Aquatic Ecology 36: 235–243, 2002. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.

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Growth of dominant zooplankton species feeding on plankton microflora in Lake Shira Tatiana A. Temerova, Alexander P. Tolomeyev and Andrei G. Degermendzhy Institute of Biophysics of SB RAS, Akademgorodok, Krasnoyarsk, 660036 Russia (E-mail: [email protected]) Accepted 29 October 2001

Key words: Arctodiaptomus salinus, Brachionus plicatilis, life history, reproduction, specific growth rate

Abstract Batch cultures and continuous flow cultures were used to study the growth rates of zooplankton species from Shira lake, the rotifer Brachionus plicatilis Muller and calanoid copepod Arctodiaptomus salinus Daday, which were fed on phytoplankton and bacterioplankton from the lake. Analyses of the birth and survival rates were used to demonstrate that the lake phytoplankton, consisting mostly of cyanobacteria and diatomaceous algae, is inadequotes for optimal realisation of the reproductive potential of B. plicatilis when compared with the bacterial diet. The study revealed that the kinetic growth characteristics of the two zooplankters were similar: B. plicatilis rmax , 0.120 d−1 ; S0 , 0.253; and Ks , 0.114 mg dry mass l−1 ; and for A. salinus rmax , 0.129 d−1 ; S0 , 0.240; and Ks , 0.171 mg dry mass l−1 . Fluctuations in natural food concentration reduced the growth rate of both species. Even though the threshold concentration of food for B. plicatilis and A. salinus were quite similar, the copepods were less sensitive to food limitation.

Introduction The rates of growth, development and reproduction of zooplankton receive focused attention in aquaculture and aquatic ecology literature (see reviews by Vijverberg, 1989 and Walz, 1995). Numerous studies deal with the effects of physico-chemical and biotic factors on the zooplankton growth. This allows us to get a deeper insight into the biology of study organisms, especially with regards to their abundance and composition in water bodies of differing trophic status. Most of the experiments have been conducted under controlled laboratory conditions and research is focused mainly on the effects of the most important controlling factors, namely, the concentration of food, food quality and water temperature. However, light, pH, oxygen, salinity and predators may also change characteristics of growth and development (Frolov et al., 1991; Nagata, 1992; Navarro & Yufera, 1998; Rombaut et al., 1999). Taxonomic position together with life history strategy of zooplankton species can be considered as an inherent growth-controlling factor. In other words,

under comparable environmental conditions the behaviour of species can differ. For example, during a period of food limitation a transient improvement in food availability leads cladocerans to increase egg production, while copepods use the additional energy to restore their somatic reserves (Lampert & Muck, 1985). When determined in the field, the life-history characteristics of zooplankton growth and development reflect to a certain extent the general condition of the ecosystem. The dominance of zooplankton groups within a known food niche may provide information about the trophic structure of an ecosystem. The growth rates of zooplankton actually reflect the efficiency of energy and matter flux through the first two trophic levels. One of the tasks of the Shira Lake comprehensive research programme (see papers in Gulati & Degermendzhy, 2002) was to investigate the trophic structure and interactions at different levels. The total absence of fish in the lake allows us to focus our attention to more specifically on the role of both food quality and quantity for zooplankton. The inte-

236 grating instrument of the research studies in progress on Shira Lake is a simulation mathematical model of dynamic type using kinetic growth characteristics of mass hydrobiont species and their interaction with the nutrition elements (Degermendzhy & Gladyshev, 1995, Degermendzhy & Gubanov, 1997). Growth characteristics available in literature cannot always be successfully applied to model a certain object. Development of zooplankton largely depends on food conditions, which are unique for every water body mainly because of the specific quality of food. Even similarity in species composition of phytoplankton provides no reason to assume that the quality of food is similar. For example, the content of many nutrients important for sustaining the development of animals, primarily, phosphorus (Gulati & DeMott, 1997; DeMott & Gulati, 1998), can considerably differ in the same algal species from different water bodies. The aim of the present study was to define kinetic characteristics of growth based on the natural food of two zooplankton species in the lake: the rotifer, B. plicatilis and the calanoid copepod A. salinus, which together account for up to 99% of the zooplankton biomass in Shira Lake (Zotina et al., 1999). These species are known to frequently coexist in brackish lakes all over the world (Diaz et al., 1998; Zhao Wen & He Zhi-hui, 1999). For most of the vegetative season B. plicatilis is known to reproduce partenogenetically, yet shortage of food and (or) decrease of temperature can make the animals produce mictic eggs (Lubzens & Minkoff, 1988; Kogane et al., 1997). Like all copepods A. salinus, reproduces only sexually, the cycle of development including 6 naupliar and 6 copepodite instars. The rates of somatic and generative growth of the copepods are determined by both food conditions and temperature (Koski & Kuosa, 1999), while the development time of the different developmental stages is controlled by the temperature. (Herzig, 1983). This study is restricted to the effect of only one factor – the food. All experiments were carried out with periodic variation of temperature – up to 20 ◦ C in the daytime and 17 ◦ at night. To make experimental conditions similar to the natural environment we let the temperature vary as in the lake. B. plicatilis is a fairly large species up to 0.5 mm in size and appears to compete with A. salinus (1 mm) for its food. The nutrition spectrum of B. plicatilis is up to a particle size of 12 µm (Rothhaupt, 1990a). However, while the copepods are known to be ‘macrofiltrators’, inefficiently consuming particles less than 2 µm in diameter, the role of rotifers in consuming

bacteria and, consequently, participation in the ‘microbial loop’ needs careful examination (Ooms-Wilms, 1997). The objective of the present study was also to test the importance of picoplankton as a source of food. The effect of trophic conditions on the growth and development of B. plicatilis can be qualitatively estimated by comparing the dynamics of birth and death rates in three possible ways, as proposed by Galkovskaya (Galkovskaya et al., 1988): type I corresponds to the optimal development dynamics when the death rate in a cohort begins at the moment of maximum birth rate. This demonstrates that the energy that sustains the organism is successfully diverted to reproduction. In type II the death rate starts at the point when the birth rate starts to decline or after the reproduction period, demonstrating extensive reproduction due to shortage of food or effect of below-optimal temperature. Lastly, in Type III the mortality starts before the reproduction rate reaches its maximum. It shows that the increased expenditures for reproduction decrease the energy that is needed to sustain the organism, and the death rate accordingly increases. This type actually indicates the existence of conditions that prevent an optimal realisation of maximum reproductive potential.

Study area Shira Lake is located in the north of Minusinsk basin (N 54 30 , E 60 ) (Republic of Khakasia). The lake has no outflow; the inflow of the small Son River amounts to 42% of the total water income. The lake’s catchment is about 35 km2 and the maximum depth is 22.4 m. The major ions in lake water are sulphate– chloride-hydrocarbonate-sodium-magnesium. The reaction is alkaline. Salinity of the lake increases from 18 g l−1 at its surface to 30 g l−1 in the near-bottom layer (Krivosheyev, 1997; Parnachev & Vishnevitsky, 1997; Parnachev & Degermendzhy (2002). Life in the lake is found down to a depth of 13 m. Below this depth lies the hydrogen sulphide zone. In summer the temperature at the surface reaches between 20 and 24 ◦ C, decreasing to 1.6 ◦ C in the deeper layers. Lake biota. The species composition of the lake is scanty. According to data from 1996–1998 (Zotina et al., 1999) the summer phytoplankton has more than 27 species belonging to three major groups. Lyngbya contorta Lemm., Microcystis sp. and Syne-

237 chocystis sp. are dominant cyaorobacteria; the diatoms include Cyclotella sp., and the green algae include Dictyosphaerium tetrachotomum Printz and Oocystis submarina Lagerh. In terms of biomass- the dominant cyanobacterium is L. contorta, the subdominant is Microcystis sp., while C. tuberculata is the dominant diatom. Cyanobacteria comprise from 57 to 90% of the total phytoplankton biomass, the diatoms 0.2–5.2%, and the green algae 2.4 to 5.2%. Bacterioplankton density in summer varied from 2.5 to 16 × 106 cells ml−1 and was, on the average, about 10.7 × 106 cells ml−1 . The contribution of single bacterial cells in these densities was ≈86%, the rest being microcolonies. Diversity of zooplankton species was relatively low and included Arctodiaptomus salinus Daday, Brachionus plicatilis Muller and Hexarthra oxyuris Zernov. Some Cladoceran genera, Moina and Daphnia, appear to be present in extremely low numbers in the eastern part of the lake (Zotina et al., 1999). This is also noted the eggs hatched from the lake sediments in the laboratory. During the vegetation period the zooplankton is dominated by A. salinus and B. plicatilis. In winter B. plicatilis is absent, only A. salinus and H. oxyuris are found in the zooplankton (Zotina et al., 1999). The ichthyofauna is absent. The population of the amphipod Gammarus lacustris Sars, with a benthic-planktonic mode of life, is well developed.

Materials and methods Growth characteristics of B. plicatilis and A. salinus were studied in July–August 1998 at ‘Shira Lake’ field laboratory of the Institute of Biophysics (Russian Academy of Sciences, Siberian Branch), Krasnoyarsk. The animals were grown in closed microaquaria and in chambers with a continuous exchange of a food medium. The former method was used to obtain detailed information on the nature of individual development of a cohort by life history examination and qualitative estimation of trophic existence conditions. This method is well known and widely used in laboratory studies to estimate effect of factors of different kinds (temperature, food, illuminance, etc.) on ontogenetic development of rotifers (Ricci, 1983; Kokova, 1982; Hirayama et al., 1989; Oltra & Todoli, 1997). The method of continuous flow was used to examine dependence of the specific growth rate (SGR) of zooplankton on food concentration. The method was chosen because it allows the maintenance of a steady concentration in the course of experiment and prevents

the accumulation of metabolites which may inhibit growth of the animal (Gladyshev et al., 1993). Individual cultivation of B. plicatilis The rotifers were caught in the lake and put in equal amounts (≈60 individuals) into several Petri dishes. On the following day the newborn young, which were distinct because of their small size (170 µm), were transferred singly into sixty 2-ml microaquaria. Once a day the whole cohort was examined to record the births or deaths of the animals. The offspring were counted and removed from the microaquaria. All the remaining rotifers were replaced into a fresh food medium. In one case food we obtained using natural phytoplankton and bacterioplankton in the lake water from which the zooplankton was removed by filtering through a nylon net with mesh size 120 µm; in the other case, only bacterioplankton filtered through a membrane filter with mesh size 0.95 µm was used as natural food. The lake water for the experiments was sampled daily from the epilimnion not at a sampling point about 100 m from the shore. Experiments were conducted until the death of the last rotifer from the cohort under study. The data obtained during observation were used to calculate the average life expectancy (L), duration of juvenile (Djuv ), reproductive (Drepr ) and senile (Dsen ) periods. The juvenile period was considered as the time duration from the hatching until the rotifer had its first egg, the reproductive period ranged from the moment the rotifer had its first egg to the last reproduction in the course of life, and senile period from the last reproduction until death. The duration of each development period was expressed as a fraction (%) or part of the total time of life expectancy. Basic growth characteristics were calculated according to Birch’s computational method (Pianka, 1981). For each age (x) survival rate (lx ) as part of individuals survived until age x and birth rate (mx ) as the average number of offspring per one individual at age x were calculated. The following three formulae were used to calculate: Reproduction rate (R0 , ind. female−1), for the life expectancy
lx mx , (1) R0 = x

Average generation time (T , d),  lx mx x T = x , x lx mx

(2)

238 and SGR (r, d−1 ) ln(R0 ) . (3) r= T Complicated and long-time individual development of A. salinus, including the diapause, prevented us from applying this method to investigate the growth of copepods. Continuous flow cultures of B. plicatilis and A. salinus The study animals with a known biomass were placed in special 50-ml chambers with continuous flow of food medium (Gladyshev et al., 1993). To prevent the animals and their eggs (>150 µm) from escaping the chambers the inflow and outflow openings were covered with nets with mesh size 120 µm. Two types of experiments were performed: In the first case constant food concentration at different flow rates was used. The food medium was water from the lake from which zooplankton was removed by filtering with a nylon net (mesh size 120 µm), so that it contained phyto- and bacterioplankton in natural concentration. In the second case the food medium was continuously refreshed. The food concentrations were varied using mainly microalgae prepared by dilution of the lake seston fraction, concentrated on 0.95 µm ‘Vladipor’ mesh filter, with lake water filtrate obtained on a 0.2 µm filter. Experiments were performed in 5–7 cultivators. The animals were caught in the lake immediately before the experiment. Experiments with rotifers lasted 5 days. Each cultivator had 7 individuals. Experiments with copepods lasted up to 8 days. Each cultivator had 5 CII-CIII copepods (0.5–0.75 mm). The growth rate of an animal was evaluated from the animal’s biomass in each cultivator at the end of experiment and formed the basis to calculate SGR according to the known formula: ln(B2 ) − ln(B1 ) , (4) r= t where r is the SGR, d−1 ; B1 and B2 are the initial and final biomass; t is the exposure time in days. Assuming that the average weight of rotifers at the beginning and the end of experiment varies insignificantly, their substition of the rotifer numbers for the biomass can suffice in formula (4). The increment of copepod biomass was evaluated by the increase of the linear size of their bodies by the formula (Balushkina et al., 1979): W = 0.038l 3.178,

(5)

where W is the fresh weight of biomass (mg); l is the linear size (mm). The confidence of the effect of the flow rate on SGR of animals was estimated by one way ANOVA statistics. The functional dependence of SGR of B. plicatilis and A. salinus r on food concentration S was taken according to Monod equation accounting for the threshold concentration (e.g., Rothhaupt, 1990b) S − S0 . (6) r = rmax S − S0 + Ks The maximum SGR rmax , half-saturation constant Ks and threshold food concentration S0 were calculated by nonlinear regression equations. The estimate was made by the quasi-Newton method. In the course of the experiments qualitative and quantitative composition of phytoplankton and bacterioplankton were evaluated by direct count under a microscope and were practically stable. Bacteria were counted with DAPI. The weight of the cells was derived from their volume. Cell density was taken for 1 and the dry weight/freshweight ratio of 0.3 (Bakken & Olsen, 1983). All experiments were performed at a temperature of 17–20 ◦ C

Results Phyto- and bacterioplankton of the lake The algae and bacteria had an approximately comparable biomass that amounted to 0.75 mg DW l−1 (Table 1). In the algal part the main bulk was comprised of cyanobacteria (56.3%) and diatoms (34.2%). The green algae accounted for a small portion – 10.2%. Seston <120 µm did not contain any small rotifers. Ciliates were sparse and their biomass was not more than 0.2 µg l−1 . Growth indices of B. plicatilis in individual cultivation Life expectancy of a cohort of the rotifers was 18 days when feeding on the algal-bacterial community and 6 days feeding on bacteria. However, the difference in the pure reproduction rate and in the development period was not as considerable (Table 2). In either case the reproductive period accounted for about 60% of the total life expectancy, but juvenile part was slightly less when feeding on bacteria only. Considerable differences were observed in the dynamics of birth rates and survival rates. When feeding

239 Table 1. Biomass (B) and numbers (N) of phyto- and bacterioplankton in the lake water used for experiments on investigation of zooplankton growth (mean ± SE) Component

B, (mg DW l−1 )

N (cell l−1 )

Bacterioplankton Cyanobacteria Diatoms Green Total phytoplankton

0.37 ± 0.03 0.21 0.13 0.04 0.37 ± 0.05  = 0.75

10.4 ± 0.8 × 109

% of the total phytoplankton mass

55.3 34.2 10.5 146.9 ± 38.1 × 106

Figure 1. Survival (lx ,%) and fecundity (mx , ind. femal−1 ) of B. plicatilis individually cultivated on algae – bacterial food (a) and bacterial food (b) from Shira Lake. Table 2. Indices of net reproduction rate (R0 ), regeneration time (T ) and SGR (r), parts of juvenile (Djuv ), reproductive (Drepr ) and senile (Dsen ) ontonegesis periods in total life expectancy (L) of B. plicatilis individually cultured at natural concentration (S) of lake algae-bacteria and bacterial food (mean ± SE) Growth parameters

Algae-bacteria

Bacterial

S, mg DW l−1

0.75 1.68 5.14 0.101 6.25±0.19 31.5 ±2.4 56.7 ±5.3 11.9 ±2.1

0.38 1.54 3.53 0.122 4.50±0.15 26.0 ±1.5 57.3 ±2.2 16.7 ±1.2

R0 , ind. female−1 T , day r, d−1 L, days Djuv , % Drepr , % Dsen , %

on an algal-bacterial community, the survival rate decreased if the birth rates were high (if intensive

reproduction occurred) (Figure 1a), i.e., the death rate of the juveniles increased. Such a ratio of the birth rate and survival rate belongs to reproduction type III (Galkovskaya et al., 1988). While feeding on bacteria only, the reproduction maximum decreased early during the reproduction cycle and the survival rate increased to 100% (Figure 1, b). Such dynamics correspond to optimal reproduction type I. Specific growth rates, rates of medium exchange and food concentration The input concentration of the food medium was 0.75 mg of dry mass l−1 . Dependencies of SGR of animals on the flow rate of the medium are shown in Figure 2. The flow rates ranged from 1.4 to 24.2 d−1 for the rotifers and from 1 to 11.3 d−1 for the copepods. The flow rate significantly influenced the growth rate of the rotifers (Fexp = 268.77 < Fcrit = 3.47, df=4, P > 0.99), which reached its maximum at a flow rate of 5.3 d−1 . This was not true for copepods:

240

Figure 2. SGR (r) of dominant zooplankton species vs. medium exchange rate (D) (mean ± SE).

Figure 3. SGR (r) of dominant zooplankton species vs. food concentration (S) (mean ± SE).

their growth rate practically showed no dependence on the flow rate (Fexp = 0.34 < Fcrit = 2.57, df=6, P = 0.91) and was about 0.08 d−1 . Specific growth rates, algal concentrations and flow of food medium The dependence of SGR of the rotifer population on food concentration was evaluated at the optimal rate of medium exchange D = 5 d−1 . With natural concentration of microalgae 0.37–0.39 mg of dry mass l−1 the specific growth rates of both rotifers and copepods were relatively low – 0.035 ± 0.003 d−1 and 0.054 ± 0.001 d−1 , respectively. They increased with concentration. However, the r did not exceed 0.137 ± 0.007 d−1 for the rotifers and 0.121 ± 0.007 d−1 for the copepods.

When the algal concentrations decreased below their density in the lake the specific growth rates of both the species reached zero. An increase of the algal concentration of > 1 mg of DW l−1 also resulted in some decrease of the growth rates. Kinetic constants: rmax calculated by equation 5 were: B. plicatilis: rmax = 0.120 d −1 ; S0 = 0.253 and Ks = 0.114 mg DW l−1 (R 2 = 0.88); and A. salinus copepods: rmax = 0.129 d −1 , S0 = 0.240 and Ks = 0.171 mg DW l−1 (R 2 = 0.80). Discussion Despite their taxonomic differences, B. plicatilis and A. salinus displayed marked similarity in the dependence of their specific growth rates on the concentration of seston particles <120 µm. The growth kinetics

241 facilitates prolonged coexistence of the species because, even if they compete for the same resource, the competitive elimination, in this case, is very slow. It seems, however, that these animals coexist mainly because of somewhat different food niches. The consumption optimum of calanoid copepods of similar size (e.g., Eudiaptomus gracilis) is 19 µm (Hansen et al., 1994; Bern, 1994; Horn, 1985) over a fairly broad range from 2 µm to large particles of 50 µm. B. plicatilis demonstrated optimal consumption of food particles (algae Tetraselmis suecica) 8.3 µm in size of equivalent spherical diameter, while the particles in the size range 6.5 and 12.9 µm were consumed with an efficiency of only 60% (Hansen et al., 1997). Yet the issue of picoplankton consumption by the rotifers has not been solved unambiguously. According to some authors they are unable to efficiently consume particles less than 1 µm (Starkweather et al., 1979), while in several cases the bacteria increased the growth rate of the rotifers (Rombaut et al., 1999). Our experiments indicate that the bacteria are an important source of food for B. plicatilis in Shira, Lake as the rotifers did not exhibit a decrease of growth rate on food fractions <0.95 µm (Table 2). Moreover, on bacteria the rotifers displayed type I of optimal reproduction dynamics, that i.e. when the death rate in a cohort begins at the moment the birth rate is at a maximum. As opposed to the bacterial diet, the algal-bacterial diet, consisting impart of 56.6% cyanobacteria (Table 1), triggered the onset of death rate before the reproduction maximum (Figure 1), indicating that the diversion of energy to reproduction enhanced the sensitivity of the rotifers to the influence of adverse factors. Cyanobacteria seem to have a toxic effect on the rotifers, which are less sensitive to them before the reproduction (Figure 1). According to different workers Brachionus displays poor taste selectivity to food particles (DeMott, 1986), yet, it has elevated tolerance to the effect of cyanobacterial toxins, even when feeding on their filamentous forms (e.g., Vareschi & Jacobs, 1984). Moreover, in individual cases, cyanobacteria (Planktothrix (= Oscillatoria) agardhii) together with green algae yielded a higher growth rate of Brachionus, than the rate observed on each of these kinds of food, separately (Weithoff & Walz, 1995). The calanoid copepods, to which group A.salinus also belongs, display a different survival strategy due to their highly selective mode of feeding. No increase in the growth rate of B. plicatilis, which would be expected with an increase in the concentration of natural food, may be associated with an elevated concentration of

algae (which it cannot avoid) toxic to this species. A. salinus can regulate consumption of toxic algae, but when their concentration is high it also has to spend more energy on selective feeding. Deterioration of food conditions, arising both when the natural concentration of algae-bacterioplankton is diluted and when the rates of medium exchange are low, decreased the growth rate of B. plicatilis more than that of A. salinus. Even though the food threshold of the rotifers was similar to, yet somewhat higher than those of the copepods. Thus, the survival strategies r and K, respectively of these species differ. The rotifers are less tolerant to food deficiency than the copepods, but exhibit faster response and better exploration of new sources of food. On the whole, the growth rates of both B. plicatilis and A. salinus on natural food turned out to be quite low. SGR of B. plicatilis can reach 0.9–1 d−1 (Yufera, 1987; Weumann et al, 1989) and that of A. salinus was also relatively low, as for most copepods the growth rate ranges from 0.1 to 0.4 d−1 (e.g. Ivanova, 1985). From the viewpoint of functioning of the trophic system of the lakes, the low growth rates of zooplankton reflect low efficiency of transformation of matter and energy of the primary producers, and this is associated primarily with the low quality of the natural food. The comparable specific growth rates of the rotifers on bacteria and on the entire algal-bacterial food indicate that the rotifers use the energy of the detritus chain equally.

Conclusion (1) Kinetic constants of growth on seston <120 µm for B. plicatilis rotifer were: rmax = 0.120 d−1 , S0 = 0.253 and Ks = 0.114 mg DW l−1 (R 2 = 0.88) and for A. salinus copepods: rmax = 0.129 d−1 , S0 = 0.240 and Ks = 0.171 mg DW l −1 (R 2 = 0.80). (2) Similar growth rates of B. plicatilis on the algabacterial community and on bacteria of µ = 0.10 and 0.12 d−1 , respectively, demonstrate that in Shira Lake bacteria are an important source of energy. (3) A. salinus revealed a tendency to a lower sensitivity to the shortage of food than B. plicatilis. The growth rate of A. salinus did not significantly depend on the flow rate of the medium in the cultivator (Fexp = 0.34 < Fcrit = 2.57, df=6, P = 0.91) and the threshold concentration was somewhat lower (without statistics) than that of B. plicatilis: 0.240 and 0.253 mg DW l −1 , respectively.

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