Plankton community properties determined by nutrients and size-selective feeding

The potential impacts of climate change on marine planktonic ecosystems remain difficult to predict. Climate forcing can alter nutrient availability and preda- tor community composition, and here we show that these shifts may dramatically alter plankton trophic structure, size distributions and biomass. We modeled phytoplank- ton and zooplankton as a highly resolved size spectrum with size-dependent nutrient uptake and predation and analyzed the model both as a size spectrum and as a food web. Model results identified 2 distinct regimes defined by the average zooplankton feeding preferences. Regime I communities, where planktonic predators are specialists or large relative to prey, had low omnivory, many top predators, low connectance and relatively flat size spec- tra. Regime II communities, where predators are general- ists or small relative to prey, had a high degree of om- nivory, no top predators, high connectance and steep size spectra. Model ecosystems with generalist predators had lower size diversity, smaller plankton and gappier size distributions than ecosystems with specialist predators. Nutrient availability had little influence on trophic struc- ture but strongly impacted size structure and biomass. Most surprisingly, phytoplankton biomass sometimes de- creased with added nutrients if predators were small rela- tive to prey, implying that both predators and nutrients mediate shifts between bottom-up and top-down control. Based on our synthesized estimates of size-selective feed- ing parameters, we infer that size and trophic structure should be strongly affected by abundances of generalist, bloom-forming taxa such as salps and jellyfish, many of which are responsive to ocean temperature. Size-selective feeding fundamentally affects community structure and is a likely mechanism of change in planktonic ecosystems where community composition varies with temperature.

[1]  P. K. Bjørnsen,et al.  Zooplankton grazing and growth: Scaling within the 2‐2,‐μm body size range , 1997 .

[2]  U. Larsson,et al.  Size-selective grazing by a microflagellate on pelagic bacteria , 1986 .

[3]  J. T. Turner Zooplankton fecal pellets, marine snow and sinking phytoplankton blooms , 2002 .

[4]  Simon Jennings,et al.  Use of size-based production and stable isotope analyses to predict trophic transfer efficiencies and predator-prey body mass ratios in food webs , 2002 .

[5]  S. Pearre Feeding by Chaetognatha : the relation of prey size to predator size in several species , 1980 .

[6]  B. Hansen Feeding behaviour in larvae of the opisthobranchPhiline aperta , 1991 .

[7]  E. Tang,et al.  The allometry of algal growth rates , 1995 .

[8]  E. Houde,et al.  Relative predation potentials of scyphomedusae ctenophores and planktivorous fish on ichthyoplankfon in Chesapeake Bay , 1993 .

[9]  P. K. Bjørnsen,et al.  The size ratio between planktonic predators and their prey , 1994 .

[10]  T. Shiganova Invasion of the Black Sea by the ctenophore Mnemiopsis leidyi and recent changes in pelagic community structure , 1998 .

[11]  J. H. Cowan,et al.  Predation by the scyphomedusan Chrysaora quinquecirrha on Mnemiopsis leidyi ctenophores , 1995 .

[12]  D. Scavia,et al.  Feeding rate of Diaptomus sicilis and its relation to selectivity and effective food concentration in algal mixtures and in Lake Michigan , 1984 .

[13]  Per Juel Hansen,et al.  Zooplankton grazing and growth: Scaling within the 2–2,000‐µm body size range , 2000 .

[14]  M. Ohman,et al.  Composition and potential grazing impact of salp assemblages off Baja California during the 1997-1999 El Niño and La Nina , 2006 .

[15]  Claudia E. Mills,et al.  Evidence for a substantial increase in gelatinous zooplankton in the Bering Sea, with possible links to climate change , 1999 .

[16]  Martin Edwards,et al.  Climate‐related increases in jellyfish frequency suggest a more gelatinous future for the North Sea , 2007 .

[17]  Neo D. Martinez,et al.  Network structure and biodiversity loss in food webs: robustness increases with connectance , 2002, Ecology Letters.

[18]  J. G. Field,et al.  General allometric equations for rates of nutrient uptake, ingestion, and respiration in plankton organisms , 1989 .

[19]  Nicholas R. Bates,et al.  Pelagic functional group modeling: Progress, challenges and prospects , 2006 .

[20]  J. Passarge,et al.  Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells , 1996 .

[21]  K. Rothhaupt,et al.  Feeding rates of macro- and microzooplankton on heterotrophic nanoflagellates , 1996 .

[22]  Andrea Rinaldo,et al.  Microbial size spectra from natural and nutrient enriched ecosystems , 2001 .

[23]  James J. McCarthy,et al.  HALF‐SATURATION CONSTANTS FOR UPTAKE OF NITRATE AND AMMONIUM BY MARINE PHYTOPLANKTON1 , 1969 .

[24]  J. Purcell Dietary composition and diel feeding patterns of epipelagic siphonophores , 1981 .

[25]  P. J. Hansen Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale , 1992 .

[26]  Daniel E. Schindler,et al.  Climatic effects on the phenology of lake processes , 2004 .

[27]  F. Ibaňez,et al.  Long‐term fluctuations (1974‐99) of the salps Thalia democratica and Salpa fusiformis in the northwestern Mediterranean Sea: Relationships with hydroclimatic variability , 2006 .

[28]  P. Morand,et al.  Long-term fluctuations of Pelagia noctiluca (Cnidaria, Scyphomedusa) in the western Mediterranean Sea. Prediction by climatic variables , 1989 .

[29]  L. Bern Postcapture particle size selection by Daphnia cucullata (Cladocera) , 1990 .

[30]  L. Naustvoll Prey size spectra in naked heterotrophic dinoflagellates , 2000 .

[31]  M. Barangé,et al.  Diet and feeding of Euphausia hanseni and Nematoscelis megalops (Euphausiacea) in the northern Benguela Current: ecological significance of vertical space partitioning , 1991 .

[32]  T. Kiørboe,et al.  Mortality of marine planktonic copepods: global rates and patterns , 2002 .

[33]  Glenn R. Flierl,et al.  Behavior of a simple plankton model with food-level acclimation by herbivores , 1986 .

[34]  A. Alldredge,et al.  Feeding rates of the doliolid, Dolioletta gegenbauri , on diatoms and bacteria , 1991 .

[35]  J. Benndorf,et al.  Climate-driven warming during spring destabilises a Daphnia population: a mechanistic food web approach , 2007, Oecologia.

[36]  Mark E. Baird,et al.  A size-resolved pelagic ecosystem model , 2007 .

[37]  Dieter Gerten,et al.  Climate‐driven changes in spring plankton dynamics and the sensitivity of shallow polymictic lakes to the North Atlantic Oscillation , 2000 .

[38]  M. Landry,et al.  Predatory feeding behavior of the marine cyclopoid copepod Corycaeus anglicus , 1985 .

[39]  H. Saito,et al.  Feeding rates in the chaetognath Sagitta elegans: effects of prey size, prey swimming behaviour and small-scale turbulence , 2001 .

[40]  W. Hahm,et al.  Prey selection based on predator/prey weight ratios for some northwest Atlantic fish , 1984 .

[41]  Ulrich Brose,et al.  Complex food webs prevent competitive exclusion among producer species , 2008, Proceedings of the Royal Society B: Biological Sciences.

[42]  Werner Ulrich,et al.  Consumer-resource body-size relationships in natural food webs. , 2006, Ecology.

[43]  R. W. Sheldon,et al.  Structure of Pelagic Food Chain and Relationship Between Plankton and Fish Production , 1977 .

[44]  R. P. Hassett,et al.  Feeding behavior of large calanoid copepodsNeocalanus cristatus andN. plumchrus from the subarctic Pacific Ocean , 1983 .

[45]  Dean Roemmich,et al.  Climatic Warming and the Decline of Zooplankton in the California Current , 1995, Science.

[46]  M. Ohman,et al.  Long-term changes in pelagic tunicates of the California Current , 2003 .

[47]  S. Wood,et al.  Mortality estimation for planktonic copepods: Pseudocalanus newmani in a temperate fjord , 1996 .

[48]  G. Paffenhöfer,et al.  Modes of algal capture by the freshwater copepod Diaptomus sicilis and their relation to food‐size selection1,2 , 1985 .

[49]  A. Brierley,et al.  Jellyfish abundance and climatic variation: contrasting responses in oceanographically distinct regions of the North Sea, and possible implications for fisheries , 2005, Journal of the Marine Biological Association of the United Kingdom.

[50]  K. Šimek,et al.  Direct and Indirect Evidence of Size-Selective Grazing on Pelagic Bacteria by Freshwater Nanoflagellates , 1992, Applied and environmental microbiology.

[51]  David A. Siegel,et al.  Climate-driven trends in contemporary ocean productivity , 2006, Nature.

[52]  The stability of an NPZ model subject to realistic levels of vertical mixing , 2000 .

[53]  M. Ohman,et al.  Coherence of long-term variations of zooplankton in two sectors of the California Current System , 2007 .

[54]  John H. Steele,et al.  A Simple Plankton Model , 1981, The American Naturalist.

[55]  Ø. Moestrup,et al.  Prey size spectrum and bioenergetics of the mixotrophic dinoflagellate Karlodinium armiger , 2008 .

[56]  J. Purcell,et al.  Effects of climate on relative predation by scyphomedusae and ctenophores on copepods in Chesapeake Bay during 1987‐2000 , 2005 .

[57]  A. Atkinson Omnivory and feeding selectivity in five copepod species during spring in the Bellingshausen Sea, Antarctica , 1995 .

[58]  K. Šimek,et al.  Functional response and particle size selection of Halteria cf. grandinella, a common freshwater oligotrichous ciliate , 2000 .

[59]  Thomas M. Powell,et al.  Bottom–up and top–down forcing in a simple size-structured plankton dynamics model , 2008 .

[60]  Daniel Kamykowski,et al.  Predicting plant nutrient concentrations from temperature and sigma-t in the upper kilometer of the world ocean , 1986 .

[61]  W. G. Sprules,et al.  Plankton Size Spectra in Relation to Ecosystem Productivity, Size, and Perturbation , 1986 .

[62]  H. Stibor,et al.  Feeding selectivities of the marine cladocerans Penilia avirostris, Podon intermedius and Evadne nordmanni , 2004 .

[63]  R. Armstrong A hybrid spectral representation of phytoplankton growth and zooplankton response: The control rod model of plankton interaction , 2003 .

[64]  Edward Brinton,et al.  Decadal variability in abundances of the dominant euphausiid species in southern sectors of the California Current , 2003 .

[65]  M. Sprung,et al.  Physiological energetics of mussel larvae (Mytilus edulis). II. Food uptake , 1984 .

[66]  Neo D. Martinez,et al.  Predicting invasion success in complex ecological networks , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[67]  T. Gross,et al.  Predicting the distribution of the scyphomedusa Chrysaora quinquecirrha in Chesapeake Bay , 2007 .

[68]  C. Duarte,et al.  Biomass distribution in marine planktonic communities , 1997 .

[69]  E. Sherr,et al.  Clearance rates of < 6 µm fluorescently labeled algae (FLA) by estuanne protozoa. potential grazing impact of flagellates and ciliates , 1991 .

[70]  T. Nielsen,et al.  On the trophic coupling between protists and copepods in arctic marine ecosystems , 2000 .

[71]  R. Lukatelich,et al.  Ratio-based trophic niche breadths of fish, the Sheldon spectrum, and the size-efficiency hypothesis , 1986 .

[72]  P. Driessche,et al.  Dispersal data and the spread of invading organisms. , 1996 .

[73]  O. Setälä,et al.  Simultaneous measurement of food particle selection and clearance rates of planktonic oligotrich ciliates (Ciliophora: Oligotrichina) , 1995 .

[74]  John H. Steele,et al.  The Structure of Plankton Communities , 1977 .

[75]  A. Hastings,et al.  Weak trophic interactions and the balance of nature , 1998, Nature.

[76]  J. G. Field,et al.  The size-based dynamics of plankton food webs. I. A simulation model of carbon and nitrogen flows , 1991 .

[77]  T. F. Hansen,et al.  Feeding selectivities and food niche separation of Acartia clausi, Penilia avirostris (Crustacea) and Doliolum denticulatum (Thaliacea) in Blanes Bay (Catalan Sea, NW Mediterranean) , 2004 .

[78]  S. Navarrete,et al.  Feeding by larvae of intertidal invertebrates: assessing their position in pelagic food webs. , 2006, Ecology.

[79]  Neo D. Martinez,et al.  Allometric scaling enhances stability in complex food webs. , 2006, Ecology letters.

[80]  Thilo Gross,et al.  Generalized Models Reveal Stabilizing Factors in Food Webs , 2009, Science.

[81]  Anthony J. Richardson,et al.  Climate Impact on Plankton Ecosystems in the Northeast Atlantic , 2004, Science.

[82]  James H. Brown,et al.  Toward a metabolic theory of ecology , 2004 .

[83]  H. Jakobsen,et al.  Prey size selection, grazing and growth response of the small heterotrophic dinoflagellate Gymnodinium sp. and the ciliate Balanion comatum--a comparative study , 1997 .

[84]  B. Monger,et al.  Foraging Behavior and Prey Selection by the Ambush Entangling Predator Pleurobrachia Bachei , 1986 .

[85]  K. Rothhaupt Differences in particle size-dependent feeding efficiencies of closely related rotifer species , 1990 .

[86]  W. Silvert,et al.  Energy flux in the pelagic ecosystem: A time‐dependent equation , 1978 .

[87]  S. Arima,et al.  Feeding characteristics of two tintinnid ciliate species on phytoplankton including harmful species: effects of prey size on ingestion rates and selectivity. , 2001, Journal of experimental marine biology and ecology.

[88]  J. Huggett,et al.  Prey selection by Euphausia lucens (Hansen) and feeding behaviour in response to a mixed algal and animal diet , 1992 .

[89]  R. W. Sheldon,et al.  The Size Distribution of Particles in the OCEAN1 , 1972 .

[90]  L. Naustvoll Prey size spectra and food preferences in thecate heterotrophic dinoflagellates , 2000 .

[91]  B. Meyer,et al.  Feeding and energy budgets of Antarctic krill Euphausia superba at the onset of winter—I. Furcilia III larvae , 2002 .

[92]  B. Meyer,et al.  Feeding and energy budgets of Antarctic krill Euphausia superba at the onset of winter—II. Juveniles and adults , 2002 .

[93]  M. Edwards,et al.  A long‐term chlorophyll dataset reveals regime shift in North Sea phytoplankton biomass unconnected to nutrient levels , 2007 .

[94]  B. K. Sullivan,et al.  Vulnerability of the copepod Acartia tonsa to predation by the scyphomedusa Chrysaora quinquecirrha : effect of prey size and behavior , 1998 .

[95]  I. Urrutxurtu Seasonal succession of tintinnids in the Nervión River estuary, Basque Country, Spain , 2004 .

[96]  Joan Saldaña,et al.  Body sizes of animal predators and animal prey in food webs , 1993 .

[97]  W. Peterson,et al.  Copepod biodiversity as an indicator of changes in ocean and climate conditions of the northern California current ecosystem , 2006 .

[98]  B. S. Baldwin Selective particle ingestion by oyster larvae (Crassostrea virginica) feeding on natural seston and cultured algae , 1995 .

[99]  P. Franks,et al.  Size-structured planktonic ecosystems: constraints, controls and assembly instructions , 2010, Journal of plankton research.

[100]  M. Ohman,et al.  Planktonic Foraminifera of the California Current Reflect 20th-Century Warming , 2006, Science.

[101]  F. Rassoulzadegan,et al.  Grazing rate of the tintinnid Stenosemella ventricosa (Clap. & Lachm.) Jorg. on the spectrum of the naturally occurring particulate matter from a Mediterranean neritic area1 , 1981 .

[102]  U. Båmstedt,et al.  Euphausiid predation on copepods in coastal waters of the Northeast Atlantic , 1998 .

[103]  M. Neubert,et al.  Body size and food web structure: testing the equiprobability assumption of the cascade model , 2000, Oecologia.

[104]  Jerry C. Blackford,et al.  Self-assembling food webs : a global viewpoint of coexistence of species in Lotka-Volterra communities , 1992 .

[105]  H. Moser,et al.  Long-term trends and variability in the larvae of Pacific sardine and associated fish species of the California Current region , 2003 .

[106]  C. Greene,et al.  Patterns of Prey Selection in the Cruising Calanoid Predator Euchaeta elongata , 1985 .

[107]  Laurence P. Madin,et al.  Field observations on the feeding behavior of salps (Tunicata: Thaliacea) , 1974 .

[108]  Charles M. Newman,et al.  A stochastic theory of community food webs I. Models and aggregated data , 1985, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[109]  Johan van de Koppel,et al.  Reconciling complexity with stability in naturally assembling food webs , 2009, Nature.

[110]  G. Hays,et al.  Interspecific differences in the diel vertical migration of marine copepods: The implications of size, color, and morphology , 1994 .

[111]  Mark Kot,et al.  Dispersal and Pattern Formation in a Discrete-Time Predator-Prey Model , 1995 .

[112]  L. Madin,et al.  Zooplankton feeding ecology: clearance and ingestion rates of the salps Thalia democratica, Cyclosalpa affinis and Salpa cylindrica on naturally occurring particles in the Mid-Atlantic Bight , 2004 .

[113]  L. Madin,et al.  Feeding, metabolism. and growth of Cyclosalpa bakeri in the subarctic Pacific , 1992 .

[114]  Owen L Petchey,et al.  Size, foraging, and food web structure , 2008, Proceedings of the National Academy of Sciences.

[115]  K. Børsheim,et al.  Grazing and food size selection by crustacean zooplankton compared to production of bacteria and phytoplankton in a shallow Norwegian mountain lake , 1987 .

[116]  H. Jeong,et al.  Growth and Grazing Rates of the Heterotrophic Dinoflagellate Polykrikos kofoidii on Red-Tide and Toxic Dinoflagellates , 2001, The Journal of eukaryotic microbiology.

[117]  M. Martinussen,et al.  Nutritional ecology of gelatinous planktonic predators. Digestion rate in relation to type and amount of prey , 1999 .

[118]  Dietmar Straile,et al.  The North Atlantic Oscillation and plankton dynamics in two European lakes –‐ two variations on a general theme , 2000 .

[119]  R. Law,et al.  Size-spectra dynamics from stochastic predation and growth of individuals. , 2009, Ecology.