prey capture by the four larval instars of chaoborus crystallinus

Prey Capture by the Four Larval Instars of Chaoborus crystallinusAuthor(s): Michael C. SwiftSource: Limnology and Oceanography, Vol. 37, No. 1 (Jan., 1992), pp. 14-24Published by: American Society of Limnology and OceanographyStable URL: http://www.jstor.org/stable/2837755 .

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Limnol. Oceanogr., 37(1), 1992, 14-24 ? 1992, by the American Society of Limnology and Oceanography, Inc.

Prey capture by the four larval instars of Chaoborus crystallinus

Michael C. Swift' Department of Biological Sciences, Wright State University, Dayton, Ohio 45435

Abstract Prey capture ability of fourth-instar Chaoborus larvae has been studied widely but relatively

little comparable information is available for the first three larval instars. In this laboratory study I measured strike and contact efficiencies of all four instars of Chaoborus crystallinus. The effectiveness of prey escape behavior was also recorded. As larval size increased the size of successfully captured and ingested prey also increased. There was no loss of ability to ingest the smallest prey by the largest larvae. Prey width was a better index of successful capture and ingestion than was prey length. Fast swimming and infrequent swimming were effective precontact prey escape behaviors. The effectiveness of akinesis and spininess, two postcontact escape mechanisms, depended on larval size; they were effective when prey width approached larval gape diameter but relatively ineffective when prey width was much less than larval gape diameter. Gelatinous prey were readily attacked once but were almost always immediately rejected and seldom attacked again. Early instar Chaoborus larvae are abundant and effective predators whose role in structuring zooplankton communities is only beginning to be appreciated.

The effect of predation by Chaoborus larvae on zooplankton population dynamics and community structure has been studied extensively. This research has focused on larval diet (e.g. Kajak and Ranke-Rybicka 1970; Fedorenko 1975a; Lewis 1977), me- chanics of prey capture and prey selectivity (e.g. Swift and Fedorenko 1975; Vinyard and Menger 1980; Riessen et al. 1984), and impact on prey populations (e.g. Fedorenko 1 975b; Kajak and Rybak 1979; Neill 1981). Despite extensive research on Chaoborus

I Present address: Monticello Ecological Research Station, University of Minnesota, P.O. Box 500, Mon- ticello 55362. Acknowledgments

This research was done while I was an exchange scientist in the scientific exchange program between the National Academy of Sciences and the Polish Academy of Sciences. A. Hillbricht-Ilkowska provided logistical support. L. Kufel provided space and logistical support at the Institute of Ecology Hydrobiolog- ical Station in Mikolajki. The scientific staffs of the Department of Hydrobiology, Institute of Ecology, in Warsaw and Mikolajki and the Department of Hydro- biology of the University of Warsaw were helpful in all aspects of my visit. Y. Ejsmont-Karabin, A. Kar- abin, J. Pijanowska, P. Dawidowicz, A. Kowalczewski, and M. Gliwicz provided assistance with collections and identifications and stimulating discussions. Special thanks are due to R. Wisniewski. M. Moore provided discussions about Chaoborus predation and critical comments on the manuscript.

predation, few studies have examined the feeding behavior of the first three larval instars.

Early studies of feeding by young instars were mostly qualitative but indicated that differences existed between diets of "old" and "young" larvae as did quantitative de- scriptive studies by Fedorenko (1975a), Lewis (1977), and Moore (1988). Experi- mental studies of larval feeding have documented differences in prey selection among species and instars (Fedorenko 1975b; Chimney et al. 1981; Moore and Gilbert 1987) and their relationship to mouth size. In a detailed study of prey capture by young Chaoborus larvae, Moore and Gilbert (1987) demonstrated ontogenetic shifts in strike efficiency among the first three instars and the effects of prey characteristics (size, body texture, behavior) on prey capture. Their study included first-, second-, and third-instar larvae feeding on rotifer prey.

No one has studied systematically prey capture by all four instars from the same population. To predict the impact of Chao- borus predation on prey populations it is necessary to know the predatory capabilities of each of the four instars feeding on various prey species. This study is the first to measure parameters of the prey capture process for all four larval instars from a single population feeding on a diverse suite of prey

14



Chaoborus prey capture 15

species including protozoans, rotifers, and crustaceans.

Methods Larvae of Chaoborus crystallinus (De

Geer) used in these experiments were collected from outdoor cement troughs (1 x 1 x 10 m) located on grounds of the Hy- drobiological Station of the Institute of Ecology in Mikolajki, Poland. Larvae were collected with a dipnet (240-,um mesh) and sorted by instar into pans of water filtered to remove zooplankton. Sorting was done by hand with a pipet. Head-capsule length differed among instars enough that sorting without magnification was essentially without error; odd-looking individuals (e.g. newly molted larvae with large heads and small bodies) were measured. Larvae were usually collected and sorted in the morning for feeding trials in the afternoon; occasionally larvae were collected and sorted in the evening and used in feeding trials the following morning. All available instars were sorted each day; usually all four instars were available during June and July when these experiments were done.

In addition to hand sorting, first-instar larvae were hatched in the laboratory from egg rafts collected in the troughs. All larvae were used in experiments within 24 h of being collected. Instar determinations were made from head-capsule length measurements of preserved larvae. Mouth size (Swift and Fedorenko 1975) (=gape diameter of Moore and Gilbert 1987) was measured for each instar (Table 1).

Prey taxa were collected from the same troughs as the Chaoborus larvae or from Mikolajskie Lake. Prey initially were sorted by size and taxon with graded sieves (500- 30-,um mesh). Unwanted individuals (wrong size or taxon) were removed from the prey population with a pipet and dissecting microscope. Prey size was characterized as body length, body width, and, for culicid and chironomid larvae, head-capsule width (Table 2). For cladocerans, body length was measured from the top of the head to the base of the tail spine and body width was measured at the widest part of the carapace. For rotifers, length and width measurements included spines. For other taxa, length

Table 1. Head-capsule length (mm) and gape diameter (mm) of Chaoborus crystallinus instars.

Head capsule length Gape diameter

Instar n Mean(SD) n Mean(SD)

I 77 0.26(0.01) 42 0.17(0.01) II 103 0.47(0.03) 31 0.27(0.02) III 100 0.86(0.06) 42 0.44(0.03) IV 104 1.36(0.09) 87 0.65(0.04)

and width were measured along the ante- rior-posterior axis and dorsal-ventral axis.

Predatory behavior was studied by watching larvae feed on various zooplankton prey. Observations were made by unaided eye or with a dissecting microscope (6 x or 12 x). The microscope was used routinely for observations of first- and second- instar larvae and for observations of third- and fourth-instar larvae feeding on small prey (rotifers, nauplii, protozoans). Obser- vations routinely included success or failure of attacks, success or failure of ingestion following capture, orientation of prey when ingested, prey behavior after capture, and often handling time. Often crops were dis- sected following a feeding trial as a check on observational data.

The experimental chamber varied with larval size and included a clear plastic dish (2.5-cm diam, 1 cm deep), a petri dish (5- cm diam, 1.5 cm deep), and a ceramic cru- cible (5-cm diam, 4 cm deep). Prey density was not standardized, but ranged from the equivalent of several hundred per liter for large prey (e.g. Daphnia magna) to nearly 100,000 liter-' for small prey (e.g. small rotifers). Prey density was high enough that larval-prey interactions occurred several times a minute; there was no observable effect of prey density on normal prey swimming behavior. One larva was tested at a time. Once a particular prey taxon or size category was sorted, it was tested with all available instars. Usually one prey taxon or size category was tested per day.

To prevent satiation effects, I allowed larvae to ingest only enough prey to fill the crop partially ( 1/2 full) during a feeding trial. This predetermined number of prey varied from several (large larva, small prey) to only one (prey size near crop size). Larvae



16 Swift

Table 2. Size characteristics of prey taxa used in observations of predation behavior by Chaoborus crystallinus instars.

Body length (mm) Body width (mm) Head-capsule width (mm)

Taxon n Mean(SD) n Mean(SD) n Mean(SD)

Protozoan 16 0.07(0.01) * Euglena sp. 16 0.08(0.01) * Filinia cornuta 20 0.10(0.01) 0.06t F. cornuta 50 0.16(0.01) 40 0.10(0.01) Keratella cochlearis 127 0.16(0.02) 24 0.06(0.01) Cyclopoid nauplii 101 0.18(0.03) 29 0.10(0.01) Keratella quadrata 50 0.20(0.01) 51 0.13(0.01) Synchaeta spp. 7 0.21(0.02) * Brachionus urceus 100 0.22(0.03) 100 0.19(0.02) Bosmina longirostris 66 0.23(0.02) 33 0.16(0.01) Mixed rotiferst 177 0.30(0.08) * Chydorus sphaericus 28 0.32(0.02) 0.25t Gelatinous protozoan 10 0.34(0.19) * C. sphaericus 50 0.39(0.03) 30 0.31(0.04) Daphnia pulex 34 0.54(0.04) 47 0.25(0.02) Cyclops sp. 102 0.74(0.03) 29 0.23(0.01) Daphnia magna 93 0.90(0.09) 47 0.57(0.07) Daphnia hyalina 100 1.05(0.25) 27 0.46(0.04) Culicid larvae 68 1.12(0.07) 37 0.14(0.01) 67 0.29(0.01) D. magna 100 1.38(0.12) 27 0.87(0.04) Culicid larvae 93 1.53(0.08) 28 0.12(0.02) 51 0.30(0.01) D. pulex 26 1.69(0.17) 47 0.99(0.12) Culicid larvae 45 1.93(0.14) 27 0.25(0.01) 45 0.49(0.01) Culicid larvae 73 2.25(0.16) 40 0.27(0.03) 39 0.49(0.02) Chironomid larvae 58 2.32(0.36) 25 0.27(0.04) 24 0.26(0.02) Culicid larvae 61 0.56(0.24) 45 0.44(0.04) 67 0.77(0.02) * Body-width measurements not available. t Calculated from the length: width ratio of other measurements of the same taxon. t K cochlearis, K quadrata, Synchaeta spp., Euchlanis sp., and Polyarthra sp.

usually readily attacked prey. Larvae that did not strike at prey readily within a few minutes were assumed to be damaged in some way and were replaced; these larvae were not scored. Larvae were replaced after 15-20 unsuccessful strikes. These strikes were scored as misses. Thus, the number of strikes per larva in a feeding trial varied from one, when a small larva ingested a large prey item on its first strike, to as many as 15-20 when a larva was unsuccessful at ingesting a particular prey. Larvae that successfully captured a prey item were allowed enough time to either ingest it or release it.

Attacks were scored following Swift and Fedorenko (1975) as strikes (misses), captures (strikes that hit or held prey), and ingestions (captures that resulted in ingestion). Strike efficiency (SE) and contact efficiency (CE) (Swift and Fedorenko 1975) were calculated as the probability of ingestion after attack [ingestions/(strikes + captures)] and the probability of ingestion after

contact (ingestions/captures). Strike and contact efficiencies were calculated for each larval feeding trial; mean SE and CE were calculated for each larval instar-prey combination. The SE and CE values (x) for each larva were arcsine, square-root-trans- formed (arcsine x)-l before mean values were calculated. The number of larvae tested per instar-prey combination varied but was usually 15 (instar I: mean 20, range 7-27; II: mean 15, range 8-26; III: mean 15, range 5-26; IV: mean 15, range 5-25).

Results Strike efficiencies of first-instar larvae

ranged from 0 to 76% on the prey tested and their contact efficiencies ranged from 0 to 100% (Fig. 1, I). Attacks on Filinia were most successful (SE -75%) and those on Keratella quadrata, Euglena, and a small, fast protozoan were least successful (SE < 30%). Ingestion was most successful on the small protozoan, Filinia and copepod nau-




1. protozoan 2. Filinia cornuta

100 3. Keratella cochlearis 2 4. cyclopoid nauplii

'4 5. Synchaeta spp. 6. Brachionus urceus

50 3 7. Bosmina longirostris - I t , 6 8. mixed rotifers

9. gelatinous protozoan O 18111 10. Chydorus sphaericus o A 11. Keratella quadrata 100 V 012 Cyclops sp. -lz 5i , } L 13. Daphnia magna

1T71 14. Daphnia pulex 50 _ ; 46 t W 1 5. Daphnia hyalina

3 18 16 16. culicid larvae 16 17. chironomid larvae o_ :,10 14 12 18. Euglenasp.

>% 0~III .'IK I I I I I I 0 1000 0

t ,' 1014 1516 W 502 0.2 16 16

12 16 14 m 10~~1 13 1

9 14 0 1 1-famil I I Q.,

I I I a

100 T 61

67 17 II

50 1315~1 1

N I ~~~ ~~~~13 14

0 0.2 0.4 0.8 1.2 1.6 2.0 2.4 3.6 Prey Length (mm)

Fig. 1. Strike and contact efficiencies as a function of prey length. Mean strike efficiency (0) and contact efficiency (0) are shown for each instar (I-IV). The vertical dashed line marks the gape diameter of each instar. Numbers associated with the data points refer to the prey listed in the legend. Vertical bars-standard errors.

plii and least successful on K. quadrata and Euglena. There were qualitative differences in the responses of first-instar larvae to these prey. Keratella quadrata was attacked readily (65% of strikes hit the prey) but individ-

uals were too "large" to be ingested. Eugle- na was attacked rarely and only 44% of all strikes at it were contacts. Euglena was actively rejected after being captured even though these larvae ingested Filinia that were



18 Swift

contaminants in the Euglena feeding trials. Prey with soft bodies were always ingested even when they seldom were attacked successfully (e.g. protozoa, nauplii).

Ranges of SE and CE for second-instar larvae were 0-77% and 0-100% (Fig. 1, II). Strike efficiency was >50% for most prey and CE was usually > 80%. Soft-bodied prey were nearly always ingested after being captured. Large differences between SE and CE occurred only when prey were difficult to catch (protozoa, Cyclops) or when larvae struck repeatedly and rapidly at "attrac- tive" prey (e.g. Keratella, mixed rotifers); many of these strikes missed. Several taxa were essentially uneaten. Chydorus sphaericus was attacked readily and captured (42% of 191 strikes were captures) but was rarely ingested. The gelatinous protozoan was seldom attacked, but most attacks (95%) were successful. Once captured this prey was actively rejected. Daphnia pulex neonates were frequently attacked and captured (42%) but were only rarely ingested.

Strike efficiency and contact efficiency ranged from 0 to 95% and 0 to 100% in feeding experiments with third-instar larvae (Fig. 1, III). For most prey SE was 50% or more, and CE was close to 100%. These larvae attacked the gelatinous protozoan more frequently than did second-instar larvae, and 83% of those strikes resulted in captures. These larvae also actively rejected this protozoan after contact. Of attacks on D. magna, 44% resulted in captures, but it was rarely ingested. Daphnia hyalina was captured with about the same frequency as D. magna but was ingested more successfully (Fig. 1, III).

The strike efficiency and contact efficiency of fourth-instar larvae ranged from 0 to 95% and 1 to 100% (Fig. 1, IV). All prey taxa tested were captured efficiently and ingested except the gelatinous protozoan and some daphnids. SE was 50% or more for all taxa successfully ingested, and CE was nearly 100% for all those taxa except cladocerans. Fourth-instar larvae seldom struck at the gelatinous protozoan, although 73% of those strikes were captures. This protozoan usually was actively rejected by these larvae; a few were successfully ingested. Daphnia magna (1.38 mm long) was aggressively at-

tacked and captured (49% of 311 strikes) but was too large to be ingested, as was D. pulex (1.69 mm long) (37% of 205 strikes were captures). These fourth-instar larvae ate small prey as effectively as large prey.

Maximal prey size for each of the four instars was closely related to their gape diameter (Fig. 2). Gape diameter (Table 1) increased 59, 63, and 48% from instar I to II, II to III, and III to IV. Maximal prey length increased by 695, 147, and 158% for the same intervals, and maximal prey width increased by 58, 63, and 57%. Prey width was more important than prey length in set- ting ingestion limits.

The relationship between mouth gape and maximal prey size was not simple; it was affected by prey morphology and texture. First-instar larvae successfully ingested Brachionus urceus slightly larger than their gape diameters, yet they could not ingest the somewhat smaller, but spiny K. quadrata (Fig. 2, 1; Table 2). Second-instar larvae successfully ingested prey much longer than their gape diameters (Fig. 1, II). Their mean gape diameter (0.27 mm) is very close to the head-capsule width of the culicid larvae successfully ingested (0.29, 0.30 mm) even though the length of those culicid larvae was several times greater than the larval mouth size (Table 2). These larvae were unable to ingest D. pulex with a body width less than their gape diameter; D. pulex is irregularly shaped and has a tail spine.

Third-instar larvae with a gape diameter of 0.44 mm successfully ingested culicid larvae with head-capsule widths of 0.49 mm yet had little success ingesting D. hyalina and D. magna whose body widths were 0.46 and 0.57 mm (Fig. 2, III). Fourth-instar larvae (mouth gape, 0.65 mm) had little trouble ingesting small daphnids (Fig. 2, IV) but were unable to ingest either D. magna or D. pulex whose body widths were larger than their gape diameters. They were, however, less effective at ingesting irregularly shaped daphnids with body widths smaller than their gape diameters than they were at ingesting culicid larvae with head-capsule widths of comparable sizes. They had little trouble ingesting large culicid and chironomid larvae whose head-capsule widths were less than their mouth gapes.




100

2 + 2 1 l 1. protozoan 6 2. Flilnia cornuta 50- I i 3. Keratella cochlearis

,4 4. cyclopoid nauplii l 5. Synchaeta spp.

3I 3 6. Brachionusurceus 0 -- 7. Bosmina longirostris

100 8. mixed rotifers - Y j Y , X , 9. gelatinous protozoan - t t I l 16 10. Chydorus sphaericus II

7 6 12 111. Keratella quadrata { 6 121 50 - 7 12. Cyclops sp. 3 11 13. Daphnia magna

14o 10 14. Daphnia pulex 00

, 14 i 10 15. Daphnia hyalina > ' '0 I 16. culicid larvae c t"' 16 17. chironomid larvae

O , ,,3I 18. Euglena sp. 50 2 6 10

~~I ~ ~ 6 :0151 2 t~~~1 I 13

50 0.102 0.3 0.1 . . . . . .

m 14~~~~~~

0 '''~~~ig.2.AsFi. 1, but_as __functin_of_pry_width

100

7 6 ,17 ~ 16

50 II ~~~~~~~~~1O 1 16

3 15 1

1 13 14

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0

Prey Width (mm) Fig. 2. As Fig. 1, but as a function of prey width.

The largest culicid larvae tested in the feeding trials had head-capsule widths greater than the mouth gapes of fourth-instar larvae. Usually, the entire bodies of those culicids were ingested either head or tail first; occasionally their head capsules protruded from the mouth of the Chaoborus larvae after most of the body had been ingested.

For most instar-prey combinations, orientation of the prey after capture had little effect on ingestion. Prey that were small

(length or width) relative to larval mouth size were ingested head first, tail first, or even sideways. Long soft-bodied prey (culicid and chironomid larvae) were also eaten head or tail first and were simply folded into the crop. Handling time (attack to ingestion) was usually only a few seconds (<20) for prey small relative to larval mouth size. When prey were large relative to larval mouth size or were irregular in shape, handling time increased and was occasionally as long as 8-10 min. Multiple strikes at the



20 Swift

same prey were very common, especially by first- and second-instar larvae. Individual prey were often caught, released, and caught again several times before they were ingested or lost. Prey taxa that elicited multiple strikes included Brachionus, Keratella, and Chydorus.

Swimming speed and postcontact behavior affected the probability of capture and ingestion. The fast swimming of the small protozoans and the relative lack of movement of nauplii made them difficult to capture and detect, respectively. Once captured, however, they were ingested easily. First- and second-instar larvae, in particular, appeared to require prey movement following capture to stimulate the appropriate movements of mouthparts for ingestion. Chydorus, which closed its valves and remained motionless when captured, was almost always released by second-instar larvae. In some cases the valves closed tightly on the antennal setae of these larvae, and the larvae had to shake the Chydorus off. This "deadman" response was very effective against second-instar larvae, but it was of little use against third- and fourth-instar larvae, which ingested Chydorus in a few seconds (Figs. 1, 2). Keratella cochlearis was also observed to cease all motion when caught by first-instar larvae; it was occasionally released and escaped ingestion. The gelatinous protozoan was actively rejected by instars I-IV following capture. Only fourth-instar larvae occasionally ingested one of these protozoans.

Body rigidity also affected ingestion. The relatively delicate D. hyalina was ingested more easily than the more robust but somewhat smaller D. magna. Successfully ingested D. magna were undamaged; D. hyalina was always bent or crushed during ingestion. Mouth gape strictly limited ingestion of D. magna but limited ingestion of D. hyalina to a lesser extent.

Prey taxa of any particular size were usually more readily captured and ingested as larval size (instar) increased (Table 1). For example, Chydorus was seldom eaten by second-instar larvae, but the probability of ingestion increased in third- and fourth-instar larvae. The same effect was seen for Synchaeta, Keratella, Brachionus, and small

D. pulex and D. magna. There was no ev- idence from the prey sizes tested that large larvae were unable to feed on the smallest prey. Indeed, my observations suggest that fourth-instar larvae were able to capture very small prey (-0. 1 mm) by striking with their mandibular fans alone, without movement of the head capsule or antennae.

Discussion Size effects-Results of my experiments

with C. crystallinus confirm and expand previous results showing that Chaoborus instars I, II, and III (Moore and Gilbert 1987) and IV (Swift and Fedorenko 1975; Swift and Forward 1981; Pastorok 1981) are gape- limited predators. My results show that for a variety of prey types, and for all four instars, prey width is a much better predictor of maximal prey size than is prey length. This conclusion is obvious from the strike efficiency data and from the ratios of maximal prey length: mouth size (1.29, 5.67, 5.11, and 5.48 for instars I-IV) and prey width: mouth size (1.11, 1.11, 1.11, and 1.18 for instars I-IV) for those prey ingested reg- ularly.

The relationship between prey width and mouth size is the most important factor de- termining successful ingestion, but it is modified by other characteristics of prey morphology. All four larval instars successfully ingested prey in which the body width was greater than the larval mouth size. In all these cases the prey were soft bodied (Brachionus) or crushable (culicid larvae). Occasionally third- and fourth-instar larvae succeeded in ingesting daphnids larger than their mouth sizes but these exceptions required very long handling times. Prey that were seldom or never ingested but that had body widths less than larval mouth size occurred in the feeding trials with first- and second-instar larvae. These prey had spines and were irregular in shape or hard bodied.

Strike efficiency is the best measure of predatory ability because it integrates the behavior of both predator and prey. Strike efficiency increased for a particular prey taxon-size combination as larvae grew from first to fourth instar. This result has been reported by Moore and Gilbert (1987) for Chaoborus punctipennis and by Walton




(1988) for Chaoborus americanus. Strike efficiencies measured in this study were high- er for all four instars than those reported (Table 3). Comparisons of SE are difficult to interpret because of differences in prey sizes, shapes, and behaviors and in larval mouth sizes. These factors undoubtedly result in the large between-laboratory differences in SE measurements within species (e.g. C. americanus IV) (Table 3).

The gape diameter of C. crystallinus larvae is intermediate between those of C. punctipennis and C. americanus. When larvae with approximately the same mouth sizes (crystallinus II, americanus II, punctipennis III; crystallinus III, americanus III, punctipennis IV) feeding on prey with about the same sizes and behaviors are compared, C. crystallinus was more successful at catch- ing and ingesting prey. Further studies in which standardized prey are tested against a range of Chaoborus species and instars will be required to define clearly the compara- tive predatory abilities of Chaoborus larvae.

For most prey types, if Chaoborus larvae are able to ingest them at all, the probability of ingestion after capture (contact efficiency, Swift and Fedorenko 1975; Pc.n Riessen et al. 1984, 1988; IC, Moore and Gilbert 1987) is very high for all instars. This relationship has been demonstrated for C. americanus IV (Swift and Fedorenko 1975; Riessen et al. 1988), Chaoborus trivittatus (Swift and Fedorenko 1975; Pastorok 1981; Riessen et al. 1988), and now for C. crystallinus. Uni- formly high CE values are found when prey width is less than mouth gape. Only Swift and Fedorenko (1975) have shown a gradual decrease in CE as prey size increased. From their data it is not possible to relate prey width to mouth gape precisely, but at least some of their Daphnia had a width (their "height") larger than the gape diameter of C. americanus and close to that of C. trivittatus.

Little is known about the minimal prey size of larval Chaoborus. Wilson (1975) suggested that capture success should decrease toward the minimum size that can be captured. The smallest prey that have been used in feeding studies of Chaoborus are rotifers (Moore and Gilbert 1987; this study) and protists (Walton 1988; this study). These

Table 3. Strike efficiencies of Chaoborus larvae on various prey. Values are the mean strike efficiency (%) calculated following arcsine, square-root transforma- tion of tabulated values in each reference. Gape values are the gape diameter.

c. c. c. Instar punctipennis crystallinus americanus

I Mean (SD) 24(1) 49(4) 36(3) Gape (mm) 0.13 0.17 - Reference* 1 2 3

II Mean (SD) 40(<1) 62(2) 49(12) Gape (mm) 0.20 0.27 0.30 Reference* 1 2 3,4

III Mean (SD) 52(1) 71(6) 64(8) Gape (mm) 0.33 0.44 0.43 Reference* 1 2 3,4

IV Mean (SD) 42(1) 81(2) 22(3) Gape (mm) 0.45 0.65 0.71 Reference* 5 2 3,4

IV Mean (SD) 31(<1) Reference* 6 Mean (SD) 59(9) Reference* 7

* 1-Moore and Gilbert 1987; 2-this study; 3-Walton 1988; 4-Fe- dorenko 1975a; 5-Swift and Forward 1981; 6-Riessen et al. 1984; 7-Vinyard and Menger 1980.

small prey are readily captured by first-, second, and third-instar larvae (Moore and Gilbert 1987; Walton 1988) and by fourth- instar C. crystallinus larvae. There was no decrease in prey capture ability by fourth- instar larvae feeding on the smallest prey. There are no experimental measurements of absolutely minimal prey size for any instar. Parma (1971) and Swuste et al. (1973) reported that they could raise Chaoborus on phytoplankton alone and several studies have reported phytoplankton in crop con- tents (Hare and Carter 1987; Moore 1988; Shei et al. 1988). In all these studies the protists or algae were motile.

Chaoborus larvae apparently strike in response to hydrodynamic disturbances (Hor- ridge 1966; Giguere and Dill 1979). It is not clear whether they would be able to sense pressure disturbances caused by nonmotile phytoplankton. At some size, potential prey must be too small to be handled efficiently



22 Swift

by the prey-capture apparatus of the larvae-antennae, antennal setae, prelabral appendages, labrum, mandibles, and mandibular fan. This lower size limit for efficient prey handling may be smaller than expect- ed. Observations on fourth-instar C. crystallinus feeding on small prey consistently resulted in more prey in the crops than the number of strikes made with the head capsule. These "extra" prey could have been captured incidentally while the larvae struck at other prey items, a phenomenon well de- scribed for planktivorous fish (Wright et al. 1983). Giguere and Dill (1983) suggested that the mandibular fans might be used for filter feeding. I think it is more likely that larvae strike actively at small, motile prey using their mandibular apparatus alone. The mechanism by which Chaoborus larvae ingest very small prey remains to be discovered.

Prey vulnerability-Prey vulnerability has been defined as (encounter rate) x (strike efficiency) (Pastorok 1981). My data demonstrate that both precontact and postcontact prey behavior can be effective at reducing capture and ingestion by Chaoborus larvae. These data also demonstrate that the effectiveness of particular prey behaviors, especially after contact, is instar-dependent.

Two precontact prey behavior patterns were effective at reducing Chaoborus predation. The very small, fast protozoan readily elicited strikes but most missed. Cy- clopoid nauplii reduced encounter frequen- cies by remaining motionless for long pe- riods occasionally interrupted by rapid darting movements. This behavior seldom elicited strikes by first-instar larvae; it was less successful against second-instar larvae.

Postcontact defenses exhibited by prey taxa included morphological characteristics (spines which increased "effective width," carapace rigidity, body texture) and behavior (cessation of movement). The effectiveness of these postcontact defenses was also instar-specific.

The most obvious example of the effectiveness of spines in preventing ingestion was the interaction between first-instar larvae and K. quadrata. First-instar larvae were able to ingest B. urceus that was 10% longer and 46% wider than K. quadrata; B. urceus

was even slightly wider than the gape diameter of first-instar larvae. Keratella quadrata, however, had short, curved spines on the corners of the lorica that prevented these larvae from ingesting them. This effect was entirely a postcontact phenomenon; 65% of strikes at K. quadrata successfully hit and held this rotifer. Moore and Gilbert (1987) suggested that manipulation of prey by Chaoborus larvae before ingestion may prevent spines from being an effective deterrent to ingestion. The rotifer species they studied, however, had spines in the posterior midline of the body that did not change the effective body width of spined individuals. Anterolaterally projecting spines in Kera- tella taurocephala may inhibit Chaoborus predation (Moore and Gilbert 1987); these rotifers coexist with Chaoborus in acid- stressed lakes in Ontario (Yan and Geiling 1985). Body rigidity affected ingestion indepen-

dently from prey width. Daphnia hyalina was always bent and crushed when ingested; it was the only daphnid successfully ingested whose intact body width was larger than the larval mouth size. The apparently more rigid D. pulex and D. magna were never damaged during ingestion and were rarely ingested when their body widths were larger than the larval mouth size. Culicid larvae, on the other hand, were easily ingested when their head-capsule widths were greater than larval gape diameter. Their smooth head capsule was easily crushed during ingestion. Chironomid larvae are often planktonic and may be a significant food source for Chao- borus larvae. Crops of third- and fourth- instar Chaoborus flavicans larvae from Mikolajskie Lake, Poland, often contained chironomid head capsules (pers. obs.).

A gelatinous sheath may be an effective postcontact deterrent to predation by Chao- borus larvae. The gelatinous protozoan used as prey in my experiments was attacked readily by naive second-, third-, and fourth- instar larvae but was rarely ingested. Fol- lowing contact, larvae usually dropped the protozoan, shook their head capsules, and repeatedly scraped their antennal setae with their mandibles in a cleaning motion. Lar- vae seldom struck at the protozoan again during the feeding trial. It is not known




whether this active rejection is caused by taste (sensu Kerfoot et al. 1980) or simply by texture.

Holopedium gibberum is the most common freshwater gelatinous zooplankter. Moore (1988) suggested that rotifer or cla- doceran zooplankton enclosed in gelatinous sheaths are probably unsuitable prey for Chaoborus. Vinyard and Menger (1980) also reported that large Holopedium was avoid- ed and small Holopedium was rarely ingested (SE = 22%, 1 mm long) in feeding trials with C. americanus. The protective value of the gelatinous sheath of Holope- dium may depend on the larval instar. Fe- dorenko (1975a) found that in October, Holopedium made up 30-50% of the number and biomass of the diet of fourth-instar C. americanus and C. trivittatus. The mechanism of the relative protection conferred by gelatinous sheaths needs to be elucidat- ed.

The most conspicuous example of postcontact protective behavior was cessation of motion-akinesis or the deadman response (Kerfoot et al. 1980). Keratella cochlearis occasionally escaped first-instar larvae by not moving after capture. My observations suggest that Chaoborus larvae require the stimulus of prey movement to initiate prey ingestion-especially in first- and second-instar larvae. This observation has not been reported previously even though both Moore and Gilbert (1987) and Walton (1988) observed predation of instars I and II on rotifers. The effectiveness of akinesis by Chydorus was highly instar- specific. Second-instar larvae seldom tried to ingest Chydorus even though it was easily caught and often caught repeatedly. Third- and fourth-instar larvae ingested Chydorus even though it remained motionless after capture. It was apparently small enough with respect to larval mouth size that reflexive movements by larval mouthparts resulted in ingestion. Culicid larvae, on the other hand, wriggled violently after capture and elicited instantaneous ingestion attempts.

Vulnerability of zooplankton prey to Chaoborus is of considerable interest because of its role in larval diet and optimal foraging models of larval predation. Most studies of larval diet have documented dif-

ferential acquisition among the various prey types available (Fedorenko 1975a; Lewis 1977; Hare and Carter 1987; Moore 1988; Riessen et al. 1988). As more has been learned about Chaoborus prey capture, the view of them has been refined from inver- tebrate predators with unknown abilities to gape-limited predators with species- and instar-specific predatory abilities defined by larval size and prey morphology and behavior. Further research will determine whether differential acquisition of prey by Chaoborus larvae is a true preference or whether it is simply the result of predator and prey size characteristics and prey defensive responses.

The ultimate goal of studies of Chaoborus prey capture is to be able to measure or predict the impact of Chaoborus larvae on zooplankton communities. The most successful approach to achieving this goal has been to manipulate larval densities experi- mentally (e.g. Neill 1981; Vanni 1988) or to carefully measure larval diet and prey population dynamics (e.g. Kajak and Ran- ke-Rybicka 1970; Fedorenko 1975b; Moore 1988). Another approach that has not been so widely used is to predict Chaoborus predation with prey vulnerability models (e.g. Pastorok 1981; Riessen et al. 1984, 1988). It remains to be seen if these models will be able to incorporate species-specific ontogenetic changes in larval prey capture ability, prey defensive tactics, depth distri- bution, and seasonal changes in prey species abundance.

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Submitted: 25 February 1991 Accepted: 16 May 1991

Revised: 26 September 1991



prey capture by the four larval instars of chaoborus crystallinus

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