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Low temperature constrains growth rates but not short-term ingestion rates of Antarctic ciliates

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Abstract

Low environmental temperature is a major factor affecting the feeding activities, growth rates, and growth efficiencies of metazooplankton, but these features are poorly characterized for most protistan species. Laboratory experiments were conducted to examine the growth and ingestion rates of cultured herbivorous Antarctic ciliates. Three ciliates fed several algal species individually at 0 °C exhibited uniformly low growth rates (<0.26 day−1), but the algae varied substantially in their ability to support ciliate growth. Specific ingestion rate (prey biomass consumed per unit ciliate biomass per unit time) was strongly affected by ciliate physiological state (starved vs. actively growing). Starved cells ingested many more prey than cells in balanced growth during short-term (minutes-to-hours) experiment but did not grow faster, indicating temperature compensation of ingestion rate but not growth rate. Field experiments were also conducted in the Ross Sea, Antarctica, to characterize the feeding rates of ciliates in natural plankton assemblages. Specific ingestion rates of two dominant ciliates were an order of magnitude lower than rates reported for temperate ciliates, but estimated rates were strongly affected by prey abundance. Our data indicate that short-term ingestion rates of Antarctic ciliates were not constrained by low environmental temperature although overall growth rates were, indicating the need for caution when designing experiments to measure the ingestion rates of these species at low environmental temperature. We present evidence that artifacts arising from estimating ingestion in short-term experiments may lead to errors in estimating feeding impact and growth efficiencies that are particularly large for polar protists.

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References

  • Allen AP, Gillooly JF, Brown JH (2005) Linking the global carbon cycle to individual metabolism. Functional Ecol 19:202–213

    Article  Google Scholar 

  • Apple JK, Strom SL, Palenik B, Brahamsha B (2011) Variability in protist grazing and growth on different marine Synechococcus isolates. Appl Environ Microbiol 77:3074–3084

    Article  PubMed  CAS  Google Scholar 

  • Archer SD, Leakey RJG, Burkill PH, Sleigh MA, Appleby CJ (1996) Microbial ecology of sea ice at a coastal Antarctic site: community composition, biomass and temporal change. Mar Ecol Prog Ser 135:179–195

    Article  Google Scholar 

  • Becquevort S (1997) Nanoprotozooplankton in the Atlantic sector of the Southern Ocean during early spring: biomass and feeding activities. Deep-Sea II 44:355–373

    Article  Google Scholar 

  • Beers JR, Stewart GL (1971) Micro-zooplankters in the plankton communities of the upper waters of the eastern tropical Pacific. Deep-Sea Res 18:861–883

    Google Scholar 

  • Beers JR, Reid FMH, Stewart GL (1975) Microplankton of the North Pacific Central Gyre. Population structure and abundance, June 1973. Int Rev Gesamten Hydrobiol 60:607–638

    Google Scholar 

  • Bell EM, Laybourn-Parry J (2003) Mixotrophy in the Antarctic phytoflagellate, Pyramimonas gelidicola (Chlorophyta: Prymnesiophyceae). J Phycol 39:644–649

    Article  Google Scholar 

  • Buitenhuis ET, Rivkin RB, Sailley S, Le Quéré C (2010) Biogeochemical fluxes through microzooplankton. Glob Biogeochem Cycles 24:GB4015

    Article  Google Scholar 

  • Calbet A, Landry MR (2004) Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol Oceanogr 49:51–57

    Article  CAS  Google Scholar 

  • Calbet A, Saiz E (2005) The ciliate-copepod link in marine food ecosystems. Aquat Microb Ecol 38:157–167

    Article  Google Scholar 

  • Caron DA, Gast RJ (2010) Heterotrophic protists associated with sea ice. In: Thomas DN, Dieckmann GS (eds) Sea ice. Wiley-Blackwell, Oxford, pp 327–356

    Google Scholar 

  • Caron DA, Rose JM (2008) The metabolic theory of ecology and algal bloom formation (reply to comment by López-Urrutia). Limnol Oceanogr 53:2048–2049

    Article  Google Scholar 

  • Caron DA, Goldman JC, Fenchel T (1990) Protozoan respiration and metabolism. In: Capriulo GM (ed) Ecology of marine protozoa. Oxford University Press, New York, pp 307–322

    Google Scholar 

  • Caron DA, Lonsdale DJ, Dennett MR (1997) Bacterivory and herbivory play key roles in fate of Ross Sea production. Antarct J US 32:81–83

    Google Scholar 

  • Caron DA, Dennett MR, Lonsdale DJ, Moran DM, Shalapyonok L (2000) Microzooplankton herbivory in the Ross Sea, Antarctica. Deep-Sea Res 47:15–16

    Google Scholar 

  • Chen B, Liu H, Lau M (2010) Grazing and growth responses of a marine oligotrichous ciliate fed with two nanoplankton: does food quality matter for micrograzers? Aquat Ecol 44:113–119

    Article  CAS  Google Scholar 

  • Choi JW, Peters F (1992) Effects of temperature on two psychrophilic ecotypes of a heterotrophic nanoflagellate, Paraphysomonas imperforata. Appl Environ Microbiol 58:593–599

    PubMed  CAS  Google Scholar 

  • Daugbjerg N (2000) Pyramimonas tychotreta, sp. nov. (prasinophyceae), a new marine species from antarctica: light and electron microscopy of the motile stage and notes on growth rates. J Phycol 36:160–171

    Article  Google Scholar 

  • Dennett MR, Mathot S, Caron DA, Smith WO, Lonsdale DJ (2001) Abundance and distribution of phototrophic and heterotrophic nano- and microplankton in the southern Ross Sea. Deep-Sea Res II 48:4019–4037

    Article  CAS  Google Scholar 

  • DiTullio GR, Smith WO Jr (1996) Spatial patterns in phytoplankton biomass and pigment distributions in the Ross Sea. J Geophys Res 101:18,467–418,478

    Google Scholar 

  • Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580

    Article  PubMed  CAS  Google Scholar 

  • Fenchel T (1980) Suspension feeding in ciliated protozoa: functional response and particle size selection. Microb Ecol 6:1–11

    Article  Google Scholar 

  • Fenchel T (1986) The ecology of heterotrophic microflagellates. Adv Microb Ecol 9:57–97

    Google Scholar 

  • Fenchel T, Lee CC (1972) Studies on ciliates associated with sea ice from Antarctica: II. temperature responses and tolerances in ciliates from Antarctic, temperate and tropical habitats. Arch Protist 114:237–244

    Google Scholar 

  • First M, Hollibaugh J (2008) Protistan bacterivory and benthic microbial biomass in an intertidal creek mudflat. Mar Ecol Prog Ser 361:59–68

    Google Scholar 

  • First M, Hollibaugh J (2010) Environmental factors shaping microbial community structure in salt marsh sediments. Mar Ecol Prog Ser 399:15–26

    Google Scholar 

  • Garrison DL (1991) An overview of the abundance and role of protozooplankton in Antarctic waters. J Mar Syst 2:317–331

    Article  Google Scholar 

  • Garrison DL, Gowing MM (1993) Protozooplankton. In: Friedmann EI (ed) Antarctic microbiology. Wiley, New York, pp 123–166

    Google Scholar 

  • Garrison DL, Sullivan CW, Ackley SF (1986) Sea ice microbial communities in Antarctica. Bioscience 36:243–250

    Article  Google Scholar 

  • Gast RJ, Dennett MR, Caron DA (2004) Characterization of protistan assemblages in the Ross Sea, Antarctica by denaturing gradient gel electrophoresis. Appl Environ Microbiol 70:2028–2037

    Article  PubMed  CAS  Google Scholar 

  • Gifford DJ, Caron DA (1999) Sampling, preservation, enumeration and biomass of marine protozooplankton. In: Harris RP, Wiebe PH, Lenz J, Skjoldal HR, Huntley M (eds) ICES zooplankton methodology manual. Academic Press, London, pp 193–221

    Google Scholar 

  • Gifford DJ, Fessenden LM, Garrahan PR, Martin E (1995) Grazing by microzooplankton and mesozooplankton in the high latitude North Atlantic ocean: spring versus summer dynamics. J Geophys Res 100:6665–6675

    Article  CAS  Google Scholar 

  • Gismervik I (2005) Numerical and functional responses of choreo- and oligotrich planktonic ciliates. Aquat Microb Ecol 40:163–173

    Article  Google Scholar 

  • Gowing MM, Garrison DL (1992) Abundance and feeding ecology of larger protozooplankton in the ice edge zone of the Weddell and Scotia Seas during the austral winter. Deep-Sea Res 39:893–919

    Article  Google Scholar 

  • Gradinger R, Friedrich C, Spindler M (1999) Abundance, biomass and composition of the sea ice biota of the Greenland Sea pack ice. Deep-Sea II 46:1457–1472

    Article  Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Publishing, New York, pp 29–60

    Chapter  Google Scholar 

  • Hansen PJ, Bjørnsen PK, Hansen BW (1997) Zooplankton grazing and growth: scaling within the 2–2,000-μm body size range. Limnol Oceanogr 42:687–704

    Article  Google Scholar 

  • Jeong HJ, Yoo YD, Kim ST, Kang NS (2004) Feeding by the heterotrophic dinoflagellate Protoperidinium bipes on the diatom Skeletonema costatum. Aquat Microb Ecol 36:171–179

    Article  Google Scholar 

  • Jonsson PR (1986) Particle size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora: Oligotrichina). Mar Ecol Prog Ser 33:265–277

    Article  Google Scholar 

  • Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23:633–638

    Article  Google Scholar 

  • Laurion I, Demers S, Vézina AF (1995) The microbial food web associated with the ice algal assemblage: biomass and bacterivory of nanoflagellate protozoans in Resolute Passage (High Canadian Arctic). Mar Ecol Prog Ser 120:77–87

    Article  Google Scholar 

  • Lee JJ, Leedale GF, Bradbury P (2000) An illustrated guide to the protozoa. Allen Press, Inc., Lawrence

  • Li A, Stoecker DK, Coats DW, Adam EJ (1996) Ingestion of fluorescently labeled and phycoerythrin-containing prey by mixotrophic dinoflagellates. Aquat Microb Ecol 10:139–147

    Article  Google Scholar 

  • Li C, Xu K, Lei Y (2011) Growth and grazing responses to temperature and prey concentration of Condylostoma spatiosum, a large benthic ciliate, feeding on Oxyrrhis marina. Aquat Microb Ecol 64:97–104

    Article  Google Scholar 

  • Lonsdale DJ, Caron DA, Dennett MR, Schaffner R (2000) Predation by Oithona spp. on protozooplankton in the Ross Sea, Antarctica. Deep-Sea II 47:3273–3283

    Article  Google Scholar 

  • López-Urrutia Á (2008) The metabolic theory of ecology and algal bloom formation. Limnol Oceanogr 53:2046–2047

    Google Scholar 

  • Lovejoy C, Massana R, Pedros-Alio C (2006) Diversity and distribution of marine microbial eukaryotes in the Arctic Ocean and adjacent seas. Appl Environ Microbiol 72:3085–3095

    Article  PubMed  CAS  Google Scholar 

  • Marchant HJ (1985) Choanoflagellates in the Antarctic marine food chain. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin, pp 271–276

    Google Scholar 

  • Mayes DF, Rogerson A, Marchant H, Laybourn-Parry J (1997) Growth and consumption rates of bacterivorous Antarctic naked marine amoebae. Mar Ecol Prog Ser 160:101–108

    Article  Google Scholar 

  • Montagnes DJS (1996) Growth responses of planktonic ciliates in the genera Strobilidium and Strombidium. Mar Ecol Prog Ser 130:241–254

    Article  Google Scholar 

  • Montresor M, Lovejoy C, Orsini L, Procaccini G, Roy S (2003) Bipolar distribution of the cyst-forming dinoflagellate, Polarella glacialis. Polar Biol 26:186–194

    Google Scholar 

  • Moorthi SD, Caron DA, Gast RJ, Sanders RW (2009) Mixotrophic nanoflagellates in plankton and sea-ice of the Ross Sea. Aquat Microb Ecol 54:269–277

    Article  Google Scholar 

  • Netjstgaard JC, Tang KW, Steinke M, Dutz J, Koski M, Antajan E, Long JD (2007) Zooplankton grazing on Phaeocystis: a quantitative review and future challenges. Biogeochemistry 83:147–172

    Article  Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford

  • Petz W, Song W, Wilbert N (1995) Taxonomy and ecology of the ciliate fauna (Protozoa, Ciliophora) in the endopagial and pelagial of the Weddel Sea, Antarctica. Stapfia 40:1–223

    Google Scholar 

  • Rivkin RB, Legendre L (2001) Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291:2398–2400

    Article  PubMed  CAS  Google Scholar 

  • Roberts EC, Laybourn-Parry J (1999) Mixotrophic cryptophytes and their predators in the Dry Valley lakes of Antarctica. Freshw Biol 41:737–746

    Article  Google Scholar 

  • Rose JM, Caron DA (2007) Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold water. Limnol Oceanogr 52:886–895

    Article  Google Scholar 

  • Rose JM, Vora NM, Countway PD, Gast RJ, Caron DA (2009) Effects of temperature on growth rate and gross growth efficiency of an Antarctic bacterivorous protist. ISME J 3:252–260

    Article  PubMed  CAS  Google Scholar 

  • Schmoker C, Thor P, Hernández-León S, Hansen BW (2011) Feeding, growth and metabolism of the marine heterotrophic dinoflagellate Gyrodinium dominans. Aquat Microb Ecol 65:65–73

    Article  Google Scholar 

  • Scott FJ, Marchant HJ (2005) Antarctic marine protists. Goanna Print, Canberra, p 563

    Google Scholar 

  • Scott FJ, Davidson AT, Marchant HJ (2001) Grazing by the Antarctic sea-ice ciliate Pseudocohnilembus. Polar Biol 24:127–131

    Article  Google Scholar 

  • Sherr EB, Sherr BF (2002) Significance of predation by protists in aquatic microbial food webs. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 81:293–308

    Article  CAS  Google Scholar 

  • Sherr BF, Sherr EB, Fallon RD (1987) Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl Environ Microbiol 53:958–965

    PubMed  CAS  Google Scholar 

  • Sherr EB, Sherr BF, McDaniel J (1991) Clearance rates of <6 μm fluorescently labeled algae (FLA) by estuarine protozoa: potential grazing impact of flagellates and ciliates. Mar Ecol Prog Ser 69:81–92

    Article  Google Scholar 

  • Sherr EB, Sherr BF, Fessenden L (1997) Heterotrophic protists in the Central Arctic Ocean. Deep-Sea II 44:1665–1682

    Article  CAS  Google Scholar 

  • Sherr EB, Sherr BF, Hartz AJ (2009) Microzooplankton grazing impact in the Western Arctic Ocean. Deep-Sea Res II 56:1264–1273

    Article  Google Scholar 

  • Smetacek V, Assmy P, Henjes J (2004) The role of grazing in structuring Southern Ocean pelagic ecosystems and biogeochemical cycles. Antarct Sci 16:541–558

    Article  Google Scholar 

  • Smith WO Jr, Gordon LI (1997) Hyperproductivity of the Ross Sea (Antarctica) polynya during austral spring. Geophys Res Lett 24:233–236

    Article  Google Scholar 

  • Smith WOJ, Nelson DM, DiTullio GR, Leventer AR (1996) Temporal and spatial patterns in the Ross Sea: Phytoplankton biomass, elemental composition productivity and growth rates. J Geophys Res 101:18,455–418,466

    Google Scholar 

  • Snoeyenbos-Wes OL, Salcedo T, McManus GB, Katz LA (2002) Insights into the diversity of choreotrich and oligotrich ciliates (Class: Spirotrichea) based on genealogical analyses of multiple loci. Int J Syst Evol Microbiol 52:1901–1913

    Article  Google Scholar 

  • Stoecker DK, Buck KR, Putt M (1993) Changes in the sea-ice brine community during the spring-summer transition, McMurdo Sound, Antarctica. 2. Phagotrophic protists. Mar Ecol Prog Ser 95:103–113

    Article  Google Scholar 

  • Stoecker DK, Putt M, Moisan T (1995) Nano- and microplankton dynamics during the spring Phaeocystis sp. bloom in McMurdo Sound, Antarctica. J Mar Biol Assoc UK 75:815–832

    Article  Google Scholar 

  • Straile D (1997) Gross growth efficiencies of protozoan and metazoan zooplankton and their dependence on food concentration, predator-prey weight ratio, and taxonomic group. Limnol Oceanogr 42:1375–1385

    Article  Google Scholar 

  • Strathmann RR (1967) Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol Oceanogr 12:411–418

    Article  CAS  Google Scholar 

  • Strom S, Wolfe GV, Slajer A, Lambert S, Clough J (2003) Chemical defenses in the microplankton II: inhibition of protist feeding by B-dimethylsulfoniopropionate (DMSP). Limnol Oceanogr 48:230–237

    Article  CAS  Google Scholar 

  • Sullivan CW, Palissano AC, Kottmeier S, Roe BA (1982) Development of the sea ice microbial communities (SIMCO) in McMurdo Sound, Antarctica. Antarct J US 17:155–157

    Google Scholar 

  • Umani SF, Monti M, Nuccio C (1998) Microzooplankton biomass distribution in Terra Nova Bay, Ross Sea (Antarctica). J Mar Syst 17:289–303

    Article  Google Scholar 

  • Utermöhl H (1958) Zur Vervollkommung der quantitativen phytoplankton-methodik. Mitt Int Ver Limnol 9:38

    Google Scholar 

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Acknowledgments

The authors are grateful to Mark R. Dennett, Dawn M. Moran, Robert W. Sanders, and Peter D. Countway with assistance in the performance of the field work. This work was supported by National Science Foundation grants OPP-9714299, OPP-0125437, and OPP-0542456.

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  1. Julie M. Rose

    Present address: Northeast Fisheries Science Center Milford Laboratory, NOAA National Marine Fisheries Service, Milford, CT, USA

Authors and Affiliations

  1. Department of Biological Sciences, University of Southern California, 3616 Trousdale Parkway, AHF 301, Los Angeles, CA, 90089-0371, USA

    Julie M. Rose, Annie Wang & David A. Caron

  2. University of California at San Diego, San Diego, CA, USA

    Elizabeth Fitzpatrick

  3. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, 02543, USA

    Rebecca J. Gast

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  1. Julie M. Rose
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Correspondence to David A. Caron.

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Rose, J.M., Fitzpatrick, E., Wang, A. et al. Low temperature constrains growth rates but not short-term ingestion rates of Antarctic ciliates. Polar Biol 36, 645–659 (2013). https://doi.org/10.1007/s00300-013-1291-y

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