Differential responses of size‐based functional groups to bottom–up and top–down perturbations in pelagic food webs: a meta‐analysis

We performed a meta-analysis of 31 lake mesocosm experiments to investigate diff erences in the responses of pelagic food chains and food webs to nutrient enrichment and fi sh presence. Trophic levels were divided into size-based functional groups (phytoplankton into highly edible and poorly edible algae, and zooplankton into small herbivores, large herbivores and omnivorous zooplankton) in the food webs. Our meta-analysis shows that 1) nutrient enrichment has a positive eff ect on phytoplankton and zooplankton, while fi sh presence has a positive eff ect on phytoplankton and a negative eff ect on zooplankton in the food chains; 2) nutrient enrichment has a positive eff ect on highly edible algae and small herbivores, but no eff ect on poorly edible algae, large herbivores and omnivorous zooplankton in the food webs. Planktivorous fi sh have a positive eff ect on highly edible algae and small herbivores, a negative eff ect on large herbivores and omnivorous zooplankton, and no eff ect on poorly edible algae. Our meta-analysis confi rms that nutrient enrichment and planktivorous fi sh aff ect functional groups diff erentially within trophic levels, revealing important changes in the functioning of food webs. Th e analysis of fi sh eff ects shows the well-described trophic cascade in the food chain and reveals two trophic cascades in the food web: one transmitted by large herbivores that benefi t highly edible phytoplankton, and one transmitted by omnivorous zooplankton that benefi t small herbivores. Comparison between the responses of food webs and simple food chains also shows consistent biomass compensation between functional groups within trophic levels.

[1]  Z. Adámek,et al.  Bioturbation of sediments by benthic macroinvertebrates and fish and its implication for pond ecosystems: a review , 2012, Aquaculture International.

[2]  Miquel Lürling,et al.  Beyond the Plankton Ecology Group (PEG) Model : Mechanisms Driving Plankton Succession , 2012 .

[3]  S. Diehl,et al.  Simple rules describe bottom-up and top-down control in food webs with alternative energy pathways. , 2012, Ecology letters.

[4]  María González,et al.  Phytoplankton communities and stoichiometry are interactively affected by light, nutrients, and fish , 2011 .

[5]  Michel Loreau,et al.  From Populations to Ecosystems: Theoretical Foundations for a New Ecological Synthesis , 2010 .

[6]  J. L. Attayde,et al.  Effects of omnivorous filter‐feeding fish and nutrient enrichment on the plankton community and water transparency of a tropical reservoir , 2010 .

[7]  J. Jones,et al.  Weedbeds and big bugs: the importance of scale in detecting the influence of nutrients and predation on macroinvertebrates in plant‐dominated shallow lakes , 2010 .

[8]  M. Loreau,et al.  The Causes and Consequences of Compensatory Dynamics in Ecological Communities , 2009 .

[9]  Stéphane Legendre,et al.  Predator foraging behaviour drives food-web topological structure. , 2009, The Journal of animal ecology.

[10]  María González,et al.  Light, nutrients, and food-chain length constrain planktonic energy transfer efficiency across multiple trophic levels , 2008, Proceedings of the National Academy of Sciences.

[11]  Elena Litchman,et al.  Trait-Based Community Ecology of Phytoplankton , 2008 .

[12]  Helmut Hillebrand,et al.  A cross-system synthesis of consumer and nutrient resource control on producer biomass. , 2008, Ecology letters.

[13]  I. Vila,et al.  Short-term responses of phytoplankton to nutrient enrichment and planktivorous fish predation in a temperate South American mesotrophic reservoir , 2008, Hydrobiologia.

[14]  I. Domaizon,et al.  Community composition of lacustrine small eukaryotes in hyper-eutrophic conditions in relation to top-down and bottom-up factors. , 2007, FEMS microbiology ecology.

[15]  M. Loreau,et al.  Nutrient-limited food webs with up to three trophic levels: feasibility, stability, assembly rules, and effects of nutrient enrichment. , 2006, Theoretical population biology.

[16]  Z. Brandl.  Freshwater Copepods and Rotifers: Predators and their Prey , 2005, Hydrobiologia.

[17]  J. Huisman,et al.  Benthic-pelagic coupling in the population dynamics of the harmful cyanobacterium Microcystis , 2005 .

[18]  S. D. Cooper,et al.  WHAT DETERMINES THE STRENGTH OF A TROPHIC CASCADE , 2005 .

[19]  E. Bécares,et al.  A 2-year experimental study on nutrient and predator influences on food web constituents in a shallow lake of north-west Spain , 2004 .

[20]  T. Kairesalo,et al.  Community resistance and change to nutrient enrichment and fish manipulation in a vegetated lake littoral , 2004 .

[21]  Eloy Bécares,et al.  Responses of phytoplankton to fish predation and nutrient loading in shallow lakes: a pan-European mesocosm experiment , 2004 .

[22]  Maria Rosa Miracle,et al.  Mesocosm experiments on nutrient and fish effects on shallow lake food webs in a Mediterranean climate , 2004 .

[23]  Eloy Bécares,et al.  Continental-scale patterns of nutrient and fish effects on shallow lakes: introduction to a pan-European mesocosm experiment , 2004 .

[24]  L. Hansson,et al.  Responses to fish predation and nutrients by plankton at different levels of taxonomic resolution , 2004 .

[25]  K. Rengefors,et al.  Factors regulating the recruitment of cyanobacterial and eukaryotic phytoplankton from littoral and profundal sediments , 2004 .

[26]  Ruẑena Markošová,et al.  Bacterioplankton interactions with Daphnia and algae in experimental enclosures , 1993, Hydrobiologia.

[27]  J. D. Smith,et al.  Responses of a eutrophic pond community to separate and combined effects of N:P supply and planktivorous fish: a mesocosm experiment , 1990, Hydrobiologia.

[28]  U. Uehlinger,et al.  Can results from limnocorral experiments be transferred to in situ conditions? , 1988, Hydrobiologia.

[29]  Maria Rosa Miracle,et al.  Continental-scale patterns of nutrient and fish effects on shallow lakes: introduction to a pan-European mesocosm experiment , 2004 .

[30]  Michel Loreau,et al.  Food-web constraints on biodiversity–ecosystem functioning relationships , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Elizabeth T. Borer,et al.  A cross-ecosystem comparison of the strength of trophic cascades , 2002 .

[32]  Maria-José Caramujo,et al.  Induction and costs of tail spine elongation in Daphnia hyalina×galeata: reduction of susceptibility to copepod predation , 2000 .

[33]  K. Rothhaupt.  Plankton population dynamics: food web interactions and abiotic constraints , 2000 .

[34]  Michel Loreau,et al.  Functional diversity governs ecosystem response to nutrient enrichment , 2000, Nature.

[35]  Gérard Lacroix,et al.  Plankton dynamics in planktivore- and piscivore-dominated mesocosms , 2000 .

[36]  O. Schmitz,et al.  Trophic Cascades in Terrestrial Systems: A Review of the Effects of Carnivore Removals on Plants , 2000, The American Naturalist.

[37]  Cole,et al.  Trophic cascades revealed in diverse ecosystems. , 1999, Trends in ecology & evolution.

[38]  Micheli,et al.  Eutrophication, Fisheries, and Consumer-Resource Dynamics in Marine Pelagic Ecosystems. , 1999, Science.

[39]  G. Polis,et al.  Why Are Parts of the World Green? Multiple Factors Control Productivity and the Distribution of Biomass , 1999 .

[40]  L. Persson.  Trophic cascades : abiding heterogeneity and the trophic level concept at the end of the road , 1999 .

[41]  Gérard Lacroix,et al.  Body size and reproductive investment of Daphnia galeata under predation by cyprinid fishes : A mesocosm study , 1998 .

[42]  Peter J. Morin,et al.  Productivity controls food-chain properties in microbial communities , 1998, Nature.

[43]  L. Tranvik,et al.  Consumption patterns, complexity and enrichment in aquatic food chains , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[44]  Alan Hastings,et al.  Trophic cascades and trophic trickles in pelagic food webs , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[45]  Jonathan M. Chase,et al.  Species Turnover and the Regulation of Trophic Structure , 1997 .

[46]  Robert D. Holt,et al.  A Theoretical Framework for Intraguild Predation , 1997, The American Naturalist.

[47]  M. Leibold.  Do nutrient-competition models predict nutrient availabilities in limnetic ecosystems? , 1997, Oecologia.

[48]  Michael T. Brett,et al.  Consumer Versus Resource Control in Freshwater Pelagic Food Webs , 1997, Science.

[49]  C. Goldman,et al.  A meta-analysis of the freshwater trophic cascade. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[50]  P. Hamilton,et al.  Effects of Nutrients and Planktivorous Fish on the Phytoplankton of Shallow and Deep Aquatic Systems , 1996 .

[51]  Mathew A. Leibold,et al.  A Graphical Model of Keystone Predators in Food Webs: Trophic Regulation of Abundance, Incidence, and Diversity Patterns in Communities , 1996, The American Naturalist.

[52]  G. Polis,et al.  Food Web Complexity and Community Dynamics , 1996, The American Naturalist.

[53]  D. Culver,et al.  Separate and Combined Effects of Larval Walleye and Fertilization on Plankton Community Structure in Enclosures , 1995 .

[54]  Peter A. Abrams,et al.  Effect of Increased Productivity on the Abundances of Trophic Levels , 1993, The American Naturalist.

[55]  S. Carpenter,et al.  The trophic cascade in lakes: Contents , 1993 .

[56]  Edward McCauley,et al.  Sigmoid Relationships between Phosphorus, Algal Biomass, and Algal Community Structure , 1992 .

[57]  M. Hunter,et al.  Playing Chutes and Ladders: Heterogeneity and the Relative Roles of Bottom‐Up and Top‐Down Forces in Natural Communities , 1992, Ecology.

[58]  Donald R. Strong,et al.  ARE TROPHIC CASCADES ALL WET? DIFFERENTIATION AND DONOR-CONTROL IN SPECIOSE ECOSYSTEMS' , 1992 .

[59]  M. Power,et al.  TOP-DOWN AND BOTTOM-UP FORCES IN FOOD WEBS: DO PLANTS HAVE PRIMACY? , 1992 .

[60]  Orlando Sarnelle,et al.  Nutrient Enrichment and Grazer Effects on Phytoplankton in Lakes , 1992 .

[61]  C. Kraft,et al.  Confounded impacts of planktivorous fish on freshwater biomanipulations , 1992 .

[62]  M. Leibold,et al.  Interactions between food-web structure and nutrients on pond organisms , 1992, Nature.

[63]  Micro- and mesozooplankton grazing on natural pico- and nanoplankton in contrasting plankton communities produced by planktivore manipulation and fertilization , 1990 .

[64]  M. A. Leibold,et al.  Resource Edibility and the Effects of Predators and Productivity on the Outcome of Trophic Interactions , 1989, The American Naturalist.

[65]  J. D. Smith,et al.  Interdependence of phosphorus, fish, and site effects on phytoplankton biomass and zooplankton , 1989 .

[66]  J. J. Gilbert.  Suppression of rotifer populations by Daphnia: A review of the evidence, the mechanisms, and the effects on zooplankton community structure1 , 1988 .

[67]  M. Vanni.  Effects of Nutrients and Zooplankton Size on the Structure of a Phytoplankton Community , 1987 .

[68]  M. Vanni.  Effects of Food Availability and Fish Predation on a Zooplankton Community , 1987 .

[69]  B. Riemann.  Potential Importance of Fish Predation and Zooplankton Grazing on Natural Populations of Freshwater Bacteria , 1985, Applied and environmental microbiology.

[70]  L. Oksanen,et al.  Exploitation Ecosystems in Gradients of Primary Productivity , 1981, The American Naturalist.

[71]  M. Lynch,et al.  Predation, enrichment, and phytoplankton community structure1 , 1981 .

[72]  D. J. Hall,et al.  The Size-Efficiency Hypothesis and the Size Structure of Zooplankton Communities , 1976 .

[73]  S. Dodson.  Adaptive change in plankton morphology in response to size-selective predation: A new hypothesis of cyclomorphosis , 1974 .

[74]  C. Burns.  THE RELATIONSHIP BETWEEN BODY SIZE OF FILTER‐FEEDING CLADOCERA AND THE MAXIMUM SIZE OF PARTICLE INGESTED , 1968 .

[75]  S. Dodson,et al.  Predation, Body Size, and Composition of Plankton. , 1965, Science.