Yellow water in La Jolla Bay, California, July 1980. II. suppression of zooplankton grazing

J. E.vp. Mar. Biol. Ecol., 1982, Vol. 63, pp. 81-91

Elsevier Biomedical Press

YELLOW

WATER IN LA JOLLA BAY, CALIFORNIA,

II. SUPPRESSION

OF ZOOPLANKTON

JULY 1980.

GRAZING

MARK E. HUNTLEY institute of Marine Resources, Scripps institution of Oceanography. A-018, La Jolla. CA 92093, U.S.A. Abstract: Experiments were conducted to determine how much grazing pressure adult females of Calanus pucifcus Brodsky, a dominant planktonic herbivore in local waters, exerted upon a bloom of the dinoflagellate, Gyrnn~d~~urn~avurn Kofoid C Swezy, in the waters off La Jolla in July, 1980. One set of females

was presented with water collected from the chlorophyll maximum, and a second set was presented with Thalassiosirir wei.@ogii Grunow, which is readily ingested by Cukzntts. Filtration rates upon the diatom were significantly higher (8.4 ml copepod- I h-‘) than upon the dinoflagellate (0.30 ml copepod- ’ h I). Calanus did not exert a significant grazing pressure upon the dinoflagellate bloom. Gut content analyses support this conclusion. The persistence of the bloom was probably due, in part, to the avoidance of Gymnodiniumflavum by copepod grazers and to the consequent lack of grazing pressure.

Two types of selective feeding behavior have been identified in filter-feeding copepods: “passive” and “active” selection (Donaghay, 1980). Passive selection explains obse~ations that copepods will select the largest particles in a mixture (e.g. Harvey, 1937; Richman & Rogers, 1969; Runge, 1980). This phenomenon, also referred to as size-selection, is a purely passive property of the morphology of the filtering mesh (Boyd, 1976), and does not require a behavioral response by the copepod (Frost, 1977). If the characteristics of the filtering mesh are known, then passive selection can be defined mathematically and as such can be included in models of copepod feeding behavior (e.g. Steele & Frost, 1977; Conover & Huntley, 1980). Active selection has not yet proven amenable to quantification, and indeed the evidence for its existence is debatable. It is best defined as “any deviation of the observed filtering response from that expected based on the physical properties of the filter” (Donaghay, 1980). Several experiments previously considered as good evidence for active selection ~Richman et al., 1977; Donaghay & Small, 1979) have recentfy been called into question because of critical evaluations of their methodologies (Harbison & McAlister, 1980; Gifford et al., 198 1). Other studies have demonstrated that copepods have the ability to perform active selection, but the particle systems used have often been artificial (e.g. Poulet dc Marsot, 1978). Consequently, we know very little about what types of naturally occurring particles induce copepods to exercise active selection. The bloom of Gyrnn~dinj~rn~a~~rn Kofoid & Swezy which occurred in the waters off La Jolla, California in late July, 1980 (Cullen et al., 1982) provided an excellent 0022-0981/82/0000-0000/$02.75 Q 1982 Elsevier Biomedical Press

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MARKE.HUNTLEY

opportunity to examine the response of filter-feeding copepods to a phytoplankter which might reasonabfy be expected to induce active selection behavior (cf. White. 1979). I report here on the results of grazing experiments performed with Cahnla.s pacificus Brodsky in natural suspensions of Gymnodiniumflavum, and on the condition of animals taken from the field during the dinollagellate bloom.

MATERIAL AND METHODS GRAZING EXPERIMENTS

Zooplankton for the grazing experiments were collected from a depth of 20 m at a station % 2 km due west of Scripps Institution of Oceanography in La Jolla, California. The animals were collected with a 333~pm mesh net at midnight, 30 July 1980 and were transferred to a cooler tontine sea water, also from 20 m. Within 2 h adult females of Calanus ~ae~~cus were sorted and placed in experimental grazing containers in the laboratory. Experimental animals were presented either with a suspension of the natural Gymnod~nium~av~m bloom, or with a suspension of T~aias.~~osiraweiss~~g~iGrunow . The I: ~e~ss~ogi~were obtained from an exponential phase culture and were resuspended in sea water obtained several weeks prior to the G.~m~odi~~urn~avu~nbioom. The sea water used for resuspension was filtered through GF/C glass fiber film ters immediately after collection and once again immediately prior to its use in the grazing experiments. The Thalassiosira weissfrgii concentration was adjusted to t 2000 cells * rni- ’ (z 190 gg C . 1. ‘) for the grazing experiments. The natural suspension of Gymrwdiniumf2avum was collected from a depth of 5 m using a peristaltic pump at the same time and station as the zooplankton. The dinoflagellates at this depth were within the zone of greatest abundance (2-7 m), but were 1 m below the measured maximum at 4 m. Fig. 1 shows the size-frequency distribution of particulate matter, as measured with a model TA-II Coulter Counter, at 10 depths between the surface and a depth of 20 m. At 5 m C. fIavum comprised > 909;, of the particulate matter by volume, and 907; of the total cell abundance, as revealed by microscopic examination of preserved samples (Cullen et&., 1982). The conccn~ tration of G.,flavum in the experimental suspension was % 1000 cells ’ ml ( x 200 pg C ’ I- ‘). G.flavum has a maximum dimension of z 35 pm, and is thus larger than Tha~ass~osirawe~s~~~ngi~, which has a m~imum dimension of z 17 pm. Each grazing experiment was conducted in a 9%mi glass jar coning four adult female copepods. A total of nine repIicate grazing experiments were conducted for each treatment, and three additional jars served as controls (which did not contain zooplankton) for each treatment. The copepods were permitted to feed for NS24 h. Cell concentrations in the control suspensions were measured at the begin&g of the experiment using the TA-II Coulter Counter. At the end of the experiment cell concentrations were measured in the same manner in both the control and the experimental

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vessels. Using these measurements, ingestion and filtration rates were computed using the equations of Frost (1972).

PARTICLE VOLUME

(pm31 Fig. I. Size-frequency

distribution of particulate matter at 10 depths between the surface and 20 m at midnight, July 30.

MARK

x4

FIELD

E. HUNTLEY

MEASUREMENTS

Zooplankton were collected from depths of 0, 5, and 20 m from the same station as other samples. The animals were preserved in buffered formalin. Within 2 wk after collection 50 adult female Calunuspacificus were removed from each sample and placed in 80% lactic acid, which reduces the opacity of the exoskeleton and permits the gut contents to be examined easily (Hayward, 1978). After 20 min had passed to allow for the clearing of the integument, each of the animals was examined and the proportion of the gut occupied by food materials was estimated. RESULTS Females of Calanus paciJicus ftltered Thalassiosira weissfrog at much higher rates than they filtered the natural suspension of the Gymnodiniumflavum bloom. Figs. 2 and 3 show the results of the grazing experiment with Thalbssiosira weissflogii.Filtration rate tended to increase with cell size, reaching a maximum of 8.4 ml . copepod ’ h ’ on the largest Thalassiosira cells. The magnitude of the ingestion rate reflected the ceil size-frequency distribution, reaching a maximum of % 5300 cells . copepod ’ ’ h ’ ai the peak of the cell distribution (Fig. 3).

1'

i’\ I

‘\\

I

:SD I

-I; I

L

---

!.5

4.0

i

Fig. 2. Filtration rates of Culanuspacijcus females in the suspension of Thalassiosira we&jZogiias a function of particle volume: the filtration rates (ml copepod-’ ’ h-‘, means (k 1 SD) of nine replicates) are shown as solid lines: dashed lines represent partide concentration (cells ml-‘).

Figs. 4 and 5 show the filtration and ingestion rates, respectively, of Calanuspacificus feeding on the natural suspension of Gymnodiniumfivum. The maximum fhration rate was 2.3 ml . copepod-’ . h-“, and this was on natural particles which were slightly smaller than G.flavum. Within the size range of particles dominated by G. ji’avum the

MEAN

$8_1

CELL

INGESTION

-I)

i3 0 8 8 kellsvnl-9

(cellscopepod-‘ah

CONCENTRATION

RATE “r

MEAN

1

CELL

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I

i3 0 8 8 (cellsml-‘1

(mbcopepod-l-h y a

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RATE 7

CONCENTRATION

FILTRATION “: p

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--rc 8

I

I

RATE

3

CELL CONCENTRATION

i

(cells-ml-‘:

icelIsqcopepod-‘.h

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gp<;,:

INGESTION

-’

X6

MARK E. HUNTLEY

filtration rate was 0.3 ml . copepod ’ . h--l. The ingestion rates, although barely posrtive, were < 50 cells copepod-- ’ h I for all cell sizes. Fig. 6 shows the percent gut contents of 50 female Cafanus pacr$c~~ caught at 0. i. and 20 m as a function of the animal number, beginning with the fullest of individuais

ANIMAL NUMBER

50

Fig. 6. Gut contents (‘?, gut Fullness) for 50 Calanus puc&us females at 0, 5, and 20 m iks a fun&ion (ii animal number, beginning with the fullest animal and declining to the emptiest: mean gut fullness :tt eat’; depth is also shown.

and declining to the emptiest. At 20 m, below the G~~~~di~ium~a~~ biomass peak, aimost all the animals had some material in their guts. The fullest of these animals had 90% gut fullness; the mean gut fullness was 34.3%. Of the animals caught at 5 m, less than one-third had any mater% in their guts, and the fullest of these individuals had only 30% gut fullness. The mean gut fullness of copepods at 5 m was 5.6%. Of the animals from the surface haul, only six had any material in their guts, and the mean gut fullness was 1.8 %. The gut contents of animals at 0 m and 5 m were significantly lower than for animals at 20 m (P < 0.005, ~usk~-W~~is analysis of variance), Having no data on the die1 vertical distribution of Calanu~ pacificus, it is impossible to determine whether the capepods were “avoiding” the concentrated layers of GJVYP nodiniurnjlavum.

The location of the gut in which food contents were found differed according to whether the animals were caught within or above the G.flavum biomass maximum, or whether they were caught below it. In surface waters the animals with gut contents had them only in the hindgut. This indicates that those which had been feeding had not fed recently, and impliis that they fed at a depth other than the depth of capture. By contrast, animals caught at 20 m contained material in the foregut as well as in the hindgut, indicating that at least some of them had been feeding at the depth of capture.

SUPPRESSED

ZOOPLANKTON

GRAZlNG

x7

These field observations lend further support to the results of the grazing experiments, namely that Calanus pacificus did not graze significantly upon the Gymnodiniumflavum bloom. An investigation of the particulate matter revealed that, with the exception of the 20-m sample, G.~avum dominated the microplanktonic biomass at all depths. At 20 m G. jlavum comprised only 75 “/, of the cell numbers, whereas most of the remaining 25 % was composed of a large oligotrich (Z 50 pm diameter). It is possible that Calanus pacl~cu~ caught at 20 m were feeding on the oligotrich cells.

The results of both the laboratory and the field feeding studies presented here strongly indicate that Cafanus pacificus did not eat significant quantities of the bloom of ~ymnodi~ium~avum which occurred in the waters off La Jolla in July, 1980. This is one of the few instances in which a zooplankton herbivore has been shown to avoid ingesting naturally occurring particulate matter. It has become popular to think of copepods and other filter-feeding zooplankton as mechanical feeders, moving their mesh-like feeding appendages through the water and capturing particles in an indiscriminate fashion (Boyd, 1976; Nival & Nival, 1973, 1976). If this were true then zooplankton herbivores should display only one type of selection, size-selection, in which the size of particles captured is determined by the efficiency of the feeding “sieve” in capturing particles of a given size. In principle this model does explain observations of higher feeding rates on large particles than on small ones (e.g. Mullin, 1966; Frost, 1972). Indeed, Caianus paciJicus has been shown to conform to the predictions of such a model when fed centric diatoms of different sizes but of essentially the same shape (Frost, 1977). The act of particle capture may have very little to do with retaining particles upon a sieve-like filtering mesh (Alcaraz et af., 1980; Koehl & Strickler, 1981). These recent cinematographic observations have shown that the Reynolds number in the vicinity of a copepod’s moving mouthparts is very low. In this highly viscous environment the mouthparts appear to behave more like paddles than like sieves: rather than flowing through the setose appendages, water is pushed about by their movement. These observations cast doubt upon the mechanical model of copepods as passive, sizeselective filter-feeders. The direct film observations suggest that copepods do indeed have the behavioral flexibility to discriminate between particles of different food quality. A limited number of experiments have purported to demonstrate active selection using traditional techniques for estimating feeding rates, but many of these have recently been challenged. For example, Richman et al. (1977) presented results from a series of experiments with natural sea water and calculated filtering rates based upon measurements of particle concentration made with an electronic particle counter. A variety of feeding behaviors were observed, ranging from increasing filtering rate with increasing particle size (classic size-selection) to filtering activity only within very restricted ranges

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MARK E. HUNTLEY

of the particle size-spectrum. They suggested that the latter result could be attributed to differing food quality within the particle spectrum. Harbison & MGAlister (19801, however, critically evaluated the use of electronic particle counters in copepod feeding experiments, and stated that “we cannot regard the conclusions drawn by Poulet (1974, 1978), Richman et al. (1977), or Cowles (1979) as based on experimental evidence” This criticism is based on the inability of the electronic particle counter to estimate the size of non-spherical cells correctly. Harbison & McAlister’s results effectively negate any experiment where a diverse natural particle spectrum containing non-spherical cells is analyzed with an electronic particle counter. My experiments with the Gymnodinium flavum bloom cannot be similarly criticized because (1) G. jlavum is virtually spherical. (2) it is unicellular and thus cannot give rise to the artifacts created by the breaking ot chain diatoms, and (3) it so dominated the natural particulate matter (90”/ by volume) that, for all practical purposes, it was the only cell therein. Other experimental results which seem to demonstrate active selection have also been challenged. Donaghay & Small (1979) presented evidence, also based upon electronic particle counter data, indicating that Acartia clausi actively selected cells of Thalassiosirafluviatilis HUstedt ( = T. weissjlogii Grunow) in preference to inert beads of a similar size. Some clones of T.fluviatiiis are known to produce extremely long chitan spines (McLachlan et al., 1965). It has been suggested that the presence of spines should increase the effective diameter of such cells, as perceived by filter-feeding copepods. Since the spines do not contribute appreciably to the total cell volume, no difference between spined and unspined cells would be detected by an electronic particle counter. Gifford er al. (1981) have shown that Cafanusfinmarchicus feeds at higher rates on spined cells than on cells which have had their spines experimentally removed. In reference to the experiments of Donaghay & Small (1979) they suggest that “the postulated rejection of plastic spheres in favor of Thalassiosira cells may be an artifact of experimental design. Such results may require reinterpretation if food particles usually considered to be 14-17 pm in diameter in fact appear to be much larger to the organism consuming them.” From observations of the T. weissflogii clone in culture at Scripps Institution of Oceanography, we know that it has spines similar w those described by McLachlan et al. (1965). It could be argued that, although the equivalent spherical diameter (ESD) of T. weisq‘logii appears from electronic particle counter measurements to be less (12.7 pm) than the ESD of Gymnodinium ji’avum (20.2 pm), the Thalassiosira weissflosii cells are made so much larger by virtue of their spines that they are therefore filtered at the higher rate. Such an argument may make sense qualitatively, but not quantitatively. The filtering rate on the Gymnodiniumflcvum biomass peak was 0.30 ml . copepod-’ . hh ’ (SD = 0.36), not significantly different from zero. Consider, then, the results of other experiments in which Calanus pacijkus has been presented with suspensions of dinoflagellates of similar size and shape. Paffenhsfer (1976) fed Gymnodinium spleendens(ESD = 29.6 pm) to Calanus pacificus females collected off La Jolla and obtained filtration rates > 10 ml . copepod-- ’ . h- ‘. He obtained

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GRAZING

89

even higher rates for feeding on Prorocentrum micans (ESD = 28.7 pm). Femandez (1979) found that nauplii and early stage copepodites of Calanuspacifcus had about the same filtration rates on Thalassiosirafluviatilis as on Gymnodin~um spiendens. Judging from the results of PafTenhofer (1976) and Fernandez (1979), one would have expected a significant filtration rate on C. jluvum and furthermore, similar filtration rates on the two phytoplankton used in my experiments. Calanus pacificus, however, filtered upon Thalassiosirafluviatilis at a rate more than ten times higher than the rate on Gyrn~~d~~~urn JJavum. The implication of this result is obvious: Calanus pacifirus consumed very few, if any, cells in the dinoflagellate bloom. The significant reduction in gut contents of copepods within the biomass maximum relative to those below the maximum, and the absence of material in the foreguts of copepods within the dinoflagellate biomass maximum, further support this conclusion. The avoidance of Gymnodin~um~avum by Calanuspacz~cus can perhaps be explained by the bioluminescence of the d~o~age~ate. White (1979) showed that Aeartia tonsu ingested highly luminescent cultures of G~nyau~ax excavatu at much lower rates than cultures of the same organism which had a low capacity for biolum~escence. Esias & Curl (1972) obtained similar results, and suggested that the dinofl~ellate flash startles the zoop~ankton predator and permits the cell to escape. The bloom in La Jolla Bay did not appear to have the intense bioluminescence which has been previously attributed to Gymnodin~um~avum (Kofoid & Swezy, 1921). My results warrant some speculation on the significance of active selection as it might be related to the development of dinoflagellate blooms. It is a curious fact that, although dinoflagellate blooms often occur in the late summer, at a time of year when zooplankton biomass is much higher than in the spring, they nevertheless can attain concentrations similar to vernal phytoplankton blooms. This is all the more curious since dinoflagellates typically have growth rates which are about three times lower than the growth rates of most diatoms (Chan, 1978; Hoogenhout & Amesz, 1965). How is it possible that dinoflagellates are capable of producing massive blooms under these seemingly adverse conditions? Grazing, or the lack of it, can be an important factor in the ph~opl~kton dynamics of temperate waters. The decline of spring diatom blooms has been shown to be caused by grazing rates of up to 50% of the standing stock per day (Riley et al., 1949). Conversely, the release of grazing pressure has been shown to permit an increase in standing stock of phytopl~kton previously limited by grazing (Huntley & Hobson, 1978). I suggest that in the case of the bloom of G.~a~rn, the absence of grazing pressure by CaZa~~spac~~cus,an impo~ant grazer in local waters, permitted the bloom of dino~agellates to persist and perhaps even permitted it to accumulate. Zooplankton do not always display active selection in the presence of dino~age~ates. Indeed, Mullin & Brooks (1970) were able to rear C. pacz~cus on a diet of Gymnodinjum .~~~e~de~.~. This same dinoflagellate has also proved to be an excellent source of food for larvae of the northern anchovy, Engraulis mordax (Scura & Jerde, 1977). Whether Calanus avoided ingesting Gymnodiniumjiavum because of its bioluminescent properties,

90

MARKE.HUNTLEY

or whether some other mechanism, such as the production of a distasteful chemical compound, is responsible for the i&$&ion offabding is not at issue, What is s@&icant is that Calanus pacificlrs did display active selection in nature, and that this behavior in all likelihood contributed to the success of the dinoflagelktte bloom. In the light of these observations, it seems worthwhile to continue studies aimed at determining what types of naturally occurring particles induce active selection behavior in filter-feeding zooplankton.

Support for this project was provided by a NATO postdoctoral f~owshi~ administered by the Natural Sciences and Engineering Research Council (NSERC) of Canada and by DOE Contract ~~-A~Q3-~~S~~l~.

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HOOGENHOUT, H. & J. AMESZ, 1965. Growth rates of photosynthetic microorganisms in laboratory cultures. Arch. Mikrobiol., Vol. 50, pp. 10-24. HUNTLEY, M. E. & L.A. HOBSON, 1978. Medusa predation and plankton dynamics in a temperate fjord. British Columbia. J. Fish. Res. Board Canada, Vol. 35, pp. 257-261. KOEHL, M.A.R. & J.R. STRICKLER, 1981. Copepod feeding currents: food capture at low Reynolds number. Limnol. Oceanogr., Vol. 26, pp. 1062-1073. KOFOID, C.A. & 0. SWEZY, 1921. The free-living unarmored Dinoflagellata. University of California Publications in Zoology, Memoirs, Vol. 5, pp. l-562. MCLACHLAN, J., A.G. MACINNES & M. FALK, 1965. Studies on the chitan (chitin: poly-n-acetyl glucosamine) fibers of the diatom Thalassiosira fluviafilis Hustedt. Can. J. Bat., Vol. 43, pp. 707-713. MULLIN, M. M., 1966. Selective feeding by calanoid copepods from the Indian Ocean. In, Some contemporary studies in marine science, edited by H. Barnes, Allen and Unwin, London, pp. 545-554. MULLIN, M.M. & E.R. BROOKS, 1970. Growth and metabolism of two planktonic, marine copepods as influenced by temperature and the type of food. In, Marine food chains, edited by J. Steele, University of California Press, Berkeley, pp. 74-95. NIVAL, P. & S. NIVAL, 1973. Efficacite de la filtration des copepodes planctoniques. Ann. Inst. Oceanogr. Paris (N.S.), Vol. 49, pp. 135-144. NIVAL, P. KLS. NIVAL, 1976. Particle retention efficiencies of an herbivorous copepod, Acartia clausi (adult and copepodite stages): effects of grazing. Limnol. Oceanogr., Vol. 21, pp. 24-38. PAFFENH~FER, G.-A., 1976. Continuous and nocturnal feeding of the marine planktonic copepod Calanus helgolandicus. Bull. Mar. Sci., Vol. 26, pp. 49-58. POULET, S.A., 1974. Seasonal grazing of Pseudocalanus minutus on particles. Mar. Biol., Vol. 25, pp. 109-123. POULET, S. A., 1978. Comparison between five coexisting species of marine copepods on naturally occurring particulate matter. Limnol. Oceanogr., Vol. 23, pp. 1126-1143. POULET, S.A. & P. MARSOT, 1978. Chemosensory grazing by marine calanoid copepods (Arthropoda : Crustacea). Science, Vol. 200, pp. 1403-1405. RICHMAN, S., D.R. HEINLE & R. HUFF, 1977. Grazing by adult estuarine calanoid copepods of the Chesapeake Bay. Mar. Biol., Vol. 42, pp. 69-84. RICHMAN, S. & J.N. ROGERS, 1969. The feeding of Calanus helgolandicus on synchronously growing populations of the marine diatom Ditylum brightwellii. Limnol. Oceanogr., Vol. 14, pp. 701-709. RILEY, G.A., H. STOMMEL & D.F. BUMPUS, 1949. Quantitative ecology of the plankton of the western North Atlantic. Bull. Bingham Oceanogr. Collect., Vol. 17, pp. 66-82. RUNGE, J.A., 1980. Effects of hunger and season on the feeding behavior of Calanus pacificus. Limnol. Oceanogr., Vol. 25, pp. 134-145. SCURA, E. D. & C. W. JERDE, 1977. Various species of phytoplankton as food for larval northern anchovy, Engraulis mordax, and relative nutritional value of the dinoflagellates Gymnodinium splendens and Gonyaulax polyedra. Fish. Bull. NOAA, Vol. 75, pp. 577-583. STEELE, J. H. & B. W. FROST, 1977. The structure of plankton communities. Trans. R. Sot. London, Ser. B, Vol. 280, pp. 485-535. WHITE, H.H., 1979. Effects of dinoflagellate bioluminescence on the ingestion rates of herbivorous zooplankton. J. Exp. Mar. Biol. Ecol., Vol. 36, pp. 217-224.