Limnol. Oceanogr., 33(5), 1988, 1037-1054 0 1988, by the ... · 0 1988, by the American Society of Limnology and Oceanography, Inc. Phytoplankton succession in microcosm experiments

Limnol. Oceanogr., 33(5), 1988, 1037-1054 0 1988, by the American Society of Limnology and Oceanography, Inc.

Phytoplankton succession in microcosm experiments under simultaneous grazing pressure and resource limitation

Ulrich Sommer Max Planck Institute of Limnology, P.O. Box 165, 2320 PISn, FRG

Abstract

The influence of grazing pressure on the occurrence and outcome of nutrient competition among planktonic algae was studied in two-chamber microcosms where there was a flow in both directions between a light reactor without zooplankton and a dark reactor with zooplankton (Daphnia fongi- spina and Daphnia magna). The phytoplankton inoculum was a mixed, natural assemblage. Zoo- plankton could influence the dynamics of phytoplankton both by selective grazing and by differential excretion of limiting nutrients. Grazing pressure did not prevent the occurrence of nutrient limitation in algae and, hence, of nutrient competition between them. Zooplankton did, however, influence the outcome of competition by lowering Si: P ratios. A comparison with my previous experiments shows that diatoms need higher Si: P supply ratios for dominance over green algae in the presence of grazers than in grazing-free competition with steady or weekly pulsed nutrient SUPPlY.

Phytoplankton ecology has long been dominated by the view that community dynamics are controlled by physical factors. Temperature, turbulence, and stratification have been thought to determine species composition, species seasonality, and sea- sonal biomass and productivity patterns. This attitude still persists (Harris 1986), but since the mid- 1970s biotic interactions also have become appreciated by plankton ecologists. As a consequence, a controversy between “bottom-up” and “top-down” control of communities has emerged. As early prototypes, the studies of Tilman (1977, for bottom-up) and Porter (1973, for top-down) can be cited. Meanwhile, most ecologists have accepted that bottom-up and top-down control of community dynamics are not mutually exclusive, at least in theory.

Both concepts have received considerable theoretical refinement during the last years. The concept of bottom-up control took the form of an elaborate theory of resource competition (Tilman 1982); that of top- down control culminated in the concept of the “trophic cascade” (Carpenter et al. 1985), where each trophic level is considered to be controlled by the next higher one, and the

Acknowledgments I gratefully acknowledge technical assistance by H.

Buhtz and B. Groegcr. J. Lehman and S. Carpenter wrote constructive reviews for my manuscript and R. Sterner reviewed an earlier draft.

structure of the entire food web by the top .- -- predators. In phytoplankton ecology%%- tom-up vs. top-down control is often equated with growth-rate (better: reproductive rate) vs. loss-rate control (Kalff and Knoe- chel 1978). This is not entirely correct because one of the major loss-rate compo- nents, sedimentation, has nothing to do with top-down control whereas regeneration of resources by higher trophic level organisms is a top-down mechanism with impact on the reproductive rate.

Many illustrative examples both for bottom-up and for top-down control have been published, and most workers accept that the bottom-up vs. top-down controversy is not an “either-or” question but rather a “how much” and “how often” question. Still, studies which give balanced attention to both have been rare (Lehman and Sandgren 1985; Sterner 1986; Carpenter et al. 1987). In a system, natural or experimental, where both competition for limiting resources and predation from higher trophic levels can occur, three outcomes are possible. First, predation may be too weak to change the outcome of competition; second, predation on all prey species may be so strong that they never exploit their resources sufficiently to make competition detectable; third, predation may tilt the balance of competition.

The first alternative is likely to occur when the predator populations themselves are strongly exploited. The second alternative

1037

1038 Sommer

requires that none of the prey populations are resistant to predation and that a steady state develops where prey populations reproduce at their resource-saturated rates (Goldman et al. 1979). The third alternative may occur through three different mecha- nisms. First, increasing predation losses increase the resource requirement for repro- duction to equal mortality. The smaller this resource requirement, the better the competitive ability of a given species for a given resource (Tilman 1982). Interspecific differences in predation resistance can thus lead to a change in the competitive rank order. Second, differential regeneration of different resources may also change the ratio of the supply rates of potentially limiting resources, which in a system with at least two potentially limiting resources is the param- eter most important for determining the t;~xonomic~?&come of competition (Til- man 1982). Since zooplankton excrete phosphorus and nitrogen in dissolved form and diatom silicate as particulate debris, it seems plausible that in a phytoplankton- zooplankton system Si : P or Si : N supply ratios will decline. Since diatoms have been shown to become dominant in multispecies competition experiments at high Si : P ratios but to become excluded at low ones (Som- mer 1983; Kilham 1986; Tilman et al. 1986), a decline of Si : P ratios is predicted to lead to a shift away from diatoms. Third, zooplankton may change the temporal and spatial pattern of nutrient supply both by creating spatial microscale patchiness via their excretion plumes (Goldman et al. 1979; Lehman and Scavia 1982) and by creating macroscale temporal fluctuations, if their population densities undergo oscillations (McCauley and Murdoch 1987). At least macroscale patchiness of nutrient supply has been shown to influence the outcome of competition (Sommer 1985).

Here, I report on microcosm experiments with three trophic levels, inorganic resources, algae, and herbivorous zooplankton. The experiments were meant to study intrinsic trends in relative importance of bottom-up and top-down control in a phytoplankton-zooplankton system without physical perturbation and without exploitation of the grazer population by carni-

vores. To calculate grazing losses for the algal populations, I separated production (in the light) and grazing (in darkness) into two different containers with bidirectional flow between them. Into the grazing compartment, flow transported freshly produced algae and those dissolved nutrients that had not been incorporated into algal biomass. Into the production compartment were transported the ungrazed algae together with freshly e:xcreted nutrients. In addition to ex- creted nutrients, leakage from dead animals contributed to recycling. External exchange of material and organisms (sampling and replacement of the sample volume by fresh medium) was negligible in comparison to internal cycling. Since sedimentary losses were excluded, algal loss rates could be equated with grazing. Initial nutrient concentrations before consumption by organisms were high enough to permit maximal reproductive rates of algae. Therefore, sub- sequent limitation of reproductive rates could be equated with exploitative competition. Silicon and phosphorus were used as potentially limiting resources, since those nutrients had most often been used in the pure competition expeiments that underpin the discussion here.

The following questions were asked. Do algae-grazer systems without physical perturbation and without exploitation of the grazers tend toward strong resource limitation of the algae or toward a very rapid turnover at nearly resource-saturated reproductive rates (the “spinning wheel” sensu Goldman 1984)? Does the postulated succession from diatoms to other taxa take place? Do such systems tend toward steady state or toward oscillations? Is there a tendency toward a stable (“climax”) species composition of the phytoplankton, as can be observed in competition experiments? Do different species become dominant in competition experiments without grazers?

Methods Experiments were conducted in pairs of

14-liter polycarbonate containers. Culture volume in each was 12 liters. One of the containers (“light reactor”) was illuminated (270-320 pmol quanta m-2 s-l in the center of the container, depending on algal light

Grazing and competition in microcosms 1039

attenuation) and contained no zooplankton. The other container was kept dark (“dark reactor”) and contained zooplankton. The algal suspension was circulated between the two containers with a peristaltic pump. The flow rate was 1 liter h-l, which meant that the algae should on average experience a 12 : 12 L/D cycle. Zooplankton were pre- vented from entering the back flow into the light reactor by sucking the back flow from the surface of the culture through a hori- zontally oriented pipette with an opening of x0.5 mm. This aperture was cleaned several times per week. Animals which never- theless entered the back flow were either crushed in the peristaltic pump or killed by the more intense stirring in the light reactor. Living zooplankton were never observed in the light reactor. Dead animals might have been an additional source of dissolved nutrients. Cultures were kept in suspension by gentle aeration (-40 liters h-l) and mixing with a floating stirring bar (Nalgene Lab- ware) which rotated continuously at 30 t-pm in the light reactor and at 10 rpm for 10 min at hourly intervals in the dark reactor. The cultures were kept at 18°C by a circu- lating water bath.

The inoculum consisted of 1 liter of natural plankton suspension enriched with net- phytoplankton (1 O-250 pm) taken from the epilimnion of moderately eutrophic Schiih- see. Large zooplankton were screened off by a 250-pm mesh-size net. Small zooplankton’ (rotifers and Protozoa) disappeared relatively rapidly in the course of the experiments. After 3-4 weeks they became un- detectable, and they never exceeded 10% of the algal biomass. Hence, their influence on the outcome of the experiments is considered negligible. Zooplankton (Daphnia longispina or Daphnia magna) was ob- tained from pure cultures. With the zooplankton inoculum a variable amount of their food alga, Scenedesmus acutus, was also introduced into the cultures.

The medium consisted of filter-sterilized (0.2 pm) Schohsee water, enriched by nitrate, phosphate, and silicate. Nitrate was always offered in excess (N : P > 30 : 1); Si : P ratios varied between experiments. Exper- iments are characterized by the letters L (for D. longispina) or M (for D. magna) followed

by a number indicating the Si : P ratio. The medium in experiment L 12 contained 13.56 PM Si and 1.13 PM P, in experiment L20 41.6 PM Si and 2.08 PM P, in experiment L34 22.6 PM Si and 0.665 yM P, in experiment L550 257 PM Si and 0.468 PM P, in experiment Ml8 39.6 PM Si and 2.2 PM P, andin experiment M510 357 PM Si and 0.7 PM P. Probably due to adsorption to the walls, total Si and total P within the reactors gradually declined by about half per 50 d and in fairly constant (f 15%) proportions. Total nitrogen, however, slightly increased by about 20% per 50 d. Since nitrogen-fixing blue-greens were extremely rare, uptake of gaseous ammonium from the air seems the most plausible source.

Samples for phytoplankton counts and chemical analyses were taken at weekly intervals. The sample volume (1 liter from each reactor) was replaced with fresh medium. This sample size was insufficient for reliable zooplankton counts; therefore, these data are not reported here. Phytoplankton counts were performed according to the standard Utermijhl technique, with about 400 individuals (cells or colonies) counted per each reported species. If we assume a Poisson distribution, this procedure gives a counting precision of + 10% (95% C.L., Lund et al. 1958). Specific net growth rates of algae (k = dN/N dt) for each sampling interval were calculated as (In N, - In NJ/ (tl - tJ, where N is cell number and t time in days; the subscripts 1 and 2 indicate the interval’s beginning and end. Table 1 gives a list of symbols and their meanings.

Mortality rates due to grazing (y) were calculated as In B, - In B,. Even though grazing was the only important source of mortality, calculation of grazing rates (y) was not straightforward. It is not known whether cell division rates differed between the two reactors. It can, however, be assumed that algal biomass production occurred only in the light reactor. Therefore, grazing rate estimates were not based on numbers but on biomasses. The only available species-specific measure of biomass was cell volume, which for this purpose had to be measured individually for both reactors. Cell volumes were estimated by approxi- mation to the nearest standard geometric

1040 Sommer

Table 1. List of symbols, with their definitions and units.

- Meaning IJnits

N, cell number, beginning of liter-l interval

N; cell number, end of liter-l interval

4. biomass (cell volume) in mm3 liter-’ light reactor

4, biomass (cell volume) in mm3 liter-l dark reactor

k specific net growth rate d-’ Y grazing rate d-’ Y “lZlX grazing rate on maximally d ’

grazed alga CL reproductive rate d-’ P,,,,x maximal reproductive rate d- ’ P*cl relative growth rate dimensionless a edibility index dimensionless SL. dissolved nutrient concen- PM

tration in light reactor s,, dissolved nutrient concen- PM

tration in dark reactor 4 cell quota of limiting dimensionless

nutrient (normalized to carbon)

40 minimal cell quota dimensionless --

-___

-~

L12 L20 L34 L550 Ml8 M510

Designators ofexperimcnts

Grazer species Si : P (medium)

Daphnia longispina 12 D. longispina 20 D. longispina 34 D. longispina 550 Daphnia magna 18 D. magna 510

solid after measurement of at least 40 individuals. The near identity of POC (mg) per unit of cell volume (mm3) between the light and dark reactor (0.121 mean, 0.029 SD vs. 0.123 mean, 0.032 SD, respectively) excludes the possibility that a systematic difference in water content of the biomass between the two reactors would have biased the estimates of grazing rates (the assump- t ion of no production in the dark reactor being guaranteed only for carbon production, not necessarily for cell volume production). Further, assuming even distribution of organisms within each reactor, biomass entering the dark reactor must equal biomass in the light reactor (B3 and bio- rnass entering the light reactor must equal biomass in the dark reactor (BP). Given the average algal residence time of 12 h in each reactor and the fact that grazing was re-

stricted to the 12 h in the dark reactor, the grazing rate (y) becomes ln(BJBn) with the time dimension d-l. If we assume no losses other than grazing, the reproductive rate was estimated as p = k + y.

Particulate organic carbon (POC), soluble reactive phosphorus (SRP), total dissolved phosphorus (TDP), total phosphorus (TP), nitrate, nitrite, ammonium, and soluble reactive silicate (SRSi) were determined according to Strickland and Parsons (1968), total diatom silicate (TSi) according to Tes- senow (1966), and total nitrogen according to D’Elia et al. (1977).

Results Phytoplankton biomass and species com-

position-In most experiments temporal variation of POC comprised one order of magnitude or slightly more. However, in experiment L12 the range of variation was only about a factor of 5. As expected, biomass was always lower in the dark reactor, usually by lo-50%. Temporal changes of biomass were relatively smooth (L12, L550) to extremely rapid (L20). Figures 1 and 2 show only the chemically extreme experiments L,12 and L5 50 as examples; these two experiments are shown as examples throughout this paper.

Initially, diatoms (usually Asterionella formosa) were dominant in all experiments. In experiment L34 Nitzschia actinastroides was dominant initially, but Asterionella showed a marked increase from day 1 to day 8. In experiments L12, L20, and L34 diatoms declined to minimal levels of < 1% of total phytoplankton biomass within the first 50 d. In experiments L550, Ml 8, and M5 10 minimal diatom levels were mark- edly higher (> lo%, see Fig. 8) but I cannot state with certainty whether the experiments had been conducted long enough to reach the real minimal level. Experiment M 18 was relatively short (53 d), and in the experiments with high Si : P ratios (L550 and M5 10) the decline of diatoms was slower than in the other experiments. In experiments L12 and L34 a slight though significant recovery of diatoms could be observed after ablout 2 months.

Among the nonsiliceous algae, S. acutus was typical of early succession. In experi-


500

T L aJ .; 1oc

s 5c ks =L .

ki a 10

cn fro v) E 0 .- n

z s 0

100

50 ln VI E” 0 .- n rc 0

$0

day5 L 12 0 10 20 30 40 50 60 70 I)0 90 100 110

Asterionella

Fig. 1. Time-course of experiment L12. Top-particulate organic carbon in the light (L) and dark (D) reactor. Center-percent contribution of major diatoms (Asterioneflaformosa) to total phytoplankton biomass (measured as cell volume). Bottom-percent contribution of major nondiatomaceous algae (Scenedesmus acutus and Mou- geotia thylespora).

ments L12, L550, and M 18 it reached ap- appeared from the cultures, perhaps be- preciable biomasses, but in no experiment cause of the detrimental effect of stirring or did a significant population persist until the because they are highly selected food items end. Small flagellates, such as Cryptomonas of many herbivorous zooplankton, includ- spp., Rhodomonas minuta, and Chryso- ing Daphnia (Knisely and Geller 1986). It

\ chromulina parva (see Fig. 3) rapidly dis- is noteworthy, however, that they had never

1042 Sommer

5oc

C I L a CI

.=1 oc E 2 5c

z

ki a 10

u) 50 u)

E 0 \c 0

SO

100

$ 50

E .- n Y- 0

SO

days L 550 0 10 20 30 40 50 60 70 00 I- -----

=I

\ Asterionella

Motgeotia

Fig. 2. As Fig. 1, but of experiment L550. Center-Asterionella formosa, Synedra acus, and Synedra minuscula. Bottom-Scenedesmus acutus, Rhizochrysis sp., and Mougeotia thylespora.

been successful in multispecies competition merous during periods in the middle of the experiments without grazer interference (e.g. experiments, but never became dominant. Sommer 1983). The maximum ever attained by one of them

Gelatinous green algae and blue-greens was a A 3% contribution to total biomass by (Sphaerocystis schroeteri, Planktosphaeria Sphaerocystis on day 18 in experiment L20. gelatinosa, Elakatothrix gelatinosa, Chroo- These groups are considered resistant against coccus limneticus) were typically quite nu- digestion by zooplankton and may even


Asterionelta

Fig. 3. Grazing losses in experiment L12. Top-diatoms (Asterionella formosa and Nitzschia actinastroides). Bottom-Nondiatomaceous akae (Scenedesmus acutus and Mougeotia thylespora). Thin line in both graphs: losses of maximally grazed species.‘

profit from nutrient enrichment during gut passage (Porter 1973). Another characteristic midsuccessional species was the amoeboid chrysophyte Rhizochrysis sp., which in L34, L550, and M510 persisted in appre- ciable numbers until the end of the experiment. From a form-function point of view this species is quite different from the gelatinous greens. Mechanical considerations (<30-pm diam, no gelatinous sheath, no solid cell wall) suggest that it should be edible by Daphnia. Its amoeboid life form sug- gests that it could supplement its nutrition by feeding on bacteria, a quite widespread feature among chrysophytes (Bird and Kalff 1986). I have no data in support of this idea, however.

In the final phase of all experiments, the filamentous green alga Mougeotia thylespora (Zygnematales) was dominant. In all experiments it comprised > 50% of total algal biomass at the end-in experiments L12 and L20 >90%, in experiments L34 and

L5 5 > 7 5%. Another filamentous green alga, Ulothrix subtilissima (Ulotrichales), was co- dominant at the end of experiment Ml 8 (26%).

Grazing-The sample size (1 liter) was insufficient for reliable counts of Daphnia. Moreover, the animals seemed to escape from the sampling tube. As a rough estimate, peak densities were about 20-30 ind. liter-l. To obtain an estimate of the grazing pressure, I assumed that the most strongly grazed alga (ym,,) on each sampling occasion was filtered at 100% efficiency. Typi- cally, the maximally grazed alga was C. par- vu, Rhizochrysis sp., S. acutus, Nitzschia spp., or Achnanthes minutissima. This conforms to the widespread assumption that Daphnia spp. are most efficient in the size range of nanoplankton (Burns 1968; Gli- wicz 19 7 7; Geller and Miiller 19 8 1; Knisely and Geller 1986).

Maximal grazing rates generally varied between 0.5 and 1.5 d-l (Figs. 3 and 4),

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Fig. 4. As Fig. 3, but in experiment L550. Top-Asterionellaformosa, Synedra acus, and Synedra minuscula. Bottom-Scenedesmus acutus, Mougeotia thylespora, and Rhizochrysis sp.

except in experiment L34 peak values were 2.2 d-l. The experiments were not conducted long enough to judge whether 7max showed regular oscillations or irregular fluctuations. In all experiments except L550 (Fig. 4) and M5 10, peak grazing rates were separated by 25-50 d, well within the range of periods of Daphnia population oscillations reported by McCauley and Murdoch (1987).

The edibility of phytoplankton species was expressed by the index @ (Vanderploeg and Scavia 1979) which gives the probability that an algal individual contained in the filtered volume of water will be ingested and killed. It was calculated as 9 = 71~~~. For all species, the index @ fluctuated between wide limits, the values of arcsin @ being fairly normally distributed. In Fig. 5 the principal species are ranked according to their mean f@ for D. longispina. Means and

standard deviations were calculated from individual values (one species per sampling occasion and one experiment constituted an individual case). For the ANOVA, however, means of the separate experiments were used instead of the individual values. The two-factor ANOVA of the @ values showed a highly significant effect of the algal species (F = 39.4, df = 10,44, P < O.OOOl), no effect of the grazer species (F = 0.04, df = 1,44, P = 0.85), and no two-factor interaction (F = 0.39, df = 10,44, P = 0.40). Comparison at the single algal species level showed no significant differences in + values for the two Daphnia species in 10 cases and a margin- ally significant difference in one (Synedra minuscula, t-test, P = 0.041).

In conclusion, the two grazer species be- haved quite similarly. This finding is no great surprise, given the similarity of feeding mode. The empirical relationship between


0 0.25 0.5 0.75 1 0 0.25 0.5 0.75 1

ALGA

Achnanthes minutissima Nitzschia actinastroides

See ned esmus acutus Rhizochrysis sp. Synedra minuscula

Synedra acus Elakatothrix gelatinosa Ulothrix subtilissima Asterionella formosa Mougeot ia thy lespora Sp haerocyst is schroe teri

GRAZER Daphnia longispina

I 1 I I I I

I I

I I I I 4

I A I I I I-+ I

I

L ” 1 I I +

I v

+-f +-I I

”

+--I

I I

” I I I I I I

Daphnia magna Fig. 5. Edibility index Cp of the principal phytoplankton species, mean f 1 SD. Data are pooled for the L

(leftyand for the G (right) experiments. - - - -

body size and maximal size of edible particles (Burns 1968) could, however, have given rise to the expectation of a slightly enhanced edibility of the larger algae for D. magna. The algae themselves showed considerable differences in edibility. Scheffe’s multiple range test (P > 0.05) showed three homogeneous groups of algal species with D. longispina as grazer, four groups with D. magna as grazer, and six groups within the pooled data set. All three analyses had the diatoms A. minutissima, N. actinastroides, and S. minuscula, the green alga S. acutus, and the chrysophyte Rhizochrysis in the most edible group of algae. Contrary to Knisely and Geller (1986) there was no indication that coccoid algae were less vul- nerable than similarly sized species without solid cell walls (here represented by Rhi- zochrysis; in Knisely and Geller 1986 represented by Cryptomonas and Rhodomo- nas). The highly edible algae in my experiments have in common that they are < 30 pm in all linear dimensions, except for the needle-shaped S. minuscula whose length overlaps this size limit (25-37 pm). The size limit conforms well to other experimental data (Burns 1968; Gliwicz 1977). Another common feature of the highly edible algae is the absence of a gelatinous sheath.

The needle-shaped Synedra acus exceeds 30 pm (130-280 pm long) and is separated

from the optimal food algae by the Scheffe test for the full data set and for the D. magna data set, but not for the D. longispina data set. The same holds for the small gelatinous green alga E. gelatinosa (18-25 pm long, including the gelatinous sheath), whereas the larger gelatinous green alga S. schroeteri (SO- 120~pm colony diam) was the least edible alga for both Daphnia species and was sta- tistically well separated from all other algae. Asterionella formosa and M. thylespora were of intermediate edibility, with @ values widely scattered but clustered in the range 0.3-O. 5. This edibility index is greater than reported by Knisely and Geller ( 1986) whose Daphnia species were Daphnia galeata and Daphnia hyalina. They gave a value of @ = 0.14 kO.2 (SD) for A. formosa and values from 0 to 0.27&O. 17 (SD) for Mougeotia and different size classes of D. hyalina and D. galeata. Reynolds et al. (1982) gave a very wide range from 0.28 to 1 as possible @ values of Asterionella. They did not pro- vide data for Mougeotia. According to Leh- man and Sandgren (1985) the edibility of Asterionela depends on colony size.

Nutrient status and reproductive rates- With the initial diatom blooms, SRSi concentrations in all experiments rapidly fell to values near or below the limit of detect- ability (0.1 ,uM). Later one or several pulses of SRSi increase were observed (Figs. 6 and

1046 Sommer

days L 12 0 10 20 30 40 50 60 70 00 90 100 110

ZE % - cm-- _pg-o,o

a 0.01-O cx

-Lo0 0-N P O-0

UJ 0

Fig. 6. Nutrient status of phytoplankton in experiment L12. Panel 1 -concentrations of SRSi in the light reactor. Panel 2-reproductive rates of diatoms (Asterionelfuformosa and Nitzschia actinustroides). Panel 3- atomic C : P ratio in particulate matter and intensity of P limitation (community average). Panel 4-reproductive rates of nondiatomaceous algae (Mougeotiu thylesporu and Scenedesmus acutus). Panel S-concentrations of SRP in the light reactor.

7). These increases of SRSi concentration tom debris. If none of the freshly imported occurred during periods when diatom pop- silicate was consumed by the diatoms, the ulation densities were already low. There maximal possible increase in SRSi concen- were two potential sources of SRSi, replace- tration by one sample replacement would ment of the sample volume by fresh me- have been 1.14 PM in experiment L12, 3.8 dium and dissolution from particulate dia- PM in L20, 1.88 PM in L34, 21.5 PM in


days

200 z x , - 100

iii

ZJ 0

1 .+.$yn. minuscula

*._ :

7 0.5 u

.

=L 0 1

z .- % .w .- E .-

500 0.5 ; -

0 0

.- %

2. .‘I: L

a 2

100 0.1 2 LJ 0 0 .- =

See nedesmus

1

‘; 0.5 -0

.

=

l J-N 0

0.1

r 7 0.05 m

g 0.02

fl 0 Fig. 7. As Fig. 6, but in experiment L550. Panel 2-Asterionellafirmosa, Synedra minuscufa, and Synedra

acus. Panel 4-Mougeotia thylespora, Scenedesmus acutus, and Rhizochrysis sp.

L550, 3.3 PM in M18, and 29.75 PM in decay equation of Kamitani and Riley M5 10. In all experiments, larger SRSi pulses ( 1979). were occasionally observed. Apparently, In most cases diatom reproductive rates dissolution of diatom debris is not always closely followed the concentrations of SRSi. as gradual as suggested by the exponential In many cases the dependence could be ex-

1048 Sommer

Table 2. Monod parameters for silicate-limited growth of diatoms. -- -~ =-

P,,. (d-7 K, CPM) - Synedra acus 0.84 8.9

Synedra minuscula 0.92 7.2 Asterionella formosa 0.49 2.5 Nitzschia actinastroides 0.78 1.8 Achnanthes minutissima 1.28 17.4 --

Literature data (from Tilman et al. 1982, table 1, only data i’or20”C selected) Synedra frlliformis 1.1 19.7 Synedra ulna 0.65 4.6 A. firmosa (various clones) 0.42-0.8 1 1 J-3.94

r2

0.96 0.88 0.93 0.98 0.95

n _-

46 25 59 44 26

pressed by the well-known Monod (1950) equation:

PlnaxS I-C = S + k, (1)

where S is the concentration of the limiting nutrient, pmax the nutrient-saturated reproductive rate, and k, the half-saturation constant. For statistical analysis, data of all experiments were pooled. Since r2 values for all major diatom species were at least 0.88 (Table 2), limitation of their reproductive rates by factors other than Si is considered negligible.

Soluble reactive phosphorus concentrations became low during the first few days of every experiment and in most cases clear- ly stayed below 0.1 PM. The attempt to fit a Monod relationship to the reproductive rates of the nondiatomaceous algae failed in every case. This failure could have two caus- es. First, SRP might not be equivalent to biologically available phosphorus. Second, the system might not be in steady state, which makes the Monod equation inapplicable. The first explanation seems relatively implausible. Since the paper by Rigler (1966), it has become generally acknowl- edged that SRP does not measure orthophosphate. Lovstad and Wold (1984), however, showed that algae (Diatoma and Synedra) supplied with natural SRP attained growth rates identical to algae supplied with the same amount of orthophosphate. Since SRP seems to be a relatively good index of biologically available phosphorus, I infer that the lack of steady state made the Monod equation inapplicable.

Unsteady conditions are apparent from all parameters measured in the experi-

ments. Under transient conditions the sim- ple Monod relationship based on dissolved concentrations breaks down for those nu- trien ts where significant intracellular stor- age pools can be accumulated (e.g. P and N, but not Si). Under such conditions, reproductive rates can be better predicted from intracellular concentrations of the limiting nutrient (q, cell quota; Droop 1973, 1983).

P = Pnl,x(l - 404 (2)

where (go is the minimum (subsistence) cell quota. For mixed plankton samples, Eq. 2 is quite impractical because different species may have different cell quotas. Goldman et al. ( 1979) have shown a way out of this dilemma. If p is replaced by p/p,,, (“relative growth rate” in their terminology) interspecific differences in pmax disappear. If cell quotas are normalized to carbon, the prel becomes a linear function of the C : P ratio in the biomass:

&cl = 1 - qo(C : P). (3)

Equation 3 becomes applicable to mixed samples, if biomass-specific minimal cell quotas of the different species are similar. To test this assumption, I calculated regressions of a weighted average (by biomass) of prel on particulate C : P ratios. If successful, the regressions should have intercepts close to 1 .O and slopes equal to qO. The pmax values entered into the calculations were the maximal observed values of p for each species. The question remains of how to treat the hrel of algae limited by something other than P. I tried two extreme ways to enter the prel values of the silicate-limited diatoms into the calculation of community averages. First, I assumed that Si-limited diatoms had


only as much P in their cells as corresponds to their reproductive rate, i.e. the original prel was used for the calculations. Second, I assumed that Si-limited diatoms had a cell quota of P corresponding to unlimited growth, i.e. a P,,~ of 1 .O was entered into the calculations.

Although the first approach failed, the latter yielded relatively satisfactory regressions (Table 3), poorest for experiments L20 and M 18. In Figs. 6 and 7 the relative growth rates have been replaced by the “intensity of P limitation” (IL = 1 - ~~,i) because it makes the concordance between the temporal change of C : P ratios and the intensity of P limitation graphically more apparent. The intensity of P limitation either increased with the progress of the experiment (L12, L34, L510, M510) or showed pro- nounced fluctuations between weak and strong limitation (L20, Ml 8). In the latter two cases, the IL minima later in the time- course of the experiments coincided with grazing maxima. The low intensities of P limitation during initial periods of all experiments were due to dominance by silicate-limited diatoms.

The regressions in Table 3 can test a further assumption of Goldman et al. (1979). Based on culture experiments, they postulated that algae exhibiting a cellular stoichiometry near the “Redfield ratio” (C : N : P = 106 : 16 : 1) are reproducing at rates that are nearly nutrient saturated. Relative reproductive rates for a C : P ratio of 106 calculated from the regression equations ranged from 0.84 to 0.94. Confidence limits for the dependent variable, however, were very broad. The regression for the pooled data set gives a 95% C.L. from 0.43 to 1 in relative growth rates at Redfield stoichiometry. Placing unlimited growth beyond the 95% C.L. of the relative reproductive rate requires a C : P ratio of at least 233. In conclusion, if biomass stoichiometry is used as an indicator of nutrient limitation, a broad zone of uncertainty must be accepted.

Silicon : phosphorus ratios - Import of nutrients into the light reactor occurred mainly through back flow from the dark reactor. On the assumption that the dark reactor was sufficiently well mixed, the concentration of nutrients in the back flow

Table 3. Linear regressions of the weighted community average of pr,., on the C: P ratio of the particulate matter. The calculated y,, for Redfield stoichiometry (C: P = 106) is shown in the right column.

Exp. a b r2 n Prcl.106

L12 0.95 0.00085 0.66 17 0.86 L20 0.97 0.00127 0.53 8 0.84 L34 1.02 0.00162 0.79 13 0.85 L550 1.10 0.00192 0.74 13 0.90 Ml8 1.18 0.0031 0.46 8 0.85 M510 1.09 0.00139 0.94 13 0.94 Pooled data 0.98 0.00103 0.58 72 0.87

equaled the concentration in the dark reactor (SP). Simultaneously an equal amount of culture suspension was exported from the light reactor. Again assuming homogeneous mixing, the nutrient concentration in the outflow from the light reactor equaled the concentration in the light reactor (SJ. The net import of dissolved nutrient into the light reactor thus was (SP - S,). v. t-l, where v is the volume transported per unit of time. For the sake of brevity, SP - SL is called AS. Nutrient supply rate ratios have been assumed to equal AS ratios, i.e. net loading ratios into the reactor where production took place. This ratio does not account for internal cycling taking place within the light reactor, seemingly justified by the absence of significant amounts of zooplankton from the light reactor. Since ASi and AP were often near the limit of detection, the resource ratios in Fig. 8 may easily be off by a factor of 2 or 3. Gross temporal trends are apparent nonetheless. Si : P ratios showed a tendency to decline during the two experiments with initially high ratios (L550, M5 10) and during two of the experiments with low initial ratios (L20, M 18). A U-shaped pattern was observed in the other experiments with initially low ratios (L12, L34). In those experiments, the percent contribution of diatoms to total phytoplankton biomass also showed a slight recovery after increase of the Si : P ratios. It is not clear whether the same would have also happened in experiments L20 and Ml 8 had they been ex- tended.

Discussion As Figs. 6 and 7 show, none of the ex-

periments developed a situation analogous

Sommer

days 0 10 20 30 LO 50 60 70 00 90 loo 110 0 10 20 30 40 50 60 70 00 91

Ml8

Fig. 8. Percent contribution of diatoms to total biomass, Si : P supply rate ratios (ASi : AP), and S centration ratios in the light reactors (all three shown in log scale}.

L 1000 o .-

; TOO j

I

‘0 a . .

1 ‘iii

li: P con-

to Goldman’s (1984) “spinning wheel,” where phytoplankton reproduce at their resource-saturated rates and are eliminated at similar rates. Such a situation would have been characterized by atomic C : P ratios of - 100 in the biomass (Goldman et al. 1979; Sommer in press). In fact, C : P ratios nearly always exceeded 250 after day 50 (except for experiment M 18). In the longest experiment (Ll2; Fig. 6) C : P ratios were > 750 during the last 4 weeks. Community averages of the intensity of P confirmed this trend (Table 3). A few individual species (but never the dominant ones), however, had near-maximal reproductive rates late in the course of experiments, e.g. N. actinastroides in experiments L12, L20, and M 18, both Synedra spp. in L550 and M5 10, and Rhizochrysis spp. in L550 and M510.

In the case of the Synedra spp. the explanation seems easy. Synedra spp. have been shown repeatedly (Tilman 198 1; Tilman et al. 1982; Smith and Kalff 1983; Sommer

1983; Kilham 1986) to be the best competitors for P among all algae so far tested, including natural multispecies assemblages. Probably Synedra spp. were never P limited at all, and increases later in the experiments reflected increases in silicate availability. I suspect the same to be true for Nitzschia; the close correlation of reproductive rates with silicate concentrations (r2 = 0.98, Ta- ble 2) leaves practically no room for assuming P limitation. The explanation is more difficult for Rhizochrysis. Nothing is known about the nutrient requirements of this alga. It might be a good competitor for phosphorus, but it has never been reported to be successful in multispecies steady state competition experiments. Alternatively, this motile alga might profit from the supply mode of limiting nutrients generated by zooplankton (micropatchiness, excretion plumes) or it might supplement its P intake by bactetivory.

None of the dynamic parameters (repro-


ductive rates, grazing rates, nutritional state parameters) showed steady state. Twofold ranges were quite common during the late stages of the experiments. Some workers would take this as an indication that competition among phytoplankton did not occur (Harris 1986). The occurrence of competition, however, does not depend on equilibrium. Resource competition is, by definition, the depression of the reproductive rates of the competitors by exploitation of common resources (Tilman 1982). It is apparent from the data here that reproductive rates can be depressed whether they are constant or not. It is also apparent that the availability of the limiting resources (silicate and phosphorus) was depressed because of consumption by organisms.

The experiments also show algal resource competition despite the presence of an unexploited predator population. It might be argued that the physical regime (mechanical mixing) was detrimental to Daph- nia and might, therefore, have-had the same effect as exploitation. Moreover, without vertical migration zooplankton in nature could graze for 24 h d-l instead of 12. I suspect, however, that both caveats are not very powerful, because grazing rates on the most edible algae were quite high throughout the entire course of the experiments, minima being about 0.5 d-l and peaks being between 1 .O and 2.2 d-l. Such grazing rates are in the same range as the highest reported in situ rates (Haney 1973; Lampert and Taylor 1984; Jarvis 1986). The shift toward P limitation despite high activity of zooplankton is probably best explained by the fact that the late successional dominant, M. thylespora partially resisted grazing (with D. longispina as grazer, @ = 0.39kO.28; with D. magna as grazer, + = 0.3OLO. 18) and trapped an increasing part of the P in its biomass. It is noteworthy that in experiments L12, L34, L550, and M5 10 Mou- geotia became increasingly inedible with time.

To my surprise, phytoplankton succession did not proceed to algae more resistant to grazing than Mougeotia. In lakes, this category of algae is often represented by large, colonial blue-greens or large dinofla-

gellates or both (Reynolds 1984). Their failure cannot be explained by absence from the species pool, because occasionally a few individuals of Ceratium hirundinella, Aphanizomenon flos-aquae, and Anabaena flos-aquae have been found in the samples. It may be that the common late successional dominance of those algae in stratified lakes is not only due to their grazing resistance but also to their vertical motility, a trait which has no advantage in well-mixed cultures. Moreover, mechanical stress by ar- tificial turbulence might have handicapped those algae that are characteristic in low turbulence situations in stably stratified bodies of water. Carpenter et al. (1987) reported that large dinoflagellates (Peridinium) generally do poorly in experimental enclosures and can be damaged by Daphnia feeding without being ingested. The only highly grazing-resistant alga that reached count- able population densities in the experiments was S. schroeteri. It was a particularly poor competitor for P. Among all species inves- tigated it was most strongly P limited (mean IL = 0.86) and on most occasions (> 80%) had the lowest reproductive rate (mean p = O.l5d-‘,p.,,,= 1.05 d-l). Thus, its excellent grazing resistance could not compensate for its poor performance in competition.

The expected deterioration of Si : P supply rate ratios by differential recycling did take place but not always in the form of a continuous downward trend. In all experiments except M 18, Si : P supply rate ratios were considerably smaller than the initial ratios of the medium (Fig. 8). This tendency was especially apparent in the two experiments with the high initial ratios. In experiment L550 it declined to 8, in experiment M5 10 to 85 by day .78. The slight increase of Si : P ratios toward the end of experiments L12 and L30 can be explained by dissolution from diatom debris in a period when diatoms were already too rare to take up the released silicate. A similar behavior has been found in a model simulation of silicate-diatom interaction where Si uptake, Si-limited growth of diatoms, diatom mortality, and dissolution of diatom debris had been entered (Baumert 1979). In a stratified lake, however, diatom debris would have

1052 Sommer

t-4 1 Ly

0.75

0.5

0.25

0 I 0 1 5 time tag, weeks

1 s io 50 100 500 1000 Si : P ratio

Fig. 9. Left-dependence of r2 of the log percent diatoms vs. log Si: P ratio regression on the time lag. Right-percent contribution of diatoms to total biomass vs. Si: P supply ratio. Comparison between the experiments without zooplankton by Sommer (1985, chemostat, pulsed supply of P, and pulsed supply of P and Si) with the experiments of this study (with grazers, regression with a time lag of 2 weeks).

been lost from the epilimnion by sedimentation. Only vertical mixing would have increased Si : P ratios again.

In multispecies competition experiments (Smith and Kalff 1983; Sommer 1983,1985; Kilham 1986; Tilman et al. 1986), the relative importance of diatoms always showed a strong positive correlation with Si : P supply ratios. These results serve as a standard for comparison to examine the extent to which the influence of zooplankton has tilt- ed the balance of competition. I used my own experiments -for quantitative compar- isons because they had been performed at the same temperature (18°C) and in relatively large reactors (20 liters); the relative importance of algal taxa had also been expressed as percent contribution to total bio- ‘mass; and although the inoculum was taken from a different lake (Lake Constance), they had many important species in common. Rhizochrysis sp. was the only important species in the phytoplankton-zooplankton experiments that had not been observed in the competition experiments.

Those competition experiments consisted of three series. The first were classic chemostat competition experiments (Sommer 1983). In the second series there was a continuous throughflow, but one nutrient (phosphate) was added only once per week in discrete pulses (pulsed P). In the third series, throughflow was again continuous,

but two nutrients were added in a pulsed mode (pulsed P and Si). One of the major results was that the transition to diatom dominance over green algae was shifted to higher Si : P ratios by fluctuating nutrient conditions (Sommer 1985). Mougeotia thy- Zespora especially profited from that change. In the chemostat experiments it was the only persisting species at the lowest Si : P ratio (4 : 1) and was excluded at higher ones. In the pulsed experiments it contributed > 50% to total biomass at all Si : P ratios up to 40 : 1 and persisted in significant amounts even at the highest ratios (280: 1).

In order to make the dependence of phytoplankton composition on resource ratios comparable between the competition experiments and the phytoplankton-zooplankton experiments, one must consider the unsteady character of the latter. Under such conditions, time lags between resource supply ratios and the response in species composition must be considered. If, for ex- ample, high Si : P ratios shift the competitive advantage toward diatoms, they will start to increase and, therefore, bind an increasing amount of silicate in their biomass. When diatoms reach their maximal dominance, Si : P ratios will have already dete- riorated. To account for that effect, I performed regression analysis of percent diatoms on Si : P ratios with various time lags (Fig. 9). Among the four regression


models tried (linear-linear, log-linear, linear-log, log-log), the log-log model with a time lag of 2 weeks had the best fit. The regression equation was ln(% diatoms,+,) = -2.43 + 1 .Ol ln(Si : P),; r2 = 0.53; n = 60. I consider it noteworthy that the time lag of 2 weeks is about the same as the time’ shift between maximal Si : P ratios (dissolved concentrations) and maximal diatom dominance in both Lake Constance and in Schohsee.

Comparison of this equation with the results of both the chemostat and of the pulsed nutrient experiments (Fig. 9) shows that in the presence of grazers diatoms need higher Si : P ratios to become dominant. Differ- ences in grazing resistance probably cannot be invoked as explanations because one of the diatoms, A. formosa, was about as resistant as M. thylespora (Fig. 5). Asterionella is known as a good competitor for P, and in experiment M5 10 Si : P ratios never fell much below its optimum of about 90 (Til- man 1977). Alternatively, Mougeotia might have profited from the nutrient supply mode (macroscale fluctuations and micropatchi- ncss in the dark reactor) or from the spe- ciation of P. Note that in the competition experiments all P was orthophosphate, whereas here some part of the SRP might have been unavailable, and some of the nonreactive soluble P might have been available-possibly with important interspecific differences.

In conclusion, in the experiments reported here the presence of an unexploited grazer population (0. longispina or D. magna) did not prevent the occurrence of resource competition between algae. Moreover, grazing did not result in the dominance of an algal species that had not been reported as a successful competitor before. Grazing did, however, influence the outcome of competition by shifting resource ratios. In addition, diatoms needed higher Si : P ratios to become dominant in the presence of grazers than they needed in their absence. With- in the bottom-up vs. top-down controversy my experiments support an intermediate point of view. Predation tilts the balance of competition. It is conceivable, however, that other experimental conditions might have yielded quite different conclusions. Besides

24 h d-l of grazing instead of 12 h d-l, the use of a multispecies grazer community would be of great interest.

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1054 Sommer

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Submitted: 13 August 1987 Accepted: 22 March 1988

Revised: 3 June 1988

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Limnol. Oceanogr., 33(5), 1988, 1037-1054 0 1988, by the ... · 0 1988, by the American Society of Limnology and Oceanography, Inc. Phytoplankton succession in microcosm experiments