ISSN 1607-6729, Doklady Biochemistry and Biophysics, 2006, Vol. 411, pp. 346–348. © Pleiades Publishing, Inc., 2006. Original Russian Text © A.P. Tolomeyev, E.S. Zadereev, A.G. Degermendzhy, 2006, published in Doklady Akademii Nauk, 2006, Vol. 411, No. 4, pp. 549–552.
BIOCHEMISTRY, BIOPHYSICS, AND MOLECULAR BIOLOGY
Fine Stratified Distribution of Gammarus lacustris Sars (Crustacea: Amphipoda) in the Pelagic Zone of the Meromictic Lake Shira (Khakassia, Russia) A. P. Tolomeyev, E. S. Zadereev, and Corresponding Member of the RAS A. G. Degermendzhy Received July 5, 2006
DOI: 10.1134/S1607672906060068
Gammaridae are widely spread in many types of water ecosystems and may dominate the community of large benthic invertebrates with respect to both numbers and biomass [1]. Detritus is the main source of food for most species of Gammarus; therefore, the crustaceans usually accumulate near the coast and feed on allochthonic organic matter. However, benthic life is not always typical. Amphipoda are characterized by high morphological diversity and a very flexible nutrition type. Gammarus can use any available animal and plant food, which allows them to spread to new habitats and extend their ecological niche. The spread to untypical habitats is clearly illustrated by the example of sea Gammaridae, which display all stages of the spread to the pelagic zone, from a short-term rising into the bottom water layer to living exclusively in the pelagic zone (about 4% of the total number of species) [2]. The species of Gammarus that have become part of plankton have to feed on other component of plankton (microalgae and zooplankton) [1]. Gammarus spreading over the pelagic zone begin to play an important role in the function of plankton. There is evidence that Gammarus can control zooplankton abundance. For example, the abundance of zooplankton in some North American lakes is closely correlated with the population density of G. lacustris [1]. A few cases of Gammarus colonizing pelagic zones of fresh waters (e.g., Alpine lakes not inhabited by fish) have been reported [3]. Regarding these cases, little is known about the characteristics of Gammarus staying in water without contacting the bottom. There are almost no data on the vertical distribution of Gammarus in lake ecosystems or the adaptation of these animals to plankton life for long periods of time. The spatial structure has been poorly studied because the methods are
Institute of Biophysics, Siberian Division, Russian Academy of Sciences, Krasnoyarsk, 660036 Russia
inefficient. The standard method of studying the vertical distribution of large invertebrates is to catch them with a plankton net or a water pump [4, 5]. However, the vertical structure is studied too roughly, because the numbers of organisms caught at the same horizons vary considerably. In some cases, it is possible to increase the accuracy by using echolocation; however, this method has substantial limitations in the case of low population density [5]. Taking into account the drawbacks of existing methods, we performed studies with the use of underwater video recording for studying the fine spatial distribution of Gammarus. To estimate the capacity of Gammarus for long stay in the pelagic zone, we performed experiments on Gammarus kept in isolated individual mesocosms in the lake itself. The study was performed in the brackish, meromictic Lake Shira. The maximum depth of the lake was 23 m. The salinity was 11.5 and 14.5 g l–1 in the epilimnion and hypolimnion, respectively. The hydrogen sulfide zone began at a depth of 11–12 m in summer. Phytoplankton was dominated by cyanobacteria from genera Lyngbya and Aphanocapsa. Zooplankton was represented by Arctodiaptomus salinus, the dominating species of Calanoida (Copepoda) and the rotifer Brachionus plicatilis. Ichthyofauna and predatory zooplankton are absent altogether [6]. Video observation. The spatial distribution of G. lacustris in the central part of Lake Shira was studied in the daytime and nighttime with the use of a KPC600BH highly sensitive (0.0003 lx) black-and-white CCD camera (KT&C, Korea) placed into a waterproof case. For recording at night, we used two torches set near the video camera. The camera was submerged from the surface to the upper boundary of the hydrogen sulfide zone (12 m) at a speed of 0.1 m s–1. We recorded a total of ten nighttime and ten daytime verticals. The abundances of Gammarus at different depths (at a step of 20 cm) were estimated by the number of animals in the corresponding frame.
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FINE STRATIFIED DISTRIBUTION OF GAMMARUS LACUSTRIS SARS
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The mortality and mean biomass (grams of dry weight) of Gammarus at the beginning (B1) and the end (B2) of the 20-day mesocosm experiment with different compositions of food: (1) phytoplankton; (2) phytoplankton and zooplankton; (3) filtered lake water (control) Food composition
Mortality, %
B1 ± SE
B2 ± SE
t-pr
µ
1 2 3
30 15 100
1.05 ± 0.08 1.41 ± 0.15 0.91 ± 0.09
1.30 ± 0.10 1.56 ± 0.16 –
6.22 > t01 = 3.01 3.38 > t01 = 2.92 –
0.010 ± 0.001 0.005 ± 0.002 –
Note: SE, standard error; µ, specific growth rate (day–1). The significance of increase has been estimated using Student’s paired test (t-pr).
Growth of G. lacustris in mesocosms. We used groups of animal caught in the central and coastal parts of the lake. The animals were placed into 1-l mesocosms (sealed polyethylene bags) filled with lake water differing in food composition: (1) phytoplankton, (2) phytoplankton and zooplankton, or (3) filtered lake water (control). To provide the animals with a sufficient amount of oxygen, about 100 ml of air was left in each mesocosm. The mesocosms were exposed in the central part of the lake at a depth of 5 m for 20 days. The biomass increment was calculated on the basis of the difference in linear sizes at the beginning and the end of the experiment using an equation relating the linear size and body weight of the animals [7]. We measured the vertical profiles of temperature, salinity, and oxygen content by means of a Hydrolab submersible probe (Hydrolab, United States). Chlorophyll concentration was estimated by the fluorescent method [8]. The Brunt–Vaisala frequency (N, s–1) characterizing the work that would be necessary to perform against the force of gravity to overcome the temperature stratification within the water layer was calculated according to [9]. Direct video observations showed a characteristic peak of Gammarus numbers in a thin layer at a depth of 5.5–6.5 m in the daytime. The daytime and nighttime vertical distributions of Gammarus distinctly differed from each other. This layer sank to a greater depth and became less distinct in the nighttime. The small difference between the positions of the daytime and nighttime maximums (about 1.5 m) suggested that the vertical migration activity of these crustaceans in Lake Shira was weak. The model of Gammarus behavior obtained in our study is not common for this species; apparently, it depends on the adaptation of animals to each particular ecosystem. For example, in the Alpine Lake Snowflake (Canada), which is not inhabited by fish, G. lacustris, conversely, stays at the bottom in the daytime and rises to the pelagic zone by midnight [10]. The authors of the study [10] relate this behavior to active feeding on zooplankton and phytoplankton. In Lake Shira, G. lacustris use other sources of food. Earlier analysis of stomach contents showed that freshly precipitated seston and microalgae were the main food of the animals [11]. Collation of the vertical position of the maximum numbers of Gammarus (Fig. 1a) and data on environmental factors (Fig. 1b) shows that the crustaDOKLADY BIOCHEMISTRY AND BIOPHYSICS
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ceans occupied the metalimnion zone. This zone was characterized by the highest hydrodynamic stability (the Brunt–Vaisala frequency was the maximum), and seston particles precipitating from the epilimnion were most likely to be accumulated here. Thus, a local ecological niche favorable for G. lacustris was formed in the hydrodynamically stable metalimnion of the stratified body of water. The results of the 20-day experiment demonstrated that Gammarus could stay in the pelagic zone without contacting the bottom for a long time. Since the Gammarus that were selected for the experiment from the littoral and pelagic zones of the lake had similar growth parameters, they were pooled into a single sample. Under the metalimnion conditions (16°C), the specific somatic growth rate was 0.005–0.013 day–1 (table). Note that Gammarus grew two times more rapidly in mesocosms that did not contain zooplankton. Apparently, zooplankton competed with Gammarus for food (microalgae). Therefore, the feeding conditions for Gammarus in the mesocosms containing both phytoplankton and zooplankton were worse than in mesocosms containing phytoplankton alone; hence, the growth rate in the former case was lower. Gammarus could not survive for 20 days on their internal store of nutrients. In mesocosms from which phytoplankton and zooplankton were removed by filtration, 100% of the animals died. Therefore, Gammarus must entirely switch to feeding on plankton to live in the pelagic zone for a long time. It is obvious that the narrow layer of Gammarus in the center of Lake Shira, which had not been detected before by standard methods, is very important from the ecological viewpoint. It was demonstrated earlier that the contribution of Gammarus to phosphorus regeneration could be as large as 9.5–32.9% of the total phosphorus regeneration by the planktonic community [12]. According to our data, the biomass of Gammarus in a narrow layer of metalimnion of Lake Shira (at depths of 5.5–6.5 m) may be as large as 1.09 g dry weight/m3, which is three times higher than in Lake Snowflake (0.014–0.364 g/m3) [12]. Gammarus form a “live barrier” in the way of precipitating seston, which is utilized before it reaches the hydrogen sulfide zone. As a result, biogenic elements and valuable biochemical substances are retained by the pelagic ecosystem and are involved in the cycle again. 2006
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TOLOMEYEV et al. (‡) 40 0
(b)
Frequency, rel. units 20 0 20 40 Night
60
T, °C, Chl a, µg 0 10
l–1,
S, g l–1, O2, mg l–1 20
Day
2
Depth, m
3
4
5
4 1 6 2 8
10
12
0
0.02
0.04
0.06
0.08 N, s–2
Fig. 1. The vertical distribution of (a) the abundance of G. lacustris and (b) physical and chemical factors in the pelagic zone of Lake Shira in 2005. Designations: 1, Brunt–Vaisala frequency (N); 2, chlorophyll a (Chl a); 3, oxygen (O2); 4, salinity (S); 5, temperature (T).
Thus, we used a system of underwater video recording to detect a narrow peak of G. lacustris population density in the metalimnion of Lake Shira. The crustaceans proved to be capable of transiting to an entirely pelagic life for a long time and growing in the pelagic zone while feeding on plankton.
3. Wilhelm, F.M., Schindler, D.W., and McNaught, A.S., J. Plankton Res., 2000, vol. 22, no. 9, pp. 1719–1734. 4. Abakumova, V.A., Rukovodstvo k metodam gidrobiologicheskogo analiza poverkhnostnykh vod i donnykh otlozhenii (Manual of Hydrobiological Analysis of Surface Waters and Bottom Sediments), Leningrad: Gidrometeoizdat, 1983. 5. Trevorrow, M.V. and Tanaka, Y., Limnol. Oceanogr., 1997, vol. 42, no. 1, pp. 121–132.
ACKNOWLEDGMENTS This study was supported by the Program of Basic Research of the Presidium of the Russian Academy of Sciences “The Origin and Evolution of the Biosphere” (project “Experimental and Theoretical Analysis of the Mechanisms of the Biotic Cycle as the Basis of Stability of Complex Superorganismal Systems”), BRHE (project no. RUX0–002–KR–06), Russian Foundation for Basic Research–KKFN (project no. 05–04–97708r_enisei_a), and Russian Foundation for Basic Research–NOW (project no. 2004 0.47.011.2004.030).
6. Zotina, T.A., Tolomeyev, A.P., and Degermendzhy, N.N., Int. J. Salt Lake Res., 1999, no. 8, pp. 211–232. 7. Yemelyanova, A.Y., Temerova, T.A., and Degermendzhy, A.G., Aquat. Ecol., 2002, vol. 36, no. 2, pp. 245–256. 8. Gaevsky, N.A., Zotina, T.A., and Gorbaneva, T.B., Aquat. Ecol., 2002, vol. 36, no. 2, pp. 165–178. 9. Doronin, Yu.P., Fizika okeana (The Physics of the Ocean), Leningrad: Gidrometeoizdat, 1978. 10. Wilhelm, F.M. and Schindler, D.W., Canad. J. Fish. Aquat. Sci., 1999, vol. 56, no. 8, pp. 1401–1408.
REFERENCES 1. Macneil, C., Dick, J.T.A., and Elwood, R.W., Biol. Rev., 1997, vol. 72, pp. 349–364. 2. Vinogradov, G.M., Zh. Obshch. Biol., 1992, vol. 53, no. 3, pp. 328–339.
11. Gladyshev, M.I., Emelianova, A.Y., Kalachova, G.S., et al., Hydrobiology, 2000, vol. 431, pp. 155–163. 12. Wilhelm, F.M., Hudson, J.J., and Schindler, D.W., Canad. J. Fish. Aquat. Sci., 1999, vol. 56, no. 9, pp. 1679–1686.
DOKLADY BIOCHEMISTRY AND BIOPHYSICS
Vol. 411
2006
