SHORT COMMUNICATION. Evaluation of non-predatory mortality of two Daphnia species in a Siberian reservoir
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1 SHORT COMMUNICATION Evaluation of non-predatory mortality of two Daphnia species in a Siberian reservoir MICHAIL I. GLADYSHEV*, OLGA P. DUBOVSKAYA, VLADIMIR G. GUBANOV AND OLESIA N. MAKHUTOVA 1 INSTITUTE OF BIOPHYSICS OF SIBERIAN BRANCH OF RUSSIAN ACADEMY OF SCIENCES, AKADEMGORODOK, KRASNOYARSK, AND 1 KRASNOYARSK STATE UNIVERSITY, SVOBODNY AV., 79, KRASNOYARSK, , RUSSIA *CORRESPONDING AUTHOR: glad@ibp.ru A new method of estimating non-predatory mortality of zooplankton based on live/dead sorting and sediment trap measurement is described. Preliminary results on Daphnia cucullata and Daphnia longispina are given. Estimations of average non-predatory mortality demonstrated a significant contribution of this kind of mortality to total mortality. Mortality is known to be one of the principal factors that determine the dynamics of natural populations. For decades, mortality (death rate) in zooplankton populations was calculated indirectly, as the difference between the estimated rates of birth and of population growth (Polishchuk and Ghilarov, 1981). As authors who used such calculations remark, there are a number of shortcomings that give rise to significant errors in mortality estimates. Moreover, biologically nonsensical negative mortality was often obtained. Furthermore, death rate values include both predatory (consumptive) and nonpredatory (non-consumptive) mortalities. It is now recognized that it is important to study these two processes separately. For instance, the trophic cascade hypothesis/ top-down biomanipulation theory is based on the maintenance of a high abundance of large-bodied Daphnia by a decrease in abundance of planktivorous fish (Wright and Shapiro, 1990). If non-predatory mortality of Daphnia dominates in an ecosystem, biomanipulation will be ineffective; data on predatory and non-predatory mortality of the zooplankton may be crucial for wholelake management. Non-predatory mortality, sometimes designated as ecological or realized mortality, includes natural death due to senescence, disease, limiting physical or chemical factors, etc., and contributes to detritus food webs (Velimirov, 1991). Without measurements of this type of mortality, it is impossible to make accurate conclusions on energy fluxes within a lake (Wetzel, 1995). A number of attempts to estimate non-predatory mortality of zooplankton have now been made (Gladyshev and Gubanov, 1996; Dubovskaya et al., 1999; Gries and Gude, 1999). The present article describes a new method and presents preliminary results of its application to a 4-year study of the dynamics of mortality of Daphnia species in a small Siberian reservoir based on live/dead sorting using special staining and measurements of sedimentation rates for dead individuals. The reservoir, Bugach pond, is situated at N, E in the Bugach river (secondary tributary of the Yenisei river), at the north-west edge of Krasnoyarsk city, Russia. Its surface area is ~0.32 km 2, with a maximum depth of 7 m. During summer, nuisance blooms of cyanobacteria occur in the pond. Detailed descriptions of the reservoir ecosystem are given elsewhere (Gladyshev et al., 2001; Sushchik et al., 2003). The dynamics of abundance of dead individuals are described by: d y dt = mn - Gy (1) where y is the abundance of dead individuals (ind. m 3 ) at time t (day), m is non-predatory specific mortality (NPSM; day 1 ), N is the abundance of live individuals (ind. m 3 ) Journal of Plankton Research 25(8), Oxford University Press; all rights reserved
2 and G is the specific rate of elimination of dead individuals from the water column (or sampling part of the column). For real discrete field data, equation (1) is transformed as: yi = mn i i- Gi yi, i = 1, 2,..., n (2) t i where n is the number of samples during the study period at the given sampling site; t i = t i + 1 t i, with t i the time of taking sample i; y i = y i + 1 y i, with y i and N i being the abundance of dead and alive individuals, respectively, in sample i; and m i and G i being the specific mortality and elimination, respectively, at time t i. From equation (2), NPSM is obtained: y yi m i = + G i $ ti$ N i N (3) i The specific rate of elimination, G, includes decomposition, consumption and sedimentation of dead individuals, but sedimentation is assumed to be the principal (the fastest) component of the elimination (Gladyshev and Gubanov, 1996; Dubovskaya et al., 1999). To assess the sinking velocity of dead zooplankton, a closing, replicate-sample sediment trap was used (Kimmel et al., 1977). The main features of the trap were an aluminium plate holding four aluminium cylindrical collectors and a messenger-actuated closing mechanism. Each collector had an inner diameter of 7.4 cm with an inner height of 39.5 cm, giving the diameter/height ratio >5, as recommended for calm-water situations in small lakes (Bloesch and Burns, 1980). The top of each collector was provided with a baffle (waffle-like grid cm) to prevent resuspension. The trap was suspended in the central part of the reservoir (sampling station 1) at 4 m below the surface (1.5 2 m above the bottom) on a rope stretched between a subsurface buoy and smaller surface buoy from a bottom anchor weight. Collection time was 24 h (Bloesch and Burns, 1980); the trap was closed before retrieval by the horizontally rotating closing plate. The sinking velocity of dead individuals, v (m day 1 ), is calculated as: v = Y (4) S $ y* where Y is the number of dead individuals accumulated in a given trap collector per day (ind. day 1 ), S is the input area of the collector (m 2 ) and y* is the abundance of dead individuals (ind. m 3 ) at the layer of exposure of the trap. Consequently, the specific rate of elimination for equation (3) is calculated as G = v/h, where h is the depth of the layer of sampling of N i and y i. Pooled samples of zooplankton were taken at station 1 weekly, from the 0 2 m layer using a Ruttner-like 8 l sampler. Thus, h was 2 m in this study. During the trap exposure, additional zooplankton samples were taken from the layer of exposure one to three times per day. Zooplankton samples (8 32 l) as well as samples from the trap collectors were filtered through a plankton net (mesh size 0.08 mm). To distinguish between live and dead organisms, samples were vitally stained with aniline blue immediately after sampling (Seepersad and Crippen, 1978) using a special staining device (Gladyshev, 1993) and fixed with 10% formalin. Zooplankton were counted and measured under a microscope. Size was converted to wet weight using conventional species coefficients (Balushkina and Vinberg, 1979). Daphnia cucullata Sars and Daphnia longispina O. F. Muller inhabited the study reservoir. In 1997, D. cucullata dominated (>90%), and in the other years D. longispina became the dominant species. We consider the dominant Daphnia species only, since estimations of species with low biomass give very high errors. The seasonal dynamics of abundance of live Daphnia are given in Figure 1a. Abundance of dead individuals was an order of magnitude lower than that of live individuals (Figure 1b). Maxima of abundance of dead individuals occurred after pronounced declines in density of the populations (Figure 1a and b). Three exposures of the trap were carried out in 1997 and one in Results are given in Table I. Thereby, at h = 2 m, the specific rate of elimination, G, was on average 1.26 day 1, while minimal and maximal values were 0.26 and 2.33 day 1, respectively. For the following calculations of NPSM, we used the average value of G. In 1997, a comparatively high level of NPSM occurred in the first half of summer, coinciding with low abundance of the population (Figure 1). In the second half of the summer, the mortality became low and an intensive development of D. cucullata took place. In 1998, a low level of NPSM occurred in June; the first part of July correlated with a comparatively long period of a high level of abundance of the D. longispina. In the second part of July August, the mortality and abundance fluctuated. At the beginning of August 1999, an extremely high NPSM was observed with an unusually low level of abundance of D. longispina in August and September. In July August 2000, D. longispina had extremely low abundance (there were no D. cucullata in this year), which coincided with the seasonal maximum of the NPSM value. In general, every year, local maxima of mortality occurred at the beginning of the growth season, in May June. Furthermore, maxima of NPSM coincided with a lower average value of the population abundance (Figure 1a and c), except for 2000, which was unusual in respect of seasonal dynamics of Daphnia. 1000
3 M. I. GLADYSHEV ET AL. NON-PREDATORY MORTALITY OF DAPHNIA SP. Fig. 1. Characteristics of Daphnia species in Bugach pond (Siberia, Russia), sampling station 1. (a) Abundance of live individuals. (b) Abundance of dead individuals. (c) Non-predatory specific mortality. (d) Average size of individuals (bold line, dead; solid line, alive). 1997, D. cucullata; ; D. longispina. In 1997, 1998 and especially in 2000, average sizes of dead individuals were higher during the majority of the season (Figure 1d). In contrast, in 1999, dead individuals had lower body sizes. Nevertheless, during all 4 years, at the beginning of the seasons (first date of sampling) sizes of dead individuals were lower than those of live individuals. Summer disappearances of Daphnia in many lakes are often believed to be due to consumptive mortality. Nevertheless, estimations of the contribution of fish predation to Daphnia mortality, based on variants of Paloheimo and bioenergetic models for fish consumption, demonstrate that predation cannot explain the population declines, especially at the beginning of the growing season and for smaller size-classes (Boersma et al., 1996; Hulsmann and Mehner, 1997; Mehner et al., 1998; Hulsmann et al., 1999; Romare et al., 1999; Hulsmann and Weiler, 2000). A common explanation is that the contradictory results may reflect different computations of Daphnia growth, which is critical for estimates of mortality. More conclusive evidence for mortality is believed to be possible using sediment traps (Hulsmann and Weiler, 2000). Our data based on the trap measurements may be regarded as the calculation of mortality that was independent of estimated birth and growth rates. Our data on the non-predatory mortality dynamics are preliminary due to the low number of sinking rate measurements and give only average order-of-magnitude estimations of mortality. The sinking velocity of corpses is evidently not constant during a season and depends on wind speed; for 1001
4 Table I: Number of dead individuals accumulated in a trap collector during the exposure (Y; ind. day 1 ), abundance of dead individuals (y*; ind. m 3 ) at the layer of exposure of the trap, the sinking velocity of dead individuals (v; m day 1 ) and its standard error (SE) in Bugach pond No. of collector 21 June July August June nd 36 y* v ± SE 1.51 ± ± ± ± 0.40 nd, no data. accurate estimations of NPSM, a quantitative relationship between wind speed and sinking velocity must be obtained. If the equation relating sinking velocity to wind speed were known, the daily velocity rates could be derived using routine meteorological data on wind speed. In spite of evident errors in our calculations owing to assumptions about the constant sinking velocity, average order-of-magnitude NPSM estimations seem to be reasonable. First, in contrast to the other calculations [e.g. (Polishchuk and Ghilarov, 1981)], no biologically nonsensical negative values of mortality were obtained. Secondly, some of our findings give independent support for conclusions drawn by other authors on mortality dynamics. For instance, we also revealed comparatively high mortality at the beginning of the growing season at the expense of smaller size-classes. Periods and years of high mortality, measured on the basis of our model, coincided with periods and years of low abundance of the populations. We compared our data on NPSM of 1997 with the total specific mortality (death rate) calculated using the modified Paloheimo model (Dubovskaya et al., 1999) and found that, during the sampling season, the NPSM on average made up to 38% of total mortality. The standing stock of planktivorous fish in Bugach pond was on average ~100 kg ha 1 (data of Chair of Hydrobiology and Ichthyology of Krasnoyarsk State University). This figure is higher than the critical fish biomass of 57 kg ha 1 claimed to induce a decline in Daphnia (Hulsmann and Mehner, 1997). In August 1999, the population decline evidently took place due to non-predatory mortality: at the average G value, m 1, i.e. 100% of the population decline could be explained without consumption by predators. Except for the beginning of the growing season, in , sizes of dead and live individuals were very close to each other. Gries and Gude also reported the similar size distribution of Daphnia in the pelagic zone and in the sediment traps, which indicated no size bias for mortality factors (Gries and Gude, 1999). In contrast, in 2000, during most of the sampling season sizes of dead individuals tended to be higher than those of live individuals. This finding is in agreement with data on Bautzen reservoir, where the summer decline in the population of Daphnia galeata was caused mainly by enhanced mortality of adult daphnids (Hulsmann and Weiler, 2000). Hence, interannual shifts in predatory and nonpredatory mortality, as well as in juvenile and adult mortality, may take place in the same reservoir. Sharp fluctuations of mortality during sampling seasons, revealed in our study, have been reported by other authors (Polishchuk and Ghilarov, 1981). At present, we cannot explain these fluctuations, as well as the differences in mortality between years. The nonpredatory mortality may be caused by a species-specific infection (Gries and Gude, 1999), poisoning by cyanobacterial toxins, such as microcystin (Rohrlack et al., 1999), or low food quality (Muller-Navarra, 1995; Gulati and DeMott, 1997; Elser et al., 2000). Evidently, to understand the non-predatory mortality fluctuations, more detailed studies are necessary. ACKNOWLEDGEMENTS We are grateful to Kevin Flynn and two anonymous referees for providing helpful comments on the manuscript. The work was supported by grant No of the Russian Foundation for Basic Research, by a joint grant of the US Civilian Research & Development Foundation for the Independent States of the Former Soviet 1002
5 M. I. GLADYSHEV ET AL. NON-PREDATORY MORTALITY OF DAPHNIA SP. Union (CRDF) and Ministry of Education of Russian Federation No. REC-002. At the stage of generalization, the work was also supported by a personal grant of the Russian Science Support Foundation, by grant No. UR from the Ministry of Education of the Russian Federation and by grant No. 11F015C of Krasnoyarsk Regional Science Foundation. REFERENCES Balushkina, E. V. and Vinberg, G. G. (1979) Relation between mass and body size of plankton animals. In Vinberg, G. G. (ed.), General Backgrounds for Study of Aquatic Ecosystems. Nauka, Leningrad, pp (in Russian). Bloesch, J. and Burns, N. M. (1980) A critical review of sediment trap technique Schweiz. Z. Hydrol., 42, Boersma, M., van Tongeren, O. F. R. and Mooij, W. M. (1996) Seasonal patterns in the mortality of Daphnia species in a shallow lake. Can. J. Fish. Aquat. Sci., 53, Dubovskaya, O. P., Gladyshev, M. I. and Gubanov, V. G. (1999) Seasonal dynamics of number of alive and dead zooplankton in a small pond and some variants of mortality estimation. Zh. Obshch. Biol., 60, (translated into English). Elser, J. J., Sterner, R. W., Galford, A. E., Chrzanowski, T. H., Findlay, D. L., Mills, K. H., Paterson, M. J., Stainton, M. P. and Schindler, D. W. (2000) Pelagic C:N:P stoichiometry in a eutrophied lake: responses to a whole-lake food-web manipulation. Ecosystems, 3, Gladyshev, M. I. (1993) A device for staining of zooplankton in order to allow live/dead sorting of preserved samples. Gidrobiol. Zh., 29, Gladyshev, M. I. and Gubanov, V. G. (1996) Seasonal dynamics of specific mortality of Bosmina longirostris in a forest pond determined on the basis of counting of dead individuals. Dokl. Akad. Nauk, 348, (translated into English). Gladyshev, M. I., Gribovskaya, I. V., Moskvichova, A. V., Muchkina, E. Y., Chuprov, S. M. and Ivanova, E. A. (2001) Content of metals in compartments of ecosystem of a Siberian pond. Arch. Environ. Contam. Toxicol., 41, Gries, T. and Gude, H. (1999) Estimates of the nonconsumptive mortality of mesozooplankton by measurement of sedimentation losses. Limnol. Oceanogr., 44, Gulati, R. D. and DeMott, W. R. (1997) The role of food quality for zooplankton: remarks on the state-of-the-art, perspectives and priorities. Freshwater Biol., 38, Hulsmann, S. and Mehner, T. (1997) Predation by underyearling perch (Perca fluviatilis) on a Daphnia galeata population in a short-term enclosure experiment Freshwater Biol., 38, Hulsmann, S. and Weiler, W. (2000) Adult, not juvenile mortality as a major reason for the midsummer decline of a Daphnia population. J. Plankton Res., 22, Hulsmann, S., Mehner, T., Worischka, S. and Plewa, M. (1999) Is the difference in population dynamics of Daphnia galeata in littoral and pelagic areas of a long-term biomanipulated reservoir affected by age-0 fish predation? Hydrobiologia, 408/409, Kimmel, B. L., Axler, R. P. and Goldman, C. R. (1977) A closing, replicate-sample sediment trap. Limnol. Oceanogr., 22, Mehner, T., Hulsmann, S., Worischka, S., Plewa, M. and Benndorf, J. (1998) Is the midsummer decline of Daphnia really induced by age-0 fish predation? Comparison of fish consumption and Daphnia mortality and life history parameters in a biomanipulated reservoir. J. Plankton Res., 20, Muller-Navarra, D. (1995) Evidence that a highly unsaturated fatty acid limits Daphnia growth in nature. Arch. Hydrobiol., 132, Polishchuk, L. V. and Ghilarov, A. M. (1981) Comparison of two approaches used to calculate zooplankton mortality. Limnol. Oceanogr., 26, Rohrlack, T., Dittmann, E., Henning, M., Borner, T. and Kohl, J.-G. (1999) Role of microcystins in poisoning and food ingestion inhibition of Daphnia galeata caused by cyanobacterium Microcystis aeruginosa. Appl. Environ. Microbiol., 65, Romare, P., Bergman, E. and Hansson, L.-A. (1999) The impact of larvae and juvenile fish on zooplankton and algal dynamics. Limnol. Oceanogr., 44, Seepersad, B. and Crippen, R. W. (1978) Use of aniline blue for distinguishing between live and dead freshwater zooplankton. J. Fish. Res. Board Can., 35, Sushchik, N. N., Gladyshev, M. I., Kalachova, G. S., Kravchuk, E. S., Dubovskaya, O. P. and Ivanova, E. A. (2003a) Particulate fatty acids in two small Siberian reservoirs dominated by different groups of phytoplankton. Freshwater Biol., 48, Velimirov, B. (1991) Detritus and the concept of non-predatory loss. Arch. Hydrobiol., 121, Wetzel, R. G. (1995) Death, detritus, and energy flow in aquatic ecosystems. Freshwater Biol., 33, Wright, D. and Shapiro, J. (1990) Refuge availability: a key to understanding the summer disappearance of Daphnia. Freshwater Biol., 24, Received on August 1, 2001; accepted on May 8,
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