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Microzooplankton Grazing Along the Western Antarctic Peninsula

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Microzooplankton Grazing Along the Western Antarctic Peninsula Vol. 70: 215–232, 2013 AQUATIC MICROBIAL ECOLOGY Published online September 18 doi: 10.3354/ame01655 Aquat Microb Ecol FREEREE ACCESSCCESS Microzooplankton grazing along the Western Antarctic Peninsula Lori M. Garzio1,*, Deborah K. Steinberg1,*, Matthew Erickson2, Hugh W. Ducklow3 1Virginia Institute of Marine Science, College of William & Mary, PO Box 1346, Gloucester Pt., Virginia 23062, USA 2Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA 3Lamont-Doherty Earth Observatory, Palisades, New York 10964, USA ABSTRACT: The significance of microzooplankton as grazers in pelagic ecosystems has been established, yet relatively few studies of microzooplankton grazing, compared to that of macro- zooplankton, have been conducted in the Southern Ocean. We report phytoplankton and bacterial growth and grazing mortality rates along the Western Antarctic Peninsula (WAP), a region of rapid climate change. Growth and grazing rates were determined by dilution experiments at select stations along the WAP in January of 2009 to 2011 and in the nearshore waters near Palmer Station in February and March 2011. Microzooplankton exerted higher grazing pressure on bac- teria compared to phytoplankton along the WAP and also selectively grazed on smaller phyto- plankton (picoautotrophs and nanophytoplankton) and on the more actively growing (high nucleic acid) bacterial cells. Among all phytoplankton size classes, growth rates ranged from undetectable (i.e. not significant; NS) to 0.99 d−1, grazing mortality rates were NS to 0.56 d−1, and microzooplankton removed <100% of daily phytoplankton production in all but one experiment. For high and low nucleic acid content bacteria, growth rates were NS to 0.95 d−1, and grazing mor- tality rates were NS to 0.43 d−1; microzooplankton often removed >100% of daily bacterial produc- tion. There was a significant (albeit weak) exponential relationship between temperature and phytoplankton mortality, although the range of experimental temperatures was small. The present study provides a reference point of microzooplankton grazing impact along the WAP in the sum- mer and contributes valuable information to studies modeling the flow of carbon through the WAP food web, improving our ability to predict climate-induced changes in the WAP ecosystem. KEY WORDS: Microzooplankton · Protozoa · Grazing · Western Antarctic Peninsula · Southern Ocean · Climate Resale or republication not permitted without written consent of the publisher INTRODUCTION have been relatively few studies of microzooplank- ton, compared to meso- and macrozooplankton (i.e. Microzooplankton are significant grazers on phyto- >200 µm). This is due in part to the historical focus on plankton and bacteria, can consume a wide range of the role of krill as grazers, along with the inherent prey types and sizes (Sherr & Sherr 2002), and influ- difficulty of studying microzooplankton and measur- ence phytoplankton and bacterial assemblages due ing their grazing rates (Landry & Hassett 1982, Dolan to selective feeding (Stoecker 1988, Banse 1992, Sherr et al. 2000, Calbet & Landry 2004, Dolan & McKeon & Sherr 1994). Although the importance of micro zoo - 2004), especially in an extreme environment. plankton grazers in the Southern Ocean has been Studies that quantify microzooplankton grazing established (von Bröckel 1981, Buck & Garrison 1983, impact on primary producers in the Southern Ocean Hewes et al. 1985, Heinbokel & Coats 1986), there report extremely variable phytoplankton mortality *Corresponding authors. © Inter-Research 2013 · www.int-res.com Email: [email protected]; [email protected] 216 Aquat Microb Ecol 70: 215–232, 2013 rates (Garrison 1991), from low to undetectable graz- with chlorophyll a (chl a) during a spring bloom in the ing (maximum grazing mortality = 0.26 d−1, Caron et northern Antarctic Peninsula and concluded that the al. 2000) to removal of >100% of primary production bacterial response to the phytoplankton bloom was (maximum grazing mortality = 2.36 d−1, Pearce et al. likely suppressed by grazing by heterotrophic nano- 2010). Pearce et al. (2008) reported that micrograzers flagellates. Summer bacterial abundances in the removed up to 762% of primary production (grazing WAP are relatively constant (Ducklow et al. 2012a), mortality = 1.13 d−1) in the marginal ice zone near which could be explained by microzooplankton graz- Davis Station, East Antarctica, and concluded that ing pressure. microzooplankton are key to controlling and ending The WAP is a region undergoing rapid warming, phytoplankton blooms at the end of summer in with 1°C increases in average winter air temperature coastal Antarctic waters. In contrast, Caron et al. each decade since 1950 (Smith et al. 1996, Vaughan (2000) assessed microzooplankton grazing in the et al. 2003, Ducklow et al. 2012a). The waters along Ross Sea and found grazing rates statistically greater the WAP are seasonally productive and support large than zero in only 9 of 34 experiments. Of those 9, all populations of zooplankton (e.g. krill) and top preda- the rates were low (<0.26 d−1), and they concluded tors, such as penguins, seals, and whales (Ducklow et that much of the phytoplankton bloom was not al. 2007, Ross et al. 2008, Vernet et al. 2008, Stein- grazed but removed by aggregation and sinking. In berg et al. 2012). Many components of the food web the Ross Sea, these low to negligible grazing rates in this region have been studied extensively (Duck- may be due to very low water temperatures that con- low et al. 2012a), while microzooplankton have been strain microzooplankton activity and to the presence largely overlooked until recently (Garzio & Steinberg of large colonies of Phaeocystis antarctica and possi- 2013). A previous study that assessed microzoo- bly large, unpalatable diatoms that potentially deter plankton grazing rates near our sampling area (to the microzooplankton grazing (Caron et al. 2000). north, near the tip of the WAP) showed that although In a meta-analysis of the role of temperature on there was significant variability in phytoplankton growth rates of aquatic protists, Rose & Caron (2007) growth (0 to 1.16 d−1) and mortality (0 to 0.29 d−1), a proposed that temperature differentially affects het- balance between phytoplankton growth and mortal- erotrophic protist and phytoplankton growth rates, ity was observed in half of the experiments (Tsuda & which could lead to imbalances between phyto- Kawaguchi 1997). plankton growth and mortality in this system. Colder In the present study, we report the first comprehen- temperatures constrain the growth of heterotrophic sive analysis of microzooplankton grazing rates protists to a greater degree than phytoplankton, along the WAP. We present phytoplankton and bac- potentially causing low microzooplankton grazing terial growth and mortality rates as measured by the rates at very low temperatures (as seen by Caron et dilution method (Landry & Hassett 1982) at select al. 2000). This release from microzooplankton graz- locations along the WAP as well as in the nearshore ing pressure could allow for the large phytoplankton waters near Palmer Station. We investigate selective blooms often observed in the Southern Ocean (Rose feeding by microzooplankton on different phyto- & Caron 2007). plankton size classes and bacterial types, in addition In addition to their importance as herbivores, micro- to temperature effects on microzooplankton grazing zooplankton are key consumers of bacterioplankton. rates. These measurements of microzooplankton graz- Flagellate populations can graze from 25% to >100% ing rates on phytoplankton and bacteria will help us of the measured daily production of bacterioplankton better understand microbial food web dy na mics in a (Sherr & Sherr 1994) and can considerably alter bac- region of rapid climate change and will provide a ref- terial assemblages by selective feeding (Sherr et al. erence point for future studies. 1992, Sherr & Sherr 1994). Bacteria in coastal Antarc- tic waters ultimately depend on phytoplankton pro- duction for organic matter and therefore should be MATERIALS AND METHODS coupled to the phytoplankton dynamics. In a recent time series analysis (2003 to 2011) of bacterial pro- Study site duction along the Western Antarctic Peninsula (WAP) during austral summer, bacterial production As part of the Palmer Antarctica Long-Term Ecolog- was positively correlated with phytoplankton bio- ical Research (PAL LTER) project (Ducklow et al. mass (Ducklow et al. 2012b). However, Bird & Karl 2012a), phytoplankton and bacterial growth and mor- (1999) reported that bacteria were not correlated tality rates were calculated using the dilution method Garzio et al.: Microzooplankton grazing along the Western Antarctic Peninsula 217 (Landry & Hassett 1982) on research cruises aboard and rinsed with Milli-Q water prior to use and be- the ARSV ‘Laurence M. Gould’ in January (austral tween experiments. Plastic nitrile gloves were worn summer) 2009, 2010, and 2011 (a total of 12 experi- throughout all sampling and experimental mani- ments) in continental shelf waters along the WAP. Ex- pulations. Filtered seawater (FSW) for experiments periments were also conducted using near-shore wa- was generated by gentle gravity filtration using car- ter collected from small boats near Palmer Station, tridge filters (0.2 µm pore size), and ‘whole’ seawater Ant arctica (sampling location: 64.78° S, 64.04° W) in was collected by gentle, reverse-flow filtration through February through March
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