Skip to main content
Log in

The effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

We analyzed heterotrophic, pelagic bacterial production and specific growth rate data from 57 studies conducted in fresh, marine and estuarine/coastal waters. Strong positive relationships were identified between 1) bacterial production and bacterial abundance and 2) bacterial production and algal biomass. The relationship between bacterial production and bacterial abundance was improved by also considering water temperature. The analysis of covariance model revealed consistent differences between fresh, marine and estuarine/coastal waters, with production consistently high in estuarine/coastal environments. The log-linear regression coefficient of abundance was not significantly different from 1.00, and this linear relationship permitted the use of specific growth rate (SGR in day−1) as a dependent variable. A strong relationship was identified between specific growth rate and temperature. This relationship differed slightly across the three habitats. A substantial portion of the residual variation from this relationship was accounted for by algal biomass, including the difference between marine and estuarine/coastal habitats. A small but significant difference between the fresh- and saltwater habitats remained. No significant difference between the chlorophyll effect in different habitats was identified. The model of SGR against temperature and chlorophyll was much weaker for freshwater than for marine environments. For a small subset of the data set, mean cell volume accounted for some of the residual variation in SGR. Pronounced seasonality, fluctuations in nutrient quality, and variation of the grazing environment may contribute to the unexplained variation in specific growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Aitkin M, Anderson D, Francis B, Hinde J (1989) Statistical modelling in GLIM. Clarendon Press, Oxford

    Google Scholar 

  2. Aizaki, M, Otsuki A, Fukushima T, Hosomi T, Muroaka K (1981) Applications of Carlson's trophic state index to Japanese lakes and relationships between the index and other parameters. Verh Int Verein Limnol 21: 675–681

    CAS  Google Scholar 

  3. Albright LJ, McCrae SK (1987) Annual bacterioplankton biomasses and productivities in a temperate west coast Canadian fjord. Appl Environ Microbiol 53: 1277–1285

    PubMed  Google Scholar 

  4. Alldredge AL, Cole JJ, Caron DA (1986) Production of heterotrophic bacteria inhabiting macroscopic organic aggregates (marine snow) from surface waters.Limnol Oceanogr31: 68–78

    Google Scholar 

  5. Alldredge AL, Youngbluth MJ (1985) The significance of macroscopic aggregates (marine snow) as sites for heterotrophic bacterial production in the mesopelagic zone of the subtropical Atlantic. Deep Sea Res 32: 1445–1456

    Article  Google Scholar 

  6. Allen DM (1971) Mean square error of prediction as a criterion for selecting variables. Technometrics 13: 465–475

    Article  Google Scholar 

  7. Banse K (1977) Determining the carbon-to-chlorophyll ratio of natural phytoplankton. Mar Biol 41: 199–212

    Article  CAS  Google Scholar 

  8. Bell RT (1990) An explanation for the variability in the conversion factors deriving bacterial cell production from incorporation of [3H]thymidine. Limnol Oceanogr 35:910–915

    CAS  Google Scholar 

  9. Bell RT, Ahlgren GM, Ahlgren I (1983) Estimating bacterioplankton production by measuring [3H]thymidine incorporation in a eutrophic Swedish lake. Appl Environ Microbiol 45: 1709–1721

    PubMed  Google Scholar 

  10. Bell RT, Kuparinen J (1984) Assessing phytoplankton and bacterioplankton production during early spring in Lake Erken, Sweden. Appl Environ Microbiol 48: 1221–1230

    CAS  PubMed  Google Scholar 

  11. Bird DF, Kalff J (1984) Empirical relationships between bacterial abundance and chlorophyll concentrations in fresh and marine waters. Can J Fish Aquat Sci 41: 1015–1023

    Article  Google Scholar 

  12. Bloem J, Bär-Gilissen MJB (1989) Bacterial activity and protozoan grazing potential in a stratified lake. Limnol Oceanogr 34: 297–309

    Google Scholar 

  13. Bloem J, Ellenbroek FM, Bär-Gilissen MJB, Cappenberg TE (1989) Protozoan grazing and bacterial production in stratified Lake Vechten estimated with fluorescently labeled bacteria and by thymidine incorporation. Appl Environ Microbiol 55: 1787–1795

    CAS  PubMed  Google Scholar 

  14. Børsheim KY, Andersen S (1987) Grazing and food size selection by crustacean zooplankton compared to production of bacteria and phytoplankton in a shallow Norwegian mountain lake. J Plank Res 9:367–379

    Google Scholar 

  15. Børsheim KY, Andersen S, Johnsen GH, Kambestad EØ, Norland S (1988) Primary and bacterial production compared to growth and food requirements ofDaphnia longispina in Lake Kvernavatnet, west Norway. J Plank Res 10:921–939

    Google Scholar 

  16. Bratbak G (1985) Bacterial biovolume and biomass estimation. Appl Environ Microbiol 49: 1488–1493

    PubMed  Google Scholar 

  17. Bratbak G, Dundas I (1984) Bacterial dry matter content and biomass estimations. Appl Environ Microbiol 48: 755–757

    CAS  PubMed  Google Scholar 

  18. Brock TD (1971) Microbial growth rates in nature. Bacteriol Rev 35: 39–58

    CAS  PubMed  Google Scholar 

  19. Chrzanowski TH, Hubbard JG (1988) Primary and secondary production in a southwestern reservoir. Appl Environ Microbiol 54: 661–669

    PubMed  Google Scholar 

  20. Cole J, Findlay S, Pace M (1988) Bacterial production in fresh and saltwater ecosystems: A cross system overview. Mar Ecol Prog Ser 43:1–10

    Google Scholar 

  21. Coveney M (1982) Bacterial uptake of photosynthetic carbon from freshwater phytoplankton. Oikos 38:8–20

    Article  CAS  Google Scholar 

  22. Currie DJ (1990) Phosphorus deficiency and its variation among lakes. Can J Fish Aquat Sci 47: 1077–1084

    CAS  Google Scholar 

  23. Currie DJ (1990) Large-scale variability and interactions among phytoplankton, bacterioplankton and phosphorus. Limnol Oceanogr 35: in press

  24. Douglas DJ, Novitsky JA, Fournier RO (1987) Microautoradiography-based enumeration of bacteria with estimates of thymidine-specific growth and production rates. Mar Ecol Prog Ser 36:91–99

    CAS  Google Scholar 

  25. Ducklow HW (1982) Chesapeake Bay nutrient and plankton dynamics. 1. Bacterial biomass and production during spring tidal destratification in the York River, Virginia, estuary Limnol Oceanogr 27:651–659

    CAS  Google Scholar 

  26. Ducklow HW (1986) Bacterial biomass in warm-core gulf stream ring 82-B: Mesoscale distributions, temporal changes and production. Deep Sea Res 33: 1789–1812

    Article  CAS  Google Scholar 

  27. Ducklow HW, Kirchman DL (1983) Bacterial dynamics and distribution during a spring diatom bloom in the Hudson River plume, USA. J Plank Res 5:333–355

    Google Scholar 

  28. Ducklow HW, Kirchman DL, Rowe GT (1982) Production and vertical flux of attached bacteria in the New York Bight as studied with floating sediment traps. Appl Environ Microbiol 43: 769–776

    PubMed  Google Scholar 

  29. Edwards RT, Meyer JL (1986) Production and turnover of planktonic bacteria in two southeastern blackwater rivers. Appl Environ Microbiol 52: 1317–1323

    PubMed  Google Scholar 

  30. Fenchel T, Blackburn TH (1979) Bacteria and mineral cycling. Academic Press, New York

    Google Scholar 

  31. Findlay S, Meyer J, Risley R (1986) Benthic bacterial biomass and production in two blackwater rivers. Can J Fish Aquat Sci 43: 1271–1276

    Article  Google Scholar 

  32. Fuhrman JA, Azam F (1980) Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Appl Environ Microbiol 39: 1085–1095

    PubMed  Google Scholar 

  33. Fuhrman JA, Azam F (1982) Thymidine incorporation as a measure of heterotrophic bacterioplankton in marine surface waters: Evaluation and field results. Mar Biol 66: 109–120

    Article  Google Scholar 

  34. Fuhrman JA, Eppley RW, Hagström Å, Azam F (1985) Diel variations in bacterioplankton, phytoplankton, and related parameters in the southern California bight. Mar Ecol Prog Ser 27:9–20

    Google Scholar 

  35. Fuhrman JA, McManus GB (1984) Do bacteria-sized marine eukaryotes consume significant bacterial production? Science 224: 1257–1260

    Article  PubMed  Google Scholar 

  36. Güde H (1986) Loss processes influencing growth of planktonic bacterial populations in Lake Constance. J Plank Res 8: 795–810

    Google Scholar 

  37. Güde H (1988) Direct and indirect influences of crustacean zooplankton on bacterioplankton of Lake Constance. Hydrobiologia 159:63–73

    Google Scholar 

  38. Güde H (1989) The role of grazing on bacteria in plankton succession. In: Sommer U (ed) Plankton ecology. Springer-Verlag, Berlin Heidelberg New York, pp 337–364

    Google Scholar 

  39. Güde H, Haibel B, Müller H (1985) Development of planktonic bacterial populations in a water column of Lake Constance (Bodensee-Obersee). Arch Hydrobiologia 105: 59–77

    Google Scholar 

  40. Hall KJ, Northcote TG (1990) Production and decomposition processes in a saline meromictic lake. Hydrobiologia 197: 115–128

    Article  CAS  Google Scholar 

  41. Hanson RB, Lowery HK, Shafer D, Sorocco R, Pope DH (1983) Microbes in Antarctic waters of the Drake Passage: Vertical patterns of substrate uptake, productivity and biomass in January 1980. Polar Biol 2: 179–188

    Article  Google Scholar 

  42. Henebry MS, Gorden RW (1989) Summer bacterial populations in Mississippi River Pool 19: Implications for secondary production. Hydrobiologia 182: 15–23

    Article  CAS  Google Scholar 

  43. Hobbie JE (1988) A comparison of the ecology of planktonic bacteria in fresh and salt water. Limnol Oceanogr 33: 750–764

    CAS  Google Scholar 

  44. Hobbie JE, Cole JJ (1984) Response of a detrital food web to eutrophication. Bull Mar Sci 35: 357–363

    Google Scholar 

  45. Hobbie JE, Helfrich JVK III (1988) The effect of grazing by microzooplankton on production of bacteria. Arch Hydrobiologia Beih 31: 281–288

    Google Scholar 

  46. Hoppe HG (1976) Determination of properties of actively metabolizing bacteria in the sea, investigated by means of microautoradiography. Mar Biol 36:291–302

    Article  Google Scholar 

  47. Hudak JP, McDaniel J, Lee S, Fuhrman JA (1988) Mineralization potentials of aromatic hydrocarbons by estuarine microorganisms: Variations with seston, location, and bacterioplankton production. Mar Ecol Progr Ser 47: 97–102

    CAS  Google Scholar 

  48. Iriberri J, Muela A, Egea L (1985) Heterotrophic bacterial activity in coastal waters: Functional relationship of temperature and phytoplankton population. Ecol Mod 28: 113–120

    Article  Google Scholar 

  49. Johnstone BH, Jones RD (1989) A study on the lack of [methyl-3H] thymidine uptake and incorporation by chemolithotrophic bacteria. Microb Ecol 18:73–77

    Article  CAS  Google Scholar 

  50. Jones JG (1976) The microbiology and decomposition of seston in open water and experimental enclosures in a productive lake. J. Ecol 64:241–278

    Article  CAS  Google Scholar 

  51. Kankaala P (1988) The relative importance of algae and bacteria as food forDaphnia longispina (Cladocera) in a polyhumic lake. Freshwater Biol 19:285–296

    Article  Google Scholar 

  52. Kirchman D, Soto Y, Wambeck FV, Bianchi M (1989) Bacterial production in the Rhône River plume: Effect of mixing on relationships among microbial assemblages. Mar Ecol Prog Ser 53: 267–275

    Google Scholar 

  53. Kottmeier ST, Grossi SM, Sullivan CW (1987) Sea ice microbial communities. VIII. Bacterial production in annual sea ice of McMurdo Sound, Antarctica. Mar Ecol Prog Ser 35: 175–186

    Google Scholar 

  54. Laanbroek HJ, Verplanke JC (1986) Tidal variations in bacterial biomass, productivity and oxygen uptake rates in a shallow channel in the Oosterschelde basin, The Netherlands. Mar Ecol Prog Ser 29:1–5

    Google Scholar 

  55. Lee S, Fuhrman JA (1987) Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl Environ Microbiol 53: 1298–1303

    CAS  PubMed  Google Scholar 

  56. Li WKW, Dickie PM (1987) Temperature characteristics of photosynthetic and heterotrophic activities: Seasonal variations in temperate microbial plankton. Appl Environ Microbiol 53: 2282–2295

    PubMed  Google Scholar 

  57. Lovell CR, Konopka A (1985) Primary and bacterial production in two dimictic Indiana lakes. Appl Environ Microbiol 49:492–500

    PubMed  Google Scholar 

  58. Malone TC, Ducklow HW (1990) Microbial biomass in the coastal plume of Chesapeake Bay: Phytoplankton-bacterioplankton relationships. Limnol Oceanogr 35:296–312

    CAS  Google Scholar 

  59. McManus GB, Peterson WT (1988) Bacterioplankton production in the nearshore zone during upwelling off central Chile Mar Ecol Prog Ser 43:11–17

    Google Scholar 

  60. Montgomery DC, Peck EA (1982) Introduction to linear regression analysis. John Wiley and Sons, Inc, New York

    Google Scholar 

  61. Moriarty DJW (1986) Bacterial productivity in ponds used for culture of Penaeid prawns. Microb Ecol 12:259–269

    Article  CAS  Google Scholar 

  62. Moriarty DJW, Roberts DG, Pollard PC (1990) Primary and bacterial productivity of tropical seagrass communities in the Gulf of Carpentia, Australia. Mar Ecol Prog Ser 61:145–157

    Google Scholar 

  63. Nagata T (1987) Production of planktonic bacteria in the north basin of Lake Biwa, Japan. Appl Environ Microbiol 53:2872–2882

    PubMed  Google Scholar 

  64. Neidhardt FC, Ingraham JL, Schaechter M (1990) Physiology of the bacterial cell. Sinauer Associates, Inc, Sunderland, MA

    Google Scholar 

  65. Newell SY, Fallon RD (1982) Bacterial productivity in the water column and sediments of the Georgia (USA) coastal zone: Estimates via direct counting and parallel measurement of thymidine incorporation. Microb Ecol 8: 33–46

    Article  Google Scholar 

  66. Neyman J, Scott EL (1960) Correction for bias introduced by a transformation of variables. Ann Math Stat 31:643–661

    Google Scholar 

  67. Nielsen TG, Kiørboe T, Bjørnsen PK (1990) Effects of aChrysochomulina polylepis subsurface bloom on the planktonic community. Mar Ecol Progr Ser 62:21–35

    Google Scholar 

  68. Nielsen TG, Richardson K (1989) Food chain structure of the North Sea plankton communities: Seasonal variations of the role of the microbial loop. Mar Ecol Prog Ser 56: 75–87

    Google Scholar 

  69. Paul JH, DeFlaun MF, Jeffrey WH, David AW (1988) Seasonal and dial variability in dissolved DNA and in microbial biomass and activity in a subtropical estuary. Appl Environ Microbiol 54: 718–727

    CAS  PubMed  Google Scholar 

  70. Pedrós-Alió C, Newell SY (1989) Microautoradiographic study of thymidine uptake in brackish waters around Sapelo Island, Georgia, USA Mar Ecol Prog Ser 55:83–94

    Google Scholar 

  71. Pomeroy LR, Macko SA, Ostrom PH, Dunphy J (1990) The microbial food web of Arctic seawater: Concentration of dissolved free amino acids and bacterial abundance and activity in the Arctic Ocean and in Resolute Passage. Mar Ecol Prog Ser 61: 31–40

    CAS  Google Scholar 

  72. Pomeroy LR, Wiebe WJ (1988) Energetics of microbial food webs. Hydrobiologia 159: 7–18

    Google Scholar 

  73. Psenner R (1990) From image analysis to chemical analysis of bacteria: A long term study. Limnol Oceanogr 35: 234–236

    CAS  Google Scholar 

  74. Ricker WE (1973) Linear regression in fishery research. J Fish Res Board Can 30: 409–434

    Google Scholar 

  75. Riemann B (1983) Biomass and production of phyto- and bacterioplankton in eutrophic Lake Tystrup, Denmark. Freshwater Biol 13:389–398

    Article  Google Scholar 

  76. Riemann B, Bell RT (1990) Advances in estimating bacterial biomass and growth in aquatic systems. Arch Hydrobiologia 118: 485–502

    Google Scholar 

  77. Riemann B, Søndergaard M (1986) Regulation of bacterial secondary production in two eutrophic lakes and in experimental enclosures. J Plank Res 8:519–536

    CAS  Google Scholar 

  78. Riemann B, Søndergaard M, Schierup H, Bosselmann S, Christensen G, Hansen J, Nielsen B (1982) Carbon metabolism during a spring diatom bloom in the eutrophic Lake Mossø. Int Revue Ges Hydrobiologia 67:145–185

    CAS  Google Scholar 

  79. Sanders RW, Porter KG, Bennett SJ, DeBiase AE (1989) Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol Oceanogr 34:673–687

    Google Scholar 

  80. Scavia D, Laird GA, Fahensteil GL (1986) Production of planktonic bacteria in Lake Michigan. Limnol Oceanogr 31:612–626

    Google Scholar 

  81. Sherr BF, Sherr EB, Andrew TA, Fallon RD, Newell SY (1986) Trophic interactions between heterotrophic protozoa and bacterioplankton in estuarine water analyzed with selective metabolic inhibitors. Mar Ecol Prog Ser 32:169–180

    CAS  Google Scholar 

  82. Sherr BF, Sherr EB, Pedrós-Alió C (1989) Simultaneous measurement of bacterioplankton production and protozoan bacterivory in estuarine water. Mar Ecol Prog Ser 54:209–219

    Google Scholar 

  83. Simek K, Straskrabova V (1989) Seasonal dynamics of planktonic protozoans in the Rimov reservoir and their grazing on bacterioplankton. 29th Annual Report—Section of Hydrobiology, Institute of Landscape Ecology, Czechoslovak Academy of Sciences

  84. Simon M (1987) Biomass and production of small and large free-living and attached bacteria in Lake Constance. Limnol Oceanogr 32:591–607

    CAS  Google Scholar 

  85. Smith V (1979) Nutrient dependence of primary productivity in lakes. Limnol Oceanogr 24: 1051–1064

    Google Scholar 

  86. Sorokin VI (1990) Comparative evaluation of the isotopic methods for the measurement of microbial production in the sea. Arch Hydrobiologia Beih 34:157–164

    Google Scholar 

  87. Sorokin VI, Paveljeva EB (1972) On the quantitative characteristics of the pelagic ecosystem of Dalnee lake (Kamchatka). Hydrobiologia 40: 519–552

    Article  Google Scholar 

  88. Svedrup HU, Johnson MW, Fleming RH (1949) The oceans: Their physics, chemistry, and general biology. Prentice-Hall Inc, New York

    Google Scholar 

  89. Torréton JP, Guiral D, Arfi R (1989) Bacterioplankton biomass and production during destratification in a monomictic eutrophic bay of a tropical lagoon. Mar Ecol Prog Ser 57: 53–67

    Google Scholar 

  90. Tranvik LJ, Hoffe MG (1987) Bacterial growth in mixed cultures on dissolved organic carbon from humic and clear waters. Appl Environ Microbiol 53:482–488

    CAS  PubMed  Google Scholar 

  91. Vadstein O, Jensen A, Harkjerr BO, Olsen Y, Reinertsen (1989) Cycling of organic carbon in the photic zone of a eutrophic lake with special reference to the heterotrophic bacteria. Limnol Oceanogr 34:840–855

    CAS  Google Scholar 

  92. Vadstein O, Olsen Y, Reinertsen H, Jensen A (1988) Growth and phosphorus status of limnetic phytoplankton and bacteria. Limnol Oceanogr 33: 489–503

    CAS  Google Scholar 

  93. Van Es FB, Meyer-Reil LA (1982) Biomass and metabolic activity of heterotrophic marine bacteria. Adv Microb Ecol 6:111–170

    Google Scholar 

  94. Velleman PF, Welsch RE (1981) Efficient computing of regression diagnostics. Am Stat 35: 234–242

    Article  Google Scholar 

  95. Weisse T (1989) Microbial loop in the red sea-dynamics of pelagic bacteria and heterotrophic nanoflagellates. Mar Ecol Prog Ser 55:241–250

    Google Scholar 

  96. Wetzel RG (1982) Limnology. Saunders Publishing, Philadelphia

    Google Scholar 

  97. Wikner J, Andersson A, Normark S, Hagström Å (1986) Use of genetically marked minicells as a probe in measurement of predation on bacteria in aquatic environments. Appl Environ Microbiol 52:4–8

    PubMed  Google Scholar 

  98. Wikner J, Rassoulzadegan F, Hagström A (1990) Periodic bacterivore activity balances bacterial growth in the marine environment. Limnol Oceanogr 35:313–324

    Article  Google Scholar 

  99. Wilkinson L (1987) SYSTAT: The system for statistics. SYSTAT Inc, Evanston, IL

    Google Scholar 

  100. Wright RT, Coffin RB, Lebo ME (1987) Dynamics of planktonic bacteria and heterotrophic microflagellates in the Parker Estuary, northern Massachusetts. Continental Shelf Res 7: 1383–1397

    Article  Google Scholar 

  101. Zar JH (1984) Biostatistical analysis, Prentice-Hall Inc, Englewood Cliffs, NJ

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

White, P.A., Kalff, J., Rasmussen, J.B. et al. The effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats. Microb Ecol 21, 99–118 (1991). https://doi.org/10.1007/BF02539147

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02539147

Keywords

Navigation