey density (600 Synchaeta liter- ) over a 6-h feeding period. It was accomplished by transferring Chaoborus individuals to new containers with 600 Synchaeta liter- at successive intervals (15 min, 15 min, 1 h, 1 h, 2 h, 2h). The brief initial intervals were chosen to ensure detection of the anticipatcd drop in feeding rates from maximal initial rates to lower steady state rates. After each time interval, the uneaten rotifers were counted in experimental and control (three replicates lacking Chaoborus) containers. Gut evacuation time was observed dircctly for nine Chaoborus larvae feeding separately on both a soft-bodied and loricatc rotifer species. Chaoborus swallows prey whole, and mastication and preliminary digestion occur in the muscular crop. Only liquid prey material passes into the intes- tine, where absorption occurs. Undigested remains ofboth crustacean prey and loricate rotifers are regurgitated (Pastorok 1980a; Moore and Gilbert 1987). Chaoborus gut evacuation time was directly observed with the following methods. All the larvae were starved for 4-6 h before transferring them to a dense concentration (N 70 per 5 ml) of rotifers. Three Chaoborus individuals were exposed to S. pectinata and six to Keratella cochlearis f. tecta (unspincd form). Both rotifer species had previously ingested cryptomonad algae which color the guts of the rotifers reddish-brown. When Synchaeta or K. cochlearis tecta was eaten by Chaoborus the cryptomonad algae in the rotifers spread throughout the food mass, making it clearly visible through the transparent body of Chaoborus. When the crops of individual Chaoborus were half to completely full (usually after 5-20 min of fceding), each Chaoborus was transferred to a 5-ml Petri dish and deprived of food until its crop and intestine were completely empty. The position of the food bolus in the crop and the position of liquid prey material in the intestinal tube were observed with a

5 260 Moore 7 6 S. pectinata T Total prey density (rotifers / 100 ml) Fig. 1. Functional response curve of second-instar,chaohorus punctipennis preying on a three-species asscmblage ofrotifcrs. Svnchaeta tmtinata. Keratella tesfudo, aid Keratella cochlearis typica were offered in equal proportions at five total prey densities. Mean ingestion rates for each density (n = 4, &SD) are shown by squares and vertical bars. The line represents the predicted relationship between ingestion rate and prey density when Holling s disk equation is fitted to the functional rcsponsc data. stereomicroscope (40-50 X) and recorded at regular intervals on Xeroxed drawings of the digestive system of Chaoborus (Main 1953). The length of time between successive observations ranged from 15 min during the first hour of food deprivation to 60 min after 1.5 h. Although these visual estimates were made after Chaoborus ceased feeding, they were compatible with estimates from the time-series predation experiments, which assumed that gut passage time is a function of ingestion rate, because Chaoborus ingestion (swallowing) time for rotifers is very brief (mean = 1.9 s for S. pectinata; Moore and Gilbert 1987) and probably had a negligible effect on ingestion rates. Predation rate estimates for field-collected Chaoborus (Moore 198 8) were calculated with the equation NPC E R = - GPT (2) where FR is the feeding rate (rotifers per Chaoborus h-l), NPC the average number of rotifers per Chaoborus crop (Moore 1 SSS), and GPT the Chaoborus gut passage time in h, here estimated as time to equilibrium and time to complete evacuation. Rates at 2-1 -, j *' I I I I K. testudo I typica Fig. 2. Functional response curves of ingestion rates (t-sd) for second-instar Chaoborus punctipennis preying on each of three rotifer species (as in Fig. I). All three rotifers were offered to Chaoborus simultaneously and in equal proportions. Curved lines explained in legend to Fig. 1. which Chaoborus fed on the loricate rotifer, K. cochlearis typica, and the soft-bodied rotifer, F. longiseta, were estimated separately. As recommended by Feigenbaum and Maris (1984), NPC for K. cochlearis typica was a mean of two estimates-one for daytime and one for nighttime collections-be-

6 Juvenile Chaoborus predation 261 Table 3. Comparison of mean ingestion rates (rotifers per Chaoborus h-l) estimated for Chaoborus feeding on Filinia longiseta and Keratella cochlearis f. typica using the gut-content method and a functional response experiment. Mean ingestion rates for the gut-content method represent mean number of rotifers per crop adjusted for gut passsage time. Prey dcnsitics (rotifers liter- ) are those observed in Post Pond (Moore 1988). (NA-Not applicable to this method.) F. longiseta Gut-content Functional method response K. cochlearis f. typica Gut-content method Functional response * Values in parenthcscs based on SD in column 2. Prey density cause Chaoborus showed diel differences in predation rate when feeding on this rotifer species (Moore 1988). Results Functional response- Second-instar C. punctipennis exhibited a type 2 functional response when feeding on a mixed-species assemblage of rotifers (Fig. 1). Prey density explained 93% of the variation in predation rates (Table 2) when the data were fit to Holling s model. Mean per capita predation rate ranged from 2.0 rotifers h-l at a total prey density of 180 liter-l to an asymptotic maximum of -8.2 rotifers h-l at 2,880 liter-l. Ingestion rate curves of Chaoborus for each of the three rotifer species in the functional response experiment seem different when compared by visual inspection (Fig. 2). Holling s disk equation can be fitted directly to the three curves, but the quality of the fit (as determined by r2) varies greatly (Table 2). The best fit occurred for S. pectinata. Chaoborus ingestion rates for this rotifer were significantly higher (Student s t = 4.95, 58 df, P < 0.001) than those for the other two prey species, and the ingestion rates for it largely determined the shape of the functional response for the total prey assemblage (Fig. 1). It is possible that a type 3 functional response better describes the curve for K. cochlearis typica (Fig. 2), but no one has statistically fit functional response data to the sigmoid model (Livdahl and Stiven 1983). The difficulty, according to my own trials and Houck and Strauss Mean No. rotifers per crop (SD) l.o(ko.8) NA 0.2(kO. 1) NA Mean ingestion rate 1.0(0.2-l.8)* ( )* 0.7 (1985), seems to be in obtaining appropriate seed values for the nonlinear regression analysis. Furthermore, Chaoborus ingestion rates at the highest prey density of K. cochlearis typica declined rather than approaching an asymptote characteristic of a type 3 response. Chaoborus predation rates (rotifers per Chaoborus h-l) for K. cochlearis typica in the upper thermocline and predation rates for Filinia in the hypolimnion of Post Pond (Table 3) were estimated by substituting the observed prey densities in Post Pond (Table 3) and the estimated a and Th values (Table 2) from the nonlinear regression analyses into Holling s disk equation. These a and Th values are approximations for the field situation because they were determined with a three-species prey assemblage where prey were in equal abundance. Predation rates estimated with the laboratory-determined a and Th values were three times higher for the more abundant K. cochlearis typica than for Filinia (Table 3). Observations can be made about Chaoborus predatory behavior from the laboratory experiment, when a type 2 functional response is assumed for Chaoborus feeding on each of the prey species. For example, the attack rate (a ), or rate of approach to the plateau of ingestion rate, is much slower for Chaoborus feeding on K. testudo and K. cochlearis f. typica than when it feeds on S. pectinata (Table 2). This finding means that second-instar Chaoborus will attack the two former rotifer species at a lower rate or search less efficiently for them than for S. pectinata. Estimates of handling time (Th) range

7 262 Moore Total prey density (rotifers/l00 ml) Fig. 3. Median selectivity values (n = 4 per density) as determined in the laboratory for second-instar C haohorus punctipennis preying on a three-species assemblage of rotifers. The experiment was conducted at five total prey densities. Vertical lines span the middle two of ihe four replicate values. The horirontal line indicates neutral selectivity; values above the line indicate positive selection and those below it represent negative selection.!rrom 13 min for S. pectinata to 26 min for K. cochlearis typica (Table 2). Selectivity-TThe selectivity of Chaoborus changed with increasing prey density (Fig. 3). At the three lowest prey densities, Chaoborus positively selected S. pectinata over both species of Keratella (Mann-Whitney U-test; U = 238, n, n2 = 12, 24, P < 0.01). At the two highest prey densities, however, Chaoborus preference values for the three rotifer species were similar (Kruskal-Wallis tests: for 1,440 rotifers liter-i, H = 0.04, 2 df, P > 0.05; for 2,880 rotifers liter-l, H = 5.5, 2 df, P > 0.05). Median selectivity values for S. pectinata and K. testudo did not change significantly among the five prey densities (Kruskal-Wallis tests: S. pectinata, H = 7.2, 4 df, P = 0.13; K. testudo, II = 1.4, 4 df, P = 0.85), but Chaoborus preference values for K. cochlearis typica were not similar at all prey densities (Kruskal-Wallis test: H = 11.2, 4 df, P < 0.05). A Mann-Whitney U-test showed that Chaoborus selectivity for K. cochlearis typica was significantly greater at the three highest prey densities (2,800, 1,440, Time (h) Fig. 4. Continuous predation n := 4 per time) for starved (4-6 h) second-instar Chaoborus punctipennis feeding on Synchaeta prey (600 prey liter- I). and 720 liter ) than at the two lowest (U = 86, n, n2 = 12, 8, P < 0.0 1). Gut passage kinetics- Mean ingestion rates for starved Chaoborus during the first 30 min of a time-series predation experiment were two to three times higher than rates during the 6th hour (Fig. 4) and were significantly greater than rates at all later times (I = 3.38, df = 22; P < 0.01). During the last four time intervals (lst, 2nd, 4th, and 6th hour), differences among mean ingestion rates were not significant (ANO- VA; E;j,,2= 1.13, P > 0.25). This constancy suggests that a steady state ingestion rate, of approximately 2.5 Synchaeta per Chaoborus h-, had been reached. Gut passage time for C. punctipennis feeding on Synchaeta can be estimated as the time when a steady state ingestion rate begins, and this occurred at about 1 h or less (Fig. 4). Direct observations OF the evacuation of Synchaeta from the crop and intestine of Chaoborus suggest a total gut passage time of <: 1 h (Table 4). Crop emptying time ranged from 15 to 30 mm and was always shorter than the time required to empty the intestine (45-60 min). Remains of regurgitated Synchaeta were not found in the experi mental containers, suggesting that this soft-bodied rotifer can be digested completely. Total gut evacuation time for Chaoborus feeding on the loricate rotifer, K. coch/earis tecta, ranged from 1 to 3 h and was generally -

8 Juvenile Chaoborus predation 263 Table 4. Results of direct observations of prey passage time through the crop and intestine of second-instar Chaoborus. Crop emptying time (min) began with ingestion and ended with regurgitation. Intestine emptying time (min) began with ingestion and ended when the colored prey material (see text) was no longer visible in the intestinal tube. Kotikr spccics Chaoborus individual No. ingested Synchaeta pectinata Keratella cochlcaris f. tecta 1 6 * Intcstinc emptied bcforc final crop regurgitation > 5-6 No. regurgitated Crop Emptying time lntesline * > longer than those times for soft-bodied S. pectinata (Table 4). Longer crop residence times for K. cochlearis tecta occurred in part because often only part of the food bolus was regurgitated. For example, two Chaoborus individuals (No. 1 and No. 6) regurgitated only part of a food bolus comprised of empty Keratella loricas after min (Table 4), and some loricas remained in their crops for an additional 2 h. During this latter interval, no movement of food material occurred in the intestinal tube. Prey residence time in the crop also depended on ration size. For example, Chaoborus that ingested two to four K. cochlearis tecta had crop passage times of 150 to > 180 min, whereas those individuals that ingested five to six Keratella emptied their crops either completely or partially in min. If WC assume that gut passage times for K. cochlearis tecta and S. pectinata are equal to those for K. cochlearis typica and F. lon- giseta, respectively, Chaoborus predation rates for the two latter prey species can be estimated separately with Eq. 2. This assumption is reasonable because K. cochlearis tecta and K. cochlearis typica arc nearly identical in size (Table 1) and have similar body textures. Likewise, both Synchaeta and F. longiseta are soft-bodied rotifers, and both arc positively selected by second-instar Chaoborus (Moore 1988; Moore and Gilbert 1987). With an intermediate gut passage time of 2 h for K. cochlearis typica and an average of 0.2 (SD = 0.1) K. cochlearis typica per Chaoborus crop (mean of day and night collection), the estimated feeding rate is 0.1 K. cochlearis typica per Chaoborus h-l. Likewise, the estimated predation rate on F. longiseta by second-instar Chaoborus is 12.0 Filinia per 12-h day using a 1 -h gut passage time and a mean of 1.O (SD = 0.8) Filinia per Chaoborus crop (Table 3). Discussion Predation rates-maximal predation rates of second-instar Chaoborus feeding on rotifers are among the highest reported for a pelagic invertebrate predator. The highest predation rate reported for a cyclopoid copcpod feeding on rotifers is for Mesocyclops edax feeding on Brachionus (Williamson 1983). Mesocyclops edax can consume 40 Brachionus individuals per Mesocyclops d- l or about 8 bg dry-wt of prey biomass d-l. The Calanoid copepod Diaptomus pallidus will ingest 129 Synchaeta oblonga or about 4 pg dry-wt d-l (Williamson and Butler 1986). In contrast, this study shows that individual Chaoborus can maximally ingest 3.8 and 7.5 times more rotifer biomass per day than can Mesocyclops and D. pallidus, respectively. These high predation rates by Chaoborus are not entirely a result of using starved Chaoborus in the functional response experiment. For example, in the time-series predation experiment (Fig. 4), the ingestion rates of Chaoborus stabilized when Chaoborus presumably was sated, yet

9 264 Moore this steady state ingestion rate averaged 2.5 S. pectinata per Chaoborus h-l or 13.2 pg dry-wt per Chaoborus d-l (weight of one S. pectinata = 0.22 pg). This figure is still much higher than the rates exhibited by either copepod species. Clearly, second-instar Chaoborus individuals are capable of removing imore rotifers on a per capita basis than are copepods. Rotifer intake, when expressed as a percentage of Chaoborus body weight, is relmarkably high for early instar Chaoborus, and values are among the highest reported For an aquatic invertebrate predator. When Malueg s (1966) body weight data for firstto fourth-instar C. punctipennis and agespecific Chaoborus predation rates (total rotifer density = 600 liter-i) determined for Chaoborus feeding on a five-species assem- blage of rotifers (Moore and Gilbert 1987).were used, sated first- to fourth-instar Chaoborus ingested 17 1, 116, 54, and 10% of their body weight per day, respectively. Early instars of Chaoborus consumed more than their body weight per day, contradicting Pastorok (1980a), who concluded that Chaoborus intake values (% of ingested body wt d-l) are low when compared to other invertebrate predators. Values reviewed by Pastorok ranged from only 0.8 to 13.2% of Chaoborus body weight and represent val- ues for five Chaoborus species (mostly instar IV), each feeding on crustaceans. Few copepod and cladoceran predators consume more than their body weight per day (Hall et al. 1976). For example, the predation rates of M. edax and D. pallidus described above represent 73 and 65% of their body weight per day. The high intake values for the early instars of C. punctipennis suggest that first and second instars may be susceptible to food limitation. It has, in fact, been demonstrated for C. trivittatus in field manipulations (Neil1 and Peacock 1980; Neil1 1985). Despite the high predation rates of individual Chaoborus, population predation pressure by Chaoborus on rotifers in midsummer is probably much less than that exhibited by copepods. For example, the highest densities of M. edax and secondinstar Chaoborus in Post Pond (Moore 1988) were 7.6 and 0.13 liter-l. The removal rate of rotifers (all rotifer species assumed to be randomly distributed and equally and highly preferred prey by both predators) by Chaoborus and copepods can be calculated. Total rotifer density was -330 liter-l, and at this density Williamson s (1983) func- tional response data for Mesocyclops feeding on the preferred prey Brachionus predicts an ingestion rate of 4.6 pg dry-wt of rotifers per Mesocyclops d-l (dry weight of Brachionus = 0.2 pg). My study (Fig. 1) predicts Chaoborus will ingest 17.8 pg dry-wt of rotifers per Chaoborus dml at a total rotifer density of 330 liter-. This estimate is liberal for Chaoborus because it assumes that the three rotifer species in the experiment each had a dry weight equal to S. pectinata (0.22 pg). If Mesocyclops and Chaoborus densities are used, the population predation rate by Mesocyclops (3 5 pg dry-wt of rotifers liter-l cl-l) will be 14 times greater than that for second-instar Chaoborus (2.5 pg dry-wt of rotifers liter- d-l). This comparison can be expanded to include all four instars of Chaoborus, each of which ingests rotifers. But even when all Chaoborus instars are included, it is doubtful that their combined ingestion rates could equal or surpass that of all copepods in a temperate lake during midsummer. Late instars (III and IV) of Chaoborus exhibit predation rates three to four times higher than the second instar (Moore and Gilbert 1987), but due to metamorphosis and emergence the late instars are not as abundant as the second instar in midsummer. During early spring, however, densities as high as 2.5 liter-l for fourth-instar larvae have been reported for eutrophic lakes (Roth 1968), and, at that time, population predation rates of Chaoborus feeding on rotifers may dwarf those of newly hatched copepods. Selectivity-The inverse relationship be- tween Chaoborus selectivity and prey density is interesting because it contradicts predictions of optimal foraging theory and the results of Pastorok (1980b). According to optimal foraging theory, Chaoborus should become more selective as the more valuable prey type (Synchaeta: see Moore and Gilbert 1987) increases in abundance. In my experiment, the opposite occurred; Chaoborus became less selective at high total

10 Juvenile Chaoborus predation 265 prey densities. Pastorok (1980b), however, observed that fourth-instar C. trivittatus feeding on an equal mixture of Daphnia and Diaptomus selected the more valuable Diaptomus over Daphnia when total prey density was high. There are several explanations possible for the disparity of these results. First, at high prey densities ( rotifers ml- ), Chaoborus may have difficulty discriminating the swimming signals of different prey species and may feed opportunistically. If Pastorok had used greater total prey densities (> 90 prey liter- ), a response similar to that in my study might have occurred. Second, Chaoborus may become more efficient at capturing and handling less preferred prey at high prey densities because encounters with such prey are more frequent. The tendency toward a sigmoid functional response for Chaoborus feeding on K. cochlearis typica (Fig. 2) suggests this alternative. Another possibility, mentioned by Folt et al. (1982), is that prey or predator behavior may change with increasing prey density. For example, the predator s searching tactics may differ at high and low prey densities, resulting in different predator-prey encounter rates. Moore and Gilbert (1987) noted that the swimming rate of Chaoborus may influence its encounter rate with rotifers. I have noted that Chaoborus frequently darts and changes the position of its ambush site when prey are scarce, but at high prey densities Chaoborus assumes a motionless stalking position until it strikes. As a result of this behavioral response to prey density, the movement of Chaoborus, in addition to that of its prey, may determine encounter rates, and hence selectivity, when prey are scarce. To determine whether predator or prey swimming speeds determine encounter rates, we need accurate measurements of Chaoborus movement rates over a range of prey densities. Density-dependent change in search tactics has been reported for two other ambush predators-a predacious diving beetle (Formanowicz 1982) and mantids (Inoue and Matsura 1983). In neither my observations nor the study of Formanowicz (1982) was the predator s change in search tactics due to satiation. This finding suggests that some predators may assess prey density from their encounter rates with prey and adopt different search tactics at different prey densities. Gut passage kinetics-factors contributing to the high predation rates of Chaoborus compared to copepods include the rapid gut passage time of Chaoborus and its ability to swallow prey whole. Copepod predators must chew large prey before swallowing them, probably increasing their ingestion time compared to Chaoborus. For example, Mesocyclops handles Keratella crassa from several to 30 min before swallowing it (Gilbert and Williamson 1978), whereas swallowing time by second-instar Chaoborus for the same prey species averages 39 s (Moore and Gilbert 1987). Ingestion times for both predators, however, are negligible compared to the time they require to digest their prey. For example, secondinstar Chaoborus can consume S. pectinata in 1.9 s (Moore and Gilbert 1987), yet total gut passage for this prey species can take up to 1 h (Fig. 4 and Table 4). Gut passage time for Chaoborus, however, is shorter than that for copepod predators feeding on similar prey. For example, Stemberger (1986) showed a gut passage time of 7-8 h (15OC) for Diacyclops feeding on S. pectinata, and Williamson (1984) reported a 5-7 h (1 7 C) gut passage time for Mesocyclops. These rates are five to eight times longer than that for Chaoborus feeding on the same prey. Digestion times of Chaoborus feeding on rotifer prey, particularly soft-bodied species, are remarkably short when compared to the times reported for Chaoborus feeding on chitinous crustaceans. For example, Fedorenko (1975a) directly observed a crop passage time of 5 h (ingestion to regurgitation at 20 C) for fourth-instar C. trivittatus feeding on Bosmina longirostris and a crop passage time of 24 h for C. trivittatus feeding on Diaptomus kenai at 5 C. Likewise, Gi- guerc (1986) calculated that the crop evacuation rate for C. americanus feeding on Diaptomus leptopus varied between 10 and 15 h at 13 C. In contrast, I observed that second-instar Chaoborus could empty its crop containing a food bolus of the softbodied S. pectinata in as little as min at 20 C (Table 4). The rapid digestion times reported in my study are likely a result of

11 266 Moore both prey type and a higher weight-specific metabolic rate for young Chaoborus (instar II). Gut passage kinetics can also be quantified with the Th parameter of Holling s disk equation. Spitze (1985), using Holling s method, reported handling times of - l-10 h at 15 C by third- and fourth-instar C. americanus preying on small and large Daphnia pulex, respectively. I found, however, that the mean Th value for secondinstar C haoborus feeding on rotifer prey (5 min) was 1 l-l 11 times shorter than those reported by Spitze (cf. Table 2 and Spitze 1985). Spitzc emphasized that T/, values include both swallowing and digestion time and that each ingestion represents an incremental reduction in the predator s efficiency. In other words, Th measures the cost of ingesting and digesting each prey in terms of tirne lost for capturing future prey. Clearly, handling costs per item are much greater for Chaoborus when feeding on Daphnia than when feeding on soft-bodied rotifers. Probably the very low T,, value found in my study was caused in part because starved Chaoborus were used in the functional response experiment. Spitze ( 198 5) used sated Chaoborus. Starved Chaoborus exhibited high feeding rates for up to 30 min when given food (Fig. 4), and these high shortterm feeding rates no doubt influenced the results of my experiment, particularly because I used a feeding period (60 min) about equal to gut passage time. Thus Chaoborus predation rates probably were near maximurn during most of the experiment. The rapid digestion rates of Chaoborus for soft-bodied rotifers, and its ability to elevate its feeding rate following brief periods of food deprivation, may enable it to maintain a high average energy intake even when its prey are clumped. Figure 4 shows how briefly starved Chaoborus can feed rapidly for a short period in moderately high concentrations of prey. Also, I have observed Chaoborus pack its crop with rotifers in 5 min (pers. obs.). One study of copepod predation (Stemberger 1986) and several studies of vertebrates (Sibly 198 1; Diamond et al. 1986) show that ingestion rates can be limited by rates of digestion. Such digestive bottlenecks may be minimized by Chaob- orus when it feeds on soft-bodied rotifers becaus e crop emptying time seems to be much more rapid for this prey type than for chitinous crustaceans. In fact, a short-term elevation of feeding rate coupled with a rapid digestion time may allow Chaoborus to obtain more than one meal (a packed crop) in a patch, assuming that the lifetime of the patch is longer than the time required for prey digestion. If assimilation efficiencies are similar among hard- and soft-bodied prey types, Chaoborus may achieve its maximum energy intake when it feeds on softbodied rotifers that are distributed in patches. C omparing predation rate predictions - Estimiates for the rate of Chaoborus predation on rotifer prey generated by the functional response experiment and the gut-content rnethod were of the same order of magnitude (Table 3). The predation rate predicted for Filinia from the functional response experiment, even though five times lower than those rates estimated with the gut-content method, still fell within the range of values estimated by the gut-content method. It should be noted, however, that both methods assume temperatures from 20 to 22X, while second-instar Chaoborus preyed on Filinia in the hypolimnion where temperatures were 8 C (Moore 1988). Thus, predation rates on Filinia in Post Pond are most likely lower than both rates shown in Table 3. The predation rate on K. cochlearis typica estimated from the gut-content method was seven times lower than the rates derived from Holling s disk equation (Eq. 1). The latter rate did not overlap with the range of values estimated from the gut-content method. This discrepancy may be because crop passage time for Chaoborus feeding on K. cochlearis typica varied systematically. Murtaugh (1984) showed that gut evacuation rates of Neomysis were highly variable and depended on the number of Daphnia consumed and the prior feeding history of Neomysis. Gut evacuation rates increased with the number of Daphnia consumed and greatly decreased if Neomysis was starved. In fact, starved mysids retained undigested material in the stomach for > 3 d. Although the gut-content method can

12 Juvenile Chaoborus predation 267 yield rough estimates of Chaoborus feeding rates on rotifers, it should be used with caution. Many factors, including meal size, prey type, predator age, and temperature, are known to influence gut passage time in insects (Bernays and Simpson 1982), and there are theoretical reasons why animals that are energy maximizers should be capable of adjusting their gut passage time (Sibly 1981). Because Chaoborus probably has a flexible crop evacuation rate, the use of functional response experiments or in situ enclosure experiments to estimate feeding rates is preferrable to gut evacuation. Second-instar Chaoborus exhibited both density-dependent predation rates and prey selectivity when feeding in multispecies assemblages of prey at different total prey densities. This study and several others (Murtaugh 1984; Spitze 1985; Stemberger 1986) emphasize the role of digestion times for invertebrate predator-prey interactions. Chaoborus became less selective at high total prey densities. Such shifts in selectivity may affect the stability of predator-prey intcractions (Hassell 1978) and warrant further investigation. References ALLAN, J. D Feeding habits and prey consumption of 3 sctipalpian stoneflics (Plccoptera) in a mountain stream. Ecology 63: BAJKOV, A. D How to estimate the daily food consumption of fish under natural conditions. Trans. Am. Fish. Sot. 65: BERNAYS, E. A., AND S. J. SIMPSON Control of food intake, p In M. J. Berridge et al. [cds.], Advances in insect physiology. Academic. CHIMNEY, M. J., R. W. WINNER, ANI) S. K. SEILKOP Prey utilization by Chaoboruspunctipennis Say in a small eutrophic reservoir. Hydrobiologia 85: 193-l 99. DIAMOND, J. M., W. H. KARASOV, D. PHAN, AND F. L. CARPENTER Digestive physiology is a determinant of foraging bout frequency in hummingbirds. Nature 320: FEDORENKO, A. Y. 1975a. Instar and spccics-specific diets in two species of Chaoborus sp. Limnol. Oceanogr. 20: Feeding characteristics and predation impact of Chaoborus (Diptera, Chaoboridae) larvat in a small lake. Limnol. Oceanogr. 20: FEIGENBALJM, D. L., AND R. C. MARIS Feeding in the Chaetognatha. Oceanogr. Mar. Biol. Annu. Rev. 22: FOLT, C. L., J. T. RYBOCK, AND C. R. GOLDMAN The effect of prey composition and abundance on the predation rate and selectivity ofmysis rclicta. Hydrobiologia 93: FORMANOWICZ, D. R Foraging tactics of larvae ofllytiscus verticalis (Coleoptera: Dytiscidae): The assessment ofprcy density. J. Anim. Ecol. 51: GAULD, D. T The grazing rate of planktonic copepods. J. Mar. Biol. Assoc. U.K. 29: GIFFORD, D. J Laboratory culture of marine planktonic oligotrichs (Ciliophora, Oligotrichida). Mar. Ecol. Prog. Ser. 23: GIGUERE, L. A The estimation of crop evacuation rates in Chaoborus larvae (Diptcra: Chaoboridac) using natural prey. Frcshwatcr Biol. 16: GILBERT, J. J., AND C. E. WILLIAMSON Predator-prey behavior and its effect on rotifer survival in associations of A4esocyclops edax, Asplanchna girodi, Polyarthra vulgaris, and Keratella cochlearis. Occologia 37: HALL, D. J., S. T. THRELKELD, C. W. BURNS, AND P. H. CROWLEY The size efficiency hypothcsis and the size structure of zooplankton communities. Annu. Rev. Ecol. Syet. 7: HARE, L., AND J. C. H. CARTER Zooplankton populations and the diets of three Chaoborus species (Diptera, Chaoboridae) in a tropical lake. Frcshwatcr Biol. 17: HASSELL, M. P The dynamics of arthropod predator-prey systems. Princeton. HILDREW, A. Cr., AND C. R. TOWNSEND Predators and prey in a patchy environment: A frcshwater study. J. Anim. Ecol. 51: HOLLING, C. S Some characteristics of simple types of predation and parasitism. Can. Entomol. 91: HOUCK, M. A., AND R. E. STRAUSS The comparative study of functional responses: Experimental design and statistical interpretation. Can. Entomol. 117: TNOUE, T., AND T. MATSURA Foraging strategy of a mantid, Paratenodera angustipennis S: Mechanisms of switching tactics bctwccn ambush and active starch. Oecologia 56: JULIANO, S. A., AND F. M. WILLIAMS On the evolution of handling time. Evolution 39: KAJAK, Z., AND J. RYBAK The feeding of Chaoborus Jlavicans Mcigen (Diptcra, Chaoboridac) and its predation on lake zooplankton. Int. Rev. Gesamtcn Hydrobiol. 64: 36 l-378. LIVDAHL, T. P., AND A. E. STIVEN Statistical difficulties in the analysis of predator functional response data. Can. Entomol. 115: 1365-l 370. MAIN, R. A A limnological study of Chaoborus (Diptera) in Hall Lake, Wash. M.S. thesis, Univ. Washington. 106 p. MALUEG, K. W An ecological study of Chaoborus sp. Ph.D..thcsis, Univ. Wisconsin. 255 p. MOORE, M. V Method for culturing the phantom midge, Chaoborus (Diptera: Chaoboridae), in the laboratory. Aquaculture 56: Diflcrcntial use of food resources bv

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