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Oecologia

, Volume 186, Issue 3, pp 755–764 | Cite as

Interplay between r- and K-strategists leads to phytoplankton underyielding under pulsed resource supply

  • Lydia A. PapanikolopoulouEmail author
  • Evangelia Smeti
  • Daniel L. Roelke
  • Panayiotis G. Dimitrakopoulos
  • Giorgos D. Kokkoris
  • Daniel B. Danielidis
  • Sofie Spatharis
Community ecology – original research

Abstract

Fluctuations in nutrient ratios over seasonal scales in aquatic ecosystems can result in overyielding, a condition arising when complementary life-history traits of coexisting phytoplankton species enables more complete use of resources. However, when nutrient concentrations fluctuate under short-period pulsed resource supply, the role of complementarity is less understood. We explore this using the framework of Resource Saturation Limitation Theory (r-strategists vs. K-strategists) to interpret findings from laboratory experiments. For these experiments, we isolated dominant species from a natural assemblage, stabilized to a state of coexistence in the laboratory and determined life-history traits for each species, important to categorize its competition strategy. Then, using monocultures we determined maximum biomass density under pulsed resource supply. These same conditions of resource supply were used with polycultures comprised of combinations of the isolated species. Our focal species were consistent of either r- or K-strategies and the biomass production achieved in monocultures depended on their efficiency to convert resources to biomass. For these species, the K-strategists were less efficient resource users. This affected biomass production in polycultures, which were characteristic of underyielding. In polycultures, K-strategists sequestered more resources than the r-strategists. This likely occurred because the intermittent periods of nutrient limitation that would have occurred just prior to the next nutrient supply pulse would have favored the K-strategists, leading to overall less efficient use of resources by the polyculture. This study provides evidence that fluctuation in resource concentrations resulting from pulsed resource supplies in aquatic ecosystems can result in phytoplankton assemblages’ underyielding.

Keywords

Nutrient pulses Competition Species traits Resource saturation Nutrient limitation 

Notes

Acknowledgements

The authors would like to thank Ulrich Sommer, Jason Matthiopoulos, Georg Pohnert and three anonymous reviewers for their essential comments on this research work.

Author contribution statement

DLR and SS originally formulated the idea. SS and ES designed the experiments. LAP performed the experiments. DBD, ES, LAP measured the species traits. SS, ES, GDK, LAP performed statistical analysis. ES, SS, PGD, DLR provided the ecological and mechanistic interpretation of experimental results. SS, ES, GDK, LAP wrote the manuscript and DLR provided editorial advice. LAP, ES, SS and DLR revised the manuscript.

References

  1. Beckage B, Gross LJ (2006) Overyielding and species diversity: what should we expect? New Phytologist 172:140–148.  https://doi.org/10.1111/j.1469-8137.2006.01817.x CrossRefPubMedGoogle Scholar
  2. Bruno JF, Lee SC, Kertesz JS, Carpenter RC, Long ZT, Duffy JE (2006) Partitioning the effects of algal species identity and richness on benthic marine primary production. Oikos 115:170–178.  https://doi.org/10.1111/j.2006.0030-1299.14927.x CrossRefGoogle Scholar
  3. Buyukates Y, Roelke D (2005) Influence of pulsed inflows and nutrient loading on zooplankton and phytoplankton community structure and biomass in microcosm experiments using estuarine assemblages. Hydrobiologia 548:233–249.  https://doi.org/10.1007/s10750-005-5195-x CrossRefGoogle Scholar
  4. Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera P, O’Connor MI, Gonzalez A (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:1–21.  https://doi.org/10.3732/ajb.1000364 CrossRefGoogle Scholar
  5. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67.  https://doi.org/10.1038/nature11148 CrossRefPubMedGoogle Scholar
  6. Corcoran AA, Boeing WJ (2012) Biodiversity increases the productivity and stability of phytoplankton communities. PLoS One 7(11):e49397.  https://doi.org/10.1371/journal.pone.0049397 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Dimitrakopoulos PG, Schmid B (2004) Biodiversity effects increase linearly with biotope space. Ecol Lett 7:574–583.  https://doi.org/10.1111/j.1461-0248.2004.00607.x CrossRefGoogle Scholar
  8. Duffy JE (2009) Why biodiversity is important to the functioning of real-world ecosystems. Front Ecol Envir 7:437–444.  https://doi.org/10.1890/070195 CrossRefGoogle Scholar
  9. Fox JW (2005) Interpreting the ‘selection effect’ of biodiversity on ecosystem function. Ecol Lett 8:846–856.  https://doi.org/10.1111/j.1461-0248.2005.00795.x CrossRefGoogle Scholar
  10. Fridley JD (2001) The influence of species diversity on ecosystem productivity: how, where, and why? Oikos 93:514–526.  https://doi.org/10.1034/j.1600-0706.2001.930318.x CrossRefGoogle Scholar
  11. Gamfeldt L, Hillebrand H (2008) Biodiversity effects on aquatic ecosystem functioning: maturation of a new paradigm. Int Rev Hydrobiol 93:550–564.  https://doi.org/10.1002/iroh.200711022 CrossRefGoogle Scholar
  12. Grover JP (1990) Resource competition in a variable environment: phytoplankton growing according to Monod’s model. Am Nat 136:771–789.  https://doi.org/10.1086/285131 CrossRefGoogle Scholar
  13. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239.  https://doi.org/10.1139/m62-029 CrossRefPubMedGoogle Scholar
  14. Hector A (1998) The effect of diversity on productivity: detecting the role of species complementarity. Oikos 82:597–599.  https://doi.org/10.2307/3546380 CrossRefGoogle Scholar
  15. Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn JA, Freitas H, Giller PS, Good J, Harris R, Hogberg P, Huss-Danell K, Joshi J, Jumpponen A, Korner C, Leadley PW, Loreau M, Minns A, Mulder CPH, O’Donovan G, Otway SJ, Pereira JS, Prinz A, Read DJ, Scherer-Lorenzen M, Schulze ED, Siamantziouras ASD, Spehn EM, Terry AC, Troumbis AY, Woodward FI, Yachi S, Lawton JH (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127.  https://doi.org/10.1126/science.286.5442.1123 CrossRefPubMedGoogle Scholar
  16. Hector A, Hautier Y, Saner P, Wacker L, Bagchi R, Joshi J, Scherer-Lorenzen M, Spehn EM, Bazeley-White E, Weilenmann M, Caldeira MC, Dimitrakopoulos PG, Finn JA, Huss-Danell K, Jumpponen A, Mulder CPH, Palmborg C, Pereira JS, Siamantziouras ASD, Terry AC, Troumbis AY, Schmid B, Loreau M (2010) General stabilizing effects of plant diversity on grassland productivity through population asynchrony and overyielding. Ecology 91:2213–2220.  https://doi.org/10.1890/09-1162.1 CrossRefPubMedGoogle Scholar
  17. Hill GA, Robinson CW (1974) Measurement of aerobic batch culture maximum specific growth rate and respiration coefficient using a dissolved oxygen probe. Biotechnol Bioeng 16:531–538.  https://doi.org/10.1002/bit.260160409 CrossRefPubMedGoogle Scholar
  18. Hillebrand H, Durselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424.  https://doi.org/10.1046/j.1529-8817.1999.3520403.x CrossRefGoogle Scholar
  19. Huston A (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110:449–460.  https://doi.org/10.1007/s004420050180 CrossRefPubMedGoogle Scholar
  20. Katechakis A, Stibor H, Sommer U, Hansen T (2002) Changes in the phytoplankton community and microbial food web of Blanes Bay (Catalan Sea, NW Mediterranean) under prolonged grazing pressure by doliolids (Tunicata), cladocerans or copepods (Crustacea). Mar Ecol Prog Ser 234:55–69.  https://doi.org/10.3354/meps234055 CrossRefGoogle Scholar
  21. Kilham P, Kilham SS (1980) The evolutionary ecology of phytoplankton. In: Morris I (ed) The physiological ecology of phytoplankton. University California Press, Berkley, pp 571–597Google Scholar
  22. Kirk JTO (1994) Light and photosynthesis in aquatic ecosystems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  23. Lambers JHR, Harpole WS, Tilman D, Knops J, Reich PB (2004) Mechanisms responsible for the positive diversity—productivity relationship in Minnesota grasslands. Ecol Lett 7:661–668.  https://doi.org/10.1111/j.1461-0248.2004.00623.x CrossRefGoogle Scholar
  24. Loreau M (1998) Separating sampling and other effects in biodiversity experiments. Oikos 82:600–602.  https://doi.org/10.2307/3546381 CrossRefGoogle Scholar
  25. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiment. Nature 412:72–76.  https://doi.org/10.1038/35097128 CrossRefPubMedGoogle Scholar
  26. Moore CM, Mills MM, Arrigo KR, Berman-Frank I, Bopp L, Boyd PW, Galbraith ED, Geider RJ, Guieu C, Jaccard SL, Jickells TD, La Roche J, Lenton TM, Mahowald NM, Marañón E, Marinov I, Moore JK, Nakatsuka T, Oschlies A, Saito MA, Thingstad TF, Tsuda A, Ulloa O (2013) Processes and patterns of oceanic nutrient limitation. Nat Geosci 6:701–710.  https://doi.org/10.1038/NGEO1765 CrossRefGoogle Scholar
  27. Mueller KE, Tilman D, Fornara DA, Hobbie SE (2013) Root depth distribution and the diversity–productivity relationship in a long-term grassland experiment. Ecology 94:787–793.  https://doi.org/10.1890/12-1399.1 CrossRefGoogle Scholar
  28. O’Connor MI, Gonzalez A, Byrnes JEK, Bradley J, Cardinale J, Duffy E, Gamfeldt L, Griffin JN, Hooper D, Hungate BA, Paquette A, Thompson PL, Dee LE, Dolan KL (2016) A general biodiversity—function relationship is mediated by trophic level. Oikos 000:001–014.  https://doi.org/10.1111/oik.03652 Google Scholar
  29. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, OxfordGoogle Scholar
  30. Power LD, Cardinale BJ (2009) Species richness enhances both algal biomass and rates of oxygen production in aquatic microcosms. Oikos 118:1703–1711.  https://doi.org/10.1111/j.1600-0706.2009.17585.x CrossRefGoogle Scholar
  31. Ptacnik R, Solimini AG, Andersen T, Tamminen T, Brettum P, Lepistö L, Willén E, Rekolainen S (2008) Diversity predicts stability and resource use efficiency in natural phytoplankton communities. PNAS 105:5134–5138.  https://doi.org/10.1073/pnas.0708328105 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Pujo-Pay M, Raimbault P (1994) Improvement of the wet oxidation procedure for simultaneous determination of particulate organic nitrogen and phosphorus collected on filters. Mar Ecol Prog Ser 105:203–207.  https://doi.org/10.3354/meps105203 CrossRefGoogle Scholar
  33. Reynolds CS (1993) Scales of disturbance and their role in plankton ecology. Hydrobiologia 249:157–171.  https://doi.org/10.1007/BF00008851 CrossRefGoogle Scholar
  34. Reynolds C (2006) The ecology of phytoplankton. Cambridge Univ. Press, New YorkCrossRefGoogle Scholar
  35. Roelke DL, Spatharis S (2015) Phytoplankton succession in recurrently fluctuating environments. PLoS One 10:e0121392.  https://doi.org/10.1371/journal.pone.0121392 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Roscher C, Thein S, Schmid B, Scherer-Lorenzen M (2008) Complementary nitrogen use among potentially dominant species in a biodiversity experiment varies between two years. J Ecol 96:477–488.  https://doi.org/10.1111/j.1365-2745.2008.01353.x CrossRefGoogle Scholar
  37. Schabhüttl S, Hingsamer P, Weigelhofer G, Hein T, Weigert A, Striebel M (2013) Temperature and species richness effects in phytoplankton communities. Oecologia 171:527–536.  https://doi.org/10.1007/s00442-012-2419-4 CrossRefPubMedGoogle Scholar
  38. Schmidtke A, Gaedke U, Weithoff G (2010) A mechanistic basis for underyielding in phytoplankton communities. Ecology 91:212–221.  https://doi.org/10.1890/08-2370.1 CrossRefPubMedGoogle Scholar
  39. Shurin JB, Abbott RL, Deal MS, Kwan GT, Litchman E, McBride RC, Mandal S, Smith VH (2013) Industrial-strength ecology: trade-offs and opportunities in algal biofuel production. Ecol Lett 16:1393–1404.  https://doi.org/10.1111/ele.12176 CrossRefPubMedGoogle Scholar
  40. Singh M, Awasthi A, Soni SK, Singh R, Verma RK, Kalra A (2015) Complementarity among plant growth promoting traits in rhizospheric bacterial communities promotes plant growth. Sci Rep 5:15500.  https://doi.org/10.1038/srep15500 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Smeti E, Roelke DL, Spatharis DL (2016) Spatial averaging and disturbance lead to high productivity in aquatic metacommunities. Oikos 125:812–820.  https://doi.org/10.1111/oik.02684 CrossRefGoogle Scholar
  42. Sommer U (1989) The role of competition for resources in phytoplankton ecology. In: Sommer U (ed) Plankton ecology: succession in plankton communities. Springer-Verlag, Berlin, pp 57–106CrossRefGoogle Scholar
  43. Spatharis S, Tsirtsis G, Danielidis DB, Chi TD, Mouillot D (2007) Effects of pulsed nutrient inputs on phytoplankton assemblage structure and blooms in an enclosed coastal area. Estuar Coas Shelf Sci 73:807–815.  https://doi.org/10.1016/j.ecss.2007.03.016 CrossRefGoogle Scholar
  44. Suttle CA, Stockner GJ, Harrison PJ (1987) Effects of nutrient pulses on community structure and cell-size of a freshwater phytoplankton assemblage in culture. Can J Fish Aquat Sci 44:1768–1774.  https://doi.org/10.1139/f87-217 CrossRefGoogle Scholar
  45. Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton, New JerseyGoogle Scholar
  46. Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversityin grassland ecosystems. Nature 379:718–720.  https://doi.org/10.1038/379718a0 CrossRefGoogle Scholar
  47. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845.  https://doi.org/10.1126/science.1060391 CrossRefPubMedGoogle Scholar
  48. Utermöhl H (1958) Zur vervollkommnung der quantitativen phytoplankton-methodik. Verh Int Ver Theor Angew Limnol 9:1–38Google Scholar
  49. Wardle DA (1999) Is "sampling effect" a problem for experiments investigating biodiversity-ecosystem function relationships? Oikos 87:403–407.  https://doi.org/10.2307/3546757 CrossRefGoogle Scholar
  50. Weis JJ, Cardinale BJ, Forshay KJ, Ives AR (2007) Effects of species diversity on community biomass production change over the course of succession. Ecology 88:929–939.  https://doi.org/10.1890/06-0943 CrossRefPubMedGoogle Scholar
  51. Weis JJ, Madrigal DS, Cardinale BJ (2008) Effects of algal diversity on the production of biomass in homogeneous and heterogeneous nutrient environment: a microcosm experiment. PLoS One 3:e2825.  https://doi.org/10.1371/journal.pone.0002825 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Lydia A. Papanikolopoulou
    • 1
    • 2
    Email author
  • Evangelia Smeti
    • 1
  • Daniel L. Roelke
    • 3
  • Panayiotis G. Dimitrakopoulos
    • 4
  • Giorgos D. Kokkoris
    • 1
  • Daniel B. Danielidis
    • 6
  • Sofie Spatharis
    • 5
  1. 1.Department of Marine SciencesUniversity of the AegeanMytileneGreece
  2. 2.Institute for Inorganic and Analytical ChemistryFriedrich Schiller University JenaJenaGermany
  3. 3.Department of Wildlife and Fisheries Sciences, and Department of OceanographyTexas A&M UniversityCollege StationUSA
  4. 4.Department of Environment, Biodiversity Conservation LaboratoryUniversity of the AegeanMytileneGreece
  5. 5.School of Life Sciences and Institute of Biodiversity, Animal Health and Comparative MedicineUniversity of GlasgowGlasgowUK
  6. 6.Department of Ecology and Systematics, Faculty of BiologyUniversity of AthensAthensGreece

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