Abstract
Knowledge of variations in microbial food web interactions resulting from atmospheric nutrient loads is crucial to improve our understanding of aquatic food web structure in pristine ecosystems. Three experiments mimicking atmospheric inputs at different nitrogen/phosphorus (N/P) ratios were performed in situ covering the seasonal biological succession of the pelagic zone in a high-mountain Spanish lake. In all experiments, abundance, biomass, algal cell biovolume, P-incorporation rates, P-cell quota, and N/P ratio of algae strongly responded to P-enrichment, whereas heterotrophic bacteria remained relatively unchanged. Ciliates were severely restricted when a strong algal exploitation of the available P (bloom growth or storage strategies) led to transient (mid-ice-free experiment) or chronic (late ice-free experiment) P-deficiencies in bacteria. In contrast, maximum development of ciliates was reached when bacteria remained P-rich (N/P < 20) and algae approached Redfield proportions (N/P∼16). Evidence of a higher P-incorporation rate supports the proposition that algae and bacteria shifted from a mainly commensalistic–mutualistic to a competitive relationship for the available P when bacterial P-deficiency increased, as reflected by their unbalanced N/P ratio (N/P > 20–24). Hence, the bacterial N/P ratio proved be a key factor to understand the algae–bacteria relationship and microbial food web development. This study not only demonstrates the interdependence of life history strategies, stoichiometric nutrient content, and growth but also supports the use of bacterial N/P thresholds for diagnosing ciliate development, a little-studied aspect worthy of further attention.
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References
Ăgren GI (2004) The C:N:P stoichiometry of autotrophs-theory and observations. Ecol Lett 7:185–191
Ăgren GI, Bosatta E (1996) Theoretical ecosystem ecology, understanding element cycles. Cambridge University Press, Cambridge, UK
American Public Health Association (1992) Standard methods for the examination of water and wastewater, 18th edn. American Public Health Association, Washington, DC
Berman-Frank I, Dubinsky Z (1999) Balanced growth in aquatic plants: myth or reality? Bioscience 49:29–37
Bratbak G, Thingstad F (1985) Phytoplankton-bacteria interactions: an apparent paradox? Analysis of a model system with both competition and commensalism. Mar Ecol Prog Ser 25:33–30
Carlsson P, Caron DA (2001) Seasonal variation of phosphorus limitation of bacterial growth in a small lake. Limnol Oceanogr 46:108–120
Caron DA, Lim EL, Sanders RW, Dennett MR, Berninger UG (2000) Response of bacterioplankton and phytoplankton to organic carbon and inorganic nutrient additions in contrasting oceanic ecosystems. Aquat Microb Ecol 22:175–184
Carrillo P, Cruz-Pizarro L, Morales-Baquero R (1990) Effects of unpredictable atmospheric allochthonous inputs on the light climate of an oligotrophic lake. Verh Int Ver Limnol 24:97–105
Carrillo P, Medina-Sánchez JM, Villar-Argaiz M (2002) The interaction of phytoplankton and bacteria in a high mountain lake: importance of the spectral composition of solar radiation. Limnol Oceanogr 47:1294–1306
Carrillo P, Medina-Sánchez JM, Villar-Argaiz M, Delgado-Molina JA, Bullejos FJ (2006) Complex interactions in microbial food webs: stoichiometric and functional approaches. Limnetica 25(1–2):189–204
Chrzanowski TH, Grover JP (2001) Effects of mineral nutrients on the growth of bacterio- and phytoplankton in two southern reservoirs. Limnol Oceanogr 46:1319–1330
Chrzanowski TH, Kyle M, Elser JJ, Sterner RW (1996) Element ratios and growth dynamics of bacteria in an oligotrophic Canadian shield lake. Aquat Microb Ecol 11:119–125
Cotner BJ, Biddanda BA (2002) Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5:105–121
Daufresne T, Loreau M (2001) Ecological stoichiometry, primary producer-decomposer interactions and ecosystem persistence. Ecology 82:3069–3082
Downing JA, McCauley E (1992) The nitrogen:phosphorus relationship in lakes. Limnol Oceanogr 37:936–945
Duarte CM, Agustí S, Vaque D, Agawin NSR, Felipe J, Casamayor EO, Gasol JM (2005) Experimental test of bacteria–phytoplankton coupling in the Southern Ocean. Limnol Oceanogr 50(6):1844–1854
Duarte CM, Agustí S, Gasol JM, Vaqué D, Vázquez-Domínguez E (2000) Effect of nutrient supply on the biomass structure of planktonic communities. An experimental test on a Mediterranean coastal community. Mar Ecol Prog Ser 206:87–95
Elser JJ, Dobberfuhl D, Mackay NA, Schampel JH (1996) Organism size, life history, and N:P stoichiometry: Toward a unified view of cellular and ecosystem processes. Bioscience 46:674–684
Escudero M, Castillo S, Querol X, Avila A, Alarcón M, Viana MM, Alastuey A, Cuevas E, Rodríguez S (2005) Wet and dry African dust episodes over eastern Spain. J Geophys Res 110:D18S08
Estrada M, Berdalet E, Vila M, Marrasé C (2003) Effects of pulsed nutrient enrichment on enclosed phytoplankton: ecophysiological and successional response. Aquat Microb Ecol 32:61–71
Healey FP, Hendzel LL (1980) Physiological indicators of nutrient deficiency in lake phytoplankton. Can J Fish Aquat Sci 37:442–453
Hessen DO, Faeovig PJ, Andersen T (2002) Light, nutrients, and P:C ratios in algae: grazer performance related to food quality and quantity. Ecology 83:1886–1898
Joint I, Henriksen P, Fonnes GA, Bourne D, Thingstad TF, Riemann B (2002) Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms. Aquat Microb Ecol 29:145–159
Krom MD, Crees N, Brenner S, Gordon LI (1991) Phosphorus limitation of primary productivity in the eastern Mediterranean Sea. Limnol Oceanogr 36:424–432
Makino W, Cotner JB (2004) Elemental stoichiometry of a heterotrophic bacterial community in a freshwater lake: implications for growth- and resource-dependent variations. Aquat Microb Ecol 34:33–41
Makino W, Cotner JB, Sterner RW, Elser JJ (2003) Are bacteria more like plants or animals? Growth rate and substrate dependence of bacterial C: N:P stoichiometry. Funct Ecol 17:121–130
Matz C, Boenigk J, Arndt H, Jürgens K (2002) Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellates Spumella sp. Aquat Microb Ecol 27:137–148
MCQueen D, Johannes S, Post R, Stewart J, Lean D (1989) Bottom–up and top–down impacts on freshwater pelagic community structure. Ecol Monogr 59:289–309
Medina-Sánchez JM, Villar-Argaiz M, Sánchez-Castillo P, Cruz-Pizarro L, Carillo P (1999) Structure changes in a planktonic food web: biotic and abiotic controls. J Limnol 58:213–222
Medina-Sánchez JM, Villar-Argaiz M, Carrillo P (2002) Modulation of the bacterial response to spectral solar radiation by algae and limiting nutrients. Freshwater Biol 47:2191–2204
Medina-Sánchez JM, Villar-Argaiz M, Carrillo P (2004) Neither with nor without you: a complex algal control on bacterioplankton. Limnol Oceanogr 49:1722–1733
Medina-Sánchez JM, Villar-Argaiz M, Carrillo P (2006) Solar radiation-nutrient interaction enhances the resource and predation algal control on bacterioplankton: a short-term experimental study. Limnol Oceanogr 51:913–924
Möller H, Geller W (1993) Maximum growth rates of aquatic ciliated protozoa: the dependence on body size and temperature reconsidered. Arch Hydrobiol 126:315–327
Morales-Baquero R, Pulido-Villena E, Reche I (2006) Atmospheric inputs of phosphorus and nitrogen to the southwest Mediterranean region: biogeochemical response of high mountain lakes. Limnol Oceanogr 51:830–837
Morris DP, Lewis WM (1988) Phytoplankton nutrient limitation in Colorado mountain lakes. Freshwater Biol 20:315–327
Norland S (1993) The relationship between biomass and volume of bacteria. In: Kemp PF, Sherr BF, Sherr EB Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis, Boca Raton, pp 303–307
Oata Y, Nakajima H (2001) Mutualistic relationship between phytoplankton and bacteria caused by carbon excretion from phytoplankton. Ecol Res 16:288–299
Obernosterer I, Herndl GJ (1997) Phytoplankton extracellular release and bacterial growth: dependence on the inorganic N:P ratio. Mar Ecol Prog Ser 116:247–257
Porter KG, Feig YS (1980) Use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948
Prospero JM, Lamb PJ (2003) African droughts and dust transport to the Caribbean: climate change implications. Science 302:1024–1027
Psenner R (1999) Living in a dusty world-airborne dust as a key factor for alpine lakes. Water Air Soil Poll 112:217–227
Ptacnik R, Sommer U, Hasen T, Martens V (2004) Effects of microplankton and mixotrophy in an experimental planktonic food web. Limnol Oceanogr 49:1435–1445
Pulido- Villena E, Reche I, Morales-Baquero R (2006) Significance of atmospheric inputs of calcium over the southwestern Mediterranean region: high mountain lakes as tools for detection. Global Biogeochem Cycles 20:GB2012
Putt M, Stoecker DK (1989) An experimentally determined carbon: volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnol Oceanogr 34:1097–1103
Redfield AC, Ketchum BH, Richards FA (1963) The influence of organisms on the composition of seawater. In: Hill MN (ed) The sea, vol. 2. Wiley Interscience, New York
Rivkin RB, Anderson MR (1997) Inorganic nutrient limitation of oceanic bacterioplankton. Limnol Oceanogr 42:730–740
Roberts EC, Priscu JC, Laybourn-Parry J (2004) Microplankton dynamics in a perennially ice-covered Antarctic lake–Lake Hoare. Freshwater Biol 49:853–869
Rocha O, Duncan A (1985) The relationship between cell carbon and cell volume in freshwater algal species used in zooplankton studies. J Plankton Res 7:279–294
Rothaupt KO (1997) Nutrient turnover by freshwater bacterivorous flagellates: differences between a heterotrophic and a mixotrophic chrysophyte. Aquat Microb Ecol 12:65–70
Samuelsson K, Berglund J, Haecky P, Andersson A (2002) Structural changes in an aquatic food web caused by inorganic nutrient addition. Aquat Microb Ecol 29:29–39
Schlesinger WH (1997) Biogeochemistry: an analysis of global change. Academic, San Diego, CA
Šimek K, Jürgens K, Nedoma J, Comerma M, Armengol J (2000) Ecological role and bacterial grazing of Halteria spp.: small freshwater oligotrichs as dominant pelagic ciliate bacterivores. Aquat Microb Ecol 22:43–56
Sommer U (1985) Comparison between steady state and nonsteady state competition: Experiments with natural phytoplankton. Limnol Oceanogr 30:335–346
Statsoft (2005) Statistica for Windows. Release 7.1 edn. Statsoft, Inc., Tulsa, OK
Stelzer RS, Lamberty GA (2001) Effects of N:P ratio and total nutrient concentration on stream periphyton community structure, biomass, and elemental composition. Limnol Oceanogr 46:365–367
Sterner RW, Elser JJ (2002) Ecological soichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, USA
Straskrabová V, Callieri C, Fott J (eds) (1999a) Pelagic food webs in mountain lakes -Mountain LAkes Research Program. J Limnol 58:77–222
Straskrabová V, Callieri C, Carrillo P, Cruz-Pizarro L, Fott J, Hartman P, Macek M, Medina-Sánchez JM, Nedoma J, Simek K (1999b) Investigations on pelagic food webs in mountain lakes—aims and methods. J Limnol 58:77–87
Tadonléké RD, Planas D, Lucotte M (2005) Microbial food webs in boreal humic lakes and reservoirs: ciliates as a major factor related to the dynamics of the most active bacteria. Microbial Ecol 49:325–341
Tarapchack SJ, Moll RA (1990) Phosphorus sources for phytoplankton and bacteria in Lake Michigan. J Plankton Res 12:743–758
Teira E, Pazó MJ, Serret P, Fernández E (2001) Dissolved organic carbon production by microbial population in the Atlantic Ocean. Limnol Oceanogr 46:1370–1377
Urabe J, Gurung TB, Yoshida T, Sekino T, Nakanishi M, Maruo M, Nakayama E (2000) Diel changes in phagotrophy by Cryptomonas in Lake Biwa. Limnol Oceanogr 45:1558–1563
Vaqué D, Blough HA, Duarte CM (1997) Dynamics of ciliate abundance, biomass and community composition in an oligotrophic coastal environment (NW Mediterranean). Aquat Microb Ecol 12:71–83
Villar-Argaiz M, Medina-Sánchez JM, Carrillo P (2001) Inter- and intra-annual variability in the phytoplankton community of a high mountain lake: the influence of external (atmospheric) and internal (recycled) sources of P. Freshwater Biol 46:1017–1024
Villar-Argaiz M, Medina-Sánchez JM, Carrillo P (2002) Microbial plankton response to contrasting climatic conditions: insights from community structure, productivity and fraction stoichiometry. Aquat Microb Ecol 29:253–266
Vrede K (1999) Effects of inorganic nutrients and zooplankton on the growth of heterotrophic bacterioplankton-enclosure experiments in an oligotrophic clearwater lake. Aquat Microb Ecol 18:133–144
Vrede K, Vrede T, Isaksson A, Karlsson A (1999) Effects of nutrients (phosphorous, nitrogen and carbon) and zooplankton on bacterioplankton and phytoplankton—seasonal study. Limnol Oceanogr 44:1616–1624
Wang L, Miller TD, Priscu JC (1992) Bacterioplankton nutrient deficiency in a eutrophic lake. Arch Hydrobiol 125:423–439
Weisse T, MacIsaac E (2000) Significance and fate of bacterial production in oligotrophic lakes in British Columbia. Can J Fish Aquat Sci 57:96–105
Zubkov MV, Sleigh MA (1995) Bacterivory by starved marine heterotrophic nanoflagellates of two species which feed differently, estimated by uptake of dual radioactive-labeled bacteria. FEMS Microbiol Ecol 17:57–66
Acknowledgements
The authors gratefully acknowledge the help of laboratory crew in routine sampling and Richard Davies for English writing assistance. We are grateful to Maria del Mar Rueda Professor of Statistical and Operative Research University of Granada for their advice on statistical analysis This study was supported by the Spanish Ministry Science and Technology Project REN2001–2840 HID (to PC) and MEC Project CGL2005-01564 (to PC) and Spanish Ministry of Environment Project (PN 2003/25) (to PC).
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Carrillo, P., Villar-Argaiz, M. & Medina-Sánchez, J.M. Does Microorganism Stoichiometry Predict Microbial Food Web Interactions After a Phosphorus Pulse?. Microb Ecol 56, 350–363 (2008). https://doi.org/10.1007/s00248-007-9353-8
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DOI: https://doi.org/10.1007/s00248-007-9353-8