Autochthonous and allochthonous organic matter in trophic chain of lake ecosystems

V.V. Boulion

Proceedings of the Zoological Institute RAS, 2017, 321(2): 115–128 · https://doi.org/10.31610/trudyzin/2017.321.2.115

Full text

Abstract

This work presents analysis of mass–balance model simulating biotic flows of energy in pelagial of the large lakes of Russia (Ladoga, Onego, and Baikal) and small lake in northern part of the Karelia. The model had been developed on the basis of software package Stella and intended to predict an annual production of phytoplankton, bacterio plankton and consumers (non predatory and predatory zooplankton, planktivorous and piscivorous fishes). The input (independent) abiotic parameters of the model were latitude, mean lake depth, total phosphorus content and water color. The model analyzed an involvement of the autochthonous and allochthonous organic matter in the total energy flow through trophic chain. It was underlined that bacteria are important component of the planktonic community linking the dissolved organic matter (DOM) with organisms of the trophic chain. In high humic and oligotrophic boreal lakes the plankton respiration exceeds the primary production, therefore allochthonous DOM transformed to bacterial production replaces photosynthetic production in consumer feeding. The efficiency of bacterial growth (the ratio of bacterial production to consumed energy) depends on the ratio between autochthonous and allochthonous DOM. It had been shown that efficiency of bacterial growth in lakes with high primary production was higher than in oligotrophic waters with dominated allochthonous DOM. The author discussed different–type organic matter contribution to hydrobiont production depending on total phosphorus and humic matter content. Bacterioplankton consuming allochthonous DOM is additional energy source for zooplankton. For prediction of the total biological productivity it was recommended to take into account also production of heterotrophic bacterioplankton which is involved in utilization of allochthonous DOM.

Key words

biotic energy flows, dissolved organic matter, environmental factors, lakes, modelling, prediction of biological productivity

Submitted January 23, 2017 · Accepted April 11, 2017 · Published June 26, 2017

References

Alimov A.F. and Golubkov S.M. (Ed.) 2012. Dynamics of biotic diversity and bioresources in continental water bodies. Nauka, Saint Petersburg, 369 р. [In Russian].

Ashhepkova L.Ja. 2002. The use software package Stella for modelling of the complex system. Far Eastern University, Vladivostok, 27 р. [In Russian].

Baines S.B. and Pace M.L. 1991. The production of dissolved organic matter by phytoplankton and its importance to bacteria: Patterns across marine and freshwater systems. Limnology and Oceanography, 36: 1078–1090. https://doi.org/10.4319/lo.1991.36.6.1078

Bano N., Moran M.A. and Hodson R.E. 1997. Bacterial utilization of dissolved humic substances from a freshwater swamp. Aquatic Microbial Ecology, 12(3): 233–238. https://doi.org/10.3354/ame012233

Berggren M., Laudon H. and Jansson M. 2010. Bacterial utilization of imported organic material in three small nested humic lakes. Verhandlungen des Internationalen Verein Limnologie, 30(9): 1393–1396. https://doi.org/10.1080/03680770.2009.11902339

Biddanda B., Ogdahl M. and Cotner J. 2001. Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnology and Oceanography, 46(3): 730–739. https://doi.org/10.4319/lo.2001.46.3.0730

Bird D.F. and Kalff J. 1984. Empirical relationships between bacterial abundance and chlorophyll concentration in fresh and marine waters. Canadian Journal of Fisheries and Aquatic Sciences, 41: 1015–1023. https://doi.org/10.1139/f84-118

Boulion V.V. 1988. Extracellular production of the phytoplankton and methods its investigation. Hydrobiological Journal, 24(3): 64–73. [In Russian].

Bussmann I. 1999. Bacterial utilization of humic substances from the Arctic Ocean. Aquatic Microbial Ecology, 19(6): 37–45. https://doi.org/10.3354/ame019037

Cole J.J. 1999. Aquatic microbiology for ecosystem scientists: new and recycled paradigms in ecological microbiology. Ecosystems, 2: 215–225. https://doi.org/10.1007/s100219900069

Cole J.J., Findlay S. and Pace M.L. 1988. Bacterial production in fresh and saltwater ecosystems: a cross-system over-view. Marine Ecology Progress Series, 43: 1–10. https://doi.org/10.3354/meps043001

Cole J.J., Likens G.E. and Strayer D.L. 1982. Photosynthetically produced dissolved organic carbon: An important carbon source for planktonic bacteria. Limnology and Oceanography, 27: 1080–1090. https://doi.org/10.4319/lo.1982.27.6.1080

Del Giorgio P.A. and Cole J.J. 1998. Bacterial growth efficiency in natural aquatic systems. Annual Review of Ecological Systems, 29: 503–541. https://doi.org/10.1146/annurev.ecolsys.29.1.503

Del Giorgio P.A. and Peters R.H. 1994. Patterns in planktonic P:R ratios in lakes: influence of lake trophy and dissolved organic carbon. Limnology and Oceanography, 39: 772–787. https://doi.org/10.4319/lo.1994.39.4.0772

Derenbach J.B. and Willams P.J. 1974. Autotrophic and bacterial production: fractionation of planktonic population by differential filtration of samples from English Channel. Marine Biology, 25: 263–269. https://doi.org/10.1007/BF00404968

Drachev S.M. 1964. The pollution control of industrial and domestic draining. Nauka, Moscow, 274 р. [In Russian].

Filatov N.N. (Ed.) 1999. Onega Lake. Ecological problems. Karelian Research Centre of the RAS, Petrozavodsk, 259 р.

Findlay S.E.G. and Sinsabaugh R.L. (Ed.) 2003. Aquatic ecosystems: interactivity of dissolved organic matter. Academic Press, San Diego, 512 р. https://doi.org/10.1016/B978-012256371-3/50021-4

Flora and vegetation of the Baikal Lake. www.baikal-center.ru

Häkanson L. and Boulion V.V. 2002. The lake foodweb – modelling predation and abiotic/biotic interactions. Backhuys Publishers, Leiden, 344 р.

Hessen D. and Tranvik L. (Eds.) 1998. Aquatic humic substances – ecology and biogeochemistry. Springer, Berlin, 346 p. https://doi.org/10.1007/978-3-662-03736-2

Informational site about Baikal, www.ozerobaikal.info

Inkina G.A. 1979. Rate of the oxygen consumption by bacterioplankton. In: experimental and field investigation of the biological basis of lake productivity. Zoological Institute of the RAS, Saint Petersburg: 103–120.

Iturriaga R. and Hoppe H. 1977. Observations of heterotrophic activity on photoassimilation organic matter. Marine Biology, 40(2): 101–108. https://doi.org/10.1007/BF00396254

Ivanova M.B. 1985. Production of the planktonic Crustacea. Zoological Institute of the RAS, Saint Petersburg, 222 p. [In Russian].

Jones R.I. 1992. The influence of humic substances on lacustrine planktonic food chains. Hydrobiologia, 229: 73–91. https://doi.org/10.1007/BF00006992

Kaufman Z.S. (Ed.) 1990. Ecosystem of Onega Lake and tendency of its change. Nauka, Leningrad, 264 p. [In Russian].

Klekovskij R.Z. and Menshutkin V.V. 2003. Ecological modelling in terms of the Stella. Polish Academy of Sciences, Dzekanov Lesny, 159 p. [In Russian].

Kritzberg E.S., Cole J.J., Pace M.M. and Graneli W. 2005. Does autochthonous primary production drive variability in bacterial metabolism and growth efficiency in lakes dominated by terrestrial C inputs? Aquatic Microbial Ecology, 38: 103–111. https://doi.org/10.3354/ame038103

Kulikova T.P., Kustovljankina N.B. and Sjarki M.T. 1997. Zooplankton as ecosystem component of the Onega Lake. Karelian Research Centre of the RAS, Petrozavodsk, 112 p. [In Russian].

Kuznecov S.I. 1970. Microflora of lakes and its geochemical activities. Nauka, Saint Petersburg, 440 p. [In Russian].

Larson U. and Hagström A. 1979. Phytoplankton exudate release as an energy source for the growth of pelagic bacteria. Marine Biology, 52(3): 199–206. https://doi.org/10.1007/BF00398133

Letanskaja G.I. 2002. Structural and functional indicators of Ladoga Lake phytoplankton in modern conditions. Abstract of the Candidate of Biological Sciences thesis. Institute of Limnology of the RAS, Saint Petersburg, 26 p. [In Russian].

Lozovik P.A. and Musatova M.V. 2013. Separation of organic materials of nature waters into autochthonous and allochthonous components by diethylaminoethyl-cellulose adsorption. Bulletin MSRU. Series Natural Sciences, 3: 63–68. [In Russian].

Lozovik P.A., Ryzhakov A.V. and Sabylina A.V. 2011. The processes of transformation, cycle, and formation of the matter in natural waters. Transactions of Karelian Research Centre of the RAS, 4: 21–28. [In Russian].

Menshutkin V.V. 2010. The workmanship of modelling. Karelian Research Centre of the RAS, Petrozavodsk, 419 p. [In Russian].

Meshherjakova A.I. 1975. Primary production in the Baikal. In: Circulation of matter and energy in lake waterbodies. Nauka, Novosibirsk: 20–27. [In Russian].

Mineeva N.M., Shhur L.A. and Bondarenko N.A. 2012. The functioning of phytoplankton in large freshwater systems under different provision by resources. Hydrobiological journal, 48(3): 21–33. [In Russian]. https://doi.org/10.1615/HydrobJ.v48.i5.20

Moran M.A. and Hodson R.E. 1990. Bacterial production on humic and nonhumic components of dissolved organic carbon Limnology and Oceanography, 35: 1744–1756. https://doi.org/10.4319/lo.1990.35.8.1744

Morana C., Sarmento H., Descy J.P., Gasol J.M., Borges A.V., Bouillon S., and Darchambeau F. 2014. Production of dissolved organic matter by phytoplankton and its uptake by heterotrophic prokaryotes in large tropical lakes. Limnology and Oceanography, 59(4): 1364–1375. https://doi.org/10.4319/lo.2014.59.4.1364

Ostapenia A.P., Parparov A. and Berman T. 2009. Lability of organic carbon in lakes of different trophic status. Freshwater Biology, 54: 1312–1323. https://doi.org/10.1111/j.1365-2427.2009.02183.x

Rumjancev V.A. and Kondrat’ev S.A. (Eds.) 2013. Ladoga. Institute of Limnology of the RAS, Saint Petersburg, 568 p. [In Russian].

Rumjancev V.A. and Kuderskij L.A. 2010. Ladoga Lake: overall performance of the ecological status. Society. Environment. Development (Terra Humana), 1: 171–182. [In Russian].

Skopincev B.A. and Bakulina A.G. 1966. Organic matter in water of the Rybinskoe reservoir in 1964. In: Production and cycle of organic matter in inner waterbodies. Nauka, Moscow–Leningrad: 3–52. [In Russian].

Skopincev B.A. and Goncharova I.A. 1987. The use of meanings of relation different organic matter indicators in natural water for its qualitative assessment. In: Modern problems of the regional and applied hydrochemistry. Gidrometeoizdat, Leningrad: 95–117. [In Russian].

Sokolov D.I. 2013. Effect of reservoirs on oxidability and color change in river water (in terms of water-supply source for Moscow). Candidate of Biological Sciences thesis. Moscow State University, Moscow, 179 p. [In Russian].

Søndergaard M. and Middelboe M. 1995. A cross-system analysis of labile dissolved organic carbon. Marine Ecology Progress Series, 118: 283–294. https://doi.org/10.3354/meps118283

Søndergaard M., Riemann B. and Jorgensen N.O.G. 1985. Extracellular organic carbon (EOC) released by phytoplankton and bacterial production. Oikos, 45(3): 323–332. https://doi.org/10.2307/3565567

Sorokin Ju.I. 1973. Primary production in seas and oceans. General ecology. Biocoenology. Hydrobiology, 1: 7–46. [In Russian].

Tranvik L.J. 1988. Availability of dissolved organic carbon for planktonic bacteria in oligotrophic lakes of differing humic content. Microbial Ecology, 16(3): 311–322. https://doi.org/10.1007/BF02011702

Tranvik L.J. 1992. Allochthonous dissolved organic matter as an energy source for pelagic bacteria and the concept of the microbial loop. Hydrobiologia, 229: 107–114. https://doi.org/10.1007/BF00006994

Tulonen T. 2004. Role of allochthonous and autochthonous dissolved organic matter (DOM) as a carbon source for bacterioplankton in boreal humic lakes. Helsinki University, Helsinki, 32 p.

Volkova S.S. 2015. Physicochemical features of organic matter composition and carbonate system formation in little lakes of Western Siberia. Candidate of Biological Sciences thesis. Tyumen State University, Tyumen, 108 p. [In Russian].

Votincev K.K. and Popovskaja G.I. 1973. About organic matter circulation in Baikal Lake. In: Circulation of matter and energy in lakes and reservoirs. Limnological Institute of the Siberian branch of the Academy of Sciences USSR, Listvenichnoe na Baikale: 75–77. [In Russian].

Waite D.T. and Duthie H.C. 1975. Heterotrophic utilization of phytoplankton metabolites by the microbiota of Sunfish Lake, Ontario. Verhandlungen des Internationalen Verein Limnologie, 19(1): 672–681. https://doi.org/10.1080/03680770.1974.11896110

Weibe W.J. and Smith D.F. 1977. Direct measurement dissolved organic matter released by phytoplankton and incorporation by microheterotrophs. Marine Biology, 42(3): 213–223. https://doi.org/10.1007/BF00397745

Wetzel R.G., Rich P.H., Miler M.C. and Allen H.L. 1972. Metabolism of dissolved and particulate detrital carbon in a temperate hard water lake. Memorie Istituto Italiano di Idrobiologia, 29: 185–243. https://doi.org/10.2172/4614952

Winberg G.G. 1960. Primary production of water bodies. Academy of Science Belorussian SSR, Minsk, 329 p. [In Russian].

Winberg G.G. (Ed.) 1975. Biological productivity of northern lakes Krivoe and Krugloe. Nauka, Leningrad, 228 p. [In Russian].

Winberg G.G. (Ed.) 1985. Ecological system of the Naroch lakes. Belarussian State University, Minsk, 303 p.

Wolter K. 1982. Bacterial incorporation of organic substances released by natural phytoplankton population. Marine Ecology Progress Series, 17(3): 287–293. https://doi.org/10.3354/meps007287