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Emergent multiple predator effects in an experimental microbial community

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Ecological Research

Abstract

Studies on multiple predator effects have typically focused on metazoans. Here we examined the effects of multiple consumers on bacteria. Specifically, we investigated the separate and combined effects of two common bacterivorous ciliates, Colpidium striatum and Paramecium caudatum, on a simple bacterial assemblage. Non-additive multiple predator effects emerged for all bacterial species significantly affected by grazing, where bacterial responses in the two-consumer treatment cannot be predicted by summing the separate effects of the two consumers. Some species showed risk reduction (observed responses less than expected), whereas others showed risk enhancement (observed responses larger than expected). We attributed risk alteration to the interference between the two consumers. Contradictory to theoretical predictions, total bacterial abundance in the two-consumer treatment did not differ from single-consumer treatments and consumer-free controls, due largely to risk reduction and compensatory responses within the bacterial assemblage. Decomposition of particulate organic matter was greater in the two-consumer treatment than the Paramecium single-consumer treatment, but did not differ among other treatments. These results suggest that the presence of multiple consumers may have unexpected impacts on the structure and functioning of bacterial communities.

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References

  • Aarssen LW (1997) High productivity in grassland ecosystems: effected by species diversity or productive species. Oikos 80:183–184

    Article  Google Scholar 

  • Begon M, Townsend CR, Harper JL (1998) Ecology: individuals, populations and communities. Blackwell Science, Malden

    Google Scholar 

  • Belovsky GE, Slade JB (2000) Insect herbivory accelerates nutrient cycling and increases plant production. Proc Natl Acad Sci USA 97:14412–14417

    Article  PubMed  CAS  Google Scholar 

  • Brett MT, Goldman CR (1997) Consumer versus resource control in freshwater pelagic food webs. Science 275:384–386

    Article  PubMed  CAS  Google Scholar 

  • Cardinale BJ, Harvey CT, Gross K, Ives AR (2003) Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecol Lett 6:857–865

    Article  Google Scholar 

  • Cochran-Stafira DL, von Ende CN (1998) Integrating bacteria into food webs: studies with Sarracenia purpurea inquilines. Ecology 79:880–898

    Article  Google Scholar 

  • Duffy JE (2002) Biodiversity and ecosystem function: the consumer connection. Oikos 99:201–219

    Article  Google Scholar 

  • Duffy JE (2003) Biodiversity loss, trophic skew and ecosystem functioning. Ecol Lett 6:680–687

    Article  Google Scholar 

  • Duffy JE, Richardson JP, Canuel EA (2003) Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol Lett 6:637–645

    Article  Google Scholar 

  • Fenchel T, Harrison P (1976) The significance of bacterial grazing and mineral cycling for the decomposition of particulate detritus. In: Anderson JM, MacFadyen A (eds) The role of terrestrial and aquatic organisms in the decomposition processes. Blackwell, Oxford, pp 285–289

    Google Scholar 

  • Finke DL, Denno RF (2004) Predator diversity dampens trophic cascades. Nature 429:407–410

    Article  PubMed  CAS  Google Scholar 

  • Fort C, Goldman CR (1981) Allelopathy between zooplankton: a mechanism for interference competition. Science 213:1133–1135

    Article  Google Scholar 

  • Fox JW (2004) Effects of algal and herbivore diversity on the partitioning of biomass within and among trophic levels. Ecology 85:549–559

    Article  Google Scholar 

  • Gamfeldt L, Hillebrand H, Jonsson PR (2005) Species richness changes across two trophic levels simultaneously affect prey and consumer biomass. Ecol Lett 8:696–703

    Article  Google Scholar 

  • Holt RD, Loreau M (2002) Biodiversity and ecosystem functioning: the role of trophic interactions and the importance of system openness. In: Kinzig AP, Pacala SW, Tilman D (eds) The functional consequences of biodiversity. Princeton University Press, Princeton, pp 246–262

    Google Scholar 

  • Hooper DU, Vitousek PM (1997) The effects of plant composition and diversity on ecosystem processes. Science 277:1302–1305

    Article  CAS  Google Scholar 

  • Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35

    Article  Google Scholar 

  • Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJM (2001) Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microbiol 67:4399–4406

    Article  PubMed  CAS  Google Scholar 

  • Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110:449–460

    Article  Google Scholar 

  • Ives AR, Cardinale BJ, Snyder WE (2005) A synthesis of subdisciplines: predator-prey interactions, and biodiversity and ecosystem functioning. Ecol Lett 8:102–116

    Article  Google Scholar 

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

    Article  PubMed  CAS  Google Scholar 

  • Jiang L, Morin PJ (2004) Temperature-dependent interactions explain unexpected responses to environmental warming in communities of competitors. J Anim Ecol 73:569–576

    Article  Google Scholar 

  • Kinzig AP, Pacala SW, Tilman D (eds) (2002) The functional consequences of biodiversity: empirical progress and theoretical extensions. Princeton University Press, Princeton

    Google Scholar 

  • Kirchman DL (ed) (2000) Microbial ecology of the oceans. Wiley-Liss, New York

  • Krupa JJ, Sih A (1998) Fishing spiders, green sunfish, and a stream-dwelling water strider: male–female conflict and prey responses to single versus multiple predator environments. Oecologia 117:258–265

    Article  Google Scholar 

  • Legrand C, Rengefors K, Fistarol GO, Graneli E (2003) Allelopathy in phytoplankton—biochemical, ecological and evolutionary aspects. Phycologia 42:406–419

    Article  Google Scholar 

  • Loreau M, Naeem S, Inchausti P (eds) (2002) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford

    Google Scholar 

  • McNaughton SJ (1985) Ecology of a grazing ecosystem: the Serengeti. Ecol Monogr 3:259–294

    Article  Google Scholar 

  • Micheli F (1999) Eutrophication, fisheries, and consumer–resource dynamics in marine pelagic ecosystems. Science 285:1396–1398

    Article  PubMed  CAS  Google Scholar 

  • Mikola J, Setala H (1998) Relating species diversity to ecosystem functioning: mechanistic backgrounds and experimental approach with a decomposer food web. Oikos 83:180–194

    Article  Google Scholar 

  • Morin PJ (1999) Community ecology. Blackwell Sciences, Malden

    Google Scholar 

  • Mulder CPH, Koricheva J, Huss-Danell K, Hoegberg P, Joshi J (1999) Insects affect relationships between plant species richness and ecosystem processes. Ecol Lett 2:237–246

    Article  Google Scholar 

  • Muller AK, Westergaard K, Christensen S, Sorensen SJ (2002) The diversity and function of soil microbial communities exposed to different disturbances. Microb Ecol 44:49–58

    Article  PubMed  CAS  Google Scholar 

  • Naeem S, Hahn DR, Schuurman G (2000) Producer–decomposer co-dependency influences biodiversity effects. Nature 403:762–764

    Article  PubMed  CAS  Google Scholar 

  • Norberg J (2000) Resource-niche complementarity and autotrophic compensation determines ecosystem-level responses to increased cladoceran species richness. Oecologia 122:264–272

    Article  Google Scholar 

  • Olff H, Ritchie ME (1998) Effects of herbivores on grassland plant diversity. Trends Ecol Evol 13:261–265

    Article  Google Scholar 

  • Pace ML (1988) Bacterial mortality and the fate of bacterial production. Hydrobiologia 159:41–49

    Google Scholar 

  • Paine RT (2002) Trophic control of production in a rocky intertidal community. Science 296:736–739

    Article  PubMed  CAS  Google Scholar 

  • Petchey OL, McPhearson PT, Casey TM, Morin PJ (1999) Environmental warming alters food-web structure and ecosystem function. Nature 402:69–72

    Article  CAS  Google Scholar 

  • Pimm SL, Russell GJ, Gittleman JL, Brooks TM (1995) The future of biodiversity. Science 269:347–350

    Article  PubMed  CAS  Google Scholar 

  • Pinhassi J, Zweifel UL, Hagstrom A (1997) Dominant marine bacterioplankton species found among colony-forming bacteria. Appl Environ Microbiol 63:3359–3366

    PubMed  CAS  Google Scholar 

  • Pinhassi J, Azam F, Hemphala J, Long RA, Martinez J, Zweifel UL, Hagstrom A (1999) Coupling between bacterioplankton species composition, population dynamics, and organic matter degradation. Aquat Microb Ecol 17:13–26

    Article  Google Scholar 

  • Polis GA (1991) Complex trophic interactions in deserts: an empirical critique of food-web theory. Am Nat 138:123–155

    Article  Google Scholar 

  • Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846

    Article  Google Scholar 

  • Proulx M, Mazumder A (1998) Reversal of grazing impact on plant species richness in nutrient-poor vs. nutrient-rich ecosystems. Ecology 79:2581–2592

    Article  Google Scholar 

  • Rainey PB, Travisano M (1998) Adaptive radiation in a heterogeneous environment. Nature 394:69–72

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen LD, Sorensen SJ (2001) Effects of mercury contamination on the culturable heterotrophic, functional and genetic diversity of the bacterial community in soil. Fems Microbiol Ecol 36:1–9

    Article  PubMed  CAS  Google Scholar 

  • Ratsak CH, Maarsen KA, Kooijman S (1996) Effects of protozoa on carbon mineralization in activated sludge. Water Res 30:1–12

    Article  CAS  Google Scholar 

  • Relyea RA (2003) How prey respond to combined predators: a review and an empirical test. Ecology 84:1827–1839

    Article  Google Scholar 

  • Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Biodiversity—global biodiversity scenarios for the year 2100. Science 287:1770–1774

    Article  PubMed  CAS  Google Scholar 

  • Schoener TW (1989) Food webs from the small to the large. Ecology 70:1559–1589

    Article  Google Scholar 

  • Sherr BF, Sherr EB, Berman T (1982) Decomposition of organic detritus: a selective role of microflagellate protozoa. Limnol Oceanogr 27:765–769

    Article  CAS  Google Scholar 

  • Sih A, Crowley P, McPeek M, Petranka J, Strohmeier K (1985) Predation, competition, and prey communities: a review of field experiments. Annu Rev Ecol Syst 16:269–311

    Article  Google Scholar 

  • Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355

    Article  Google Scholar 

  • Sommer U, Sommer F, Santer B, Jamieson C, Boersma M, Becker C, Hansen T (2001) Complementary impact of copepods and cladocerans on phytoplankton. Ecol Lett 4:545–550

    Article  Google Scholar 

  • Strom SL (2000) Bacterivory: interactions between bacteria and their grazers. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, pp 351–386

    Google Scholar 

  • Thebault E, Loreau M (2003) Food-web constraints on biodiversity-ecosystem functioning relationships. Proc Natl Acad Sci USA 100:14949–14954

    Article  PubMed  CAS  Google Scholar 

  • Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton

    Google Scholar 

  • Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E (1997a) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302

    Article  CAS  Google Scholar 

  • Tilman D, Lehman CL, Thomson KT (1997b) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci USA 94:1857–1861

    Article  CAS  Google Scholar 

  • Torsvik V, Goksoyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787

    PubMed  CAS  Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499

    Article  CAS  Google Scholar 

  • Wetzel RG, Likens GE (1991) Limnological analyses. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Wissinger S, McGrady J (1993) Intraguild predation and competition among larval dragonflies: direct and indirect effects on shared prey. Ecology 74:207–218

    Article  Google Scholar 

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Acknowledgements

We thank Aabir Banerji, Marcel Holyoak, and Peter Morin for comments on the manuscript. Jennifer Krumins was supported by NASA Graduate Student Researchers Program Fellowship.

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Authors and Affiliations

  1. School of Biology, Georgia Institute of Technology, 310 Ferst Drive, Atlanta, GA, 30332, USA

    Lin Jiang

  2. Department of Ecology, Evolution and Natural Resources, Cook College, Rutgers University, 14 College Farm Road, New Brunswick, NJ, 08901, USA

    Jennifer Adams Krumins

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  1. Lin Jiang
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Correspondence to Lin Jiang.

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Jiang, L., Krumins, J.A. Emergent multiple predator effects in an experimental microbial community. Ecol Res 21, 723–731 (2006). https://doi.org/10.1007/s11284-006-0181-y

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