Abstract
Zooplankton is generally affected by both top-down and bottom-up regulations in aquatic ecosystems. However, the relative strength of top-down and bottom-up controls on zooplankton assemblages is not well understood. Here, we analyzed this question in five lakes of the Yangtze River basin, an area with high population density and thousands of lakes, many of them suffering multiple environmental pressures. We sampled the whole communities of five lakes in the middle reaches of Yangtze River basin from 2006 to 2011 and used structural equation modeling to evaluate the relative importance of joint top-down and bottom-up effects. With increasing total phosphorous (TP), a major shift occurred in trophic structure. Biomass of phytoplankton, rotifers, cyclopoids, and planktivorous fish significantly increased, while cladocerans and calanoids were negatively correlated with increasing TP. The bottom-up effects were strongest at the bottom of the food web (e.g., effects of TP on phytoplankton). Direct bottom-up effects of phytoplankton and other food resources (latent variable) on rotifers and cyclopoids were greater than top-down controls from planktivores. The predation pressure on crustacean zooplankton by planktivores was higher than that on rotifers. In planktivore-dominated systems, piscivores only played a marginal role, whereas they seem affected by water quality. These results suggest not only in the food web processes the important role of nutrient pollution in affecting the top of the food web in these lakes, but also that the impacts and relative strength of bottom-up and top-down controls may vary with zooplankton assemblages, indicating the complexity of food webs in degraded lakes in China.
Similar content being viewed by others
References
Akaike H (1998) Information theory and an extension of the maximum likelihood principle. In: Parzen E, Tanabe K, Kitagawa G (eds) Selected papers of Hirotugu Akaike. Springer Series in Statistics. Springer, New York, pp 199–213
APHA (American Public Health Association) (1992) Standard methods for the examination of water and wastewater, 18th edn. American Public Health Association, Washington DC
Arhonditsis G, Stow CA, Steinberg LJ, Kenney MA, Lathrop RC, McBride SJ, Reckhow KH (2006) Exploring ecological patterns with structural equation modeling and Bayesian analysis. Ecol Model 192:385–409
Attayde JL, Bozelli RL (1998) Assessing the indicator properties of zooplankton assemblages to disturbance gradients by canonical correspondence analysis. Can J Fish Aquat Sci 55:1789–1797
Bays JS, Crisman TL (1983) Zooplankton and trophic state relationships in Florida Lakes. Can J Fish Aquat Sci 40:1813–1819
Bollen KA (1989) Structural equations with latent variables. Wiley, New York
Bollen KA, Long JS (1993) Testing structural equations models. Sage, Newbury Park
Bottrell HH, Duncan A, Gliwicz ZM, Grygierek E, Herzig A, Hillbricht-Ilkowska A, Kurasawa H, Larson P, Weglenska T (1976) A review of some problems in zooplankton production studies. Nor J Zool 24:419–456
Brett MT, Goldman CR (1997) Consumer versus resource control in freshwater pelagic food webs. Science 275:384–386
Brooks LJ (1968) The effects of prey size selection by lake planktivores. Syst Biol 17:273–291
Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–35
Carpenter SR, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. Bioscience 35:634–639
Carpenter SR, Cole JJ, Hodgson JR, Kitchell JF, Pace ML, Bade D, Cottingham KL, Essington TE, Houser JN, Schindler DE (2001) Trophic cascades nutrients and lake productivity: whole-lake experiments. Ecol Monogr 71:163–186
Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323:1014–1015
Cremer MC, Smitherman RO (1980) Food habits and growth of silver and bighead carp in cages and ponds. Aquaculture 20:57–64
Cui Y, Li Z (2005) Fishery resources and conservation of environment in lakes of the Changjiang River basin. Science Publishing Company, Beijing
Culver DA, Boucherle MM, Bean DJ, Fletcher JW (1985) Biomass of freshwater crustacean zooplankton from length–weight regressions. Can J Fish Aquat Sci 42:1380–1390
Drenner RW, Strickler JR, Obrien WJ (1978) Capture probability: the role of zooplankter escape in the selective feeding of planktivorous fish. J Fish Res Board Can 35:1370–1373
Dumont HJ, Vandevelde I, Dumont S (1975) The dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters. Oecologia 19:75–97
Duncan A (1989) Food limitation and body size in the life cycles of planktonic rotifers and cladocerans. Hydrobiologia 186–187:11–28
Egertson CJ, Downing JA (2004) Relationship of fish catch and composition to water quality in a suite of agriculturally eutrophic lakes. Can J Fish Aquat Sci 61:1784–1796
Fretwell SD (1977) The regulation of plant communities by food chains exploiting them. Perspect Biol Med 20:169–185
Gough L, Grace JB (1999) Effects of environmental change on plant species density: comparing predictions with experiments. Ecology 80:882–890
Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge
Grace JB, Jutila H (1999) The relationship between species density and community biomass in grazed and ungrazed coastal meadows. Oikos 85:398–408
Grace JB, Keeley JE (2006) A structural equation model analysis of postfire plant diversity in California shrublands. Ecol Appl 16:503–514
Grace JB, Anderson TM, Olff H, Scheiner SM (2010) On the specification of structural equation models for ecological systems. Ecol Monogr 80:67–87
Hansson LA, Annadotter H, Bergman E, Hamrin SF, Jeppesen E, Kairesalo T, Luokkanen E, Nilsson PÅ, Søndergaard M, Strand J (1998) Biomanipulation as an application of food-chain theory: constraints, synthesis, and recommendations for temperate lakes. Ecosystems 1:558–574
Horton PA, Rowan M, Webster KE, Peters RH (1979) Browsing and grazing by cladoceran filter feeders. Can J Zool 57:206–212
Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732
Hurlbert S, Mulla M (1981) Impacts of mosquitofish (Gambusia affinis) predation on plankton communities. Hydrobiologia 83:125–151
Jeppesen E, Jensen JP, Søndergaard M, Lauridsen TL, Pedersen LJ, Jensen L (1997a) Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth. Hydrobiologia 342:151–164
Jeppesen E, Lauridsen TL, Mitchell SF, Burns CW (1997b) Do planktivorous fish structure the zooplankton communities in New Zealand lakes? N Z J Mar Freshw Res 31:163–173
Jeppesen E, Jensen JP, Søndergaard M, Lauridsen TL, Landkildehus F (2000a) Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshw Biol 45:201–218
Jeppesen E, Lauridsen TL, Mitchell SF, Christoffersen K, Burns CW (2000b) Trophic structure in the pelagial of 25 shallow New Zealand lakes: changes along nutrient and fish gradients. J Plankton Res 22:951–968
Jürgens K, Jeppesen E (2000) The impact of metazooplankton on the structure of the microbial food web in a shallow, hypertrophic lake. J Plankton Res 22:1047–1070
Karr JR, Dudley DR (1981) Ecological perspective on water quality goals. Environ Manag 5:55–68
Kline RB (1998) Principles and practice of structural equation modeling. Guilford Press, New York
Lazzaro X (1987) A review of planktivorous fishes: their evolution, feeding behaviours, selectivities, and impacts. Hydrobiologia 146:97–167
Lazzaro X, Drenner RW, Stein RA, Smith JD (1992) Planktivores and plankton dynamics: effects of fish biomass and planktivore type. Can J Fish Aquat Sci 49:1466–1473
McNaught DC (1975) A hypothesis to explain the succession from calanoids to cladocerans during eutrophication. Verh Int Ver Theor Angew Limnol 19:724–731
McQueen DJ, Post JR, Mills EL (1986) Trophic relationships in freshwater pelagic ecosystems. Can J Fish Aquat Sci 43:1571–1581
McQueen DJ, Johannes MRS, Post JR (1989) Bottom-up and top-down impacts on freshwater pelagic community structure. Can J Fish Aquat Sci 43:1571–1581
Mehner T, Benndorf J, Kasprzak P, Koschel R (2002) Biomanipulation of lake ecosystems: successful applications and expanding complexity in the underlying science. Freshw Biol 47:2453–2465
Mittelbach GG, Osenberg CW, Leibold MA (1988) Trophic relations and ontogenetic niche shifts in aquatic ecosystems. In: Ebenman B, Persson L (eds) Size-structured populations. Springer, Berlin
Pace ML (1986) An empirical analysis of zooplankton community size structure across lake trophic gradients. Limnol Oceanogr 31:45–55
Pace ML, Cole JJ, Carpenter SR (1998) Trophic cascades and compensation: differential responses of microzooplankton in whole-lake experiments. Ecology 79:138–152
Persson L, Diehl S, Johansson L, Andersson G, Hamrin SF (1991) Shifts in fish communities along the productivity gradient of temperate lakes—patterns and the importance of size-structured interactions. J Fish Biol 38:281–293
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Australia
Rahel FJ (1984) Factors structuring fish assemblages along a blog lake successional gradient. Ecology 65:1276–1289
Richman S, Dodson SI (1983) The effect of food quality on feeding and respiration by Daphnia and Diaptomus. Limnol Oceanogr 28:948–956
Riginos C, Grace JB (2008) Savanna tree density, herbivores, and the herbaceous community: bottom-up vs. top-down effects. Ecology 89:2228–2238
Rosemond AD, Pringle CM, Ramírez A, Paul MJ (2001) A test of top-down and bottom-up control in a detritus-based food web. Ecology 82:2279–2293
Rosseel Y (2012) lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36
Ruttner-Kolisko A (1977) Suggestions for biomass calculations of plankton rotifers. Arch Hydrobiol 8:71–76
Sanders RW, Wickham SA (1993) Planktonic protozoa and metazoa: predation, food quality and population control. Mar Microb Food Webs 7:197–223
Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195:260–262
Schindler DW (1987) Detecting ecosystem responses to anthropogenic stress. Can J Fish Aquat Sci 44:6–25
Schriver P, Bøgestrand J, Jeppesen E, Søondergaard M (1995) Impact of submerged macrophytes on fish–zooplankton–phytoplankton interactions: large-scale enclosure experiments in a shallow eutrophic lake. Freshw Biol 33:255–270
Shapiro J, Lamarra V, Lynch M (1975) Biomanipulation: an ecosystem approach to lake restoration. In: Brezonik PL, Fox JL (eds) Water quality management through biological control. University of Florida, Gainesville, pp 85–96
Sládeček V (1983) Rotifers as indicators of water quality. Hydrobiologia 100:169–201
Smith VH, Tilman GD, Nekola JC (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 100:179–196
Timms RM, Moss B (1984) Prevention of growth of potentially dense phytoplankton populations by zooplankton grazing, in the presence of zooplanktivorous fish, in a shallow wetland ecosystem. Limnol Oceanogr 29:472–486
Ullman JB, Bentler PM (2012) Structural equation modeling. In: Weiner IB, Schinka JA, Velicer WF (eds) Handbook of psychology. Wiley, New York
van Donk E, van de Bund WJ (2002) Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquat Bot 72:261–274
White TCR (1978) The importance of a relative shortage of food in animal ecology. Oecologia 33:71–86
Xie P, Liu J (2001) Practical success of biomanipulation using filter-feeding fish to control cyanobacteria blooms: a synthesis of decades of research and application in a subtropical hypereutrophic lake. Sci World J 1:337–356
Yang Y, Huang X, Liu J, Jiao N (2005) Effects of fish stocking on the zooplankton community structure in a shallow lake in China. Fish Manag Ecol 12:81–89
Yoshida T, Urabe J, Elser JJ (2003) Assessment of ‘top-down’ and ‘bottom-up’ forces as determinants of rotifer distribution among lakes in Ontario, Canada. Ecol Res 18:639–650
Acknowledgments
We thank Sabine Giessler, the editor, and two anonymous reviewers for helpful comments and suggestions on the manuscript. This work was supported by a Special Fund for Agro-scientific Research in the Public Interest (Grant No. 20130356); the R and D Project of the Ministry of Science and Technology of China (Grant No. 2012BAD25B08); and Projects of the National Natural Science Foundation of China (Grant Nos. 30830025 and 31201994). Financial support to EGB was provided by the Spanish Ministry of Economy and Competitiveness (Project CGL2013-43822-R), the Government of Catalonia (Ref. 2014 SGR 484), and the European Commission (Erasmus Mundus Partnerships “TECHNO” and “TECHNO II”).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Sabine Giessler.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Du, X., García-Berthou, E., Wang, Q. et al. Analyzing the importance of top-down and bottom-up controls in food webs of Chinese lakes through structural equation modeling. Aquat Ecol 49, 199–210 (2015). https://doi.org/10.1007/s10452-015-9518-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-015-9518-3