Predation by estuarine zooplankton on tintinnid ciliates

Estuarine,

Coastal and Shelf Science (1983) 16, 27-36

Predation by Estuarine Zooplankton on Tintinnid Ciliates”

J. Roy Robertson University

of

Georgia Marine

Received 4 February

I

Keywords: predation;

Institute,

Sapelo Island, Georgia

U.S.A.

3I3.27,

982

zooplankton;

Copepod;

Ciliata;

Sapelo

Island

Laboratory experiments were conducted to determine the feeding performances of Uca zoeae and the estuarine copepods Acartia tonsa and Tortanus setacaudatus when these zooplankton preyed upon the co-occurring tintinnids Favella panamensis (length 265 pm) and Tintinnopsis tubulosa (length 148 pm). Predation by Favella on Tinlinnopsis was also studied. Over the range of experimental prey densities used, Acartia ingestedTint& nopsis at rates linearly related to prey density. Favella was ingested by Aractia at higher rates than was Tintinnopsis. Tortanus ingested Favella more readily than did Acartia, but Tortanus did not ingest Tintinnopsis. Uca ingested both Tintinnopsis and Favella while Tintinnopsis was also ingested by the larger tintinnid Favella. Comparisons of Acartia predation on tintinnids with published data on ingestion of nauplii and phytoplankton showed that when the phytoplankton are dominated by small (diameters IO pm are present in significant concentrations, tintinnids merely supplement algae in the diet of Acariia. Generally, tintinnids are more important food items for Acartia than are comparably sized nauplii. Only at concentrations exceeding IO* cop. m-s can Acartia depress tintinnid population growth.

Introduction Marine, loricate ciliates belonging to the suborder Tintinnida graze most effectively on particles in the nanoplankton size-range (Spittler, 1973; Blackburn, 1974; Heinbokel, 1978a,b; Rassoulzadegan& Etienne, 1981). If these protozoans are effectively preyed upon by metazoanzooplankton they could play an important role in the pelagicfood web dynamics of estuarine and coastalwaters where nanoplankton can seasonallydominate phytoplankton productivity and biomass(McCarthy el al., 1974; Van Valkenburg & Flemer, 1974; Durbin et al., 1975; Durbin & Durbin, 1981). Berk et al. (1977) demonstratedthat aloricate ciliates having linear dimensionsbetween 8.88 and 17.3pm were acceptableasfood to the estuarine copepod Eurytemora aflinis. However, tintinnid loricae typically have linear dimensions ranging from 20 to 200 pm. This fact has led Hargraves (1981) to suggestthat membersof the common estuarine copepod genus,Acartia, may be too small to prey effectively on most tintinnids. This view does not appear to be tenable, since it is known that A. tonsa can capture and ingest crustaceannauplii having linear dimensionsgreater than IOOpm (Anraku & Omori, 1963; Lonsdale et al., 1979). “Contribution

number

465 from

the University

of Georgia

Marine

Institute.

27 0272-7~1~/83/01002~+10

$03.00/O

Q

1983

Academic

Press Inc.

(London)

Limited

28

J. R. Robertson

The purpose of the present study was to provide a preliminary evaluation of the role of estuarine tintinnids as potential prey for some common estuarine metazoan zooplankton. In addition, experiments were conducted to determine if the large tintinnid Fuvella panamends would ingest smallersympatric tintinnids. The impetus for theseexperimentswasthe observation that preserved F. panamensis sometimescontained smaller tintinnids within their loricae. Methods The metazoanpredators usedin this study were adult femalesof the copepodspeciesAcartiu setacaudutus (Williams) along with decapodzoea identified asbelonging to the genus Uca (Kurata, 1970). Measurementsmade at IOO x under a stereomicroscopeof the tip to tip distancebetween the decapod larvae’s rostra1and dorsal spines(650-720 pm) indicated that the larvae were most likely stage I zoea (Kurata, 1970). The averagedry weight of adult female Acartia tcnra collected during the courseof these experiments was determined using methods similar to those used by Miller et al. (1977). After being rinsed in distilled water on a filter, 350 freshly collected animalswere transferred with sablebrushesto tared foil cups, dried at 60 “C to constant weight, all weighingsbeing carried out on an M5 Mettler balance.The resulting meanweight of 4.97 Pg agreeswell with the dry weight of adult female A. tonsa taken in the ChesapeakeBay at temperatures’similar to those in the Duplin River during the course of this study (Miller et al., 1977). The carbon content of adult female A. tonsa was estimated by applying a carbon : dry weight ratio of 0.47 (Durbin & Durbin, 1978) to the above-determined dry weight. The respiration rate of A. tonsa at prevailing summer temperatures was estimated by extrapoIating the summer 0, consumption curve in Anraku (1964) to 27 “C. Oxygen consumption was converted to joules using the factors 4.825 x IO-~ cal0, (Phillipson, 1970)and 4.184J Cal-l. The prey tintinnids were Tintinnopsis tubulosa and Favella panamensis. Tintinnid protoplast volumes were estimated from specimenspreserved in Karnovsky’s fixative (Gold, 1976) by assumingthat the shape of the fixed protoplast was spherical. The protoplast diametersof 50 preserved individuals of each prey specieswere measuredat 200 x using an inverted microscopeand the diameterswere converted to the equivalent spherical volume. The mean protoplast volumes were 5.61 x 10~ pm3 for Tintinnopsis tubulosa and 5.43 x 10~ pm3for Fuvellupanamensis. These volumes were converted to dry weight and energy content using the factors 0-17 pg pm3 (Laybourn & Finlay, 1976) and 20.0 J (mg dry weight)-i (Laybourn & Stewart, 1975). Carbon content was assumedto be 40% of dry weight. The respiration rate of Fuvella at 27 “C was estimatedfrom the relationship of oxygen consumption to dry weight in Laybourn & Finlay (1976) and corrected for temperature by applying a Ql,, of 2.0. Loricae linear dimensions were determined concurrently with protoplast diameters. Loricae volumes were estimated from the linear dimensionsby assumingthe loricae were composedof conjoined regular solids.The meanvaluesfor the maximum widths and lengths of the measured loricae were 47.5 x 147.5 pm for T. tubulosa and 82.5 X 265 Pm for F. panamensis. The respective mean volumes were 140.41 and 1575.07 x xo3 pm3. Experimental organismswere collected during July and August 1981 in the Duplin River, a tidal lagoon located on the western margin of SapeloIsland, Georgia. Copepodsand zoeae were collected with a plankton net hung from a dock during ebbing or flooding tide. Upon return to the laboratory the predators were sorted to species(or genuswhere appropriate) and placed in 4-l glass beakers containing 3.5 1 of freshly collected Duplin River water tonsa and Tortanus

Zooplankton

predation

on tintinnid

ciliates

29

screened through zo-pm mesh netting. Cultures were maintained at 27 “C under low continuous light levels. These culture conditions reflect ambient conditions in the Duplin River during the time the experiments were conducted. Culture densities never exceeded 25 organisms 1-l. Acartiu cultures were augmented with the dinoflagellate Prorocentrum micans while Tortanus and zoeae cultures were augmentedwith plankton concentrated by successivelyfiltering Duplin River water through 200- and r25-pm meshnetting. Predators were maintained in the laboratory for no lessthan I but no more than 3 days before being used in experiments. Tintinnids were collected by pouring water pumped into a carboy through zo-pm mesh netting and rinsing the concentrated sample into a soo-ml plastic bottle. Damage to the tintinnids during collection was reduced by using a diaphragm-type bilge pump instead of one employing an impellor. In the laboratory, tintinnids were sorted to specieswith a braking mouth micropipette having a finely drawn tip (Salt, 1964). The ciliates were maintained in 25o-ml flasks containing zo-pm screenedDuplin River water. Culture conditions for prey were the sameasthoseexperienced by their potential predators. Tintinnopsiscultures were augmented with the flagellate Chroomonassp. and Favella cultures were augmented with Prorocentrummicans(Ehrenberg). The liquid medium used in all experiments was freshly collected Duplin River water screenedthrough zo-pm mesh netting. The use of particle-free water as an experimental medium resulted in excessiveprey mortality in control populations. Copepod and zoeae experiments were conducted in 1-1jars containing 500 ml of screenedDuplin water. Experiments pitting Favella against Tintinnopsiswere conducted in 25 x ISOmm screw-cap tubes containing 20 ml of screenedDuplin water, Predators were carefully transferred with Pasteur pipettes into experimental chambers from Petri dishescontaining water decantedfrom culture beakers.This technique promoted 100% survival of predators in all experiments. The initial prey densitieswere constructed by enumerating tintinnids as they were transferred with a braking micropipette to so-ml beakerscontaining smallvolumes of medium from the experimental chambers.Experiments were begun by pouring the final contents of these beakersinto the experimental chambers containing medium and predators. Four replicates of experimental and predator free control vesselswere incubated in the dark at 27 “C. Experimental prey densitiesranged from 250 to 2000 prey l-l, while samplesof tintinnids in the Duplin River revealed densities ranging from 250 to IOOO tintinnids 1-l. Experiments were terminated by pouring the incubation water into plastic bottles containing mercuric chloride (Pace & Orcutt, 1981). The preserved sampleswere concentrated by sedimentation and aspiration of the overlaying supernatant. The resulting concentrates were examined in their entirety with a stereomicroscopeto enumeratepredators and prey loricae. The latter were classifiedaseither thosedevoid of or containing preservedprotoplasts. Volumes swept clear and ingestion rates were estimatedfor metazoan predators by applying the equations of Frost (1972) to appropriate control and experimental concentrations of the preserved loricae that contained protoplasts. BecauseFavella reproduced during the incubation periods, the volumes swept clear by this predator were estimatedby substituting average predator density into Frost’s equations(Heinbokel, 1978~). Experiments were also conducted to determine if the presenceof predators would cause the growth constants of experimental tintinnids to be different from those of control prey. Screened Duplin River water was incubated with the appropriate predators in the absence of prey under conditions identical with those used in several predator-prey experiments. At the end of the incubation period predators were removed by pouring the water through

J. R. Robertson

30

rzg-pm mesh netting. The conditioned water was then reincubated with tintinnids under conditions identical with those used in appropriate control incubations. Incubations were terminated and tintinnids enumerated using methods described above. Tintinnid growth constants were calculated using Frost’s (1972) equation and comparedwith growth constants of tintinnids incubated under identical conditions in unconditioned water drawn from the samebatch used for the conditioning experiments. Results and discussion Table I showsthat the growth constants of tintinnids incubated in ao-pm screenedDuplin River water preconditioned with predators did not differ significantly from the growth constants of tintinnids incubated in unconditioned water. Thus, differences between prey growth constants in predator containing incubations and in controls without predators reflect the effects of predation unconfounded by competition between predators and prey. Over the range of prey densities used, the ingestion rate of Acartiu tonsa feeding on TinGznopsistubulosawas linearly related to prey density (Figure I). This relationship implies that the importance of tintinnids in the diets of A. tonsamay increaseat tintinnid densities higher than thoseusedin the presentstudy. Although present estimatesof tintinnid densities in the Duplin River never exceeded2 x 10~ organismsI- l, the samplingregime usedwasnot designedto determine the potential patchinessof tintinnid distribution. In view of the fact that Heinbokel & Beers (1979) and Hargraves (1981) observed tintinnid densitiesthat at times exceeded10~ organisms1-l it is possiblethat A. tonsufeed opportunistically on dense transient patchesof tintinnids. TABLE water, by the where

Predator __Favella panamensis Acartia

tonsa

Tortanus setacaudatus Uca sp. zoea

Prey Tintinnopsis tubulosa Tintinnopsis tubulosa Favella panamensis Favella panamensis Favella panamensis Tintinnopsis tubulosa

I. Comparisons of growth constants of tintinnids incubated in unconditioned k,, with growth constants of tintinnids incubated in water preconditioned presence of predators, ke. Means with 95 yO confidence limits in parentheses applicable

Incubation period (h)

Initial prey density (prey l- ‘)

Initial predator density (pred. l- ‘)

8 8 24

2000

500

2000 2000

1000 500

8

1000

8

(h’i) 0.046 0.055 0.039

(0.018) (0.0081) (0.014)

0’043 0.060 0.032

(0.015) (0.017) (0.022)

40

0.065

(0.016)

0’073

(0.0066)

1000

40

0.107

(0.01

0.116

(0.016)

8

1000

20

0’094

(0.025)

0.088

(0.015)

8

1000

20

0.115

(0.012)

0.121

(0.029)

8

1000

20

0.041

(0.024)

0.037

(0.006)

I)

Figure I alsoshowsthat Acurtiu tonsuadult femalesfed equally well or better on the larger tintinnid Fuvellu punamensis.These results vitiate the suggestionby Hargraves (1981) that A. tonsuis too small to ingest tintinnids. To date F. punamensis is the largest particle known to be ingested by A. tonsu(seeTable 3 later). Since no broken loricae of either T. tubulosu or F. pancmensiswere found in preserved samplesfrom experimental treatments, it is likely

Zooplankton

predation

Initial

prey

on tintinnid

concentmtion

ciliates

(IO’

pr*y

I-9

Figure I. Ingestion rates of zooplankton feeding rates observed when prey was Favellapanamemis. when prey was Z’intinnopsis tubulosa. Symbols

on tintinnids. Closed symbols

Open symbols are are rates observed

for predators are: circles=Acartia setacaudatus, squares=Uca sp. Vertical bars are 9.5% about means, Regression line is for Acartia feeding on Tintinnopsis,

tonsa, triangles=?brtanus confidence w.9662.

limits Crosses

are the rates

at which

nauplii

were

ingested

by Acartia

tonsa

(Lonsdale et al., 1977).

that theselarge living particleswere ingestedwhole. This supposition is further substantiated by the observation that someof the copepod feces found in experimental treatments contained intact loricae. Tortanus setacaudatusfemales effectively ingested Favella panamensis,but ingested no Tintinnopsis tubulosa(Figure I). This result is consistent with studies showing that the congener Tortanus discaudatusfeeds strictly by predation on crustaceanimmature forms (Anraku & Gmori, 1963; Ambler & Frost, 1974). The difference in predation intensity on the two tintinnid speciesmay not be strictly a function of particle size. Visual observations indicated that F. panamensisswims faster than T. tuberlosa.BecauseT. setacaudatusis an ambush predator, the difference in predation rates may reflect lower rates of predator encounter with T. tubulosa than with F. panamensisalong with less water disturbance produced by swimming T. tubuha (Strickler, 1975; Gerritsen & Strickler, 1977). Uca stage I zoea fed as effectively as Acartia tonsa on Tintinnopsisstubulosabut less effectively on Favella panamensis.Preliminary studies have shown Duplin River zoeal densities in the summer to be less than half those of A. tonsa (Robertson, unpublished), implying that theselarvae may not be very important predators of tintinnids. The data of Table z verify the hypothesis that Favella panamensiscan ingest smaller tintinnids. Clearancerates of F. panamensis feeding on T. tubulosa (Table 2) are one to two orders of magnitude larger than those found by Heinbokel (1978a) for smaller tintinnids feeding on microflagellates. This difference may occur becausethe larger Favella has a higher swimming or capture rate than smallertintinnids do. Heinbokel (1978a) has also shown that herbivorous tintinnids can ingest up to 2407~ of their body weight in microflagellatesper day. Rassoulzadegan& Etienne (1981) observed a value of 43% body weight ingestedper day by the particulate feeding tintinnid Stennosomella ventricosa. Both of theseingestion ratesare much higher than those reported in Table 2

J. R. Robertson

32

for F. panamensis, suggestingthat tintinnids are a supplementary food source to Favella’s primarily herbivorous diet. At prey densitiesof z x 10~ organisms1-l Favella can obtain a large fraction of its respiratory lossesby eating smaller tintinnids (Table 2). z. Feeding

TABLE

by

Favella panamensis on Tintinnopsis tubulosa. Initial

concentrationin all experiments2.0x limits in parentheses whereapplicable Predator density (10~pred. 1-l) 0.500 0.500 1’000

Incubation time 04 8 24 8

Predator clearancerate (~1pred.-’ h-l) 52’13 129.86 63.63

(7’70) (17.48) (17.69)

10~

prey

prey 1-l. Meansk95°/0 confidence Ingestionrate (% dry body weightday- ‘) 27’27 24.80 22.81

Ingestionrate (% respired energyday-‘) 101.27

92.06 84.70

Further discussionwill be restricted to feeding by Acartia tonsa, becauseit is the dominant metazoan zooplankter in the estuarine waters surrounding Sapelo Island (Robertson, unpublished). Table 3 compares the feeding performances of A. tonsa feeding on phytoplankton, copepod nauplii and tintinnids. All rates obtained from experiments conducted below 27 “C have been corrected to 27 “C using a Qlo of 2.0. Q, ovaluesobtained in the range 20-30 “C by extrapolating the summerdata in Anraku (1964) are 2.2 for A. tonsa 0, consumption and 1.22-1.83 for A. tonsa clearancerates. The latter values imply that a Q1,,of 2.0 will slightly over estimateactual clearanceand ingestion rates obtained at 27 “C. Experimental feeding concentrations given in Table 3 for Phaeodactylum and Dunalliella were taken directly from the figures in Reeve& Walter (1977). Pseudoisochrysis densitieswere originally given in parts IO-’ by volume (Lonsdale et al., 1979). These valueswere converted to chlorophyll a concentrations by converting parts IO-~ to cell density using the cell volume in Table 3 and then applying the carbon cell-l relationship in Strathman (1967). Carbon concentration was converted to chlorophyll a concentration using a carbon : chlorophyll a ratio of 35 : I (Reeve & Walter, 1977). Experimental cell concentrations of Thallasiosivus were calculated from Anraku’s (1964) data as the quotient of ingestion rate divided by clearance rate (Frost, 1972). This value was converted to chlorophyll a concentration using the carbon cell-l data from Mullin et al. (1966) along with the carbon : chlorophyll a ratio given above. Clearance rates of Acartia feeding on tintinnids were much higher than those of Acartia feeding on small phytoplankton, but clearance rates on the larger diatom Thallasiosirus weissfogii (jkviatilis) were comparablewith those observed in the present study (Table 3). These results are consistent with the observation that large particles are more effectively captured by copepodsthan are small particles (Frost, 1972, 1977).The fact that T.JIuviatilis is none the lessmuch smaller than the tintinnids used in the present experiments suggests that Acartia capture efficiencieshave an upper boundary or Acartia experience difficulty in handling tintinnids. Clearancerates calculated from the data in Lonsdale et al. (1977) were lower for Acartia preying on nauplii than for Acartia preying on tintinnids (Table 3). Since these differences are also reflected in ingestion rates (Figure I), it is likely that differences in prey escape behavior contribute to the difference in capture efficiency (Lonsdale et al., 1977; Paffenhofer & Knowles, 1980). Personalobservationsare that tintinnids are quite easyto capture with a braking micropipette, while it is virtually impossibleto obtain nauplii this way becausethey actively avoid the mouth of the pipette.

Source

colcntvo

199)

“Reeve & Walter length-volume data in Parson data in Mullin Durhin, 1978)

27 94.94-288.91 106.58

278 278 250-2000 250-IO00

204.8 483.5 140’4 IS75’0

36.97 I 64.90

0.96-8.470

O’SI4-I’379

0.072 0.670

1.024

0.408-3.604

0.06S-o~S86

0.031 0.285

0.436

0’141 0.332

0.096

12.889

52-s

278

30.29’

0~000-6~071

o~ooo-r4~266k

rate ;l(body

0-305-1~099 0.862-4.143

Ingestion C W’

experiments

2.027~9'736J

0.717-2.582‘

Cg

non-tintinnid

94’93

278

232’9

I 162.1

from

Ingestion rate bg C day-‘)

Rates

0'220

‘)

sources.

0.226’” 0.518

20.35~ 9’09

I4S.00

0.08-4.81 4.83-10.86 -

278 278

478.6’ 1098.0

5.98

2.2s’

22.5

20

10~~0-135~84

0.065 b

0.30’

food

Volume swept clear (ml cop.- 1 day-

on different

(1977); bLonsdale et al. (1974); ‘Anraku (1964); "This study; ‘Parson et al. ( t 96 I) ; ‘Mullin et al. (I 966) ; gCalculated from relationship for A. tonsa in Miller et al. (1977); ‘Calculated from average ingestion rates in Lonsdale et al. (1979); ‘Based on et al. (1961); ‘Based on data in Mullin et al. (1966); ‘Based on relationship in Strathman (1967); ‘Calculated by applying “Estimated by applying carbon: dry wt. ratio of 0.47 (Durbin & et al. (1966) to daily cell ingestion rate in Anraku (1964); to dry wt. calculated from length-dry wt. relationship in Miller et al. (1977).

(Bowman) (I-III ; 83) (IV-VI; 136) Tintinnidsd (length in pm) Tintinnopsis tubulosa (Levander) (I 48) Favella ponamensis (Kofoid & Campbell) (265)

Oithono

(IV-VI;

tonsa feeding

Food concentration (phytoplankton in pgchl.al-’ zooplankton in organisms l- ‘)

of Acartia

10~0~8yoo Io'oo-100'00

Prey volume (10~ pm3)

performances

0.12=

2.0

21 21 20

Temperature PC)

3. Comparisons of feeding to 27 “C using QtO of

Phytoplankton Phaeoabctylum tricornutum (Boh1i.n)” Dunalliello tertiolecta (Butcher)“ Pseuabbchrysis sp. b Thallasiosirus WeissfIogii (Grun.) (G. Fryx. et Hasle) (formerly T. j?uuiatilis) Copepod naupliib (stage; length in pm) Acartiu tonsu (Dana) (I-III; 135) (Iv-v; 193) Scottolada canadensis (Willey) (I-III; 112)

Food

TABLE

corrected

34

J. R. Robertson

When the small diatom Phaeodactylumand the microflagellatesDunalliella and Pseudoisochrysiswere present at densities eliciting maximum ingestion rates, Acartia obtained more ingestedcarbon grazing on thesefood sourcesthan they did when preying on the small tintinnid, Tintinnopsistubulosa(Table 3). At prey densitiesof 10~ tintinnids 1-r predation on the large tintinnid Favella panamensis did result in carbon ingestion rates comparableto those observed for Acartia feeding on the smaller algae.Although phytoplankton in some shallow water marine systemsmay approach the equivalent chlorophyll a concentrations neededto induce the maximum ingestion rates given in Table 3 (Durbin & Durbin, 1981), the summer chlorophyll a concentrations in the Duplin River have not been observed to exceed IO pg ch1.a 1-r (Sherr, Whitney & Pomeroy, unpubhshed).Table 3 showsthat at this equivalent concentration of small phytoplankton, small tintinnids at relatively high concentrations and large tintinnids at lower concentrations can be important sourcesof carbon. Larger algae,such as the diatom Thallasiosirusweissfogii(juviatilis), appearto be superior to tintinnids as a food source even when present in equivalent concentrations of below IO pg chl. a 1-l (Table 3). At prey densitiesnear 250 organisms1-l most of the nauplii listed in Table 3 provided more carbon to Acartia than did T. tubulosa,while at this prey density Favella wassuperior to most nauplii asa carbon source(Table 3). Table 3 alsoshowsthat the relative importance of nauplii and Tintinnopsisas carbon sourcesis reversed when the latter prey are present in densitiesof 2 x 10~ prey l- l. Becausepeak estuarinenaupliar densitiesare typically in the range 50-100 organisms1-i (Heinle, 1966; Durbin & Durbin, 1981), the ingestion rates for naupliar prey listed in Table 3 may be higher than thoseoccurring in natural estuarinewaters (Lonsdale et al., 1977).This postulateimplies that at densitiesexceeding250 organismsl-l, tintinnids will be more important than nauplii ascomponentsof Acartia diets. In general, the data in Table 3 suggestthat small tintinnids will be relatively important componentsof Acartia’s diet only if tintinnid densitiesequal or exceed 10~ organisms1-l and the phytoplankton are dominated by small species(equivalent spherical diameters < IO pm), which are present in low concentrations. At a density of 2 x 10~organismsI-‘, Tintinnopsiscan provide Acartia with 68% of its daify respiratory losses.Large tintinnids can have dietary importance when present at densitiesequal to or exceeding 10~ organisms1-l as long as small speciesdominate the phytoplankton. At the experimental prey densitiesused in the presentstudy Favella can supply Acartia with 48-422% of its basicmetabolic requirements. When large algae(equivalent spherical diameters > IO pm) are present in significant concentrations,tintinnids and nauplii will only be supplementary to phytoplankton in the diet of Acartia. The impact of Acartia on tintinnid populations can be estimatedusing the relationships F=g(N/V)-’ and r=h-g; F is clearancerate; N/V is predator density; R is prey growth constant; g is grazing coefficient; and Y is instantaneousrate of prey increasein the presence of predators (Frost, 1972). When g> K predation pressure is sufficient to depressprey population growth. The maximum K values reported to date for small tintinnids are near 0.05 h-l (Table I) (Heinbokel, 1978a).Substituting a g value of 0.05 h-l and an F value of 4.5 ml cop.-’ h-l (the mean clearance rate of Acartia feeding on Tintinnopsis) into the equation N/V=g/F gives a critical Acartia concentration of I-I I x 10~ cop. me3; copepod concentrations above this value will causetintinnid population densities to decline. Since this critical density of adult Acartia is rarely achieved in nature (Heinle, 1966; Durbin & Durbin, 1981) and since maximum tintinnid growth constants have been observed at phytoplankton carbon concentrations equivalent to lessthan 3.0 ug chl. a 1-l (Heinbokel, I978a), it seemsthat during periods of peak estuarine productivity Acartia would have

Zooplankton

predation

on tintinnid

ciliates

35

minimal impact on tintinnid populations. The validity of this conclusion requires further investigation into the feeding performance of Acartiu copepedid stages preying on tintinnids because in growing populations these immature stages generally have higher population densities than do adults (Heinle, 1966; Durbin & Durbin, 1981). Tintinnids can be an important numerical component of estuarine microzooplankton (Hargraves, 1981). Along with other small zooplankton such as rotifers and invertebrate larvae, these ciliates can exert significant grazing pressureon the small phytoplankton not effectively grazed by larger zooplankton (Capriulo & Carpenter, 1980). The present study indicates that under certain conditions tintinnids can alsobe important asa food sourcefor the abundant estuarine copepod A. tonsa. However, only rarely will A. tonsaexert enough predation pressureto significantly depresstintinnid population densities.

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