k CHAPTER 15 Sea ice as a habitat for micrograzers David A. Caron,1 Rebecca J. Gast2 and Marie-Ève Garneau1 1Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA 2Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA, USA 15.1 Introduction biomass are single-celled eukaryotic microorganisms displaying heterotrophic ability, usually phagotrophy, Sea ice makes up a physically complex, geographically which is the engulfment of food particles. The term extensive, but often seasonally ephemeral biome on ‘protozoa’ has traditionally been employed and is Earth. Despite the extremely harsh environmental still commonly used to describe these species, but conditions under which it forms and exists for much of wholesale revision of the evolutionary relationships the year, sea ice can serve as a suitable, even favourable, among eukaryotic taxa throughout the past decade (Adl habitat for dense assemblages of microorganisms. Our et al., 2012), and greater understanding of the complex knowledge of the existence of high abundances of nutritional modes exhibited by single-celled eukaryotes microalgae (largely diatoms) in sea ice spans at least have called the accuracy of this term into question. a century, but for many years it remained unknown In particular, the traditional distinction between pho- whether these massive accumulations were composed totrophic protists (i.e. unicellular algae) and their heterotrophic counterparts (protozoa) presupposes that k of metabolically active or merely inactive cells brought k together through physical processes associated with phototrophy and heterotrophy are mutually exclu- ice formation. Work began approximately a quarter sive nutritional modes, but they are not. Technically, century ago started to fill this void in our knowledge of the word ‘protozoa’ adequately describes truly het- sea ice microbiota. erotrophic protists, but it does not take into account the Algal populations and their attendant bacterial fact that phagotrophy is a common behaviour among assemblages were initially believed to exist largely in many microscopic algae, nor does it recognize that some the absence of grazing mortality from herbivorous and apparently photosynthetic species of protists are in fact bacterivorous organisms. Our perception of these micro- kleptoplastidic, i.e. heterotrophs that consume photo- bial assemblages has changed, however, and it is now synthetic prey and retain the chloroplasts in a functional clear that sea ice supports highly enriched, taxonomi- state. Due to the existence of these mixotrophic species, cally diverse and trophically active microbial consumers the expression ‘phagotrophic protists’ provides a more in Arctic and Antarctic environments (Laurion et al., accurate description of the many protistan species 1995; Sime-Ngando et al., 1997a; Thomas & Dieckmann, employing heterotrophic nutrition, regardless of the 2002; Kaartokallio, 2004; Riedel et al., 2007). presence or absence of chloroplasts. These deficiencies Biological aspects of sea ice bacteria and microalgae having been noted, the term ‘protozoa’ will be used have been detailed in Chapters 13 and 14, respectively, synonymously with ‘heterotrophic protists’ (which of this book. The present chapter focuses on the micro- includes mixotrophic species) in this text for the sake of bial consumers that characterize these unique marine brevity. habitats. Within the complex microbial communities Scientific understanding of the diversity, abundances of sea ice, the major consumers of bacterial and algal and trophic activities of sea ice microconsumers has Sea Ice, Third Edition. Edited by David N. Thomas. © 2017 John Wiley & Sons, Ltd. Published 2017 by John Wiley & Sons, Ltd. 370 k k Sea ice as a habitat for micrograzers 371 only emerged within the past few decades, and much Ikavalko, 1998; Garrison et al., 2003), but this similarity remains to be learned. Although their ecology is still decreases as the assemblages adapt to conditions and not as thoroughly described or investigated as that of food availability in the ice (Rózanska et al., 2008). many photosynthetic taxa, bacteria and even some Demonstrations of different dominant taxa in sea metazoa from polar ecosystems, a basic understanding ice and the water column underlying or adjacent to of the breadth of their abundances and activities now the ice have been documented using traditional and, exists. Protozoan populations in sea ice reduce bacterial more recently, genetic techniques (Figure 15.1). DNA and algal abundances, remineralize major nutrients fragment analysis, gene sequencing and fluorescent in contained in their biomass, and constitute additional situ hybridization (FISH) approaches have corroborated sources of nutrition for metazoa within or associated such differences in drifting and landfast ice, underlying with the ice. The available information, complemented water and overlying snow in Antarctica, the Arctic by a wealth of knowledge regarding the ecology of and the Baltic Sea (Gast et al., 2004, 2006; Bachy heterotrophic microbial eukaryotes from temperate and et al., 2011; Terrado et al., 2011; Majaneva et al., 2012; tropical regions, is beginning to clarify the pivotal role Comeau et al., 2013; Piwosz et al., 2013). For example, played by protozoa in polar marine ecosystems. microbial eukaryotic assemblages in ice samples col- lected from different sites in the Antarctic were more similar to each other than to the assemblages from 15.2 Origins and fates of sea ice water samples collected at the same sites as the ice protists samples (Gast et al., 2004). Similarly, a microscopical study of sea ice protistan assemblages collected from The processes giving rise to sea ice protozoan assem- different locations in the Ross Sea, Antarctica, showed blages presumably are the same for phytoplankton, a relatively high degree of similarity in major biomass bacteria and invertebrates. Microbial populations can be components, presumably indicating the dominance of k either entrained into ice platelets formed in subsurface specific taxa that were more adapted to existence within k waters, trapped at the surface during the formation of the sea ice than in the water (Garrison et al., 2005). frazil ice, or invade existing ice through brine channels Similarities in protistan assemblages within ice from or fissures (Garrison et al., 1986; Petrich & Eicken, freshwater ecosystems have even been noted between 2015). These processes may selectively concentrate Arctic and Antarctic samples (Jungblut et al., 2012). certain microbial taxa because of size selection or other Heterotrophic protists were observed in all ice samples, characteristics (e.g. pennate diatoms may attach to ice, often at significant abundances. while foraminifera possess sticky pseudopodia that may These similarities in ice communities notwithstand- result in their scavenging by ice crystals). Thus, the ing, vertical gradients of environmental conditions initial colonizing assemblages in sea ice may represent within sea ice can create microhabitats that differ a ‘biased’ sampling of microorganisms in the water significantly in their physico-chemical characteristics column (Eicken, 1992). (Figure 15.2). Snow cover on ice dramatically affects Microbes that are incorporated into the ice experience light penetration, an important variable controlling chemical and physical characteristics that are vastly algal biomass within and especially at the bottom of different from the surrounding seawater environment. the ice (Grossi & Sullivan, 1985; Gosselin et al., 1986). The structure of the ice microbial community is there- Gradients of temperature and salinity resulting from fore dictated by the growth and mortality of species seawater infiltration and/or melting of snow and ice contained within the initial colonizing assemblage (or produce small-scale spatial heterogeneity in the ice. invading from the water column), under selective pres- These factors can lead to dramatic differences in the sures that differ greatly from those in the surrounding composition and biomass of the microbial communities water. These selective pressures result in a divergence growing there. Brine channels, compression ridges, in community composition from that in the water as meltwater (slush) at the snow-ice interface, and the the ice ages. For this reason, protistan assemblages in bottom of the ice are often microhabitats of excep- newly formed sea ice have been shown to be similar to tionally high microbial biomass, and at times high assemblages in the water column initially (Gradinger & diversity (Figure 15.2), as are meltwater ponds on sea k k 372 Chapter 15 90 80 70 60 50 40 30 Percentage of clones per library 20 k k 10 Diatom RSdino Dinoflagellate Stramenopile Prymnesiophyte 0 Prasinophyte Water Water Flagellate Water Water Euglenozoa 014 016 Water Slush 018 020 Slush Cryothecomonas 022 014 Slush Slush 016 Slush Ice Ciliate 018 020 Ice Ice Choanoflagellate 022 014 Ice 016 018 Ice Sample type and station 020 022 Figure 15.1 Differences in protistan community structure in sea ice, water and meltwater communities (slush) on ice floes from the Ross Sea, Antarctica, as determined from small subunit ribosomal RNA gene sequence libraries. Note the strong dominance of diatoms among the photosynthetic protists within sea ice, but also differences in the abundances of dinoflagellates (including RS dino, which is a kleptoplastidic form) and ciliates within the ice, slush and water. ice in the Arctic