Phosphorus excretion by zooplankton

PIIOSPIIORUS EXCRETION BY ZOOPLANKTON

Barry T. Haqyme’ and Glen H. Geed Dcpartmcnt of Biology, Dalhousie University, Halifax, Nova Scotia

ABSTRACT

The cxcrction of dissolved inorganic and organic phosphorus by scvcrnl species of marinc crustaceans and a planktonic rotifer was measured under laboratory conditions. The rate of excretion decrcascd as bacterial activity and duration of cxperimcnts increasctl and was directly related to tempcraturc and salinity. Excretion rates were higher in early evening than at other times of day.

The claily phosphorus r&miremcnts of the phytoplankton, calculated from 14C mcasurcd rates of production and an assunrcd C : P ratio of 40 : 1, were compared with phosphorus released by zooplankton. The rates of excretion and the abundance of zooplankton were used to calculate an average daily adclition of inorganic phosphorus to the photic zone. Jn Bras d’Or Lake, zooplankton released twice the average daily phytoplankton phosphorus requirement; in Morrison’s Pond, only one-fifth was supplied by animal excretion. Micro- zooplankton excretion (not considered in this study) may explain the discrepancy between phytoplankton rcquiremcnts and rcgencrntion rate in Morrison’s Pond. Phosphorus supplied from the hypolimnion by eddy diEfusion in Bras d’Or Lake was one-tenth that rc- generated by the-zooplankton- -

In Bras d’Or Lake and Morrison’s Pond, Nova Scotia, enrichment cxpcriments using various inorganic salts showed that phos- phatc led to the most pronounced increase in algal growth and may have been present in limiting concentrations (Hargravc 1965). Phosphorus concentrations were low and relatively constant throughout summer, so a rapid mechanism of regeneration must be operating. This study evaluates the cxcrction of inorganic phosphorus by zooplankton as a rcgcnerative mechanism.

In recent years scvcral workers have demonstrated the cxcrction of inorganic phosphorus (Pomeroy, Mathews, and Min 1963; Johannes 1964c) and nitrogen (Harris 1959) by zooplankton. Barlow and Bishop (1965) mcasurcd the excretion of phosphorus by zooplankton in Cayuga Lake and concluded that the amount would meet phytoplankton requirements. WC have mcasurcd excretion in controlled laboratory cxpcriments and have cvaluatcd the cffccts of various cxperimen tal and cnvironmcntal paramctcrs on excretion rate. --

L F’rescnt address: Department of Zoology, Uni- vcrsity of British Columbia, Vancouver 8, B.C.

2 E’rcsent address : Department of Biological Sciences, Simon Fraser University, Burnaby 2, B.C.

This study was conducted in Bras d’Or Lake and adjacent Morrison’s Pond on Cape Brcton Island, Nova Scotia; carlicr work provided information on the rate of algal photosynthesis, nutrient concentrations, and zooplankton abundance (Geen 1965; Gecn and Hargravc 1966; Hargrave 1965).

This work was conducted at Dalhousie University, IIalifax, Nova Scotia, and sup- ported by a National Rcscarch Council studentship held by BII. and by a National Research Council grant-in-aid of research held by Drs. K. E. von Maltzahn and G. A. Riley. Grateful acknowledgments arc cx- tended to M. Muhammad, D. J. MacDonald, and E. Christiansen for assistance in the field. Drs. D. II. Chitty and P. A. Larkin rcviewcd the manuscript.

MATERIALS AND METHODS

To determine the rate of excretion of dissolved organic (DOP) and inorganic (DIP) phosphorus, WC used planktonic copepods from Bras d’Or Lake and adjacent brackish Morrison’s Pond. Bras d’Or Lake, an cncloscd arm of the Atlantic Ocean, is connected to the ocean by three channels and has surface salinities ranging Erom 20- 25%. Morrison’s Pond is separated Erom Bras d’Or Lake by a narrow gravel beach.

332

ZOOPLANKTON PIIOSl?IIORUS EXCRETION 333

Salinities ranged from 5% at the surface to 23% at the bottom (4.5 m ) during summer 1965. Further details of the study area arc :rcportcd by Geen ( 1965).

The copepods Pseudocalanus minutus :Kr@ycr, Temora longicorn.is Miiller, and Qithona similis Claus were obtained from Bras d’Or Lake with a 0.3-m-diam NO. 10 nylon net towed slowly for brief periods at cl Id to 10 XL Acartia towa Dana was col- l&ted with a No. 2, 6, or 10 net in Morri- son’s Pond at 2 m. Asplanch,na sp., a common rotifer in Morrison’s Pond, was taken I+om surface waters with a No. 10 net. ,$ftcr collection the zooplankton were trans- I&red to a 2-liter dark-glass bottle; water from the sampling depth was added to pre- 1Jcnt overcrowding. Samples were main- taincd at in situ tcmpcraturcs until the cxpcrimcnts. Benthic crustaceans ,$Vysis c~mericanus, Crangon septumspinosus, and Gammal-us oceanicus) were collected from the littoral areas of a shallow bay.

Samples were usually collected bctwccn 0800 and 1000 hours, and cxperimcnts com- menced within an hour. Water obtained from the depth at which the animals were collected was strained through a 35p-pore- diam net into tight 275-ml black-taped bottles. This proccdurc removed most of the zooplankton but did not affect the phytoplankton population (primarily flag- cIlatcs < 15 p in max dimension). Active snimals were added to four or more bottles --the remaining containers acting as con- trols. In experiments with benthic sp&es, single animals were placed in cxpcrimental 1)ottlcs. Antibiotics at a concentration of 50 mg/liter of p cnicillin G and 100 mg/ liter of streptomycin sulfate were added to some of the expcrimcntal and control hot- ties to rcducc bacterial uptake of the cx- creted phosphorus. The effectivcncss of this procedure, which inhibited bacterial activity for up to 12 hr, was evaluated by plating 1 ml of sample on ZoBell’s 2216 nutrient medium and counting colonies after 18-24-hr incubation at 18C. We measured zooplankton respiration and uptake of 14C by the flagellated phytoplankton in four cxperimcnts; these rates were

not significantly changed by the addition of antibiotics.

During experiments with plankton, bot- tics wcrc rotated at 0.25, rpm in a constant tcmperaturc water bath; this rate maintained plankton homogeneity. After counting the animals in each bottle at the end of the experiment, we dctcrmined excretion by comparing phosphorus concentrations in the sample and control bottles.

A second method used to detcrminc phosphorus excretion was to follow changes in body phosphorus during extended pc- riods of starvation. A 5-liter sample of membrane-filtered water containing 500 copepods was maintained at in situ tem- pcrature for up to four days. Antibiotics were added at the beginning of the expcri- mcnt and at 12-hr intervals thcrcafter .to limit bacterial growth. Periodically lo-20 animals were rcmovcd, rinsed with distilled water and transfcrrcd to a beaker for total phosphorus determinations. At the same time, a 3OO-ml sample of the water that had contained the starved animals was mcmbranc filtcrcd and analyzed for dissolved inorganic and total phosphorus.

We have assumed that the increase in DIP and DOP we measured was due to the excretory activity of the planktonic animals. It is possible that epizoic bacteria break down organic compounds, and also that DIP or DOP is leached out of fecal pcllcts, relcascd from partially digested food, or produced by the action of enzymes present in water. No attempt has been made to distinguish true excretion from these methods of phosphorus rclcase.

Total phosphorus and dissolved inorganic phosphorus wcrc determined as dc- scribed by Strickland and Parsons ( 1965). Our terms DIP and DOP are equivalent to their terms SRP and SUP, Since DIP was higher in unfiltered than filtcrcd water, probably owing to charring of particulate matter, all samples were passed through prerinscd 47-mm-diam HA Millipore filters before DIP analysis. Dissolved organic phosphorus was considered to bc the dif- ference bctwecn total phosphorus and DTP, since all particulate matter had been rc-

334 BARRY T. HARGRAVE AND GLEN H. GEEN

TABLE 1. Average rates of DIP and DOP excretion (,ug-at. x 10d6 animal-’ day-l) and standard deviations (6) for Zahomtory experiments with and without antibiotics. Ratios of DOP excretion to total excretion are expressed as percentages. The average density of animals was 750/liter. Feeding was possible;

temperature ranged from lci-19C. C ZZ-C VZ indicates the copepodite stage

Species DIP

+ Antibiotics - Antibiotics

DOP DOP %--

6 DOP %--

8 DIP & DOP DIP 6 DOP 8 DIP & DOP

Oithona 12.2 1.4 35.5 13.3 74.4 4.0 3.1 7.9 8.2 66.2 similis C V

Acartia tonsa

nauplii 9.3 4.1 - iii - 4.2 1.3 - c II - C IV 16.5 6.2 35.6 68.3 6.0 3.1 G 3; 60.8 cv-CVI 26.1 14.1 51.9 16.3 66.5 15.0 2.8 11.0 5.5 42.5

Pseudocalanus minutus

nauplii 4.6 1::; - - - 1.8 0.9 - - - CIV-CVI 46.6 93.4 66.8 66.8 30.6 8.0 12.3 4.8 28.7

moved by filtration, We found, as did Rigler ( 1964), that the amount of DOP decreased with pore size of the membrane filter. Evidently no clear distinction exists between particulate and dissolved phosphorus components.

The molybdenum blue method may rc- suit in acid hydrolysis of some DOP compounds. Rigler (1966) suggested that such hydrolysis might contribute to a substantial overestimate of DIP concentration. How- ever, we have measured excretion by comparing the concentration of phosphorus in control and experimental vessels; any analytical errors will be similar for both dcter- minations. At most we have overestimated the excretion of DIP relative to DOP, but the total dissolved phosphorus released is not altered.

RESULTS

Effect of bacterial activity

Table 1 summarizes the rates of excretion by zooplankton in the presence and absence of antibiotics. In all three species, measured release of DIP and DOP was higher when bacterial activity was reduced. According to Johannes ( 1964a), bacteria removed both DIP and DOP from solution although little of the DOP assimilated was regenerated. If the DOP released is CX-

pressed as a percentage of the total dissolved phosphorus excreted (Table l), it is significantly lower (p < 0.05) when bacteria are present, suggesting a selective uptake of DOP by bacteria.

The rate of excretion decreased as the experimental period increased, regardless of whether antibiotics were used. Highest rates were always recorded in experiments of less than 6-hr duration (Fig. 1). Early in experiments, measured excretion was higher in bottles with antibiotics but later, possibly as the effect of the antibiotics wore off, rates were frequently lower. Sim- ilar trends were reported by Johannes (1964b). Factors other than bacterial activity may contribute to the time-dependent decrease in excretion rate. As shown later, excretion is directly related to food intake, which declines with time in bottle experiments (Mullin 1963; Hargrave 1965). Ob- served changes in excretion may be primarily a function of decline in feeding rate.

Effect of density

Excretion decreased at zooplankton densities greater than 400 per liter (Fig. 2). This trend was apparent in all planktonic species, with and without antibiotics added, an d may have been due to physical inter- fcrcnce at high densities, social effects, or

ZOOPLANKTON PIIOSPIIORUS EXCRETION 335

Antibiotics added

I I 6 12 18 24

No antibiotics

I2 18 24

Experimental duration (hrs 1

FIG. 1. Relative rate of DIP excretion by Acmtin tona copcpoditcs (primarily Stage V). Upper histogram : 50 mg/liter of penicillin G and I00 mg/liter streptomycin sulfate per bottle added. Lower histogram: no antibiotics added. Each bar represents the average of three experiments; 650- 750 copepods per liter; temperature 1%20C. FIG. 2. Excretion rate of DIP as a percentage

of the maximum (80 yg-at. DIP copepod-l day” x 10e6), and standard deviations, with varied num- bcrs of Acmth tonsa Stage V copepodites. Dura- tion 8 hr, temperature lS-21C; feeding always possible; antibiotics added to half the bottles.

= Antibiotics

l No antibiotics

T 8 1 T 8 T T[ 8 8 1 4 1

250 350 500 1000 Number of copepods / liter

2000

accumulation of excretory products. Or fcod intake, and hence excretion, might bc rcduccd under crowded conditions because of a reduction in food supply and rcfiltra- tion of the same water.

These laboratory experiments nccessi- tated crowding to an average of 750 copepods per liter to increase the changes being measured; extrapolation of the rates of excretion to nature requires a correction for the differences in animal numbers. Zoo- plankton densities in the photic zone of Bras d’Or Lake seldom exceeded an average of 100 animals per liter, including all species and developmental stages. In Mor- rison’s Pond, A. tonsa reached 150-200 animals per liter. The results shown in Fig. 2 suggest that laboratory excretion rates should bc doubled to account for density differcnccs between field and laboratory.

Sample agitation to prevent settling 0E animals during experiments increased cx- cretion. In five experiments with P. minutus and 2’. hgicods, half the bottles were rotated and the rest left unstirred in the water bath for 9 hr. Numbers of copepods were approximately the same in all experiments. There was a noticcablc conccntra- tion of animals in the lower half of the unstirred jars, whereas animals were well dis- tributed throughout stirred bottles. Mean excretion rate in stirred samples (41.0 -F 8.5 pg-at. DIP copepod-l day-l X lo-‘)) was significantly higher (p < 0.05) than in unstirred samples (23.3 +- 7.1 pg-at. DIP copepod-’ day-l x W5).

336 BARRY T. IIARCRAVE AND GLEN II. GEEN

6am noon 6pm midnight 6am

Mean of experimental period (hr)

Frc. 3. Excretion rate of DIP as n percentage of the maximum, and standard deviation, in a series of 6-8-hr experiments with Aca&n tonsa Stage V copepodites. All copepods collected at 1000 hours and held in the dark at 18-22C (in situ temp) until the cxperimcnt began. The points are plotted at the midpoint of the experimental period; 700-000 copepods per liter; antibiotics always added.

Time of clay

A. tonsa copepodites were used in lah- oratory experiments to assess effects of time oF day on excretion (Fig. 3). Increased excretion was shown during early evening hours when the feeding rate in A. tonsa increases ( IIargravc 1965) and animals arc migrating toward the surface.

Salinity

The results summarized in Fig. 4 show a direct relationship between salinity and cxcrction, suggesting that DIP excretion is in part governed by the osmotic pressure of the medium; this was also suggested by Kgler (1961). A. tonsa, the principal copc- pod. in Morrison’s Pond, regularly migrates through lavers of markedly differing salin-

1

5 IO 15 20 25

Salinity %o

FIG. 4. Rate of DIP excretion by Acnriin tonsa copepodites as a function of salinity. Vertical lines represent one standard deviation on either side of the mean. Copepods were held in Morrison’s Pond water, previously membrane-filtered (0.45-p pore) and diluted with distilled water. Antibiotics always added to bottles with 500-700 copepods per liter; ls-22c.

ities. Excretion would be reduced by more than 50% in the low salinity surface water. In contrast, excretion by the more steno- haline copepods from Bras d’Or Lake was the same over a range of salinities above the lower lethal level.

Temperature

An increase in DIP excretion with tem- pcrature by A. tonsa was apparent (Fig. 5). Marshall and Orr ( 1961) found a positive relationship hctwccn temperature and rate of excretion in CaTanus at 5, 10, and 15C.

In Morrison’s Pond the rate of excretion might be doubled when the plankters move into the warmer surface layers at night. On the other hand, low surface salinity would tend to lower the rate.

Food supply

According to Corner (1961), excretion is a function of both quantity and quality of food, That excretion is related to food in-

ZOOPLANKTON l’l3OSPIIORUS EXCRETION

I I 8 I

IO 15 20 25

Temperature (“C )

FIG. rj. Rate of DIP excretion by Acmtin tonsa copepodites as a function of tempcrnture. Expcri- ments 8-12 hr long, after 4-5 hr equilibration at the test tcmpcrature. Antibiotics always used; 800- 1,000 copepods per liter. Vertical lines rcprescnt one standard deviation on either side of a mean o F five cxpcrimen ts.

trtkc is evident from Table 2. Animals in filtered water may have taken in some food in the form of organic aggregates, which we found were formed as plaquclikc par- ti’cles up to 10-p diameter in the filtrate, Apparently this was associated with foam- ing in the flask, as particle formation was eliminated when the water was filtered by gravity. Excretion was lower in the particle-free water than in water thought to contain aggregates (Table 2).

Fig. 6 illustrates the results of a 4%hr cxpcriment in which we compared changes in total body phosphorus with excretion of DIP and DOP. After one day of starvation, body phosphorus had declined considcr- ably to a level that remained relatively co:ns tant thereafter. During the initial 6

.0035 I I r-- I-I 0 IO 20 30 40 5 0

Hours of starvation

FIG,. 6. Change with time of total body phos-

.65

.55 p (D ij. 0

.45; * I s

.35 E "7

: .25 Q

-. ;a' -I

.I5

.05

phorus of Acn~+tin tonsa copcpoditcs, held in mcmbranc-filtered (0.45-p pore) water. Changes in D0P and DIP in the medium arc also clepictcd. Experiments conductecl at 18-2OC; antibiotics always added; approximately 100 copepods per liter.

hr, an increase in body phosphorus and a corresponding dccrcase in DIP and DOP was recorded. This may bc due to the in- gestion of aggregates-the only particulate matter of any consequence. Alternatively, cpizoic or intestinal bacteria might have been converting dissolved phosphorus into a particulate form, which would be measured as an increase in zooplankton body phosphorus. Unless the antibiotics used during these cxpcrimcnts arc less effcctivc against thcsc than against free-living bac- tcria, this latter suggestion seems unlikely,

Phosphorus released during the 6-24-hr period may correspond to the labile pool postulated for Calanus by Conovcr, Mar- shall, and Orr (1959). The relatively rapid loss indicates an unbound phosphorus source, and the relatively constant level reached after 24 hr of starvation could be a measure of the stable, or assimilated, pool of body phosphorus.

There is fair agreement bctwecn the loss of body phosphorus per 100 copepods (the number per liter) and the sum of DIP and DOP added to a liter of water by cxcrction.

337

338 BARRY T. IIARGRAVE AND GLEN II. GEEN

TABLE 2. Average excretion rates (rug-at. x .ZO-” DIP copepod-l day-*) and standard deviations for experiments with and without food particles. Starved animals were held in water filtered, through a 0.45~p-pore-diam membrane filter. Other animals zoere fed on phytoplankton at the densities occurring naturally. Experiments lasted 8-12 hr. Anti- biotics were added to all samples. Differences in excretion rates between starved and fed animals

were significant in all cases (p < 0.05)

Starved Fed

Oithona similis 6.2 -t- 4.8 13.9 +- 4.8 Pseudocalanus minutus 27.6 IL 9.7 65.5 2 14.9

19.0 & 8.9”

A Calanus x 5 2,9-

3

Aixrtia. tonsa 10.4 2 2.8 14.4 2 2.6

* Animals in this set of experiments were held in particlc- free water prepared by gravity filtration through membrnnc filters. The other starved experiments were conauctcd in water prepared by vacuum filtration.

IIowcver, a discrepancy exists in the 6-20- hr period. Measured addition of DOP and DIP during this period was 0.58 pg-at./ liter. The loss of body phosphorus by the animals contained in a liter was only 0.31 pg-at. If we assume that a high 20-hr value of DOP resulted from an analytical error, and that DOP concentration increased in a linear manner from 6-24 hr, then the total addition between 6 and 20 hr would be 0.36 pug-at. This still exceeds the total loss in body phosphorus but is probably within the limits of the analytical tech- niques.

FIG. 7. Relationship between dry weight and excretion rate for a series of marine planktonic and benthic organisms. Results of at least eight experiments of 6-8-hr duration used to derive the average v&e for each species; antibiotics always added.

Body size

controlled. Therefore, we must extrapolate from cxcrction measured in the laboratory under various conditions to estimates of cxcrction in nature.

The relationship between excretion and dry weight in seven crustaceans and a ro- t&r is presented in Fig. 7. The larger benthic species (Mysis, Gammarus, and Crangon) excreted much more phosphorus per animal than the copepods or rotifers. However, excretion per unit weight in the copepods and rotifers was substantially higher, as would be anticipated from the metabolic studies of Zeuthen (1953) and Johannes ( 1964c).

DISCUSSION

In laboratory experiments conducted in the presence of bacteria, excretion was one-third to two-thirds of that measured when bacterial activity was inhibited (Table 1). Both situations are artificial. If no antibiotics wcrc added to the experimental container, a rapid growth of bacteria on the walls of the vessel and a dis- proportionately large uptake of DIP would result. Bacteria use the excreted phosphorus, so the net addition in nature will fall between the extremes. We have arbitrarily assumed that bacterial populations in nature would reduce by one-third the rate measured in the absence of bacteria. This simply represents the average oE the two cxtrcmcs.

Previous attempts to measure the excretion rate of copepods in a column of Morri- son’s Pond water were unsuccessful he- cause a number of variables could not be _

2.1 I.0 2.0 30 4.0 5-o

Log dry weight @gLe,

ZOOPLANKTON PIIOSPHORUS EXCRETION 339

The length of the laboratory experiment also has an influence on the measured rate of excretion (Fig, l), but it is difficult to assess this in terms of excretion in nature. Bates of excretion may be abnormally high in the early part of an experiment or in short experiments. In 16-24-hr experiments bacterial activity will increase considerably and reduce measured DIP excretion. Again arbitrarily, we have assumed that rates of c,xcretion measured in 8-hr experiments represent the natural situation. The average rates measured in the laboratory are assumed to be one-third too high and appropriate corrections have been made in calculating expected excretion in nature.

WC have also had to correct for diffcr- cnces in animal densities. Laboratory excretion rates were determined at densities of approximately 750 copepods per liter. E:xcretion rates at these densities (Fig. 2) are only half those expected at the densities occurring in Bras d’Or Lake and Mor- rison’s Pond (< 150/liter).

We have not applied corrections for salinity and temperature effects. Gradients were relatively small in the lake and correction unnecessary. In the pond salinity in creased and temperature decreased with depth. The appropriate corrections would have cancelled each other.

Excretion experiments were usually conducted in the late morning and afternoon. However, excretion was substantially higher during early evening when copepods move towards the surface (Fig. 3). The average rates (Table 1) were derived mainly from daytime experiments, and the peak excretion rates of the evening hours have not been adequately considered in deriving th:is average. Best evidence suggests that the excretion rate should be increased by 30% to account for this source of error. These four corrections put our estimate of excretion rate in nature about 25% above that measured in the laboratory in the ab- sencc of bacteria. The rates in Table 1 have been corrected by this factor in calculating zooplankton contributions of DJP to the photic zone.

Evaluation of the significance of phos-

phorus excretion to primary production necessitates information on the daily phosphorus requirement of the phytoplankton in the area studied.

For our purposes, we have assmned that only DIP is available for photosynthesis. In the laboratory as much as 75% of the phosphorus excreted was DOP. The extent to which algae can use DOP directly is not clear although Overbeck ( 1962) has shown little or no uptake of DOP.

Average summer rates of primary production were approximately 300 and 600 mg of C m-2 day-1 in Bras d’Or Lake and Morrison’s Pond ( Gecn 1965). To convert these rates to a daily phosphorus requirc- ment, we must make some assumption about the C: P ratio. In the absence of any measurements of the elementary com- position of phytoplankton from these areas, we have assumed a ratio of 40: 1 by weight. This is an average value in common use,

but as Strickland (1960) has pointed out, considerable variation does occur. For example, the ratio for Chlorophyceae may bc 25 : 1. Seasonal variations also occur. Any substantial departure from the ratio we have assumed could have a considerable effect on the estimate of daily DIP required.

These estimates are also in error to the extent that the 14C method underestimates the rate of primary production. The work of Fog-g and Watt ( 1966) and others has demonstrated that even during short ex- perimcnts algae lose labeled organic compounds, and this may represent a substantial proportion of measured production, WC have not corrected for this source of error so our estimates of daily DIP required will be low. On the basis of a C: P ratio of 40: 1, we have calculated that 7.5 and 15 mg of DIP m-2 day-l are required to sup- port phytoplankton photosynthesis in Bras d’Or Lake and Morrison’s Pond,

Total DIP excreted by zooplankton in the photic zone (Tables 3 and 4) can bc obtained from their average corrected CX- cretory rate and their mean numbers, ob- taincd by averaging numbers of animals in day and night samples taken from the photic zone during summer. The amount

340 BARRY T. HARGRAVE AND GLEN I-1. GEEN

TABLE 3. Average daily excretion of DIP by planktonic copepods in Bras d’Or Lake, calculated. from corrected excretion rates determined in the labora.tory and abundance of the various developmental

stages in the Zake. Species: Pseudocalanus minutus, Temora longicornis, and Oithona similis

Stage hl”l”t:r”- i Avg dry Biomass ‘., wt l/-u) ( mg m-” )

C;$m;t;d - .

mg-l day-1 excreted

yg-at. P m-3 day-l released

Exdo~l 8

day-1

Avg mg I? excrctcd

nl+ day-l in 20-m

photic zone

Nauplii 20 3.0 60 0.049 2.94 0.09 1.8 Copepoclitcs 60 9.0 540 0.030 16.20 0.50 10.0 Adulta; 8 14.0 112 0.041 4.59, 0.14 2.8

14.6

excreted apparently exceeds the daily algal requirement in the lake and is less than that theoretically required in the pond. Since DIP does not accumulate, we can only assume that a balance between addition and utilization exists. Several explana- tions may be offered for an excretion of DIP in apparent excess of daily photosynthetic requirement. Either the C:P ratio is lower than the 40: 1 assumed in our calculations, or alternatively, photosynthesis may be substantially greater than that estimated by the 14C method. If, for example, the C : P ratio was 25 : 1 and 30% of the labeled photosynthetic product was cxcrcted by the algae-both reasonable possibilities-the daily algal requirement for DIP in Bras d’Or Lake would exceed that contributed by zooplankton. If this line of reasoning is applied to data from Morrison’s Pond, zooplankton contributions would be even lower than shown in Table 4.

The zooplankton biomass values (Tables 3 and 4) arc averages for Eivc summer

months. If the monthly changes in abundance of various developmental stages are considered, daily contributions of DIP are markedly altered. For example, in August the zooplanktcrs in Bras d’Or Lake were predominately Pseuclocdanus and Oitho~, adults and late copepodites. Calculated excretion was 9.6 mg of DIP m-2 day-‘, only slightly greater than the theoretical daily phytoplankton rcquiremcnt for the month of August.

Altemative nutrient sources Excretion of phosphorus by zooplankton

represents recycling of existing nutrients within the water column and not a mccha- nism of supply, Since DIP concentrations in adjacent coastal waters are comparable to those in Bras d’Or Lake and Morrison’s Pond, no appreciable increase in phosphorus can bc expected as a result of tidal inflow, and little increase can be expected from drain- age. At best, some enrichment could only be expected in the vicinity of river mouths.

TAHLE 4. Average daily excretion of DIP by Acartia tonsa and Asplanchna sp. in Morrison’s Pond, calculated from corrected excretion rates determined in the laboratory a.nd abundance of the various de-

velopmental stages

Avg mg P Corrected excretecl

fig-at. P /Lg-at . P zzrpee;2 m-2 day-l

stage Jytfro* -4% dry Biomass mg-1 day-1 m-:1 day-l :1 in 3-m

1 wt (l-c) ( mg in-” ) excreted released &by-’ photic ~onc

A. tonsa nauplii 50 3.0 150 0.045 6.9 0.21 0.63 A. tonsa C II-C IV 50 50 250 0.041 10.3 0.32 0.96, A. tonsa C V-C VI 25 10.0 250 0.033 8.3 0.26 0.78 Asplanchna sp. 500 0.5 250 0.060 15.0 0.46 1.38

3.75

ZOOPLANKTON PIIOSPIIORUS EXCRETION 341

#Some increase in DIP does occur at the ,surfacc of Morrison’s Pond after a heavy :rainfall and the subsequent increase in run- off. IIowever, this is an intermittent increase in the low salinity surface layer, which has a relatively low level of primary production.

Apparently the bulk of the nutrient rc- generation takes place within the bodies of water. We have presented evidence in- dicating an important role for planktonic animals in the regeneration of DIP. Some DIP will also be excreted by fish and benthic organisms. The DIP contribution of the benthic organisms is unknown but would only bc immediately available to the phytoplankton in the shallow, well- mixed regions near shore. In deeper arcas, DIP excreted by the benthic fauna will be returned to the photic zone at times of overturn or by turbulent mixing processes. The contribution of the fish is also unknown but is probably low if, as might be expected, the biomass at this terminal point in the food web is relatively small.

Turbulent mixing will also contribute to the return of DIP or other nutrients to the photic zone from the hypolimnctic region. Eddy diffusion coefficients have been calculated from several summers’ temperature data from Bras d’Or Lake. These cocffi- cicnts were used to calculate the flux of DIP into the photic zone from the hypolimnion as described by Riley ( 1956). The average contribution to the photic zone from June through August 1962, and I964 was 1.30 and 1.67 mg of P m-2 day-l respectively. This amounts to about 20% of the estimated daily phytoplankton requirement and 10% of the DIP cxcretcd by the zooplankton, Evidently zooplankton excretion is the major mechanism of nutrient rcgcncration in Bras d’Or Lake during summer months. Work on Cayuga Lake by Barlow and Bishop (1965) has led to a similar conclusion,

In Morrison’s Pond, zooplankton excretion supplies only 20% of the daily phytoplankton requirement. Return of DIP to the photic zone in this area was not Cal- culatcd bccausc of an unmcasurcd effect

of water diffusing through the gravel beach that separates the pond from the lake. At any rate, turbulent mixing was probably relatively limited.

The discrepancy bctwecn daily rcquirc- ments and regeneration may indicate the importance of the smaller zooplankton We did not determine the numbers of ciliates and Littorintc veliger larvae, although each of these was occasionally abundant. Our data on the rotifer Aspkmchna indicate the importance of these smaller forms (Table 4). The other microzooplankton may re- generate much of the DIP required by the phytoplankton. Some workers have sug- gcstcd that bacteria are important agents in the regeneration of inorganic phosphorus. In our experiments, bacteria accumulated rather than released phosphorus; this agrees with results of Johannes (1964n). But Overbcck (1962) and others have shown that bacteria do rcgencrate DIP. The relative importance of bacterial and zooplankton regeneration of DIP is not clear. Our studies have indicated that regeneration of inorganic phosphorus by zooplankton is oE considerable, if not of prime, importance in our study areas.

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Phosphorus excretion by zooplankton

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