I Int. Revueges. Hydrobiol. I 75 I 1990 1 2 I 143-151 1

B O R I S [ A . ~~TITE1,MAIEHER and ELENA 8. MAKARTSEVA

Zoological Institute of the Academy of Sciences, USSR, and Timnological Tnstitute of the Acndemy of Sciences, USSR, Leningrad

The Significance of Zooplankton in the Cycling of Phosphorus in Lakes of Different Trophic Categories

key uwds : phosphorus cycling, zooplankton, lakrs, rxcrction rate

Abstract

The species composition, number, biomass and phosphorus excretion rate (PER) of zooplankton (Crustacea and Rotatoria) in 8 mesotrophic and eutrophic lakes were studied. PER were calculated using specific expenditures on metabolism estimsted from the oxygen uptake, phosphorus content in zooplankton and field observations of number and biomass of planktonic Rotatoria and Crusta- cea. The zooplankton biomass and PER increased from mesotrophic to eutrophic lakes. The values of PER were compared with primary production and spring phosphorus concentration. The rela- tive significance of zooplankton in phosphorus cycling declined with increasing trophic category of lakrs.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143 2. StudyArea. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 144 3 . M e t h o d s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 144

3.1. Zooplankt,on sampling . . . . . . . . . . . . . . . . . . . . . . . . . . . 144 3.2. Phosphate excretion. . . . . . . . . . . . . . . . . . . . . . . . . . . . 145

4. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146 5. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 148 6. References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150

1. Introduction

Biological productivity of lakes depends on the external and internal nutrient load- ing. Relations between external phosphorus loading and primary production or chloro- phyll concentration are well known (e.g. SAKAMOTO, 1966; VOLLENWEIDER, 1968 ; DILLON & RIGLER, 1974). The internal phosphorus loading or cycling is caused by organisms through their metabolical activity. It includes excretion rates and phos- phorus requirement for growth of algae assemblages or for primary production. The number of these data for lakes with different trophy collected simultaneously and with use of the same methods are quite limited.

Crustacea and Rotatoria are the main components in the plankton conirriiinities. Therefore we attempt in this paper to estimate their significance in phosphorus cycling.

144 B. L. GUTELMAKIIER and E. S. MAKARTSEVA

2 . Study Area

The investigations were carried out on 8 lakes. The lakes are located within 1-3 knl of each other in the Latvian region a t 56O30' N, 27'30' E. Intensive agriculture is a typi- cal feature of the region, where 80 O/" of the same is ploughed. The lakes have a small surface area (6-19 ha), only two of them are relatively deep with a maximuni depth of 26 and 14 in respcctively (Table i).

Table 1. Morphornetric characteristicsof lakesand their Carlson'strophic state indices (IC?d* - chlorophyll index, ISD* - transparency index) (TRIE'ONOVA, 1986)

Lake Surface Depth, m lChl ISL) area, rntbximum mean ha

Raltas 15 14.0 3.8 42 43 Udrinka 19 26.0 7.8 43 46

llzes 12 5 . 4 2.4 49 52 Gridzanskoe 15 7.0 4.5 55 56 Rudushskoe 6 8.2 4.2 56 51 Zahordzskor 9 4.0 2.6 62 63 Kazi mir ovskoe 8 3.8 1.7 60 65

* lChZ = 10 [6 - (2.04 - 0.68 InChl) : In21

Zapiytis 13 3.5 1.8 44 51

ISU = 10 [G - (InSD : ln2)], where Ch1 is chlorophyll in mg m-.', ATD is transparency in m.

The level of productivity of the lakes was characterized by primary production values and Cnrlson's trophic state indices which were calculated on the basis of chloro- phyll content and water transparency. The values and indices denionstrated that four of the lakes were mesotrophic and the others eutrophic with a primary production of 87-149 and 230-367 g C 111-2 year-1, respectively; the indices were 42-52 and 51-65 (Table 1).

The shallow snii~ll lake Kazirrrirovskoe was overgrown by niacrophytes especially in the second half of the summer. These peculiarities indimte the transition to a hyper- eutrophic stage.!

3. Methods

3.1. Zooplankton sampling

Zooplankton samples were collected on the deepest parts of t'he lakes by vertical httuls through the water column wit'li a 110 pm-mesh Juday net and preserved with formaline. This was done to identify Crustacea and big Rotatoria species and to det,ermine their abundance. For the identifi- cation and counting of small Rotatoria, 1 1 samples were collected with a bathometer, preserved with formaline and subjected to sedimentation. Zooplankton lengths were subsequently converted to volumes and wet mames with empirical equations by BALUSHKINA and WINRERG (1979). Accord- ing to the temperature stratification, samples were collected from 1 or from 3 layers. Zoopankt'on and various biological, physical and chemical properties were monitored in each lake at, 10 days intervals between April and October and monthly in the other parts from 1982 to 1984.

Zooplankton in the Cycling of Phosphorus 145

3.2. Phosphate excretion

lndividual excretion rates as well as other experimental values are not always actual values, because they depend on many different factors. Therefore i t is necessary to ascertain a general pattern, set up by comparison of phosphorus and daily energy losses that, have been studied quite sufficiently.

GUTELMAKHER (1983) summarized PE'R by freshwater and marine Crustacea in relation to their body masses. All data from available literature and own experimental data (GUTELMAEHER, 1977) were used for statistical treatment, based on the least- squares method (UMNOV, 1976). The following exponential equation was obtained :

where E is PER in pg P * ind-1. day-1, W is the dry mass in ing . ind-1. Before ste- tistical treatment, all data were converted to 20" using Qi0=2,3 (WINBERG, 1983).

Siniultaneously with summarizing of P E R data of the phosphorus content in Crustacea dry mass were collected. Different species of niarine and fresh-water animals had similar phosphorus levels which ranged mostly from 1.0 to 1.5 0,b (GUTELMAKHEH, 1983).

For the calculation of energetic losses SUSHCIIENYA'S (1972) equation was used. This has been obtained by summarizing 2284 experimental data on oxygen uptake froin different species of Crustacea:

where R is oxygen uptake in m l 0 , - ind-i * h-I, W is the wet mass in g. The tenipera- ture is 20 OC. It was suggested that 1 ml oxygen =4.86 cal and 1 mg of dry niass of Crustacea is equal to 5.5 cal. The nietabolisin losses estimated from the P E R and oxygen uptake were practically the same when the animals had the abovementioned phosphorus and energy contents in their bodies (Fig. 1).

R=1.047 WO.801, (n=129, r=0.911) (1)

R = 0.125 W0.7j9, (2)

I I

0.01 0 .I 1 10 W,mg

Figure 1. Relationship between cxpenditurc for metabolism (yo) and dry mass of Crustaceans (tr) cdculated from the oxygen uptake rate, assuming 5.0 (1) and 5.5 (2) cal * mg-1 and from PER,

assuming 1.0 (3) and 1.5 (4) yo phosphorus in dry matter.

It is known that for the oxldation of organic matter, in which the atomic ratio of C : N : P = 106 : I6 : 1, 276 atonis of oxygen are used or 142 units of oxygen mass are needed (REDFIELD ot ul., 1963; RICHARDS, 1965). It iseasy to calculate (1,2) that an animal with a dry iiiass equal to 1 rng or with a wet mass of 10 ing has a daily oxygen uptake of 91 pl iiid-1 or 130 pg 0 * ind-land excretes 1 pg P ind-I. There is a strilr- ing similarity between theoretical calculations and data obtained from equations (1,2) based on experjniental data.

146 B. L. GUTELMAKIIER and E. S. MAKARTSEVA

The present comparison of phosphorus and energetic losses indicates that w e can calculate these two kinds of losses using equations (1,Z) and phosphorus or energy contents in the animal bodies, too, since the oxygen uptake has been investigated better than PER.

For our specific aini we have used the following equations with oxygen uptake ( R ) and body mass ( W )

for Rotatoria R =0.0753 F 0 . m (GALKOVSKAYA, 1980) for Cladocera li =0.143 Wo.8oJ (SUSHCHENYA, 1972) for Copepoda 11 = 0.200 WO.777 (SUSHCHENYA, 1972)

(3) (4) ( 5 )

The units and temperature are the same as in ( 2 ) . The energy content in animal bodies is 0.55 cal * ing wet i r i a s s ~ ~ except Asplanohnu

and Leptodora. Their bodies contain 0.20 eal nig wet mass-1 because the proportion of dry to wet mass is three times less (BOTTRELL et al., 1976). Percent cornposition of phosphorus as dry body mass is nearly equal for Rotatoria (1 and for Crustacea 1.5 ‘’,’o.

Using the ;tl.)ovenientioned equations (3,4,5) and assumptions, we have calculated PER for each species of zooplankton in each observation period. Calculations for spe- cies with different body masses of individuals (naupli, copepodids, males, females) have been separately carried out. All data were related to water temperature using Qlo = 2.3. All obtained data were divided into two periods: open water of the lake from May to October (180 days) and ice-covered water from December to March (120 days).

4. Results

In lake zooplankton conimunities 106 species were identified, more than half of them were Rotatoria. There were only I0 species common for all lakes: Polyarthra dolychoptera IDELSON, Asplanchna priodontn GOSSE, Keratella eneldearis (Gosss), K. quadrata (MULLEX.), Sida orystallina (MULLER), Diaphanosowia brachhyururn (LIEVIN), Daphnia cucullata SARS, Scapholeberis mucronata (MULLER), Leptodora kindtii (FOSKE), Mesocyclops kuckarti CLAUS. The SBRENSEN’S similarity index ( SPIREMEN, 1948) showed the composition peculiarities well. It ranged from 0.50 to 0.76 for mesotrophic and from 0.52 to 0.80 for eutrophic lakes. The species cornposition was very different in lakes of various trophic categories. For example, the SBRENSEN’S index value was the lowest when we compared the species lists for lakes Baltas and Kazimirovskoe (Table 2).

Table 2. 2G

a f b TheSBRENSEN’Ssiniilarityindicesinlakes(J). J=-, a and b - the nuniber

of species in communities A and B, e - the number of common species

Lake Bal- Udrin- Ilzes Zepiy- Grin- Rudu- tas ka tis zan- shskoe

skoe

- - - - Udrinka 0.60 - Ilzes 0.52 0.64 - Zapiytis 0.50 0.60 0.76 - - - Gridzanskoe 0.48 0.62 0.70 0.78 - - Rudushskoe 0.44 0.60 0.66 0.74 0.80 - Zabordzskoe 0.42 0.62 0.70 0.76 0.74 0.80 Kazimirovskoe 0.36 0.40 0.50 0.54 0.56 0.58

- - -

Ze- Kazimi- bord- rovskoe zskoe

Zooplankton in the Cycling of Phosphorus 147

Crustaceans were dominant species in the bioniass of ritesotrophic lakes, especially Eudiuptomus gruciloides, Mesocyclops oithonoides, Duphnia cucullata, Diaphanosoma bruchyurum, Bosniina longirostris. From May to October zooplankton biomass was small in mesotrophic: lakes and increased in eutrophic ones from 0.54 to 3.32 g . i x1 -J .

It was small in hypereutrophic lakes too. During the other part of the year, bioniass in the lakes decreased to 0.01-0.30 g * ni-J (Table 3). Zooplankton seasonal dynairiics had one peak in mesotrophic and two peaks in eutrophic lakes (Figs. 2,3). The main part of iriesotrophic lake bioniasses consisted of Crustaceans contrary to the eutrophic ones, where Rotatoria were the dominating species.

Our estiniations show that in summer, when biomasses reached a niaxiniurn, PEHs reached a rnaxiniiini, too, i.0. up to 4.8 mg I’ . m-J - d-1 in Zabordskoe lake a t the end of August. The maxiniurn values were 2-4 timcs smaller in the other lakes. Zooplank- ton cxcreted from 124 to 898 mg P * ni-2 during the open water period (Table 3). In t,he icwcovered period excretion rates were comparatively small and equaled 1-21 rrig P * ni-2.

Table 3 . Priiriary production during theopen-water period (PP, g C .ni-2, TRIFONOVA, 1986), zooplankton biomass (B, g * n - 3 ) , P E R during open-water and ice-covered periods (mg P * 111-2) and spring phosphorus (P, nig .111-3, KULISHEVA and STRAVIN-

SKAYA, 1988)

Open-water period Ice-covered period

PP B PER P B P E A - Lake

Baltas Udrinka Zapiytis Ilzes Gridzmskoe Rudushskoo Zabordzskoe Kszimirovskoe

94 130 68

102 195 215 326 270

0.54 396 0.68 640 2.42 579 1.44 653 2.95 485 2.36 898 3.32 688 0.68 124

PER--- B -

18 0.30 30 0.05 2 9 0.28 19 0.02 72 0.30 88 0.09 73 0.01 - -

PER, mg P.m-3day-l

2

1

21.1 6.0 7.2 2.0

15.6 9.4 1.0 -

Apr May Jun J u l Aug Sep Oct

Figure 2. Seasonal dynamics of zooplankton bioniass (B) and PER in lake Baltas.

148 B. 1,. GIJTELMAKHER and E. S. MAKARTSEVA

PER, rng Ern-3day-'

4

2

4pr May Jun Jul Aug Sep Oct

Figure 3. Seasonal dynamics of zooplankton biomass (B) and PER in lake Gridzanskoe.

According to equations (3,4,5) the individual niass of animals changes by D factor of 10, the PER per unit of zooplankton hionlass changes only by a factor of almost 1.6. We observed this situation when either small Rotatoria or big Crustacea dominated in the biornass. In spite of the fact that specific PEH of Rotatoria was higher than that of Crustacea, the share of Rotatoria in total PER was small. It ranged from 6.0 to 9.9 "/o. Only in Kazimirovskoe lake it was 31 Compared to other lakes, in this lake the relative rate of Rotatoria in zooplankton bioniass was high, nearly 68 %, but in others only 15-44 o/(, during the period of investigations; the big species of genus Asplnnchna dominated.

5 . Discussion

The suggested method of estimating PER is based on the rate of nietabolisni in zooplankton arid the phosphorur content) in its dry niass. An earlier published review (GUTELMAKHER, 1983) and the application of the results in the present study convince us that our assurnptions are real. There are certainly short periods in life cycles of different zooplankton species in which the invariability of expenditures on metabolisni, estimated from the oxygen uptake and phosphorus excretion rates, cannot be remained depending on the oxidized substances (lipids, proteins, carbohydrates) and thc phos- phorus content in the dry matter of animal food. However during long periods thc mean values of these parameters correspond to normal ratio of nutrients (C : N : J? = I06 : I6 : 1). Consequently, direct siniultaneous measurings of oxygen uptake, phos- phorus and nitrogen excretion are very important. An exaniple of this kind of work has been given by JKEDA and MITCHELL (1982). They nieasured daily losses in carbon (oxygen uptake), nitrogen and phosphorus (as percent of body content of these ele- ments) in antarctic. zooplankton. Using their data only for Crustacea (Table 7 , p. 296), we have obtained daily losses in carbon, nitrogen and phosphorus of 1.46, 1.33 and 3.67 (I,',,. The coniparison of these data has shown that differences between carbon and nitrogen losses are insignificant, but between C and N on the one hand and phospho- rus on the other they are significant and bigger hy 2.6 times. This difference is so big,

Zooplankton in the Cycling of Phosphorus 148

50

because the authors digested phosphorus samples in 50 H,SO, for 1 h at nearly 100 "C. The method doesn't result in complete mineralization of organic matter (GoL- TERMAN, 1969). Therefore the mean phosphorus content in Crustacea (Table 3, p. 287) was only 0.79 and the C : P ratio was high (55 : 1 wtlwt). Usually these va- lues are 1.0-1.5 ",,, and 30-40 : 1 (wt/wt). According to these remarks the differences in specific metabolic rates, estimated from losses of nutrients, become less important.

Recently EJSMONT-KARABIN (1983) published an equation for a specific phosphorus excretion rate by planktonic rotifers in relation to their body weights. The value of exponent in their equation was -1.27, that was not obtained before. We tried to cal- culate the rate of excretion using their equation and our field data of Rotatoria num- ber and individual body inass. The calculations have shown that during summer the Rotatoria excretion was so high that it exceeded the requirenients for photosynthesis by more than one order of magnitude especially in highly eutrophic lakes. I n this case, inorganic phosphate must be accumulated in the lake water. Nevertheless we didn't obtain these values. Usually, the inorganic phosphate content was near zero. Conse- quently, experinientPl data are necessary to compare different field investigations.

First of allwe have chosen two criteria for validating our calculations of zooplankton phosphorus excretion rates: plankton primary production and inorganic phosphate a t the end of the ice-covered period. For the cornparison of primary production and PEB we have rnultiplied this value by 40, taking into account that in phytoplankton the mean C : P ratio (wtlwt) is about 40. Thus, the values of primary production (P,) that can be obtained from zooplankton-excreted phosphorus ranged from 5.0 to 35.9 g C . r u - 2 during the open-water period. Using the data of P, and the primary prodiic- tion (P) in the lakes we obtained the equation:

Pe=8.5 P0.29 (n=l6, r=0.53) (6) where P, and P were measured in g C * 111-2 during the open-water period (Fig. 4).

The range of Pis small, which enables us to discuss the trends of variations in P and Pe in lakes of different trophic categories. It is important that the correlation coeffi-

-

10

5 I I I I I

50 100 200 500 tg P

Figure 4. Relationship betmccn P, and P during open-water period in g C . m-2. The explanations are given in the text.

150 B. L. GUTELMAKHER and E. S. RIAKARTSXVA

cient is positive and the exponent is less than 1 ; but for the specific values ( l ’ , / l ’ ) the exponent is negative -0.71. According to equation (6) the specific values of P, de- crease with increasing P. For example, in the less productive lake Zapiytis the ratio P,lP is the highest (34 ole), andin the highlyproductive lake Zahordzskoe only 8 0, ,). An extremely low ratio ( 2 o,;,) was obtained in the shallow lake Kaziniirovskoe with iiiacro- phyt.es.

Uuring winf,er, i n iriost lakes the zooplankt,on-miiieralized phosphorus amounted to 10-25 (I;;, cwtrrpared with the concentration of t’his element in spring. Only in lake Baltas value was higher, but in lake Zabordzskoe the ratio was low, near 1 (1:;. The conventionalities of the coiiiparisons are obvious. For example, rare sampling in win- t>er periods can give greater errors in nuinber and biomass estiiiiations of zooplankton. Besides that the phosphorus spring saniples were collected after the lake opening and perhaps algae developed taking up nutrients. The role of zooplankt.on in nutrient cycling is niorc significant in deep lakes. In shallow lakes, the inineralisation in thc bott,orn layer and nutrient release froni sediments can play a big role.

Although the main attention in our work has been paid to the role of Crustacea and Rotatoria in phosphorns cycling ciliates and other protozoans should be taken into consideration, too. With increase of t’he productivity of the lakes the rclative part of their bioniass and their relative significance in t,he internal lake processes are increas- ing. This spwia 1 question about. the significance of different systematic arid size groups in the lakes with different trophy is wort,h to be taken into separate consideration.

In general, our investigation shows that t,he suggested method for calculating P E B gave the approximate estimation for zooplankton in lakes of different trophic catego- ries in phosphorus cycling. It is only rough approach for estimation. However, t’he significance of zooplankton in phosphorus cycling is high in lakes with a low produc- tivity and declines in highly productive lakes, where nutrients require phytoplankton growth owing to its inflow froni t,he watershed and froin bottom sediments.

7. References

BOTTKM,L, H. H., A. DUNCAN, Z. M. CIJWICZ, E. DDRYCIEKEK, A. HEKZIG, A. HILLBRICHT-TLKOW- SKA, H. KUROSAWA, P. LARSSON and T. WEGLYNSKA, 1976: A review of some problems in zoo- plankton prodnc,tion studies.-Norw. J. 2001. 24: 419-456.

CARLSON, R. E., 1977: Atrophic state index for lakes.-Limnol. Oceanogr. 22: 367-369. DILLON, P. J., and F. H. RiUmR, 1974 : The phosphorus-chlorophyll rclationship in Iakcs.--Limnol.

Oceanogr. 19: 767.- 773. EJSMONT-KARARIN, J., 1983 : Ammonia nitrogen and inorganic phosphorus excretion by the

planktonic rotifers.~Hydrobiologia 104: 231-236. GALKOVSKAYA, G. A., 1980: The oxygen consumption rate by rotifcrs from the natural popula-

tions.-Vesti Acad Nank BSSH, scr. biol. 6: 114-116 (in Russi;~:~). GoLTERrvr AN, H. T,., 1969: Xethods for Chemical Analysis of Fresh Waters.--Oxford, Edinburgh,

171 pp. GUTELMAKHEK, B. L., 1977: Quantitative assessment of the importance of zooplankton in phos-

phorus cycle in a lake.-Zh. obshch. biol. 38: 914-923 (in Russian). GUTELMAKHER, B. L., 1983 : Rate of phosphorus excretion by marine and freshwater Crustaceans. - Gidrobiol. zh. 19: 1-16 (in Russian).

IKEDA, T., and A. W. MITCHELL, 1982 : Oxygen uptake, ammonia excretion and phosphorus cx- cretion by krill arid other antarctic zooplankton in relation to their body size and chemical com- position. - ”Ir. Biol. 71: 283-298.

KULESHEVA, T. I. and E. A. STRAVINSKAYA, 1988 : Hydrochemical lakc character. In: The cluing- ing in structure lake ecosystems during increasing nutrients loading.-Published by “Nauka”, Leningrad (in Russian).

Zooplankton in the Cycling of Phosphorus 151

KEDFIELD, A. C., B. H. K HUM and E’. A. RICHARDS, 1963: The influence of orgttnisnis on the cornpositon of sea w;tter.--ln: The sea. N. Y., L., vol. 2: 26-77.

KICIIARDS, F. A., 1965: Anoxic basins and fjords.-In: Chernicd Oceanography. vol. 1: 611 bis 845.

SAKAMOTO, M., 1966: Primary production by phytoplankton community in some Japanese lakes and its dependence on lake depth. - Arch. Hydrobiol. 62: 1-28.

RCIKENSEN, T. A., 1948: A method of establishing groups of equal amplit,ude in plant sociology based on similarity of specics content and its application to analyses of the vegetation on Dmish cornmom-Biol. Skr. 5: 1-34.

STJSHCHENYA, L. &I., 1972: lritensivnost dykhaniya rakoobraznykh. - Kiev, Naulrova Dnmka : I98 pp. (in Eussian).

TRIVONOVA, I. S., 1986: Determinntion of the trophic status of two lake rcgioris of the USSR north- west by primary product,ion, chlorophyll content and trophic indices.-Shornik t,rudov Gos- XIORH 252: 78-86 (in Russian).

UMNOV, A . A , , 1070: Utilization of statistical methodsfor the evduation of the par;unet,ers of empi- rical equations dcscrihing the relationship between energy metabolism and body mass in animals. --Zh.obshch. biol. 37: 71-86 (in Russian).

VOLLENWEIDER, R. A., 1968: Scieritific fundamentals of the Eutrophication of Lakes and Flowing Waters, with Particular Reference to Nitrogen and Phosphorus as Factors in E[it,ropliic~~tii~n.- Paris, OECD, Technical rcport: 250 pp.

WINBERG, G. G., 1983: Vant-Hoff’s temperature coefficient and Arrhenius’ equation in biology.- Zh. obshch. biol. 44: 31-42. (in Russian).

n. I,. CUTELMAKHER Zoological Institut of the Academy of Sciences USSR, Leningrad 190034 USSR.

E. S. MAKARTSEVA Limnological Institute of the Acndcmy of Sciences USSR, Leningrad, 196199, Sevastyanova 9.

Manuscript accepted: July 15th, 1989