Journal of Plankton Research Vol.12 no.5 pp.933-946, 1990

Perceptive performance and feeding behavior of calanoid copepods

Gustav-Adolf Paffenhdfer and Kellie D.LewisSkidaway Institute of Oceanography, PO Box 13687, Savannah, GA 31416, USA

Abstract. The goal of this study was to determine variables associated with calanoid feedingbehavior, and thus, to improve our understanding of the basics of calanoid feeding rates. Thesevariables included periods and frequency of appendage motion, rates of cell clearance, distance atwhich a copepod first reacts to a cell which is eventually captured, and rate of water flow through thearea covered by the motions of a copepod's feeding appendages. The effects of these variables onfeeding rates were determined for copepodids and adult females of the calanoid copepod Eucalanuspileatus at phytoplankton concentrations covering the range encountered by this species on thesouth-eastern shelf of the USA. Our results indicate that the distance at which E.pileatus perceivesphytoplankton cells increases ~2-fold as food concentrations decrease from 1.0 to 0.1 mm3 I"1.These results lead us to hypothesize that this is due to increased sensitivity of chemosensors on thecopepods' feeding appendages. This 2-fold increase in perceptive distance amounts to a near 4-foldincrease in perceived volume which is close to the 6-fold increase in volume swept clear (VSC) from1.0 to 0.1 mm3 I"1 of Thalassiosira weissflogii. We assume that the increases in VSC by planktoniccopepods, when food levels are below satiation, are largely a function of the sensory performance ofthe individual copepod.

Introduction

Many calanoid copepod species are known for their ability to exist overextended periods of varying food limitation which occurs during most of anycopepod's life history. Numerous studies of feeding rates have indicated thatclearance rates (volume swept clear per copepod per unit time) increase non-linearly with decreasing food concentration (e.g. Corner et al., 1972). Knownmechanisms underlying such performances were recently reviewed (Price, 1988;Paffenhofer, 1988). To obtain sufficient food particles for growth and repro-duction in the usually food-limited ocean requires active means by a copepod.This can be facilitated by specific swimming behavior, by feeding currents(Strickler, 1982), and by sensors which either perceive chemical (e.g. Friedmanand Strickler, 1975) or hydrodynamic signals (e.g. Strickler and Bal, 1973).However, encounter and sensing alone are insufficient. Copepods need tocapture food to ingest it. Earlier studies showed that certain calanoids react toapproaching algae before these reach their appendages (Paffenhofer et al., 1982)and displace the particles towards themselves. These observations supportedCushing's (1968) theory of estimating algal mortality rates (due to copepodingestion) from these animals' perceptive ranges (and swimming speeds).However, there is no empirical confirmation of his theory: we do not yet knowthe distances at which phytoplankton cells of certain sizes are perceived, howmany of the cells within that distance are perceived and eventually captured, andhow that is related to cell volume and concentration, and the copepod'scondition and size or stage. This study was designed to test the hypothesis thatperceptive range was one of the main variables governing feeding rates.

© Oxford University Press 933

G.-A.Paffenhofer and K.D.Lewis

Materials and methods

Adult females of the copepod Eucalanus pileatus, one of the characteristiccalanoids on the south-eastern shelf of the USA (Bowman, 1971), were collectedon the middle shelf off Savannah, GA. For studies with adult females, we mostlyused animals which were obtained at environmental temperatures between 18and.23°C. They were usually acclimated to 20°C and towards their respectiveexperimental food concentration for 3 days. The food species was the diatomThalassiosira weissflogii (11 p,m diameter). Food concentrations, simulating therange of environmental phytoplankton abundances, ranged from 0.03 to3.0 mm3 I"1 which is equal to 2.4-240 u,g C I"1.

Observations on copepodid stages of E.pileatus were conducted with animalswhich had been reared at 0.1, 0.3 or 1.0 mm3 P 1 of T. weissflogii at 20°C in ourlaboratory in 1900 ml screw-cap jars rotated at 0.2 r.p.m. on a ferris wheel at14 h/10 h light-dark cycle. Six to 24 h prior to filming we glued a thin cat hair oneach copepod's carapace. Attachment to a cat hair allowed us to keep eachcopepod in a fixed position during filming. After hair-glueing, all copepods werereturned to their experimental jars. For filming each copepod was placed in acuvette of 140 ml capacity using the same water in which the copepod had beenfeeding for the past 12-24 h. Specifics on the filming have been presented byAlcaraz et al. (1980). Two to three films at either 125 or 250 frames s"1 weretaken of each individual copepod, each lasting 32 or 16 s, respectively. Each filmwas taken ~2 min after the release of a fecal pellet, as the shortest intervalbetween pellet releases was 4 min. Pellet release rates, observed for most filmedcopepods in their cuvette, were used as an indicator of each copepod's conditionin relation to the other specimens at the same food concentration. Filmingobservations were made between 12.00 and 18.00 to minimize differences due todiel changes in feeding behavior. Previousstudies of ours showed no differencesbetween feeding rates of E.pileatus CIV to adult female during day and nighthours (Paffenhofer, 1984). A total of 118 films were analyzed with a Vanguardmotion analyzer covering all variables presented in Results.

Results

Feeding rates can be affected by the proportion of time during which a copepodmoves its appendages, thus creating a feeding current and/or swimming slowly(Price and Paffenhofer, 1986). Ontogenetic changes of this variable werepronounced (Table I). Older naupliar stages continuously moved their appen-dages, copepodid stages 1, 2 and 4 spent about two-thirds, and adult females82% of their time creating a feeding current. There were no significantdifferences between copepodids and adult females {P > 0.05, Kruskal-Wallistest; Conover, 1980). Differences in food concentration did not result in anysignificant differences in proportion of time of appendage motion of females, orcopepodid stage 2 (C2), although the latter spent increasing percentages of timeon appendage motion as food concentration decreased (Figure 1). Anothervariable which could affect feeding rates is the frequency of appendagemovement (Hz). Higher frequencies could lead to increasing amounts of water

934

Feeding behavior of calanoid copepods

Table I. Eucalanus pileatus: variables associated with feeding on the diatom T.weissflogii at aconcentration of 1.0 mm31"1 (±1 SE)

Appendage frequency(Hz)

% of time spentflapping appendages

Distance of cellperception

Number of animalsstudied

•Paffenhofer and Lewis

31001.i

% o

f to

tal t

o

oI

1 1

g 40-

2 20-o

n

A2Mxp

(1989).

#

0.03

N5/6*

16.3

100

92 ±

5

± 0.4

19

•

10.1

Cl

26.2

66.7

112 ±177 ±

6

±0.8

±5.8

1829

•

i

i0.3

C2

25

63

181168

6

.3

.0

++

o

±0.7

±4.7

2227

*

i

-C2

1.0

C4

22

69

182329

7

.0 ± 0.4

.3 + 6.7

±24± 41

3.0

Female

25.1 ± 1.1

82.1 ± 4.1

241 ± 19222 ± 2 0

7

Phytoplankton Concentration

Fig. 1. Eucalanus pileatus: percentage of time when copepods move their feeding appendages inrelation to food concentrations. ( • ) , female; (O), C2.

displaced in a current past a copepod. The frequencies of movement by naupliiwere significantly lower than those of copepodids (Table I; Paffenhofer andLewis, 1989), the frequencies of which decreased slightly with increasing stage.Only those of C4 were significantly different (Kruskal-Wallis and multiplecomparison tests, P < 0.05) from other stages, excluding nauplii. Appendagefrequency of adult females decreased from 0.3 mm31"1 on with decreasing foodconcentration (Figure 2). Comparing all values resulted in only the frequency of0.03 mm31"1 being significantly different from others (0.3, 1.0 and 3.0 mm31"1,P < 0.05, Kruskal-Wallis and multiple comparison tests). No significantdifferences were found for Cl.

The volume swept clear (VSC) by an animal per unit time is indicative of thatanimal's feeding performance. Our data are the results of observations ofindividual copepods (Figure 3). Clearance rates were obtained from counting

935

G.-A.Paffenhofer and K.D.Lewis

30- ,

I I I0.03 0.1 0.3 1.0

Phytoplankton Concentration (mm^

I3.0

Fig. 2. Eucalanus pileatus: appendage frequency as a function of food concentration. Symbols as inFigure 1.

_3o

•= 2 5 -

T3O 2 0 -

<DQ.OO 1 5 -

CO 1 0 -

"oQ. cCD a

(0

« n

<1

o-C2>

T*

T I I0.03 0.1 0.3 1.0 3.0

Phytoplankton Concentration (mirror1)

Fig. 3. Eucalanus pileatus: volume swept clear (VSC) as a function of food concentration. Symbols asin Figure 1.

the number of cells ingested during the filming period which ranged from 48 to96 s. The number of observed animals per food concentration ranged from 5(0.03, 0.1 and 3.0 mm3 P 1 ) to 7 (1.0 mm3 P 1 ) . Clearance rates increased from1.0 to 0.1 mm3 P 1 , and slightly decreased as the food concentration decreased

936

Feeding behavior of calanoid copepods

b

elle

'

a

ScrCDCOCO«

12-

10-

-

8 -

6 -

4 -

~

2 -

_

•

$

i

•

*

o-

CDQ.

0.03I

0.11

0.3I

1.0

Phytoplankton Concentration (mm -I ')3 , - 1 - ,3.0

Fig. 4. Eucalanus pileatus: pellet release rates as a function of food concentration of copepodidsstage 2 and adult females. Bars represent one standard error.

further. A comparison among all clearance rates showed no significantdifferences (Kruskal-Wallis and multiple comparison tests, P > 0.05) between0.3 and 0.1 mm3 I"1, 0.3 and 3.0, 1.0 and 3.0 mm3 I"1. At 0.03 mm3 I"1 anE.pileatus female ingested ~ 5 % of its body carbon daily which was insufficientto balance its metabolic expenses. At 0.1 mm3 I"1 it ate daily 17% of its bodycarbon. VSC of C2 increased significantly with decreasing food concentrationfrom 1.0 to 0.1 mm3 I"1 (P < 0.05). We could not obtain reliable data for C2 at0.03 mm3 I"1 because cells were encountered too infrequently. Whereasvariability of VSC increased with decreasing food concentration from 1.0 mm3

I"1 on (standard error increased although the number of observed copepodshardly changed), the pellet release rate (Figure 4) which can be used as ameasure of ingestion rate (Ayukai, 1987) showed little change in variability overthe entire range of food concentrations. Whereas VSC was based on obser-vations of up to 96 s, pellet release integrated over periods of up to 60 min.

When we determined the number of cell captures and ingestions per copepodwith the motion analyzer we also measured the distance at which a copepod firstreacted on an incoming cell which was eventually captured and ingested. Thesedistances were measured when viewing the copepods laterally. This first reactionwas the beginning of an irregular motion of either one of the second antennae(A2) or the maxillipeds (Mxp). Such motion indicated the displacement of aparcel of water, containing an algal cell, towards the copepod's median (Alcarazet al., 1980). These reactive distances which we call distance of-cell perceptionare considered minimum values because (i) there is most likely a delay of micro-or milliseconds between cell perception and reaction to it, and (ii) ourobservations were in two dimensions which will either be the exact distance ifcell and appendage are both in focus, or an underestimate if one is out of focus.

937

G.-A.PafTenhdfer and K.D.Lewis

The distance measured was from the tip of the A2 exopod or endopod or fromthe tip to the Mxp, excluding the setae, to the respective T.weissflogii cell.Longest perception distances were observed at the lower food concentrations(Figure 5). Cell perception distances for Mxp at 0.03, 0.1 and 0.3 mm3 P 1 ofT.weissflogii were significantly different from those at 1.0 and 3.0 mm3 I"1

(Kruskal-Wallis and multiple comparison tests). Note the relatively low valuefor A2 at 0.3 mm3 I"1: of the six females studied, those three which hadunusually short average perception distances for A2 showed unusually long onesfor Mxp. A Kruskal-Wallis test did not allow rejection of the null hypothesisthat perceptive distances of the A2 at all five food concentrations were identical(P > 0.05). The same result was obtained for A2 and Mxp of copepodid stage 2(C2, Figure 6). Perceptive distances increased ontogenetically for A2 from N 5/6

E 500-i

1 400-Q.

O

2 300-

o* - 200-

O

(0(0

b

100-

(

i

-

tii

JO - 2. Antennae• - Maxillipeds

if 0

0.03 0.1 0.3

Phytoplankton Concentration

i1.0 3.0

Fig. 5. Eucalanus pileatus: distance of cell perception of second antennae and maxillipeds as afunction of food concentration by adult females.

_ ~ 300-o 3-

S § 2 0°-CO 0 )

« y iooHQ.

O- 2. Antennae•-Maxillipeds

ft 9I 1 I

0.03 0.1 0.3Phytoplankton Concentration

Fig. 6. Same as Figure 5, but for copepodids stage 2.

938

1.0 3.0

Feeding behavior of calanoid copepods

to adult female at 1.0 mm3 P 1 of T.weissflogii (Table I). Maxilliped values werenearly identical for Cl and C2, with C4 recording, unexpectedly, the longestdistance.

To understand better the relationship between VSC and distance of first cellperception as a_ function of food concentration, we drew the flow fields offemales' feeding currents from 18 (front view) and 16 (lateral view) incomingcells respectively (Figures 7 and 8). The flow field seen from frontal (Figure 7)provided several insights: (i) water was displaced towards the copepod's median;(ii) it was accelerated towards the median; and (iii) outside the 1 mm s"1

isopleth the current reaching the tips of the setae of the mxp had a width of~4 mm. The lateral view (Figure 8) indicated that (i) algae over a range of~120° from near the first antennae (Al) to the rearward-pointing Mxp weredisplaced towards the copepod's appendages, and (ii) that most algae weredisplaced toward the copepod over an angle of ~95° (Figure 9a). The largearrow at 45° to the copepod's body (Figure 9a) is the approximate angle aroundwhich most cells are displaced towards E.pileatus. Using the maximum (—120°angle) and common (~95° angle) range of algae approaching (lateral view), andmaximum (4 mm current width) and common (3 mm) range from anterior(Figures 7 and 9b) we calculated the volume V of water passing through themaximum and common range of the feeding appendages respectively. Thesecalculations were based on the following variables: (i) looking at the female fromventral we assumed that the flow field surface at the 1.5 mm s"1 isopleth formedan ellipse with the radius rx along the body axis; and (ii) the radius r2 wasperpendicular to the body axis between A2 and Mxp, both radii being curvedalong the 1.5 mm s"1 isopleth (Figure 9). Instead of the 1.5 mm s"1 isopleth wecould have used also the 1, 2 or 3 mm s"1 isopleths. The volume V passing persecond through the appendage-swept range would be

V = ri x r2 x TT x 1.5 mm s"1 x % of active time

The period of activity was on average 91% of total time. Thus,

Vm!a = 2.25 mm x 1.95 mm x u x 1.5 mm s"1 x 0.91 = 18.8 mm3 s"1

or 1610 ml 24 h"1 female"1

common = 1-70 mm x 1.55 mm x u x 1.5 mm s"1 x 0.91 = 11.3 mm3 s"1

or 975 ml 24 h"1 female"1

Discussion

During our studies several conditions existed which may have influenced theresults. First, the animals observed were held in position and thus could notswim freely. Observations on free-swimming E.pileatus (G.-A.Paffenhofer,S.Richman and J.R.Strickler, unpublished data) have shown that their feeding

939

G.-A.Paffenhofer and K.D.Lewis

1mm

Fig. 7. Eucalanus pileatus: front view of part of an adult female and the flow field with the paths offive different cells of T.weissflogii, being displaced in the feeding current towards the copepod. Thenumbers 1-6 near the isopleths represent current velocity (mm s"1).

1.5

1mm

Fig. 8. Eucalanus pileatus: lateral view of an adult female and the flow field with the paths of fourdifferent cells of T.weissflogii, being displaced towards the copepod. The numbers 1.5-4 in eachisopleth indicate current velocity (mm s"1).

940

Feeding behavior of calanoid copepods

' 1.5 7-. / / >2 ' / . / AMXP

Fig. 9. Eucalanus pileatus: lateral (a) and frontal (b) views of an adult female showing radii ofmaximum (r, and r2 max) and common (>, com and r2 com) ranges of algae displaced in the feedingcurrent towards the copepod.

currents are similar in velocity and angles (lateral view) as observed for fastenedanimals. Second, our observations were made in two dimensions. We tried tocorrect this by obtaining some frontal footage. Nevertheless at most times wecould not observe any flicking activity of the mandibular palps or first maxillae,but could observe all captures by the second maxillae.

Ontogenetic changes

Part of this study included describing ontogenetic changes in variables onfeeding behavior (Table I) which had already been addressed earlier for naupliiand early copepodids (Paffenhofer and Lewis, 1989). At 1.0 mm3 P 1 ofT.weissflogii we observed major changes of per cent active periods and ofappendage frequency from N 5/6 to Cl of E.pileatus, and only small changesfrom Cl to C4. Partly due to the high food concentration, the copepodid stages,fairly close to satiation, spent only about two-thirds of the total time creating afeeding current. The frequency of appendage motion seems to be one of thevariables which characterizes a calanoid species: adult females of Paracalanussp. which are similar in length and weight to Cl of E.pileatus move theirappendages about three times faster than the latter (Price et al., 1983). Thisassumption is supported by the fact that appendage frequency is a variable oflittle variability compared with the other variables studied here. The averagedistance of cell perception for A2 and Mxp did not show the same relationshipfor each stage (Table I), and did not increase at an even rate with increasingstage. The generally observed increase of cell perception distance for A2 couldbe related to increased velocity of the feeding current which resulted in further

941

G.-A.Paffenhofer and K.D.Lewis

elongation of the active space around a phytoplankton cell (Andrews, 1983), andpossible ontogenic changes in sensory performance. One variable which couldaccount for much of the variability here is cell quality (Cowles et al., 1989) whichwe could not control perfectly. However, since at each filming session weincluded at least two different copepodid stages, variability due to food qualitybetween stages should not have been an important variable. We point out thatvariability of perception distances between individuals of one stage wasconsiderable, and was partly due to the limited number of cells perceived andcaptured per animal per 48-96 s, the wide range of perception distances perindividual, and the number of animals studied.

Effects of food concentration

Of major interest to us have been the partly unknown variables affecting theclearance rate of a copepod as food concentrations change. We know that theclearance rate for certain calanoids increases non-linearly with decreasing foodconcentration, attains a maximum, and decreases sharply once food concen-trations are lowered further (e.g. Corner et al., 1972). From experience with theoceanic E.hyalinus (Price and Paffenhofer, 1986) we decided to determineclearance rates, periods of activity, appendage frequencies and distances of cellperception by direct visual observations on individual females of E.pileatus.They remained active which we largely attributed to environmental foodabundances on the south-eastern shelf which rarely drop to a level similar to0.03 mm3 I"1 of food organisms encountered here. The only variable whichchanged similarly to VSC with decreasing food concentration was the cellperception distance of the Mxp, and, less pronounced, of the A2 (Figure 5). Asimilar tendency was found for the Mxp of E.pileatus C2 (Figure 6). These datalet us assume that VSC could be related to receptor performance. Increasedreceptor sensitivity had been assumed for the freshwater calanoid Diaptomussicilis when the ratio of active to passive captures of the alga Chlamydomonasproteus increased with decreasing cell concentration (Vanderploeg and Paffen-hofer, 1985).

To sense and capture food particles many calanoids create double shearscanning currents with their appendages. Without the feeding current a calanoidcopepod even swimming at 3-4 mm s"1 (versus the <1 mm s"1 of swimmingwhen feeding) would not encounter as many algae as with its feeding current(assuming it detected particles after bumping into them). The importance of afeeding current to the feeding performance of calanoids has been amplypresented (Strickler, 1984, 1985). The feeding current for a mainly herbivorouscalanoid has two functions: (i) to let large amounts of water pass close by or overthe copepod's sensors; and (ii) to create an elongated active space in the doublysheared flow field (Strickler, 1982), providing the copepod with an early warningthat an alga is approaching (Andrews, 1983). The latter hypothesized function isbased on a modeling study. To utilize the feeding current optimally, sensorsshould be arranged in three dimensions on the calanoid. Ultrastructural studieson setae of first and second maxillae and the mandibular palps of calanoids

942

Feeding behavior of calanoid copepods

revealed numerous chemo- but no mechanosensors (Friedman and Strickler,1975). We assume that they similarly occur on all feeding appendages ofE.pileatus. Since these appendages are arranged in two dimensions and extendin a third dimension with numerous setae, they could scan a body of water overtime as it flows by. The Al with its extended chemo- and mechanosensors(Barrientos Chacon, 1980) could only scan a rather small volume of water perunit time, and therefore alone would not be able to scan 20 ml of water per hour.The possibility of mechanosensory (Legier-Visser et al., 1986) is ruled out in ourcase because cells were only 11 u.m in diameter and were displaced mainlytowards chemoreceptors. This is also consistent with observations that inertparticles of this size are not captured actively (Paffenhofer and Van Sant, 1985;Vanderploeg et al., 1990).

Now we would like to address the following variables: perceptive range(Cushing, 1968), perceptive volume and sensor sensitivity in relation to VSC.Perceptive range is a function of the sensitivity of a copepod's receptors, theirlocation on the copepod, and signal strength of a potential food particle thatdepends on both non-nutritional and nutritional factors, e.g. size, physiologicalcondition and mobility of a living particle (Cowles et al., 1989; Vanderploeg etal., 1990). The maximum perceptive range reported so far was 1.25 mm for anundisclosed larger alga {E.pileatus female; Strickler, 1982). In our studies themaximum distances of perception of a T.weissflogii cell by a Mxp increasedwith decreasing food concentration from 0.56 mm at 3.0 mm31"1 to 1.94 mm at0.1 mm3 P 1 of T.weissflogii. However, these maximum and average values(Figures 5 and 6) would be insufficient to calculate a perceptive volume, becausethe moving appendages (A2, mandibular palp MdP, first maxillae Ml and Mxp)do not fully scan the entire cross-section of incoming feeding current, even whenthey are closest to each other. Since they are moving back and forth at ~25 Hz(Table I, Figure 2), they complete one sweep every 40 ms, and pass through thesame middle position every 20 ms. During 4 ms the feeding current is displaced280 (xm towards the copepod at 0.25 mm distance from the tip of a Mxp (Figure7), 200 \im at 0.50 mm distance and 60 u,m at 1.9 mm. A distance of 0.25 mm isnear the average perceptive range of a Mxp at 1.0 and 3.0 mm3 I"1 ofT.weissflogii, 0.50 mm the average at 0.1 and 1.9 mm the maximum range of0.1 mm3 I"1. Since lengths of setae on each A2 and Mxp range from ~80 to510 \xm, and most of them between 200 and 320 p,m respectively, most waterpassing through the path of appendage motion at 280 \LTCI 40 ms"1 should passvery close or between setae of the moving appendages. The greater the distancefrom the appendage, the slower the feeding current and the more frequently thesame water could be scanned by the moving appendage. Indeed if the appendagesensors lower their sensitivity thresholds with decreasing food concentration(Lorenz, 1981, his p. 151), as assumed from Figures 5 and 6, then the probabilityof perceiving a cell should be increased not only because of increased perceptiverange but also because of increased frequency of scanning the same water. Mostcells perceived at 1.0 and 3.0 mm3 I"1 were within the range of length of theaverage seta; at 0.1 mm3 I"1 most cells were perceived outside of the length ofan average seta.

943

G.-A.Paffenhofer and K.D.Lewis

The next step was to obtain a comparison of perceptive volumes at 1.0 and0.1 mm3 r 1 , and compare that relationship to VSC at 1.0 and 0.1 mm3 I"1. Weestimated perceptive volumes of individual maxillipeds (Mxp). Since their setaeare assumed to be covered with chemosensors (Friedman and Strickler, 1975),we took the average perception distance for the fan-like setae (Figure 7), andcalculated approximately the area covered by setae at a distance of 0.22 mm(1.0) and 0.46 mm (0.1 mm3 I"1) from the tip of the Mxp limb, which resulted in0.093 and 0.264 mm2 respectively. These data were multiplied by the distancetraveled at 25 Hz by each of the two areas of a Mxp per hour. The resultingperceptive volume was 2.20 ml Mxp"1 h"1 at 1.0 and 10.04 ml Mxp h"1 at0.1 mm3 I"1, the latter being 4.58 times larger than the former. In essence, the 2-fold increase in perceptive distance (one-dimensional) amounted to a 4.6-foldincrease in volume (three-dimensional) perceived by Mxp, which is fairly close tothe nearly 6-fold increase of VSC (Figure 4) over the range of these foodconcentrations. The increase of perceptive distance of the A2 from 1.0 to0.1 mm3 I"1 was only —1.2 fold (Figure 5) and thus would diminish the overallperceived volume considerably. However, overall perceived volume will not bethat much reduced because 53-72% of the cell perceptions with ensuingcaptures were made by Mxp. We cannot provide an exact value for theperceptive volumes of the A2 at different food concentrations because theycould not be adequately tracked at 125 frames s"1 at anterior and lateral views.An approximate calculation results in a 1.5-fold increase in perceptive volume ofA2 from 1.0 to 0.1 mm31""1. Since ~65% of the cells were perceived by Mxp and35% by A2, the overall increase in perceptive volume would be close to 3.5-fold.We assume that the difference of 6-fold (VSC) minus 3.5-fold = 2.5-fold inVSC-increase could be partly attributed to the fact that our longer (0.1 mm31"1)perceptive distances were far greater underestimates due to two-dimensionalobservations than those at shorter (1.0 mm3 I"1) distances.

One might ask what swimming would add to perceptive volume. Adultfemales of E.pileatus swam at speeds between 0.5 and 1.0 mm s~l when movingtheir feeding appendages (G.-A.Paffenhofer, S.Richman and J.R.Strickler,unpublished observations). Irrespective of swimming speed they passed similaramounts of water by their body which meant that the feeding current volumehardly changed. Swimming, however, implied that this copepod traveledthrough a large volume of water, increasing the probability of encounteringadvantageous food organisms and concentrations, in which it could remain forextended periods.

Lastly, we would like to compare VSC obtained from all captures/ingestions(Figure 3) with amounts of water passing in the feeding current within theappendage-swept area of the copepod. The maximum VSC observed was21.1 ml h"1 female"1 = 506 ml 24 h female (Figure 3). This value represents31% of the 1610 ml which passed daily through the appendage area, and let usassume that even at very low food concentrations, E.pileatus was not perfect inintercepting all T.weissflogii cells. However, 1610 ml 24 h"1 were not con-sidered an unrealistic value. The ratio of VSC of E.pileatus CV feeding onRhizosolenia alata (20 \um cell width, 250 u-m length) at 0.5 mm3 I"1 (8 n-g C

944

Feeding behavior of calanoid copepods

I"1) to that on T.weissflogii (12 n-m cell diameter) at 0.1 mm3 I"1 (8 jtg C I"1)was 3.4 (Paffenhofer and Van Sant, 1985, their figures 1 and 3). If this ratio wasapplied to females, then R.alata would be cleared at 1720 ml female"1 24 h"1 at0.5 mm3 I""1 and 20°C. This would mean that all cells passing through theappendage-swept area of the feeding current would be eaten. The excess feedingwould be due to cells being perceived at far greater distances, and capturedthrough realignment of the copepod. The probability that all R.alata in thefeeding current would be perceived (at that low food concentration) becomesobvious because R.alata (i) aligns itself in the current, and because its length willbe at least twice closely passed by an appendage while being displaced past thecopepod, (ii) should have a rather large elongated active space (Andrews, 1983)which increases the probability of being perceived, and (iii) could be perceivedhydrodynamically by the mechanosensors of the Al (Vanderploeg etal., 1990).When feeding on R.alata at low, non-satiating food levels, E.pileatus should benear-perfect in perceiving cells approaching its appendage-swept area.

In recent publications, the main emphasis had been placed on feedingcurrents, appendage morphology and flow around them (e.g. Koehl, 1983,1984;Strickler, 1985). However, appendages are of little value for food capture if theydo not perceive signals directly from approaching food particles, or indirectlyreceive information from the Al or any of the other appendages that a foodparticle has been perceived (M2 which can capture small particles passively).The functioning of the biological 'filter' of many mainly herbivorous calanoids isa function of a feeding current, sensor arrays, and sensor specificity and range ofperformance. Since sensor arrays on the Al vary between species (e.g.Barrientos Chacon, 1980), as well as swimming and feeding behavior, wehypothesize that co-existence of many copepods could be largely explained by (i)each species' sensory perception ability, in conjunction with (ii) each particularspecies' response to the input.

Acknowledgements

We would like to dedicate this paper to the memory of Dr Harold E.Edgerton.We would like to thank Drs D.W.Menzel and H.A.Vanderploeg for reviewingthe manuscript, Dannah McCauley and Judy Leonard for typing it and AnnaBoyette for the graphic work. This research was supported by NSF grantsOCE85-00917 and OCE87-23174 (Biological Oceanography).

References

Alcaraz.M., Paffenhofer.G.-A. and Strickler ,J.R. (1980) Catching the algae: a first account of visualobservations on filter feeding calanoids. In Kerfoot.W.C. (ed.), The Evolution and Ecology ofZooplankton Communities. University Press of New England, Hanover, NH, pp. 241-248.

Andrews,J.C. (1983) Deformation of the active space in the low Reynolds number feeding current ofcalanoid copepods. Can. J. Fish. Aquat. Sci., 40, 1293-1302.

Ayukai.T. (1987) Discriminate feeding of the calanoid copepod Acartia clausi in mixtures ofphytoplankton and inert particles. Mar. Biol., 94, 579-587.

Barrientos Chacon.Y. (1980) Ultrastructure of sensory units of the first antennae of calanoidcopepods. M.S.Tnesis, University of Ottawa, Ontario, Canada.

Bowman,T.E. (1971) The distribution of calanoid copepods off the southeastern United States

945

G.-A.Pafienhofer and K.D.Lewis

between Cape Hatteras and Southern Florida. Smithson. Contrib. Zool. No. 96. SmithsonianInstitution Press, Washington, DC.

Conover.W.J. (1980) Practical Nonparametric Statistics. John Wiley & Sons, New York.Corner.E.D.S., Head.R.N. and Kilvington.C.C. (1972) On the nutrition and metabolism of

zooplankton. VIII. The grazing of Biddulphia cells by Calanus helgolandicus. J. Mar. Biol. Assoc.U.K., 52, 847-861.

Cowles.T.J., Olson,R.J. and Chisholm.S.W. (1989) Food selection by copepods: discrimination onthe basis of food quality. Mar. Biol., 100, 41-49.

Cushing.D.H. (1968) Grazing by herbivorous copepods in the sea. /. Cons. Perm. Int. Explor. Mer.,32, 70-82.

Friedman,M.M. and Strickler,J.R. (1975) Chemoreceptors and feeding in calanoid copepods(Arthropoda: Crustacea). Proc. Nad. Acad. Sci. USA, 72, 4185-4188.

Koehl.M.A.R. (1983) The morphology and performance of suspension-feeding appendages. / .Theor. Biol., 105, 1-11.

Koehl.M.A.R. (1984) Mechanisms of particle capture by copepods at low Reynolds numbers:possible modes of selective feeding. In Meyers,D.G. and Strickler,J.R. (eds), Trophic InteractionsWithin Aquatic Ecosystems. AAAS Selected Symposium 85, Westview Press, Inc., Boulder, CO,pp. 135-166.

Legier-Visser.M., Mitchell.J.G., Okubo,A. and Fuhrman.J.A. (1986) Mechanoreception incalanoid copepods: a mechanism for prey detection. Mar. Biol., 90, 529-536.

Lorenz.K.Z. (1981) The Foundations of Ethology. Springer-Verlag, New York, Wien.Paffenhofer,G.-A. (1984) Calanoid copepod feeding: grazing on small and large particles. In

Meyers.D.G. and Strickler,J.R. (eds), Trophic Interactions Within Aquatic Ecosystems. AAASSelected Symposium 85, Westview Press, Inc., Boulder CO, pp. 75-95.

Paffenhofer,G.-A. (1988) Feeding rates and behavior of zooplankton. Bull. Mar. Sci., 43, 430-445.Paffenhofer,G.-A. and Lewis,K.D. (1989) Feeding behavior of nauplii of the genus Eucalanus

(Copepoda, Calanoida). Mar. Ecol. Progr. Ser., 57, 129-136.Paffenhofer,G.-A. and Van Sant.K.B. (1985) The feeding response of a marine planktonic copepod

to quantity and quality of particles. Mar. Ecol. Progr. Ser., 27, 55-65.Paffenhofer,G.-A., Strickler.J.R. and Alcaraz,M. (1982) Suspension-feeding by herbivorous

calanoid copepods: a cinematographic study. Mar. Biol., 67, 193-199.Price.H.J. (1988) Feeding mechanisms in marine and freshwater zooplankton. Bull. Mar. Sci., 43,

327-343.Price.H.J. and Paffenhofer,G.-A. (1986) Effects of concentration on the feeding of a marine

copepod in algal monocultures and mixtures. /. Plankton Res., 8, 119-128.Price.H.J., Paffenhofer,G.-A. and Strickler.J.R. (1983) Modes of cell capture in calanoid copepods.

Limnol. Oceanogr., 28, 116-123.Strickler,J.R. (1982) Calanoid copepods, feeding currents, and the role of gravity. Science, 218,

158-160.Strickler.J.R. (1984) Sticky water: a selective force in copepod evolution. In Meyers.D.G. and

Strickler.J.R. (eds), Trophic Interactions Within Aquatic Ecosystems. AAAS Selected Symposium85, Westview Press, Boulder, CO, pp. 187-239.

Strickler.J.R. (1985) Feeding currents in calanoid copepods: two new hypotheses. In Laverack.M.S.(ed.), Physiological Adaptations of Marine Animals. Symp. Soc. Exp. Biol., 89, 459-485.

Strickler,J.R. and Bal.A.K. (1973) Setae of the first antennae of the copepod Cyclops scutifer (Sars):their structure and importance. Proc. Natl. Acad. Sci. USA, 70, 2656-2659.

Vanderploeg.H.A. and Paffenh6fer,G.-A. (1985) Modes of algal capture by the fresh-watercopepod Diaptomus sicilis and their relation to food-size selection. Limnol. Oceanogr., 30,871-885.

Vanderploeg.H.A., Paffenhofer,G.-A. and Liebig,J.R. (1990) Concentration-variable interactionsbetween calanoid copepods and particles of different food quality: observations and hypotheses.In Hughes.R.N. (ed.), Behavioral Mechanisms of Food Selection. NATO ASI-Series, A-LifeSciences, Springer-Verlag, Berlin, Heidelberg, New York, pp. 595-613.

Received on November 6, 1989; accepted on April 16, 1990

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