Journal of Plankton Research Vol.12 no.5 pp.933-946, 1990 Perceptve performance and feedng behavor of calanod copepods Gustav-Adolf Paffenhdfer and Kelle D.Lews Skdaway Insttute of Oceanography, PO Box 13687, Savannah, GA 31416, USA Abstract. The goal of ths study was to determne varables assocated wth calanod feedng behavor, and thus, to mprove our understandng of the bascs of calanod feedng rates. These varables ncluded perods and frequency of appendage moton, rates of cell clearance, dstance at whch a copepod frst reacts to a cell whch s eventually captured, and rate of water flow through the area covered by the motons of a copepod's feedng appendages. The effects of these varables on feedng rates were determned for copepodds and adult females of the calanod copepod Eucalanus pleatus at phytoplankton concentratons coverng the range encountered by ths speces on the south-eastern shelf of the USA. Our results ndcate that the dstance at whch E.pleatus perceves phytoplankton cells ncreases ~2-fold as food concentratons decrease from 1.0 to 0.1 mm 3 I" 1. These results lead us to hypothesze that ths s due to ncreased senstvty of chemosensors on the copepods' feedng appendages. Ths 2-fold ncrease n perceptve dstance amounts to a near 4-fold ncrease n perceved volume whch s close to the 6-fold ncrease n volume swept clear (VSC) from 1.0 to 0.1 mm 3 I" 1 of Thalassosra wessflog. We assume that the ncreases n VSC by planktonc copepods, when food levels are below sataton, are largely a functon of the sensory performance of the ndvdual copepod. Introducton Many calanod copepod speces are known for ther ablty to exst over extended perods of varyng food lmtaton whch occurs durng most of any copepod's lfe hstory. Numerous studes of feedng rates have ndcated that clearance rates (volume swept clear per copepod per unt tme) ncrease nonlnearly wth decreasng food concentraton (e.g. Corner et al., 1972). Known mechansms underlyng such performances were recently revewed (Prce, 1988; Paffenhofer, 1988). To obtan suffcent food partcles for growth and reproducton n the usually food-lmted ocean requres actve means by a copepod. Ths can be facltated by specfc swmmng behavor, by feedng currents (Strckler, 1982), and by sensors whch ether perceve chemcal (e.g. Fredman and Strckler, 1975) or hydrodynamc sgnals (e.g. Strckler and Bal, 1973). However, encounter and sensng alone are nsuffcent. Copepods need to capture food to ngest t. Earler studes showed that certan calanods react to approachng algae before these reach ther appendages (Paffenhofer et al., 1982) and dsplace the partcles towards themselves. These observatons supported Cushng's (1968) theory of estmatng algal mortalty rates (due to copepod ngeston) from these anmals' perceptve ranges (and swmmng speeds). However, there s no emprcal confrmaton of hs theory: we do not yet know the dstances at whch phytoplankton cells of certan szes are perceved, how many of the cells wthn that dstance are perceved and eventually captured, and how that s related to cell volume and concentraton, and the copepod's condton and sze or stage. Ths study was desgned to test the hypothess that perceptve range was one of the man varables governng feedng rates. Oxford Unversty Press 933
G.-A.Paffenhofer and K.D.Lews Materals and methods Adult females of the copepod Eucalanus pleatus, one of the characterstc calanods on the south-eastern shelf of the USA (Bowman, 1971), were collected on the mddle shelf off Savannah, GA. For studes wth adult females, we mostly used anmals whch were obtaned at envronmental temperatures between 18 and.23 C. They were usually acclmated to 20 C and towards ther respectve expermental food concentraton for 3 days. The food speces was the datom Thalassosra wessflog (11 p,m dameter). Food concentratons, smulatng the range of envronmental phytoplankton abundances, ranged from 0.03 to 3.0 mm 3 I" 1 whch s equal to 2.4-240 u,g C I" 1. Observatons on copepodd stages of E.pleatus were conducted wth anmals whch had been reared at 0.1, 0.3 or 1.0 mm 3 P 1 of T. wessflog at 20 C n our laboratory n 1900 ml screw-cap jars rotated at 0.2 r.p.m. on a ferrs wheel at 14 h/10 h lght-dark cycle. Sx to 24 h pror to flmng we glued a thn cat har on each copepod's carapace. Attachment to a cat har allowed us to keep each copepod n a fxed poston durng flmng. After har-glueng, all copepods were returned to ther expermental jars. For flmng each copepod was placed n a cuvette of 140 ml capacty usng the same water n whch the copepod had been feedng for the past 12-24 h. Specfcs on the flmng have been presented by Alcaraz et al. (1980). Two to three flms at ether 125 or 250 frames s" 1 were taken of each ndvdual copepod, each lastng 32 or 16 s, respectvely. Each flm was taken ~2 mn after the release of a fecal pellet, as the shortest nterval between pellet releases was 4 mn. Pellet release rates, observed for most flmed copepods n ther cuvette, were used as an ndcator of each copepod's condton n relaton to the other specmens at the same food concentraton. Flmng observatons were made between 12.00 and 18.00 to mnmze dfferences due to del changes n feedng behavor. Prevousstudes of ours showed no dfferences between feedng rates of E.pleatus CIV to adult female durng day and nght hours (Paffenhofer, 1984). A total of 118 flms were analyzed wth a Vanguard moton analyzer coverng all varables presented n Results. Results Feedng rates can be affected by the proporton of tme durng whch a copepod moves ts appendages, thus creatng a feedng current and/or swmmng slowly (Prce and Paffenhofer, 1986). Ontogenetc changes of ths varable were pronounced (Table I). Older nauplar stages contnuously moved ther appendages, copepodd stages 1, 2 and 4 spent about two-thrds, and adult females 82% of ther tme creatng a feedng current. There were no sgnfcant dfferences between copepodds and adult females {P > 0.05, Kruskal-Walls test; Conover, 1980). Dfferences n food concentraton dd not result n any sgnfcant dfferences n proporton of tme of appendage moton of females, or copepodd stage 2 (C2), although the latter spent ncreasng percentages of tme on appendage moton as food concentraton decreased (Fgure 1). Another varable whch could affect feedng rates s the frequency of appendage movement (Hz). Hgher frequences could lead to ncreasng amounts of water 934
Feedng behavor of calanod copepods Table I. Eucalanus pleatus: varables assocated wth feedng on the datom T.wessflog at a concentraton of 1.0 mm 3 1" 1 (±1 SE) N5/6* Cl C2 C4 Female Appendage frequency (Hz) % of tme spent flappng appendages Dstance of cell percepton Number of anmals studed A2 Mxp 16.3 ± 0.4 100 92 ± 19 5 26.2 ±0.8 66.7 ±5.8 112 ± 177 ± 6 18 29 25.3 ±0.7 63.0 ±4.7 181 168 6 + + 22 27 22.0 ± 0.4 69.3 + 6.7 182 ±24 329 ± 41 7 25.1 ± 1.1 82.1 ± 4.1 241 ± 19 222 ±20 7 Paffenhofer and Lews (1989). 3 100 1. % of total t o o I 1 1 # * g 40-2 20- o n o -C2 0.03 1 0.1 0.3 1.0 Phytoplankton Concentraton 3.0 Fg. 1. Eucalanus pleatus: percentage of tme when copepods move ther feedng appendages n relaton to food concentratons. ( ), female; (O), C2. dsplaced n a current past a copepod. The frequences of movement by naupl were sgnfcantly lower than those of copepodds (Table I; Paffenhofer and Lews, 1989), the frequences of whch decreased slghtly wth ncreasng stage. Only those of C4 were sgnfcantly dfferent (Kruskal-Walls and multple comparson tests, P < 0.05) from other stages, excludng naupl. Appendage frequency of adult females decreased from 0.3 mm 3 1" 1 on wth decreasng food concentraton (Fgure 2). Comparng all values resulted n only the frequency of 0.03 mm 3 1" 1 beng sgnfcantly dfferent from others (0.3, 1.0 and 3.0 mm 3 1" 1, P < 0.05, Kruskal-Walls and multple comparson tests). No sgnfcant dfferences were found for Cl. The volume swept clear (VSC) by an anmal per unt tme s ndcatve of that anmal's feedng performance. Our data are the results of observatons of ndvdual copepods (Fgure 3). Clearance rates were obtaned from countng 935
G.-A.Paffenhofer and K.D.Lews 30-, I I I 0.03 0.1 0.3 1.0 Phytoplankton Concentraton (mm^ I 3.0 Fg. 2. Eucalanus pleatus: appendage frequency as a functon of food concentraton. Symbols as n Fgure 1. = 25- T3 O 20- <1 > o-c2 <D Q. O O 15- CO 10- "o Q. c CD a (0 «n _3 o T * T I I 0.03 0.1 0.3 1.0 3.0 Phytoplankton Concentraton (mrror 1 ) Fg. 3. Eucalanus pleatus: volume swept clear (VSC) as a functon of food concentraton. Symbols as n Fgure 1. the number of cells ngested durng the flmng perod whch ranged from 48 to 96 s. The number of observed anmals per food concentraton ranged from 5 (0.03, 0.1 and 3.0 mm 3 P 1 ) to 7 (1.0 mm 3 P 1 ). Clearance rates ncreased from 1.0 to 0.1 mm 3 P 1, and slghtly decreased as the food concentraton decreased 936
Feedng behavor of calanod copepods b elle' a 12-10- - 8- $ * 6- S cr CD CO CO «CD Q. 4- ~ 2- _ o- I 1 I 0.03 0.1 0.3 1.0 Phytoplankton Concentraton (mm 3,-1-, -I ') 3.0 Fg. 4. Eucalanus pleatus: pellet release rates as a functon of food concentraton of copepodds stage 2 and adult females. Bars represent one standard error. further. A comparson among all clearance rates showed no sgnfcant dfferences (Kruskal-Walls and multple comparson tests, P > 0.05) between 0.3 and 0.1 mm 3 I" 1, 0.3 and 3.0, 1.0 and 3.0 mm 3 I" 1. At 0.03 mm 3 I" 1 an E.pleatus female ngested ~ 5% of ts body carbon daly whch was nsuffcent to balance ts metabolc expenses. At 0.1 mm 3 I" 1 t ate daly 17% of ts body carbon. VSC of C2 ncreased sgnfcantly wth decreasng food concentraton from 1.0 to 0.1 mm 3 I" 1 (P < 0.05). We could not obtan relable data for C2 at 0.03 mm 3 I" 1 because cells were encountered too nfrequently. Whereas varablty of VSC ncreased wth decreasng food concentraton from 1.0 mm 3 I" 1 on (standard error ncreased although the number of observed copepods hardly changed), the pellet release rate (Fgure 4) whch can be used as a measure of ngeston rate (Ayuka, 1987) showed lttle change n varablty over the entre range of food concentratons. Whereas VSC was based on observatons of up to 96 s, pellet release ntegrated over perods of up to 60 mn. When we determned the number of cell captures and ngestons per copepod wth the moton analyzer we also measured the dstance at whch a copepod frst reacted on an ncomng cell whch was eventually captured and ngested. These dstances were measured when vewng the copepods laterally. Ths frst reacton was the begnnng of an rregular moton of ether one of the second antennae (A2) or the maxllpeds (Mxp). Such moton ndcated the dsplacement of a parcel of water, contanng an algal cell, towards the copepod's medan (Alcaraz et al., 1980). These reactve dstances whch we call dstance of-cell percepton are consdered mnmum values because () there s most lkely a delay of mcroor mllseconds between cell percepton and reacton to t, and () our observatons were n two dmensons whch wll ether be the exact dstance f cell and appendage are both n focus, or an underestmate f one s out of focus. 937
G.-A.PafTenhdfer and K.D.Lews The dstance measured was from the tp of the A2 exopod or endopod or from the tp to the Mxp, excludng the setae, to the respectve T.wessflog cell. Longest percepton dstances were observed at the lower food concentratons (Fgure 5). Cell percepton dstances for Mxp at 0.03, 0.1 and 0.3 mm 3 P 1 of T.wessflog were sgnfcantly dfferent from those at 1.0 and 3.0 mm 3 I" 1 (Kruskal-Walls and multple comparson tests). Note the relatvely low value for A2 at 0.3 mm 3 I" 1 : of the sx females studed, those three whch had unusually short average percepton dstances for A2 showed unusually long ones for Mxp. A Kruskal-Walls test dd not allow rejecton of the null hypothess that perceptve dstances of the A2 at all fve food concentratons were dentcal (P > 0.05). The same result was obtaned for A2 and Mxp of copepodd stage 2 (C2, Fgure 6). Perceptve dstances ncreased ontogenetcally for A2 from N 5/6 E 500-1 400- Q. O 2 300- O (0 (0 b o *- 200-100- - ( t 0.03 0.1 0.3 Phytoplankton Concentraton J O - 2. Antennae - Maxllpeds f 1.0 0 3.0 Fg. 5. Eucalanus pleatus: dstance of cell percepton of second antennae and maxllpeds as a functon of food concentraton by adult females. _ ~ 300- o 3- S 20 - CO 0) «y ooh Q. O- 2. Antennae -Maxllpeds ft 9 I 1 I 0.03 0.1 0.3 Phytoplankton Concentraton 1.0 3.0 Fg. 6. Same as Fgure 5, but for copepodds stage 2. 938
Feedng behavor of calanod copepods to adult female at 1.0 mm 3 P 1 of T.wessflog (Table I). Maxllped values were nearly dentcal for Cl and C2, wth C4 recordng, unexpectedly, the longest dstance. To understand better the relatonshp between VSC and dstance of frst cell percepton as a_ functon of food concentraton, we drew the flow felds of females' feedng currents from 18 (front vew) and 16 (lateral vew) ncomng cells respectvely (Fgures 7 and 8). The flow feld seen from frontal (Fgure 7) provded several nsghts: () water was dsplaced towards the copepod's medan; () t was accelerated towards the medan; and () outsde the 1 mm s" 1 sopleth the current reachng the tps of the setae of the mxp had a wdth of ~4 mm. The lateral vew (Fgure 8) ndcated that () algae over a range of ~120 from near the frst antennae (Al) to the rearward-pontng Mxp were dsplaced towards the copepod's appendages, and () that most algae were dsplaced toward the copepod over an angle of ~95 (Fgure 9a). The large arrow at 45 to the copepod's body (Fgure 9a) s the approxmate angle around whch most cells are dsplaced towards E.pleatus. Usng the maxmum ( 120 angle) and common (~95 angle) range of algae approachng (lateral vew), and maxmum (4 mm current wdth) and common (3 mm) range from anteror (Fgures 7 and 9b) we calculated the volume V of water passng through the maxmum and common range of the feedng appendages respectvely. These calculatons were based on the followng varables: () lookng at the female from ventral we assumed that the flow feld surface at the 1.5 mm s" 1 sopleth formed an ellpse wth the radus r x along the body axs; and () the radus r 2 was perpendcular to the body axs between A2 and Mxp, both rad beng curved along the 1.5 mm s" 1 sopleth (Fgure 9). Instead of the 1.5 mm s" 1 sopleth we could have used also the 1, 2 or 3 mm s" 1 sopleths. The volume V passng per second through the appendage-swept range would be V = r x r 2 x TT x 1.5 mm s" 1 x % of actve tme The perod of actvty was on average 91% of total tme. Thus, V m!a = 2.25 mm x 1.95 mm x u x 1.5 mm s" 1 x 0.91 = 18.8 mm 3 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 mm 3 s" 1 Dscusson or 975 ml 24 h" 1 female" 1 Durng our studes several condtons exsted whch may have nfluenced the results. Frst, the anmals observed were held n poston and thus could not swm freely. Observatons on free-swmmng E.pleatus (G.-A.Paffenhofer, S.Rchman and J.R.Strckler, unpublshed data) have shown that ther feedng 939
G.-A.Paffenhofer and K.D.Lews 1mm Fg. 7. Eucalanus pleatus: front vew of part of an adult female and the flow feld wth the paths of fve dfferent cells of T.wessflog, beng dsplaced n the feedng current towards the copepod. The numbers 1-6 near the sopleths represent current velocty (mm s" 1 ). 1.5 1mm Fg. 8. Eucalanus pleatus: lateral vew of an adult female and the flow feld wth the paths of four dfferent cells of T.wessflog, beng dsplaced towards the copepod. The numbers 1.5-4 n each sopleth ndcate current velocty (mm s" 1 ). 940
Feedng behavor of calanod copepods ' 1.5 7-. / /> 2 '/./ AMXP Fg. 9. Eucalanus pleatus: lateral (a) and frontal (b) vews of an adult female showng rad of maxmum (r, and r 2 max) and common (>, com and r 2 com) ranges of algae dsplaced n the feedng current towards the copepod. currents are smlar n velocty and angles (lateral vew) as observed for fastened anmals. Second, our observatons were made n two dmensons. We tred to correct ths by obtanng some frontal footage. Nevertheless at most tmes we could not observe any flckng actvty of the mandbular palps or frst maxllae, but could observe all captures by the second maxllae. Ontogenetc changes Part of ths study ncluded descrbng ontogenetc changes n varables on feedng behavor (Table I) whch had already been addressed earler for naupl and early copepodds (Paffenhofer and Lews, 1989). At 1.0 mm 3 P 1 of T.wessflog we observed major changes of per cent actve perods and of appendage frequency from N 5/6 to Cl of E.pleatus, and only small changes from Cl to C4. Partly due to the hgh food concentraton, the copepodd stages, farly close to sataton, spent only about two-thrds of the total tme creatng a feedng current. The frequency of appendage moton seems to be one of the varables whch characterzes a calanod speces: adult females of Paracalanus sp. whch are smlar n length and weght to Cl of E.pleatus move ther appendages about three tmes faster than the latter (Prce et al., 1983). Ths assumpton s supported by the fact that appendage frequency s a varable of lttle varablty compared wth the other varables studed here. The average dstance of cell percepton for A2 and Mxp dd not show the same relatonshp for each stage (Table I), and dd not ncrease at an even rate wth ncreasng stage. The generally observed ncrease of cell percepton dstance for A2 could be related to ncreased velocty of the feedng current whch resulted n further 941
G.-A.Paffenhofer and K.D.Lews elongaton of the actve space around a phytoplankton cell (Andrews, 1983), and possble ontogenc changes n sensory performance. One varable whch could account for much of the varablty here s cell qualty (Cowles et al., 1989) whch we could not control perfectly. However, snce at each flmng sesson we ncluded at least two dfferent copepodd stages, varablty due to food qualty between stages should not have been an mportant varable. We pont out that varablty of percepton dstances between ndvduals of one stage was consderable, and was partly due to the lmted number of cells perceved and captured per anmal per 48-96 s, the wde range of percepton dstances per ndvdual, and the number of anmals studed. Effects of food concentraton Of major nterest to us have been the partly unknown varables affectng the clearance rate of a copepod as food concentratons change. We know that the clearance rate for certan calanods ncreases non-lnearly wth decreasng food concentraton, attans a maxmum, and decreases sharply once food concentratons are lowered further (e.g. Corner et al., 1972). From experence wth the oceanc E.hyalnus (Prce and Paffenhofer, 1986) we decded to determne clearance rates, perods of actvty, appendage frequences and dstances of cell percepton by drect vsual observatons on ndvdual females of E.pleatus. They remaned actve whch we largely attrbuted to envronmental food abundances on the south-eastern shelf whch rarely drop to a level smlar to 0.03 mm 3 I" 1 of food organsms encountered here. The only varable whch changed smlarly to VSC wth decreasng food concentraton was the cell percepton dstance of the Mxp, and, less pronounced, of the A2 (Fgure 5). A smlar tendency was found for the Mxp of E.pleatus C2 (Fgure 6). These data let us assume that VSC could be related to receptor performance. Increased receptor senstvty had been assumed for the freshwater calanod Daptomus scls when the rato of actve to passve captures of the alga Chlamydomonas proteus ncreased wth decreasng cell concentraton (Vanderploeg and Paffenhofer, 1985). To sense and capture food partcles many calanods create double shear scannng currents wth ther appendages. Wthout the feedng current a calanod copepod even swmmng at 3-4 mm s" 1 (versus the <1 mm s" 1 of swmmng when feedng) would not encounter as many algae as wth ts feedng current (assumng t detected partcles after bumpng nto them). The mportance of a feedng current to the feedng performance of calanods has been amply presented (Strckler, 1984, 1985). The feedng current for a manly herbvorous calanod has two functons: () to let large amounts of water pass close by or over the copepod's sensors; and () to create an elongated actve space n the doubly sheared flow feld (Strckler, 1982), provdng the copepod wth an early warnng that an alga s approachng (Andrews, 1983). The latter hypotheszed functon s based on a modelng study. To utlze the feedng current optmally, sensors should be arranged n three dmensons on the calanod. Ultrastructural studes on setae of frst and second maxllae and the mandbular palps of calanods 942
Feedng behavor of calanod copepods revealed numerous chemo- but no mechanosensors (Fredman and Strckler, 1975). We assume that they smlarly occur on all feedng appendages of E.pleatus. Snce these appendages are arranged n two dmensons and extend n a thrd dmenson wth numerous setae, they could scan a body of water over tme as t flows by. The Al wth ts extended chemo- and mechanosensors (Barrentos Chacon, 1980) could only scan a rather small volume of water per unt tme, and therefore alone would not be able to scan 20 ml of water per hour. The possblty of mechanosensory (Leger-Vsser et al., 1986) s ruled out n our case because cells were only 11 u.m n dameter and were dsplaced manly towards chemoreceptors. Ths s also consstent wth observatons that nert partcles of ths sze are not captured actvely (Paffenhofer and Van Sant, 1985; Vanderploeg et al., 1990). Now we would lke to address the followng varables: perceptve range (Cushng, 1968), perceptve volume and sensor senstvty n relaton to VSC. Perceptve range s a functon of the senstvty of a copepod's receptors, ther locaton on the copepod, and sgnal strength of a potental food partcle that depends on both non-nutrtonal and nutrtonal factors, e.g. sze, physologcal condton and moblty of a lvng partcle (Cowles et al., 1989; Vanderploeg et al., 1990). The maxmum perceptve range reported so far was 1.25 mm for an undsclosed larger alga {E.pleatus female; Strckler, 1982). In our studes the maxmum dstances of percepton of a T.wessflog cell by a Mxp ncreased wth decreasng food concentraton from 0.56 mm at 3.0 mm 3 1" 1 to 1.94 mm at 0.1 mm 3 P 1 of T.wessflog. However, these maxmum and average values (Fgures 5 and 6) would be nsuffcent to calculate a perceptve volume, because the movng appendages (A2, mandbular palp MdP, frst maxllae Ml and Mxp) do not fully scan the entre cross-secton of ncomng feedng current, even when they are closest to each other. Snce they are movng back and forth at ~25 Hz (Table I, Fgure 2), they complete one sweep every 40 ms, and pass through the same mddle poston every 20 ms. Durng 4 ms the feedng current s dsplaced 280 (xm towards the copepod at 0.25 mm dstance from the tp of a Mxp (Fgure 7), 200 \m at 0.50 mm dstance and 60 u,m at 1.9 mm. A dstance of 0.25 mm s near the average perceptve range of a Mxp at 1.0 and 3.0 mm 3 I" 1 of T.wessflog, 0.50 mm the average at 0.1 and 1.9 mm the maxmum range of 0.1 mm 3 I" 1. Snce lengths of setae on each A2 and Mxp range from ~80 to 510 \xm, and most of them between 200 and 320 p,m respectvely, most water passng through the path of appendage moton at 280 \LTCI 40 ms" 1 should pass very close or between setae of the movng appendages. The greater the dstance from the appendage, the slower the feedng current and the more frequently the same water could be scanned by the movng appendage. Indeed f the appendage sensors lower ther senstvty thresholds wth decreasng food concentraton (Lorenz, 1981, hs p. 151), as assumed from Fgures 5 and 6, then the probablty of percevng a cell should be ncreased not only because of ncreased perceptve range but also because of ncreased frequency of scannng the same water. Most cells perceved at 1.0 and 3.0 mm 3 I" 1 were wthn the range of length of the average seta; at 0.1 mm 3 I" 1 most cells were perceved outsde of the length of an average seta. 943
G.-A.Paffenhofer and K.D.Lews The next step was to obtan a comparson of perceptve volumes at 1.0 and 0.1 mm 3 r 1, and compare that relatonshp to VSC at 1.0 and 0.1 mm 3 I" 1. We estmated perceptve volumes of ndvdual maxllpeds (Mxp). Snce ther setae are assumed to be covered wth chemosensors (Fredman and Strckler, 1975), we took the average percepton dstance for the fan-lke setae (Fgure 7), and calculated approxmately the area covered by setae at a dstance of 0.22 mm (1.0) and 0.46 mm (0.1 mm 3 I" 1 ) from the tp of the Mxp lmb, whch resulted n 0.093 and 0.264 mm 2 respectvely. These data were multpled by the dstance traveled at 25 Hz by each of the two areas of a Mxp per hour. The resultng perceptve volume was 2.20 ml Mxp" 1 h" 1 at 1.0 and 10.04 ml Mxp h" 1 at 0.1 mm 3 I" 1, the latter beng 4.58 tmes larger than the former. In essence, the 2- fold ncrease n perceptve dstance (one-dmensonal) amounted to a 4.6-fold ncrease n volume (three-dmensonal) perceved by Mxp, whch s farly close to the nearly 6-fold ncrease of VSC (Fgure 4) over the range of these food concentratons. The ncrease of perceptve dstance of the A2 from 1.0 to 0.1 mm 3 I" 1 was only 1.2 fold (Fgure 5) and thus would dmnsh the overall perceved volume consderably. However, overall perceved volume wll not be that much reduced because 53-72% of the cell perceptons wth ensung captures were made by Mxp. We cannot provde an exact value for the perceptve volumes of the A2 at dfferent food concentratons because they could not be adequately tracked at 125 frames s" 1 at anteror and lateral vews. An approxmate calculaton results n a 1.5-fold ncrease n perceptve volume of A2 from 1.0 to 0.1 mm 3 1"" 1. Snce ~65% of the cells were perceved by Mxp and 35% by A2, the overall ncrease n perceptve volume would be close to 3.5-fold. We assume that the dfference of 6-fold (VSC) mnus 3.5-fold = 2.5-fold n VSC-ncrease could be partly attrbuted to the fact that our longer (0.1 mm 3 1" 1 ) perceptve dstances were far greater underestmates due to two-dmensonal observatons than those at shorter (1.0 mm 3 I" 1 ) dstances. One mght ask what swmmng would add to perceptve volume. Adult females of E.pleatus swam at speeds between 0.5 and 1.0 mm s~ l when movng ther feedng appendages (G.-A.Paffenhofer, S.Rchman and J.R.Strckler, unpublshed observatons). Irrespectve of swmmng speed they passed smlar amounts of water by ther body whch meant that the feedng current volume hardly changed. Swmmng, however, mpled that ths copepod traveled through a large volume of water, ncreasng the probablty of encounterng advantageous food organsms and concentratons, n whch t could reman for extended perods. Lastly, we would lke to compare VSC obtaned from all captures/ngestons (Fgure 3) wth amounts of water passng n the feedng current wthn the appendage-swept area of the copepod. The maxmum VSC observed was 21.1 ml h" 1 female" 1 = 506 ml 24 h female (Fgure 3). Ths value represents 31% of the 1610 ml whch passed daly through the appendage area, and let us assume that even at very low food concentratons, E.pleatus was not perfect n nterceptng all T.wessflog cells. However, 1610 ml 24 h" 1 were not consdered an unrealstc value. The rato of VSC of E.pleatus CV feedng on Rhzosolena alata (20 \um cell wdth, 250 u-m length) at 0.5 mm 3 I" 1 (8 n-g C 944
Feedng behavor of calanod copepods I" 1 ) to that on T.wessflog (12 n-m cell dameter) at 0.1 mm 3 I" 1 (8 jtg C I" 1 ) was 3.4 (Paffenhofer and Van Sant, 1985, ther fgures 1 and 3). If ths rato was appled to females, then R.alata would be cleared at 1720 ml female" 1 24 h" 1 at 0.5 mm 3 I"" 1 and 20 C. Ths would mean that all cells passng through the appendage-swept area of the feedng current would be eaten. The excess feedng would be due to cells beng perceved at far greater dstances, and captured through realgnment of the copepod. The probablty that all R.alata n the feedng current would be perceved (at that low food concentraton) becomes obvous because R.alata () algns tself n the current, and because ts length wll be at least twce closely passed by an appendage whle beng dsplaced past the copepod, () should have a rather large elongated actve space (Andrews, 1983) whch ncreases the probablty of beng perceved, and () could be perceved hydrodynamcally by the mechanosensors of the Al (Vanderploeg etal., 1990). When feedng on R.alata at low, non-satatng food levels, E.pleatus should be near-perfect n percevng cells approachng ts appendage-swept area. In recent publcatons, the man emphass had been placed on feedng currents, appendage morphology and flow around them (e.g. Koehl, 1983,1984; Strckler, 1985). However, appendages are of lttle value for food capture f they do not perceve sgnals drectly from approachng food partcles, or ndrectly receve nformaton from the Al or any of the other appendages that a food partcle has been perceved (M2 whch can capture small partcles passvely). The functonng of the bologcal 'flter' of many manly herbvorous calanods s a functon of a feedng current, sensor arrays, and sensor specfcty and range of performance. Snce sensor arrays on the Al vary between speces (e.g. Barrentos Chacon, 1980), as well as swmmng and feedng behavor, we hypothesze that co-exstence of many copepods could be largely explaned by () each speces' sensory percepton ablty, n conjuncton wth () each partcular speces' response to the nput. Acknowledgements We would lke to dedcate ths paper to the memory of Dr Harold E.Edgerton. We would lke to thank Drs D.W.Menzel and H.A.Vanderploeg for revewng the manuscrpt, Dannah McCauley and Judy Leonard for typng t and Anna Boyette for the graphc work. Ths research was supported by NSF grants OCE85-00917 and OCE87-23174 (Bologcal Oceanography). References Alcaraz.M., Paffenhofer.G.-A. and Strckler,J.R. (1980) Catchng the algae: a frst account of vsual observatons on flter feedng calanods. In Kerfoot.W.C. (ed.), The Evoluton and Ecology of Zooplankton Communtes. Unversty Press of New England, Hanover, NH, pp. 241-248. Andrews,J.C. (1983) Deformaton of the actve space n the low Reynolds number feedng current of calanod copepods. Can. J. Fsh. Aquat. Sc., 40, 1293-1302. Ayuka.T. (1987) Dscrmnate feedng of the calanod copepod Acarta claus n mxtures of phytoplankton and nert partcles. Mar. Bol., 94, 579-587. Barrentos Chacon.Y. (1980) Ultrastructure of sensory unts of the frst antennae of calanod copepods. M.S.Tness, Unversty of Ottawa, Ontaro, Canada. Bowman,T.E. (1971) The dstrbuton of calanod copepods off the southeastern Unted States 945
G.-A.Pafenhofer and K.D.Lews between Cape Hatteras and Southern Florda. Smthson. Contrb. Zool. No. 96. Smthsonan Insttuton Press, Washngton, DC. Conover.W.J. (1980) Practcal Nonparametrc Statstcs. John Wley & Sons, New York. Corner.E.D.S., Head.R.N. and Klvngton.C.C. (1972) On the nutrton and metabolsm of zooplankton. VIII. The grazng of Bddulpha cells by Calanus helgolandcus. J. Mar. Bol. Assoc. U.K., 52, 847-861. Cowles.T.J., Olson,R.J. and Chsholm.S.W. (1989) Food selecton by copepods: dscrmnaton on the bass of food qualty. Mar. Bol., 100, 41-49. Cushng.D.H. (1968) Grazng by herbvorous copepods n the sea. /. Cons. Perm. Int. Explor. Mer., 32, 70-82. Fredman,M.M. and Strckler,J.R. (1975) Chemoreceptors and feedng n calanod copepods (Arthropoda: Crustacea). Proc. Nad. Acad. Sc. USA, 72, 4185-4188. Koehl.M.A.R. (1983) The morphology and performance of suspenson-feedng appendages. /. Theor. Bol., 105, 1-11. Koehl.M.A.R. (1984) Mechansms of partcle capture by copepods at low Reynolds numbers: possble modes of selectve feedng. In Meyers,D.G. and Strckler,J.R. (eds), Trophc Interactons Wthn Aquatc Ecosystems. AAAS Selected Symposum 85, Westvew Press, Inc., Boulder, CO, pp. 135-166. Leger-Vsser.M., Mtchell.J.G., Okubo,A. and Fuhrman.J.A. (1986) Mechanorecepton n calanod copepods: a mechansm for prey detecton. Mar. Bol., 90, 529-536. Lorenz.K.Z. (1981) The Foundatons of Ethology. Sprnger-Verlag, New York, Wen. Paffenhofer,G.-A. (1984) Calanod copepod feedng: grazng on small and large partcles. In Meyers.D.G. and Strckler,J.R. (eds), Trophc Interactons Wthn Aquatc Ecosystems. AAAS Selected Symposum 85, Westvew Press, Inc., Boulder CO, pp. 75-95. Paffenhofer,G.-A. (1988) Feedng rates and behavor of zooplankton. Bull. Mar. Sc., 43, 430-445. Paffenhofer,G.-A. and Lews,K.D. (1989) Feedng behavor of naupl of the genus Eucalanus (Copepoda, Calanoda). Mar. Ecol. Progr. Ser., 57, 129-136. Paffenhofer,G.-A. and Van Sant.K.B. (1985) The feedng response of a marne planktonc copepod to quantty and qualty of partcles. Mar. Ecol. Progr. Ser., 27, 55-65. Paffenhofer,G.-A., Strckler.J.R. and Alcaraz,M. (1982) Suspenson-feedng by herbvorous calanod copepods: a cnematographc study. Mar. Bol., 67, 193-199. Prce.H.J. (1988) Feedng mechansms n marne and freshwater zooplankton. Bull. Mar. Sc., 43, 327-343. Prce.H.J. and Paffenhofer,G.-A. (1986) Effects of concentraton on the feedng of a marne copepod n algal monocultures and mxtures. /. Plankton Res., 8, 119-128. Prce.H.J., Paffenhofer,G.-A. and Strckler.J.R. (1983) Modes of cell capture n calanod copepods. Lmnol. Oceanogr., 28, 116-123. Strckler,J.R. (1982) Calanod copepods, feedng currents, and the role of gravty. Scence, 218, 158-160. Strckler.J.R. (1984) Stcky water: a selectve force n copepod evoluton. In Meyers.D.G. and Strckler.J.R. (eds), Trophc Interactons Wthn Aquatc Ecosystems. AAAS Selected Symposum 85, Westvew Press, Boulder, CO, pp. 187-239. Strckler.J.R. (1985) Feedng currents n calanod copepods: two new hypotheses. In Laverack.M.S. (ed.), Physologcal Adaptatons of Marne Anmals. Symp. Soc. Exp. Bol., 89, 459-485. Strckler,J.R. and Bal.A.K. (1973) Setae of the frst antennae of the copepod Cyclops scutfer (Sars): ther structure and mportance. Proc. Natl. Acad. Sc. USA, 70, 2656-2659. Vanderploeg.H.A. and Paffenh6fer,G.-A. (1985) Modes of algal capture by the fresh-water copepod Daptomus scls and ther relaton to food-sze selecton. Lmnol. Oceanogr., 30, 871-885. Vanderploeg.H.A., Paffenhofer,G.-A. and Lebg,J.R. (1990) Concentraton-varable nteractons between calanod copepods and partcles of dfferent food qualty: observatons and hypotheses. In Hughes.R.N. (ed.), Behavoral Mechansms of Food Selecton. NATO ASI-Seres, A-Lfe Scences, Sprnger-Verlag, Berln, Hedelberg, New York, pp. 595-613. Receved on November 6, 1989; accepted on Aprl 16, 1990 946